ADVANCES IN THE STUDY OF BEHAVIOR V 11, Volume 11 (v. 11)

Advances in THE STUDY OF BEHAVIOR VOLUME 11 Contributors to This Volume ABRAM AMSEL R. J. ANDREW AND& CORNET DAVID C...

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Advances in

THE STUDY OF BEHAVIOR VOLUME 11

Contributors to This Volume ABRAM AMSEL R. J. ANDREW AND& CORNET DAVID CREWS MICHAEL DOMJAN GUNTER EHRET PIERRE JOUVENTIN JOHN R. KREBS DONALD E. KROODSMA PIERRE LE NEINDRE PASCAL POINDRON MARK STANTON

Advances in

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

ROBERTA. HINDE Medical Research Council Unit on the Development and Integration of Behaviour University Sub-Department of Animal Behaviour Madingley, Cambridge, England COLINBEER Institute of Animal Behavior Rutgers University Newark, New Jersey MARIE-CLAIRE BUSNEL Laboratoire de Physiologie Acoustique Institut National de la Recherche Agronomique Jouy en Josas (78350),France

VOLUME 1 1

ACADEMIC PRESS A Subsidiary of Harcourt Brace Jovanovich, Publishers

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1980

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80 81 82 83

9 8 7 6 5 4 3 2 1

Contents

List of Conrributors . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Preface . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

ix xi

Interrelationships among Ecological. Behavioral. and Neuroendocrine Processes in the Reproductive Cycle of Anolis carolinensis and Other Reptiles DAVID CREWS

I . Introduction ............................................

I1 . Natural History of Anolis carolinensis . . . . . . . . . . . . . . . . . . . . . . 111. Behavioral Repertoire of Captive Anolis carolinensis . . . . . . . . . .

1 3 6

IV . Studies of the Biological Bases of Species-Typical Behavior Patterns . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . V . Studies of the Behavioral Ecology of Anolis . . . . . . . . . . . . . . . . . . VI . Extension to Other Reptilian Species . . . . . . . . . . . . . . . . . . . . . . . . VII . Concluding Remarks . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

44 51 65 66

10

Endocrine and Sensory Regulation of Maternal Behavior in the Ewe PASCAL POINDRON AND PIERRE LE NEINDRE I . Introduction ............................................ 76 I1. Influence of the Endocrine State of the Ewe on the Onset of Maternal Behavior ....................................... 77 111. Influence of the Newborn Lamb on the Development of Postpartum Maternal Behavior . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 88 IV . Mother-Young Relationships beyond the Postpartum Period . . . . . 99 V . Maternal Behavior in Inexperienced Ewes . . . . . . . . . . . . . . . . . . . . 108 VI . Conclusion and Future Prospects of Research . . . . . . . . . . . . . . . . . 113 References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 115

V

vi

CONTENTS

The Sociobiology of Pinnipeds PIERRE JOUVENTIN AND ANDRE CORNET I , Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . I1. Social Structures ........................................ 111. Adaptive Strategies among Phocidae and Oteriidae . . . . . . . . . . . . References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

121 123 133

139

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

I. I1. I11. IV .

Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Repertoires ............................................. Geographical Variation ................................... Conclusion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

143 144 159

170 170

Development of Sound Communication in Mammals GUNTER EHRET

I . Introduction ............................................ I1. Components of Sound Communication Systems: General Aspects of Development . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 111. Time Courses of the Development of Vocal Behavior and Hearing in Subhuman Mammals and Man ........................... IV . Characteristics and Common Tendencies of the Development of Vocal Behavior ......................................... V . Characteristics and Common Tendencies in the Development of Sound Communication . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . VI . Conclusions ............................................ VII . Summary .............................................. References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

179

181

183 198

208 216 216 218

Ontogeny and Phylogeny of Paradoxical Reward Effects ABRAM AMSEL AND MARK STANTON I . Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

I1. Paradoxical Effects of Reinforcement .......................

227 230

CONTENTS

vii

I11 . Frustration Theory as One Mechanism for the Paradoxical Effects 234 236 V . Toward an Ontogenetic Analysis of Paradoxical Effects . . . . . . . . 242 VI . Comments on the Neural Substrate of Paradoxical Effects . . . . . . . 257 VII . Concluding Considerations: Implications for Behavior and Behavior Theory . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 263 References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 267

IV . The Comparative Analysis of Learning ......................

Ingestional Aversion Learning: Unique and General Processes MICHAEL DOMJAN 1. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 276 I1. The Associative-NonassociativeControversy . . . . . . . . . . . . . . . . . 278

111. Poison-Avoidance Learning and the Complexity of the Ingestive

Sequence . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . IV . The Selectivity of Associations in Ingestional Aversion Learning . V . Limitations on Ingestional Aversion Learning . . . . . . . . . . . . . . . . . VI . Conclusion: A Continuing Search for General and Unique Characteristics of Ingestional Aversion Learning . . . . . . . . . . . . . . References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

292 303 318 326 330

The Functional Organization of Phases of Memory Consolidation R . J . ANDREW

I . Phases of Memory in Higher Vertebrates: Evidence from Amnestic Agents . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . I1 . Human Memory . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 111. Models of Memory Formation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1v . Previous Studies of Memory. Using Pecking in the Chick . . . . . . . V . Hormones and Other Enhancing Agents in the Chick: Opposition to Arnnestic Agents . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . VI . Conclusion: General Implications ........................... References .............................................

Index . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Contents of Previous Volumes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

338 347 348 350 352 361 363

369 315

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

ABRAM AMSEL, Department of Psychology, University of Texas at Austin, Austin, Texas 78712 (227) R. J . ANDREW, Ethology and Neurophysiology Group, School of Biological Sciences, Universit), of Sussex, Brighton, United Kingdom (337) ANDRE CORNET, Laboratoire d’Evolution des Vertebres, Universite des Sciences et Techniquesdu Languedoc, 34000 Montpellier-Cedex,France (12I ) DAVID CREWS, Departments of Biology, Psychology and Social Relations, and Museum of Comparative Zoology, Harvard University, Cambridge, Massachusetts 02/38 ( I ) MICHAEL DOMJAN, Department of Psychology, University of Texas at Austin, Austin, Texas 78712 (275) GUNTER EHRET, Fakultat Biologie, Universitat Konstanz, 0-7750 Konstanz, Federal Republic of Germany ( I 79) PIERRE JOUVENTIN, Laboratoire d’Evolution des Vertebres, Universite des Sciences et Techniques du Languedoc, 34000 Montpellier-Cedexx,France (12I J JOHN R. KREBS, Department of Zoology, Edward Grey Institute of Field Ornithology, South Parks Road, Oxford OX1 3PS, England (143) DONALD E. KROODSMA, Rockefeller University, Field Research Center, Millbrook, New York 12545 (143) PIERRE LE NEINDRE, Laboratoire de Production de Viande, I.N.R.A. de Theix, 63110 Beaumont, France (75) PASCAL POINDRON, Laboratoire de Comportement Animal, 1.N.R.A . de Nouzilly, 37380 Monnaie, France (75) MARK STANTON, Department of Psychology, University of Texas at Austin, Austin, Texas 78712 (227)

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Preface With the publication of the eleventh volume of Advances in the Srudy of Behavior, we wish to restate in more contemporary terms the aims stated in the original preface, namely, to serve ". . . as a contribution to the development of cooperation and communication among scientists in our field. " Since that preface was written in 1965, an increasing number of scientists from disciplines as widely separated as behavioral ecology and the biochemistry of behavior have become engaged in the study of animal behavior, employing the specialized techniques and concepts of their disciplines. Even then, the boundaries of ethology and comparative psychology were no longer distinct: now they have been merged with broader syntheses of social and individual functioning and have together provided the bases for studies of the neural and biochemical mechanisms of behavior. 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 engaged in studying animal behavior now range from ecologists through evolutionary biologists, geneticists, endocrinologists, ethologists, and comparative and developmental psychologists, to neurophysiologists and neuropharmacologists. The task of developing cooperation and communication among scientists whose skills and concepts necessarily differ in accordance with the diversity of the phenomena they study has become more difficult than it was at the inception of this publication. Yet the need to do so has become even greater as it has become more difficult. The Editors and publisher of Advances in the Srudy of Behavior will continue to provide the means by publishing critical reviews of research in our field, 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.

xi

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ADVANCES LN THE STUDY OF BEHAVIOR

VOL. I I

Interrelationships among Ecological, Behavioral, and Neuroendocrine Processes in the Reproductive Cycle of Anolis carolinensis and Other Reptiles DAVIDCREWS DEPARTMENTS OF BIOLOGY, PSYCHOLOGY A N D SOCIAL RELATIONS, A N D MUSEUM OF COMPARATIVE ZOOLOGY

H A R V A R D UNIVERSITY CAMBRIDGE, MASSACHUSETTS

I. Introduction . . . . . . . . . . . . . . . . . . ......................... 11. Natural History of Anolis rrrrohe ..... ... ......... 111. Behavioral Repertoire of Captive Anolis carolinmsis . . . . . . . . . . . . . . . . . . . IV. Studies of the Biological Bases of Species-Typical Behavior Patterns . . . . . . A. Hormonal Control of Female Sexual Receptivity B. Stimulus Control of Male Mounting Behavior . . . . . . . . . . C. Sociosexual Control of Seasonal Gonadal Recru D. Hormonal Control of Male Aggressive and Sexual Behavior . . . . . . . . . . Secretion . . . . . . .

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

1 3 6 10 10

17 25

33

37 44 45

................. C. Crocodilians . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . D . Parthenogenetic Lizards . . . . . . . . . . . . . . . . . . . . ......... VII. Concluding Remarks. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . References .......................... ........................

I.

48 51 51 57 59 61 65

66

INTRODUCTION

More than 1 5 years ago Niko Tinbergen ( 1963)argued that to understand fully a naturally occurring behavior pattern, it is necessary to study how the behavior adapts the organism to its environment, how the behavior evolved through his1

Copynphl @ 1980 by Academic Ress. lnc All nghts ofrepmduclim in any form reserved. ISBN 0-12-004511-7

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DAVID CREWS

toric time, how the behavior develops within the organism’s own lifetime, and, finally, the mechanisms underlying the behavior (see also Beach, 1950). Each of these “questions” are today represented in the fields of behavioral ecology, evolutionary biology, behavioral development, and behavioral physiology or physiological psychology. Although the boundaries of these areas are artificial and often times indistinct, it is not uncommon to find that behavioral ecologists know little of the development of the behavior they are investigating. Similarly, few physiological or developmental psychologists know the principles of evolutionary biology or appreciate the potential of an evolutionary investigation of behavior. In addition to the differences in training scientists receive within these different disciplines, the lack of communication between these areas of behavioral investigation can be traced to the ultimate questions being asked and the level of analysis that characterizes the area. Thus, behavioral ecologists and evolutionary biologists have traditionally been concerned with problems above the level of the behavior of the individual organism. Researchers interested in the immediate causation of behavior, on the other hand, have tended to concentrate at or more typically below the level of the behavior of organisms. Such division and specialization, however, was not the intention of Tinbergen. As exemplified by Tinbergen’s own research, the combination and integration of all levels of analysis, cellular, physiological, organismal, and evolutionary, into a single research program make this approach an extremely powerful method for achieving an understanding of the biological bases of behavior. For example, after the behavioral repertoire of the species has been described and quantified, the latest techniques in physiological analysis can be used to study the mechanisms underlying the behavior. Ideally, behavioral hypotheses arising from the laboratory should then be tested in the field to learn what role the behavior plays in the animal’s natural history as well as what constraints the environment places on individual behavior. Although there are relatively few examples of such comprehensive investigations, those that do exist have led to major advances in our understanding of the adaptive significance of behavior and of the forces controlling the behavior of organisms in nature (Dewsbury, 1975, 1978; Hinde, 1965; Hinde and Steele, 1978; Konishi, 1973; Leon, 1974, 1978; Murton and Westwood, 1977; Roeder, 1967, 1974). One reason why there are so few practitioners of this multileveled approach is the difficulty in obtaining an organism that lends itself to such a wide-ranging investigation. Indeed, I believe this problem of suitability is the major reason behind the long-standing differences between field-oriented versus laboratoryoriented behavioral biologists. That is, an animal that a behavioral ecologist might find interesting (e.g., a mountain gorilla) cannot conveniently be brought into a laboratory and expected to behave normally. Conversely, it is rare to find in nature animals as convenient (and genetically similar) as the inbred strains of small mammals commonly used by many laboratory behavioral physiologists.

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3

A candidate species for such a psychobiological approach to the study of behavior should satisfy at least six criteria. The species chosen must not be secretive in its natural habitat but should be obvious and preferably conspicuous. It should reproduce reliably and at frequent intervals in the laboratory and should grow rapidly. This is particularly important if one is interested in studying the developmental and genetic basis of behavior. The species should have an interesting and sufficiently complex social organization. Experimental manipulation of the animal in the field should be possible and, when transferred into seminatural laboratory conditions, the animal should continue to exhibit similar behavioral patterns and social organization to that observed in the field. The species should also belong to a taxon whose members occupy a variety of diverse habitats for it is likely that species that show different behavior patterns as a consequence of different environmental constraints are also likely to differ in the underlying physiological mechanisms. Finally, it would be preferable if there existed some knowledge of the evolution, ecology, behavior, and physiology of the species to be studied on the basis of which experiments can be designed. Many species of the lizard genus Anolis satisfy the aforementioned criteria.

11.

NATURAL HISTORYOF Anolis carolinensis

The genus Anolis consists of more than 200 species found throughout the West Indies and South and Central America. A considerable amount of information on the evolution and ecology of the different anoles has been gathered by Ernest Williams and his colleagues and students (Etheridge, 1960; Huey and Slatkin, 1976; Huey and Webster, 1975, 1976; Kiester e r a / . , 1975; Paul1 et a/.,1976; Rand, 1967; Roughgarden, 1974; Schoener, 1970, 1975; Trivers, 1976; Williams, 1969, 1972; and Yang et uf., 1974). The outstanding characteristic of Anolis is its diversity. Anoles are found in a very wide variety of habitats from montane cloud forest to lowland desert. The adaptive radiation within each life zone is equally remarkable (Fig. I ) with each species specialized to live in different parts of the habitat. Anoles are similar to birds; that is, in multispecies communities they are distributed vertically such that a single tree might contain several species. Typically, one very large "giant" species inhabits the crown and thick branches of the tree while slightly smaller species reside on the tree trunk. Even smaller species tend to be found at the periphery of tree branches, on twigs, in grassy areas, and in the underbrush surrounding the trees. This ecological and evolutionary diversity makes anoles excellent candidates for an investigation of not only ecological principles, but also of behavior and its controlling mechanisms. One species of Anolis, A . carolinensis, is particularIy well suited for study of the ecological aspects of behavioral endocrinology. This species is found throughout much of the southeastern United States and is especially abundant in

-

4

DAVID CREWS

A N O L E RADIATION

.

(sunny area 1

.

(deep shade 1

FIG. I . Andis lizards have undergone an extensive adaptive radiation in Central and South American and in the West Indies. Species differ in (I) body size, with “giant” species of greater than 100 mm snout-vent length to “dwarf” or twig species of less than 50 mm snout-vent length; (11) diameter of preferred perch, with species inhabiting the tree crown to species living in bushes andor grass; and (111) microclimate, with species living in open, sunny areas to species living in deep shade. From Crews and Williams (1977) with permission of the American Society of Zoologists.

Louisiana, reaching densities of more than 1500 lizards per acre (Gordon, 1956); they are most numerous around clearings, forest edges, and in disturbed ecotones. Like most iguanid lizards, the males and females are sedentary, establishing and defending discrete areas against conspecifics. The size and shape of the territories vary depending upon the vegetation, but may average 20 ft in diameter and encompass 400-600 fig.Generation time is short and, if maintained in the laboratory under a constant stirnulatory environmental regimen, A . carolinensis will undergo three to four complete reproductive cycles within a year (Crews, unpublished). Eggs incubate for approximately 6-8 weeks before hatching in the field but in the laboratory a 30-day incubation is common. Young born in the laboratory grow rapidly and are reproductively mature in 6 months; in nature, males grow more rapidly than females and usually are mature before the

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5

winter of their birth (Gordon, 1956). Further, A . carolinensis is a hardy animal, living up to 3 years in captivity. Laboratory housed animals exhibit the same behavioral displays as in nature even if housed in small cages containing only a food dish, drinking tube, and a stick on which to perch (Crews, 1975b, 1977). Finally, more is known of the ecology, behavior, and physiology of this species than of any other reptile, making A . carolinensis the best candidate for a systematic investigation of the psychobiology of reptilian reproduction. Anolis carolinensis breeds in the spring and summer (Fig. 2) with the exact timing and length of the reproductive season varying with geographic locality (Gordon, 1956; King, 1966). In late summer decreasing daylength causes the gonads to regress (Licht, 1971), and the animals enter into a month long refractory period (Crews, 1975c, 1978b). During this time, they are insensitive to the high temperatures which in the spring and summer stimulate and maintain breeding activity (Crews and Licht, 1974; Licht, 1971). Following this refractory period, which in the female is maintained by a substance (probably progesterone) produced by the degenerating follicles (Crews and Licht, 1974), the male and female begin winter hibernation. During the winter, animals can be found singly or clustered in groups beneath the bark of dead trees and under fallen logs or rocks in areas of dense vegetation such as swamps and woods. Although there is some testicular growth at this time (Licht, 1971), ovarian activity is minimal (Crews, 1975c, 1978b). In early spring, the increase in temperature stimulates 0

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FIG. 2. Major physiological and behavioral events in the annual reproductive cycle of the green anole, Anofis carofinensis. See text for further details. From Crews ( 1 9 7 5 ~ ) with permission of the American Association for the Advancement of Science.

6

DAVID CREWS

both the emergence and the final phases of testicular activity in the males, who quickly establish breeding territories. Approximately 1 month later, the females emerge (Gordon, 1956) and establish home ranges within the males’ territories although they may move during the breeding season, establishing another home range. Typically, a single male’s territory will encompass a home range of two or three females and will also contain several subordinate males in the underbrush. During the breeding season which follows, the females show periods of sexual receptivity (Crews, 1973a; G. Gorman, personal communication; Greenberg and Noble, 1944; Stamps, 1975; Trivers, 1976). A considerable amount is known about the daily activity cycle and behavioral ecology of A . carolinensis (Crews, unpublished observations; Gordon, 1956; W. Haas, unpublished manuscript; King, 1966). In the summer, A . carolinensis become active approximately 30-60 min after sunrise, leave their sleeping sites (usually a twig or grass stem), and spend several hours basking. There is some evidence that females sleep in less exposed positions than males (Gordon, 1956). Social displays (see Section 111) are frequent during this period but then diminish and are rarely seen around midday (6-9 hr after dawn) at which time animals mostly feed on small, soft-bodied insects. In the late afternoon, animals again interact frequently and most copulations occur at this time, a fact also noted by Stamps (1975) for A . aeneus in Grenada. Copulations which occur during the morning activity period are usually brief, whereas those in the afternoon are usually of long duration; only after the long matings during the afternoon does the female show behavioral nonreceptivity (see Section IV,A). Lizards move from their territory or home ranges to sleeping perches about 1 hr before sunset.

III. BEHAVIORAL REPERTOIRE OF CAPTIVE Anolis carolinensis Anolis carolinensis exhibit a varied and easily identifiable behavioral repertoire in the laboratory that resembles closely that seen in nature. Assertion, challenge, and courtship displays all share an up-and-down bobbing movement but differ in both the cadence and the patterning of the bobbing as well as in other characteristics (Cooper, 1977; Crews, 1975b, 1979b; Greenberg, 1977; Greenberg and Noble, 1944) (Table I). Male aggressive behavior, which actually is a continuum of agonistic displays, is dramatic and unmistakable (Fig. 3). A sexually active male will patrol his territory, stopping at prominent perches to exhibit the Assertion display. This display is given while standing still and is characterized by a species-typical bobbing movement coordinated with the extension of a red throat fan called the dewlap. If a strange A. carolinensis enters the territory of a male, the resident will immediately challenge the intruder. The Challenge display is identified by an extreme lateral compression of the body and a highly stereotyped, species-typical bobbing movement. If the intruding animal

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TABLE I SOCIAL DISPLAYS I N LABORATORY POPULATIONS O F Anolis carolinensis AND THEIR IDENTIFYINGCHARACTERISTICP Display

Context

Orientation Posture Movement

Dewlap Approach

Assertion

Challenge

Courtship

Submission

Response often seen performed by dominant animal after an aggressive bout or when reaching favorite perch; occasionally seen when animal alone in cage None apparent

Response to strange lizard, subordinate, or toward any displaying conspecific

Response to the introduction of a female or toward any lizard giving submission display

Response to the approach, challenge display or courtship display by a dominant lizard

Oriented toward recipient Laterally compressed Bobbing with forepart of body Extended None, display stationary

Oriented toward recipient Relaxed Bobbing with forepart of body Extended Approaches other lizard, stopping to display

Variable

Relaxed Bobbing with forepart of body Extended None, display stationary

Relaxed Nodding of head only Absent None, display stationary

“From Crews (1975a), with permission.

does not immediately give the Submission display (a rapid nodding of the head) or if it reacts aggressively to the resident male’s challenge, the resident will approach the intruder and a fight will ensue. During a fight, the dewlap is not extended but the entire hyoid apparatus is lowered and the throat region is engorged in both contestants. As the fight progresses, a crest is erected along the back and neck, and a black spot forms immediately behind the eye (the eye spot). It is not uncommon for males to lock jaws while circling one another, each trying to throw the other off the perch. Fights may last several hours, after which the winning male (almost always the resident) will typically climb to a prominent perch and perform a series of Assertion displays. During courtship, the male advances toward the female, pausing to perform a series of bobbing-dewlap displays (Fig. 4). The number of bobbing movements during the Courtship display varies greatly between individual males and so may aid in individual recognition (Crews, 1975b). When approached by a courting male, female A . carolinensis will either flee immediately and hide or remain stationary. As the male nears, the female may begin to whip her tail (TailWhip), indicating nonreceptivity, or remain immobile until the male comes in contact. A

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DAVID CREWS

FIG.3 . Agonistic behavioral displays of the lizard, Anolis carolinensis. (A) A sexually active, temtorial male performs an assertion display. (B) A dominant male performs a challenge display. The extreme lateral compression and engorged throat are the identifying characteristics of the challenge display. See Table I and text for further details.

FIG.4. Mating sequence in Anolis carolinensis. (A) A sexually active male performs a courtship display toward a female. The relaxed body posture ana distinctive cadence of the bobbing movement are characteristic of courtship (see also Table I and text). (B) Female exhibits a neckbend as courting male approaches. This behavior is seen only if the female is sexually receptive. (C) After taking a neck grip, the male mounts the female and intromits one of his two hemipenes.

10

DAVID CREWS

receptive female will then arch her neck (Neckbend), pointing the snout down, as the male grasps her neck skin between his jaws; a highly receptive female will stand and neckbend in response to the courtship display of a male performed at a distance or she may even approach the male and solicit courtship by performing submissive headnods to attract the male’s attention. After taking the neckgrip, the male straddles the female’s back and usually within 1 min of mounting swings his tail to the right or left, trying to appose the cloaca1 regions (see Section IV,B). This is not always successful and the male may twist his body to the right and left several times before intromission is achieved. OF THE BIOLOGICAL BASESOF SPECIES-TYPICAL IV. STUDIES BEHAVIOR PATTERNS

A.

HORMONAL CONTROL OF FEMALE SEXUAL RECEPTIVITY

During the breeding season, the female periodically lays a single egg often in moist leaves or in a shallow hole (Tokarz and Jones, 1979). The interval between egg laying is usually 2 weeks but this may vary with the humidity (Brown and Sexton, 1973) and the species (King, 1966). In all anoline lizards, the ovaries alternate in the production of a single ovum (Smith et al., 1973)and,

FIG.5 . Urogenital system of a reproductively active female Anolis carolinensis. Stippled follicles in both ovaries are yolked (vitellogenic); other follicles are previtellogenic. Note the alternating hierarchial pattern of follicle maturation between the ovaries. See text for further details.

REPRODUCTION IN

Anolis carolinensis

11

within each ovary, the follicles mature in a hierarchical manner (Jones, 1975) (Fig. 5). Typically, a breeding female has one shelled oviducal egg about to be oviposited and, in the contralateral ovary, a large preovulatory follicle. In A . carolinensis, an egg is ovulated once every 10-14 days and, during the breeding season, a female may lay as many as 15 eggs (Crews, 1973a; Hamlett, 1952; Licht, 1973); Gordon (1956), however, estimates from field samples that the average reproductive potential for a single female is seven eggs per season. Coincident with this cycle of ovarian activity are predictable fluctuations in the female’s sexual behavior with estrus (receptivity) occurring prior to ovulation (Crews, 1973a) (Fig. 6). These cycles reflect corresponding fluctuations of circulating sex steroids, although the levels of circulating ovarian hormones during the estrous cycles of lizards are still being investigated. The pattern and sequence of circulating hormone levels during the follicular cycle of both recently captured, breeding females and gonadotropin-stimulated females have been determined. In A . carolinensis as in other oviparous reptiles (cf. Callard rral., 1978), plasmaestradiol levels increase during follicular development, reaching a peak immediately before the surge in progesterone around the time of ovulation (Fig. 7). As would be expected, removal of the ovaries abolishes sexual receptivity in female A , carolinensis (Valenstein and Crews, 1977), and estrogen replacement therapy reinstates this behavior in a dose-related manner (Crews, 1978b, 1979). For example, the threshold dose for the neckbending response, one of the components of female sexual receptivity, appears to be 0.6 pg of estradiol benzoate (EB) (McNicol and Crews, 1979).

I

7

14

21

28

DAYS

35

42

49

56

nonreceptiwe

0

receptive

FIG.6. Relationship between maturation and ovulation of the ovarian follicle and sexual receptivity in Anolis carolinensis. During the breeding season, female A . carolinrnsis undergo cycles of sexual receptivity which are correlated with the maturation and ovulation of a single follicle alternately between ovaries. The exact onset of estrus varies between females, occurring when the largest ovarian follicle is between 3.5 and 6 0 mm in diameter. Females are receptive to male courtship behavior until ovulation or until mating. From Crews (1977) with permission of Sigma Xi.

12

DAVID CREWS

3.0-

0

0

h

r" 2.0-

\

-z c3

0

Elc3

0

0

OO

0 CI

0

I-

.

I/)

w 1.0-

1

0

0

, f,2,",3 AOaO

".'~ I

,

4 5 6 7 8 DIAMETER OF LARGEST OVARIAN FOLLICLE ( M M ) FIG.7. Correlation between diameters of the largest ovarian follicles and plasma levels of estrogen in the untreated- and follicle-stimulating hormone (FSH)-treated female lizard, Anolis carolinensis. Adult female lizards with seasonally inactive ovaries were obtained in February and housed in a laboratory animal colony room. After 1 week in the laboratory, a number of these animals were sacrificed (A). The remaining animals were treated with ovine FSH (10 pg/animal/day) for either 7 (0)or 14 (0) days prior to sacrifice to stimulate ovarian follicular growth. Following sacrifice, the diameter of the largest ovarian follicle in each animal was measured and the plasma estrogen level was determined by radioimmunoassay. Analysis of the data revealed a significant positive correlation between follicular diameters and plasma estrogen levels (r(46)= 0.59, p < 0.01). Sexually active females bled during the breeding season exhibit a similar correlation between follicular diameter and circulating estrogen levels. From Tokarz and Crews, unpublished. I

Females ovariectomized while reproductively inactive and long-term ovariectomized females are much less sensitive to exogenous estrogen; such females fail to show signs of sexual receptivity at the end of 48 hr following an injection of 1.4 pg of EB; pretreatment with low amounts of estrogen (0.2 pg) results in a much more rapid response to suprathreshold estrogen dosages (Fig. 8). It is possible that estrogen receptors in brain areas subserving female receptivity are diminished in these females (Hutchison, 1978; Lisk, 1978).

REPRODUCTION IN

Anolis carolinensis

13

As in many mammalian species (reviewed in Lisk, 1978), progesterone plays a major role in regulating female sexual receptivity. Also, as in some mammals, progesterone in A . carolinensis also appears to be involved in controlling estrous behavior. When administered done, progesterone (up to 160 pg) fails to induce female sexual receptivity (Crews, 1975c, 1978b) but when administered 24 hr after subthreshold estrogen priming (a single injection of 0.4 pg EB), progesterone (60 pg) will synergize with estrogen to facilitate sexual receptivity (McNicol and Crews, 1979) (Fig. 9). This pretreatment with estrogen is neces-

DAYS FIG. 8. Effect of estrogen pretreatment on the induction of female sexual receptivity in the lizard, Anolis carolinensis. Ovariectomized females were injected daily for 3 days with either 0.2 p g of estradiol benzoate (EB) or with steroid suspension vehicle (SSV). The following day (arrow), animals pretreated with EB received a single injection of 0.8 pg EB (circles); females pretreated with SSV received a single injection of 1.4 pg EB (triangles) at the same time. Daily behavioral testing for sexual receptivity began on day 1. Female receptivity was scored as follows: 0, unreceptive, female runs from courting male; I , low receptivity, female allows male to take a neckgrip but then struggles; 2, moderate receptivity, female passively allows male to take a neckgrip and mating is accomplished with little or no struggling; 3, high receptivity and proceptivity , female performs distinct neckbend as male approaches to take a neckgrip, female may also solicit male courtship. Sample sizes are shown in parentheses. From Tokarz and Crews (unpublished).

14

DAVID CREWS

FIG.9. Effects of varying amounts of progesterone on the sexual receptivity of estrogen-primed female Anolis carolinensis. Ovariectomized females were given a single injection of 0.4 pg estradiol benzoate (EB) and a second injection of steroid suspension vehicle (SSV) or progesterone 24 hr later. All females were tested 24 hr following the second injection. Sample sizes are shown in parentheses. From McNicol and Crews (1979) with permission of Academic Press.

sary for the induction of progesterone receptor in the hypothalamus (Crews, Tokarz, and McEwen, unpublished data). Studies of the time course of this facilitatory role of progesterone indicate that progesterone begins to exert its effect within 3 hr of its injection following estrogen priming (Fig. 10). Recent experiments have demonstrated that both luteinizing hormone-releasinghormone

FIG.10. Facilitatory effects of a single injection of 60 p g progesterone (P)or steroid suspension vehicle (SSV) on sexual receptivity in estrogen-primed ovariectomized Anolis carolinensis. All females were primed with a single subthreshold dose of 0.4 pg estradiol benzoate 24 hr prior to injection of progesterone. Sample sizes are shown in parentheses. From Crews (1979a) with permission of the Society for the Study of Reproduction.

REPRODUCTION I N

Anolis carolinensis

15

(LHRH) and thyrotropin-releasinghormone (TRH) rapidly induce sexual receptivity in ovariectomized, estrogen-primed female lizards (Alderete et al., 1980) (Fig. 11). The finding that TRH is capable of stimulating estrus is novel and suggests a major difference in the neuroendocrine regulation of receptivity in female lizards as compared to that of birds and mammals. Experiments with small mammals indicate that progesterone can also inhibit estrus, depending upon when it is administered in relation to estrogen (reviewed in Feder, 1977; Feder and Marrone, 1977; Morin, 1977). This may also be true in lizards. For example, by 72 hr following progesterone facilitation of estrogen-primed ovariectomized lizards, only a small percentage of females are still sexually receptive (see Fig. 10). This decline may indicate an active inhibition by progesterone, since females receiving a single injection of 0.8 p g of EB alone continue to be highly receptive for 1 4 4 hr (Crews, unpublished). Other experiments indicate that a single injection of 160 p g of progesterone 48 hr after 3.0W

LL

1

8 in > t

>

2.0-

W W 0

Qz J

a

3 X W

in

w 1.0-

-I

: c LL

z, Y

453, I

I

I

O.Obre+es+ 2 4 6 / TIME (HOURS) FOLLOWING INJECTIONS

H

4

FIG. 1 1 Both luteinizing hormone-releasing hormone (LHRH) and thyrotropinreleasing hormone (TRH) induce sexual receptivity in ovariectomized, estrogen-primed female Anolis carolinensis. Deamido TRH under the same conditions fails to induce sexual receptivity. Females were pretreated with three daily injections of a subthreshold dose (0.2 pg) of estradiol benzoate (EB). Behavioral tests were conducted 48 hr following the last EB injection. Immediately following the pretest, each female received a single injection of 1000 ng of LHRH (filled circles), TRH (filled triangles), deamido TRH (open triangles), or a comparable volume of steroid suspension vehicle (open circles). Behavioral tests were conducted 2, 4,6, and 24 hr following injection. Sample sizes are shown in parentheses; mean and SEM are shown. See Fig. 8 for explanation of receptivity score. From Alderete er al. (1980) with permission of S. Karger. I

16

DAVID CREWS

a priming injection of 0.8 pg of EB will completely inhibit the effects of the estrogen (Crews, unpublished). Again, the effect of the progesterone is extremely rapid, and the majority of females are no longer receptive within 24 hr of progesterone administration. In many mammalian species, mating has at least two effects apart from sperm transfer and fertilization. First, copulation terminates or markedly reduces female sexual receptivity (Carter and Schein, 1971; Goldfoot and Goy, 1970; Hardy and DeBold, 1972). Second, vaginocervical stimulation arising from mating induces hormonal changes leading to the establishment of corpora lutea necessary for successful pregnancy (Adler, 1974, 1977). In A . carolinensis, intact females are no longer sexually receptive following mating (Crews, 1973b). This transition from receptivity to nonreceptivity (a) is extremely rapid, beginning immediately after the male dismounts, and ( h ) is maintained for several days until ovulation; ovulation in this species appears to be spontaneous. The presence of the ovary is critical for the maintenance of this matinginduced refractoriness (Valenstein and Crews, 1977): if ovariectomized, estrogenprimed females are allowed to mate, they will again be receptive to male courtship in about 6 hr following the mating (Table 11). Intact, reproductively active females, on the other hand, continue to be unreceptive to male courtship for several days if treated with estrogen. This suggests that the presence of the ovaries or some change in ovarian hormone production (progesterone?) is critical for long-term inhibition of female sexual receptivity. Intromission of the hemipenis by the male is a critical component underlying inhibition of female sexual receptivity. Intact, preovulatory females that are

INFLUENCE

TABLE I1 OVARIES ON POSTCOPULATORY SEXUAL RECEPTIVITY THE FEMALE L I Z A R D , Anolis carolinensis"

OF T H E IN

Treatment Sham-operated females A. 0.8 pg EB injection B . 6 mm EB implant Ovariectomized females C. 0.8 f i g EB injection C. 6 mm EB implant

Number initially receptive

Percentage receptive 24 hr after copulation

9 5

22% 20%

9

1 OO%b

15

93%'

From Valenstein and Crews ( I 977). with permission * p <0.001. pp <0.005. 'I

REPRODUCTION IN

Anolis carolinensis

17

courted and mounted but not mated continue to be receptive (Crews, 1973b). The precise copulatory stimulus triggering this inhibition of female receptivity, however, is still unknown. One possibility is the duration of male intromission: this may involve a cumulative effect since females interrupted during mating continue to be receptive until they are allowed to mate to completion. Another possibility is that the deposition of ejaculate in the female’s reproductive tract may terminate female receptivity. The initial facilitatory and later inhibitory influences of progesterone on female sexual behavior and the copulation-induced termination of estrus in A . carolinensis suggest that a neuroendocrine reflex triggered by mating may control sexual receptivity in the lizard as in small mammals. Presumably, estrogen and progesterone released from the developing follicle synergize to facilitate estrous behavior. The sensory stimulation received from the male during mating initiates the postcopulatory inhibition phase which is then maintained hormonally until ovulation.

B. STIMULUS CONTROL OF MALEMOUNTINGBEHAVIOR In mammals and birds, peripheral sensations from the secondary sex structures play an extremely important role in the coordination and completion of speciestypical behavior patterns (Adler, 1978; Diakow, 1974; Komisaruk, 1978). Recent studies indicate that the squamate reptiles (lizards and snakes) provide a unique vertebrate model for studying the peripheral sensory control of behavior and for investigating the lateralization of the neural control of species-typical mating behavior. The lizards and snakes are the only vertebrates having bilaterally symmetrical, yet functionally separate, urogenital tracts complete with two intromittent structures called hemipenes (Fig. 12). During mating, the male curves his tail beneath the female’s tail so as to appose the cloaca1 regions and he everts a single hemipenis. (It is possible to determine quickly which hemipenis the male is using by simply noting the direction the tail is angled; if a male is on the female’s left side, he will intromit the right hemipenis by curving the tail to the right and vice versa.) Observation of individual males has revealed that males tend to alternate in their use of the right and left hemipenes (Fig. 13). Although some males appear to prefer one hemipenis, none of the males mated more than three times in succession with a single hemipenis. Recently, Zweifel (1979) has reported that in the king snakes (Lampropelris),the male never uses the same hemipenis in successive matings. Sensory stimuli from the hemipenis play a major role in the control of both the initial orientation of the male during copulation (Fig. 14) and the male’s termination of copulation (Crews, 1973b, 1978a) (Table III). This is in agreement with studies on mammals which indicate that sensory feedback from the penis is

18

DAVID CREWS

VAS DEFERENS

HEMIPENIS

I FIG. 12. Urogenital system of the male lizard, Anolis carolinensis. All squarnate r e p tiles (lizards and snakes) have functionally separate, bilaterally symmetrical urogenital tracts complete with two intromittent organs known as hemipenes. Note that the vasa deferentia from the testes do not join into a medial collecting duct as in mammals. See text for further details. From Crews (1978a) with permission of the American Association for the Advancement of Science.

necessary for normal species-typical mating behavior (Larsson, 1979). Experiments in which males were unilaterally castrated also indicate that proprioceptive feedback from the testes has a similar but less pronounced influence on the male's copulatory posture (Fig. 14). These behavioral findings in A . carolinensis are best interpreted in terms of recent reports of a contralateral neural connection between each gonad and specific hypothalamic nuclei in mammals (Burden, 1978; Gerendai and Halasz, 1978; Gerendai et al., 1976; Van den Pol, 1975). A functional interpretation of this pattern may also be suggested: the hemipenile alternation that is observed in successivecopulations in A . carolinensis may serve to ensure an adequate number of mature sperm for each mating.

REPRODUCTION IN

Anolis carolinensis

19

Recent experiments indicate that the female's behavior is also important in determining the male's mounting behavior, a possibility that was overlooked in the initial investigations because the majority of stimulus females used were ovariectomized and estrogen-primed. The unique pattern of ovarian activity in anoline lizards as well as the fact that the ostium of the oviduct encapsulates the preovulatory follicle (see Fig. 5 ) , ensuring that it is transported into the ipsilateral oviduct upon ovulation, led to experiments aimed at determining whether the ovarian state of the female is related to the side on which the male ultimately copulates with the female. In initial experiments completed during the breeding season, it was found that in all but one instance males mounted recently captured females on the side opposite the ovary containing the preovulatory follicle (Fig. 15). For example, females, mounted on the left such that the tail of the male was curved to the right (right hemipenis intromitted), were later found to have the largest preovulatory follicle on the right. Further studies with intact, reproductively inactive females given gonadotropin injections to stimulate follicular development yielded similar results (Fig. 15). Gonadotropin stimulation of ovarian growth frequently disrupts the hierarchical alternation in follicle size, resulting in the follicle opposite the preovulatory follicle being larger than normal (Licht, 1970). This may account for the greater number of males mounting on the "wrong" side of the gonadotropin-stimulated females. Bilaterally ovariectomized, estrogen-primed females ( n = 101 matings) as well as intact, gonadotropin-stimulated females with follicles equally large in both ovaries ( n = 13 matings) are as likely to be mounted on the right as on the left side.

Lizard

Hernipenis used

Total Riaht Left

lntact norma/

2 3

5 6 A

8 C

F G H J

LLRLRLRLRLR LLRLRL

5 2

LRLLRLL LLRLRRLR RLRLRR

2

5

4

4

4 5 5

RLLRRL

4 3 3

2 1 1 2 3 3

RLRRLR

4

2

RRRLRR RRRLRR LRRRLR RLRRLL

6 4

FIG. 13. Male Anolis carolinensis tend to alternate in their use of the right (R)and left (L) hemipenes in successive matings. Although some males appear to prefer mounting with a particular hemipenis (e g . , B and C), it is rare for malesto use the same hemipenis more than twice in succession.

20

DAVID CREWS Lizord

A -___

Intact Hemipenis

Hemipenis used

~

Total Right Left

_

_

Uni/aferaf hernipeneclomy

3 5 6

R

a

L

/G?@b

C

L

J

L

B

Lizard

Io! '

!

\

RRRRRRRR RRRRRRRR RRRLRRRR LLLLLL LLLLLLLL LLLLLLLL

R

R

Intact

8 8 7 0

0 0 1 6

0

8

0

8

Total Riaht Left

Hemipenis used

Uni/atera/ costratm 3 R RRLRRRLRLRLR 4 L RRLLLRLLL 5 L LLLLLRLL R RLRLRRLRRRLRR L RLLLRLLRLRRLLLRL R LRLRLRRLRR L LLRLRLLRL 10 R LRRLLRRRLRRLLRLR

0 3 1 9 6 6 3 9

4 6 7 4 10 4 6 7

( X 2= 9 32,p e 01)

C

Lizord

I

Hemipenis used

Total Riaht Left

2

LLRLRR RRLRLLR

3 4

3 3

II 12

LRRLRL LRRRLRRLR

13

RRLRLRRLLRLRRLR

3 6 9

3 3 6

15

2 3 4 4

Unilateral casfrafian 8 hemipenecforny

14-1

RRRRLRRRRRRRRRRRL

15-C 16-1 17-C

RLLRRLR LLLL RRRLRRLRLL

4 0 6

I = ipsiloterol C = controloteral

FIG.14. Proprioceptive feedback from the hemipenes and testes directs male mounting behavior in the green anole lizard, Anolis carolinensis. (A) Removal of one hemipenis subsequently causes the male to mount the female so as to use the remaining hemipenis. (B) Unilateral castration results in a shift in male mounting behavior such that the male mates on the side with the intact testes. (C) Bilaterally hemipenectomized or castrated males mount females equally often on the left as on the right side. Removal of one testis and its ipsilateral hemipenis results in a marked shift in mounting behavior; males in which one hemipenis and the contralateral testis are removed alternate in their mounting behavior. R, right; L, left.

REPRODUCTION I N

TABLE 111 REMOVAL OF THE HEMIPENES INCREASES COPULATION TIMEI N Anolis Intact

Male 1 2 3 4

21

Anolis carolinensis

carohensis"

Hemipenec tomized

Number of matings

Mean time (sec)

Number of matings

Copulation time (sec)

7 4

728 320 665 1202

2

2138, 2808 1198 2370, 3975,4343 3185

3 3

I 3 I

Modified from Crews (1973b).

Removal of one ovary altered male mating patterns such that males were more likely to mount on the ovariectomized side rather than on the side with the intact ovary (Fig. 16). However, it is possible in these experiments that the suture material left in place following unilateral ovariectomy caused some local initation, so that some of the females allowed males to mount on the side opposite the ovariectomized side. Removal of a single oviduct had no influence on the mating posture

INTACT, REPRODUCTIVELYACTIVE FEMALES OVARY WITH LARGEST FOLLICLE

k: -1 , 1 ," r-

HEMIPENIS USEDDURING MATING

~~

5

p = 003, C =

65

INTACT, FSH - STIMULATED FEMALES OVARY WITH LARGEST FOLLICLE

+-Rm/ HEMIPENIS USED DURING MATING

-Left 1

-

] ;L

1-

9

3 1

p = 044, C

I

39

FIG. 15 Dissection of copulating female Anolis (arolrrirnvs captured during the breeding season reveals a significant correlation between the side on which the male mounts the female, and hence the hemipenis used, and the ovary containing the preovulatory follicle (A) Winter dormant females that have received daily injections of 10 pg mammalian follicle-stimulating hormone (FSH) for 10-14 days mate in a similar manner (B). Fisher's exact probability test and contingency coefficient ( C ) are shown

22

DAVID CREWS

UNILATERAL OVARIECTOMY (FSH -STIMULATED FEMALES)

(a I

OVARY WITH LARGEST FOLLICLE

MATING

UNILATERAL OVIDUCTECTOMY (FSH-STIMULATED FEMALES)

(b I E;;:NG MATING

REMAINING WIDUCT

+:j p = 338, Ca. 05

(C

I

OVARY WITH LARGEST FOLLICLE

" I HEMIPENIS

p=.036; C s . 4 8

FIG.16. The side on which a male Anolis carolinensis mounts the female is influenced by removal of one ovary (a) but not by removal of one oviduct (b). Reanalysis of male mounting behavior of unilaterally oviductectomized females according to the ovary containing the largest follicle, however, reveals a relationship between ovarian condition and side on which the female is mounted (c). Females having ovaries with equally large

follicles in both ovaries were excluded from analysis. the male assumed ( n = 22, p = 0.338, C = 0.05),but reanalysis of these data according to ovarian state again revealed that females tended to be mounted on the side opposite that containing the largest follicle ( p = 0.036, C = 0.48). Finally, to determine if the presence of an egg in the oviduct influences male mounting behavior, a thread was surgically implanted in the magnum of one oviduct. There was no relationship between the oviduct receiving the thread and the side of the female the male mounted ( n = 10, p = 0.392, C = 0.00). However, when male mounting behavior was analyzed according to ovarian state of the female, males were found to tend to mount opposite the ovary containing the largest follicle ( p = 0.117, C = 0.60). The results of these experiments suggest either that the male is capable of detecting which ovary contains the preovulatory follicle or, more likely, that the

REPRODUCTION IN

Anolis carolinensis

23

female maneuvers the male to mount on a particular side. Although the stimuli directing male mounting behavior have been identified (Fig. 17), the functional significance of the relationship between the side on which the male mounts the female and the ovary containing the preovulatory follicle is as yet unknown. Studies in which mating pairs were frozen in copula and the urogenital systems dissected free and serially sectioned reveal that during copulation the hemipenis is positioned in the female’s cloaca such that the apical openings of the sulcus spermaticus are directly opposite the openings to the oviducts (Conner and Crews, 1980) (Fig. 18). By killing females at varying intervals following mating,

FIG. 17. Schematic illustration of the relationship between the side on which male Anolis carolinensis mount females and the female’s ovarian condition.

FIG.IS. Structure and function of male and female reproductive organs in the lizard, Anolis carolinensis. (A) Apical view of everted left hemipenis of the lizard, A . carolinensis. Note calyces and two apical openings (AO) of the sulcus spermaticus (SS). (B) Longitudinal section of the male’s hemipenis and female’s cloaca in copula. Note that the sulcus spermaticus bifurcates into two apical openings (AO) and the opposition of right A 0 with oviducal opening (00); left A 0 and 00 not in plane of section.

REPRODUCTION I N

Anolis carolinensis

25

FIG. 19. Stereo pair scanning electron micrographs of tubule area inside oviduct wall of female Ariolis carolinensis. Lumen (LU) runs from lower left to upper right. Several sperm storage tubules (ST) appear with ends cut off. Note fold fusing (FF) into tubule middle left. (Stereo pair should be viewed from either the left or right sides using stereo glasses.) Magnification: X200. From Conner and Crews (1980) with permission of Wistar Press.

it has been possible to monitor sperm transfer and transport in the oviduct. These studies indicate that sperm are funneled into sperm storage ducts located in the uterovaginal transition of the female's reproductive tract (Fig. 19). C.

SOCIOSEXUAL CONTROL OF SEASONAL GONADAL RECRUDESCENCE

If winter dormant, reproductively inactive males are exposed to long days (above 12.5 hr) and warm temperature (above 30°C), pituitary gonadotropin is

26

DAVID CREWS -Mole

-

Male Aggression O------.O Male Assertion *---*Mole-Male Aggression/ Mole Assertion a-• Male Courtship

I

2

3

i

WEEKS

FIG. 20. Transition in aggressive and sexual behavior in winter dormant male Anolis carolinensis upon exposure to a stirnulatory environmental regimen. See text for further details. After Crews (1974a).

secreted, and this, in turn, causes gonadal androgen secretion and sperm production (Licht, 1971). This increase in testicular activity leads to a change in behavior in a newly emerged group of males, with aggressive behavior initially predominating (Fig. 20). As a single male of the group becomes dominant over the other males in the cage, male challenge behavior becomes less frequent and assertion displays (by the dominant male) more frequent. Male courtship behavior begins with the emergence of a dominant male; the dominant male in the group does not allow other (subordinate) males to court and mate the females. The courtship behavior of the male has an important influence on the reproductive physiology of the female. Reproductively inactive, winter dormant females, exposed to a stimulatory environmental regimen, either alone or when housed with other females, show some ovarian growth (Crews el a l ., 1974) (Fig. 21). But if they are also exposed to a sexually active male, the rate of ovarian recrudescence and the number of females ovulating is increased significantly. Other experiments show that it is the courtship behavior of the male that facilitates the stimulatory effects of the environment and is necessary for normal pituitary gonadotropin secretion in the female (Crews, 1974a). Moreover, the amount of gonadotropin secreted by the female is correlated with the amount (frequency) of male courtship behavior to which she is exposed (Fig. 22). Ritualized behavior patterns, such as male courtship, are species-typical, consisting of integrated sequences of discrete motor components or acts. Which aspects of the display are responsible for producing this long-term physiological response in the female? To answer this question, the stimulus configuration

REPRODUCTION IN

27

Anolis carolinensis

presented by the courting male to the female was altered by either removing the portion of the hyoid apparatus responsible for dewlap extension (Fig. 23) or injecting India ink subcutaneously into the gular area (Crews, 1975b). This produced males that otherwise courted frequently but either could not extend the dewlap, or displayed a dewlap color different from the reddish pink color typical of animals from around New Orleans, Louisiana. Ovarian growth in females housed with males that extended the wrong color dewlap was comparable to that shown by females housed with red-dewlapped males after 2 weeks (Fig. 24). In contrast, females housed with hyoidectomized males, who could not extend the dewlap but otherwise courted normally, exhibited significantly slower ovarian gowth; the rate was almost identical to that of females exposed to castrated, sexually inactive males. These results suggest that it is the ability of the male to change his body shape and not the color of the dewlap that is critical for courtship facilitation of ovarian growth. Male assertion and challenge behavior, on the other hand, completely inhibit the stimulatory effect of long photoperiod and warm days on female ovarian

I

2

3

4

5

6

Weeks

FIG. 21. Patterns of ovarian recrudescence exhibited by winter dormant female Anolis carolinensis exposed to a stirnulatory environmental regimen in isolation or with conspecifics. Sample sizes are shown by each point. From Crews et a / . (1974) with permission of J . B. Lippincott Company.

28

DAVID CREWS

FIG.22. Ovarian response of winter dormant female Anolis carolinensis exposed to high versus low frequencies of male courtship behavior. All females were exposed to the same stimulatory environmental regimen. Sample sizes are shown in parentheses. Modified from Crews (1974a).

FIG. 23. Hyoid apparatus of the male lizard, Anolis carolinensis.

REPRODUCTION IN 100

-

90

-

Anolis carolinensis

29

Field control ul

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0 Intact male

0 Blue-dewlapped male

A Hyoid-x male

A

Castrated male

0

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70-

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50-

ul

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._ 3

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FIG. 24. Patterns of environmentally induced ovarian recrudescence exhibited by winter dormant female Anolis ctrrolinensis exposed to the courtship of different stimulus males. Field control represents samples of freshly captured females. Sample sizes are shown by each point. Redrawn from Crews (1975a).

development. In one experiment, winter dormant females were exposed for 6 weeks to predominantly male-male aggressive behavior (consisting mostly of challenge displays) by housing them with six sexually active males, each of whom was dominant in its home cage (Crews, 1974a) (Fig. 25). Other females were exposed to predominantly male courtship (i.e., the behavioral display of a dominant male most frequently seen in cages containing one dominant male and five subordinate males) for 3 weeks either following (aggressiodcourtship group; Fig. 25) or preceding (courtship/aggression group; Fig. 25) 3 weeks of aggression. There was a low, unchanging level of ovarian development among females exposed to male-male aggression for the entire 6-week period (Fig. 26). Females exposed to male-male aggression for the first 3 weeks showed a comparable low level of ovarian activity initially, but when the social stimulus was changed to male courtship, there was a very rapid increase in ovarian development. Finally, females initially exposed to male courtship exhibited the immediate and marked facilitation of ovarian growth as expected, but upon reversal of the social conditions, ovarian activity declined. This is the first demonstration that female observation of aggressive behavior between males (predominantly male challenge displays) actively inhibits ovarian growth. These findings further illustrate how female reproduction can be turned “off” as well as “on” simply by varying the cociosexual environment.

30

DAVID CREWS COURTSHIP / AGGRESSION GROUP Courtship Phase

I

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Aggression Phase

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4

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AGGRESSION / COURTSHIP GROUP

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Aggression Phase

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AGGRESSION GROUP

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Weeks FIG.25. Relative frequency of aggressive and sexual behavior of males in different experimental groups. See text for further details. Redrawn from Crews (1974a).

The lack or decrease in ovarian development among females exposed to male-male aggression cannot be considered an instance of “nonactivation, ” or to be due to a lack of courtship stimulation. An increasing number of females exposed to male-male aggression during the latter half of the experiment showed follicular atresia and no new follicular cycle was initiated. In addition, the recent demonstration of an endogenous circannual ovarian cycle in A . carolinensis (Crews and Garrick, 1979) combined with the observation that freshIy captured females were undergoing recrudescence at a time when the majority of females

REPRODUCTION IN

Anolis carolinensis

31

exposed to constant male-male aggression had inactive ovaries would further argue for an active inhibition of ovarian development. If the inhibition effect was indirect, and due to crowding and not aggression, females exposed to different male behavior patterns but housed under otherwise identical experimental conditions would be not expected to exhibit as strikingly different patterns of ovarian activity as they did. Finally, to counter the argument that it was perhaps the absence of courtship and not the presence of male-male aggression that inhibited ovarian growth, it should be remembered that females exposed to castrated males, who show neither courtship nor male-male aggression, exhibit significant ovarian development. It would be of considerable interest to know if this inhibition is mediated by the pituitary-gonadal axis or the pituitary-adrenal axis. That females housed with castrated males, who are neither aggressive nor sexual, as well as females exposed to other females or females exposed solely to the stimulatory environmental regimen, show a gradual increase in ovarian condition suggests 0 Fleld Control

+ Aggression /Courtship Group

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Group

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f

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Weeks FIG. 26. Patterns of environmentally induced ovarian recrudescence exhibited by winter dormant female Anolis cardinensis exposed to different sociosexual conditions (see Fig. 25). Sample sizes are shown by each point. Redrawn from Crews (1974a).

32

DAVID CREWS

that the perception of male-male aggression actively suppresses pituitary gonadotropin secretion in the female. Although the stimulus responsible for this physiological response is unknown, it is possible that the lateral compression of the body characteristic of male challenge display is the critical cue in the suppression of the environmental induction of ovarian growth. Although the dewlap is not extended during challenge behavior, this would not be expected to contribute to the lack of ovarian activity (see preceding). Alternatively, the absence of ovarian growth in the females in cages in which male-male aggression is the predominant behavior pattern may be stress-related, a finding reported for a variety of vertebrate species (Christian, 1971). Note, however, that the effect of A . carolinensis is not due to malnutrition; females living in cages with high frequencies of male-male aggression feed unmolested and their nutritional condition is comparable to that of females housed in socially stable cages (Crews, 1974a). Taken together, these experiments suggest that male courtship ensures normal gonadotropin secretion, that the absence of male courtship results in subnormal gonadotropin secretion (as indicated by the laying of unshelled eggs (Licht, 1973) by females exposed to castrated males, other females, or solely to the stimulatory environmental regimen), and that the presence of male-male aggression inhibits or greatly reduces environmentally induced gonadotropin secretion. These experiments also provide a plausible functional explanation for the differential emergence of males and females following winter reproductive inactivity in many seasonally breeding animals. In the spring, aggression between the newly emerged (or arriving) males predominates on the breeding grounds as territories are established. Usually, it is only after territorial boundaries stabilize that the females appear and courtship and pair-bonding, if it is to occur, begins. The results with A . carolinensis suggest that those females arriving on the breeding grounds after the males would have a selective reproductive advantage over those females arriving along with the males. That is, not only would the “early” females be exposed to predators for a longer period, but they would also be exposed to male aggressive behavior as the males compete for territories. These females would be unable to offset the longer period of time they are vulnerable to predators with a corresponding increase in reproductive effort. Females that arrive after the males, on the other hand, would initiate reproduction rapidly because of the stable social conditions and the predominance of stimulating male courtship behavior from males holding territories, and, of course, they would be exposed to predation for a shorter period. The presence of females has a dramatic effect on testicular activity of the male. Males housed with females have, within 3 weeks, a significantly more rapid rate of testicular growth and are at more advanced stages of spermatogenesis than males housed with other males (Fig. 27). Experiments are currently in progress to determine which female behavior patterns are responsible for the

REPRODUCTION I N 6.0-

5'0-

0--0

Anolis carolinensis

33

field control

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all male group

L,Lg KPTEMBER

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OCTOBER

20

30

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NOVEMBER

40DAY?

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DECEMBER

I

70

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00

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FIG. 27. Patterns of environmentally induced testicular recrudescence exhibited by winter dormant male Anolis carolinensis housed with females and/or males. Sample sizes are shown in parentheses; mean and standard error of mean are shown. From Crews and Gamck (1979) with permission of Society for the Study of Amphibians and Reptiles.

acceleration of testicular growth. It is likely that the male and female are exerting reciprocal effects on one another but that these may differ when a female is caged singly with a male or as a group (Fig. 27). Thus, the initial acceleration followed by lower testis weight in males from the isolated malefemale pair may reflect the more rapid ovarian response shown by females housed under this condition (see Fig. 21). Recall that once ovarian activity is initiated, females exhibit regular cycles of sexual receptivity and that following mating, females are unreceptive to males. In the group housing situation, the large number of females ensures that there would always be females receptive to the male's courtship (there is no evidence for estrus synchrony in this species), hence female stimulation would be expected to be maintained at a continuously high level in this situation. It is also possible that the lowered rate of testicular development in all-male groups might represent an inhibitory effect of males on one another (similar to their effect on females when they are exhibiting aggression). CONTROL OF MALEAGGRESSIVE A N D SEXUAL D. HORMONAL BEHAWOR

Male sexual behavior in A . carolinensis is seasonal (Fig. 28, top) and is under the control of testicular androgens. Castration causes a rapid decline in male

34

DAVID CREWS

FIG.28. Hormonal control of male reproductive behavior in Anolis carolinensis. Top: Relationship between plasma testosterone levels and behavioral and physiological events in the annual reproductive cycle of the male lizard Anolis carofinensis. Modified from Crews (1975). The number of animals assayed in each monthly sample are as follows: N = 6; D = 1 0 J = 14; F = 10; A = 10; M = 17; J = 8; S = 12. Tokarz and Crews (unpublished). Bottom: Effect of castration and androgen (testosterone) replacement therapy on the sexual and aggressive behavior of the male lizard, Anolis carolinensis. In these experiments, sexually active males were castrated after baseline levels of sexual and aggressive behavior were determined. Two weeks following castration, males were given Silastic implants (0.06 cm i.d. x 0.12 cm 0.d.) containing testosterone subcutaneously. Males were tested daily first with a male intruder and then with a female intruder for 15 min each. Mean and SEM are shown; n = 12. From Crews (1979a) with permission of the Society for the Study of Reproduction.

courtship behavior, and androgen replacement therapy reinstates this behavior to precastration levels (Crews, 1974b; Crews et al., 1978) (Fig. 28, bottom). Aggressive behavior, however, is not as affected by castration as male courtship behavior, but is strongly influenced instead by environmental factors. For example, if a male is returned to his home cage following castration, aggressive behavior declines only gradually, whereas if he is placed in an unfamiliar cage, aggressive behavior decreases much more quickly (Crews, 1974b). It has long been assumed that in vertebrates, male reproductive behavior is caused by the direct action of androgens on the brain. An alternative hypothesis (known as the androgen aromatizationhypothesis; Naftolin el al., 1975)proposes that in the brain testosterone serves as a precursor, or prohormone, that is converted by aromatase enzymes to estrogens (e.g., estradiol) before activating behavior. In stimulating secondary sex structures, on the other hand, testosterone is believed to act directly or to be converted to nonaromatizable metabolites such

REPRODUCTION IN Anolis

35

carolinensis

as 5a-dihydrotestosterone. Several studies now indicate that aromatization of androgens to estrogens occurs normally in the brain of many (but not all) mammalian species and that estradiol, not testosterone, activates male sexual behavior (reviewed in McEwen et al., 1979). Significantly, aromatase enzymes have been identified and localized in the brain of turtles and snakes (Callard et al., 1977, 1978). Callard and co-workers also reported that incubation of specific parts of the brain (hypothalamic and strioamygdaloid areas) with radioactive androgen (androstenedione) yields labeled estrone and estradiol. This discovery has led to the proposition that androgen aromatization is a phylogenetically ancient property of the vertebrate central nervous system (Callard et al., 1977). However, before the androgen aromatization hypothesis can be generalized to reptiles, it is essential to test the effect of aromatizable and nonaromatizable androgens on reptilian reproductive behavior. Lizards are well suited to such an investigation. In both lizards and snakes, the distal collecting ducts of the kidney (renal sex segment) are modified to produce a seminal fluid (Fox, 1977); the renal sex segment is thus homologous to the prostate and seminal vesicles of mammals. Activity of the renal sex segment, which is very sensitive to androgen stimulation (Prasad and Reddy, 1972), can be measured by epithelial cell height of the tubules. Using the renal sex segment as

;POST-

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HORMONE TREATMENT

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FIG.29. Effect of castration and subsequent hormone replacement therapy on sexual and aggressive behavior in male Anolis c.nru/inensis. Total mean frequency and standard error of mean in nine daily 15-rnin tests over a 14-day period are shown. Chol., cholesterol; E, estradiol; DHT, dihydrotestosterone; T , testosterone. From Crews (l978b) with permission of Raven Press.

36

DAVID CREWS

an indicator of peripheral action and the stimulation of behavior as an indicator of central action, we have conducted experiments in which castrated male lizards ( A . carolinensis) were given subcutaneous Silastic implants of testosterone (aromatizable), dihydrotestosterone (nonaromatizable), and estradiol (Crews et af., 1978). Histological examination revealed that both testosterone and dihydrotestosterone stimulated development of the renal sex segment in castrated males while estrogen-treated males had atrophied tubules similar to those of males whose pituitaries had been removed (Gerrard, 1974). Only testosterone reinstated male behavior (Fig. 29); dihydrotestosterone or estradiol were without effect. The ineffectiveness of dihydrotestosterone and estradiol when administered separately does not prove that estradiol does not act centrally, however. Several workers have shown that the administration of dihydrotestosterone and estradiol simultaneously will stimulate copulatory behavior in castrated male rats, whereas these hormones, when given alone, are ineffective (Baum and Vreeburg, 1973; Feder et al., 1974; McDonald et al., 1970). Such results have led

0

L Behavioral Test

FIG. 30. Effect of dihydrotestosterone and estradiol in combination on male courtship behavior of castrated, sexually inactive Anolis carolinensis. Animals were assigned to one of two groups on the basis of their courtship behavior following hormone administration. Group I (responders, filled circles, n = 10) included castrates exhibiting levels equivalent to or greater than that shown while intact. Group I1 (nonresponders, open circles, n = 10)included castrates exhibiting no significant change in courtship frequency. see text for further details. Modified from Crews et al. (1978).

REPRODUCTION IN

Anolis carolinensis

37

to the suggestion that both the central effects of estradiol in the brain and the action of dihydrotestosterone on the peripheral secondary sex structures are required in male reproductive behavior. In support of this hypothesis, two reports (Davidson, 1977; Davis and Barfield, 1979) have shown that intracranial implants of estradiol benzoate into the brain of castrated male rats will induce sexual behavior, but only if dihydrotestosterone is administered systemically at the same time. We examined this hypothesis by giving castrated lizards dihydrotestosterone and estradiol simultaneously. The results were striking (Fig. 30). In each of two separate replications, half of the animals suddenly exhibited the complete pattern of reproductive behavior, including mounting and mating, within a single testing period, while the rest failed to show any significant increase in behavior. This is a very different pattern from that shown by castrates receiving testosterone replacement therapy; testosterone gradually restores behavior, with mounting appearing several days after courtship displays. The marked variation in hormone sensitivity within a species found in nature could be a result of differences between local populations (our anoles are collected from a variety of sites outside New Orleans,Louisiana). This may be a naturally occurring example of differences in behavioral sensitivity to exogenously administered androgens that has been found among strains of highly inbred mammalian species (McGill, 1977, 1978a). These differences may be due to enzyme differences (in brain aromatase?) in responding and nonresponding individuals (Shire, 1976). CONTROL OF MALEREPRODUCTIVE E. NEUROENDOCNNE BEHAWOR A N D GONADOTROPIN SECRETION Recently we have undertaken an extensive investigation of hormone-brainbehavior interactions in A. carolinensis (Crews, 1979). However, rather than arbitrarily destroying and stimulating different brain sites to determine their involvement in the control of reptilian reproductive behavior and function, we first identified and localized the sex steroid concentrating sites in the brain of A . carolinensis using autoradiography (Morrell e f al., 1977, 1979). The results of this study show that in this lizard species, as in all other vertebrate species that have been studied to date (Morrell et al., 1975; Morrell and Pfaff, 1978), sex steroid hormones are concentrated in specific areas of the brain including the pituitary, the preoptic area, the anterior and basal hypothalamus, and the limbic system (Figs. 31 and 32). Moreover, no differences were detected in the pattern of hormone uptake between male and female lizards although in both sexes there were differences in the distribution of androgen versus estrogen concentrating sites. For example, only after androgen administration were many well-labeled cells found in the mesencephalic tegmentum where they appeared just caudal to the red nucleus and extended to the oculomotor nucleus as well as the torus semicircularis.

38

DAVID CREWS

FIG.31. Representative transverse sections through the brain of Anolis carolinensis following administration of ["Hlestradiol. The distribution of labeled cells is indicated on the right side of each figure by black dots; each dot represents a labeled cell. Brain structures are identified on the left of each figure. (A) Level of the medial preoptic area. (B) Level of the anterior hypothalamus. (C) Level of the basal tuberal hypothalamus. (D) Level of the torus semicircularis. AHA, anterior hypothalamus; A, -&, amygdaloid nuclei; CG, central grey; CTX, cortex; DVR, dorsal ventricular ridge; LFB, lateral forebrain bundle; LHA, lateral hypothalamic area; LFQA, lateral preoptic area; MPOA, medial preoptic area; OC, optic chiasm; OT, optic tract; PH, nucleus periventricularis hypothalami; PO, nucleus posterior hypothalami; PR, nucleus premammallaris; S , septum; SC, suprachiasmatic nucleus; TECTUM, optic tectum; TORUS, torus semicircularis; VE, ventricular ependymal organ; VMH, nucleus ventromedialis hypothalami. From Crews (1979a) with permission of the Society for the Study of Reproduction.

A large body of research with mammals and birds indicates that the anterior hypothalamus-preoptic area is a hormone-sensitive behavioral integrative area (literature reviewed by Crews and Silver, 1980; Davidson, 1977; Komisaruk, 1978). Since this area is a major site of steroid hormone uptake in A . carolinensis, we chose to examine its role in the regulation of male reproductive behavior first (Fig. 33). Lesions of this area in intact (i.e., sexually active) males and in castrate, androgen-treated males caused an immediate and rapid decline in both sexual and aggressive behavior (Wheeler and Crews, 1978) (Fig. 34). Lesions rostra1 to this area also reduced reproductive behavior in intact males, but this effect appeared to be due to the destruction of gonadotropin-releasinghormoneproducing cell bodies in this area (Wheeler and Crews, 1978). Implantation of

REPRODUCTION IN

Anolis carolinensis

39

minute amounts of testosterone into the anterior hypothalamus-preoptic area restored sexual behavior in long-term castrated, sexually inactive lizards (Morgentaler and Crews, 1978) (Fig. 35). The reinstatement of reproductive behavior followed the pattern in which aggressive behavior appears first followed by courtship behavior. This is similar to the sequence of appearance shown by reproductively inactive, intact males upon environmental stimulation (Crews, 1974a) or by behaviorally inactive, castrated males given exogenous hormone (Crews, unpublished data). It is also similar to the pattern of reinstatement of behavior in castrated ring doves (Streptopelia risoria) following intrahypothalamic androgen implantation (Hutchison, 1974). Intracranial implantation of estradiol or dihydrotestosterone also stimulates reproductive behavior in long-term castrated lizards (Crews and Morgentaler, 1979) and the response is much more rapid than following testosterone or testosterone propionate implantation (Fig. 36). This contrasts with previous findings that these hormones are totally ineffective when administered systemically (Crews et al., 1978). The finding that the effectiveness of hormone replacement therapy in restoring a reproductive behavior that depends on the gonads

FIG.32. A parasagittal view of the neuroendocrine-regulating regions in the brain of the lizard, Anolis carolinensis, and their relationship to neural areas involved in the control of reproduction behavior and pituitary function. Stippled areas indicate steroidconcentrating sites. Lesion studies as well as studies involving intracranial implantation of steroid hormones indicate that the anterior basal hypothalamus-median eminence region (horizontal lines) is involved in the feedback control of gonadotropin secretion and the preoptic area and anterior and basal hypothalamus (oblique lines) are involved in the regulation of reproductive behavior. See text for further details. AH, Anterior

hypothalamus; BH, basal hypothalamus; C , cerebellum; MT, midbrain tegmentum; NH, nucleus habenularis; NR, nucleus rotundus; OC, optic chiasm; OT, optic tectum; POA, preoptic area; SA, strioamygdaloidarea (not in plane of section); T, telencephalon; TS. torus semicircularis; 111, third ventricle. From Crews and Silver (1980) with permission of Plenum Press.

40

DAVID CREWS

5

0

-

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suprochiasmatic

nucleus

-4I Anolls corollnensis

/

,

0 1 -2.25 P o 60

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,

,

,

.

2 3 4 5 6 Roffus +1.0 norvegicus A 7.25

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FIG.33. Size difference between brain of a sexually mature male Anolis carolinensis (6 gm) and a sexually mature Rattus norvegicus (200 gm). Coronal section at level of preoptic area. Coordinates of lizard from Greenberg et al. (1979) and for rat from Koning and Klippel (1%3).

may vary the mode of hormone administration is paradoxical but apparently widespread. For example, in the frog, Rana pipiens, mating behavior cannot be induced by systemic androgen injections (Palka and Gorbman, 1973), but can be elicited by intracranial implantation of testosterone (Wada and Gorbman, 1977) or estradiol (Ruane, 1978). Systemically administered hormone reaches the neural sites of action in A . carofinensis, since the anterior hypothalamuspreoptic area shows a high concentration of testosterone, dihydrotestosterone, and estradiol binding cells as determined by autoradiography (Morrell er al., 1979). It is possible that systemically administered estradiol and dihydrotestosterone have different patterns of distribution in the brain than those of estradiol and dihydrotestosterone derived from the metabolism of systemically administered testosterone (McEwen, 1976). A second possibility is that steroid hormones may also differ in the circulating biological half lives due to differences, for example, in steroid-binding protein affinities. In further investigations of A , carolinensis, castrated, androgen-treated males and intact, sexually active males receiving septal lesions exhibited a rapid decline in courtship frequency and even greater deficits in male aggressive behavior (Crews, unpublished). Note that the sharp decline in aggressive behavior following septal lesions in lizards is in direct contrast to that reported for mammals (Shipley and Kolb, 1977). Histological examination of the testes from

REPRODUCTION IN Anolis

1 1

0

carofinensis

41

control (n.10)

FIG.34. Destruction of the anterior hypothalamus-preoptic area (AH-POA) abolishes courtship behavior in castrated, androgen-implanted Anolis carolinensis. Top: Frequency of male courtship behavior in daily 15-min tests with a female during the course of the experiment. Bottom: Extent of lesions in areas dorsal to AH-POA (hatched lines) or in AH-POA (stipple). From Wheeler and Crews (1978) with permission of Academic Press.

42

DAVID CREWS implantation .60r

t. 0

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w

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REPRODUCTION IN

Anolis carolinensis

43

the intact males that received septa1 lesions showed them to be at the stage of maximum spermiogenesis, suggesting no lack of androgen and indicating moreover that the septum is not involved in pituitary regulation of the testes in A . carolinensis. This is also in contrast with findings among mammals (Kawakami and Kimura, 1975). Male courtship behavior was abolished by bilateral lesions of the rostra1 amygdaloid complex of androgen-treated sexually active castrates; male agonistic behavior was also affected. Male challenge behavior to females disappeared and the frequency of challenge displays directed to stimulus males declined to low levels while the frequency of assertion displays remained unchanged (Greenberg, Scott, and Crews, unpublished data). Lesions of the caudal amygdala had no detectable influence on courtship behavior, although this area is known to concentrate sex steroids. Bilateral testosterone implants into the amygdala of long-term castrated males resulted in the appearance of challenge display behavior toward females, but the frequency of challenge behavior to introduced males did not change (Crews and Carrow, unpublished data). This effect appears to be selective, since there was no change in male courtship or assertion behavior in tests with males and females. Confirming the lesion study, only rostrally placed implants had an influence on challenge behavior. The anterior basal hypothalamus appears to be a major site of steroid feedback regulation of pituitary gonadotropin release (Callard et al., 1972). When the anterior basal hypothalamus of A . carolinensis is lesioned, testicular collapse and atrophy follows (Farragher and Crews, 1979). Regions of the posterior basal hypothalamus have no detectable influence on testicular activity of intact males. In both androgen-treated castrates and intact males, basal hypothalamic lesions abolish male courtship and aggressive behavior.

FIG.35. Implantation of testosterone (T) (circles) or testosterone propionate (TP) (triangles) into the anterior hypothalamus-preoptic area (AH-POA) reinstates sexual behavior in long-term castrated Anolis carolinensis. Implants in areas other than the AH-POA or cholesterol into the AH-POA have no influence on male courtship behavior. (A) Frequency of male courtship behavior in daily tests with females during course of experiment. (B) Location of implants. Hatched symbols represent levels of behavior on five daily tests within 7 days prior to implantation. All animals were then given an intracranial implant of testosterone ( n = 29), testosterone propionate ( n = 19), or cholesterol ( n = 3) and tested for 8 consecutive days beginning the day following implantation. Castrates exhibiting an increase in display frequency of greater than 100% above individual preimplantation levels on at least 2 consecutive days (solid symbols) were considered responders; castrates exhibiting no change in display frequency throughout the course of the experiment (open symbols) were considered nonresponders. Number of animals in each group is shown in parentheses. From Crews (1979a) with permission of the Society for the Study of Reproduction.

44

DAVID CREWS

FIG.36, Cumulative percentage response of castrated Anolis carolinensis exhibiting sexual behavior after intracranial hormone implantation into the anterior hypothalamuspreoptic area. T, testosterone; TP,testosterone propionate; E, estradiol; DHT, dihydrotestosterone. From Crews and Morgentaler (1979) with permission of the Journal of Endocrinology.

Androgens are also concentrated in areas of the torus semicircularis that are homologous to those regions of the nucleus intercollicularisthat exhibit hormone uptake in songbirds (Arnold e? ul., 1976). In several bird species, stimulation of this area has been found to elicit species-typical vocalizations while lesions abolish vocalizations (Phillips and Peck, 1975; Nottebohm et al., 1976). Similarly, stimulation of areas immediately peripheral to the central nucleus of the torus semicircularis elicits vocalizations in the Tokay gekko, Gekko gecko (Kennedy, 1975) and gular extension in the green iguana, fguana iguana (Distel, 1978) and the western collared lizard, Crotuphytus collaris (Sugarman and Demski, 1978), both prominent components in the social displays of these species. It is possible that this area is involved in the control of dewlap displays in Anofis as in Iguana and Croruphytus; preliminary studies indicate that androgen-treated castrated A . carolinensis no longer extend the dewlap but otherwise court normally following lesions in this brain area (Crews, unpublished).

V. STUDIES OF THE BEHAVIORAL ECOLOGY OF Anolis It is obvious that the field is the logical and necessary testing ground for hypotheses arising from experimental work with laboratory populations. Study of the behavioral endocrinology of animals in natural surroundings presents an exciting challenge, Further, research on both intra- and interspecific levels proves extremely valuable for our understanding of the evolution of mechanisms controlling reproduction. For example, the adaptive significance of mating-induced inhibition of female sexual receptivity immediately becomes apparent when the breeding biology of A . carolinensis is considered. Female A . carofinensis tend to mate with the male in whose territory they have their home

REPRODUCTION IN

Anolis carolinensis

45

range (Greenberg and Noble, 1944). In their natural habitat, these lizards characteristically mate in exposed areas such as tree trunks, fences, and walls. During this time the copulating pair are particularly vulnerable to predation since they are highly visible and can be approached and touched without immediately separating. In addition, copulation in this species is prolonged: in the laboratory, mating takes an average of 10 min although each individual male has a characteristic mating time (Crews, 1973b). Indeed, there is every indication that the lizards in the wild are heavily predated upon (Gordon, 1956); A . carolinensis constitutes up to 90% of the prey items kestrels bring to the nest during the breeding season (Johnston, 1975) and Cruz (1973, 1975, 1976) reports that A n d i s form a significant portion of the diet of several bird species in Jamaica. Estrous cyclicity may be viewed as a reproductive strategy to reduce predation during mating. It will be recalled (see Section IV,A) that during the breeding season, female A . carolinensis undergo periods of sexual receptivity that are correlated with their cyclic pattern of ovarian activity. This cyclicity in receptivity and, therefore, mating probably operates ultimately to reduce and restrict the amount of time the female is sexually receptive and, therefore, particularly vulnerable to predation, to the period when the likelihood of fertilization is greatest. Mating inhibition of further receptivity during each follicular cycle further minimizes the female’s risk of predation. Field studies of other anoline lizards support this interpretation. They also exhibit cycles of female sexual receptivity in mating that correspond to cyclic ovarian changes (Stamps, 1975; G. Gorman, personal communication). Trivers (1976) has reported mating inhibition of receptivity in female Anolis garrnani: females that completed copulation undisturbed did not copulate again for at least a month, but when copulation was interrupted, they continued to be receptive until they achieved complete copulation (see also Hunsaker, 1962; Greenberg and Noble, 1944). A.

FUNCTIONOF THE DEWLAP AS MECHANISM

A SPECIES-ISOLATING

A number of herpetologists have pointed out that many lizard species can be identified taxonomically as readily by their species-typical social displays as by their morphological features (Carpenter and Ferguson, 1977; Crews, 1975b; Jenssen, 1977, 1978, for reviews of this literature). There is now evidence that the lizards themselves may discriminate their own species from other closely related species on the basis of these stereotyped social displays. One of the most striking features of the genus Anolis is the variety of dewlap or throat fan colors exhibited by different species. The dewlap is particularly prominent in the courtship display when it is extended during a species-typical sequence of up-and-down bobbing movements. The clear cut demonstration of character displacement in dewlap color has lent support to the hypothesis that the

46

DAVID CREWS

biological significance of differences in dewlap color between closely related sympatric species lies in interspecific communication. For example, Rand and Williams (1970; see also Williams and Rand, 1977) noted that all eight sympatric species of Anolis at a single montane locality (La Palma in Hispaniola) differed in dewlap color. Similarly, Webster and Burns’ (1973) discovery that the three populations of the Anolis brevirostris complex in Haiti were actually three different species was in part based on population differences in dewlap color (Fig. 37). However, the evidence that species differences in dewlap color serve as an effective reproductive isolating mechanism among closely similar sympatric anoles is only indirect.

distichus dominiensis

brevirostris 6

FIG.37. Variation in male dewlap color and pattern in Anolis brevirostris and A . distichus in Haiti.Anolis brevirostris, identified by blackbordered white ocellus in front of shoulder, faces to the right, A . distichus to the left. Population B of A . brevirostris exhibits clinal variation in dewlap color, whereas populations to the north and south (A and C, respectively), have uniform dewlap colors. Nomenclature of the A . brevirostris complex from Webster and Burns (1973). From Crews and Williams (1977) with permission of American Society of Zoologists.

REPRODUCTION I N Anolis carolinensis

c/

speciosus

L ’,

47

inornotus

a

L/’

marmaratus

FIG. 38. Variation in body color and patterning in Anolis marmoratus complex on Guadeloupe. Anolisrn. marmoratus is larger than other subspecies; A . m . sctosus ischaracterized by conical scales. From Crews and Williams (1977) with permission of the American Society of Zoologists.

Williams (Williams and Rand, 1977) has suggested also that the bicolor dewlap exhibited by many anoline lizards (a central spot of color surrounded by a contrasting color) may serve as a flash signal that is both highly visible and readily interpretable under a wide variety of conditions. If the precise patterns of light and dark in the dewlap are morphological characters, finely adapted to specific environmental conditions, then dewlap color differences between males in a population could be an important basis of female mate selection. Choice of mate by dewlap pattern could also maximize the probability of choosing a mate of optimum genetic makeup (most likely a relative) while permitting some variability in choice if the optimum genotype, as signaled by a particular dewlap pattern, was not available. An alternative way in which species (or population) identity can be encoded in anoles has been reported by Lazell for A . martnoratus on Guadeloupe (Lazell, 1962, 1972). In this species, adult male size or body color and pattern vary while dewlap color remains a constant yellow (Fig. 38). In the Lesser Antillean anoles, permanent head and body color may also substitute as species or population recognition marks (Williams and Rand, 1977). Indeed, it appears that these differences in body color are the basis of mating preference in the same manner as has been suggested for dewlap color. For example, Lazell (1972) has stated that “behavioral evidence with captives indicates that forms strongly different in

48

DAVID CREWS TABLE IV RESPONSE OF SEXUALLY RECEPTIVE FEMAI.E Anolis caroliriensis TO THE. COURTSHIP OF HYOIDECTOMIZED A N D BLUE-DEWLAPPED MALES“ Female sexual receptivity

Test male

Number receptive

Number nonreceptive

2

10

9

3

Hyoidectomized male Blue-dewlapped male ~~

~~~~~

“Modified from Crews (1975a). bp <0.01, phi coefficient.

coloration, like A . marmoratus and A . speciosus, would not interbreed directly; females of A . marmoratus that readily accept males of their subspecies in captivity do not respond to A . speciosus males.” There has been only one attempt, however, to evaluate experimentally the role of the dewlap in intraspecific communication in Anolis (Crews, 1975a). This study (see Section I ~ dC) , demonstrated that both physiological responses [courtship facilitation of female ovarian recrudescence (see Fig. 24) as well as shortterm behavioral responses (mate selection) (Table IV)] depend on the ability of the male to extend the dewlap rather than on dewlap color itself. These results raise the question of whether dewlap color is an isolating mechanism among sympatric anoles by aiding in species recognition. It is important to keep in mind, however, that A . carolinensis is the only endemic anole throughout most of its range in the continental United States (Conant, 1975) and that the animals used in the above study came from areas around New Orleans, Louisiana, where no other Anolis species occur. The change in body shape of the displaying animal, and not the dewlap color, may be the important social signal in A . carolinensis and other solitary anoles (Crews, 1975a). The observation that dewlap color in A . carolinensis is not uniform but rather polymorphic, ranging from red to blue, over most of the species’ distribution in the United States (Crews, unpublished; N . Greenberg, personal communication), supports this interpretation. B.

BEHAVIORAL Ecor>ocuA N D CHARACTER DISPI~ACEMENT IN Anolis carolinensis AND Anolis sagrei IN FLORIDA

Florida presents an ideal “natural” laboratory for examining the role of the dewlap in intraspecific and interspecific communication in Anolis lizards. In

REPRODUCTIONI N

Anolis carohensis

49

Florida, A . sagrei, introduced approximately 30-50 years ago (Conant, 1975), has been gradually excluding the endemic species, A . curdinensis, from southem coastal areas (Fig. 39). This expulsion, which in the last 5 years has been extremely rapid, occurs apparently because the coastal area does not contain the I

\

oow ~

30"

ii akeland

k

FIG. 39. Distribution of Anolis sagrei in Florida (hatched lines). Anolis carolinensis is found throughout the state except in some coastal areas. Populations of A . disrichus in Miami and West Palm Beach.

50

DAVID CREWS

preferred habitat of A . carolinemis (Schoener, 1974) and because A . sagrei has been able to exclude A . carolinensis competitively. Anolis sagrei is a small anole that lives on the lower tree trunks and on the ground; in Cuba, where both A . sagrei and A . carolinensis coexist, these species have effectively divided the habitat such that A . carolinensis is found on the trunk and crown of trees while A . sagrei restricts its activity to the lower parts of trees and the underbrush (Fig. 40). A. sagrei is a classic sit-and-wait predator that takes its prey on the ground. It fares best in more open, arid regions and does extremely well in disturbed areas. A . carolinensis in the United States is also a trunk-ground anole but tends to spend much of its time above ground and takes many of its prey from leaves and twigs of bushes and trees (King, 1966). Further, A . carolinensis appears to be more susceptible to desiccation than A . sagrei and tends to lay its eggs in wood piles and holes in trees; A . sagrei typically lays its eggs in drier areas such as leaf litter or sand. Anolis sagrei-A . carolinensis interactions have been observed in nature, with A . sagrei being noted as the more aggressive species. In the laboratory, A . sagrei will display vigorously toward A . carolinensis and attack it. A . carolinensis, on the other hand, rarely if ever displays toward A . sagrei and has never been seen to respond to A . sagrei’s attacks other than defensively (Crews, unpublished; N. Greenberg, personal communication; Scott and Crews, 1980). Dewlap color in A . carolinemis in the continental United States is polymor-

YO

FIG.40. Stylized structural habitat of Anolis carolinensis and A . sagrei in areas of syntopy in Cuba. Anofis carofinensis. a trunk-ground anole in the southeastern United States and the West Indies, has been displaced by A . sagrei. After Collette (1961).

REPRODUCTION I N

Anolis carolinensis

51

phic, ranging from red to blue and grey-green as noted above, but in certain areas of Florida, it is more uniform and restricted to green or grey (Christman, 1972; W. Haas, unpublished). In at least several of these areas, A . carolinensis is sympatric with A . sagrei, which has an orange-colored dewlap with a yellow border. Since behavioral sensitivities and mating preferences can change extremely rapidly, in as little as 10 generations (Ehrman and Parsons, 1977), it is possible that the dewlap color range of A . carolinensis in Florida has become narrowed and different from A . sagrei. We are presently studying Florida A . carolinensis in their zone of sympatry with A . sagrei and testing Rand and Williams’ hypothesis that dewlap color plays an important role in species recognition among sympatric anoles.

VI. EXTENSION TO OTHER REPTILIAN SPECIES For the behavioral biologist, the reptiles present an impressive variety of social systems and complex communicative displays. Unlike birds and mammals, which often require radio tracking to discover their movements, most reptiles are sedentary, ranging over relatively short distances. Few species are secretive and many are seemingly oblivious to human observation. Although nocturnal forms such as the geckos exist, most species are active during the day. Studies also have revealed intricate social structures in which territoriality is common, but harems ruled by male despots have also been reported (Carpenter and Ferguson, 1977; Stamps, 1977). With this great diversity in social systems, there is a corresponding richness of vocal, olfactory, tactile, and visual displays. A.

SNAKES

Except for the very early work in the 1930s by G. K. Noble (1937), the reproductive behavior of snakes has received little attention. Interest in snake behavior has been revived in recent years, and much has been revealed about their reproductive behavior and its control (Carpenter, 1977; Crews, 1976; Ross and Crews, 1977, 1978; Camazine er al., 1980; Garstka and Crews, 1980). Most of our information about snake reproductive behavior and its underlying physiological mechanisms has come from research on the common garter snake (genus Thamnophis). In northern latitudes, garter snakes overwinter en m a w in underground dens with hibernacula containing as many as 10,OOO individuals of several species (Aleksiuk, 1975; Gregory, 1974). These dens are evacuated in early spring, with the males emerging first and surrounding the mouth of the den (Aleksiuk and Gregory, 1974; Gregory, 1974). Because of this high concentration of males, when the females emerge several weeks later each female is vigorously pursued and courted by a number of conspecific males.

52

DAVID CREWS

Indeed, the ratio of males to females in the areas around the entrance to the hibernaculum may reach as high as 50 to 1 (Gregory, 1974) (Fig. 41). Often this results in a writhing ball of snakes, sometimes containing 100 or more males courting a single female (Gardner, 1955; Hawley and Aleksiuk, 1975). Nevertheless, as soon as a single male achieves intromission, the other males cease to court the female and rapidly disperse from the mating pair (Devine, 1975; Fitch, 1965; Gardner, 1957). Upon termination of coitus, the newly mated female quickly departs from the denning area (Gregory, 1974). Females emerging from the winter hibernacula are extremely attractive to males (Hawley and Aleksiuk, 1976) and Noble’s early suggestion that this attraction is probably based on a pheromone produced by the female has recently been substantiated (Crews, 1976; Kubie et al., 1978a). Further, Kubie et al. (1978b) have demonstrated that the tongue flicking by the male picks up the odor molecules from the female’s back and delivers them to his vomeronasal organs. Observations in my laboratory of the male’s behavior preliminary to mating have demonstrated that, if the female is sexually attractive, the frequency of tongue flicks by the male increases dramatically (see also Kubie et a l ., 1978b) and at first contact with the female, the male often drapes his tongue over her back (Crews, 1976). Occasionally the male also nudges the female’s side with sharp probing movements of the snout before beginning to press his chin on the

FIG. 41. Mass of mating garter snakes (Tharnrq~hisspp.) at hibemaculum entrance during spring emergency. Photo courtesy of Michael Aleksiuk.

REPRODUCTION IN

Anolis carolinensis

53

female’s back, rapidly traversing the length of her body repeatedly. These tongue flicking and nudging behaviors tend to be concentrated along the anterior half of the female’s back and are not directed toward the female’s cloacal region, suggesting that the sites of release of the attractive pheromone are located along the anterior half of the female’s back rather than in the cloacal region (Crews, 1976; Garstka and Crews, 1980; Noble, 1937). The male then aligns his body beside the female’s with his head resting behind hers and he begins to undulate the posterior third of his body (Fig. 42). If the female is sexually receptive, she remains stationary, lifting her tail and gaping the cloaca in response to the male’s palpations (Carpenter, 1977; Ross and Crews, 1977, 1978);nonreceptive females retreat from male courtship advances. A series of knobbed scales around the male’s cloaca enables the male to locate the female’s cloaca (Pisani, 1976). This stimulates the male to evert and intromit a single hemipenis. Mating lasts approximately 20 min in T. sirtalis (Crews, 1976) and 90 min in T . radix (Ross and Crews, 1978). The copulatory plug deposited by the male does not, as originally reported by Devine (1975), solidify in these species, at least in laboratory matings. The female and male garter snake each produces a species-specificpheromone (Ford, 1978; Devine, 1977) that has distinct, yet opposite functions in coordinating their reproductive behavior (Crews, 1976; Ross and Crews, 1977, 1978).

FIG.42. Courtship of an estrogen-primed female by two male Thamnophis radix. At this stage of the mating sequence, the males will remain stationary, riding the female with their heads resting on the female’s back.

54

DAVID CREWS

‘1

t

2.5 W

OPERATION w Castrated

-*-

w Sham-operated T-implanted

p--rl

GC

002.0Cn

a_

r

1.5-

u

3

0

u

1.0-

9

0 W

z

0.5-

L -I

0-5

5

10 15 20 DAYS POST- OPERATION

25

30

35

FIG. 43. Lack of gonadal dependence of male courtship behavior in Thurnnophis sirrufis. Following castration (arrow), there is no difference in the decline in courtship of estrogen-primed stimulus females by castrated, intact (sham-operated), or castrated males that have received testosterone replacement therapy. Male courtship scored as follows: 0, Male fails to approach introduced female; 0.5, male investigates female with weak chinning behavior; 1.0, male follows female or is in constant contact with his chin; 1.5, male follows female slowly while covering her body and is not distracted; 2.0, male aligned along female’s back with rapid and repeated traverses along length of female and mild caudocephalic waves; 2.5, more intense following, traverses, and caudocephalic waves with attempt at cloaca1 apposition; 3.0, attempted copulation. Each dot represents the average of tests of all males on that day; horizontal bar represents the mean test score for all tests during testing period. From Camazine and Crews (unpublished data).

Males distinguish the reproductive state of a female, basing their discrimination upon a pheromone carried in the blood and released from the female’s dorsal skin region (Garstka and Crews, 1980). The male’s interest in females, however, does not appear to be dependent upon the presence of the testes or androgens (Fig. 43). The production of the attractant pheromone by the female is correlated with ovarian growth and the synthesis of estrogenic hormones. In hormone-replacement studies, increasing amounts of estrogen administered to both intact and ovariectomized females resulted in an increasing percentage of females courted (Crews, 1976). Still other experiments have demonstrated that sexually active males will court only females that have been primed with exogenous estrogen, while ignoring females that have received control injections. These findings agree well with field reports that most mating

REPRODUCTION IN

Anolis carolinensis

55

FIG. 44. Influence of mating on female sexual attractivity in the garter snake, Tharnnophis radix. Not all females were retested for attractivity at all postmating intervals. In two cases both at 24 and at 36-48 hr following the original mating, courtship of the females involved the same test male. Data from Ross and Crews (1978).

FIG.45. Specificity of the mating plug on the mating-induced decline in female sexual attractivity in the garter snake, Tharnriophis radix. All females were estrogen-primed and courted by two males in the initial test (untreated). A cloaca1 lavage taken from a mated female or an unmated female, or distilled (DIST.) water was then spread over the female's back and the female was retested. In the final stage of the experiment, the applied material was removed by an ethanol-water wash and the females were retested. Data from Ross and Crews (1978).

56

DAVID CREWS

occurs in the spring when females are close to ovulation and circulating levels of estrogen are highest. Male garter snakes will not court a female that has recently mated (Ross and Crews, 1978) (Fig. 44). Since all females in these experiments continued to receive injections of estrogen (estradiol benzoate), something about the mating itself appeared to be responsible for this dramatic shift in the “attractivity” (Beach, 1976) of the females. We have since found that this change in attractiveness following copulation is due to the mating plug deposited by the male (Ross and Crews, 1978); indeed, a mated female remains attractive to other males if the mating plug is removed shortly after copulation whereas an unmated, estrogentreated females will not be courted if the material of the mating plug from a mated female is spread along her back (Fig. 45). The mating plug is formed by secretions of an accessory sex structure in the male called the renal sex segment (see Section IV, D), a structure homologous to the prostate and seminal vesicles of mammals. Experiments with castrated and intact males in which the vasa diferentia were ligated between the renal sex segment and the hemipenes indicate that it is the secretion produced by the sex segment that contains the pheromone (Ross and Crews, 1978) (Table V). The mating plug pheromone also temporarily abolishes courtship behavior in

TABLE V

RELATIVECONTRIBUTIONS OF SPERM A N D RENALSEXSEGMENT SECRETIONS I N MATING PLUG-INDUCED TERMINATION OF FEMALE SEXUAL ATTRACTIVITY A N D INHIBITION OF MALE COURTSHIP BEHAVIOR’ Postmating retest Inhibition of male courtship

Female attractivity

Original mating male Intact with implant” Castrate with implant Vasectomized male

x‘

tests: Intact with castrate Intact with Vas-X, Castrate with Vas-X

Number females courted after mating

2 0 6

n.s.‘ p <0.01 p <0.05

(N) (21) ( 1 1)

(6)

Number males inhibited following exposure to mated female 9 10 0

(N) (1 1) ( 1 1)

(6)

n.s. p <0.01 p
“From Ross and Crews (1978). with permission. *Implants were 2 cm Sitastic tubing capsules (0.058 in. i.d. X 0.077 in. 0.d.) of free testosterone. ‘Not significant.

REPRODUCTION IN Anolis carolinensis

57

exposed males (Ross and Crews, 1977, 1978); for example, males exposed to a mated female often will not court unmated, attractive females until at least 24 hr after exposure! Thus, the deposited mating plug from a mating male not only advertises the mated status of the female to other males but also renders impotent any male that may come in contact with that female. The significance of the attractive and inhibitory pheromones becomes clear when the natural history of northern temperate garter snakes is considered (see preceding). Males discriminate, and are attracted to, conspecific females on the basis of the attractant pheromone, which is species-specific. In addition, by inhibiting the sexual behavior of other males via the sperm plug deposited in the female, a male in effect removes competitors from the breeding population temporarily while he is sexually refractory. There are advantages for the female as well: mated females are not courted by other males in the area and thus are not subjected to repeated mating attempts as they leave the area, consequently reducing to a minimum the total time they are exposed to predators. Because a number of closely related species of garter snakes may occupy a single hibernaculum and emerge in the spring simultaneously, it would be interesting to see if the seminal plug pheromone is species-specific in its effect as is the female attraction pheromone (Devine, 1976; Ford, 1978).

B. TURTLES Like snakes, turtles are somewhat constrained by body morphology, but nevertheless have evolved an unappreciated variety of social and sexual displays. For example, aquatic freshwater turtles appear to rely mostly on tactile signals during courtship (Evans, 1961); there are several descriptions of the courtship behavior of pond turtles in which the male faces the female and backpaddles with the hindfeed while “titillating” the female with the elongated foreclaws. Auffenberg’s (1966, 1977, 1978) studies on the courtship and mating behavior of land tortoises (Geochelone and Gophorus) have revealed a highly complex signal repertoire in all sensory modalities; vocalizations, visual displays, tactile stimulation, and scent marking all play roles in the reproductive cycle of land tortoises. For example, during courtship a male tortoise typically scrapes the enlarged medial scale of his forelimb across the subdentary glands of the chin (Fig. 46), presenting it to the female for her inspection (Auffenberg, 1966). Auffenberg ( 1977) has suggested that the secretion produced by these glands communicates sexual and possibly social status as well as species identity. Further, there is evidence that the production of this pheromone(s) is under hormonal control (Weaver, 1970; R. Taylor, unpublished); the size and secretory activity of the chin glands are correlated with the breeding season and out-of-season glandular activity can be induced by injections or subcutaneous Silastic implants of testosterone.

58

DAVID CREWS

The courtship behavior of land tortoises is highly stereotyped. According to Auffenberg,courtship begins with the male trailing the female, stopping whenever the female stops and bobbing his head in a species-typical manner. During this period, which may last for several days, the male gradually reduces the distance between himself and the female. This is followed by the male’s ramming the female and biting her shell and hind legs (Fig. 47). Auffenberg (1977, 1978) has suggested that the ramming and biting before copulation may be necessary to synchronize male and female reproductive states much like the displays of male lizards serve to stimulate ovarian development in female lizards. During mating in the gopher tortoise, the tail of the male first searches for and locates the female’s cloaca and then serves as a guide as the single penis is inserted (Patterson, cited in Auffenberg, 1977; see also Weaver, 1970; Auffenberg, 1978). A receptive female will often invite copulation by withdrawing the forelimbs and head and partially extending the hindlimbs, presenting the end of

B

FIG.46.Secondary sexual structures in male Gopherus tortoises. (A) Enlarged subdentary glands (arrow) of a breeding male G. berlandieri. (B) Enlarged medial scale (arrow) of breeding G . polyphemus. During courtship, the male rakes the subdentary gland with the foreleg before presenting his foot to the female. From Auffenberg (1977) with permission of the author and the American Society of Zoologists.

REPRODUCTION IN

Anolis caro/inensis

59

FIG.47. Major phases in the courtship of Gophrrus polyphenrus. (A) Male walks in circle, bobs head, and female approaches him. (B) Male bites female on shell and limbs. (C) Biting becomes more vigorous and female moves backward and stretches hind legs. (D) Mounting and copulation. From Auffenberg (1966) with permission of the author and The Herpetologists League. the shell to the male and extruding her cloaca (Weaver, 1970). Copulation lasts about 10 min and is accompanied by thrusting movements and vocalizations by the male; copulation is terminated when the female walks out from under the male. Robert Taylor, a graduate student at the University of Florida, Walter Auffenberg, and Harvey Feder of the Institute of Animal Behavior are currently investigating the hormonal bases of reproductive behavior of land tortoises. In addition to observing males and females in nature, periodic blood samples are being analyzed to determine circulating levels of various gonadal hormones.

C. CROCODILIANS The reproductive behavior of the fourth major group of reptiles, the alligators and crocodiles, is equally dramatic, but much less known, partly because of their size and temperament as well as the inaccessability of remaining populations (Garrick and Lang, 1977; Garrick et al., 1978; Joanen and McNease, 1976). In the American alligator, courtship activity lasts for 6 weeks with mating occurring toward the end of this time. The courtship behavior of the American alligator (Alligator mississippierisis) has been described recently and the signals used have been identified (Garrick et al., 1978). Characteristically, the female swims towards the male, lifting and arching her tail out of the water (Fig. 48). The male responds by blowing spouts of water through his nostrils (called narial geysering by Garrick and Lang), and splashing water by snapping the jaws shut.

I

I

9 submerges ond/or

d or ? submerges

I

1

I

bellow

porollel swim

owrwches

o +8 contocts o s

I

(Chumpfing yoMli2otion by

8--=,

?oppmoche$d+?comoch6's I I I

I I I

I

Snml

8 or?)

heodslop

(1)

I I

ond/or swims off

I I

d ond 0 (chumpftnq Mcolizotion bybOnd9)

d submerges ond/or

I

swims off

I I

(2)

I I

I I

I I

I I I

I I I

I

I

II

/nKh/SM"l

t

swims off

ond heOd rubb~nq

by I

? submerges ond/or

and/or swims off

(3)

I I

I

(4)

FIG.48. Sequence of courtship behavior in the American alligator, Alligufor mississippiensis. The vertical dashed lines separate (from left to right): (1) attraction, advertisement,and other signals; (2) initial pair formation; (3) the precopululatoy behaviors;and (4) copulation. Modified and redrawn from Garrick et al. (1978).

REPRODUCTION I N

Anolis carolinensis

61

It is also common to see water suddenly ripple about the male as he vibrates his body under water. During copulation, the pair first circle one another before the male rides and eventually mounts the female. Copulation usually occurs in shallow water and is relatively brief (2-4 min) compared to that of other reptiles. Since copulation occurs in the water, it has not been possible to determine how intromission is achieved, but the posture employed is probably similar to that used by lizards. By regularly sampling the blood of breeding animals, we may learn something of the hormonal changes during the alligator’s reproductive cycle; such information will be extremely useful in planning the conservation of this endangered species.

D. PARTHENOGENETIC LIZARDS All-female, parthenogenetic species present a unique test of hypotheses regarding the nature and evolution of sexuality. Whereas the majority of vertebrates are gonochoristic (i.e., fertilization of female ova by male sperm), at least 27 species of reptiles are known to consist entirely of females and to reproduce only clones of all-female offspring (Cole, 1975). Although some information exists regarding the genetics and ecology of one genus of lizards (Cnemidophorus) having parthenogenetic species (Cole, 1975; Cuellar, 1977 for reviews), nothing is known of the behavior of these animals. We have discovered recently, from observations of captive populations of

FIG.49. Agonistic behavior in the parthenogenetic lizard, Cnernidophorus uniparens. ( 1 -3) Brief lunging and biting attacks always occur in the beginning of an encounter. (4-6) Tail-gripping is a prolonged behavior that precedes mounting in which the tail is gripped firmly by the jaws. The mounting female may also grip the foreleg or neck

while mounted.

62

DAVID CREWS

three parthenogenetic Cnemidophorus species (C. uniparens, C. velox, and C. tesselatus), behavior patterns remarkably similar to the courtship and copulatory behavior of closely related sexual species (Crews and Fitzgerald, 1979, 1980). In all three species, one animal in the pair begins by gripping with its jaws the tail of its cagemate following a brief period of agonistic behavior during which it

FIG.50. Pseudocopulation in captive parthenogenetic Cnemidophorus uniparens. Following lunging attacks directed at the smaller female, the larger female approaches the now passive small female, first gripping the foreleg in her jaws. This is accompanied by mounting and riding behavior (1, 2) during which the active female scratches the side of the mounted female with her fore- and hindlegs and strokes the back of her neck with her jaw. Shortly afterward the active female twists her tail beneath the other’s tail (3), apposing the cloacae, and assumes the copulatory posture characteristic of sexual cnemidophorine lizards (4). Females were housed in pairs in aquaria measuring 76.2 X 30.5 cm. Heat was provided by a 75-W 120-V lamp suspended 10 cm from the sand substrate. A water bowl was provided at the opposite end of the cage. Each cage was illuminated by two Durotest Vita Lights 30 cm above the cage bottom. A 14:lO hr 1ight:dark cycle was employed, with a daily temperature gradient of 25°C near the water dish and 47°C directly under the heat lamp. The temperature dropped to 21°C at night. Lizards were fed both mealworms and crickets ad libitum. Further details of care and housing procedures of unisexual Cnemidophorus are provided in Crews and Fitzgerald (1980). Both pairs were observed daily from 11:OO AM to 2:OO PM, the period of peak activity for the animals in this laboratory.

REPRODUCTION I N Anolis

carohensis

63

TABLE VI REPRODUCTIVE CONINI I O N OF THREESPECIES OF PARTHENOGENETIC LIZARDS (Cnemidophorus uniparens. C . velox. A N D C . rcsselams) AT TIME OF OBSERVATIONS" Ovarian condition and size of largest follicles (mm)

Snout-vent length Species

Behavior

Cnemidophorus uniporens Pair A: No. 1 Mountee Mounter L Pair B: 3 Mountee 4 Mounter Cnemidophorus velox Pair A: No. I Mountee 2 Mounter Pair B: 3 Mountee 4 Mounter Pair C: 5 Mountee 6 Mounter Cnemidophorus tesselatus Pair A: No. 1 Mountee 2 Mounter

(mm) 68 59 67

Vitellogenic (4.8-5.4) Revitellogenic ( I .2-2.2) Vitellogenic (6.0-6.2) Previtellogenic

51 67 69 5s 66 63

Vitellogenic (6.5-7.0) Previtellogenic ( I .2-2.0) Vitellogenic (6.5-7.5) Previtellogenic ( I .2- I .4) Vitellogenic (6.4-7.0) Previtellogenic (0.8-1 .O)

75 69

Vitellogenic (7.5-8.0) Previtellogenic (1.2-2.0)

51

Number of preovulatory follicles

5 8

"From D. Crews and K. T. Fitzgerald, unpublished data.

lunges and quickly bites the other lizard (Fig. 49). This, in turn, is followed by a masculine-like behavior in which the active lizard mounts the back of the now passive second lizard, riding atop the other female for as long as 2 min (Fig. 50). During this time, the active lizard intermittently rubs its cloaca against the dorsal pelvic area of the female beneath it and strokes her back and neck with the jaws and forelimbs. The active lizard then grasps the back of the neck or some regions of the shoulder of the other female in its jaws and curves its tail beneath the other's tail to appose the cloaca1 regions. Dissection of the lizards reveals that in each case the courted animal is reproductively active, having ovaries containing large, preovulatory follicles, while the courting animal reproductively inactive, having ovaries containing only small, undeveloped follicles (Table VI). These observations are significant for the questions they raise. For example, is this behavior necessary for successful reproduction in these species (e.g., by priming reproductive neuroendocrine mechanisms as has been demonstrated in sexual species) or are they a nonfunctional vestige of the ancestry of this species? It would also be of interest to determine the hormonal status of the females exhibiting masculine behavior patterns versus those exhibiting feminine behavior patterns. Further, can specific components of the ancestral behavior still be

64

DAVID CREWS

FIG.51. Research with the lizard Anolis carolinensis demonstrates that traditionally separate lines of inquiry can be integrated, leading to a better understanding of the causes and function of reproductive behavior. Examples of studies at each level of analysis employed in this research program are illustrated in the figure. (A) Character displacement in dewlap color. The recent introduction of A . sagrei into Florida has resulted in

REPRODUCTION IN

Anolis carolinensis

65

influenced by hormone manipulation and can complete behavior sequences be elicited by hormone therapy? Do females alternate in their roles? Our observations indicate that “courting” females subsequently lay eggs. In the parthenogenetic gecko, Lepidoductylus lugubris, which also exhibits mating-like behavior, paired females produce about half as many eggs as isolated females (M. Falaruuw , personal communication), suggesting that only one individual is producing at a time.

MI. CONCLUDING REMARKS To return to the beginning of this article, it is clear that each of the studies presented here could be relegated to one of the four questions proposed originally by Tinbergen. When viewed together rather than separately, however, another level of information is revealed, showing the power of a multileveled approach to the study of behavior. Thus, while the research program detailed here is diverse, ranging from the mechanisms of action of steroid hormones in the expression of reproductive behavior to individual variation in species-typical display patterns and sexual selection, the basic underlying theme is an integrative one (Fig. 51). In addition to combining ordinarily separate lines of investigation (observation with experimentation in both the laboratory and field), I have attempted to proceed from the organismal and, in some cases, population and species level, toward the physiological without obscuring the relation of the behavioral and ecological phenomena under study at each level of analysis. Thus, by concentrating on a single species at several levels, it has been possible to learn how an animal’s reproductive strategy is functionally adapted to its environment, For example, a female’s perception of a male performing a particular display has important consequences for her reproductive state. The observation that male courtship stimulates, whereas aggression between males inhibits, ovarian development presents a plausible functional explanation of how the sex differences in time of vernal emergence observed in many seasonally breeding species may have evolved. Investigation of estrous behavior during the breeding season in both the field and laboratory has pointed to some of the environmental constraints that have shaped behavior and its underlying physiological mechanisms. The dual processes controlling female sexual receptivity, that is, its hormonal depenboth ecological and morphological changes in A . carolinensis (Section V). (B)Sociosexual displays of Anolis carolinensis. On the top branch, two territorial males challenge each other while on the middle branch a dominant male is performing an assertion display after a fight, On the bottom branch, a male is courting a female (Section 111). (c)Some of the principal intrinsic and extrinsic factors mediating reproductive events in Anolis carolinensis and their feedback relationship (Section IV). GTH, gonadotropic hormones; OC, optic chiasm.

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dence during fo1licula.r maturation coupled with immediate termination of receptivity by copulation, reduce the risks associated with mating to a minimum. The primary objective of my research has been to study in detail the neural and endocrine substrates of behavior as well as the effects of social stimuli upon neuroendocrine function in reptiles. By combining behavioral-endocrinological research, in both the field and laboratory, with experimental studies on the origin and maintenance of species differences, we gain not only a comparative perspective to the already considerable literature concerning the biological bases of reproductive behavior but also fresh insights into how physiology-behavior interactions adapt animals to their particular environments. Acknowledgments

I wish to thank the editors of this series and Anne Schneiderman for their many helpful comments on the manuscript; Neil Greenberg and Richard Tokarz also read earlier drafts and offered many suggestions for improvement. 1 would also like to express my gratitude to my colleagues and students who were instrumental in much of the work reported here. My appreciation to Laszlo Meszoly for his excellent artwork and to Fritz Goro and Kenneth Miyata for the photographs. Roy Ashton, John Iverson, and Albert Schwartz kindly provided data on the distributian of Anolis sagrei in Florida. This research has been generously supported by grants from the National Science Foundation, National Institutes of Mental Health, National Institute of Neurological and Communicative Disease and Stroke, National Institute of Child Health and Human Development, and Harvard College.

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tus” (T. E. McGill, D. A. Dewsbury, and B. D. Sachs, eds.), pp. 161-188. Plenum, New York. McNicol, D., and Crews, D. 1979. Estrogedprogesterone synergy in the control of female sexual receptivity in the lizard, Anolis carolinensis. Gen. Comp. Endocriml. 38, 68-74. Morgentaler, A., and Crews, D. 1978. Role of the anterior hypothalamuspreopticarea in the reglation of reproductive behavior in the lizard, Anolis carolinensis: Implantation studies. Horm. Behav. 11, 61-73. Morin, L. P. 1977. Progesterone:Inhibition of rodent sexual behavior. Physiol. Behav. 18,701-715. Morrell. J . I., and Pfaff, D. W. 1978. A neuroendocrine approach to brain function: Localization of sex steroid concentrating cells in vertebrate brains. Am. Zool. 18, 447-460. Morrell, J. I., Kelley. D. B., and Pfaff, D. W. 1975. Sex steroid binding in the brains of vertebrates: Studies at light microscropic autoradiography. In “The Ventricular System in Neuroendocrine Mechanisms” (K. N. Knigge, D. E. Scott, M. Kobayashi, and S. Ishii, eds.), pp. 230-256. Karger, Basel. Morrell, J . I., Crews, D., Morgentaler, A., Ballin, A., and Pfaff, D. W. 1977. Autoradiographic localization of 3H-estradiol, 3H-testostemne, and 3H-dihydrotestostemnein the brain of the lizard, Anolis carolinensis. SOC. Neurosci. Abstr. 7th Annu. Meet., p. 352. Morrell, J . I., Crews, D., Ballin, A,, Morgentaler, A,, and Pfaff, D. W. 1979. 3H-estradiol, 3H-testosterone and SH-dihydrotestosterone localization in the brain of the lizard, Anolis carolinensis: An autoradiographic study. J . Comp. Neurol. 188, 201 -224. Murton, R. K . , and Westwood, N. J. 1977. “Avian Breeding Cycles.” Oxford Univ. Ress, London and New York. Naftolin, F., Ryan, K. J . , Davies, 1. J . , Reddy, V. V., Flores, F., Petro, Z., Kuhn, M., White, R. J., Takaoda, Y., and Wolin, L. 1975. The formation of estrogens by central neuroendocrine tissues. Rec. Prop-. Horm. Res. 31, 295-319. Noble, G. K. 1937. The sense organs involved in the courtship of Storeria. Thamnophis and other snakes. Bull. Am. Mus. Nar. Hisr. 73, 673-725. Nottebohm, F., Stokes, T. M., and Leonard, C. M. 1976. Central control of song in the canary, Serinus canaria. J . Comp. Neurol. 165, 457-486. Palka, Y. S . , and Gorbman, A. 1973. Pituitary and testicular influenced sexual behavior in male frogs (Rana pipiens). Gen. Comp. Endocrinol. 21, 148-151. Paull, D., Williams, E. E., and Hall, W. P. 1976. Lizard karyotypes from the Galapagos Islands: Chromosomes in phylogeny and evolution. Breviora No. 441, 1-31. Phillips, R. E., and Peck, F. W. 1975. Brain organization and neuromuscularcontrol of vocalizations in birds. In “Neural and Endocrine Aspects of Behavior in Birds” (P. Wright, P. Caryl, and D. M. Vowles, eds.). pp. 243-274. Elseview, Amsterdam. Pisani. G. R. 1976. Comments on the courtship and mating mechanisms of Thamnophis (Reptilia, Serpentes, Colubridae). J . Herp. 10, 139-142. Prasad, M.R. N., and Reddy, P. R. K. 1972. Physiology of the sexual segment of the kidney in reptiles. Gen. Comp. Endocrinol Suppl. 3, 649-662. Rand, A. S. 1967. Ecology and social organization in the iguanid lizard Anolis lineatopus. U . S . Nar. Mus. Proc. 122, 1-79. Rand, A. S . , and Williams, E. E. 1970. An estimation of redundancy and information content of anole displays. Am. Nat. 104, 99-103. Roeder, K. D. 1967. “Nerve Cells and Insect Behavior” (Rev. ed.). Harvard Univ. Press, Cambridge, Massachusetts. Roeder, K. D. 1974. Some neural mechanisms of simple behavior. In “Advances in the Study of Behavior” (D.S. Lehrman, J. S . Rosenblatt, R. A. Hinde, and E. Shaw, eds.), Vol 5 , pp. 2-47. Academic Press, New York. Ross, P., and Crews, D. 1977. Influence of the seminal plug on mating behavior in the garter snake. Nanre (London) 267, 344-345.

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73

Ross, P., and Crews, D. 1978. Stimuli influencing mating behavior in the garter snake, Thamnophis radix. Behav. Erol. Sociohiol. 4, 133-142. Roughgarden, J. 1974. Niche width: Biogeographic patterns among Anolis lizard populations. Am. Nar. 108, 429-442. Ruane, S. E. 1978. Hormonal control of sexual behavior in the male frog. Am. 2001. 18,667. Schoener, T. W. 1970. Size patterns in West Indian Anolis lizards. 11. Correlations with the sizes of particular sympatric species-displacement and convergence. Am. Naf. 104, 155-174. Schoener, T. W. 1974. Resource partitioning !i ecological communities. Science 185, 27-39. Schoener, T. W. 1975. Presence and absence of habitat shift in some widespread lizard species. Ecol. Monogr. 45, 233-258. Scott, M., and Crews, D. 1980. Agonistic and courtship displays of male Anolis sugrei. Submitted. Shipley, J. E., and Kolb, B. 1977. Neural correlates of species typical behavior in the Syrian golden hamster. J . Comp. Physiol. Psycho/. 91, 1056-1073. Shire, J . G . M. 1976. The forms, uses, and significance of genetic variation in endocrine systems. Biol. Rev. 51, 105-141. Smith, H., Fawcett, J . , Sinelnik, G., and Jones, R. E. 1973. The Occurrence and significance of a protracted reproductive season with alternation of ovulation in lizards. Bull. Can. Amphib. Rept. Cons. Soc. 11, 1-4. Stamps, J. A. 1975. Courtship patterns, estrus periods, and reproductive condition in a lizard, Anolis aeneus. Physiol. Behav. 14, 531-535. Stamps, J. A. 1977. Social behavior and spacing patterns in lizards. I n "Biology of the Reptilia" (C. Gans, and D. W. Tinkle, eds.), Vol. 7, pp. 265-334. Academic Press, New York. Sugarman, R. A., and Demski, L. A. 1978. Agonistic behavior elicited by electrical stimulation of the brain in western collared lizards, Crotaphytus collarus. Bruin Behav. Evol. 15, 446-469. Tinbergen, N. 1963. On the aims and methods of ethology. 2.Tierpsychol. 20, 410-433. Tokarz, R. R., and Crews, D. 1980. Induction of sexual receptivity in the female lizard, Anolis carolinensis: Effects of estrogen and the antiestrogen, CI-628. Horm. Behav. (in press). Tokarz, R., and Jones. R. E. 1979. A study of egg-related maternal behavior in Anolis carolinensis. J . Herp. 13, 283-288. Tokarz, R. R., Crews, D., and McEwen, B. 198Oa. Estrogen sensitive progestin binding sites in the brain and oviduct of the lizard Anolis carolinensis. Submitted. Tokarz, R. R., Ghosh, D., and Crews, D. 1980b. Relationship between circulating testosterone levels and male reproductive behavior during the annual reproductive cycle of the lizard. Anolis carolinensis. Submitted. Trivers, R. L. 1976. Sexual selection and resource accruing ab es in Anolis garmani. Evolution 30, 253-269. Valenstein, P..and Crews, D. 1977. Mating-induced termination of behavioral estrus in the female lizard, Anolis carolinensis. Horm. Behav. 9, 362-370. Van den Pol, A. N. 1975. Asymmetrical nuclear size difference in neurones in magnocellularpart of paraventricular nucleus following unilateral castration in rat. P r o p . Sor. Neurosci. Annu. Meer. Abstr. No. 708. Wada, M., and Gorbman, A. 1977. Relation of mode of administration of testosterone to evocation of male sex behavior in frogs. Horm. Behav. 8, 310-319. Weaver, W. G . 1970. Courtship and combat behavior in Gopherus berlandieri Bull. Flu. Srare Mus. Biol. Sci. IS, 1-43. Webster, T. P., and Burns, J. M. 1973. Dewlap color variation and electrophoretically detected sigling species in a Haitian lizard, Anolis brevirosfris. Evolurion 27, 368-377. Wheeler, J. M . , and Crews, D. 1978. The role of the anterior hypothalamuspreoptic area in the regulation of male reproductive behavior in the lizard, Anolis carolinensis: Lesion studies. Horn. Behav. 11, 42-60.

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Williams, E. E. 1969. The ecology and colonization as seen in the zoogeography of anoline lizards on small islands. Q.Rev. Biol. 44, 345-389. Williams, E. E. 1972. The origin of faunas. Evolution of lizard congeners in a complex island fauna: A trial analysis. Evol. Biol. 6, 47-89. Williams, E. E., and Rand, A. S. 1977. Species recognition, dewlap function and faunal size. Am. Zool. 17, 265-274. Yang. S. Y.. Soul6, M.,and Gonnan, G. C. 1974. Anolis lizards of the eastern Caribbean: A case study in evolution. I. Genetic relationships, phylogeny and colonization sequence of the roquer group. SJ’St. ZOOl. 23, 387-399. Zweifel, R. 1980. Aspects of the biology of a laboratory population of kingsnakes. I n ‘‘Reproductive Biology and Diseasesof Captive Reptiles” (J. B. Murphy and J. T. Collins, eds.), pp. 141-162. Society for the Study of Amphibians and Reptiles, Lawrence, Kansas.

ADVANCES

IN THE STUDY OF BEHAVIOR VOL.

1I

Endocrine and Sensory Regulation of Maternal Behavior in the Ewe PASCALPOINDRON LABORATOIRE DE COMPORTEMENT ANIMAL I.N.R.A. DE NOUZILLY, MONNAIE, FRANCE

PIERRE LE NEINDRE LABORATOIRE DE PRODUCTION DE VIANDE I . N . R . A . DE THEIX, BEAUMONT, FRANCE

.................................................. Endocrine State of the Ewe on the Onset of Maternal Behavior. A . Induction of Maternal Behavior in Nonpregnant Ewes B, Fading of Postpartum Maternal Responsiveness Neonate ................................ C. Discussion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 111. Influence of the Newborn Lamb on the Development of Postpartum Maternal Behavior . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . A. Influence of the Characteristics of the Neonate on the Display o Behavior ............................... B. Influence of Information Provided by the Newb Maintenance of Maternal Behavior ................. C. Discussion. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . IV. Mother-Young Relationships beyond A . Suckling Behavior. . . . . . . . . . . . . ................. B. Recognition of the Young . . . . . . ......... C. Discussion . .......................................... V. Maternal Behavi xperienced Ewes ............................ A. Comparison of Maternal Behavior at Parturition in Primiparous and ............................ Multiparous Ewes B. The Role of Hormones in the Regulation of Maternal Behavior in

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

..... .................. C. Discussion.. ........... VI. Conclusion and Future Prospects of Research . . . . . . . . . . . . . . . . . . . . . . . . . References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

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15 Copyright @ 1980 by Academic FTess. lnc. All rights of repmduction in any form reserved. lSBN 0-12-00451 1-7

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I. INTRODUCTION In sheep, a lasting mother-young bond is established very rapidly after parturition. Within a few minutes following expulsion, the mother starts to lick the newborn lamb. The young is soon able to stand up and usually starts to suck within the first hour of life. Maternal care quickly becomes exclusive. The ewe accepts only her lamb at suckling and rejects, often violently, any alien young which may try to suck. The study of mother-young relationships in sheep has developed in two main directions. The formation of the mother-young bond at parturition is important, practically speaking, since perturbations at this time may result in a loss of animal production. This is why a number of studies have focused on the maternal behavior of parturient ewes in the field and on the performances of the neonates in relation to postnatal mortality (Wallace, 1949; Alexander, 1958, 1960; Alexander and Williams, 1964, 1966). Basically, however, studying the establishment of mother-offspring relationships in sheep is attractive in itself because a stable, exclusive mother-young bond is established rapidly at parturition. Such a model offers the possibility of studying the mechanisms of attachment in mammals in a manner somewhat similar to that already used in birds (Heinroth, 1911; Lorenz, 1937; Hinde et al., 1956; Hess, 1957, 1958; Guiton, 1958, 1959). This partially explains why early fundamental studies carried out on sheep focused on the possible existence of an imprinting process in young ungulates (Scott, 1945; Blauvelt, 1955; Liddell, 1960; Hersher et al., 1962; Cairns and Johnson, 1965; Smith et al., 1966). However, interest in the sheep model was further enhanced because a “critical period” in the dam as well as in the lamb was likely to be involved in the development of the mother-young bond in ungulates (Collias, 1956; Hersher et al., 1957, 1958). Studies dealing with the display of maternal behavior of ewes in the field have documented the exclusive nature of this behavior (see reviews of Fraser, 1968; Geist, 1971; Hafez et al., 1969). In contrast to the analysis of the newborn’s attachment to the mother, analysis of the mechanisms of the mother’s formation of a bond with the newborn progressed much more slowly. The enormous amount of labor necessarily involved in waiting for parturition, whose timing is quite unpredictable, certainly accounts in part for this slow progress. In comparison, studies of laboratory animals have developed more rapidly, due to the shortness of their reproductive cycle and also to their low maintenance cost. The studies on laboratory animals have emphasized the existence of interactions between the physiology of the female and the manifestation of maternal behavior (see reviews by Noirot, 1972; Richards, 1967; Rosenblatt et al., 1979). Recently, the control over the reproductive physiology of the ewe, particularly the timing of fertilization and parturition, has minimized methodological impediments associated with the study of ewes at

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lambing. Better understanding of the regulation of maternal behavior in rodents, together with progress in our understanding of the endocrinology of the parturient ewe, have contributed to the development of recent studies on maternal behavior in sheep. The formation of mother-young relationships depends on mutual bonding between the dam and the offspring. However, the present article is limited to the regulation of maternal behavior in the ewe with reference to recent experimental work concerning the onset, establishment, and maintenance of this behavior. Study of the young is thus limited to the role they play in the manifestation of maternal behavior by the ewe.

11.

INFLUENCE OF THE ENDOCRINE STATEOF THE EWEON ONSETOF MATERNAL BEHAVIOR

THE

The onset of maternal behavior in the ewe appears closely associated with parturition (cf. Fig. 1). Attraction for newborn lambs in barren females is uncommon (Scott, 1945), whereas it becomes increasingly easy to observe in ewes during the last 2 weeks of pregnancy and, even more so, in the last 12 hr preceding parturition (Alexander, 1960; Arnold and Morgan, 1975). Also, after parturition, maternal responsiveness seems to fade within a few hours when the dam is deprived of her lamb from birth (Collias, 1956; Hersher et al., 1963a). A similar phenomenon exists in goats (Klopfer et al., 1964) and in cattle (Hudson and Mullord, 1977; L.e Neindre and Garel, 1976). Thus, a temporary attraction of the mother for the newborn exists around parturition and this has led to the conclusion that a “critical period” exists for the development of maternal attachment of the dam for her offspring (Hersher et al., 1963a,b; Smith et al., 1966). Due to the close synchrony between parturition and the onset of maternal behavior, it was tempting to hypothesize that the development of pregnancy and parturition, by providing endocrine and nervous stimulation, were of some importance in controlling the onset of maternal behavior, as suggested by Hersher et al. (1963a) and Klopfer and Klopfer (1968). The large hormonal changes associated with the initiation of the birth process could be involved in this regulation. This has proved to be correct for laboratory animals such as the rat (Terkel and Rosenblatt, 1972) and initial results obtained on sheep tend also to support this hypothesis. Evidence for a hormonal regulation of maternal behavior in the ewe comes mainly from two types of studies. The first consists of inducing maternal responsiveness with hormones in nonpregnant ewes, and the second, in altering the characteristics of the so-called “critical period” of temporary re-

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FIG. 1. Various aspects of maternal behavior in parturient ewes. (a) Reparturient ewe showing strong interest for the genital region (forelegs of lamb apparent) of another ewe ready to lamb (Ile-de-France breed); (b) preparturient ewe licking alien newborn lamb (Ile-de-France breed); (c) licking of the neonate (Prealpes-du-Sud ewe); (d) pawing on the lamb (Realpes-du-Sud); (e) first suckling (Ile-de-France).

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79

sponsiveness, which occurs immediately after parturition, by manipulating the hormonal balance at that time. A.

INDUCTION OF MATERNAL BEHAVIOR I N NONPREGNANT EWES

I . Possibility of Inducing Maternal Behavior with Hormones Inducing milk production in nonpregnant females using various hormonal treatments has been used in sheep to study the role of hormones in lactation. Several methods have been developed involving the use of progesterone and estrogens (Fulkerson and McDowell, 1974; Head et al., 1975); both hormones play a role during pregnancy and parturition in sheep (Nathanielsz, 1978). Such methods therefore provided a possible model for the study of maternal behavior, by using hormone treatments which mimic to some extent the hormonal changes occurring during late pregnancy and parturition. Thus ewes were studied during lactation without the animals experiencing parturition. In the first series of experiments (Le Neindre e?a l . , 1979), we investigated the possibility of inducing maternal behavior by using either a long-term treatment [Fulkerson and McDowell, 1974; 60 mg progesterone + 240 p g estradiol benzoate (EB) every third day for 30 days and 20 mg of EB on day 301 or a short-term treatment (Head et al., 1975; 62.5 mg progesterone + 25 mg estradiol per day for 7 days). The behavior of primiparous ewes will be discussed in Section V,B; the results reported here and in all other sections of this article, unless otherwise specified, concern multiparous animals, i.e., animals having reared their young at least once. Ewes were tested on the day milking would normally have commenced (days 3 1 and 2 1, respectively, in the above studies) by presenting them with newborn lambs that remained with the ewes for 2 hr. In addition, some ewes undergoing a short-term hormonal treatment were tested on day 14 to obtain an idea of the latency of response to the treatment. Regardless of the type and length of hormonal treatment, a number of ewes showed maternal behavior after the hormones were administered (9/19 for the long-term treatment and 14/23 for the short treatment-tests on days 14 and 21 being pooled). In contrast, none of the control animals displayed maternal behavior (0/7 intact, untreated ewes and 0/11 ovariectomized ewes, Fig. 2). Another interesting fact was that a high proportion of ewes tested on day 14 of the short course treatment were already maternal at that time (7/12). This further supported the idea that the length of hormonal treatment was not an essential factor influencing the proportion of ewes displaying maternal behavior. Therefore, it appeared clear from these results that inducing maternal behavior without the experience of parturition is possible and that the induced behavior is complete, including licking of the newborn, emission of low-pitched bleats, acceptance at suckling, and the establishment of a discriminating bond. The response

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PASCAL POINDRON AND PIERRE LE NEINDRE

n=14

n=ll

nal9

a

b

c

Long-term treatment

'

l

I

n=?

n=23

d

e

Short-term treatment

FIG.2. Hormonal induction of maternal behavior in nonpregnant ewes. (a) Parturient ewes. (b) Ovariectomized nontreated ewes. (c) Intact ewes treated with 60 mg of progesterone + 240 p g of EB every third day for 30 days + 20 mg of EB on day 30. (d) Intact nontreated ewes. (e) Intact ewes treated with 1.5 mg of progesterone + 0.5 mg EBkg body weight every day for 7 days. Adapted from Poindron and Le Neindre (1979). to the treatments did not, however, appear very specific since abnormal behavior such as nudging and mounting was observed in several ewes. These studies did not allow us to assess the respective roles of progesterone and estrogen in the induction of maternal behavior. Moreover prolactin was secreted in large amounts during the treatment and its role also could not be determined (G. Kann, personal communication).

2 . Role oj'the Physiological State of the Ewe Further studies were carried out to determine under what conditions ewes could display maternal behavior without exogenous treatment, during various reproductive states. An attempt was also made to dissociate the respective roles of progesterone and estradiol in the hormonal induction of maternal behavior in either intact or ovariectomized ewes. In all these experiments, experimental conditions and procedures were similar to those described for the initial study of Le Neindre er al. (1979). Ewes were tested individually with newborn lambs which remained with the ewes for 2 hr. The possibility that maternal behavior can occur without exogenous hormone treatment was investigated in the following groups: Group 1: Nine intact ewes were tested at estrus (within 12 hr of the onset of estrus).

MATERNAL BEHAVIOR IN THE EWE

81

Group 2: Five, four, and five females were tested at 45, 75, or 105 days of pregnancy, respectively. Group 3: Twenty females were tested at 135 days of pregnancy. Group 4: Ten females were observed with their lambs at parturition. This study enabled us to obtain information from ewes with high levels of progesterone and little estradiol (Fig. 3, Group 2), high levels of progesterone and rising levels of estradiol (Group 3), and low levels of progesterone and high levels of estradiol (Groups 1 and 4). Results are shown in Fig. 3, together with a representation of the profiles of I& and progesterone during a reproductive cycle. They show that maternal behavior can be observed independently of parturition. Maternal behavior appeared during estrus when ELwas at a high level and during late pregnancy when ELlevels were either beginning to rise or had reached a peak at parturition. To assess the exact role of treatment with progesterone and & in eliciting maternal behavior in the nonpregnant ewes, two experiments were carried out. In the first study, intact ewes were injected for 7 days with either progesterone or estradiol (1 -25 and 0.5 mg/kg body weight, respectively; nine and eight females, n.9

0.5

n-4

n=5

n-ZOn-I0

t 2 * u estrus

cycle +-

days of pregnancy

I

'

SO ' 70

,

I

90

,

110

.

i 0

.

150

FIG.3. Maternal responsiveness of ewes toward newborn lambs at various stages of the reproductive cycle with parallel changes in serum levels of progesterone and estradiol17p. Hormone data adapted from Terqui (1974) and Stabenfeldt (1974).

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PASCAL POINDRON A N D PIERRE LE NEINDRE

respectively) and tested 14 days after the start of the treatment. In a second study, the response of ovariectomized ewes to a single injection of either hormone was carried out between 6 and 10 hr after injection. Ewes that did not respond at this time were tested a second time 18 to 26 hr after injection. In a control group, nontreated, ovariectomized ewes were tested three times in 24 hr, to investigate a possible onset of maternal behavior due to the repetitive presentation of the young. The comparison of results observed in ewes treated with E& or progesterone indicates that both hormones can elicit maternal behavior (4/8 vs 4/9, respectively for a 7-day treatment). Estradiol seems slightly more effective than progesterone in a single injection (9/11 vs 5/11, respectively; Fig. 4) given to ovariectomized females. The study done on ovariectomized ewes indicates that the response is very rapid. In contrast to our initial study (Le Neindre et al., 1979), a few untreated ovariectomized ewes showed maternal behavior, and it would appear that this is enhanced by repeated presentation of newborn lambs (Fig. 4) * Our results indicate that two factors influence which hormones can elicit maternal behavior in ewes: these are whether the female is intact or ovariectomized and whether she receives exogenous hormone treatment or is stimulated by endogenous sources of hormone. In ovariectomized ewes estrogen is slightly more effective than progesterone in eliciting maternal behavior. In intact ewes, endogenous estrogen is more closely related to maternal behavior than endogenous progesterone, but both hormones are equally effective when given exogenously. This could reflect a conversion of progesterone into estrogens in the latter case, whereas this process does not occur in ewes during midpregnancy.

E

P

C

Following two or lhrn Iosls (from 6 to 24 hr after injection 1

j I

I

I

E

P

C

At lh. first t d ( 6 l o 10 tw oflw Injoclion )

I I

FIG. 4. Onset of maternal behavior in ovariectomized ewes following a single injection of progesterone (P,60 mg), estradiol-17P (E, 25 mg), or no treatment (C). Same letters for two groups indicate that there is no significant difference between these groups.

83

MATERNAL BEHAVIOR I N THE EWE

B . FADING OF POSTPARTUM MATERNAL RESPONSIVENESS IN ABSENCE OF THE NEONATE

THE

Ewes not allowed to have contact with their newly born lamb(s) just after birth rapidly show a fading of maternal behavior within 2 hr (Collias, 1956). A similar phenomenon has been observed in goats after a shorter period of 1 hr (Klopfer et al., 1964). In contrast, among goats a mother-offspring separation, of the same length of time, occurring after an initial contact, does not lead to rejection of the newborn (Hersher et al., 1958; Klopfer et al., 1964). During their initial contact with their young, mother sheep and goats establish a discriminating bond which has led several investigators to propose that the establishment of maternal behavior in sheep and goats depends on a mechanism somewhat comparable to the one described by Lorenz (1937) in young precocial birds, known as “imprinting. This imprinting process, which establishes an exclusive bond, is believed to occur during the so-called “critical period” just after parturition, and the absence of contact between mother and young at this time is believed to result in failure to establish this response. In both sheep and goats, however, further investigation has revealed discrepancies in this hypothesis. Compared to the results of Collias (1956), Smith et a / . (1966) found that among sheep separations of up to 8 hr postpartum did not affect the establishment of maternal behavior. Hersher e f al. (1963b) found that in goats forcing contact with an alien young could lead to the formation of an additional bond long after the end of the critical period. Also, Smith e f al. (1966) suggested that the duration of contact necessary for the ewe to establish discriminating behavior did not depend on the time at which contact occurred in relation to parturition. Within 20 to 30 min of contact with their lambs all ewes showed signs of discriminative behavior, despite the fact that the length of separation from parturition between dams and their offspring ranged from 15 min to 5 hr. Furthermore it was found in goats that acceptance of a young could occur without necessarily involving the presence of an exclusive response (Klopfer and Ganhle, 1966; Klopfer and Klopfer, 1968). Goats made anosmic at the time of parturition still accepted their kids, though they did not show signs of a selective behavior. Thus, when studying the establishment of maternal behavior, it is important to distinguish between manifestation of interest for a young (any young-that we will refer to as maternal responsiveness) and the formation of an exclusive bond. ”

1 . Existence and Duration of the Sensitive Period

Recently, with the use of a method for synchronizing deliveries in sheep, further studies have been made possible, employing a relatively large number of animals. A recent study using multiparous, Merino ewes has enabled us to confirm the existence of a clear effect on maternal responses to lambs according

84

PASCAL POINDRON AND PIERRE LE NEINDRE n.10

0’

n-8

n=8

n.8

4 hr*

12 hr*

24 hr*

n.10

24 hr*

FIG.5 . Proportion of ewes showing maternal behavior after various lengths of mother-young separation either at parturition or 2 to 4 days after lambing (Merino breed). Length of mother-young separation: +, removal of the young at lambing; separation at 2 to 4 days after lambing. From Poindron and Le Neindre (1979).

*,

to when separation is performed relative to parturition (Poindron et al., 1979). A mother-young separation of 24 hr, starting at birth, leads, in most ewes, to the fading of maternal responsiveness (in six cases out of eight) (Fig. 5 ) , whereas the same separation performed 2 to 4 days after parturition is of little consequence (1 temporary rejection out of 10 ewes tested, p = 0.009). This study also indicated that there is large individual variation in the duration of the postpartum period of responsiveness. While four dams out of eight already were not maternal after a 4-hr separation, two ewes out of eight remained maternal up to 12 hr postpartum and a similar proportion were maternal after the 24-hr separation (Fig, 5). It would appear therefore that the decline in maternal responsiveness is most marked in the first 12 hr following parturition and this is probably the limit of the sensitive period in most ewes. It can be noted in the present experiment that the fading of maternal responsiveness was analyzed without taking the exclusive character of maternal behavior into account. Therefore the postpartum period during which maternal behavior is established appears more as a period of sensitivity to a neonate (any neonate) than as a period during which an exclusive response toward orte lamb has to be established to allow the maintenance of maternal behavior. For this reason it seems more appropriate to use the term “sensitive” period rather than “critical” period, the latter being generally understood more restrictively. 2 . Endocrine Regulation of Postparturient Maternal Responsiveness

Finding the limits of this period of maternal sensitivity toward offspring, which may be referred to as the “sensitive period” rather than the “critical

MATERNAL BEHAVIOR IN THE EWE

85

period,” is of interest. This does not, however, provide us with information on the mechanisms controlling this period of maternal responsiveness. It has been shown that the onset of maternal behavior is stimulated by hormones. It was tempting to assume that the fading of maternal responsiveness in the absence of an offspring-thus the length of the sensitive period-was also under hormonal control, as suggested by Hersher et al. (1963a) and Klopfer and Klopfer (1968). If this hypothesis is correct, changing the time course of estrogen level in maternal blood should lead to a modification in the duration of postpartum maternal responsiveness, since estrogen appears to be the hormone which is closely associated with the onset of maternal behavior (see Fig. 3). For this purpose, ewes were induced to lamb with the administration of a high dose of EB (20 mg) to ensure high levels of estradiol-17/3 for much longer than is normally observed in noninduced ewes (Thorburn ef al., 1972), as shown in Fig. 6A. A control group consisted of ewes induced to lamb by administration of 15 mg of dexamethasone. This second method is known to initiate parturition mainly by acting on the fetus (Bosc, 1974), thereby inducing hormonal changes in the mother, comparable to those occurring during spontaneous delivery (Bassett and Thorburn, 1969; Liggins et al., 1972; Thorburn et al., 1972). By contrast, estrogens are thought to act on the placenta and the uterus, by increasing the secretion of prostaglandins and by stimulation of uterine contractions

FIG.6. Estradiol-17P and prolactin levels at parturition in Merino ewes injected with either 15 mg dexamethasone (D) or 20 mg estradiol benzoate (EB) (A), together with the fading of maternal behavior in these same ewes when deprived of their lambs at delivery (B). Adapted from Poindron er al. (1979).

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PASCAL POINDRON AND PIERRE LE NEINDRE

(Nathanielsz, 1978; Terqui, 1978). All ewes were tested for spontaneous acceptance of their lamb following a mother-young separation of either 4, 12, or 24 hr starting at parturition. The procedure was similar to the one used when studying the duration of the sensitive period in ewes lambing spontaneously and is fully described in Poindron et ,ul. (1979). A larger number of ewes treated with 20 mg of EB remained maternal up to the end of testing at 24 hr than did ewes treated with dexamethasone(22/29 vs 12/39; p = 0.02; see Fig. 6B). Ewes treated with dexamethasone did not show spontaneous acceptance in a higher proportion than ewes that had received no hormone treatment (12/39 vs 8/24, p = 0.7; Figs. 5 and 6B). Whereas untreated ewes or females treated with dexamethasone showed a significant decrease in the proportion of ewes remaining maternal as a function of the duration of separation [Sokal and Rohlf, 1969; G(2)= 6.9, p C 0.051, no similar trend was observed in ewes treated with EB [G(2) = 0.2, p > 0.51. As a consequence, the difference in the proportion of spontaneous acceptances observed between ewes is most marked for the longer periods of separation (Fig. 6B; 60 vs 30% for the 12-hr separation and 56 vs 17% for the 24-hr separation). These results, therefore, support the hypothesis that the duration of the sensitive period for the establishment of maternal behavior is under hormonal control. A pharmacological effect of estrogen cannot be excluded, since levels found in ewes induced to lamb with dexamethasone were much lower than those of ewes treated with EB (Fig. 6A). However, the schedule of blood sampling (every 12 hr) can account partly for this difference. Estradiol benzoate injection ensures a rapid rise in E2 followed by a very slow decrease, whereas in ewes treated with dexamethasone (as in untreated females), there is a sharp rise followed by a rapid decrease. Therefore it is likely in the second situation that the maximum values for & were missed due to the sampling schedule. In fact, intensive studies of parturition in sheep indicate that E$ can rise to levels ranging from 200 to 900 pg/ml in preparturient ewes (Terqui, 1974; Thorburn et af., 1972), which is not very far from values observed in EB-treated ewes. In any case, these results do not necessarily imply that estrogen is directly responsible for the control of maternal behavior. Other hormonal changes subsequent to the high levels of estrogen could also be involved in the regulation of maternal responsiveness: for example, it is well known that the pattern of prolactin secretion varies under the influence of estrogen (Labrie et af., 1978; Terqui, 1978). Indeed this was noticed in ewes treated with EB: prolactin levels remained high for a period of time longer (Fig. 6A) than had previously been reported in parturient ewes, especially in a situation in which the ewes did not suckle (Davis el af., 1971; Chamley et af., 1973). However, a study was done on ewes induced to lamb with either dexamethasone, EB (20 mg), or EB and dibromoergocryptine simultaneously administered to block the release of prolactin (CB 154, 1 mg every 12 hr from the

MATERNAL BEHAVIOR IN THE EWE

87

FIG. 7. Prolactin levels (A) in Prealpes-du-Sud ewes induced to lamb with 15 mg dexamethasone (D) or 20 mg estradiol benzoate (EB) or 20 mg estradiol benzoate and 1 mg dibromoergocryptine from the time of EB injection up to 24 hr after delivery (EB + CB 154) together with the fading of maternal behavior in the same ewes when deprived of their lamb for 24 hr (B). From Poindron er al. (1980b).

time of the EB injection until the time of testing). The results failed to confirm the prolactin hypothesis (Poindron et al., 1980b). Ewes were separated from their lambs at birth and tested for maternal behavior 24 hr later, by being reunited with the lambs. Only 3 ewes out of 22 remained maternal in the group treated with dexamethasone, whereas, as expected, a high proportion of females were maternal in the group treated with EB (15/23, p = 0.001). Although CB 154 was effective in blocking prolactin release, as shown in Fig. 7A, ewes treated with both EB and CB 154 did not differ from ewes treated with EB only (17/22, p = 0.88, see Fig. 7B). If prolactin alone was responsible for lengthening the sensitive period, ewes treated with dexamethasone should have performed better than ewes treated with EB and CB 154, which was not the case, and if it acted synergistically with EB, then the EB and EB + CB groups should have differed significantly. C.

DISCUSSION

The results of these experiments concerning both the hormonal induction of maternal behavior in nonpregnant ewes and the effect of estrogen on the length of the sensitive period indicate clearly that the hormonal balance of the mother plays

88

PASCAL POINDRON A N D PIERRE LE NEINDRE

an important role in the regulation of her attraction to the neonate. It would appear that neither parturition, lactation, nor even a long period of hormone treatment is absolutely required in multiparous ewes to elicit maternal behavior since responses were obtained in such nonpregnant ewes given a single injection. The association of maternal behavior in intact ewes with the probable presence of estrogen, together with the observed effects of estradiol benzoate on the sensitive period, suggest that estrogen is involved in the control of maternal responsiveness, and it is likely that the appearance of maternal behavior as well as its fading after parturition, when the neonate is withdrawn, are both based upon common mechanisms. Whether estrogen is the direct initiator that acts on the brain or whether it is merely an indirect component interacting with other hormones, is not known. An estrogen-induced release of prolactin is unlikely to be important according to our results and to those of Kann ef al. (1978) on parturient ewes, in which the injection of dibromoergocryptine failed to affect maternal behavior. Estrogen can affect the release of hormones other than prolactin, however. This is the true for oxytocin and neurophysin, which is associated with the release of oxytocin (Roberts and Share, 1969; Robinson, 1975a,b; Robinson et al., 1976; Legros, 1976; Seif and Robinson, 1978). As a matter of fact, it must be stressed that we never obtained a 100% induction of maternal behavior in nonpregnant females, even when testing the effects of EB during the sensitive period, despite the fact that the doses of EB were sufficient to produce blood levels of estradiol at least as high as those observed during the prepartum peak. Therefore, it is likely that other factors are also involved in the onset of maternal behavior. Either the synergistic action of more than one hormone is involved or a temporal patterning of several hormones at certain relative levels is important to ensure optimal maternal responsiveness. Also, despite the fact that parturition is not indispensable for the onset of maternal behavior, this does not exclude the hypothesis that the delivery experience facilitates the onset of maternal behavior. Whatever the exact mechanism of regulation, it is clear that physiological factors around parturition are involved in eliciting maternal attraction to lambs independently of the presence of the offspring. However, it would be wrong to postulate that the neonate plays only a passive role, allowing the ewe to exhibit adequate maternal behavior on an endogenous basis.

111. INFLUENCE OF THE NEWBORN LAMBON

THE DEVELOPMENT OF POSTPARTUM MATERNAL BEHAVIOR

The results discussed in Section I1 lead to the conclusion that in sheep (and presumably goats also), there is certainly a limited period for the establishment of maternal behavior. This initial responsiveness appears largely under hormonal

MATERNAL BEHAVIOR IN THE EWE

89

regulation, at least in sheep. There is however a postpartum interval after which hormones can no longer account for the maintenance of maternal behavior. After delivery, the experience provided to the ewe by her contact with the neonate rapidly begins to influence her subsequent maternal behavior. Therefore, it is important to study the role played by the lamb at this time in order to understand how maternal behavior continues and develops further after parturition. First, it is important to clarify whether maternal attraction observed at parturition is specific to well-defined characteristics of the neonate or whether, on the contrary, the dam can be attracted by a wide range of stimuli provided by the young. Also, the nature of the information, specific or nonspecific, which enables the ewe to remain maternal beyond the limits of the sensitive period remains to be investigated. Last, the exact role played by maternal discriminating behavior with respect to her own and alien lambs in the establishment of lasting maternal behavior is not clear. Investigations concerning the first two aspects of the role played by the young provided additional elements for an answer to the question of the influence of the newborn lamb on the development of postpartum maternal behavior. A.

INFLUENCEOF ON THE

THE CHARACTERISTICS OF THE NEONATE DISPLAY OF MATERNAL BEHAVIOR

To evaluate how the newborn lamb can influence maternal behavior, it may be useful to recall some of the characteristics which belong to the newborn. The first element that may be of importance is the presence of placental fluids on the lamb's coat. These fluids disappear within about an hour, when the dam cleans her offspring. When the lamb is not kept with the mother, drying of the coat is usually completed within 4 to 8 hr. In any case, it is clear that placental fluids are present only during the first hours of life. A second element which changes rapidly concerns the lamb's behavior. Initially, within a few minutes, the young starts to move and it is usually able to stand up and obtain access to the udder within an hour after birth (Hulet er al., 1975). Whether these characteristics of the newborn are important for the manifestation of maternal behavior at parturition is worth being considered. In sheep, and also in goats, parturient mothers accept day-old alien young (Hersher et al., 1963a; Klopfer and Klopfer, 1968). At first sight, this might suggest that the characteristics of the newborn are of little importance in the manifestation of maternal behavior at parturition. However, specific studies on this matter indicate that such a conclusion would be hazardous. Smith et al. (1966) reported that newly born alien lambs were licked more than dry ones, although all were accepted. In goats, recent studies indicate that newly born alien kids are more readily accepted by parturient does than day-old ones (Gubernick et al., 1979). In sheep, the acceptance of an alien lamb is also influenced by its age. In a

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PASCAL POINDRON AND PIERRE LE NEINDRE

study carried out on multiparous, Merino ewes at the University of Western Australia, the behavior of parturient ewes whose lambs were exchanged first for an alien newborn and, 10 min later, for a 12- to 24-hr-old lamb was studied (Poindron, 1980). The exchange for the ewe’s own lamb was performed either at birth (four females) or after an initial mother-young contact of either 30 (seven females) or 60 min (seven females). All ewes were tested a second time 60 min after the first test. Except for one ewe, all ewes gave birth to only one lamb. Parturition was induced with 15 mg of dexamethasone, given on day 147 of pregnancy. Delivery was assisted in all animals when the fetal head and front legs protruded. The criteria for maternal acceptance were licking, emission of low-pitched bleats only, absence of restlessness after exchange, and standing during the attempts at suckling by the ewe. Results are represented in Fig. 8. A very clear difference exists between the overall proportion of ewes accepting a lamb when tests were performed with a newborn and with a 12- to 24-hr-old lamb (12/18 vs 5/18 when considering the sum of the first series of tests at 30 and 60 min after delivery, p = 0.02, or 20/36 vs 6/36 when including the second series of tests on these same animals). The development of maternal acceptance of an alien as a function of the prior duration of contact between the mother and her own lamb provides an idea of the dynamics of establishing the discriminating behavior in parturient ewes. There is a significant decrease in the proportion of ewes accepting an alien lamb [whether it is a newborn or a 12- to 24-hr-old offspring after mother-young contact of 30 min or more (G(4) = 11, p < 0.05); see Fig. 81. This decrease reflects the establishment of discriminating behavior in the dam. This interval is in agree-

,

n = 4 n = l n=11 n.1

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n.7

-s

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30

60

90

120 min

Length of mother- young contact before lest

FIG. 8. Acceptance of newborn or 12- to 24-hr-old alien lambs by Merino ewes after parturition in relation to the length of mother-young contact preceding the test (0 = parturition): 0 , newborn alien lamb; A, 12- to 24-hr-old alien lamb.

MATERNAL BEHAVIOR I N THE EWE

91

ment with the results of Smith et a / . (1966), although these authors reported that all ewes have established selective bond with their own lamb within 30 min after delivery, whereas in the present study, more than 50% of ewes showed no signs of discrimination between their own and alien newborn after 60 or 90 rnin of contact with their own young. The fact that in the present experiment lambs were exchanged whereas alien lambs were added in the study of Smith et a / . may account for some of these variations. Despite the clearcut difference observed in our study when ewes were tested with newly born lambs and “aged” (12- to 24-hr-old) lambs, it could not be determined if it was the characteristics of the lambs that were entirely responsible for the difference in maternal behavior. The fact that tests with the newborn were always performed before tests with the aged lambs could have influenced the results also. To verify this, a follow-up study was effected using multiparous Prealpes-du-Sud ewes, also induced to lamb with dexamethasone (15 mg). Ewes were tested for their acceptance of an alien lamb as in the first study reported, but only one test was carried out per ewe, with either a neonate or an “aged” (12- to 24-hr-old) lamb. Tests were performed by exchanging the ewe’s own lamb for an unrelated lamb either at delivery (single or twin births, Group I ) , or 30 rnin after delivery (single births only, Group 2), or at the birth of the second lamb (twin births only, Group 3), the first lamb remaining with its dam. Control tests using the ewe’s own lamb were done for all groups. Further details of the procedure are reported in Poindron et al. (198Oa). Results, which are summarized in Fig. 9, confirm that exchanging a ewe’s lamb at parturition for an alien does not result in noticeable perturbations in the ewe’s behavior. In contrast, the exchange with an “aged” alien lamb results in significant modifications of maternal behavior when considering the duration of licking, the incidence of aggressive behavior, or the type of vocalization (low or high pitch). This is true in the three experimental groups (exchange performed at delivery, after 30 min of mother-young contact, at the birth of the second lamb of the litter). However, when the swapping was performed 30 min after delivery, the difference between groups tested with a newborn alien and with an aged alien tended to be less marked, suggesting that selective behavior in relation to the ewe’s own lamb is already present 30 rnin after birth in some ewes. This agrees with results obtained on Merino ewes (cf. Fig. 8). Concerning Group 3 (exchange performed at the birth of the second lamb), ewes accepted alien newborn lambs more readily than 12- to 24-hr-old ones. However, when comparing the behavior of the control animals (behavior of dams toward their own second lamb) with that of ewes toward newly born alien lambs, there is a clear difference in the duration of licking between the two groups [4.6 _t 0.8 vs 2.5 4 0.4 min (mean k SE); p < 0.051, and the proportion of ewes accepting the newborn alien without any disturbance of maternal behavior is lower than in the control groups @/I1 vs 17/17, p = 0.05). Therefore, ewes would seem to distinguish between

92

PASCAL POINDRON AND PIERRE LE NEINDRE

FIG.9. Acceptance of an alien lamb by postparturient ewes (Prealpes-du-Sud breed) in various situations and in relation to the age of the alien lamb. Group 1 : Exchange done at birth of first lamb (single births or twin births with second lamb born after end of test with alien). Group 2: Exchange done 30 min after birth of own lamb (single births only). Group 3: Exchange done at birth of second lamb, the first lamb remaining with its dam (twin births only). Group 4:Ewes separated from their lamb at parturition and tested 12 hr later with either their own 12-hr-old lamb or an alien newborn lamb. Duration of tests: 10 min in Groups 1, 2, and 3; 30 min in Group 4.Different letters between subgroups of a same group indicates significant difference (one-tailed; p < 0.05) between these subgroups. In Group 3, p = 0.05; in Group 4, p = 0.06.

*,

+,

their second lamb and a newborn alien presented at the time of birth of the second lamb. It is not known yet whether this is due to some methodological artifact or whether it is of biological significance. Additional confirmation that some characteristics of the neonate influence the maternal response to the lamb at parturition can be drawn from additional studies that were carried out on the sensitive period (Poindron et al., 1980a). In our methodology used to study the sensitive period (cf. Section II,B), we tested ewes with their own lambs. This means that not only were we measuring the effects of the length of separation on maternal behavior, but also factors associated with the age of the lamb. This effect is best illustrated by the comparison of the proportion of ewes showing maternal behavior after a 12-hr separation from birth in groups

MATERNAL BEHAVIOR IN THE EWE

93

tested with either their own 12-hr-old lambs or with an alien newborn. Of 21 ewes tested with an alien newborn, 10 accepted the lamb (48%, Fig. 9), whereas only 8 out of 34 ewes tested with their own 12-hr-old-lambs did so [(24%) one-tailed exact probability = 0.061. Here again, there was a marked tendency for more ewes to be maternal toward a newborn than toward a 12-hr-old lamb. Also, in the light of these results, the fading of postpartum maternal responsiveness reported in Section II,B may merely reflect a decrease in the attractiveness of the young. In fact, it is possible that a reduction in the lamb’s attractiveness can account partly for the decrease in maternal responsiveness in our studies.

B . INFLUENCE OF INFORMATION PROVIDED B Y THE NEWBORN LAMBIN THE MAINTENANCE OF MATERNAL BEHAVIOR The temporary responsiveness of the parturient ewe develops rapidly into an enduring maternal behavior, since mother-young separation, which, if effected at parturition, would lead to rejection of the young, is of little consequence when performed 2 to 4 days postpartum. Thus, contact with the newborn ensures the formation of a lasting maternal bond. To assess the relative role of various cues provided by the lamb, the maintenance of maternal behavior was studied in ewes placed in situations that resulted in different degrees of deprivation of stimuli from their lambs (Fig. 10). When studying the sensitive period, it was not clear whether rejection observed after mother-young separation (cf. Section I1,B) should be interpreted as a discriminating response of the dam to a lamb that she considers to be an alien (due to the lack of previous olfactory contact), or whether it should be regarded as due to the fading of maternal responsiveness toward the lambs. To clarify this, ewes were made anosmic before parturition and then were totally separated from their lambs for 12 hr. In Group 5, where ewes could hear and see their lambs but could not smell them, a parallel study was carried out on anosmic ewes, since a similar problem was raised due to the situation in which ewes were placed. 1. The A4uintetmic.e of Muleraal Behmior

All females of Groups 1 , 4, 5, and 6 (cf. Fig. 10) were multiparous, Merino ewes. In Groups 2 and 3, females were either multiparous Merino ewes (seven females from Group 21 and seven females from Group 2E) or multiparous Prealpes-du-Sud ewes (1 3 females from Group 21 and the 1 1 females from Group 31). All ewes gave birth to one lamb except for six Prealpes-du-Sud from Group 2 and nine Prealpes from Group 3. In the case of twin births, only the first lamb remained with its dam. Parturition was induced with 15 mg of dexamethasone except for ewes of Group 1 and eight ewes from Group 5. The ewes from those two groups were the dams included in the study of the sensitive period (cf. Section I1 ,B).

E m induced t o h b with lexamdhmow o h noninduced Intact

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n = I I [gh. 31)

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n = 2 3 Ign. 611

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FIG.10. Experimental design for studying the role of various sensory cues from the lamb in the maintenance of maternal behavior beyond the sensitive period. Numbers indicate the number of ewes per group; numbers in parentheses refer to groups (gr.)as mentioned in the text and in Fig. 11 (I, intact; A, anosmic: E, estrogens). Studies were effected on aged Merino ewes except in Groups 2 and 3 which included some Prealpes-du-Sud ewes (cf. text).

MATERNAL BEHAVIOR I N THE EWE

95

Another important question raised by our study in which the sensitive period was lengthened by an EB injection concerns how estrogen affects spontaneous acceptance. To investigate the possible effects of estrogen on sensory perception, the maintenance of maternal behavior was also studied in three groups induced to lamb with 20 mg of EB (see Fig. 10) and a fourth group in which ewes were totally separated from their lambs. Additional details of the procedure are reported in Poindron (1980) and Poindron et al. (1980a). Along with the study of maintenance of maternal behavior, in some cases, it was possible to rapidly test the existence of selective behavior, using alien lambs, in ewes a f e r they had clearly accepted their own latnbs during the previous tesr. In this way, additional information was obtained in postparturient ewes. Only acceptance or rejection at the udder and aggressive behavior were noted. The age of the alien lambs presented to the ewes ranged from newborn, in a few cases, up to 12- to 24-hr-old lambs in most cases. Therefore, due to this variation, the results are only an indication of the acceptance of alien lambs rather than conclusive results. The effects of the various types of mother-young contact on the maintenance of maternal behavior are presented in Fig. 1 I . Rendering ewes anosmic did not significantly change the proportion of ewes accepting a lamb following total separation (Groups 61 and 6A) or deprivation of olfactory cues only (Groups 51 and 5A). As shown in Fig. 11, these two groups did not differ from their corresponding groups in which ewes were kept intact (3/8 vs 1/23 in the case of total separation and 2/7 vs 2/14 in the case where lambs were in an airtight box). Thus, the rejection of lambs by their dams following mother-offspring separation is probably not directly related to the existence of a discriminative behavior. The most clear-cut fact emerging from the comparison of the various types of partial mother-young separation in dexamethasone-treated ewes is that sight and hearing are not enough for a ewe to remain maternal after parturition, whereas when they receive olfactory cues in addition, they stay maternal 100% of the time, Ewes whose lambs were kept either 1 m away (Group 41) or in an airtight box (Group 51) did not differ significantly from ewes totally separated from their lambs (Group 61). On the other hand, the proportion of acceptances was higher in Group 4 than in Group 5 (7/14 vs 2/14, p = 0.05). This could reflect a better acoustical and visual perception when lambs were kept 1 m away from ewes. It is also possible that olfactory perception occurred in some ewes kept 1 m away from their young. This would explain why performances in this group, in which olfactory perception was questionable, were situated midway between those of ewes which could no doubt smell their lambs (Groups 2 and 3) and those of ewes that could not smell their young (Groups 5 and 6). When ewes were induced to lamb with estradiol benzoate, the proportion of acceptance was higher in all groups than in their corresponding groups treated with dexamethasone, except for ewes kept next to their lambs (Groups 21 and

96

PASCAL POINDRON A N D PIERRE LE NEINDRE

FIG.1I . Effect of decreasing degrees of mother-young contact (Groups 1 through 6) from parturition on the maintenance of maternal behavior, in relation to the type of induction at lambing. 0 I, Intact ewes, receiving 15 mg dexamethasone; 0 A, anosmic ewes, receiving 15 mg dexamethasone; E, intact ewes, receiving 20 rng estradiol benzoate. Groups, refer to Fig. 10. Statistical comparisons within the same type of lambing induction: 0 vs 0 , p < 0.05, one-tailed; 0 vs 0 , p C 0.05, one-tailed; (1) group 41 vs 51, p = 0.051, one-tailed, (2) group 2E vs 6E, p = 0.051, one-tailed. Statistical comparisons between corresponding groups treated with either dexamethasone or EB: (3) group 41 vs 4E, p = 0.03, one-tailed; (4) group 51 vs 5E, p = 0.051, one-tailed. 2E) in which all ewes accepted their lambs independently of the type of hormone treatment. However, it must be noted that the increase was maximal for ewes kept 1 m away from the lambs. All ewes but one (13/14) remained maternal, and ewes of this group differed significantly from ewes without young, whereas this was not the case in corresponding groups treated with dexamethasone. This suggests that the treatment with estrogen enhanced the ability of ewes to utilize some cues from the lambs. If this effect concerned sight and/or hearing, it should also have been observed in ewes whose lambs were kept in an airtight pen. As this was not the case, we have to hypothesize that estrogen improves the dams’ olfactory perception. However, more experiments are needed to verify whether this effect of estrogen on olfactory perception is actual and the first results presented above should be regarded with caution until further studies are undertaken.

MATERNAL BEHAVIOR IN THE EWE

97

2 . The Establishment of a Discriminating Behavior

Investigations concerning the existence of selective behavior in ewes remaining maternal when partially separated from lambs are summarized in Fig. 12. It is clear from these results that ewes which were very close to their lambs (Groups 2 and 3) and were able to smell them established discriminating behavior. In comparison, ewes of other groups remained largely nonselective, regardless of the type of situation in which they were placed before the time of test. Therefore, we have situations in which ewes remained maternal without necessarily being selective. This was most obvious for ewes kept 1 m away form their lambs and treated with estradiol benzoate (Group 4E).The fact that only ewes that were very close to their lambs were able to establish discriminating behavior is consistent with the findings of Alexander and Shillito (1977a) who reported that ewes were able to recognize their lambs by smell only when placed less than 0.25 m from them, which suggests that the olfactory components responsible for individual recognition are very slightly volatile.

FIG. 12. Acceptance of an alien lamb by postparturient ewes following various degrees of mother-young contact between parturition and test 12 hr later. Results are given only for ewes that spontaneously accepted their own young during a previous test. I, h x amethasone (15 mg), intact ewes; E, estradiol benzoate (20 mg), intact ewes; groups, refer to Fig. 10; mean, mean duration of contact for the group (in minutes) between mother and own lamb during the test before exchanging own lamb for an alien lamb; minimum and maximum, extreme values of mother-young contact for the group before the exchange. Alien lambs were 12 to 24 hr old in most cases.

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PASCAL POINDRON AND PIERRE LE NEINDRE

C . DISCUSSION Considering the influence of the young in the manifestation of postpartum maternal behavior is indeed most fruitful for a better understanding of the mechanisms regulating maternal responsiveness, especially with regard to the sensitive period. Within 12 hr of birth, the lamb loses some features of its attractiveness for the parturient mother that were important factors influencing its acceptance at delivery. On the other hand, results of Section I1 indicate that maternal responsiveness also fades rapidly after parturition. It is therefore essential when studying the formation of mother-young relationships to consider two factors, one inherent to the mother, maternal responsiveness, the other inherent to the lamb, attractiveness of the neonate. At parturition, both maternal responsiveness and lamb attractiveness are maximal, therefore ensuring the satisfactory formation of the bond. When the mother-offspring contact is delayed, the associated decrease of both factors rapidly makes it impossible for the dam to establish a bond with her lamb spontaneously. The exact factors responsible for the attractiveness of the newlyborn lamb are not known. One obvious difference between a neonate and what we called an “aged” lamb (between 12 and 24 hr old) lies in the presence of birth fluids on the newborn’s coat. The strong interest of parturient ewes for these fluids is well known (Collias, 1956; McBride er al., 1967) and they are therefore certainly a factor facilitating mother-young contact. The behavior of the lamb can also be involved. Newborn lambs are much less active than 12-hr-old lambs and thus it is possible that the degree of motor activity is a further element influencing acceptance by the mother. Observations of parturient primiparous ewes tend to support this hypothesis. Some primiparous dams show aggressive behavior toward their own newborn. Ewes tend to butt their young away mainly when the lambs try to stand up or to suck, but rarely when they are lying down or standing still, suggesting that the relative immobility of the newborn favors its acceptance (Hulet et al., 1975; Raksanyi, 1979). The study of ewes deprived of some cues from their lambs for 12 hr strongly suggests that maternal olfaction is involved in the maintenance of maternal behavior since suppressing the perception of olfactory cues prevented the development of maternal behavior in intact ewes. It is well established that maternal discriminating behavior relies on olfaction since suppressing the sense of smell during pregnancy results in the absence of selective behavior at suckling (Bouissou, 1968; Baldwin and Shillito, 1974; Morgan et al., 1975; Poindron, 1976a,b); in addition, in the experiments reported in Section II,B, only ewes kept close to their lamb and able to smell them established a selective behavior, suggesting that dams need to be very close to their young in order to perceive their specific odor. Despite this unquestionable role of olfaction in the establish-

MATERNAL BEHAVIOR IN THE EWE

99

ment of selective behavior, the cues responsible for discrimination do not appear to be vital for the development of postpartum maternal behavior. All results of Section II,B indicate that ewes can remain maternal without the necessity of establishing selective behavior. Therefore, it would appear that some other olfactory characteristics of the neonate are important for the maintenance of maternal behavior in the ewe. However, more investigations are needed to determine whether or not this hypothesis is valid, especially since the consistency of these results remains to be confirmed. Furthermore, it is not known at this stage if olfactory cues only are sufficient for a ewe to maintain maternal behavior or whether sight and/or hearing are also needed. There is another major reason for qualifying this hypothesis. Our results suggesting the role of olfaction in the development of maternal behavior per se are apparently in complete contradiction with the well-established fact that ewes made anosmic before parturition either by olfactory bulb removal (Bouissou, 1968; Baldwin and Shillito, 1974; Morgan et ul., 1975; Poindron, 1976a) or by the destruction of the nasal mucosa (Poindron, 1976b) also develop maternal behavior although olfactory cues are not available to such ewes. A possible explanation for these discrepancies would be that anosmic ewes are able to compensate for the loss of olfactory information by relying on other cues, whereas ewes whose olfactory system is intact are unable to do so as efficiently. As we shall see in Section IV, such a hypothesis should not be overlooked. Also the possible involvement of the vomeronasal system in the development of maternal interest or discriminative behavior has so far never been investigated in sheep.

Iv.

MOTHER-YOUNG RELATIONSHIR BEYOND THE POSTPARTUM PERIOD

In natural conditions a lasting mother-young relationship is established very rapidly and temporary separation of the ewe from her lamb becomes of no consequence for the further development of maternal behavior. Therefore, the characteristics of mother-young relationships become very different from those existing at the time of parturition. Whereas parturient ewes lick their lambs very intensely, this behavior disappears within a few days after delivery. Motheryoung relationships in the immediate postpartum period are mainly characterized by a high frequency of suckling, together with a tendency for dam and offspring to stay close to each other. As lambs grow older, distances between dams and their young tend to increase as do the intervals between sucklings. Two of the elements that characterize maternal behavior beyond the postpartum period have been studied in particular. One aspect relates to suckling behavior and the second concerns recognition of the lamb by its dam.

100 A.

I.

PASCAL POINDRON A N D PIERRE LE NEINDRE

SUCKLING BEHAVIOR Frequency of Suckling

The pattern of feedings in young lambs has been described often. Although frequent in the first week (one suckling or more per hour), it decreases to one or two nursing periods per 6 hr by the twelfth week postpartum (Munro, 1956; Ricordeau et a l . , 1960; Ewbank, 1964, 1967; Fletcher, 1971). At first, the lamb sucks as long as it wants but progressively the ewe ends suckling more and more frequently by moving off (Munro, 1956; Ewbank, 1964).

2. Organization of Mother-Young Relationships at the Time of Suckling At the time of suckling the behavior of the ewe and her lamb(s) is organized into well-defined patterns (Poindron, 1974a). The lamb passes near the front of its dam before reaching the udder (Fig. 13). Usually, the ewe smells her young at this time and again during suckling itself, the lamb being in a parallel-inverse position. This pattern is the most frequently observed when a lamb sucks its mother (Fig. 14). The selective behavior of the ewe prevents suckling by other lambs according to this pattern, since sniffing then leads to the rejection of the alien. Nevertheless, lambs, especially twins, still get access to the udder of alien ewes by adopting a behavior which excludes the possibility that the ewe will smell the lamb. Alien lambs suck from between the back legs and when the ewe’s own lamb is suckling (Figs. 13 and 14). In high-density conditions, lambs show this behavior within 2 to 3 weeks after birth. 3 . Effect of Anosmia on Suckling Behavior The importance of maternal olfaction in the suckling behavior is further illustrated by the study of ewes made anosmic by bulb removal before parturition and which are thus nonselective (Poindron, 1976a). In this case ewes accept any

FIG.13. Some aspects of mother-young relationships at the time of suckling in sheep (Prealpes-du-Sud breed). P, Passage near the front of ewe; SP,, suckling in parallelinverse position; SP,, suckling at right angles; SP,, suckling in rear position.

i

50.

c

a

5

0 e

25-

L

0-.

0

m

2k 25-

L

N

I

423

64

0

0

120

120

210b

FIG. 14. Proportion of various suckling patterns observed in intact Ile-de-France ewes suckling either their own single lambs (top) or twin alien lambs (bottom). Adapted from Poindron (1976a). n , Number observed for each pattern; N , total number observed (five females, 75 hr of observation). 1 to 6, Various patterns observed: 1, pattern including passage near the front of ewe, sniffing of lamb by ewe, and suckling in parallel-inverse position; 2, as in I , but no sniffing; 3, pattern including sniffing of lamb by ewe and suckling in parallel-inverse position; 4, as in 3, but no sniffing; 5 , pattern including suckling in perpendicular position, with or without sniffing of lamb by ewe; 6, pattern including suckling between the rear legs of ewe without sniffing of lamb by ewe. (a) A11 sucklings of alien lambs were performed while the own ewe's lamb was itself suckling; (b) of which 170 sucklings were performed while the own ewe's lamb was itself suckling.

1 E

1

2

3

15

4 N

9

L

5

6

36

lo

27 N

= 83

FIG. 15. Proportion of various suckling patterns observed in anosmic Ile-de-France ewes suckling either their own single lamb (top) or an alien single lamb (bottom). Adapted from Poindron (1976a). Four females, 60 hr of observation. For legend, see Fig. 14.

TABLE I POSSIBLE ROLEOF MATERNAL OLFACTION IN THE FREQUENCY OF APPEARANCE OF THE DIFFERENT LAMBACTIONS DURING SUCKLING',^

Group A. Lamb with its own intact mother

Action and its consequence

C. Lamb with its own

Adaptative character of this behavior

Effect on frequency of appearance of lamb’s behavior Increases frequency of appearance Decreases frequency of appearance Decreases frequency of appearance Increases frequency of appearance Lower frequency than in (A) Higher frequency than in (A) Higher frequency than in (B) Lower frequency than in (B)

P and SP,

Positive

SP, and SP,

Negative

P and SP,

Negative

SP and SP ,+no Sn

Olfactory perception+ rejection

SP, and SP,

Positive

P and SP,+Sn

No role

P and SP,

Zero

SP , and SP,

Zero

P and SP,

Zero

SP, and SP,

Zero

P and SP,+Sn

,

aMMmic mother SP, and SP,-mo Sn

D. Lamb with an alien anosmic mother

Nature of lamb’s behavior

Olfactory perception-, success

P and SP,+Sn SP, and SP,-mo Sn

B. Lamb with an alien intact mother

Role of olfaction

P and SP,+Sn SP, and SP,+no Sn

No role

~~

Adapted from Poindron ( 1976a). bP, passage to the front of the ewe; SP,, parallel-inverse position of suckling; SP,,position of suckling at right angles; SPp, rear position of suckling; Sn, sniffing of the lamb by the ewe.

MATERNAL BEHAVIOR IN THE EWE

103

lambs at the udder and the Iambs pass less often near the front of their dams but instead go directly to the udder in a parallel-inverse position (Fig. 15), and alien lambs also suck in this same position. This role of maternal olfaction in the organization of the suckling pattern is summarized in Table I. It was also evident from this study on anosmic ewes that suckling behavior itself was affected to a degree by olfactory bulb removal. Whereas 64% of the suckling attempts were successful in the case of intact ewes (736 suckling attempts for five females or 75 hr of observation) only 19% were so in the case of anosmic ewes (190 attempts for four females or 60 hr of observation). Whether this was a specific result of the operation is not known. It is possible, however, that olfaction is involved in the regulation of maternal behavior per se. The importance of smell in the mother-young bond has so far been mainly assessed by suppressing maternal olfaction before parturition. But in fact, to appreciate fully the role smell can play in the regulation of maternal behavior, the effect of anosmia carried out after several days of mother-young contact must be studied. To this end we investigated the effect of anosmia performed 2 weeks after lambing by irrigation of the nostrils with a solution of zinc sulfate (Poindron, 1974b). Twelve to fourteen days after lambing 18 aged Merino ewes were fasted for 24 hr and then tested for smell discrimination using the association of food with a repulsive odor (Poindron, 1974b). Dams were also tested for selective behavior at suckling following a 3-hr mother-young separation. For the next days, ewes were rendered anosmic by a single irrigation of the nostrils with a solution of 1.5%ZnSO,, plus 2%Xylocaine performed under general anesthesia. Olfactory discrimination was then tested 3 hr after irrigation and thereafter before each test of maternal behavior. Recognition at a distance was also tested 4 hr after zinc sulfate irrigation using a situation of choice between two lambs placed at a distance of 10 m (cf. Poindron and Carrick, 1976). To test maternal behavior, the I8 ewes were divided into two equal groups (nine females) (A and B) at the start of the experiment. Three hours before each test all lambs were separated from their dams. At the time of testing, Group A lambs were put with the ewes in Group B and vice versa, to test acceptance of alien lambs at suckling. Ewes and lambs were observed for 10 min and then Iambs were returned to the group they belonged to and ewes were observed for another 10 min to test acceptance at suckling of their own lambs. The criteria of acceptance at suckling are listed in Tables I1 and III. Despite the fact that all ewes were unable to show olfactory discrimination 3 hr after treatment, they were able to discriminate between their own young and an alien lamb at a distance (I4 correct choices, 2 wrong choices, and 2 not clear; significantly different from a random choice, p < 0.05). Therefore, altering the sense of smell did not appear to affect recognition at a distance and affected even less their interest in lambs per se. In contrast maternal behavior at suckling was clearly affected, disturbances ranging from rejection of any lamb (including own

104

PASCAL POINDRON A N D PIERRE LE NEINDRE

TABLE I1 BEHAVIOR AT SUCKLING OF EWESMADEANOSMIC 2 WEEKSAFTER LAMBING A N D WHICHDID NOT RECOVER SMELL DURlNG THE STUDY" Own lamb Identification of female

Alien lamb

+

*

-

+

*

-

14

9

0

0

8

0

1

25* 26 28

3 7 8 6 2

3(1) 2(2) 1 2 5

O 0 1 2

O

O 1

8

1 2

Comments

~

17

19* 15 16

I

5 8

3 8 18 33

3 I 4 5 6

4 4 2

21 30

0 0

1 1

1

8

0

3

1

5

0

0 0

1 0

3 1

1 0 1

0 0 0

3 1 0

8 8

0 0

1 0

Nonselective (%)*suckling behavior affected to a

4

'I

'9

9

Maternal and selective Suckling behavior disturbed to a degree but clear difference between own young and alien lamb Lost their suckling behavior

~~

"All ewes displayed olfactory discrimination and discriminative behavior at suckling the day before zinc sulfate irrigation. + , Acceptance of a lamb for a period of 30 sec or more; k , suckling of of lamb for a period shorter than 30 sec mixed with rejection by the ewe (ewe walking off andor showing aggressive behavior); numbers in parentheses indicate number of tests where lambs did not attempt to suck; -, rejection of the lamb.

lamb; two females) to absence of selective behavior at suckling (six females) or maintenance of selective behavior but disturbance in the ability to suckle (five females, see Table 11). Only three ewes showed signs of olfactory recovery during the study (up to 11 days after treatment), although this was associated with the restoration of normal behavior at suckling in only one case (cf. Table 111). It appears therefore that acceptance at suckling per se, as well as discriminative behavior at suckling, can be affected by the loss of olfactory perception after several days of mother-young contact. Using a different method of investigation Alexander and Stevens (reported by Shillito and Alexander, 1979) also found disturbances in maternal acceptance at suckling following the suppression of olfactory cues from the lambs. In this latter study ewes were kept intact. Lambs were either washed with a strong detergent (treated group) or only spread with the detergent (control group). Whereas ewes accepted their lambs readily when only spread with the detergent, half of the dams whose young had been washed rejected them consistently at suckling.

105

MATERNAL BEHAVIOR I N THE EWE

TABLE 111 BEHAVIOR AT SUCKLING OF EWESMADEANOSMIC 2 WEEKSAFTER LAMBING A N D WHICH RECOVERED OLFACTORY DISCRIMINATION DURING THE STUDY" Own lamb Without olfactory discrimination

Alien lamb

With olfactory discrirnination

Without olfactory discrimination

With olfactory discrimination

Identification of females

+

k

-

+

2

- +

f

20 29 22

5 4 I

1 0 0

0 0 0

3 5 8

0 0 0

0 0 0

0 1 3 3 ( 1 ) 1 3 0 0 0

5 0 I

-

+

f

-

0 0 ( I ) I 0 8

Comments

Recovery of selective behavior associated with recovery of smell

"All ewes displayed olfactory discrimination and discriminative behavior at suckling the day before zinc sulfate irrigation. + , Acceptance of a lamb for a period of 30 sec or more; L , suckling of a lamb for a period shorter than 30 sec mixed with rejection by the ewe (ewe walking off andor showing aggressive behavior); numbers in parentheses indicate number of tests where lambs did not attempt to suck; -, rejection of the lamb.

Similarly, in goats, Klopfer and Gamble (1966) found that intranasal administration of cocaine in the dam after parturition, which presumably modified olfactory perception, resulted in the loss of maternal behavior. By contrast, anosmia performed before parturition did not affect maternal acceptance. It would therefore appear that, as in sheep, effects of anosmia vary according to the time it is effected relative to parturition. These results on goats suggest that olfaction may be important also in this species for the regulation of maternal behavior after parturition. Effect of Endocrine Manipulations in the Dam on Maternal Behavior Whereas sensory information seems to play a very important role in the organization of mother-young relationships after lambing and in the ability of the ewe to care for a lamb, the endocrine state of the dam appears to be of little importance. Attempts to suppress maternal acceptance by ovariectomy and/or suppressing the release of prolactin by CB 154 treatment have so far been unsuccessful (Poindron, 1980). Experiments were carried out between 10 and 20 days postpartum and the aim was to study the possibility of affecting (within 12 hr) the acceptance of the young at short-term. Whereas smell suppression was immediately followed by disturbances in maternal behavior, no noticeable modifications were observed in ovariectomized and/or CB-treated ewes. Also in

4.

106

PASCAL POINDRON A N D PIERRE LE NEINDRE

a study of lactation in ewes, Kann et al. (1978) treated ewes with CB 154 for 5 weeks postpartum. Although milk production was effectively reduced, ewes kept suckling during the whole study (G. Kann, personal communication). This does not exclude the possibility that other physiological factors are involved in the acceptance of the young. For example, Arnold er al. (1979) have reported that weaning occurred later in ewes with high milk production compared to ewes with a low milk yield. The factors involved in this phenomenon remain unknown. B.

RECOGNITION OF THE YOUNG

Both ewes and lambs are able to recognize each other as shown by studies of Lindsay and Fletcher (1968), Shillito and Alexander (1975), and Alexander ( 1977). Whereas recognition of the dam by her offspring does not appear to occur very rapidly (Arnold et al., 1975; Shillito and Alexander, 1975), ewes are able to discriminate between lambs within an hour of parturition (cf. Section 111). When investigating the role played by various senses recognition at close quarters and recognition at a distance must be distinguished as Lindsay and Fletcher (1968) emphasized. 1 . Recognition at Close Quarters In most studies of maternal recognition at close quarters the discriminating behavior of the ewe at suckling has been used to assess recognition. In such conditions maternal olfaction has been found to be essential for recognition of the young, since suppressing the sense of smell before parturition leads to acceptance of any lamb at suckling (Bouissou, 1968; Baldwin and Shillito, 1974; Morgan et al., 1975; Poindron, 1976a,b). Sight can also play some role in the acceptance of the lamb at suckling. Some anosmic ewes reject alien lambs if they are very different from their own young (Len,fully black versus fully white, Poindron, 1976b) and intact ewes presented with their own blackened lambs tend to prevent them from suckling (Alexander and Shillito, 1977b). However, restricting the study of maternal recognition to discriminating behavior of the dam at suckling would lead to the incorrect conclusion that proximate recognition depends on olfactory cues only. When testing intact ewes placed in a situation of choice with lambs close to them (< 0.5 m) dams fail to recognize their young on the basis of olfactory cues if lambs are more than 0.25 m from them (Alexander and Shillito, 1977a). Furthermore olfactory cues are ineffective unless other cues are also available. Visual clues, especially from the face of the lamb (Alexander and Shillito, 1977b), appear of major importance even at close quarters. These results, which are at variation with those obtained for ewes made anosmic before parturition, emphasize the fact that one must be careful when interpreting results obtained with anosmic animals to apply them to normal situations with intact ewes, as already mentioned by Alexander and Shillito (1977a).

MATERNAL BEHAVIOR IN THE EWE

107

2 . Recognition at a Distance It is clear from the study of Alexander and Shillito (1977a) that olfaction is not likely to be involved in recognition of the lamb at a distance of several meters. This is further confirmed by the existence of distance recognition in ewes made anosmic 2 weeks after lambing (cf. Section IV,A). Both visual and acoustic cues from the lambs are involved in recognition at a distance. As mentioned, visual recognition depends heavily on the cues from the lamb’s head, since blackening the face of the young results in disturbances in maternal recognition as great as when the whole body of the lamb is blackened (Alexander and Shillito, 1977b). In the absence of visual cues, dams are still able to discriminate by relying on acoustical cues (Poindron and Carrick, 1976). When placed in a situation of choice at a distance between their own lamb and an alien lamb of the same age, most ewes chose their own lamb from a distance of at least 10 m (19 out 23), and only one ewe made a wrong choice. To investigate the possible role of auditory cues in maternal recognition, a second experiment was effected, in which ewes were given the choice between the recorded bleat of their own and an alien lamb, played on two loudspeakers set up 15 m apart and 13 m from the initial position of the ewe (cf. Poindron and Carrick, 1976). Under such conditions most ewes chose the side where the recording of their own lamb was played (14/18; different from a random choice; p < 0.05). The proportion of correct choices of ewes in the presence of recorded bleats only did not differ significantly from that of ewes tested with lambs (14/18 vs 22/23; p = 0.10, one-tailed). However, in all cases, discrimination is maximal when all senses are available (Morgan et al., 1975; Shillito and Alexander, 1975; Poindron and Canick, 1976; Alexander, 1977). Sensory clues can also have nonspecific effects on maternal behavior by increasing maternal interest independently of recognition. For example, Alexander and Shillito ( 1977a) reported that anesthetized lambs were less attractive than awake ones, suggesting that movement facilitated recognition and/or entrained maternal interest. Similar effects have been reported concerning acoustical cues. Hersher et a f . (1963a) mentioned that ewes separated from their lambs answer any lamb’s bleat. Alexander (1977) also found that the effects of blackening lambs on the ewes’ behavior were less marked when the voices of the young were not muted than when they were muted, and this was true even in the case of alien lambs, indicating that the different effects observed were due to a difference in maternal interest independent of recognition. C.

DISCUSSION

The most outstanding feature emerging from studies on maternal behavior beyond the period of parturition is that sensory information provided by the lamb plays a major role in the regulation of maternal behavior at this stage. Hormonal manipulations, at least those concerning ovarian steroids and prolactin, appear to

108

PASCAL POINDRON AND PIERRE LE NEINDRE

affect short-term maternal behavior very little. In contrast, findings concerning the role of sensory information converge to stress that it is essential in at least three respects. First, mother-young recognition ensures the maintenance of mother-young contact, which is vital for the young in field conditions since the ewe is both the primary source of food and a source of protection against predators (Arnold and Dudzinski, 1978). Second, maternal olfaction plays an important role in the organization of the behavior of the lamb at suckling (Poindron, 1974a, 1976a). The perception of the olfactory cues from the lamb facilitate its acceptance by the mother. This also indicates that maternal olfaction is involved in the manifestation of the suckling behavior per se. This leads us to the third important element to consider concerning the role of sensory information in the regulation of maternal behavior: the sensory information provided by the lamb to its dam appears necessary to maintain her ability to suckle, and this applies especially to olfactory cues. Such a conclusion seems correct whether the role of olfactory stimuli is investigated by suppressing the sense of smell in the dam or by suppressing the cues themselves (cf. Section IV,A). Variations between animals observed in both types of experiments can be due to technical impediments (such as partial anosmia or incomplete suppression of cues; for extensive criticism concerning olfactory impairment, see Murphy, 1976) or to individual differences, as some mothers may rely more than others on olfactory cues. Regardless of these variations, olfactory stimuli from the lambs remain important for their acceptance at suckling, in contrast to the situation in which ewes are made anosmic before parturition, indicating that the regulation of maternal behavior is different in intact and in anosmic mothers, as suggested in Section II1,C.

V.

MATERNAL BEHAVIOR I N INEXPERIENCED EWES

In the preceding sections, we have emphasized the roles of hormones and of neurosensory information in the regulation of maternal behavior in sheep, with results limited to multiparous mothers. However, the behavior of an animal at a given time depends also, in part, on its previous experience concerning this behavior. In order to assess the influence of maternal experience on the manifestation of maternal behavior we compared the behavior of primiparous and multiparous dams at the time of parturition. To complete this first analysis, a study concerning the regulation of the onset of maternal behavior in relation to panty has also been undertaken. A.

OF MATERNAL BEHAVIOR AT PARTURITION IN COMPARISON PRIMIPAROUS A N D MULTIPAROUS EWES

In sheep, studies of postnatal mortality at pasture all mention poor maternal behavior as a possible cause of the lamb’s death, although its relative importance

109

MATERNAL BEHAVIOR IN THE EWE

varies according to authors (Alexander, 1960; Alexander and Peterson, 1961; Watson et al., 1968; Shelley, 1970; Arnold and Morgan, 1975; Arnold and Dudzinski, 1978). Disturbances range from delayed interest in the newborn to permanent desertion of the young. Although results obtained in the field are difficult to interpret, due to the number of factors which all come into play at once (e.g., nutritional, climatic, sanitary, etc.), it would appear from these studies, especially those of Alexander (1960) and Alexander and Peterson (1961), that poor maternal behavior concerns mainly primiparous ewes. In a study done on sheep kept inside on zero grazing management and in which unwanted factors such as undernutrition or adverse climatic conditions were excluded, we have also found variations in maternal behavior according to the parity of the animals. Parturition was induced with 15 mg of dexamethasone.

-- -

N = 70

N = 40

10(

N

e

87

u W l

5

7!

p

px 0

.-b B

3

2!

.-P

L

$

25

PE

D ul

c

;.t

w

s

W

50

75

-- -N

100

1

6

2

76

N=62

3

4

5

6

B

-; N = 69 7

FIG.16. Comparison of postpartum maternal behavior in primiparous and multiparous ewes. 1, Occurrence of licking behavior within 5 rnin after delivery; 2, occurrence of licking behavior within 30 rnin after delivery; 3, occurrence of aggressive behavior toward own lamb in the 30 min following delivery; 4, immediate acceptance of the lamb at the udder; 5, acceptance of the lamb at the udder within 30 min after delivery, but after initial rejection; 6, rejection of the lamb at the udder for at least 30 rnin following delivery; 7, absence of maternal behavior for at least 3 hr postpartum. Differences between multiparous and primiparous ewes are significant (p < 0.05) for all behavioral elements considered in the figure.

110

PASCAL POINDRON AND PIERRE LE NEINDRE

Ewes, mainly from Ile-de-France and Prealpes-du-Sud breeds, were observed for 30 min from parturition. For this purpose they were left among the rest of the flock, where they had lambed. During this period, licking behavior, acceptance at the udder, and the existence of aggressive behavior were noted. Three hours after delivery, lamb acceptance was checked again. Further details of the procedure are reported in Raksanyi (1979). The comparison between primiparous ( n = 62) and multiparous ewes ( n = 70) is presented in Fig. 16. At delivery only 8% of multiparous dams showed temporary disturbances in maternal behavior and these difficulties disappeared within the first 30 min following delivery. In contrast, a high proportion of primiparous mothers showed difficulties of maternal behavior. The most common type of abnormal behavior consisted of the ewe’s failure to stand for the lamb during its attempts to reach the udder (61% of dams, cf. Figs. 16 and 17). However, more than half of these ewes had settled down within 0.5 hr after

FIG. 17. Evolution of maternal behavior in primiparous ewes at parturition. (a) Romanov ewe walking off when neonate attempts to suck (second lamb lying down); (b) Ile-de-France ewe butting her newborn lamb; (c and d) the same ewes less than 30 min later.

MATERNAL BEHAVIOR I N THE EWE

111

parturition. Also, the onset of licking was more often delayed in primiparous dams than in multiparous ones. Some primiparous ewes had not started to lick the neonate 5 or even 30 min after parturition (35% and 21 % respectively, Fig. 16). Aggressive behavior was observed in 17% of primiparous ewes whereas only 1.4% of multiparous ewes butted their lamb ( p < 0,OS). Ewes tended to butt their young mainly when lambs were trying to stand up or when approaching the ewes and not when lambs were either lying or standing still (Fig. 17). Similar observations have been reported by Lynch and Alexander (1973), reported in Hulet et al. (1975). It is clear therefore that even in the absence of interference by adverse environmental factors, differences in maternal behavior exist between primiparous and multiparous ewes. Differences related to parity which are reported here and in other studies (Alexander, 1960; Alexander and Peterson, 1961; Shelley, 1970) concern maternal behavior at parturition. It is thus possible that the regulation of the onset of maternal behavior differs in primiparous and in multiparous mothers. To investigate this possibility an experimental analysis was camed out on nulliparous ewes. IN THE REGULATION OF MATERNAL B. THEROLEOF HORMONES BEHAVIOR IN PRIMIPAROUS EWES

Since the onset of maternal behavior at parturition appears, at least partly, under hormonal control in multiparous ewes (cf. Section 11), and the disturbances observed in primiparous ewes concerned maternal behavior at parturition, we tried to determine whether hormonal regulation varied according to parity. To this end we carried out two studies on inexperienced ewes parallel to those which were presented in Section I1 ,A concerning experienced females.

I. Preparturn Onset of Maternal Behavior The onset of maternal behavior several days before parturition is likely to be due to hormonal changes in the ewe at that time (cf. Section 11). When testing multiparous pregnant ewes 10 days before delivery 35% are already maternal at this time (cf. Fig. 3). However when testing primigravid ewes at the same stage of pregnancy, no females were found to be maternal at that time (cf. Fig. 18). If the assumption that prepartum maternal behavior is under hormonal control is correct, it would appear that in primiparous ewes hormones are less efficient for eliciting maternal behavior than in multiparous mothers. This hypothesis is further supported by results concerning the hormonal induction of maternal behavior in nulliparous nonpregnant ewes. 2. Hormonal Induction of Maternal Behavior in Nulliparous Ewes

Injections of progesterone and estradiol (1.25 and 0.5 mg/kg body weighdday for 7 days) led to the onset of maternal behavior in 60% of the multiparous

112

PASCAL POINDRON AND PIERRE LE NEINDRE

1007

c

-i 2

-P

P 'g

O-

k

v

I

n a14

I I I I

25-

1 c

s 5075-

I

-

E In a 0 a

g

I n.7

I

5 A

n=23

I I II I I

n = 20

1 25-

I I

L

50-

v)

I

75-

'g

I I I

n=4

n=U v)

W

E

w

I I I I

v)

!I 2

I 2 a n=69 I z I-I at at controls h a t e d *

:

FIG. 18. Comparison of the influence of hormones on the onset of maternal behavior in nulliparous and in multiparous ewes. 0.5 mg estradiol 1.25 mg progesteronekg body weighdday for 7 days. Maternal behavior was studied 21 days after the beginning of the treatment. All differences between nulliparous and multiparous ewes are significant ( p < 0.05).

*,

+

females (14/23). In contrast, only one out of 13 nulliparous ewes responded to the treatment (p < 0.025, cf. Fig. 18). In fact, nulliparous ewes did not differ from untreated controls ( O h 1). C. DISCUSSION

The study of primiparous ewes suggests strongly that maternal experience plays an important role in the manifestation of adequate maternal behavior at parturition. The first experimental investigations that we reported here (cf. Section V,B) indicate, in addition, that the regulation of postpartum maternal behavior is somewhat different in primiparous and in multiparous mothers. Hormones do not appear sufficient to elicit maternal responsiveness in inexperienced

MATERNAL BEHAVIOR IN THE EWE

113

females compared to experienced ones, although this does not necessarily mean that hormones are not normally involved at all. Most likely primiparous mothers need more cues to develop maternal behavior than multiparous mothers do. The nature of this information remains to be investigated. A more complex hormonal state than the one mimicked by hormone injections may be needed to elicit maternal interest in inexperienced females. It is also possible that the neural stimulation provided by parturition facilitates the onset of maternal behavior. Lastly the fact that a significant improvement is observed in the behavior of primiparous ewes within the first hours postpartum indicates that contact with the neonate may further facilitate the development of proper maternal behavior. In other words our results suggest that inexperienced mothers need all pre-and postpartum stimuli to develop appropriate behavior, whereas for multiparous ewes some of these stimuli-such as those associated with the birth process-are not an absolute requirement. Studying the sensitive period in primiparous ewes together with the establishment of enduring maternal behavior at that time would allow these points to be cleared up.

VI.

CONCLUSION AND FUTURE PROSPECTS OF RESEARCH

When considering all the recent studies on mother-young relationships in sheep, a framework for the development of maternal behavior from parturition to weaning may be proposed. Initially, temporary maternal interest in the neonate is elicited through hormonal facilitation. This facilitation is more efficient as the animal has some maternal experience. Maternal interest ensures contact with the newborn lamb, and here again maternal experience helps the establishment of mother-young contact. From then on the lamb starts to influence maternal behavior and sensory information provided by the young become increasingly important. The few hours postpartum during which the ewe can remain maternal in the absence of a young-in other words the sensitive period-probably make up the time when maternal behavior changes from a hormonal regulation to a neurosensory control. After this postpartum period, maternal acceptance of the young seems to become largely independent of the hormonal state of the mother. In the framework that we have proposed for the development of a maternal cycle in sheep, some elements appear valid for other species of ungulates as well. It is clear that a sensitive period exists in goats also (Klopfer ef al., 1964; Klopfer and Gamble, 1966; Klopfer and Klopfer, 1968), although the role of hormones in its regulation remains to be investigated in this species. A similar phenomenon has also been reported in postparturient cows (Le Neindre and Garel, 1976; Hudson and Mullord, 1977). In addition, it is likely that in cattle hormones are involved in the onset of maternal behavior, since treatments inducing lactation can also induce maternal behavior (P. Le Neindre, unpublished; W. J. Fulkerson,

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personal communication). In goats and cattle, as in sheep, the mother-young bond is generally exclusive and olfaction seems involved to some extent in the manifestation of a discriminative suckling behavior (Klopfer and Gamble, 1966; Le Neindre and Garel, 1979) and in the organization of mother-young relationships (Poindron and Le Neindre, 1975). Therefore, it is likely that, although variations between species certainly exist, the general picture proposed above is also valid at least in part for many ungulates. As a matter of fact, in the light of research carried out on laboratory animals (cf., for example, Rosenblatt et al., 1979), it is possible that the association of a period of temporary maternal responsiveness under hormonal control followed by a time when maternal behavior becomes more dependent on mother-young interactions is a common feature in many mammals. The general picture drawn for maternal behavior in the ewe is far from being complete and investigations are still needed in order to comprehend fully how maternal behavior is regulated in sheep. In the light of results referred to in this article, four main research approaches should be developed. That maternal experience plays a role in the development of maternal behavior is clear, but how this experience is acquired remains to be clarified. In addition, the regulation of maternal behavior in inexperienced mothers is far from being understood. Also, in relation to maternal behavior in naive females, the possible importance of the conditions of breeding in infancy and in the juvenile period remains completely unexplored. A second aspect of maternal behavior worthy of further investigation concerns the endocrine regulation of the onset of maternal behavior and its possible interaction with sensory functions. Results suggest strongly that hormones are an important determinant of maternal responsiveness at parturition. But to conclude that estrogen is “the hormone of maternal behavior” would be hazardous. Although arguments for such a hypothesis exist, more experiments are necessary to make known the exact role of estrogen in relation to the possible roles of other hormones such as progesterone, oxytocin, prolactin, corticosteroids, relaxin, etc. Also regardless of the exact mechanisms of action of hormones, it seems that there are some interrelations between the hormonal state of the ewe and the way sensory information is perceived and/or treated, olfaction being the sensory function most concerned in these interrelationships. Further research in this area may help to answer questions such as why is the parturient ewe attracted by a lamb and why is the parturient ewe more responsive to a neonate than to an older lamb. The existence of recognition of the lamb by its dam is a well-established fact. However, virtually nothing is known about the processes involved in the establishment of this recognition. All the evidence on the olfactory “fixation” of the dam to her young suggests that this represents some peculiar type of learning about which the mechanisms remain completely unexplored. Also, whether es-

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tablishment of recognition of the lamb via senses other than olfaction depends on similar processes is unknown. Furthermore the possibility of interactions between various senses in the establishment of recognition has never been considered. Investigations concerning these various aspects of mother-young relationship in sheep would certainly provide a better understanding of the mechanisms of recognition and possibly of learning processes in general. Last, although neurosensory information plays an important role in motheryoung relationships at later stages following parturition, there is a clear necessity for further experimental analysis of the regulation of maternal behavior up to weaning. The relative roles of neurosensory information and of the mother’s physiological status in this respect are especially difficult to assess as behavior of the young influences behavior of the mother and vice versa, and also because the lamb influences the physiological status of the ewe-through suckling, for example. On the other hand, studying the regulation of maternal behavior after parturition in terms of feedback effects between mother and lamb may prove more fruitful for understanding the process of weaning than studying each factor individually.

Acknowledgments Thanks are due to J . S. Rosenblatt, H. Siege], J. M. Vidal, J . Gautier, F. Przekop, and Marylee Rombaud, who have read the manuscript and helped in its improvement, to Colette Lavenet for the illustrations, and to Anne de la Dure for the typing. Original work referred to or presented in this article has been partly supported by a grant of the Australian Research Committee and partly by INRA funding. P. Poindron is Attache de Recherche CNRS and P. Le Neindre is Charge de Recherche INRA.

References Alexander, G. 1958. Behaviour of newly born lambs. Proc. Aust. Soc. Anim. Prod. 2 , 123-125. Alexander, G. 1960. Maternal behaviour in the Merino ewe. Proc. Ausf. Soc. Anim. Prod. 3, 105-1 14. Alexander, G. 1977. Role of auditory and visual cues in mutual recognition between ewes and lambs in Merino sheep. Appl. Anirn. Erhol. 3, 65-81. Alexander, G., and Peterson, J . E. 1961. Intensive observations during lambing in a flock of maiden Merino ewes. Ausr. Vet. J . 31, 371-381. Alexander, G., and Shillito. E. E. 1977a. The importance of odour, appearance and voice in maternal recognition of the young in Merino sheep (Ovis aries). Appl. h i m . Erhol. 3, 127-135. Alexander, G., and Shillito, E. E. 1977b. Importance of visual clues from various body regions in maternal recognition of the young in Merino sheep (Ovis aries). Appl. Anim. Efhol. 3, 137-143. Alexander, G., and Williams, D. 1964. Maternal facilitation of suckling drive in new born lambs. Science 146, 665-666. Alexander, G., and Williams, D. 1966. Teat-seeking activity in lambs during first hours of life. Anim. Behav. 14. 166-176.

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Arnold, 0 . W., and Dudzinski, M. L. 1978. Maternal behaviour. In “Ethology of Free Ranging Domestic Animals” (G. W. Arnold and M. L. Dudzinski, eds.), Chapter 5. Elsevier, Amsterdam. Arnold, G. W., and Morgan, P. D. 1975. Behaviour of the ewe and lamb at lambing and its relationship to lamb mortality. Appl. Anim. Erhol. 2, 25-46. Arnold, G. W.. Boundy, C. A. P., Morgan, P. D., and Bartle, G. 1975. The roles of sight and hearing in the lamb in the location and discrimination between ewes. Appl. Anim. Ethol. 1, 167- 176. Arnold, G.W., Wallace, S. R., and Maller, R. A. 1979. Some factors involved in natural weaning processes in sheep. Appl. Anim. Ethol. 5, 43-50. Baldwin, B. A., and Shillito, E. 1974. The effects of ablation of the olfactory bulbs on parturition and maternal behaviour in Soay sheep. Anim. Behaw. 22, 220-223. Basset, J . M., and Thorbum, G. D. 1969. Foetal plasma corticosteroids and the initiation of parturition in sheep. J . Endocrinol. 44, 285-286. Blauvelt, H.1955. Dynamics of the mother-new born relationships in goats. In “Group Processes” (B. Schaffner, ed.),pp. 221-258. Josiah Macy, Jr. Foundation, New York. Bosc, M. J. 1974. La parturition provoqude chez les Mammiferes domestiques. In “Avortement et parturition provoqude” (M. J . Bosc, R. Palmer, and C. Sureau, eds.), pp. 1-24. Masson, Paris. Bouissou, M. F. 1968. Effet de I’ablation des bulbes olfactifs sur la reconnaissance du jeune par sa mere chez les Ovins. Rev. Comp. Anim. 2, 77-83. Cairns, R. B.. and Johnson, D. L. 1965. The development of interspecies social preferences. Psychon. Sci. 2, 337-338. Chamley, W . A., Buckmaster, J . , Cereni, M. E., Cumming, I. A., Coding, J. R., Obst, J. M., Williams, A., and Winfield, C. 1973. Changes in the levels of progesterone, corticosteroids, estrone, oestradiol-l7B, luteinizing hormone and prolactin in the peripheral plasma of the ewe during late pregnancy and at parturition. Eiol. Reprod. 9, 30-35. Collias, N. E. 1956. The analysis of socialisation in sheep and goats. Ecology 37, 228-239. Davis, S. L., Reichert, L. E., and Niswender, G.D. 1971. Serum levels of prolactin in sheep as measured by radioimmunoassay. Biol. Reprod. 4, 145-153. Ewbank, R. 1964. Observations on the suckling habits of twin lambs. Anim. Behaw. 12, 34-37. Ewbank, R. 1967. Nursing and suckling behaviour amongst Clun Forest Ewes and lambs. Anim. Eehaw. 15, 251-258. Fletcher, I. C. 1971. Relationships between frequency of suckling, lamb growth and post-partum oestrous behaviour in ewes. Anim. Behaw. 19, 108-1 11. Fraser, A. F. 1968. “Reproductive Behaviour in Ungulates,” Academic Ress, New York. Fulkerson, W. J., and McDowell, G.H. 1974. Artificial induction of lactation in ewes. J . Endocrinol. 63, 167-194. Geist, V. 1971. Behavior of ewes and lambs. In “Mountain Sheep” (G. B. Schaller, ed.),Chapter 8, pp. 239-255. Univ. of Chicago Press, Chicago, IIlinois. Gubernick, D. J . , Corbeau-Jones, K . , and Klopfer, P. H. 1979. Maternal imprinting in goats? Anim. Behav. 27, 314-315. Guiton, P. 1958. The effect of isolation on the following response of brown Leghorn chicks. Proc. R . Phys. Soc. Edinburgh 27, 9-14. Guiton, P. 1959. Socialisation and imprinting in brown Leghorn chicks. Anim. Behav. 7, 26-34. Hafez, E. S. E., Cairns, R. B., H u h , C. V., and Scott, J. P. 1969. The behaviour of sheep and goats. In “The Behaviour of Domestic Animals” (E. S. E. Hafez, ed.), pp. 293-348. Baillibre, London. Head, H. H., Delouis. C., Terqui, M., Kann, G., and Djiane, J. 1975. Hormonal induction of lactation in sheep. J . Dairy Sci. 58, 140. Heinmth, 0. 1911. Beitriige zur Biologie, namentlich Ethologie und Psychologie der Anatiden. Verh. 5 Int. O m . Kong. 589-702.

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Rosenblatt. J. S., Siegel, H. I., and Mayer, A. D. 1979. Progress in the study of maternal behavior in the Rat: Hormonal, non hormonal, sensory and developmental aspects. Adv. Study Behav. 10, 225-3 I I . Scott, J. P. 1945. Social behavior, organization and leadership in a small flock of domestic sheep. Comp. Psychol. Monogr. 18, 1-29. Seif, S. M.. and Robinson, A. G . 1978. Localization and release of neurophysins. Annu. Rev. Physiol. 40, 345-376. Shelley, L. 1970. Interrelationships between the duration of parturition, post natal behaviour of ewes and lambs and the incidence of neonatal mortality. Proc. Aust. Soc. h i m . Prod. 8, 348-352. Shillito, E. E., and Alexander, G. 1975. Mutual recognition amongst ewes and lambs of four breeds of sheep (Ovis aries). Appl. h i m . Ethol. 1, 151-165. Shillito-Walser, E. E.,and Alexander, G . 1980. Mutual recognition betweenewesand lambs. Reprod. Nurr. Develop. 20(3B), 807-816. Smith, F. V., Van Toller, C., and Boyes, T. 1966. The “critical period” in the attachment of lambs and ewes. Anim. Behav. 14, 120-125. Sokal, R.. and Rohlf, F. J. 1969. Analysis of frequencies. In “Biometry--The Plinciples and Practice of Statistics in Biological Research” (R. Sokal and F. F. Rohlf, eds.). Chapter 16. Freeman, San Francisco, California. Stabenfeldt, G. H. 1974. In “Avortement et parturition provoques,” pp. 97-122. Masson, Paris. Terkel, J., and Rosenblatt, J. S. 1972. Humoral factors underlying maternal behavior at parturition: Cross-transfusion between freely moving rats. J. Comp. Psychol. 80, 365-371. Terqui, M. 1974. Les oesrrogenes au cours de la gestation et de la parturition chez la truie et la brebis. In “Avortement et parturition provoques,” pp, 71-79. Masson, Paris. Terqui. M. 1978. Contribution a I’etude des oestrogenes chez la brebis et la truie. These de Doctorat d’Etat e s Sciences Naturelles, Universiti de Paris VI. Thorburn, G. D.. Nicol, D. H.,Basset, J. M.,Shutt, D. A., and Cox, R. I. 1972. Parturition in the goat and sheep: Changes in corticosteroids, progesterone, oestrogens and prostaglandin F . J . Reprod. Fertil., Suppl. 16, 61-84. Wallace, L. R. 1949. Observation of lambing behaviour in ewes. Proc. N.Z. Soc. Anim. Prod. 9, 85-96.

Watson, R . H., Alexander, G., Cumming, 1. A., McDonald, J . W., McLaughlin, J. W., Rizzoli, D. J . , and Williams, D. 1968. Reduction of perinatal loss of lambs in winter in western Victoria by lambing in sheltered individual pens. Proc. Ausr. Soc. Anim. Prod. 7 , 243-249.

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ADVANCES IN THE STUDY OF BEHAVIOR VOL. I 1

The Sociobiology of Pinnipeds PIERRE

JOUVENTIN

AND

ANDRBCORNET

LABORATOIRE D’EVOLUTION DES

UNIVERSITB

.... A.

VERTBBRBS

DES SCIENCES ET TECHNIQUES DU LANGUEWC MONTPELLIER, FRANCE

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,

.............................. Sex Ratio and Habitat.. ........................................

F. Effect of Sex Ratio on Sexual Dimorphism ........................ G . “Monogamy“ and Polygyny among Pinnipeds ..................... Ill. Adaptative Strategies among Phwidae and Oteriidae. ................... A . Divergences in Ways of Life . . . . . . . . . . . . B. Divergence in Rearing Methods.. ................................ C. Divergence in Geographical Distribution . . . .................. D. Convergent Evolution of Social Structures , . ............. References ......................................................

I.

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130 131 133 133 135 136 139

INTRODUCTION

David Lack ( 1968) inspired a new type of research linking ecology and evolution. J. H. Crook added a behavioral dimension to this synthesis and extended it from birds to mammals. He gave the name “social ethology” to this new approach, which goes back to the origins of “comparative ethology” and differs little from “behavioral ecology” or “sociobiology. Within this broad framework, Crook (1970a) defined more specific approaches, such as “socioecology ,” which studies the links between environment and social structure. But Crook’s hypothesis (197Ob), explaining the socioecology of primates, brought many exceptions to light, particularly in the closed environment of the equatorial forest, which has turned out to be much more complex than was implied by the original generalizations (e.g., Jouventin, 1975). When considering environmental parameters, such as the density of vegetation, confusion ap”

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pears to be inevitable, since in reality this one factor conceals a number of others, such as visibility, amount of food available, type of predation, and so on. Consequently we thought it would be interesting to leave aside those particular ungulates and primates which have been mainly the subject of socioecological studies and find a group living in a less complex environment, where the influence of environmental parameters could be easily detected. The social life of many Pinnipeds develops only during the breeding period. The small islands or pack-ice where pupping takes place constitute a particularly simple biotope. Predators are generally absent and the availability of food is of no direct consequence, since the majority of species fast during this period. The ecological parameters that determine the extreme diversity of social structure among these mammals appear to be limited in number and easier to determine than those for other zoological groups. Pinnipeds include three families: the walrus or Odebenidae; sea lions and fur seals or Otariidae; and seals or Phocidae. Odebenidae comprise only one species. In spite of the originality of its unique appearance, which is due to its use of its teeth in removing molluscs from the bottom of the sea, the walrus, Odebenus rosmunus, is more closely linked to Otariidae than to seals. It is, in fact, a highly specialized Otarid, and these two families are grouped together in the super family Otaroididae. Presently available information on the subject indicates that the problems of social evolution posed by walrus do not seem to be very different from those we will be studying in detail in connection with Otariidae. Consequently we will not pay much attention to this particular animal, which has been subject to numerous massacres and which today breeds in small harems. Sufficient information is available on 12 species of sea lion and fur seal to indicate that their social organization is very similar. All have harems containing an average of 5-15 females per male, the only exception being the northern fur sea, Cullorhinus ursinus, which has large sized harems (15-60 females per male). This family is so homogeneous that comparative studies are difficult. Socioecological studies of the 18 species of seals are particularly instructive because this family, although very homogeneous, shows extreme diversity in social structure. Authors have described both “monogamous” species and species in which the harems contain up to 100 females per male. Parallel to this diversity in social structure found among Pinnipeds, which, combined with their relatively uncomplicated environment, allows us to demonstrate their ecological determinism, is the fact that this group also exhibits considerable variation in certain other characteristics, such as sexual dimorphism: the males of the elephant seal, Miroungu sp., and of several Otariids, are three to four times larger than the females, whereas among other seals, such as the leopard seal, Hydrurgu leptonyx, the female is distinctly larger than the male. Consequently our aim was to go beyond a socioecological approach in the strictist sense of the word, in order to consider the social ethology of this group

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and to incorporate the maximum number of adaptive characteristics in a sociobiological synthesis, paying particular attention to Phocidae, which provide the most conclusive evidence. Finally we will consider the adaptive strategies which appear to have been adopted by the two polyspecific families of this suborder and which pose the problem of phylogenetic potentialities. In effect, the latter, which are specific to each zoological group, seem as important in evolution environmental adaptations inherent to each species.

II. SOCIAL STRUCTURES A.

SEXRATIOA N D HABITAT

As we have seen, all species of Otariidae form harems and, incidently, they all breed on land. In contrast, seals, which can breed on extremely varied substrata, exhibit varying social structures. Information on the biology of reproduction is insufficient for certain species, but it is certain that more than half the species of seals exhibit a sex ratio of 1 during reproduction. Thus the harem is not the usual form of social structure among Phocidae. The majority of seals described as “monogamous” or as living in “family groups” (1 male plus 1 female plus young of that year) reproduce on the pack-ice. Seals that breed on fast-ice and coastal zones usually form small harems. Finally, the large harems found among certain Otariidae and among elephant seals, Mit-ounga sp., are generally found on small islands. It would appear, as Stirling (1975) noted, that the type of social structure is linked to the amount of space available for breeding. The less surface there is, the more extreme the polygyny is among Pinnipeds (Jouventin and Cornet, 1979).

B. SOCIAL PLASTICITY In order to test this hypothesis, we referred to both the recent literature and the results of our comparative study of the Weddell seal, Lepronychotes weddelli (Comet and Jouventin, 1980) in different localities. I.

Weddell Seal

The weddell seal, Leptonychotes weddelli, lives near the fast-ice that surrounds the Antarctic continent. In order to fish, the seals maintain access to the sea by keeping cracks in the sea ice open. At the end of the austral winter, the dominant males push the other males to the periphery of the traditional pupping areas. In this area of cracked ice, which is particularly favorable to breeding (it can be easily reached and is long lasting), the females leave the water and give birth a short time Iater on the ice. They distribute themselves in the vicinity of the cracks and return to the sea when the young are to be weaned. Copulation takes

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place in the sea with a dominant male, who patrols under the surface of the water. The harems are therefore not the immediate consequence of direct competition between males for females, but of competition for a limited number of cracks in the ice. Moreover, if our data obtained on the sex ratio during reproduction at Pointe Geologie are compared with data obtained at McMurdo Sound (Stirling, 1969, 197la), we see that at Pointe Geologie, Terre Adelie (French Antarctic territory), harems contain four to five females, and harems near the American Base at McMurdo Sound contain six to eight females. How can this difference be explained? McMurdo Sound is situated inside a bay, 12" further toward the South Pole than Point Geologie and several kilometers from the edge of the permanent sea ice. The condition of the ice at McMurdo Sound is consequently quite different. It is much thicker and more solid and breaks up later. The cracks which give the seals access to the water are consequently much fewer in number. According to published photographs, the number of females gathered around the cracks is much greater than in Terre Adelie. There would therefore be much more competition for the fewer ice cracks among males, and this could explain the difference in sex ratio apparent in the two pupping areas. The weddell seal thus exhibits a social structure which varies fmm one locality to another, according to the condition of the sea ice, and consequently the amount of space available for breeding. But a plasticity of social structure may be observed even in one locality. This is the case in Terre Adelie, when we compare the years in which the ice broke up early with the years in which the ice was thick (Cornet and Jouventin, 1980). This plasticity is not peculiar to the weddell seal. In fact for each species of seal studied in detail, we noted the presence of larger harems whenever the surface area available for breeding was reduced.

2 . The Grey Seal The grey seal, Halichoerus grypus, usually breeds on the grassy slopes and sheltered beaches of the islands in the north Atlantic. The harem may contain up to 10 females per male (Anderson et al., 1975). Hewer (1960) points out that the way males control females differs according to the nature of the breeding area. When the beach is narrow and limited by cliffs, the males patrol in the water at the entry to the beach to prevent other males from approaching. If the access to the females is too difficult to control and if the surface area of the breeding area is too large, the males remain on land and defend the area on which their harems are situated directly. Copulation may take place either in the water ar on land depending on the circumstances. Similarly Mansfield (1966) and Smith (1966) point out that in Nova Scotia the social organization is more flexible than on the islands in the North Atlantic, a fact which seems linked to the abundance of space available for breeding.

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125

Certain populations of grey seal which live in colder waters breed on the pack-ice rather than on land. The authors who have observed them speak of “loose harems” (Curry-Lindhal, 1970) or even of “monogamy” (Hook, 1961). This is a good illustration of our starting hypothesis.

3 . The Common Seal In the case of the common seal, Phoca vitulina, although available data are less specific, authors speak of “spaced” family groups (pair plus young of that year) among the subspecies Phoca vitulina largha , which breeds on the pack-ice (Burns et a l . , 1972), and of relatively dense groups in which breeding takes place on land. In the latter case, Bigg (1969) points out that among Phoca virulina richardi the mortality rate differs between the sexes after sexual maturity is reached, which is an indication of polygyny, as defined in the following. 4 . The Elephant Seal

Elephant seals, Mirounga angustirostris and Mirounga leonina, have been particularly well studied, so that a comparison of sex ratios observed during breeding in different localities is possible (Barrat and Mougin, 1978). With the exception of South Georgia, where the subantarctic elephant seal, M.leonina, is harvested, which of course modifies the demographic structure of the population, all other subantarctic islands on which censuses have been carried out have harems of a similar size: Crozet Island, 1 male per 45 females; Macquarie Island, 1 male per 48 females; Kerguelen Island, 1 male per 55 females. At the limits of distribution of this species, on the other hand, the harems are much smaller. In the south, on Signy Island, near the Antarctic peninsula, the average sex ratio is 1 male per 12 females during breeding. At the northern limits, on Valdes peninsula (Argentina), the harems are even smaller: 50% contain two to three females (Le Boeuf and Petrinovich, 1974). The density of reproduction is low in these two localities and consequently the surface area available for breeding is proportionally larger than in the main breeding area.

DETERMINISM OF SOCIAL STRUCTURES C. ECOLOGICAL The female alone is responsible for rearing the young among all Pinnipeds. This is a necessary condition for the appearance of polygyny, but cannot be solely responsible for it. The tendency toward polygyny is of course not peculiar to this group, but is quite widespread among mammals. This is related to the secondary role for males in rearing the young. Figure 1 explains the mechanism of ecological determinism of social structures among Pinnipeds. The point of departure seems to us to be the necessity to breed in areas that are accessible from the water, but are also as sheltered as possible

126

PIERRE JOUVENTIN AND ANDRE CORNET ~~

~~

BREEDING AREAS USUALLY SHELTERED FROM PREDATOR8 AND DIRECTLY ACCESSIBLE FROM WATER

I

I

1

LARGE HAREMS (tarrentrial copulation)

--

SMALL HAREMS (aquatic or term.trla1 copulstlon)

NO HAREM (aquntlc copulation1

4

sopfld

loq/ld

-

-Qmy

-Elephant

-

-

weddell seal seal

Mali

m a r Obrild.

-Northern hu Mal-

6glId

1y1d

Hawaiian monk ~ a l Crabeater aeal Rtnged leal

Caspian M"1 7 Hooded

hibl m d 7

L e m ~ s e a l7 Ehrded nos1 7 Harp seal -Common mil wplnu

FIG.1. Ecological determinism of social structure among Pinnipeds. The density of females varies according to the surface area available for breeding. This density determines the size of the harems the dominant males can control. This diagram explains the variations in social structure that appear among certain species. Seals whose sex ratio during reproduction is not well known are indicated with a question mark. from land predators, since Pinnipeds, with their advanced adaptation to aquatic life, are clumsy on land. Three cases may occur: 1. The density of females is very high when breeding takes place on small islands on which the surface area is limited and the feeding grounds that surround them are immense and rich. 2. The density of females is lower when the coastal zones favorable to breeding are large in proportion to the population. The same applied to breeding on the fast-ice, which is stable enough to allow rearing the young, but cracked to allow access to the water. The result is the same, a low density of females. 3. When the fast-ice is subject to predation from the land, as is the case in the Arctic, the females disperse for breeding to escape the threat (cf. Section II,D). The same wide dispersion of females occurs on the unstable pack-ice, which is

THE SOCIOBIOLOGY OF PINNIPEDS

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broken into pieces allowing easy access to the water. Finally, in tropical seas poor in food supply, the population is low and the beaches and islands on which the females breed are abundant in proportion to the population. In these three very different cases, the same result is achieved: dispersion of females during breeding. As we noted at the beginning of this section, the females can rear their young on their own, which allows for polygyny whenever the situation permits: 1. When there is a high density of females, the dominant males can control access to a large number of females at a time. This fact determines the large harems such as those of the Otariidae, particularly the northern fur seal and among Phocidae, those of the elephant seals. The males are thus obliged to remain on land near the females to keep dominated peripheral males at a distance. Thus copulation generally takes place on land. 2. When the density of females is low, the dominant males can control access to only a few females, which leads to small harems. This is the case with the weddell seal, Leptonychotes weddelli, on the fast-ice, and, in coastal areas, with certain elephant seal populations, the common seal, Phoca vifuline, and grey seals, Halichoerus grypus. Copulation takes place either in the water or on land, depending on the circumstances. 3 . When the females are dispersed, the dominant males cannot control access to several females at once, which prevents the formation of harems and permits copulation in the water. This category includes the majority of species of seal, most of which breed on the pack-ice. It is the case with the crabeater seal, Lobodon carcinophagus, and probably with the leopard seal, Hydrurga leptonyx, and the ross seal, Ommatophoca rossi, which live on the edge of the Antarctic continent. In the northern hemisphere, on the Arctic pack-ice, it is also the case with the hooded seal, Cysfophora cristata, and the bearded seal, Erignathus.

Another example of a so-called "monogamous" seal, the Hawaiian monk seal, Monachus schauinslandi, breeds on land. At first glance this would seem to be an exception, since all other Pinnipeds that breed on land are polygynous. But it should be kept in mind that the warm seas in which this seal lives are poor in food supply (Foxton, 1956) and that food may constitute a limiting factor. In addition, from a zoogeographic point of view (Davies, 1958), it should not be forgotten that this is a relic population which only just survived the massacres of the nineteenth century (Maxwell, 1967). Be that as it may, the density of the species is relatively low and the surface area available for breeding is overabundant, which brings about a dispersion of females comparable to that of seals breeding on the pack-ice.

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If the data had been available, we would have considered it necessary, at this point, to deal with social plasticity induced by man. The walrus seal, elephant seal, Greenland seal, common seal, grey seal, and three species of monk seal have all been subject to extensive massacres. Certain populations have been (or still are) on the verge of extinction as a result of this unrestricted harvesting. Some have reestablished themselves as a result of the protective measures that have been taken (cf. Comet, 1979). The density of females consequently diminished and then rose again, and, according to our hypothesis, not only the number of harems, but also the number of females contained in them should have decreased in direct proportion. In this way the social structures may have been modified, leading, in certain cases, to the formation of pairs. D.

ADAPTATION TO ARCTICPREDATION

Like the weddell seal, the ringed seal, Pusa hispida, lives close to the fast-ice, but in the Arctic. One would therefore expect a social structure with small harems. But according to authors who have studied this species (Smith and Stirling, 1975; Stirling, 1977), the breeding females are hidden under the snow and dispersed as a result of land predation, which occurs in the Arctic but not in the Antarctic.' It is therefore not surprising to observe a sex ratio of 1 male to 1 female for this species during reproduction. Predation appears to play an important role in the biology of Arctic seals. Some authors, such as Laws (1962), assumed that the young had a white coat at birth in response to predation. Others disagreed, arguing that the polar bear, Thalarctos maritimus, hunts by smell and not by sight. Even if smell is more predominant than sight, the camouflage may be of certain value for survival. Moreover, it is interesting to note that all species that give birth to young with a white coat breed on the ice, whereas all those who give birth to young with a dark coat breed where there is no danger of predation. The only exceptions to this rule, the bearded seal, Erignathus barbatus, and the hooded seal, Cystophora cristate, give birth on the edge of the Arctic pack-ice, have a very short rearing period, and are therefore probably subject to little predation. Moreover, young common seals, Phoca virulinu, born on land, lose their white coats before birth, whereas among the subspecies Phoca vitulinu largha , which breeds on the ice, moulting takes place just before weaning (Ling, 1978). It can be noted that the life span of Arctic seals is almost twice as long as the 'One may wonder why the opposite strategy is not used. In fact, it seems that a group of seals cannot repel the attack of one or several bears, deprived as they are of any means of defense such as the walrus has. This latter fact may provide an explanation for the huge beach colonies of walruses noted by early navigators which can no longer be observed due to massive slaughters and did not fit in with our conclusions.

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THE SOC10BlOLOGY OF PINNIPEDS

0

5

10

IS

20

I5

30

3s

‘O

SEX MTIO

FIG. 2. Relation between sex ratio and age of sexual maturity. Among seals the larger the harem (sex ratio in breeding area) the larger the discrepancy in age of sexual maturity between males and females. (This discrepancy is expressed by the relation of the age of sexual maturity of the male to that of the female. Each triangle represents one species. Table I gives a list of bibliographical sources and abbreviations used.)

Antarctic species.2 To counterbalance this source of mortality (predation), Arctic seals could not increase their birthrate (since Pinnipeds only rear one young). Their demographic strategy therefore appears to have been an increase in life span. OF SEX RATIOON S E X U A L MATURITY A N D MORTALITY E. EFFECT Among highly polygynous species such as Otariidae and elephant seals, it is known that females attain sexual maturity much earlier than males. For example, among subantarctic elephant seals, Mirounga leonina, whose harems contain an average of 40 females, males start reproducing at the age of 7-8 years and females at 3-4 years (Canick et a l . , 1962). By contrast, among bearded seals, Erignarhus barbarus, considered “monogamous, ” females attain sexual maturity at 6 and males only 1 year later (McLaren, 1958b; Mansfield, 1964). Using data obtained for four other species, we can plot a curve (Fig. 2 and Table I) using the size of the harems as the abscissa and the relation of the age of sexual maturity of the male to that of the female as the ordinate. The correlation between the sex ratio during reproduction and the difference in age of sexual maturity between the sexes is evident. Note, however, that the correlation between the sex ratio during reproduction and the start of sexual maturity appears asymptotic; the difference between the ages of sexual maturity soon levels off. Nishiwaki (1972) indicates that among Otaria byronia and Callorhinus ursinus, males attain sexual maturity at 6 years whereas females attain it at 4 years. Johnson (1 968) even says that males of Callorhinus ursinus have little chance of acquiring a harem before the age of 8 or 10 years.

2Lepronychores weddelli IS+ years (Stirling, 1971a); Mirounga leonina 15-18+ years (Laws, 1960); Pagophilus groenlandicus 25+ years (Sergeant and Fisher, 1960); Halichoerus grypus 20-30+ years (Bonner, 1972).

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TABLE I SPECIESOF PHOCIDAE A N D OTAMIDAE Species Phocidae PV, Phoca vitulina PVI, Phoca vitulina largha PH, Pusa hispida PC, Pusa caspica PS, Pusa sibrica HF, Histriophoca fasciata EB , Erignarhus barbatus Pagophilus groenlandicus Halichoerus grypus Cysrophora crisrara Mirounga angustirostris Mirounga leonina Monachus monachus Monachus schauinslandi Lepronychores weddelli

HL, Hydrurga leptonyx

Reference Bonner ( 1972) Bums et al. (1972) McLaren (1958a) Heu (1977) Heu (1977) Heu ( I 977) McLaren (1958b); Mansfield (1964) Sergeant and Fisher (1960); Mansfield (1964) Mansfield ( 1966); Bonner ( 1972); Anderson er al. ( 1975) Mansfield (1964); Chistland (1964, 1975) Bartholomew (1952) Laws (1960); Carrick er al. (1962) Van Wijngaarden (1962) Kenyon and Rice ( 1959) Isenmann (1970); Stirling(l971d); Kaufmann era/. (1975); Comet and Jouventin (1980) Laws (1957); Hofman er al. (1977)

Otariidae Eumetopias jubara Callorhinus ursinus Zalophus californianus Otaria byronia Phocarcros hookeri Arctocephalus forsteri A rcrocephalus pusillus Arctocephalus gazella

Mathisen er al. (1962); Martin (1977) Scheffer and Wilke (1953); Peterson (1968); Johnson (1 968) Peterson and Bartholornew (1967); Nishiwaki (1972) Nishiwaki (1972) Nishiwaki (1972) Stirling (1971b,c); Miller (1975) Rand (1955, 1956) Paulian (1964); Bonner (1968); Payne (1979)

At the same time it has been noted that among polygynous species there is a much higher mortality rate among males than among females after the age of sexual maturity is attained. This is true of the Otariidae (Johnson, 1968; Stirling, 1971b,c), of the weddell seal (Stirling,1971a; Siniff et al., 1977), of the common seal (Bigg, 1969), and of the grey seal (Bonner, 1972). The difference in the mortality rate of the sexes is probably due to competition between males at breeding time.

F. EFFECTOF SEX RATIOON SEXUAL DIMORPHISM Other characteristics exist in connection with the pronounced imbalance in sex ratio. First, the males of these species often exhibit extraordinary attributes such

131

THE SOCIOBIOLOGY OF PINNIPEDS

as the mane of the harem bulls among sea lions, or the trunk of male elephant seals. Another apparent consequence of competition is that the biggest males dominate and transmit these morphological characteristics to their male descendants, until some other factor, such as perhaps the difficulty of moving on land, limits the size. Among Otariidae and elephant seals, this limiting factor has occurred relatively late, since the harem bulls are three to five times heavier than the females. In Fig. 3, the number of females per harem has been entered as the abscissa, and the relation of the weight of the male to the weight of the female has been entered as the ordinate. Among seals and Otariidae the larger the harems, the greater the sexual dimorphism. In addition, it is probable that the physiological fast which the harem bulls undergo strongly encouraged sexual dimorphism. In fact, the males do not leave their harem until copulation takes place, a period of up to 2 months (Peterson, 1968; Barrat and Mougin, 1978), and during this period many fights take place. It is therefore necessary for the males to accumulate enough fat to see them through this difficult period. AND POLYGYNY AMONG RNNIPEDS G . “MONOGAMY”

It should be noted that the term “monogamy” is not really applicable to this zoological group, since it implies close ties between the members of a pair. In the

SEXUAL DIMORPHISM

(b/Ql

to

2-0

30

40

SEX RATIO

FIG.3. Relation between sex ratio and sexual dimorphism. Among Phocidae (solid triangles) as well as Otariidae (open triangles) the larger the harems (sex ratio in breeding area) the greater the sexual dimorphism. (Sexual dimorphism is expressed by the relation of the weight of the male to that of the female.) See Table I for names of species.

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case of Pinnipeds, there is no cooperation between the members of a pair in rearing the young, and they do not even appear to recognize each ather individually. If recognition between mother and young has been demonstrated for several species of Pinnipeds (cf. Comet and Jouventin, 198Q)it has never been demonstrated for members of a pair and it frequently happens in polygamous species that females change harems. In fact the males attempt to control as many females as possible and at the same time to prevent rivals from approaching. According to our observations, it often happens that these two requirements are irreconcilable and that temporary pairs are formed (“monogamy”). Since, among Pinnipeds, the female rears the young on her own, polygyny becomes possible but is not inevitable, as the numerous examples of seals with a sex ratio of 1 during reproduction show. When the surface area available for breeding is reduced, density of females is high and the males fight each other. For quite some time an explanation has been sought for the extreme polygyny found among certain species of Pinnipeds. In 1891 Nutting had already drawn attention to the problem and localized possible answers. Far in advance of his time, he had noticed that among species of Pinnipeds with large harems, males were much heavier than females, and he believed that it was the intense competition between males that was responsible for this morphological and social evolution. One can continue his line of thought and ask what causes this aggression. There is no point evading the question by saying that it is due to an increase in the testosterone rate, which only involves transferring the search to what causes this increase (likewise, female gregariousness does not seem to be the former cause of the polygamy of Pinnipeds). To reformulate the question: what survival value does this aggression represent? Traditionally the problem has been considered from a genetic point of view, competition between males being considered beneficial to the descendants, the more fit transmitting their genetic characteristics. The elephant seal is given as a perfect example of sexual selection: Le Boeuf and Peterson (1969) estimated that in one zone under study, approximately 6% of the 71 males impregnated 88% of the 120 females and that, in another zone, one male alone was responsible for 73% of the copulations. In fact these figures are applicable only to one reproductive cycle. In reality, among extremely polygynous species, the females reproduce every year, while harem bulls are rapidly ousted and replaced by males immediately below them in the hierarchy. Among northern fur seal (Cullorhinus ursinus) whose harems contain approximately 20 females, a male will control a harem for an average of 1.5 reproductive cycles during the course of its life, whereas the females will give birth during an average of 5.4 reproductive cycles (Peterson, 1968;Johnson, 1968). In the long run, more males contribute to the lineage than the size of the

THE SOCIOBIOLOGY OF PINNIPEDS

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harem would lead one to suppose. Genetic advantage certainly plays a role, but a much less important role than was assumed. Another advantage brought by this hierarchy of dominance lies in the elimination by the harem bull of most other males from favorable breeding grounds. In effect, among highly polygynous species, the surface area favorable to breeding provides, as we have seen, a limiting factor, and the elimination of a great number of males must offer a survival value by allowing a few extra females to give birth. As we have seen, Pinnipeds rear only one young per year, and cannot therefore increase their productivity.

III. ADAFTIVESTRATEGIES AMONG PHOCIDAE A N D OTERIIDAE We will now try to integrate the social organization of the two polyspecific Pinniped families into the total adaptive strategies. With this aim in view, we will be referring to a variety of data. However, due to lack of data concerning the subject matter discussed in Section II1,A. we will be putting forward working hypotheses rather than definite conclusions. A.

DIVERGENCES IN WAYSOF LIFE

It is unfortunate that we know so little about the biology of Pinnipeds when they are in the water. All seals fish on their own, but observations show that at least some species of Otaridae fish in groups. The capacity for diving seems different in the two families. Whereas seals are known for their remarkable adaptation to deep diving? the Otariidae seem content to remain at a depth of between 0 and 100 m most of the time. In addition to this vertical division of the waters, we can perhaps add a horizontal division. Otariidae are generally found more frequently in coastal waters than seals. The method of swimming is also quite different in the two families. Seals propel themselves by means of their hind flippers, whereas Otariidae use their front flippers for propulsion. The method of swimming used by Otariidae is compatible with functional limbs on land. The fusiform shape of the seal limits their mobility on land. B.

DIVERGENCE IN REARINGMETHODS

While rearing their young, female Phocidae take practically no nourishment. They have to face a weight loss due to physiological fasting and suckling. Ralls (1976) assumes that fat is advantageous to females mammals in that they can feed their young better (“big mother hypothesis”). This selective pressure would ’The weddell seal, for example, dives to a depth of more than 600 m and can remain submerged for 43 min (Kooyman, 1968).

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explain the sexual dimorphism in favor of the female that is found in many species and in particular among several species of seal. We calculated the rate of growth among Phocidae and Otariidae and note that it is proportional to the size of their mother (Fig. 4). Therefore relative growth does not differ from one species to another, and the biggest females do not appear to be the “best mothers. What is more, there is no correlation between the size of the mother and the duration of lactation. The fact that the females are larger than the males among certain species of seal is perhaps simply due to a phylogenetic tendency, since we note that these species all belong to the same subfamily: the Monachinae. The duration of lactation is, however, linked to the substratum on which breeding takes place (Fig. 5 ) . When the substratum is unstable, as is the case of pack-ice, weaning takes place rapidly; the duration of lactation among hooded seals, Cystophota cristata, leopard seals, Hydrurga leptonyx, and crabeater seals, Lobodon carcinophugus, is 1 or 2 weeks. When the substratum is solid (fast-ice, land), lactation lasts at least 1 month, except in the case of elephant seals, Miroungu sp., and grey seals, Halichoerus grypus, which breed on land but where the density is high. As far as these two species are concerned, it is possible that the strategy adopted is to wean the young as soon as possible in order to teach them to feed themselves even in the open sea, since the coastal waters are not adequate for the needs of such a large population. In any case the reproductive strategy of the Phocidae is to accumulate fatty reserves to permit uninterrupted rearing of the young and early weaning. ”

FIG.4.Divergence between rearing methods of seals and Otariidae. Among Phocidae (solid squares) as well as Otariidae (open squares) daily growth of young is proportional to the size of the female. Nevertheless the Otariidae differ from seals to the extent that growth is slower, which is directly linked to the longer rearing period. See Table I for names of species.

THE SOCIOBIOLOGY OF PINNIPEDS

I

LAND

.

135

"0

.

"I

"I

FAST I C E

PACK-ICE

I

I

.* .L

9"' I

-

ec

LC

0

1

2

3

4

5

6

7

LENGTH OF LACTATION (reek81

FIG. 5. Relation between substratum of breeding area and duration of lactation. When the substratum is unstable (pack-ice) the rearing period is short (less than 1 month). When the substratum is stable (fast-ice, land) the rearing period is long (more than 1 month). Elephant seals (MA and ML) and the grey seal (HG) seem to have chosen early weaning which teaches the young to feed itself in the open area. (Coastal waters do not provide enough food for such a large population.) See Table I for names of species.

Otariidae have adopted a different strategy: during lactation they spend more than half their time in the sea, only returning to land to feed their young. Consequently, Otariidae take longer to rear their young (2 months-I year) than seals (1 week-2 months.)

c.

DIVERGENCE IN GEOGRAPHICAL DISTRIBUTION

The fatty reserves found among seals permit distribution further toward the pole. Male Otariidae also possess large reserves of fat, which probably explains the fact that they sometimes migrate to colder waters than the females of the same species. If the species of Pinnipeds living in all latitudes (20"sections) are added up (Fig. 6), it appears that the number of species decreases toward the equator, perhaps due to lack of food in warm waters, but also, as Davies (1958) pointed out, due to physiological adaptation of Pinnipeds to cold waters and the absence of competitors for food there. Close to the poles the number of species also diminishes as a result of the severe climate. If one distinguishes the percentage of the species of each of these two families, it can be noted that distribution is reversed: toward the poles seals predominate, toward the equator, Otariidae. It would seem as though the two families of Pinnipeds have divided the seas between them, the seals, which are larger, occupying the coldest waters. Moreover, if the geographical distribution of seals and Otariidae is examined, it will be seen that marine isotherms may have played almost as important a role as ecological isolation. In the northern hemisphere, the continental masses have disturbed this distribution. but the isotherms often coincide with limits of

136

PIERRE JOUVENTIN AND

PERCENTAGO OF SPECIES BELONGING M THE TWO FAMILIES

ANDRB

CORNET TOTAL NUHBER OF SPECIES +.,

T

,..

I

I

N W - T OT O - D O

ao-ao

ao-10

40.10

(0-10

IO-W

60.~0

LATITUDE

TO-WS

FIG.6. Zoogeography of Otariidae and Phocidae. The number of species of Pinnipeds (solid circles) decreases toward the equator due to the poverty of the marine food supply, to rivals for food, and to physiological adaptation to cold waters. It also decreases toward the poles due to severe climatic conditions. Otariddae (open histograms) frequent warmer waters than Phocidae (solid histograms) who are better adapted to cold waters due to their larger body size. distribution areas. In the southern hemisphere, nothing disturbs ring distribution except geographical speciation. Among other marine animals such as Euphausidae (Mackintosh, 1960) and Spheniscidae (Jouventin, 1978 and in press), this zoning in concentric circles (in relation to the temperature of the sea water) is even more evident. D.

CONVERGENT EVOLUTION OF SOCIAL STRUCTURES

Among certain mammals the development of the ovum is interrupted and its implantation in the wall of the uterus is delayed. The phenomenon of delayed implantation occurs in both families and is the result of their amphibian way of life, since grouping birth and copulation means that Pinnipeds do not have to return to land twice. Recent authors (Peterson, 1968; Bartholomew, 1970; Stirling, 1975) assume the extreme polygyny which characterizes this group results from their amphibian way of life in which birth takes place on land as opposed to offshore marine feeding. In fact sea birds exhibit the same imbalance between the immensity of their feeding areas and the exiguousness of their breeding areas. In both groups the surface area available for breeding constitutes a limiting factor. Nevertheless among sea birds the resulting gregariousness has not led to the same social structure. Pinnipeds are polygynous whenever the environment permits, whereas the 280 species of sea birds are all truly monogamous. Their colonies are made up of a mosaic of minute territories one next to the other, each defended by a pair of brooding birds.

THE SOCIOBIOLOGY OF PINNIPEDS

137

These strictly monogamous species exhibit characteristics that are directly opposed to those we have described for the most polygynous Pinnipeds (Fig. 7): equal division of tasks between sexes after laying, highly developed individual recognition between members of a pair (Jouventin, 1972, 1978, in press; Jouventin et al., 1979) who also remain extremely faithful to each other from one year to the next, and absence of sexual dimorphism, which makes determination of sex a difficult task (for more details on adaptive strategies of sea birds, see Jouventin and Mougin, in press). Thus, on the one hand, all these characteristics are interdependent and cannot be understood in isolation; on the other hand, although the environment plays a determining role in these zoological groups, it makes use only of preexisting potentials. The existence of the placenta and the mammary glands are considerable aids in making pregnancy and the rearing of young possible; the male is needed less and is therefore available to several females. Among sea birds the tasks to be carried out are more demanding and, generally speaking, both parents are needed to incubate the egg and feed the chicks, which explains the fact that 91% of avian species are monogamous (Lack, 1968). Among pelagic sea birds, the death of one parent inevitably leads to the death of the chicks, unless they are ready to fly. True monogamy also exists among certain mammals, for example, Canidae,

FIG.7 . The Pinnipeds strongly polygynous are confronted, like sea birds, with the same imbalance between the vast marine areas where food is found and the scarcity of suitable islands for reproduction (central columns). But, each of the groups adapts itself to this problem according to its own phylogenetic potential (side column). Consequently, the social structures are different as is the outcome (lower half of diagram).

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but it is the result of particularly difficult conditions governing the rearing of the young. Among predators with only irregular supplies of food at their disposal, the male and sometimes the young of the previous litter contribute to feeding the new born and even the mother. The presence of the male and his attachment to the female means a larger number of young can survive each year. Among all Pinnipeds the females give birth to only one young per year and the male does not participate directly in the rearing, so polygyny is possible. The extreme polygyny that is found among elephant seals and Otariidae (and in particular northern fur seal, Culorhinus ursinus, which have the largest harems) is the result of the coincidence between the physiological characteristics of these mammals and the scarcity of their breeding areas. These gigantic harems are just as extraordinary as the colonies of thousands and thousands of sea birds, since both are extreme adaptations to an exceptional situation. It is this spectacular aspect that has captured the attention of all authors and caused them, aside from Stirling, to neglect the more mundane but much more common and instructive case of the so-called "monogamous" seal. In an analogous situation sea birds and highly polygynous Pinnipeds have adapted themselves to limiting factors according to their phylogenetic potentialities. Colonial sea birds were obliged to submit to the limitations of incubation and the search for food for the chicks. They reduced the territory around their nest and formed lasting pairs. Pinnipeds, faced with the same problems, and being mammals, chose advanced polygyny. The families that make up the Pinnipeds are obviously more closely related among themselves that they are to sea birds! Nevertheless, on another scale, we have seen that they exhibit considerable differences in ways of life, rearing of young, and geographical distribution. Otariidae are not seals that are less well adapted; each family occupies its own place and its social structure reflects this fact. Certain convergences do exist and these have attracted the attention of previous authors. But the social diversity of the Phocidae contrasts strongly with the uniformity of the Otariidae. Otariidae live in warmer waters and breed only on land, whereas seals also breed on the ice. As a result of their ecological determinism, the social structures of the seal are more varied. Among Otariidae there is a parallel to be seen between uniform environment and uniform social structure. Thus, on two levels-that of the original divergence between sea birds and mammals and that of the recent divergence between Otariidae and seals-the evolution of the social systems has had to yield to preexistent phylogenetic potentialities, and to adapt them, at the very least, to environmental conditions. Not everything can be explained by environment. Adaptation to an unexploited source of food can be made only by available species and the destiny of any zoological group is always the result of a compromise between its past and its present.

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References Anderson, S . S . . Burton, R. W., and Summers, C. F. 1975. Behaviour of grey seals (Halichoems grypus) during a breeding season at North Rona. J. Zool. 177, 179-195. Barrat, A.. and Mougin, J. L. 1978. L’elephant de mer, Mirounga leonina, de I’ile de la Possession, Archipel Crozet. Mammalia 42, 143-174. Bartholomew, G . A. 1951. Reproductive and social behavior of northern elephant seal. Univ. Calif., Berkeley, Publ. 2001.47, 369-472. Bartholomew. G. A. 1970. A model for the evolution of Pinniped polygyny. Evolurion 24, 546-559. Bigg, M. A. 1969. The harbour seal in British Columbia. Bull.. Fish. Res. Boardcan. 172, 1-33. Bonner, W.N. 1968. The fur seal of South Georgia. Arctocephalus tropicalis gazella. Br. Anfurcf. Surv. Sci. Rep. 56, 1-81. Bonner, W. N. 1972. The grey seal and common seal in european waters. Oceatwgr. Mar. B i d . 10, 46 1-507. Bums, J. J., Ray, G. C., Fay, F. H., and Shaughnessy, P. D. 1972. Adoption of a strange pup by the ice-inhabiting harbor seal (Phoca vitulina largha). J . Mammal. 53, 594-598. Carrick, R., Csordas, S . E., Ingham, S. E., and Keith, K. 1962. Studies on the Southern elephant seal. Mirounga leonina. 111. The annual cycle in relation to age and sex. CSIRO Wildl. Res. 7, 119-160. Comer, R. W. M. 1972. Observations on a small crabeater seal breeding group. Br. Anrarcr. Surv. Bull. 30, 104-106. Cornet, A. 1979. La socioecologie du Phoque de Weddell. These d’lngenieur-Docteur, Montpellier. Comet, A., and Jouventin, P. 1980. Le phoque de Weddell (Leptonychotes weddelli L.) a Pointe Geologie et sa plasticite sociale. Mammalia (in press). Crook, J . H. 1970a. Social organization and the environment aspects of contemporary social ethology. h i m . Behav. 18, 197-209. Crook, J . H. 1970b. The socio-ecology of Primates. In “Social Organizations in Birds and Mammals” ( J . H. Crook, ed.), pp. 103-159. Academic Press, New York. Curry-Lindhal, K . 1970. Breeding biology of the Baltic grey seal (Halichoems prypus). 2001.C a r t . , Leipzig 38, 16-29. Davies, J. L. 1958, The Pinnipedia: An essay in zoogeography. Geogr. Rev. 48, 474-493. Foxton, P. 1956. The distribution of the standing crop of zooplancton in the southern ocean. ’Discovery’ Rep. 28, 191-235. Heu, R. 1977. Essai sur les phoques de I’hemisphere nord. Ecole des hautes etudes en sciences sociales (unpublished data). Hewer, H. R. 1960. Behaviour of the grey seal (Halichoems grypus) in the breeding season. Mummalia 23, 400-42 I . Hofman. R. J., Reichle. R. A., Siniff, D. B., and Muller-Schwarze. D. 1977. The leopard seal (Hydrurga leptonyx) at Palmer Station, Antarctica. I n “Adaptations within Antarctic Ecosystems,” Gulf Publ., pp. 769-782. Hook,0. 1961. Notes on the status of seals in Iceland, June-July, 1959. Proc. Zoo/. Soc. London 137, 628-630. Isenmann. P. 1970. Contribution I’ttude de la zone de vklage du phoque de Weddell a Pointe Geologie, Terre Addlie. Mammalia 34, 573-584. Johnson, A. M. 1968. Annual mortality of territorial male fur seals and its management significance. J . Wildl. Manage. 32, 94-99. Jouventin, P. 1942. Un nouveau systeme de reconaissance acoustique chez les oiseaux. Behaviour 43, 176-186. Jouventin. P. 1975. Observations sur la socio-ecologie du Mandrill. Term Vie 29, 493-532.

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Jouventin, P. 1978.Ethologie c o m p d e des Spheniscidks (Manchots). Thbse d’Etat, Montpellier. Jouventin, P. Optical and vocal signals of penguins, adaptive characteristics. Z . Tierpsychol. (in press). Jouventin, P. Ethnology. In “The Emperor Penguin.” Yale Univ. Press, New Haven, Connecticut (in press). Jouventin, P., and Comet, A. 1979.La vie sociale des phoques. La Recherche 105, 1058-1066. Jouventin, P., and Mougin, J . L. Les strategies adaptatives des oiseaun de mer. Terre h e (in press). Jouventin, P.. Guillotin, M., and Comet, A. 1979.Le chant du manchot empereur et sa signification adaptative. Behaviour 70, 231 -250. Kaufmann, C., Siniff, D., and Reichle, R. 1975.Colony behavior of Weddell seals, Leptonychotes weddelli, at Hutton Cliffs, Antarctica. Symp. B i d . Seal. pp. 228-246. Kenyon, K. W., and Rice, D. W. 1959. Life history of the hawaiian monk seal, Monachus schauinslandi. Par. Sci. 13, 215-252. Kooyman, G.L. 1968. An analysis of some behavioral and physiological characteristics related to diving in the Weddell seal. Antarct. Res. Ser. 11, 227-261. Lack, D. 1968.Ecological Adaptations for Breeding in Birds. Methuen, London. Laws, R . M. 1957 On the growth rates of the leopard seal, Hydrurga leptonyx. Sauegerierkd. Mitt.

5, 49-55. Laws, R. M, 1960. The southern elephant seal (Mirounga leonina) at South Georgia. Nor. Hvaljangst-Tid. 49, 466-476. Laws, R. M. 1962. Comparative biology of antarctic seals. C. R. Symp. Biol. Anrarcr..: lsr, pp. 445-454. Le Boeuf, B. J . , and Peterson, R. S. 1969. Social status and mating activity in elephant seals. Science 163, 91-93. Le Bwuf, B. 1., and Petrinovich, L. F. 1974. Elephant seals: interspecific comparisons of vocal and reproductive behavior. Mammalia 38, 16-32. Ling, 1. K. 1978.Pelage characteristics and systematic relationships in the PLnnipedia. Mammalia

42, 304-312. Mackintosh, N. A. 1%0. The pattern of distribution of the antarctic fauna. Proc. R. Soc.London 152, 624-631. McLaren, I. A. 1958a. The biology of the ringed seal (Phoca hispida) in the eastern Canadian arctic. Fish. Res. Board Can., Bull. 118, 1-97. McLaren, 1. A. 1958b.Some aspects of growth and reproduction of the bearded seal, Erignathus barbatus. Fish. Res. Board Can. IS, 219-227. Mansfield, A. W. 1964. Seals of eastern and Arctic Canada. Fish Res. Bawd, Can.. Bull. 137,

o0O-oO0. Mansfield, A. W. 1966.The grey seal in eastem Canadian waters. Can. dudubon 28, 161-166. Martin, R. 1977.Les mammif&es marins. Elsevier, Sequoia. Mathisen, 0.A., Baade, R. T.,and Lopp, R. J. 1962. Breeding habits, gowth and stomachcontents of the Steller sea lion in Alaska. J . Mammal. 43, 469-477. Maxwell, G. 1967. “Seals of the World.” Constable, London. Miller, E. H. 1975.Body and organ measurements of fur seals, Arctocephalus forsteri Lesson, from New Zealand. J. Mmnmal. 56, 511-513. Nishiwaki, M, 1972.General biology. In “Mammals of the Sea” (S. H. Ridgeway, ed.) pp. 1-52. Nutting, C. C , 1891.Some of the causes and results of polygamy among the Pinnipedia. Am. Nat. 2s. 103-112. Onstland, Tb 1964.The breeding biology of the female hooded seal. Fisk. Can# 50, 5-19. Oristland, T. 1975.Sexual maturity and reproductive performance of female hooded seal at Newfoundland. In?. Cvmm. Nurihwesi Ati. Fish. Res. Bull. 11, 37-41. Paulian, P. 1964.Contribution B I’etude de I’otarie de I’Ele Amsterdam. Mammnalia 28, Suppl. 1,

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Payne. M. R. 1979. Growth in the antarctic fur seal, Arctocephalus gazella. J . Zool. 187, 1-20. Peterson, R . S . 1968. Social behaviour of Pinnipeds with particular reference to the northern fur seal. In “The Behavior and Physiology of Pinnipeds” (R. J . Harrison et a / . , eds.), pp. 5-53. Appleton, New York. Peterson, R . S . , and Bartholomew, G . A. 1967. The natural history and behavior of the California sea lion. Am. Soc. Mammal. Spec. Puhl. 1 , 1-79. Ralls, K . 1976. Mammals in which females are larger than males. Q. Rev. Biol. 51, 245-276. Rand, R . W. 1955. Reproduction in the female Cape furseal, Arctocephalus pusillus. Proc. Zool. Sol.. London 124, 7 17-740. Rand, R. W. 1956. The Cape fur seal, Arctocephalus, its general characteristics and moult. Invest. Rep. Div. Fish. Union South Afr. 21, 1-52. Scheffer, V. B.. and Wilke, F. 1953. Relative growths in the northern fur seal. Growth 17,729-755. Sergeant, D. E., and Fisher, H. D. 1960. Harp seal populations in the western north Atlantic from 1950 to 1960. Fish. Res. Board Can., Circ. 5 , 1-58. Siniff, D. B.. De Master, D. P., Hofman. R. J . , and Eberhardt, L. L. 1977. An analysis of the dynamics of a Weddell seal population. Ecol. Monogr. 47, 319-335. Smith, E. A. 1966. A review of the world’s grey seal population. J. Zool. 150, 463-489. Smith, T. G., and Stirling, I. 1975. The breeding habitat of the ringed seal (Phoca hispida). The birth lair and associated structures. Can. J. Zool. 53, 1297-1305. STirling, I. 1969. Ecology of the Weddell seal in McMurdo Sound, Antarctica. Ecology 50, 573586. Stirling, 1. 1971a. Population dynamics of the Weddell seal in McMurdo Sound, Antarctica, 19661968. Antarct. Res. Ser. 18, 141-161. Stirling, I. 1971b. Studieson the behaviour of the south australian fur seal, Arctocephalus forsteri. 1. Annual cycle, postures and calls, and adult males during the breeding season. Aust. J. Zool. 19, 243-266. Stirling, 1. 1 9 7 1 ~Studieson . the behaviour of the south australian fur seal, Arctocephalus forsteri. 11. Adult females and pups. Aust. J. Zool. 19, 267-273. Stirling, I. 1971d. Leptonychotes weddelli. Mamm. Species 6, 1-6. Stirling, I. 1975. Factors affecting the evolution of social behavior in the Pinnipedia. Rapp. P.-V. Reun., Cons. Int. E.rplor. Mer. 169, 205-212. Stirling, I. 1977. Adaptations of Weddell and ringed seals to exploit the polar fast ice habitat in the absence or presence of surface predators. I n “Adaptations within Antarctic Ecosystems. Gulf Publ., pp. 741-748. Van Wijngaarden, A. 1962. The mediterranean monk seal. O v x 6, 270-273. I

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ADVANCES M THE STUDY OF BEHAVIOR VOL. I I

Repertoires and Geographical Variation in Bird Song JOHN R . KREBS DEPARTMENT OF ZOOLOGY EDWARD GREY INSTITUTE OF FIELD ORNITHOLOGY OXFORD, ENGLAND

DONALD E. KROODSMA ROCKEFELLER UNIVERSITY FIELD RESEARCH CENTER MILLBROOK, NEW YORK

I. Introduction ..................................................... 11. Repertoires . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . A . Introduction . . . . . . . . . . . . B. How Do Repnoires Contri 111. Geographical Variation . . . . . . .......................... A . Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . B. Microgeographical Variation .................................... IV. Conclusion. . . . . . . . References ........................................ .........

I.

143 144 144 146

I59 159 160 170 170

INTRODUCTION

Communication in animals can be viewed as a process in which one individual, the signaller, benefits as a result of altering the behavior of another, the receiver (Dawkins and Krebs, 1978). Some kinds of communication are easily understood within this framework: a screaming nestling induces its parents to bring food and as a result enhances its survival. But not all signals succumb to such a straightforward functional interpretation, and this is particularly true of bird song. While it is widely accepted that bird song plays a role in territory maintenance and in mate attraction (Falls, 1978),the significance in communication of song repertoires and geographical variation is not well understood. It is these two problems that we will discuss in this article. Although our discussion will be about song, we d o not propose to spend time I43

Gpydght @ 1980 by Aendemic Re%. Inc. All rights of reproduction in any form reserved ISBN 0-12-004511-7

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on the question of how song is defined. We accept that Nottebohm’s (1972, following earlier workers such as Thorpe, 1961) definition: “loud and sustained vocalizations delivered seasonally by males in possession of a breeding or courting territory” has proved adequate for most workers in the field. This definition must be qualified by the recognition that dividing bird vocalizations into songs and calls is by no means straightforward. The functional roles of song may be played by calls in some species, sometimes females as well as males sing (e..g. European robin Erithacus rubecula),and song is not always restricted to the breeding season (e.g., redwinged blackbird Agelaius phoenicus). Although the vocalizations referred to as song tend to be structurally more complex than calls, there are many exceptions, for example, the song of Henslow’s sparrow (Passerherbulusheslowii) consists of no more than a “hiccup” lasting less than 1 sec.

II. REPERTOIRES A.

INTRODUCTION

According to surveys such as those by Hartshorne (1973)and Dobson and Lemon (1975), in at least three-quarters of all the songbird species each male sings more than one variant of the species-characteristicsong. This collection of song variants, which may range in number from two to several thousands according to the species, is referred to as the song repertoire of a male. One of the major sources of fascination about repertoires is their apparently excessive redundancy. Wilson (1975) suggests that redundancy is a characteristic feature of most if not all animal signals and the elaborate repertoires of many birds seem to represent an extreme example of redundancy. Many signals appear redundant in the sense of monotonous repetition; song repertoires are “redundant” in the sense of exhibiting seemingly needless variety. Apparent redundancy in animal signals may be less puzzling if displays are viewed as having evolved to manipulate receivers rather than transmit information about the sender: the analogy between bird song and persuasion or advertising proposed by Dawkins and Krebs (1978) makes the Occurrence of repertoires more plausible (repetition and redundancy increase the effectiveness of commercial advertising), but it is still hard to imagine and formulate testable hypotheses about the selection pressures leading to the evolution of a territorial “keep out” or mate attraction signal consisting of hundreds of different song types or song sequences. It might be argued that the great complexity of repertoires when compared with other kinds of signals is illusory rather than real. It is relatively easy to think of ways of gaining an estimate of the complexity of the repertoire of a mockingbird (Mimus polyglottis), but much more difficult to compare this with a

VARIATION IN BIRD SONG

145

complex visual signal such as the plumes of a bird of paradise. However there can be no doubt than many song repertoires are extraordinarily complex, and that the functional interpretation of this complexity is still in its infancy. Any discussion of song repertoires must begin with an admission of the practical problems involved in measuring and comparing the repertoires of different species. These problems can be divided into four categories in increasing order of difficulty: ( a ) The sampling problem: In species with very large repertoires it is not always possible to be sure that all the song types or phrase types have been recorded. The size of the repertoire can, however, be estimated by a cumulative plot analogous to that used in measuring home range size (Odum and Kuenzler, 1955). One limitation of this method is that it runs into difficulties if the repertoire changes with time. (b) The unitproblem: In buds that are “discontinuous singers” [e.g., the chaffinch (Fringilla coelebs) and song sparrow (Melospiza mefodia)]the recognition of song types is usually unequivocal. There may be a problem if different repetitions of the same song type by an individual vary, but usually the variability within a song type is much less than that between types. But in rambling and continuous singers, the elements analogous to “song types” of discontinuous singers may be less obvious. The way in which a bird uses its repertoire (for example, matching to playback of phrases) may be taken as a guide to the nature of the basic units which can be treated as song types, or it might be possible to use interphrase intervals as a criterion for defining “songs” (Isaac and Marler, 1963). ( c ) The compurubiliry problem: Even if it is agreed that the repertoires of two species contain a certain number of song types, there is a difficulty in making direct comparisons of repertoire size, since the units may vary in complexity between species. For example, the song of a European wren (Troglodytestroglodytes) is an elaborate series of trills lasting about 5 sec, while the song of a chiff-chaff (Phylfoscopuscollibyta) is a two-note phrase lasting less than 1 sec. (d) The Complexity problem: This is an extension of the last point. The complexity and number of individual song types is only one aspect of assessing repertoire diversity to make cross-species comparisons. Our subjective assessment of the complexity of the song of a particular species depends also on the sequential organization of songs during a bout of singing. Thus a species that switches often between song types appears to the human ear to have more complex singing behavior than one which repeats the same song type hundreds of times before switching. Kroodsma and Verner (1978) discuss this problem in more detail and suggest various indices of repertoire complexity. We raise these four problems not because they should prevent further discussion of repertoires until they are resolved, but because they will have to be considered seriously in comparative studies of repertoire size. Repertoire size and complexity clearly vary greatly between species as well as between populations or individuals within a species, and these variations provide one of the basic methods for understanding the functions of complex repertoires.

146 B.

JOHN R. KREBS AND DONALD E. KROODSMA

CONTRIBUTE TO SURVIVAL OR How Do REPERTOIRES REPRODUCTION ?

Three methods have been used to investigate the “function” of a behavior pattern: interspecific comparisons in which differences between species are related to ecological and life history variables; intraspecific comparisons relating variations between individuals to variations in survival, reproductive success, or success in acquiring resources; and direct experimental tests of the effect of a behavior. All three methods have been applied to the study of how selection favors repertoires.

I . Repertoires and Female Choice The evolution of elaborate male displays in general is often said to result from selection pressures arising from competition between males for females. This competition could take the form of either direct female choice, or male-male competition for resources which are in demand by females, or male-male competition for access to females. The characteristic of sexual selection operating through female choice is that it leads to a runaway development of elaborate male displays because of positive feedback (Fisher, 1958). Once female preference for a particular trait has been established (because males possessing the trait were in some sense better mates), the preference itself exerts selection since females showing the preference will produce attractive sons. There are numerous unresolved controversies surrounding the theory of sexual selection (Halliday, 1978). For example, the genetic variance of any trait subject to strong directional selection will be rapidly exhausted, at which point females will gain no advantage by attempting to choose males who will produce attractive sons. Notwithstanding this and other problems, it seems likely that the extreme elaboration of song repertoires is often the result of sexual selection. Darwin recognized that the intensity of selection exerted by female choice depends on how much males stand to gain by being chosen. In polygynous or promiscuous species males probably stand to gain more than in a monogamous species, so sexual selection is expected to be more intense in the former than in the latter. Thus, for example, plumage dimorphism and conspicuous male adornments tend to be more highly developed in polygamous than in monogamous birds (Baker and Parker, 1979). Two studies have attempted to apply this reasoning to bird song repertoires. Kroodsma (1977a) compared the song repertoires of nine species of North American wrens (Troglodytidae) and found that after taking into account factors such as variations in repertoire size with population density, polygynous wrens (e.g., marsh wren Cistothorus palustris) tend to have more elaborate repertoires than their monogamous counterparts (e.g., canyon wren Catherpes mexicanus). Catchpole (1980) on the other hand found that among six European Acrocephalus warblers the two polygynous species had smaller repertoires and simpler songs than the four that were monogamous. Catchpole ex-

147

VARIATION IN BIRD SONG

plains the discrepancy between his results and Kroodsma's with an athletic piece of sociobiological theorizing. He points out that females do not always choose between polygynous males on the basis of their displays: they may choose males with good territories. While this could explain why the polygynous warblers do not have very elaborate repertoires, it does not explain why they are less elaborate than those of the monogamous species. Catchpole's suggestion is that the monogamous males compete strongly for the first females to migrate back to the breeding grounds, and that female choice is based on male display characteristics because the territories of the four monogamous species are small and do not contain resources such as food which might limit female reproductive success. Catchpole's study shows that any attempt to test by interspecific comparison the idea that repertoires are a product of female choice must take into account the ecological factors limiting female reproductive success. In order to test his post hoc interpretations of the warbler data it will be necessary to use Catchpole's reasoning to predict repertoire diversity in another group. Intraspecific correlations between repertoire size and mating success are summarized in Table I. In two monogamous species with very elaborate repertoires (mockingbird and sedge warbler) males with larger repertoires pair earlier [as pointed out by Fisher (1958), early pairing is a possible way in which males might benefit from sexual selection in a monogamous species], although in both studies age is a possible confounding variable. Repertoire size is known to increase with age in some birds, including the mockingbird (J. Baylis, personal communication), canary (Serinus cunarius) (Nottebohm and Nottebohm, 1978), and redwinged blackbird (Yasukawa et al., 1980), and older birds in nearly all species that have been studied have a higher breeding success than young ones. In the great tit (Parus major), which is also monogamous but has a small

STUDIES IN WHICH

Species''

A

TABLE I CORRELATION BETWEEN REPERTOIRESIZE AND SOME MEASURE OF MATING SUCCESS HAS BEENSTUDIED Measure of success (correlation: positive, 0, negative)

Approximate repertoire size (song types) ~

Mockingbird Sedge warbler Great tit Redwinged blackbird

Marsh warbler

100

100 2-8

6 100

~~

~

Territory quality Pairing date (positive) Pairing date (positive) Pairing date (0) Clutch size Pairing date (positive) Harem size Pairing date (0)

Age a confounding variable? -

~~

Yes No? No Yes ?

"References: Mockingbird, Howard (1974); sedge warbler, Catchpole (1980); great tit, Krebs eta/. (1978); redwingedblackbird, Yasukawa eta/.(1980); marsh warbler, Dowsett-Lemaire(1979).

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JOHN R . KREBS AND DONALD E . KROODSMA

repertoire, there is no relationship between repertoire size and either pairing date or female quality as indicated by clutch size and hatching success. In this study age was taken into account. In the polygynous redwinged blackbird there appears to be a correlation between pairing success and repertoire size, although once again age could be a confounding factor (Yasukawa ef al,, 1980), Where age is correlated with repertoire size females might use large repertoires as a means of identifying older males. These males could be preferable as mates either because they are more experienced or because they have demonstrated their ability to survive, a trait which would be beneficial to the female’s offspring. The first possibility seems quite feasible, especially in species with male parental care and in which feeding efficiency increases with age. The second idea runs into the difficulty mentioned earlier, that genetic variance for a strongly selected trait such as longevity would be probably rather small. If females select older males as mates using large repertoire size as a proximate cue, younger birds will be at an advantage if they can rapidly acquire a large repertoire, so that repertoire size may not persist as a reliable indicator of age, However the fact that repertoire size is correlated with age in some species might indicate a constraint on the speed with which males can acquire songs. Thus the possibility remains that females could use larger repertoires as a cue for identifying older, more experienced males. As with other sexually selected traits, once an initial preference has been established, the Fisher effect would reinforce the preference of females for large repertoires, Only one study so far has attempted to demonstrate experimentally that females discriminate between repertoires of different sizes (Kroodsma, 1976a). Kroodsma did not study female choice, but showed that female canaries are more likely to be stimulated to build nests when exposed to playback of lwge repertoires than playback of artificially simplified repertoires, The inference is that a large repertoire is more effective in stimulating female reproduction and hence in attracting a female in the first place. However Kmodsma’s nsults could be interpreted in several ways. ( a ) The results might reflect a female preference for large repertoires. Since repertoire size in canaries increases with age, €emales choosing large repertoires would acquire older, more experienced mates. ( b )The artificial simple songs may have been too simple to be recognized by the females as canary song. (c) The large repertoires may by chance have contained song elements which are particularly effective in stimulating females, although this seems rather unlikely. 2 , Repertoires and Competition between Males Song in many birds is intimately associated with territorial defense, and numerous authors have suggested that repertoires play an important role as a m i t o rial signal. However most of the evidence supporting this view is circumstantial and consists of descriptions of the ways in which repertoires are used during

149

VARIATION IN BIRD SONG

interactions between rival males or in spontaneous song. Before discussing this indirect evidence we will refer to a study that has attempted to test directly whether song repertoires increase the effectiveness of song as a territorial signal. a . Do Males with Large Repertoires Have More Success in Territorial Competition? The great tit has a song repertoire of (usually) one to eight song types, and Krebs et al. (1978) tested the effectiveness of different-sized song repertoires in territory maintenance. They removed territorial pairs during early spring and “occupied” the empty territories with loudspeakers broadcasting song repertoires of one, three, six, and nine song types. The results of three experiments demonstrated that repertoire-occupied territories are invaded more slowly by new birds than those ‘‘occupied’’ with a single song type, and that the additional deterrent effect of a repertoire over a single song increased with repertoire size (Fig. 1A and B). Yasukawa (1981) has recently shown in a similar experiment that large repertoires are more effective than single songs in deterring intruders in the redwinged blackbird. In the great tit, males with repertoires of four or more songs are more likely to produce young surviving to breed than are males with one to three song types (repertoire size is not age related in the great tit) (Fig. IC). This difference in fitness arises because males with larger repertoires fledge heavier young (Fig. ID) and survival of young is closely correlated with fledgling weight. Although the exact determinants of this relationship between fledgling weight and repertoire size are not known, the most likely mechanism is that males with larger repertoires obtain better territories (McGregor et al., 1980). Repertoire size and reproductive success could both be correlates of “male quality. However, McGregor et al. failed to find any correlation between repertoire size and four measures of male quality: body size, fledging weight, hatching date, and age. Thus in the great tit there is evidence both for the effectiveness of repertoires in territory maintenance and for increased fitness of males with larger repertoires, perhaps related to territory quality. It is not clear why larger repertoires make better “keep out” signals. Among the possible interpretations are that the larger repertoires contained by chance songs with particularly good carrying properties, or that larger repertoires indicated a more experienced resident. (This latter possibility seems unlikely since repertoire size is not age related in the great tit.) The explanation favored by Krebs et al. was that repertoires decrease habituation in listeners, and that this is related to density assessment by nonterritorial birds (see Section II,B,2,d for more detailed discussion). Another question raised by this and other studies that show an advantage for large repertoires is that of the constraints on repertoires size. We will return to this point in Section II,B,S. b. HOM~ Arc Repertoires Used in Competition betweeti Males? Although the evidence discussed is the most direct indication that repertoires increase the ”

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JOHN R. KREBS AND DONALD E. KROODSMA

Control Single song Repertoire

A

B

Daylight hours after start of experiment

Number of songs i n repertoire

Others n = 32

2

1

2

3

4

5

P 0.02

w n

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’ fl 5LLLLb Fathers n-29

-

1

2

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4

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6

0

0

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2 3 4 Repertoire size

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Repertoire size

FIG. 1. (A) The results of an experiment in which pairs of great tits were removed from their territories and replaced with loudspeakers broadcasting song repertoires of different sizes, or single song types. The percentage of area invaded by new birds is shown as a function of time since the start of the experiment. The new birds tended to settle f i s t in the control area (no songs), then in the single song area, and finally in the area occupied by song repertoires. (Krebs er al., 1978). (B) In three different experiments of the type shown in (A), different sized repertoires were compared with single song types. The extra deterrent effect of a repertoire increases with number of song types in the repertoire. The experiment shown in (A) is the one with nine song types. (C) Male great tits which produce young surviving to breed (“fathers”) have larger song repertoires than other males. The data were collected from 1975 to 1979 in Wytham Wood near Oxford. All the great tits breeding in the area and their young are ringed each year. Studies of dispersal (Greenwood et al., 1979a) show that birds do not usually disperse more than a few hundred meters from their birth site, so the results shown here cannot be a reflection of differential dispersal. There are no differences in clutch size, breeding date, or hatching success which correlate with repertoire size (McGregor et al., 1980). (D) Male great tits with larger repertoires tend to fledge more young which are heavier than average for

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effectiveness of song in competition between males, there are a number of suggested mechanisms by which this effect could be brought about. When it is correlated with age, repertoire size could be used as a cue for assessment of a rival's fighting experience, assuming that cheating is not possible because of the time needed to learn a large repertoire. Apart from this suggestion, there are two other ways in which repertoires could play a role in territorial interactions. The different songs could carry different messages, or repertoires might reduce the habituation rate of listeners. These two ideas are not necessarily mutually exclusive. c. Different Songs Used in Different Contexts. One of the conclusions of Tinbergen's (1959) classical studies of territorial displays in gulls was that different kinds of display given to intruders signal different probabilities of attack by the territorial resident. Different song types in the repertoires of some species may act in an analogous way (Lein. 1978; Smith er at., 1978). Lein, for example, found in the chestnut-sided warbler (Dendroicu pensylvunicu) that three song types were used in the center of the territory where the resident is very likely to attack an invader, and three others were used at the edge where attack was much less likely. He proposed that this graded signaling system is important in establishing the positions of boundaries between territorial neighbors. The existence of signals indicating different attack probabilities is at first sight surprising in light of the theoretical analyses of animal conflict by Maynard Smith, Parker, and others (e.g., Maynard Smith and Parker, 1976; Caryl, 1979). These analyses suggest that it will normally be a stable strategy for contestants to conceal their exact attack tendency until the last possible moment, since any information about this tendency can be exploited by the opponent. However this conclusion may not apply to territorial contests, in which the resource (a territory) is divisible and the additional benefit gained by acquiring more resource decreases with each further addition (Krebs et al., 1980). In a number of species that have been studied the different song types are used equally in all parts of the territory (e.g., great tit, Krebs et a t ., 1978; redwinged blackbird, Smith and Reid, 1979), but there is another apparently widespread effect of context on the use of song types, which is referred to as song matching. Song matching occurs when a bird responds to playback or a rival with a song out of its repertoire that closely resembles the stimulus song. There have been a number of demonstrations of song matching both in natural song duels and in response to playback (references in Krebs et al., 1980), and the following functional interpretation has been proposed (Krebs et al., 1980). In the great tit, matching in response to playback is associated with a strong response as measured the season. Since fledging weight is a good predictor of survival (Penins, 1965) the effect shown in (C) probably results from the differences in fledging weight shown here (McGregor et al., 1980).

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by, for example, latency, close approach to the speaker, and total singing time, and matching in song duels occurs more often during intense than weak territorial interactions (Krebs et al., 1980). Krebs et al. suggest that different probabilities of matching by a resident act to signal different levels of response to an intruder, in the same way as the different song types of the chestnut-sided warbler studied by k i n . Related to this idea is Bremond’s (in Armstrong, 1973) suggestion that by matching a resident directs its “keep out” signal at a particular intruder. Kroodsma ( 1979) suggests a completely different interpretation of matching. He showed that when two hand-raised marsh wrens (Cistothorus palustris) engaged in countersinging, the subordinate bird (measured by direct attack behavior) tended to match the songs of the dominant, but the reverse was not true. When the song of the subordinate was amplified, the dominant male increased his matching. The conclusions suggested by this experiment are that loudness of song is correlated with dominance (perhaps it is a “reliable cue”-Dawkins and Krebs, 1978) and that matching is an indication of subordinate status, although the exact significance of matching in this case has not yet been established [one possibility is that matching is an asymmetric cue used to settle contests (Maynard Smith and Parker, 1976)l. When territorial male marsh wrens respond to playback, they tend to sing in anticipation of the tape (Verner, 1975) (i.e., they become entrained to the sequence of songs on the tape and keep ahead of the playback), which seems consistent with the idea that matching is a signal of subordinate status. d . Repertoires and Habituation. One of the most influential ideas in the study of song repertoires has been Hartshorne’s (1956, 1973) “antimonotony principle. The hypothesis is that diversity in a song sequence counters the monotony of a continuously repeated signal. It was based on interspecific comparisons of repertoire size and singing behavior, but much of the subsequent work has applied it to variations within species. Although Hartshorne ’s original suggestion was that song diversity reduces monotony for the singer, the more appropriate hypothesis for communication is that diversity reduces the rate of habituation in the listener. This hypothesis was confirmed in a study of the rates of habituation to monotonous song and varied song repertoires (Krebs, 1976), but the main attraction of the idea seems to have been that many features of repertoire organization make sense in the light of the hypothesis. These features can be summarized as follows: ”

1 . Interspecific comparisons show that there is a correlation between the tendency to sing continuously and the tendency to switch rapidly between songs (Hartshorne, 1973, criticized by Dobson and Lemon, 1975, vindicated by Kroodsma, 1978a). 2. Within one species there is a tendency for males to switch more rapidly

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between songs when they are singing more continuously (Kroodsma and Verner, 1978). 3. In some species, the probability of switching between song types increases when an intrusion into a male’s territory is simulated by playback (Falls and Krebs, 1975) or when a rival sings (Kroodsma and Verner, 1978). 4. The song types in the repertoire of an individual are more variable than expected if they were drawn at random from the total population of song types in the area, variability being measured by arbitrarily chosen parameters (Krebs, 1976; Whitney, 1979). 5 . Successive song types used in a sequence of singing are more different with respect to certain measurable parameters than expected if songs were used at random (Kroodsma, 1975; Whitney, 1979; Verner, 1975). 6. In switching between song types, birds avoid low recurrence numbers. The recurrence number is the number of switches in song type between two repetitions (or bouts) of the same type: the sequence ABA has a recurrence number of two (Falls and Krebs, 1975; Todt, 1975; Krebs, 1976; Whitney, 1979; Kroodsma, 1975, but see Smith and Reid, 1979). Two main features of repertoire organization appear at first sight to be incompatible with Hartshorne’s hypothesis. The first is that in many species a bird repeats each song type in its repertoire a large number of times (perhaps hundreds of times) before switching. Some possible factors favoring repetition of song types in bouts are discussed by Krebs (19781, but there is currently no good evidence for hypotheses to account for the differences between species in tendency to repeat the same song many times in succession (see also Section II,B,5). A comparative study would probably pay dividends. The second feature is that in some species song types are not used with equal frequency (e.g., chaffinch, Slater, 1980). If repertoires promote variety, it is not easy to see why some songs should be sung more often than others, although if the repertoire is also used in song matching, the frequency of use of a song type could be related to the types possessed by neighbors and intruders. Although the habituation hypothesis is consistent with many features of repertoire organization, it is inadequate on its own as a functional account. This is because it uses a causal mechanism (habituation) to answer the functional question of why repertoires evolve. The functional answer has to explain why habituation occurs. While it could be argued that habituation is a property of all nervous systems, which arises because it is generally advantageous to ignore repeated stimuli, it is known that habituation rates vary between contexts. There is therefore no reason to suppose that the rate of habituation cannot be adjusted to an appropriate level for a particular context by natural selection. From a functional point of view, habituation by females could be seen as a mechanism whereby a female chooses large repertoires, and habituation by males might be a proximate

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mechanism by which birds avoid settling in densely populated habitats (Krebs, 1977a,b). The number of song types heard in an area is an indication of the density of territorial birds, so that by habituating more rapidly to fewer songs, the settler will choose areas of low density. According to this idea, repertoires are seen as a form of bluff, in which temtory owners discourage new settlers by simulating the presence of many individuals. The two main conceptual problems posed by this idea are ( a ) whether bluff is evolutionarily stable: the answer here seems to be that a limited amount of bluff is stable in contests with imperfect information about rivals (Maynard Smith and Parker, 1976; Hammerstein, 1980) and ( b )why repertoires do not become larger and larger as bluff escalates. This is a difficult question which applies to any hypothesis about the selective advantage of a large repertoire: this will be discussed in Section II,B,S. In summary, Hartshorne’s idea, which was originally applied to interspecific comparisons, seems to account for many features of repertoire organization, and it can be interpreted in functional terms both for female choice and for male-male interactions.

3 . Repertoires, Individual and Kin Recognirion a . Recognition of Neighbors. It is well established that territorial songbirds of some species recognize the song of their neighbors and can discriminate between familiar and unfamiliar songs. Individual recognition of voice is also well established in the use of simple calls, for example, between parents and offspring (Beer, 1970). It seems clear that repertoires do not play an important role in this kind of individual recognition. First, the clearest demonstrations of neighbor-stranger discrimination have been in species with only one song type per male (e.g., Falls, 1969), and some studies of repertoire species have produced equivocal results (Kroodsma, 1976b; Pickstock and Krebs, 1980). Second, it could be argued that repertoires actually reduce the chances of individual recognition, especially since repertoires may contain songs which are more different from one another than expected by chance (see previous section). Further, individual recognition must be based in features of song which are invariant within and differ between individuals (Brooks and Falls, 1975). b. Recognirion of Kin. Regardless of whether or not repertoires are important for recognition of individual neighbors, they could play a role as “family badges, ” allowing the recognition of classes of individuals of different degrees of relatedness (Treisman, 1978). The advantages of kin recognition to females could be avoidance of inbreeding in mate choice, and for males reduced conflict between individuals sharing territorial boundaries (Maynard Smith, 1978; Grafen, 1979, for theoretical analysis). Transmission of learned song repertoires from father to son would be a parsimonious mechanism for acquiring a family badge, and a large repertoire would allow detailed genealogical information to be encoded in the song (Treisman, 1978). If kin recognition proved to be an

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important consequence of song repertoires, song learning in general could be interpreted in the same way. Just as Bateson (1978) has argued that avoidance of inbreeding may be an important functional consequence of imprinting, so kin recognition could be a general explanation of why birds learn to sing. Unfortunately the small amount of evidence available does not support the kin recognition hypothesis. In a detailed field study of transmission of songs from father to son in great tits (McGregor et al., 1980), there was no evidence that fathers and sons are more likely than expected by chance to share song types, and no evidence that male close relatives breeding in neighboring territories have enhanced success (Greenwood et ul., 1979b). Female great tits did not show any tendency to avoid mating with males possessing song patterns resembling those of the female’s father. Jenkins ( 1977) showed that young male saddlebacks (Philesturnus curunculurus) sing the songs of neighbors when they first set up a territory, and do not include fathers’ songs in their repertoire. Similarly, in the Bewick’s wren (Thryornunes bewickii) the great majority of songs in the repertoires of young males resembled those of neighbors in the place where the youngsters first set up their territories (Kroodsma, 1974). Thus the field evidence offers no support for the idea that sons and fathers sing similar song types, although it is still possible that some can recognize their father’s songs (see also Section III,B,3). Laboratory studies of zebra finch ( f o e p h i f aguttutu) (Immelman, 1969) and bullfinch (Pyrrhuln pyrrhula) (Nicolai, 1959) have shown that young males can learn songs from their fathers, but since in the wild a young bird will be exposed to many different songs, no conclusion can be drawn about selective learning of parental song types. In the zebra finch, females can also recognize their father’s song, but it is not yet known whether this recognition is important in mate choice (Miller, 1979). 4 . Repertoires mid Mimicry

Some species include elements mimicked from other species or from inanimate sounds in their song repertoires. Mimicry,’ meaning the copying of sounds other than species-specific vocalizations, is probably very widespread. Detailed analysis often reveals unsuspected cases (e.g., Guttinger, 1977), and there is almost certainly a continuum from species which occasionally mimic the sounds of other birds [e,g., great tit (J. R. Krebs, unpublished observation) and blackbird (Turdus rnerulu) (Tretzel, 1967)] to those with a repertoire constructed largely or entirely of mimicked sounds [e.g., lyrebird (Menuru superba) (Robinson, 1975) and marsh warbler (Acrocephulus pdustris) (Lemaire, 197511. Further, the amount of mimicry shown by a species may vary greatly according to ‘See Dobkin (1979) for a detailed discussion of terminology.

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the context: Bertram (1970) showed that mynahs (Gracula religiosa), which are well known for their mimicking powers in captivity, mimic hardly at all in the wild, although they do copy sounds of conspecifics. The conclusion seems to be that at a descriptive level mimicry cannot be viewed as distinct from other kinds of song learning, but rather that it is just one way of acquiring a song repertoire. The ontogeny of mimicked and other learned songs also provides no clearcut grounds for distinguishing between the two. The males of some nonmimicking species [e.g., chaffinch (Thorpe, 1961)] learn their repertoires in the first year and do not subsequently change them, while others (e.g., saddleback, Jenkins, 1977) can change their repertoire at a later stage according to the predominant song types of neighboring birds. Similarly some mimicking species acquire their songs early in life (e.g., Viduines, Nicolai, 1964) while others can continuously modify their repertoire of mimicked sounds [e.g., greenfinch (Chloris chloris) (Giittinger, 1977) and starling (Sturnus vulgaris) (J. R. Krebs, unpublished observation)]. Are there grounds for treating mimicry as a special case in functional terms? At least four hypotheses about the function of mimicry have been put forward [see also Dobkin (1979) for further discussion]. a. Mimicry Is a Method of Acquiring a Large Repertoire. According to this view mimicry itself has no special significance. When large repertoires are favored, for example, by sexual selection (Section II,B,l), males may acquire a large repertoire by indiscriminate copying of sounds in the environment (Howard, 1974). This view is not incompatible with other hypotheses, since the initial factor leading to female preference for mimicked repertoires could have been an advantage associated with interspecific territoriality (see Section II,B,4,b or II,B ,4,c). h. Mimicry Is Important in Interspecifc Territoriality. Cody (1974) proposed that on an evolutionary time scale species competing for resources and defending interspecific territories might develop similar territorial signals including song (so-called character convergence). The same effect on an ontogenetic time scale could account for song mimicry. For example, the mockingbird is a generalist feeder which defends interspecific territories (Moore, 1978) and mimics the songs of many of its competitors (J. Baylis, personal communication). The catbird (Dumetella carolinensis) and chorister robin (Cossypha dichroa) (but not the lyrebird, which is a specialist feeder) could be similar examples of generalist feeders showing interspecific territorial aggression (Harcus, 1977b). Harcus (1977b) proposes a slight modification of the hypothesis: he suggests that interspecific mimicry is a form of acoustical interference between competing species. c . Mimicry Is a Form ofDeception. One of the classical forms of mimicry is Batesian mimicry, in which a palatable organism deceives a predator by resembling a noxious or well-defended species. Rechten (1978) has proposed a

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similar hypothesis for bird song mimicry. She points out that a number of mimicking species copy predators or large heterospecific competitors, and it is often clear that the mimicked species show no reaction to playback of the mimic songs (excluding the possibility of the previous hypothesis). However, the mimicry could be directed at other members of the mimic species. By copying the sounds of enemies and competitors the mimic reduces the apparent suitability of the habitat to its conspecific rivals in a way analogous to that proposed by Krebs ( 1977a) for song repertoires in general. While there is no evidence in support of this idea, one clear example of interspecific vocal deception is the thick-billed euphonia (Euphonia laniirostris) which mimics the mobbing calls of other species nesting near its breeding site, thus inducing them to mob a predator while the euphonia sits at a safe distance (Morton, 1976). The vocal mimicry of their hosts by nestling viduine brood parasites (Nicofai, 1964) seems to be another clear case of vocal deception. (It is perhaps worth noting that we do not include the similar songs of interspecifically territorial birds as examples of deceptive mimicry .) d . Mimicry Plays a Role in Reproductive Isolation. The work of Nicolai (1964) and Payne (1973a) has established that the mimicry of its host by the parasitic paradise whydah (Viduu parudisea) is important in reproductive isolation. The Vidua species are in general highly specific in their choice of hosts and the male parasite learns part of his song from the foster father (Pytilia spp.). Payne (1973a) showed by choice experiments in aviaries that the female paradise whydah also learns the characteristics of the foster parent’s song, and prefers to approach the song of its host (P.rnelbu) rather than the song of the closely related P. phoenicopteru. The female does not distinguish between the P . melbu song and mimicked song of males of her own species. The inference is that females are drawn both to males of their own species (for mating) and to nests of their hosts (for egg laying) by song, and that song learning maintains the high degree of specificity of most Vidua parasites. C. M. Perrins (personal communication) has generalized this in an ingeneous account of mimicry in marsh warblers. The very large mimicked repertoire of this migrant species is made up of approximately 50% songs from the winter quarters in Africa and 50% songs from the breeding grounds in Northern Europe (Lemaire, 1975; Dowsett-Lemaire, 1979). It is well established that migrant warblers such as the marsh warbler find their way to Africa with the aid of an inborn magnetic compass (Gwinner and Wiltschko, 1978) and different populations of a species appear to have different preferred compass directions according to their exact migration route. Since the directional compass is inherited, both males and females benefit as a result of mating with a partner with the migratory direction. In this way the offspring will inherit an appropriate compass. Perrins suggests that females could identify the winter quarters of a male singing on the breeding grounds on the basis of mimicked songs. Dowsett-Lemaire(1979) notes

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that it is possible to recognize which part of Africa a male has visited by listening to the mimicked repertoire. Similarly the mimicked songs of European birds in the marsh warblers’ repertoire might indicate where a male has been reared or bred in previous years. Thus a female could identify the probable migratory direction of a male and choose a mate with a compass which matches her own. This idea of selective mating could have general significance even in nonmigratory species, since there is some evidence of nonrandom mating at dialect boundaries (see Section III,B,3), and in some species dialects are characterized by mimicry of the local avifauna (e.g., Guttinger, 1977). In conclusion there are plenty of hypotheses about the significance of vocal mimicry but virtually no hard data. 5 . Constraints on Repertoire Size

We have discussed a number of ways in which natural selection might favor large repertoires, all of which leave open the important question of what sets an upper limit to repertoire size. We can offer no simple answer to this question but we suggest that some of the following factors could be important. ( a ) Memory space: In species with repertoires of hundreds of different song types (which have probably arisen as a result of sexual selection) it is at least conceivable that the upper limit on repertoire size is set by the constraints of memory. Song learning is only one of many demands on the bird’s memory and ultimately there must be a compromise in how much is allocated to any one function. (b) Impact on fisfener: As discussed in Section II,B,l, to estimate the repertoire size of many species takes a lot of listening. Whether the repertoire is directed at potential mates, or rival males, the benefit derived from increasing repertoire size will cease when it is no longer possible to sing the complete repertoire in the average time that a responding bird stops to listen or when the listening bird no longer remembers all that it has heard (Krebs, 1977a). This might be important in, for example, migrant Acrocephalus warblers where song seems to be related to mate attraction and pairing can take place within a few hours of females arriving on the breeding grounds (Catchpole, 1980). (c) Tradeoff between variely and repetition: Krebs (1978) suggested two possible advantages in repeating a song many times before switching to a new type. First, detection of a repeated signal against a noisy background is more reliable, and second, ability of listeners to discriminate between successive songs may increase if they are repeated. If the singer can be viewed as trying to demonstrate the size of its song repertoire to a listener, these two factors will lead to a tradeoff between repetition and variety, with the optima1 balance depending perhaps on ecological factors such as distance between broadcaster and listener. Among the North American wrens, species which repeat each song type many times before switching tend to live in areas of high avifaunal diversity and low wren density (Kroodsma, 1977a). This

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is consistent with the idea that repetition is in some way related to the problems of detection or discrimination by listeners. These are rather general comments about the possible constraints on repertoire size, and, as we have emphasized earlier, differences between species are best thought of in terms of differences in ecology and life history. Variation between individuals of the same species within a population might be a reflection of age, learning ability, or experience.

III. GEOGRAPHICAL VARIATION A.

INTRODUCTION

Bird vocalizations, in common with many other morphological and behavioral traits, vary from one population to another (Thielcke, 1969; Lemon, 1975; Baptista and King, 1980). Geographical variations in vocal behavior may occur between isolated populations or among contiguous groups. In the latter instance, the chance may be a gradual cline, a rapid change over a restricted contact zone in which vocalizations are intermediate, or a sudden change with a sharp boundary separating the two populations. Most songbirds learn their songs. The pattern of fine scale (“microgeographical”) variation in any species depends on the extent and accuracy of this vocal learning, the distance of dispersal from the site of song acquisition to the breeding site, and perhaps to some extent on the number of song types learned. The ecological significance of microgeographical variation must be analyzed in terms of differences between species in these three factors. On the other hand, imitation, dispersal, and repertoire size probably have less influence on the differences in song occurring over longer distances and between populations which do not normally mix. These macrogeographical variations may often be related to ecological factors such as the effects of sound propagation or attenuation in different habitats (Chappuis, 1971; Morton, 1975; Waser and Waser, 1977; Marten and Marler, 1977; Marten et al., 1977; Michelson, 1978; Wiley and Richards, 1978; Richards and Wiley, 1980; Bowman, 1980; Hunter and Krebs, 1979), the total sound environment of the local avifauna (Cody, 1969; Brown, 1977), or simply body size changing with latitude or altitude (Lanyon, 1978). We will focus in this section on microgeographical variation, and examine first the two factors which most significantly influence local spatial variation in bird song: the extent and accuracy of imitation and the site of song imitation with respect to the site of breeding. Next we will discuss the relationship between genetic separation of populations and song variations, and the influence of song

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repertoire size on the ability to establish or maintain sharp discontinuities in song traditions between neighboring populations. Finally, we will discuss the usefulness and definition of the term "dialect" and the functional significance of vocal imitation and its influence on song dialects. B. MICROGEOGRAPHICAL VARIATION I,

Extent and Accuracy of Imitation

Imitation of adult songs appears to play an important role in the development of normal wild-type songs in all species of songbird so far studied in the laboratory (Thorpe, 1958; Marler, 1970; Nottebohm, 1972; Lemon, 1975; see Kroodsma, 1977b, for a review of this particular point). In some species, imitation is so precise that distinguishing the model from the copy can prove very difficult: e.g., chaffinch (Thorpe, 1958), white-crowned sparrow (Zonotrichia leucophrys, Marler, 1970), cardinal (Cardinalis cardinalis, Dittus and Lemon, 1969), swamp sparrow (Melospiza georgiana, Marler and Peters, 1977), and marsh wren (Kroodsma, 1978b). In the field, inferences regarding the accuracy of imitation may often be made from studies of spatial variation of songs in a local population. Neighborhoods in which males share identical, relatively complex songs are an indication of accurate imitation. [Simple vocalizations which occur among all birds in a population may be under genetic control and develop without imitation-"songs" of Myiarchus flycatchers may be a good example (see Lanyon, 1978).] However, differences in the songs of neighbors could be a result of precise imitation together with dispersal from that site of vocal learning (see Section III,B,2), so that in the songs of neighbors one is not comparing the model with the copy. This may be the case with the white-throated sparrow (Zonotrichia albicollis), where no evidence of vocal imitation or microgeographical song variation can be found in nature (Borror and Gunn, 1965; Lemon and Harris, 1974), yet males in the laboratory acquire good copies of model songs (Thorneycroft, 1967). Marked differences in the songs of neighboring males could also indicate that improvisation (or invention) plays a greater role than imitation in song development. For example, neighboring male sedge wrens (Cisrothorusplatensis) share very few songs in their repertoire of approximately 100 types, even though all songs unmistakably identify the species. Sedge wrens in the laboratory do not imitate songs from training tapes; but isolated, tutored males develop songs that are not very different from those of wild birds. The difference between species that improvise and those that imitate may be related to differences in site fidelity. The sedge wren is much less sedentary than the congeneric marsh wren, which extensively imitates tutor tapes in the laboratory (Kroodsma and Verner, 1978),

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and it would be interesting to see if this pattern is also found in other species groups. 2. Site of Sorig Imitation If precise imitation is the usual form of song development for young males in the wild, then the extent of dispersal from the site of song imitation to the breeding territory will largely determine the local spatial distribution of song patterns. The site of song imitation may in some species be the natal site, but probably males more usually learn their songs at the time of breeding or territory establishment (some species may learn at both sites). This can be inferred from the fact that in many species neighboring territorial or displaying males have nearly identical song repertoires, while songs change rapidly over relatively short distances (Table II). Information on dispersal in birds suggests the general pattern is for males to disperse some distance between the birthplace and site of first breeding, and very little thereafter (Greenwood et al., 1979a). Therefore when neighbors share song types they have probably learned them from one another. Detailed data documenting the site of song learning are available from studies of individually marked birds in a few species. In village indigo birds, for example, Vidua chalybeara, Payne (1975) found that adult males may move from one “call site” (group of song posts used by a male) to another, changing the entire song repertoire in the process; thus the site of effective imitation is the location where the male will be competing with other conspecifics for mates (i.e., the breeding site). A similar system occurs in the saddleback (Jenkins, 1977). Jenkins observed that when a new song type arose in a confined area, it was learned by long established neighboring birds whose repertoires had previously been thought to be stabilized. He also found that when adult birds moved from one territory to another they changed their song types to match those of their new neighbors. Some of these changes could however have been due to a change in the relative frequency with which birds sang different songs rather than to learning of a totally new song type. While young birds are seeking a territory, they might wander over a wide area and learn song variations from all parts of the population. Thus when a male encounters neighbors with a different song type, it can select from its repertoire the appropriate song to sing. Evidence for such infrequently used song components exists for the Bewick’s wren (Kroodsma, 1974). Here, as in the indigo bird and the saddleback, males sing songs which are typical of the locality where breeding occurs. Juveniles may disperse from the birthplace by 60 days of age, and by 80 days may have already established a territory and started to sing song components which are typical of, and unique to, neighboring territorial males. One first year bird, however, was shown to possess a single song component which had probably been learned from its father (see Section II,B,3), but which was never used in normal singing.

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TABLE I1 BIRDSPECIES IN WHICHVOCALIZATIONS VARYON

A

MICROGEOGRAPHICAL SCALE"

Species Psittaciformes Psittacidae Orange-winged amazon parrot (Amazonia amazonia) Apodiformes Trochilidae Little hermit (Phaethornia longuemareus) Passeriformes-suborder passeres (songbirds) Alaudidae Flappet lark (Mirafra rufocinnamomea) Hirundinidae B m swallow (Hirundo rustica) Laniidae Bou-bou shrike (Laniarius aethiopicus major) Southern bou-bou shrike (Laniarius ferrugineus) Troglodytidae Rock wren (Salpinctes obsoletus) Long-billed marsh wren (Cistotbrus palustris) Bewick's wren (Thryomanes bewickii) Carolina wren (Thryorhorus ludovicianus) European or winter wren (Troglodytes troglodytes) House wren (Troglodytes aedon) Mimidae Catbird (Durnetella carolinensis) Mockingbird (Mimus polyglottos) Muscicapidae (Turdinae, Sylviinae) Blackbird (Turdus merula) Redwing (Turdus iliacus) Mistle thrush (Turdus viscivorus)

Reference

Nottebohm (1970)

Snow (1968); Wiley (1971)

Seibt (1 975); Payne (19 7 3 ~ )

M. McVey (personal communication) Thorpe (1972); Hooker and Hooker (1969)

Harcus (1 977a)

Kroodsma ( 1975) Vemer (1975) Kmdsma ( 1974)

E.S. Morton (personal communication) Kreutzer (1973, 1974); Kroodsma (1980) Kroodsma (1973, also unpublished data)

Thompson and Jane (1 969) Wildenthal (1965)

Tretzel ( 1967) Bjerke (1974) Isaac and Marler (1963)

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TABLE I1 (continued) ~

~~

~~

Species American robin ( Turdus migraforius) Marsh warbler ( Arrocephalus palustris) Bonelli’s warbler ( Phylloscopus bonelli) Goldcrest (Regulus rrgulus) Firecrest ( R r ~ u l uignicapillus) s Hunter’s warbler (Cisticola humeri) Paridae Great tit (Parus major) Plain titmouse (Parus inormtus) Black-crested titmouse (Parus atricristatus) Certhiidae Short-toed tree creeper (Certhia hrachydactyln) Tree creeper (Certhio Jamiliaris) Necteriniidae Splendid sunbird (Nrcterinia coccinigastra) Emberizidae Yellow bunting (Etnberiia citrinella) Ortolan bunting (Emberim hortolana) Snow bunting (Plectrophenax nivalis) Fox sparrow (Possrrellu (=Zonotrichia?) iliaca) Song sparrow (Melospiza ( =Zonotrichia?) melodiu) Swamp sparrow (Mrlospiia f =Zonotriehia:>)gror~iana) Rufous-collared sparrow (Zonotrichia capensis)

Reference

Konishi (1965) Lemaire ( 1975) Bremond ( 1976) Becker (1977 a,b) Becker ( I 977a.b) Todt ( 1970)

Gompertz (1961); Hunter and Krebs (1979); McGregor ef al. (1980) Dixon ( 1969) Lemon

(

168)

Thielcke 1961. 1965, 1969) Thielcke 1961, 1969)

Grimes (1974); Payne (1978)

Kaiser ( 1965) Conrads ( 1976); Conrads and Conrads ( I97 I ) Tinbergen ( I 939); Chapman in Gatty (1 958) Martin ( 1977, 1979) Harris and Lemon ( 1972); Eberhardt and Baptista I 1977)

D.E. Kroodsma (unpublished data) Nottebohm (1969. 1975); King (1972)

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E. KROODSMA

TABLE I1 (continued) Species White-crowned sparrow (Zonotrichia leucophrys) Darkeyed junco (Junco hyemalis) Savannah sparrow (Ammodramus sandwichensis beldingii) Vesper sparrow (Poeecetes gramineus) lndigo bunting (Passerina cyaneu) Lazuli bunting (Passerina amoena) Rufous-sided towhee (Pipilo erythrophthalmus) Cardinal (Cardinalis cardinalis) Pyrrhuloxia (Pyrrhuloxia ( =Cardinalis?) sinuata) Rose-breasted grosbeak (Pheucticus ludovicianus) Vireonidae Solitary vireo (Vireo solitarius) Yellow-throated vireo ( Vireojlavifrons) Icteridae Red-winged blackbird (Agelaius phoeniceus) Cacique (Cacicus cela) Bobolink (Dolichonyx oryzivorous) Fringillidae Chaffinch (Fringilla coelebs) Greenfinch (Chloris ( =Carduelis?) chloris) European siskin (Carduelis spinus) Pine siskin (Carduelis pinus) American goldfinch (Curduelis tristis) Twite (Carduelis (=Acanthis?)ji’avirostris) Cassin’s finch (Carpodacus cassinii)

Reference

Marler and Tamura (1962) Baptista (1975); many others Williams and MacRoberts (1977) Bradley ( 1977) Kroodsma ( 1 972) Thompson (1970); Emlen et al. (1975) E d e n et al. (1975) Kroodsma ( I97 1 ); Ewert ( 1978) Lemon (1966, 1975) Lemon and Herzog ( 1969) Lemon and Chatfield (I 973)

James (1973, 1976) James (1973, 1976)

E.S. Morton (personal communication) Feekes ( I 977) Avery and Oring (1977)

Marler ( 1 952); Metzmacher and Mairy (1974) Giittinger (1974, 1977) Mundinger ( 1970) Mundinger (1970) Mundinger ( 1970) Marler and Mundinger (1975) Samson ( 1978)

165

VARIATION IN BIRD SONG TABLE I1 (continued) Species House finch (Carpodacus mexicanus)

Pine grosbeak (Pinicola enuclearor) Bullfinch (Pyrrhula pyrrhula) Plocediae Village indigobird (Vidua chalybeata) Sturnidae Indian hill mynah (Cracula religiosa) Callaeidae Saddleback (Philesturnus ( =Creadion?) carunculatus) Corvidae Blue jay (Cyanocirta cristara) ____

Reference

Mundinger ( 1975); Bitterbaum and Baptism (1979) Adkisson (personal communication) Nicolai ( 1 959); Wilkinson and Howse ( 1 975)

Payne (1973b)

Bertram ( 1970)

Jenkins ( 1977)

Kramer and Thompson (1979)

~~

‘l In these species, songs of neighbors are more similar to one another than they are to the songs of more distant conspecifics.

Instead the young male had adopted a song component similar to that of neighboring males and abandoned the one learned from its father. Thus, indigo birds and saddlebacks may disperse as adults and modify their song repertoire to match the song types of other adults with which they interact. Juvenile Bewick’s wrens can probably imitate their father’s songs, but after dispersing to their permanent breeding territory, additional songs are acquired or the father’s songs are modified to conform to the local song neighborhood. The end result in all three species is that neighbors have similar songs. 3 . Microgeographical Variation and Genetic Isolation

It has been suggested by a number of authors (Marler and Tamura, 1962, 1964; Nottebohm, 1969) that microgeographicalpatterns of song variation might reflect genetic differentiation of local populations. The idea proposed by Nottebohm is that songs are learned close to the site of hatching, and that young birds do not disperse beyond the boundaries of the population in which their own song variation is prevalent. In consequence, pairs tend to form between birds from the same song population, and genetic differentiation of populations could arise as a result of learned song traditions (see also Section 11,B,4,d). The best data supporting this hypothesis have been collected by Baker (1974,

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1975; Baker and Mewaldt, 1978). Male white-crowned sparrows at Point Reyes, California, generally have only one song type in their repertoires and neighboring males have nearly identical songs, indicating, as had been amply demonstrated in the laboratory (Marler, 1970), that males learn their songs from one another. Very sharp boundaries exist where territorial males on opposite sides sing recognizably different song patterns (Baptista, 1975; Baker, 1974), and analyses of genetic differences (by measuring enzyme polymorphisms) and dispersal patterns among birds in the region of the song boundary suggested that birds of the two song traditions tend not to interbreed. However, these conclusions may not apply to all white-crowned sparrow populations. For example, in the Rocky Mountains of Colorado white-crowned sparrows show genetic differences within a song tradition, while in coastal California such changes in allozyme frequency occur across the boundary between two song traditions (Baker, 1975). In a detailed study of white-crowned sparrows in Berkeley, California, L. F. Baptista and L. Petrinovich (personal communication) have found that testosterone-injected females from the field may sing songs which are similar to the songs of a neighboring population. This is evidence against the idea that birds only disperse and mate within a song tradition, although there could still be some preference for mates from within a tradition. Baptista and Petrinovich also found that very few birds banded as nestlings survived within the song population. While many probably died, it also seems likely that some dispersed out of the area. Baker and Mewaldt (1978) banded birds as juveniles rather than as nestlings, and it is possible that a significant portion of the juveniles had already dispersed a considerable distance. Finally, even though white-crowned sparrows in the laboratory are capable of learning songs prior to the age when dispersal would normally occur in nature (Marler, 1970), actual patterns of vocal learning in nature have not been documented. Given the stimulation of adult singing males in nature rather than the monotonous repetition of a song pattern over a loudspeaker, a juvenile may be able to alter his song patterns much later in life (Kroodsma, 1978b). As we have already mentioned in Section 11, there are two published studies in which juveniles of known parentage have been followed during dispersal, and sonagrams of song patterns of fathers and sons have been compared (Kroodsma, 1974; Jenkins, 1977). [Nice (1943) compared songs of fathers and sons without spectrographic analysis.] In agreement with both of these studies, and with Payne’s evidence that parasitic indigo birds change their song types according to their breeding site, two unpublished studies on the great tit (McGregor et al., 1980) and Swamp Sparrow (Kroodsma and Pickert, 1980) have shown that young males do not preferentially learn their father’s songs (see Section II,B,3). Jenkins (1977) suggested that in the saddleback young males avoid settling near males with song types similar to their own fathers’ songs. This is in com-

VARIATION I N BIRD SONG

I67

plete contrast to the idea discussed earlier for white-crowned sparrows. Jenkins recognized four song groups in his island population of saddlebacks, and studied five father-son combinations. All five sons settled outside their father’s song group. This evidence may not be as convincing as appears at first sight, since it is likely that many young would settle outside the parental song group even if dispersal were random with respect to song type. If, for example, each young male had an equal chance of settling anywhere on the island, and if song groups were equal in size, three-quarters of the young males would breed outside the parental song group. Since three of the five males studied by Jenkins were born in the smallest song group, the chance of settling within the father’s song area is even smaller. Thus it is possible that Jenkin’s results do not differ significantly from chance, but more detailed calculations cannot be made without more information. 4 . Repertoire Size and Spatial Variation As repertoire size increases, thorough documentation of the spatial distribution of song components becomes extremely difficult. For example, obtaining the repertoire for an individual with 20 to 50 song types might take 1 to 2 days; at the extreme, adequately documenting the vocal repertoire of a male brown thrasher (Tamstoma rufurn) would require weeks and involve more than a million comparisons among thousands of spectrograms (Kroodsma and Parker, 1977). Studies of geographical variation require analyses of many individuals, and it is not surprising that some of our best data come from species in which males sing only one song type (e.g., Baptista, 1975; Bradley, 1977; Thielcke, 1969). Some insights into the relationship between song repertoires and the existence of sharp boundaries between song populations may be obtained by comparing three species: the white-crowned sparrow (subspecies nurtaffi) with one song type/individual (Baptista, 1975), the saddleback with an average of two songs/ individual (Jenkins, 1977), and the Bewick’s wren with an average of 16 song typeshdividual (Kroodsma, 1974). When comparable numbers of song components are examined for each species, the patterns of variation through space are strikingly similar. In all three species, studying a single song type (which is all a white-crowned sparrow has, but which is only a portion of the repertoire of the other two species) reveals the following. Some song types (or some aspect of them) may be restricted to males which share contiguous territories, and sharp boundaries with no discernible changes in habitat features may exist beyond which a given song type does not occur. Males near the boundaries may have hybrid songs, including in a single song type characteristics of songs which typically occur on opposite sides of the boundary or they may be “bilingual” (Baptista, 1975) and have enlarged song repertoires [Jenkins, 1977; see also Kaiser (1965), and Mundinger (1975) for similar data on the yellowhammer (Ernberiza citrinella) and house finch (Car-

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poducus mexicanus), respectively.] Thus, identifying a local area in which virtually all males share a single song type or component can be relatively straightforward, given that song types can be classified (see Section 11,A). The larger song repertoires, on the other hand, complicate attempts to delineate areas with homogeneous vocal behaviors. Jenkins (1977), in studying saddlebacks with 1.4 to 1.9 songs per male, found that, by extensive culling of distribution patterns which seemed of lesser importance, he could define areas to which certain combinations of song patterns were restricted. The task becomes very difficult indeed when one considers the Bewick’s wren in Oregon, where males possess an average of about 16 song types each. Even though males share most of their songs with each immediate neighbor, different song types or song components may have very different yet well-defined spatial distributions; attempts to delineate geographical areas with a given set of unique vocal behaviors are doomed to failure. 5 . The Functions of Dialects We have so far avoided using the term dialect. Instead we have referred to cultural song traditions, song neighborhoods, microgeographical variations, and so on. Some authors would use the term dialect to refer to all of these local variations in song type which can be attributed to vocal learning, while others use the word dialect to refer only to contiguous populations with clearly differentiated vocal patterns. We prefer to use the term in its more general sense, rather than abandoning it altogether as some have advocated (Mulligan, 1975). The operational criterion for recognizing the occurrence of dialects is that neighboring birds have songs which are more similar to one another than to the songs of more distant birds. There may or may not be clearly delineated boundaries between dialects, and questions about how, when, and where young males learn song types are more likely to be fruitful than attempts to define dialect boundaries have been. As with repertoires which we discussed in Section 11, it is unlikely that any single explanation will account for the selective forces leading to dialect formation. However in attempting to assess various hypotheses it is useful to think of the question of the functions of dialects in two parts: the question of why birds learn to sing, and why learned songs vary from place to place. The relationshp between learning and dialects has been viewed in two ways in the past. On the one hand it has been argued that the formation of local dialects is one of the most important selective factors favoring learning (Nottebohm, 1972), while on the other hand some view dialects as mere epiphenomena of song learning which is favored in some other context, such as matched countersinging between neighbors (Section II,B,2,b). If songs are learned and dispersal after learning is restricted, dialects are very likely to arise. As we have discussed, the evidence from a number of studies does not support the view that learned dialects

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act as strong barriers to prevent dispersal and intermixing of neighboring populations. Even if one accepts that it is advantageous for individuals to mate with partners sharing similar adaptations to the local environment, there is no convincing evidence that dialects are used as a mechanism to promote assortative mating. There might still, however, be slight effects which are detectable only on a much longer time scale. M. C. Baker (personal communication) has found, by comparison of the number of subspecies per species in different avian groups, that speciation appears to be more rapid in species with vocal imitation than in other groups. Similarly, among red-winged blackbirds and rufous-sided towhees (Pipilo erythrophthalamus) males of the widespread and largely migratory eastern nominate subspecies share few songs with neighbors, while males in the more restricted, largely resident western subspecies share many songs with neighbors (Kroodsma, 1971; Ewert, 1978; E. Morton, personal communication; K. Yasukawa, personal communication). Among the two Cistothorus wrens, the marsh wren imitates song and has subspeciated considerably, while the sedge wren improvises songs and has not subspeciated. It could be argued from these data that sedentary habits and site fidelity are either a cause or a consequence of well-developed local dialects. Although sedentary habits may be essential for both rapid speciation and dialect formation, the evidence suggests that vocal learning itself is not a prerequisite for rapid formation of new species. The Tyrrannid flycatchers, for example, have undergone intense speciation to produce over 1000 species, but they are not known to have vocal learning (Nottebohrn, 1972). In some species with clearly defined dialects, the spatial distribution of songs may arise as a consequence of microgeographical separation of small populations of singing males. For example, Lemon (1975) speculates that dispersing cardinals may introduce new songs into a breeding area, and Baker (1975) discusses the possibility that the relatively discrete song dialect areas in Nuttall’s whitecrowned sparrow of coastal California are a consequence of recolonization of regenerating habitat in a fire climax community; the existence and location of boundaries between dialect areas are then a result of secondary contact between two formerly isolated populations. In summary, there is rather conflicting evidence relating to the idea that vocal learning plays a role in promoting or maintaining genetic isolation between neighboring populations. An alternative idea is that dialects arise either as a by-product of vocal imitation of neighbors by young males, andlor as a result of geographical separation of local groups of singing males. Vocal imitation of neighbors may be favored for the kinds of reason discussed in Section II,B,2: if young birds learn songs from their parents (this does not seem to be the case in the few species so far studied) kin recognition might be an important consequence of learning. Vocal imitation may simply be an economical way of acquiring a large repertoire, or it may result in song sharing between neighbors, which

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could be important if songs are used in matching duels (Section II,B,2). R. B. Payne (personal communication) suggests that by imitating the song of the most successful male in a display group, a subordinate individual can deceptively take over the successful site if its owner disappears. Thus although there is much descriptive evidence to show that dialects exist, much more detailed information will be needed to evaluate specific hypotheses about their significance.

IV. CONCLUSION We started out by considering repertoires and dialects as two separate questions, but our conclusion is that the same kinds of data are required to understand the functional significance of both phenomena. In order to understand why birds learn to sing, and why songs vary within an individual and between populations, it will be necessary to collect more information on the following points: where, when, and from whom young birds learn their songs; how and why differences in reproductive success between males are related to differences in vocal behavior; and how female choice of mates is related to male songs.

Acknowledgments We thank the Science Research Council (J.R.K.) and National Science Foundation (D.E.K.) for financial support. A number of people kindly allowed us to quote from their unpublished results: L. Baptista, P. K. McGregor, K. Yasukawa, L. Petrinovich, J. Baylis, M. Baker, C. Catchpole, G. Morton, P. Slater, and C. M. Perrins.

References Armstrong, E. A. 1973. “A Study of Bird Song.” Dover, New York. Avery, M., and Oring, L. W. 1977. Song dialects in the bobolink (Dolochonyxoryzivorus). Condor 79, 113-118. Baker, M. C . 1974. Genetic structure of two populations of white-crowned sparrows with different song dialects. Condor 76, 351-356. Baker, M. C. 1975. Song dialects and genetic differences in white-crowned sparrows (Zunorrichia leucophrys). Evolution 29, 226-241. Baker, M. C . , and Mewaldt, L. R. 1978. Song dialects as barriers to dispersal in white-crowned sparrows, Zonotrichia leucophrys nuttalli. Evolution 32, 712-722. Baker, R. R., and Parker, G. A. 1979. The evolution of birdcoloration. Proc. R . Soc. London, Ser. B 287, 63-130. Baptista, L. F. 1975. Song dialects and demes in sedentary populations of the white-crowned sparrow (Zonotrichia leucophrys nuttalli). Univ. Calq.. Berkeley, Publ. 2001.105, 1-52. Baptista, L. F., and King. J. R. 1980. Geographical variation in song and song dialects of montane white-crowned sparrows (Zonotrichia leucophrys oriantha). In preparation.

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Bateson, P. P. G. 1978. Sexual imprinting and optimal outbreeding. Nature (London) 273,659-660. Becker, P. H. 1977a. Geographische Variation des Gesanges von Winter- und Sommergoldhahnchen (Regulus regulus, R. ignicappillus). Vogelwarte 29, 1-37. Becker. P. H. 1977b. Verhalten auf Lautausserungen der Zwillingsart, interspezifische Territorialitat und Habitatanspriiche von Winter- und Sommer-goldhahnchen (Regulus regulus, R. ignicapillus). J . Ornifhol. 118, 233-260. Beer, C. G . 1970. Individual recognition of voice in the social behaviour of birds. Adv. Siudy Behrrv. 3, 27-74. Bertram, B. 1970. The vocal behaviour of the Indian hill mynah, Gracula religiosa. Anim. Behav. Monogr. 3(2), 79-192. Bitterbaum, E., and Baptista, L. F. 1979. Geographic variation in songs of California house finches. Auk 96, 462-474. Bjerke, T. 1974. Geografisk sangvariasjon hos rodvingetrost, Turdus iliacus. Srerna 13, 65-76. Borror, D. J., and Gunn, W. W. H. 1965. Variation in white-throated sparrow songs. Auk 82, 26-47. Bowman, R . I . 1980. Adaptive morphology of song dialects in Darwin’s finches. J. Orn. Lpz. 120, 353-390. Bradley, R . A. 1977. Geographic variation in the song of Belding’s savannah sparrow (Passerculus sandwichensis beldingi). Bull Fl. Stare Mus.. Biol. Sci. 22(2), 57-100. Bremond, J . C. 1976. Specific recognition in the song of Bonelli’s warbler (Phylloscopus bonelli). Behaviour 58, 99-1 16. Brooks, R. J., and Falls, J . J. 1975. Individual recognition by song in white-throated sparrows. II1. Song features used in individual recognition. Can. J . Zool. 53, 1749-1761. Brown, R . N. 1977. Character convergence in bird song. Can. J. Zool. 55, 1523-1529. Caryl, P. G. 1979. Communication by agonistic displays: What can games theory contribute to ethology? Behavior 68, 136- 169. Catchpole. C. K. 1980. Sexual selection and the evolution of song in European warblers of the genus Acrocephalus. Behaviour (in press). Chappuis, C. 1971. Un exemple de I’influence du milieu sur les emissions vocales des oiseaux: L’evolution de chants en forkt equatoriale. Terre Vie 25, 183-202. Cody, M. L. 1969. Convergent characteristics in sympatric species: A possible relation to interspecific competition and aggression. Condor 71, 222-239. Cody, M. L. 1974. “Competition and the Structure of Bird Communities.” Princeton Univ. Press, Princeton, New Jersey. Conrads, K. 1976. Studien an Fremddialekt-Sangern und Dialekt-Mischsangem des Ortolans ( E m heriza horrulana). J . Ornithol. 117, 438-450. Conrads, K., and Conrads, W. 1971. Regionaldialekta des Ortolans (Emberiza hortulana) in Deutschland. VoRelwelt 92, 81-100. Dawkins, R . , and Krebs, J. R . 1978. Animal signals: Information or manipulation? In “Behavioural Ecology: An Evolutionary Approach” (J. R . Krebs and N . B. Davies, eds.), pp. 282-309. Blackwell, Oxford. Dittus, W. P. J . , and Lemon, R. E. 1969. Effects of song tutoring and acoustic isolation on the song repertoires of cardinals. Anim. Behuv. 17, 523-533. Dixon, K. L. 1969. Patterns of singing in a population of the plain titmouse. Condor 71, 94-101. Dobkin, D. S . 1979. Functional and evolutionary relationships of vocal copying phenomena in birds. 2. Tierpsychol. 50, 348-363. Dobson, D. W., and Lemon, R. E. 1975. Re-examination of monotony threshold hypothesis in bird song. Nulure (London) 257, 126-128. Dowsett-Lemaire, F. 1979. The imitative range of the song of the Marsh Warbler Acrocephalus palusrris with special reference to imitations of African birds. Ibis 121, 453-468.

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Eberhardt, D., and Baptista, L. F. 1977. Intraspecific and interspecific song mimesis in California song sparrows. Bird-Banding 48, 193-205. Emlen, S. T., Rising, J. D., and Thompson, W. L. 1975. A behavioral and morphological study of sympatry in the indigo and lazuli Buntings of the Great Plains. Wilson BuU. 87, 145-179. Ewen, D. N. 1978. Song of the rufous-sided towhee (Pipilo eryrhrophrhulmus) on Long Island, New York. Ph.D. Dissertation, City University of New York. Falls, J . 8. 1969. Functions of territorial song in the white-throated sparrow. In “Bird Vocalisations” (R. A. Hinde, ed.), pp, 207-232. Cambridge Univ. Press, London and New York. Falls, J . B. 1978. Bird song and territorial behaviour. I n “Advances in the Study of Communication and Affect” (L. Krames, P. Pliner, and T. Alloway, eds.), Vol. 4, pp. 61-89. Plenum, New York. Falls, J . B., and Krebs, J. R. 1975. Sequences of songs in the repertoires of western meadowlarks. Can. J . 2001.53, 1165-1178. Fisher, R, A. 1958. “The Genetical Theory of Natural Selection.” Dover, New York. Catty, H. 1958. “Nature is Your Guide.” London. Gompertz, T. 1961. The vocabulary of the great tit. Br. Birds 54, 369-418. Grafen, A. 1979. The hawk-dove game played between relatives. Anim. Behav. 27, 905-907. Greenwood, P. J., Harvey, P. H., and Pemns, C. M. 1979a. The role of dispersal in the great tit (Parus major): The causes, consequences and heritability of natal dispersal. J. h i m . Ecol. 48, 123- 142. Greenwood, P. J . , Harvey, P. H., and Perrins, C. M. 1979b. Kin selection and temtonality in birds? A test. Anim. Behav. 27, 645-651. Grimes, L. 0. 1974. Dialects and geographical variation in the song of the splendid sunbird Necrarina coccinigasrer. Ibis 116, 3 14-329. Guttinger, H. R. 1974. Gesang des Grunlings (Chloris chloris). Lokale Unterschiede und Entwicklung bei Schallisolation. J. Omirhol. 115, 321-337. Guttinger, H. R. 1977. Variable and constant structures in greenfinch songs (Chloris chloris) in different locations. Behaviow 60, 304-3 18. Gwinner, E., and Wiltschko, W. 1978. Endogenously controlled changes in migratory direction of the garden warbler Sylvia borin. J . C o y . Physiol. 125, 267-273. Halliday, T. R. 1978. Sexual selection and mate choice. In “Behavioural Ecology: An Evolutionary Approach” (J. R. Krebs and N. B. Davies, eds.), pp. 180-213. Blackwell, Oxford. Hammerstein, P. 1980. In preparation. Harcus, J. L. 1977a. The functions of vocal duetting in some African birds. 2. Tierpsychol. 43, 23-45. Harcus, J . L. 1977b. The functions of mimicry in the vocal behaviour of the chorister robin. Z. Tierpsychol. 44, 178-193. Harris, M., and Lemon, R. E. 1972. Songs of song sparrows (Melospiza melodia): individual variation and dialects. Can. J. Zoo/. 50, 301-309. Hartshome, C. 1956. The monotony threshold in singing birds. Auk 73, 176-192. Hartshorne, C. 1973. “Born to Sing.” Indiana Univ. Press, Eloomington. Hooker, T., and Hooker (Lade), B. I. 1969. Duetting. In “Bird Vocalizations” (R. A. Hinde, ed.), pp. 185-205. Cambridge Univ. Press, London and New York. Howard, R. D. 1974. The influence of sexual selection and interspecific competition on mockingbird song. Evolution 28, 428-438. Hunter, M. L., Jr., and Krebs, J . R. 1979. Geographical variation in the song of the great tit (Parus major) in relation to ecological factors. J. h i m . Ecol. 48, 759-786. Immelman, K. 1969. Song development in the zebra finch and other estrildid finches. In ”Bird Vocalisations” (R. A. Hinde, ed.), pp. 61-74. Cambridge Univ. Press, London and New York. Isaac, D., and Marler, P. 1963. Ordering and sequences of singing behavior of mistle thrushes in relationship to timing. h i m . Behav. 30, 344-374.

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Michelson, A. 1978. Sound reception in different environments. In “Perspectives in Sensory Ecology” (M. A. Ah, ed.), pp. 345-373. Plenum, New York. Miller, D. B. 1979. Long-term recognition of father’s songs by female zebra finches. Nature ILondon) 280, 389-391. Moore, F . R. 1978. Interspecific aggression: Toward whom should a mockingbird be aggressive. Behav. Ecol. Sociobiol. 3 , 173-176. Morton, E. 1975. Ecological sources of selection on avian sounds. Am. Nur. 108, 17-34. Morton, E. S . 1976. Vocal mimicry in the thick-billed euphonia. Wilson Bull. 88, 485-487. Mulligan, J. A., ed. 1975. “Symposium on Dialects in Bird Song.” Media Services, St. Louis University, Missouri (available on cassette tape only). Mundinger, P. C. 1970. Vocal imitation and individual recognition of finch calls. Science 168, 480-482. Mundinger, P. C. 1975. Song dialects and colonization in the house finch, Carpodacus mexicanus, on the east coast. Condor 77, 407-422. Nice, M. M. 1943. Studies in the life history of the song sparrows. The behaviour of the song sparrow and other passerines. Trans. Linn. Soc. N . Y . 6 , 1-324. Nicholai, J. 1959. Familientradition in der Gesangsentwicklung des Gimpels (fyrrhulapyrrhula).J . Ornithol. 100, 39-46. Nicolai. J . 1964. Der Brutparasitismus der Viduinae als ethologisches Problem. Z . Tierpsychol. 21, 129-204. Nottebohm. F. 1969. The song of the chingolo. Zonotrichia capensis, in Argentina: Description and evaluation of a system of dialects. Condor 71, 299-315. Nottebohm, F. 1970. Ontogeny of bird song. Science 167, 950-956. Nottebohm, F. 1972. The origins of vocal learning. A m . N u t . 106, 116-140. Nottebohm, F. 1975. Continental patterns of song variability in Zonotrichia capensis: Some possible ecological correlates. Am. Nut. 109, 605-624. Nottebohm, F., and Nottebohm, M. 1978. Relationship between song repertoire and age in the canary Serinus canarius. Z . Tierpsychol. 46, 298-305. Odum, E. P., and Kuenzler, E. J . 1955. Measurement of territory and home range size in birds. Auk 72, 285-312. Payne, R . B. 1973a. Vocal mimicry of the paradise whydahs (Vidua) and response of female whydahs to the songs of their hosts (Pytilia) and their mimics. Anirn. Behav. 21, 762-771, Payne, R. B. 1973b. Behavior, mimetic songs and song dialects, and relationshipsof the indigobirds (Viduu) of Africa. Ornirhol. Monogr. No. 1 I . pp. 1-333. Payne, R. B. 1 9 7 3 ~ Wingflap . dialects in the flappet lark Mirufra rufocinnamomeu. Ibis. 115, 270-274. Payne. R . B. 1975. Song dialects and population structure in the indigobirds. In “Symposium on Dialects in Bird Song” ( J . A. Mulligan, ed.). Media Services, St. Louis University, Missouri (available on cassette tape only). Payne, R . B. 1978. Microgeographic variation in songs of splendid sunbirds Necrariniu coccinigaster: Population phenetics, habitats, and song dialects. Behaviour 65, 282-308. Payne, R . B., and Payne, K . 1977. Social organization and mating success in local song populations of village indigobirds, Yiclua chalyheatu. Z . Tierpsychol. 45, 113-173. Pickstock, J. C., and Krebs, J. R . 1980. Neighbour-stranger song discrimination in the chaffinch (Fringilla coelebs) J . Ornithol. 121, 105-108. Rechten. C. 1978. Interspecific mimicry in birdsong: Does the Beau Geste hypothesis apply? h i m . Behov. 26, 305. Richards, D. G.,and Wiley, R . H. 1980. Reverberations and amplitude fluctuations in the propagation of sound in a forest: Implications for animal communication. Am. Nut. (in pres). Robinson, F. N. 1975. Vocal mimicry and the evolution of bird song. Emu 75, 23-27.

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Samson, F. B. 1978. Vocalizations of Cassin’s finch in Northern Utah. Condor 80, 203-210. Seibt, U. 1975. lnstrumentaldialekts der Klapperlerche, M i r a j a rufocinnamomea (Salvadori). J . Ornithol. 116, 103-107. Slater, P. J . B. 1980. In preparation. Smith, D. G . , and Reid, F. A. 1979. Roles of the song repertoire in red-winged blackbirds. Behav. Ecol. Sociobiol. 5, 279-290. Smith, W.J . , Pawlukiewicz, J . , and Smith, S. T. 1978. Kinds of activities correlated with singing patterns of the yellow-throated vireo. Anim. Behuv. 26, 862-884. Snow, D. W. 1968. The singing assemblies of little hermits. Living Bird 7, 47-55. Thielcke, G. 1961. Stammegeschichte und geographische Variation des Gesanges unserer Baumlaufer (Certhia familiaris L.und Cerrhia brachydacryla Brehm). Z . Tierpsychol. 18,188-204. Thielcke, G.1965. GesangsgeographischeVariation des Gartenbaurnlaufers (Cerrhia brachydactyla) im Hinblick auf das Artbildungsproblem. Z . Tierpsychol. 22, 542-566. Thielcke, G. 1969. Geographic variation in bird vocalizations. I n “Bird Vocalizations” (R. A. Hinde, ed.), pp. 311-339. Cambridge Univ. Press, London and New York. Thompson, W. L. 1970. Song variation in a population of indigo buntings. Auk 87, 58-71. Thompson, W. L., and Jane, P. L. 1969. An analysis of catbird song. Jack Pine Warbler 47, 115-125. Thorneycroft, H. B. 1967. Aspects of the development of vocalizations in the white-throated sparrow, Zonotrichia alhicollis (Grnelin). Master’s Thesis, University of Toronto, Toronto. Thorpe, W. H. 1958. The learning of song patterns by birds, with especial reference to the song of the chaffinch Fringilla coelebs. Ibis 100, 535-570. Thorp, W. H. 1961. “Bird Song.” Cambridge Univ. Press, London and New York. Thorpe, W.H. 1972. Duetting and antiphonal song in birds. Its extent and significance. Behuviour, SUPPI. 18, 1-197. Tinbergen, N. 1939. The behaviour of the snow bunting in spring. Trans. Linn. Soc. N . Y . 5 , 1-95. Tinbergen, N. 1959. Comparative studies of the behaviour of gulls (Laridae): A progress report. Behaviour 15, 1-70. Todt, D. 1970. Die antiphonen Paargesange des ostafrikanischen Grassanger Cisricola hunreri prinoides Neumann. J . Ornithol. 111, 332-356. Todt, D. 1975. Short-term inhibition of outputs occurring in the vocal behaviour of blackbirds (Turdus merula). J. Comp. Physiol. 98, 289-306. Treisman, M. 1978. Bird song dialects, repertoire size, and kin association. Anim. Behav. 26, 8 14-8 17. Tretzel, E. 1967. Imitation und transposition menschlicher Pfiffe durch Amseln (Turdus m. merulu). Z . Tierpsychol. 24, 137- 161. Verner, J. 1975. Complex song repertoire of male long-billed marsh wrens in Eastern Washington. Living Bird, 14, 263-300. Waser, P., and Waser, M. S. 1977. Experimental studies of primate vocalization: Specializationsfor long-distance propagation. Z. Tierpsychol. 43, 239-263. Whitney, C. 1979. The control of singing in varied thrushes. Ph.D. Thesis, University of British Columbia. Wildenthal, J . L. 1965. Structure in primary song of the mockingbird (Mimuspolyglottos). Auk 82, 161-189. Wiley, R. H. 1971. Song groups in a singing assembly of little hermits. Condor 73, 28-35. Wiley, R. H., and Richards, D. G . 1978. Physical constraints on acoustic communication in the atmosphere: lmplications for the evolution of animal vocalizations. Behav. Ecol. Sociobiol. 3, 69-94. Wilkinson, R., and Howse, P.E. 1975. Variation in the temporal characteristicsof the vocalizations of bullfinches, Pyrrhula pyrrhula. 2. Tierpsychol. 38, 200-21 1.

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Williams, L., and MacRoberts, M. H . 1977. Individual variation in songs of dark-eyed juncos. Condor 79, 106-1 12. Wilson, E. 0. 1975. “Sociobiology: The New Synthesis.” Belknap Press. Cambridge, Massachusetts. Yasukawa, K . 1981. Song repertoires in the red-winged blackbird (Agelaius phoeniccus): A test of the Beau Geste hypothesis. Anirn. Behav. (in press). Yasukawa, K . , Blank, J . L., and Patterson, C . B . 1980. Song repertoires and sexual selection in the red-winged blackbird (Agelaius phoenicus). Eehav. Ecol. Sociobid. (in press).

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ADVANCES IN THE STUDY OF BEHAVIOR VOL. I I

Development of Sound Communication in Mammals GUNTEREHRET FAKULTAT RIOLOGIE UNIVERSITAT KONSTANZ KONSTANZ, FEDERAL REPUBLIC OF GERMANY

1. Introduction ............................................ 11. Components of Sound Communication Systems: General Aspects Development . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . III. Time Courses of the Development of Vocal Behavior and Hearing in Subhuman Mammals and M a n . , . , . , . . . . . . . . . . . . . . . . . . . . . . , . . , , . , , . . A. Chiroptera . . . . . . . . . . . . . . . . . . . . . . . . . . . . . B. Carnivora . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . C. Rodents . . . . . . . . . ................................ D. Primates . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . IV. Characteristics and Co nt 0 Behavior . . . . . . . . . . . . .... Ut ............. A. Development of Phys 9 . Does the Development of Vocalizations Depend on Hearing? . . . . . . . . . C. Do External Stimuli and Behavioral Contexts Influence the Development of Vocalizations'? . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . D. Does Arousal Influence the Development of Vocalizations? . . . . V. Characteristics and C Communication . . . . . A . Can Infant Mamm B. Do Infant Mammals React to Sounds of the Adults? . . . . . . . . . . . . . . . . . C. Which Features of Infant Calls Do Adults Respond to? . . . D. Does Adult Responsiveness Paralle the Young? . . . . . . . . . . . . . . . . . . E. Nonacoustic Determinants of Adult Response Behavior . . . . . . . . . . . . . . VI. Conclusions .................................. VII. summary.. . . . . . . . . . . . . References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

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I. INTRODUCTION Adult mammals generally hear and they vocalize in quite a number of different behavioral contexts. The sound they produce may have communication effects in I79

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that it regularly alters the behavior of members of their own or of other species. This definition of sound communication will be used in this study and it is similar to a more general definition by Altmann (1967): “Social communication is a process by which the behavior of an individual affects the behavior of others. . . [by that] we mean that it changes the probability distribution of the behavior of others” (p. 326). We should be aware of pitfalls in using the term sound communication, which, strictly speaking, is justified only after we have established a consistent relation between the sound signal emitted by one animal and the alteration of behavior in another animal. Obviously investigating “sound communication” is always more difficult than recording “vocal behavior. In the latter one has to observe the behavior and the behavioral context of sound production in one animal, the sender, only, whereas in the former we deal with the behavior of two animals at least, which interact. Further, if the animals can see, feel, or smell each other in addition to hearing each other we face the problem of separating communication by sound from all the other possible modes. In this article an attempt is made to distinguish between vocal behavior and true sound communication. This may be helpful not only for organizing research but also and particularly for understanding ontogenetic and phylogenetic sequences of development of sound communication. It is different to ask whether an animal in a special motivational or emotional state vocalizes as an integrated part of its behavior or whether such vocalizations have signal characteristics capable of influencing the behavior of others. Our knowledge of vocal behavior in mammals exceeds what we know about sound communication by far. This is especially true with regard to the development of sound communication in young mammals. There are numerous questions on the interaction by sound between young and adults and among young during development. Many of these questions are relevant in understanding ( a ) the general organization of behavior in young and adults, ( b ) the interrelation between innate maturation patterns and influences of the social environment on the adult behavior, and ( c ) the significance of sound communication in mammals with different habitats and social organization. The purpose of this article will not and cannot be a comprehensive survey of the literature on this topic. The intention is to review the research on those mammals for which sufficient data exist and derive some common foundations and guidelines concerning the development of sound communication in mammals. Human data on the development of acoustic behavior are also included for comparative rather than for linguistic purposes. It need not be mentioned that one condition for sound communication is hearing, at least in the receiver. Thus we have to consider both the development of sound production and of hearing in order to understand who, physiologically, is able to communicate with whom. Many rodents, for example, are born in a very altricial state and do not hear during the first days of life. Therefore sound ”

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communication among the littermates is simply impossible although they can produce a variety of sounds from birth. We should also consider the analytical capacities of the auditory systems of mammals when we are interested in details of sound parameter detection and information extraction. In the development of echolocation in bats, for example, it is most important that the frequency bands of ultrasonic calls match with those of extremely good acoustic analysis. One could argue that the echolocation system in bats is one of “self-communication” rather than one of social importance. Although few data are available on sound communication in bats, there are many other mammals that produce very complex sound patterns and also ultrasound’ during infancy, so that the ability for complex sound analysis has general importance. As far as data are available, sound patterns and auditory acuity will be compared in order to approach questions of the development of “feature detection” in communication sounds.

II. COMPONENTS OF SOUND COMMUNICATION SYSTEMS: GENERAL ASPECTS OF DEVELOPMENT When we study the ontogeny of sound communication in a mammal we have to consider time courses of development of the components of the sound communication system. Why does a dog not bark in his first days of life (Rheingold, 1963; Cohen and Fox, 1976)? Is it because his vocal repertoire has not yet matured, or must he learn how to bark? Is it because an undeveloped vocal tract makes it physically impossible for him to bark? He may need external and/or internal stimuli, a special motivation, or a special behavioral context, which are not present in the nest. Or, is he not barking because he cannot hear? The answers to these questions all contribute to our understanding of the ontogeny of vocal behavior in the dog; however, they do not tell us whether or not a dog communicates by barking. In addition to the development within the sender and to changes of his environment we have to measure the behavior of a potential, usually conspecific, receiver. More precisely, we must determine the responses of another dog to the developing acoustic behavior of a puppy. These may range from no overt response to a call to a very strong and specific response. Again developmental changes are possible as, for example, an increase in accuracy and selectivity of sound pattern recognition or a decrease of the response threshold to a particular call. Figure 1 summarizes the main components of a sound communication system and shows examples of developmental changes that may occur. It also gives an ‘Calls with fundamental frequencies higher than 20 kHz will be referred to as ultrasound throughout this article. One reason is that ultrasonic communication has now been accepted as a general term for sound communication in the high frequency range (f > 20 kHz),especially in rodent communication.

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GUNTER EHRET chonges in t h e ing development

Frc. 1. Diagram of the main components of a sound communication system (inner circle) with developmental aspects of these components (outer circle). The diagram should be read from the sender side (circles) starting with the behavioral context and stimuli a sender is exposed to. Neural mechanisms representing the vocal repertoire within the brain will be activated to coordinate nervous patterns which will activate mechanisms of sound production, so that a sound signal is produced. A receiver (triangles) perceives the auditory input via the cochlea. Neural mechanisms will decode and filter the excitation pattern from the cochlea and transfer it to brain centers which can recognize signal-specific excitation patterns and will activate corresponding motor centers to produce behavior. The behavior of the receiver can feed back on the original behavioral context or on the stimuli which induced the sender to vocalize. By that, the communication system is closed. The rectangles of the diagram include some aspects and questions which have to be considered when investigating the development of the communication system.

idea of the diversity of starting points for research in the field of development of sound communication. So far points of major interests have been the behavioral contexts of sound production and the vocal repertoires of the developing young on the one hand and the development of hearing on the other. Descriptive data are accumulating but there are few detailed analyses of changes in behavioral contexts, stimuli, and motivation which could be the basis of developing vocal behavior. Thus we have a more or less incomplete knowledge of what happens during the ontogeny of the sender for a number of mammals, but we know almost nothing at all about why it happens. We have evidence that neonates and juveniles produce calls which are specific for their age and which do not occur in

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adults (compare Figs. 2-12). The mechanisms underlying these changes in vocal repertoire are not well understood. Areas ripe for study are the development of neural mechanisms of sound pattern recognition, the development of behavioral responsiveness to sound, and, most interesting for ethologists, the development of sound-mediated social interactions among littermates and between parents and their young. This brief outline of what has to be done rather than of what has been done will, I hope, set the stage for a critical and more holistic view of the data which will be presented and of the conclusions which will be drawn.

III. TIMECOURSES OF THE DEVELOPMENT OF VOCALBEHAVIOR AND

HEARINGIN SUBHUMAN MAMMALS A N D MAN

Many studies of the vocal behavior in mammals include data on the vocal repertoire of the young and the behavioral contexts in which they vocalize. Thus we have evidence for sound production by the young in most of the orders of the class Mammalia, such as Marsupialia (Eisenberg et al., 1975), Insectivora (Gould, 1969; Poduschka, 1977), Perissodactyla (Kiley, 1972; Klingel, 1977), Artiodactyla (Tembrock, 1968; Kiley, 1972), Hyracoidea (Fourie, 1977), Cetacea (Caldwell and Caldwell, 1977), and Lagomorpha (Eisenberg and Kleiman, 1977). More comprehensive investigations on the development of vocal behavior and hearing are available for species in the orders chiroptera, carnivora, and rodentia, and for primates. In the following we will be concerned with representatives of these orders. Diagrams of the development will be shown (Figs. 2-13) including days of eye opening, weaning, and sexual maturation and some other characteristic dates in the development of the young. It is important to note that the names used to characterize calls of the different species are mostly derived from situations in which the calls are produced or from the physical characteristics of the sound. They do not imply any function a call may have to influence the behavior of the other animals. Further, we cannot be sure whether the vocal repertoires described for the mammals shown in Figs. 2-12 are complete or not. Additional studies may find additional calls with different time courses of development. A.

CHIROPTERA

Bats are well known for emitting ultrasound for echolocating prey and for orienting in their environment. Since they extract information from the echoes of their own calls and change their behavior accordingly, one can speak of a highly specialized “self-communication system. The postnatal development of orientation sounds and other vocalizations was studied in the vespertilionid bats An”

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rrozous pullidus (Gould, 1975a,b; Brown, 1976), Eptesicus fuscus (Gould, 1971, 1975a,b), Myoris lucifugus (Gould, 1971, 1975a), and Myotis oxygnarhus (Konstantinov, 1973). Gould (1979) reports neonatal vocalizations in 10 species of Malaysian bats. Figure 2 shows data for Anrrozous. A very similar development was found in Eptesicus and Myotis. The young of the latter two species are born in a less altricial state and therefore progress in the development is made earlier than in Anrrozous (Gould, 1971, 1975a). Anrrozous starts hearing at the sixth or seventh day of life and adult sensitivity is reached by day 24 (P. E. Brown et al., 1978). The development of binaural hearing continues up to about day 28. Newborn Antrozous can produce only one call type, the isolation call. This call disappears from the vocal repertoire at about day 20. Another call characteristic for juveniles is the sound emitted just before take-off during the first month of self-reliant flight. The production of the other six calls starts at different times mostly after the onset of hearing, and adult patterns are reached around weaning at about day 50 at the latest. t

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-- -- -- - - - - - - - - - - - - - - - - - - - - - - - - - i-r r-i-t a- t-i o- n- - b-u- z-z- - - - - - - - - - - - - - - - - - - - - - - - - - - -squabble - - - - - - - notes - -- - --- - - - - _- -_ -_ -_ - - _ - - - - - - - - - - - - - - - - -Doin call ---------------- - - - - call before take-off 4 eyes open

pref li g ht movements

first flight

1

1

16

20 ' iL ' i6 ' 32 ' j 6 ' L O

i birth'

i

8

12

*

full weoni n g

1 ' LL ' 66

' 52

I1

<6

60 doys"odult

FIG.2. Antrozous pallidus: Diagram of the development of hearing (upper part) and of vocal behavior (lower part). In this and the following figures of this kind the development is indicated by lines and arrows. Lines start at the date when hearing or the production of a call type starts. Single lines indicate a subadult, still developing state, double lines tell that adult hearing capacity or call structure is reached. Broken lines are used either when the beginning of a development or of the adult state cannot be fixed to a certain date, or when the Occurrence of a sound type becomes very rare. The end of the occumence of a vocalization in a vocal repertoire is indicated by an arrow ending at a vertical bar. Connecting lines show the development of one call type from another.

DEVELOPMENT OF SOUND COMMUNICATION

185

A11 calls listed in Fig. 2 have differeM frequency patterns and timing. The isolation and the directive calls have frequency-modulated fundamentals (downward sweeps) and harmonics. Squabble notes, pain calls, and the call before take-off have a harmonic structure the fundamental frequencies of which are more or less constant. The irritation buzz and the orientation pulse are rapid downsweeps in frequency without harmonics. The sweep range of the calls is mostly within the frequency band between 5 and 30 kHz except for the orientation pulse which sweeps down from about 70 to 20 kHz (Brown, 1976). It is evident that juvenile Antrozous can emit calls of different sound qualities except during their first 6 days of life. P. E. Brown et al. (1978) state that after the first week Antrozous emits sound which it can hear. Thus the onset of differentiation of call patterns coincides with the onset of hearing. This is also true for Eptesicus (Gould, 1975b) and Myotis lucifugus (Gould, 1971, 1975a). Myotis lucifugus may hear and can produce different calls from birth. In all three bats the development of the echolocation system does not contrast with the general development but turns out to be an integrated part of it. B.

CARNIVORA

Here the development of hearing and acoustic behavior is best known for the house cat and its feral relatives (puma, lion, tiger, etc.) and for the dog.

I. Cat (Felis catus) Figure 3 combines data on the development of hearing from Ellingson and Wilcott (1960), Romand (1971), Jewett and Romano (1972), Romand et al. (1973), Fernandez and Hinojosa (1974), Aitkin and Moore (1975), Aitkin and Reynolds (1975), Javel et al. (1975), Romand and Marty (1975), Brugge et al. (1978), Clements and Kelly (1978), and Mair et al. (1978). Kittens may have some sensation for sound at their first day of life (Romand, 1971; Romand and Marty, 1975). Sensitivity to pure tones manifests itself at about the third postnatal day and improves until about day 28. Binaural processing, responses to clicks, and phase-locking of discharges to low-frequency tones improve up to about day 35 (Aitkin and Reynolds, 1975; Javel et al., 1975; Brugge et a!., 1978; Clements and Kelly, 1978). The developmental rate is highest between the fourth and the twenty-first day. Moelk (1944), Hiirtel (1975), and K. A. Brown et al. (1978) investigated the vocal repertoires of kittens and cats. During their first 4 days of life, kittens can emit only one, albeit very variable call, the isolation or pain call. The typical isolation call of the young can be heard until about day 28. It may develop into the pain call of the adults. A second call, characteristic for juveniles exploring their environment for the first time, is a pure ultrasonic call (about 80 kHz). Spitting is another sound occurring early in development. Two agonistic calls and a call when expecting food are

186

GUNTER EHRET

If

__--

hears pure tones

____

__

orientation to sound. normal tuning curves in VIIIth nerve and broin

-

- --- - - - - --- - - - - - - - - - - - -- - - -- - - - -- - - - - - - - - -- ---isolation colls

--

____

Dain calls 7

spittinq (defensive call) 7

call when expectina food

--_-

1

7

US while explorinq

1

__ -

b

+

I

II

I

produced first during the third and fourth week. Contact calls are produced very late starting about the seventieth day. Two calls of the mother were found, one when her kitten is inaccessible, the other, a pure ultrasonic call, when responding to the ultrasound of the young. The last call mentioned in the diagram occurs during mating. There can be considerable variation among calls of one type emitted by different individuals. However, when a kitten is able to emit one particular call there are only little changes in the frequency patterns during the further development of the individual. Altogether, however, the frequency range of the fundamental frequency in the calls is higher in kittens than in adult cats. All calls with the exception of spitting and the pure ultrasound have a harmonic structure, and some include noise (pain and agonistic calls). At the age of about 3 weeks, when kittens begin to eat solid food and to explore the area around the nest, the vocal repertoire shows the most obvious changes. The typical neonatal isolation call is replaced by a number of calls of the adults. It is remarkable that young and adult cats can produce pure ultrasound with frequencies as high as 80 kHz (Hartel, 1975). Adult cats most probably can hear

DEVELOPMENT OF SOUND COMMUNICATION

187

80 kHz since auditory thresholds at 60 kHz, the highest tested frequency, are rather low (Neff and Hind, 1955). The absolute auditory sensitivity of the cat (Neff and Hind, 1955), its frequency and intensity difference limens (Elliott et al., 1960; Raab and Ades, 1946; Elliott and McGee, 1965), and its central resolution for complex sound patterns (Keidel, 1974; Sovijiirvi, 1975) are so good that adult cats are readily able not only to discriminate the major frequency patterns of the different calls but most probably to recognize individuals by their specific subtle differences in vocalizing a special call. 2 . Other Felidae Peters (1978) published a comprehensive study on the vocalizations of adult and young pumas (Puma concolor), clouded leopards (Neofelis nebulosa), snow leopards ( Uncia uncia), leopards (Panthera pardus), jaguars (Panthera onca), tigers (Panrhera tigris), and lions (Panthera Leo). Figure 4 reproduces diagrams from Peters (1978) on the ontogeny of the main vocalizations of the puma, the tiger, the jaguar, and the lion. The diagrams do not include calls of which the development remains unclear because of lack of material. Also vocalizations during sexual behavior are not shown. Newborn of all species emit only one call during the first 2 weeks of life. This call is termed “bleating” by Peters (1978) and is identical to the isolation call described for the house cat. Bleating disappears in the sixth month at the latest. The “mew” call is the second call to occur. It corresponds to the call “when expecting food” described for the cat. The juvenile tiger at about 5 months and the other species at nearly 1 year start to emit the typical calls of the adults, the main call, the main call with grunt element, and the grunt. At this time the animals are weaned but still depend on the mother for meat supply. The vocalizations developing latest are composite vocalizations and structured call sequences. The calls mentioned are mostly harmonically structured with slight modulations of the fundamental. In addition, noise is often superimposed. During ontogeny, the frequency components with the relatively highest intensity in the calls shift from about 5 to 3 kHz in the puma and from about 3 to less than 1 kHz in the tiger, jaguar, and lion. The adult register appears between the third and the sixth month. At that time motor and sensory skills are well developed. 3 . Dog (Canis familiaris)

Although the dog probably is the most familiar animal to man there seems to have been only occasional interest in its vocalizations especially in the ontogeny of its vocal behavior and the development of hearing. The development of the vocal repertoire shown in Fig. 5 is based on data from Bleicher (1963), Rheingold ( 1 963), and Cohen and Fox (1976). The ontogeny of hearing was studied by Fox ( 1 968), Chaloupka et al. (1968), Pujol and Hilding (1 973), and Foss and Flottorp ( 1974).

188

GUNTER EHRET

blrth I

~

2

1 "

"

"

3 ~

'

"

I "

6

5

7

8

9

10

12

11

months

'

adult

n

bleating

-4

mew and whistle composite vocalisation of

vp in estrus

puma

-

: = = = I I P I I = = = = I ' = P I r l = = 5 = I = = = = P I D I I L

bleattna

- -4 mew

__

main call

main COII with qrunt element ---.. .-.-. -. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

tiger

bleotina

- -4 mew

c main call 5 main call with qrunt element

I

---jaguar

bleating

--I

mew motn call with qrunt element

_-----

structured call r e a u e n c L

lion

I . , , . , . . . , . . , . . , , , , , .

birth

1

2

-

structured call s e a u e n c b

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

3

L

5

6

7

6

9

II T

10

>

11

>

%

12

months

'I

adult

FIG. 4. Puma, tiger, jaguar, lion: Diagrams of the development of vocal behavior (for further explanations, see Fig. 2). From Peters (1978).

Figure 5 shows that newborn puppies are unable to hear. First action potentials in the auditory nerve (Pujol and Hilding, 1973) and cortex-evoked potentials (Chaloupka et al., 1968) appear around day 7;behavioral responses, however, were not detected before day 14 (Foss and Flottorp, 1974). The development of the auditory system continues until day 35. Neonatal puppies can produce a variety of sounds called mews, squeals, squeaks, clucks, grunts, and whines. These sounds are all emitted in situations of isolation or slight distress. These typical juvenile vocalizations disappear by about day 39. A second group of calls called screams and yelps appear between the first and the tenth day of life depending on the breed of the dog. The yelps may be precursors of the barks and growls, the typical calls of the adults, which first occur around day 12 (also depending on the breed). Call sequences or mixed sounds develop latest around day 17. At day 28 these vocalizations reach their adult patterns. The greatest

189

DEVELOPMENT OF SOUND COMMUNICATION

-

w .-_-.-

L _ _ _ _

hears Dure tones

.-.

-

barks. qrowls

L . . . _ _ _ _mixed __

c

*

sounds

sexually mature eyes open

weaning

I

I

9-11 weeks

1

change in the vocal repertoire coincides with the onset of hearing and of opening of the eyes. C. RODENTS

The vocalizations of rodents have been the subject of a large number of studies. The investigations can be divided into two main groups: records of the vocal repertoire of a species or analyses of one special call and the associated behavior. Records of repertoires exist for the collared lemming (Brooks and Banks, 1973), the guinea pig (Eisenberg, 1974; Arvola, 1974; Berryman, 1976) and other hysticomorph rodents (Eisenberg, 1974), and the house mouse (Ehret, 1975a). Vocalizations most frequently studied are the pure ultrasonic calls of young and adult murid and cricetid rodents. In the following section, the ontogeny of vocal behavior and hearing in the guinea pig, rat, and house mouse will be presented in more detail. I.

Guinea Pig (Cavia porcellus)

Figure 6 combines data on the development of hearing from Scibetta and Rosen (1969), Romand (1971), Pujol and Hilding (1973), and Clements and Kelly (1978). The nomenclature after Berryman (1976) was used for the vocali-

190 P

GUNTER EHRET

-15

-12

-9

-6

-3

tnrth

3

6

9

12

15

18

21

days

,

weeks5 6 7

adult

I

__..._

h e a r s pure tones

b

eyes open

weaning

1

1

sexually mature ll

I

FIG.6. Guinea pig: Diagram of the development of hearing and of vocal behavior (for further explanations, see Fig. 2).

zations. The same kinds of calls were described in Arvola (1974) and Eisenberg (1974), although they were given different names. Guinea pigs are precocial animals which are born well developed. They start hearing in the uterus about 12 days before birth (gestation time about 65 days; Romand, 1971). Auditory cortex-evoked potentials are fully developed at birth (Scibetta and Rosen, 1969). The young orient to sound at birth but binaural interaction seems to develop further until about day 21 (Clements and Kelly, 1978). Guinea pigs can produce a variety of sounds at birth and the vocal repertoire of the young is almost identical with that of the adults (Fig. 6). Only the “tweet” is a typical call of the young and is rarely heard after day 10. The “chirrup,” occurring only occasionally, may be a disturbance call of the adults, but too few observations are available to exclude its presence in the repertoire of the young. Except for the number and situations of occurrences, no obvious development of call patterns seems to take place. 2 . Rat (Rattus norvegicus) Unlike guinea pigs, rat pups are born in rather embryonic state. The onset of hearing occurs late at about the tenth day (Fig. 7) with further development of

191

DEVELOPMENT OF SOUND COMMUNICATION

sensitivity and frequency range up to about day 25 (Wada, 1923; Crowley and Hepp-Reymond, 1966; Chaloupka et af., 1968; Jewett and Romano, 1972). Data on the sound production of rat pups were taken from Allin and Banks (1971), Okon (1972), Oswalt and Meier (1975), Hofer and Shair (1978), and Sales and Smith (1978), and those of adult rats from Sales (1972a,b), Barfield and Geyer (1975), McIntosh et al. (1978), and Corrigan and Flannelly (1979). Figure 7 shows that rat pups produce pure ultrasounds in response to handling, isolation, and temperature stress from birth. They reduce the rate of calling drastically after about the first 2 weeks and finally cease ultrasound production depending on the stimulus, by day 30 the latest. An audible pain call of the young develops into the adult one probably within the first 24 days. Adult rats emit pure ultrasounds during agonistic and sexual behavior. The ultrasounds of dominant rats are short and have higher frequencies (40-70 kHz); those of submissive rats are longer and the frequencies are lower (20-30 kHz). During sexual encounters high- and low-pitched ultrasounds were recorded. The largest changes in the vocal repertoire are evident in about 14-day-old pups in which the eyes are open and which have good motor control (Altman and Sudarshan, 1975). The development of hearing proceeds fastest between day l l and day 20.

brth

2

6

1

8

10

12

16

IL

I6

r"~"'""""""""""""'

2L

28

26

30 doys

Odul! I/

hears p u r e tones

.....

t

22

20

--.

-

-__-----------------------------------..............................

U S on handllna

U S on isolotion

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

U S on temperalure stress

4

.-I

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

I

poin call

.

.

.

.

.

.

. hgh U S agonistic ............... .................

--

encounter

................. law U S ogonistic encounter ................. ....... hi g?. U 5 . -..r e x u o I behavior ............... ................ law U S sexuol behavior .............

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

rn o t or cont ro1

..........

eyes open

I.

birth

, 2

.

,

L

,

.

6

,

, , , , , 8 10 12

I,

, , , IL 16

sexuolly moture

weaning ,

1

, , , , , , , , , 18 20 22 2L 26

,

*

28

, ,

,

30 days "

1 odJt

FIG. 7. Rat: Diagram of the development of hearing and of vocal behavior. US, Ultrasound (for further explanations, see Fig. 2).

192

GUNTER EHRET

3 . House mouse (Mus musculus) Among the rodents the ontogeny of vocal behavior in the house mouse has been studied in most detail. Figure 8 includes data on the development of hearing from Alford and Ruben (1963), Mikaelian and Ruben (1963, Lieff et al. (1975), Ehret (1976a, 1977a), Henry and Haythorn (1978), and Willott and Shnerson (1978). For the ontogeny of vocalizations (Fig. 8) data from Noirot (1966), Noirot and Pye (1969), Okon (1970a,b), Bell et al. (1972), Sales (1972b), Whitney et al. (1973), Ehret (1975a, and unpublished), Nyby er al. (1976), and Sales and Smith (1978) are combined. The house mouse starts hearing at about day 10 after birth and the development proceeds until about day 18 (depending somewhat on the strain). The develop mental rate is highest between days 12 and 16. At birth the mouse pups produce one call which turns into the pain call of the young. From this, the pain call of the adults develops. Shortly after birth mouse pups can emit pure ultrasound in response to isolation, handling, and temperature stress. Ultrasound production in the young normally stops at about day 13, however, ultrasonic calls due to severe temperature stress can be recorded until day 19. Two other vocalizations are

II

heors pure ----tones

___

5

dtscrimrnotton of tones in noise

-_--

&

coll when struaalrnq for teats lip smockina

-I

U S in sexuol er$o_u_n_te-ri ond aenitol sntffino

-

I US of femo!e in confusion

~

toil rattling in ogonistic encounters-

eyes open

I

I birth 2

L

6

8

10

12

sexually mature

6-8 weeks

weoning

1L

16

18

20

II

22

24 days

I adult

FIG.8. House mouse: Diagram of the development of hearing and of vocal behavior. US, Ultrasound (for further explanations, see Fig. 2).

DEVELOPMENT OF SOUND COMMUNICATION

193

independent

FIG.9. House mouse: Frequency ranges of some calls during development. I, U1trasonic calls of the pups; 11, pain call; III, call when struggling for the teats; IV, pure ultrasound of adults during sexual encounters (a, frequent; b, weak and rare); V, defensive call of nonreceptive females. Note the rapid decrease in frequency range of the pain call between day 12 and 25.

typical of young mouse pups, the calls when struggling for the teats and the sound of smacking lips. Both disappear at day 13. Starting at about day 24 typical calls of the adults occur, the defensive call of nonreceptive females, the pure ultrasounds of males and females during sexual encounters, and the call of confusion of females, another pure ultrasound. Finally, tail rattling occurs when males get involved in agonistic encounters. The largest changes in the vocal repertoire are found around day 13, when the typical calls of the mouse pups disappear. At this time their eyes are open and their motor skills are quite well developed (Fox, 1965). This also becomes evident in Fig. 9 where the frequency bands of the calls are plotted against age. Both young and adult mice are able to produce pure ultrasounds and low-frequency calls. There is practically no sound production in undisturbed situations between day 13 and day 24. Only the pain call can readily be elicited and it shows a sharp drop in frequency range during this time. The auditory sensitivity of adult mice (Ehret, 1974), their ability to discrimi-

194

GUNTER EHRET

nate frequencies and intensities (Ehret, 1975b), and complex sound patterns (Ehret, 1976b) are sufficient for them to hear and to discriminate all the different calls including the ultrasound within at least 1 m from the sender under free-field conditions and the sender facing the receiver. This range expands drastically for low-frequency calls, D. PRIMATES The author was unable to locate any study on the ontogeny of hearing in nonhuman primates. Many data, however, are available for man. On the other hand, vocal repertoires including sounds of the young have been reported for quite a number of primates including lemurs (McGeorge, 1978), marmoset monkeys (Epple, 1968), howler monkeys (Baldwin and Baldwin, 1976), titi monkeys (Moynihan, 1966), cebus monkeys (Oppenheimer, 1973), langurs (Vogel, 1973), squirrel monkeys (Winter el al., 1966, 1973; Schott, 1975), mangabeys (Chalmers, 1968), talapoin monkeys (Gautier, 1974), macaques (Rowell and Hinde, 1962; Itani, 1963; Takeda, 1965, 1966; Grimm, 1967; Chevalier-Skolnikoff, 1974; Green, 1975a), colobus (Marler, 1970a, 1972), gorillas (Fossey, 1972), and chimpanzees (Marler and Tenaza, 1977). A more complete list can be found in Sebeok (1977, Chapters 33-36). The time courses of the development of vocalizations as shown in Figs. 2-8 are very difficult and time consuming to measure in primates especially apes because the general postnatal development is comparatively slow. Chimpanzees, for example, are weaned by about 24 months and reach sexual maturity after about 8 years. Therefore most authors distinguish only between infants, juveniles, subadults, and adults and relate the vocalizations to these age groups. In the following, diagrams of the development of sound production will be presented for the stumptail macaque and man. In addition, a different scheme will be used for listing the vocalizations of chimpanzees of different ages. 1 . Stumptail Macaque (Macaca arctoides) Chevalier-Skolnikoff ( 1974) investigated the ontogeny of communication in the stumptail macaque and Fig. 10 is a modification of a table from her study. For the first 2 weeks the newborn infants emit only three different calls, the chirp, the gecker, and the scream. The trilled whistle appears at the end of the second week and the grin at the end of the third week. The twit is heard in infants only between the fourth and sixth week. During the ninth week the whispered chirl, and in the twelfth week the screech are added to the repertoire. In the fifth month the coo, the negative squeak, and the whistle shriek can be recorded, and in the sixth month the positive squeak and round-mouthed chirl. All of these vocalizations of the young, with the exception of the chlrp, the gecker, and the twit, develop into the corresponding adult calls. During development the calls

DEVELOPMENT OF SOUND COMMUNICATION

195

generally gain intensity and lose pitch and sometimes are modified in their structure. The twit, chirp, and gecker are typical calls of infants and juveniles and do not appear in the adult repertoire. Instead there are some vocalizations typical for the adults such as chirl, crow, roar, wailing roar, grunt, and bark. The largest changes in the vocal repertoire occur between the third and fifth month of life, when the mother begins weaning. 2 . Chimpanzee (Pan troglodytes) The development of the vocal repertoire of chimpanzees is presented in Fig. 1 1 which is derived from Table 2 in Marler and Tenaza (1977). It shows the relative frequency of occurrence of the vocalizations in four different age groups: infants, juveniles, adolescents, and adults. In this diagram no distinction was made between sexes and between young and old adults. Disregarding the last four vocalizations (grunt, cough, wraaa, and lip smack) which together make only 5.5% of all vocalizations, it is evident that different age groups prefer different calls. Laughter and whimpers are most frequently produced by infants. The pant-grunt, pant-hoot, pant, and rough grunt are most typical for adults.

196

-

GUNTER EHRET

infants

juveniles

laughter

112%l

whimper

18%1

=

scream

(9%)

19

17

squeak

111%)

1 9

16

woo bark

13.5%1 1 7

3

bark

ILW)

16

2

rough grunt l i 5 O / d

10

72

38

11

B8

0

pant

(3.5%1

IL

15

pont hoot

128%) 12

1

pant grunt

112%)

1

0

grunt

(2%)

0

2

cough

(1.5%)

3

0

wraoa

Il%)

0

0

Iipsmock

(1%)

0

0

-- -adolescents

2

adults

15

37

D l 7

29

55

= =

37

L8

35

55

L7

L5

10

80

87

L

86

11

89

10

26

72

27

m70

09L

16

65

=

35

FIG.1 1 . Chimpanzee: The relative percentage frequencies of Occurrences of vocalizations in four age groups. The length of the bars expresses the indicated percentage of vocalizations of this type within an age group. After the name of a vocalization its percentage of Occurrence within the total repertoire is indicated.

Juveniles are rather nonvocal and do not contribute much to the total vocal output, although they can produce most of the commonly used calls. The bark, waa-bark, squeak, and scream are heard relatively often from adolescents. Obviously, adults emit all vocalization and they do so more frequently than any of the other age groups. This categorical description is only one of the possible ways of characterizing the vocal repertoire of chimpanzees. Their vocalizations are highly graded and there are many intermediate forms between the categories shown in Fig. 11. Nevertheless, infants and juveniles prefer calls different from those used by the adults. In addition, most calls show an alteration in their frequency spectrum (e.g., lowering of pitch) during the ontogeny of the individuals.

3 . Man The ontogeny of hearing and the development of vocalizations in human infants have been studied by many scientists from different disciplines. In man one has to distinguish between the development of speech and the development of nonspeech sounds (e.g., crying, laughing). The latter are comparable to animal vocalizations and both contrast with speech by their lack of a lexical syntax (Marler, 1977). Little attention has been paid to the development of nonspeech sounds in human infants and juveniles since speech plays such a predominant role in our vocal behavior and intraspecific communication.

197

DEVELOPMENT OF SOUND COMMUNICATION

Figure 12 combines data on the ontogeny of hearing from Fleischer (1955), Leventhal and Lipsitt (1964), Tanaka and Arayama (1969), Davis and Onishi (1969), Eisenberg (1969), Eimas et al. (1971), Barnet ef al. (1975), and Salamy and McKean (1976). The diagram of the development of vocalizations and speech acquisition is composed of data From van Oordt and Drost (1963), Sheppard and Lane (1968), Wolff (1969), Lieberman et al. (1971), DiSimoni ( 1974a,b), Tingley and Allen ( 1975), Kent ( 1976), and Fitzgerald et al. ( 1977). Hearing starts in the uterus in the seventh month of gestation (Fleischer, 1955; Tanaka and Arayama, 1969) and adult waveforms of cortical-evoked potentials are evident between the third and sixth month after birth (Salamy and McKean, 1976). Adult temporal resolution, however, which is reflected by latency decreases in the evoked potentials, occurs relatively late, 1 year after birth (Barnet et al., 1975). Newborn babies can localize sound and discriminate its pitch (Leventhal and Lipsitt, 1964). One-month-old babies already show a categorical perception of speech signals measured by their discrimination of voice onset times. Thus they divide a p-b continuum almost at the same voice onset times as adults do (Eimas et al., 1971). At birth babies can emit only one kind of vocalization, the undifferentiated cry. After about 1 month their cries start to differentiate and from the second month the repertoire of nonspeech vocalizations expands to include different

__

-,

echolalia limitallon 0 1 others)

one-word senlpc-e-s-. two-word

-4

sentences..

-. .

II

multlword sentences

1 eyes open

solid food

1

1

II

mostery ot syntox inost_ery ot DhOnOlOQY

puberty

198

GUNTER EHRET

A 504

P Y

.

both sexes

-e

ternole

300.

0

e

- - - -1 --__-

--. .--.-

al

5 200.

*.

0 C

r

-

-..- - - __ -

100,

I

rnde

01

0

/I

2

L

6

8

10

12 14 age [yearsl

16

18

"adult

FIG. 13. Man: Development of the fundamental frequency of human vocalizations. Modified after Kent (1976).

forms of cry, cooing, babbling, and laughing. The frequency spectra of these nonspeech vocalizations change until puberty (about 13 years in girls and 17 years in boys). The precursors of pronouncing words, lallation and echolallation, occur at about 6 and 8 months, respectively. By about 9-15 months one-word sentences and by about 2-4 years multiword sentences can be formed. Syntax is mastered by about 6 years, and the variability of the formant frequencies and of the minute timing of the speech decreases until the age of 9-11 years. By 11 years the process of speech acquisition is finished. The vocal fundamental frequency of the adults, however, is reached in the age of puberty. Figure 13 is a modified replot from Kent (1976) and shows the change of fundamental frequency with age. The largest changes in the fundamental frequency occur during the first 3 years. During this time the most rapid development of the vocal repertoire, especially of speech, is found (Fig. 12). We can only speculate, however, on how nonspeech vocalizations develop. Everybody knows different kinds of laughing (e.g., chuckling, yelling, fleering, sniggering) and different kinds of crying (e.g., cries of pain, wailing, sobbing). It is not known when and how the patterns of these vocalizations and sounds reach the typical forms produced by adults. IV.

CHARACTERISTICS AND COMMON TENDENCIES OF THE DEVELOPMENT OF VOCAL BEHAVIOR

The development of hearing and vocal behavior presented in Figs. 2-13 may look straightforward and comprehensible and quite natural. Why should hearing

DEVELOPMENT OF SOUND COMMUNICATION

199

and vocalizations not develop during a period of time when all the rest of the organism does? It is clear that a development takes place. But it is also evident that species differ in their development in many respects. Thus Figs. 2- 13 are not more than a framework which we now should use to ask questions about their physiological and functional background. The first series of questions will deal with changes in the physical appearance of vocalizations during ontogeny. Second, we shall be concerned with hearing and sound production. Third, questions about the stimuli and contexts of vocalizations will be discussed, and fourth, a closer look at the physiological state of the sender, his arousal, excitation, or motivation will be necessary. A.

DEVELOPMENT OF PHYSICAL CHARACTERISTICS OF VOCAL OUTPUT There is one general statement which is true for the mammals discussed in detail in Section I11 and, in addition, for some marsupials (Eisenberg et al., 1975), shrews (Gould, 1969), bats (Gould, 1971), the rock hyrax (Fourie, 1977), some hystricomorph rodents (Eisenberg , 1974), pigs (Kiley, 1972), and different species of monkeys and apes (see Chapters 34-36 in Sebeok, 1977): the number of different calls produced by adults is larger than or at least equal to the number made by the young. Often a considerable increase in vocal repertoire can be observed during ontogeny. A second statement which, however, is based on a smaller number of studies, is that the pitch of a call occurring in both young and adults decreases during the development. Good examples are the pain or distress calls in cats, dogs, house mice, stumptail macaques, and man (compare Figs. 9 and 13). These two effects of development can be explained by the postnatal structural and functional maturation of the nervous system and of the vocal tract. Since myelinization of the nerve fibers is not yet complete at birth and further connections between neurons are formed postnatally it can be assumed that central motor patterns for a differentiated vocalization are not necessarily available at birth. Further, the dimensions of the vocal tract generally increase as the size of the animal increases which may lead to a decrease in fundamental and resonance frequencies and thus to a lower pitch of the vocalizations. However, better motor control of the laryngeal muscles may also increase the subglottal pressure and by that increase the fundamental frequencies of the calls (Sheppard and Lane, 1968). The influence of both growth and pressure increase can be seen in the change of fundamental frequency in man (Fig. 13). The same call shows interindividual variations in frequency patterns, duration, intensity, and timing of a call sequence. The degree of overall variation and the means of the parameters mentioned sometimes change systematically with age. For example, the bandwidth of the fundamental frequency of ultrasonic calls of rodent pups often increases with age (Sales and Smith, 1978). On the other hand the variability of formant frequencies in macaque and human vocalizations decreases with age (Chevalier-Skolnikoff, 1974; Kent, 1976).

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The variability within call types and their changes during development sometimes make it difficiilt to decide whether various deviations of one basic form should be included in one category or be given different names, and thus appear as separate calls in the repertoire. A common feature of probably all mammalian vocal repertoires is that at least some calls within a given repertoire are part of a continuum of physical properties and are not completely distinct forms. This has been explicitly stated for some shrews (Gould, 1969), the rock hyrax (Fourie, 1977), the dog (Cohen and Fox, 1976), some ungulates (pigs, cattle, horses; Kiley, 1972), the guinea pig (Berryman, 1976) and other hystricomorph rodents (Eisenberg, 1974), the lemming (Brooks and Banks, 1973), the squirrel monkey (Schott, 1975), the stumptail macaque (Chevalier-Skolnikoff, 1974), and the chimpanzee (Marler and Tenaza, 1977). Thus some vocalizations of the adults can be derived via intermediate forms from vocalizations of the young (compare Figs. 2 , 3 , 5 , 8 , 10, and 12). Whether vocalizations in a repertoire are considered distinct or graded often depends on the amount of effort that is made to record an as complete repertoire as possible. With respect to the development of a repertoire, however, different mechanisms could be involved in producing distinct calls de novo or developing different call types from a common basic call by varying parameters. Mechanisms such as maturation of peripheral motor control and growth of the vocal tract would be the basis for a continuum between vocalizations. On the other hand, the extremes of variation of a basic form could have been favored in their occurrence during the ontogeny and phylogeny with the result that today we differentiate these extremes in the repertoire of the adults.

B.

DEVELOPMENT OF VOCALIZATIONS DEPEND ON HEARING?

DOES THE

From Figs. 2-12 it is clear that the bat Antrozous, the dog, the rat, and the mouse do vocalize without hearing. Further examples are the opossum (Larsell et a f . , 1944; McManus, 1970) and many murid and critecid rodents such as the mongolian gerbil (McManus, 1971;Fink et al., 1972; de Ghett , 1974; Broom et af., 1977) and the golden hamster (Okon, 1972; Pujol and Abonnenc, 1977). It is also evident that a number of different vocalizations can be emitted by the rat and mouse before they are capable of hearing. The mouse, for example, has a repertoire of single-tone ultrasonic calls, broadband and narrowband harmonically structured calls, and unvoiced sounds (Figs. 8 and 9), which are produced for at least 9 days without auditory feedback. Thus the inevitable conclusion is that the neonatal vocalizations of the above-mentioned mammals are based on an innate neural and motor control system like other reflexes of newborns (righting, rooting, magnus reflex, crossed extensor reflex). No auditory feedback or learning is involved. This simple conclusion has to be confirmed for those mammals that can hear from birth [e.g., guinea pigs, sheep (Bernhard et al., 1959), apes, and

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man]. Only few deprivation experiments have been done in mammals to clarify whether species-specificauditory cues or hearing of self-emitted vocalizations are necessary for the development of a normal adult repertoire. Gould (1975b) has shown that young Epresicus bats do not need species-specific auditory feedback for the development of the FM echolocation pulses; hand-raised infants emitted the normal adult calls. Berlin et al. (1969) report that the adults of Variant Waddler mice (a deaf strain of house mice) produce pain calls different from normal ones. However, adult mice of another deaf strain (DF/DF) emit quite normal pain calls. It seems, therefore, that the frequency spectrum of pain calls of different strains of mice depends on the genetic background of the strain rather than on auditory experience. It has to be mentioned, however, that the threshold for emitting a pain call at all was higher in deaf than in hearing strains. Fox (197 1) found that dogs reared in isolation vocalized much less frequently than those raised with conspecifics although they were still capable of producing all normal sounds. This supports the idea that species-specific input enhances vocal behavior. Winter et a/.(1973) raised squirrel monkeys (with normal hearing) in isolation and found that normal vocal behavior developed. Even an infant deafened 5 days after birth developed a normal adult repertoire. This is consistent with similar findings of Riggs et al. (1972) in the squirrel monkey. Therefore, Winter et al. (1973) concluded that the vocal output of the squirrel monkey is genetically determined. No auditory input, species-specific or not, seems necessary for development of normal vocal behavior. Another strong indication that frequency characteristics of calls are genetically determined comes from vocalizations from a hybrid young Cercopirhecus monkey crossed from C. ascanius and C.pogonias (Gautier and Gautier, 1977). The young hybrid emitted calls similar to those of the mother, others resembling those of the father, and intermediate calls composed of elements of calls from both parents. These results in mammals are different from those in man in so far as speech acquisition is impossible in congenitally deaf infants (Lenneberg, 1967; Lenneberg and Long, 1974). It is obvious that hearing and imitating a language are essential for learning it. Thus it cannot be expected that deaf human infants get beyond the state of lallation (Fig. 12). A comparison of the development of nonspeech signals in deaf and hearing children cannot be made because of lack of data. The only other case of a consistent modification of a basic sound pattern by learning is the local dialects of Japanese macaques with regard to sounds associated with provisioning (Green, 1975b). Separate populations of these monkeys have their own dialects which most probably are maintained by learning and not genetically, Green (1975b) suggests that learning dialects associated with food supply may be compared and evolved similarly to local customs of handling

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food. Thus vocal learning in this case may be restricted to the stimulus complex food. So far, there is no evidence in mammals (except for Japanese macaques) that the qualities of a vocalization (frequency and temporal structures and intensity) have to be learned or are otherwise influenced by hearing species-specific calls. This is very different from birds, where many species require species-specificor other auditory experience during their development in order to produce normal calls or songs as adults (e.g., Nottebohm, 1970; Marler, 1970b; Marler and Mundinger, 1971). More research, however, is necessary to prove whether or not hearing species-specificsounds or hearing in general has an effect on the development of vocalizations in mammals. The striking coincidence of major changes in vocal repertoire and onset of hearing in Antrozous (Fig. 2), dog (Fig. 3, rat (Fig. 71, and mouse (Fig. 8) suggests an influence of hearing on sound production. In Antrozous, shortly after hearing becomes manifest, the FM orientation call develops, It has been shown that species-specific auditory input is not required for the ontogeny of echolocation calls in Eptesicus (Gould, 1975b), but it has not been demonstrated that deaf bats develop a normal FM call. Dogs start to produce barks and growls shortly after the onset of hearing. Again no data from deaf animals are available. In rats, mice, and mongolian gerbils the ultrasonic calls of the young disappear after the onset of hearing. Although not indicated in Figs. 7, 8, and 9, it has to be mentioned that hearing starts at comparatively low frequencies so that until day 13 or 14 mice, for example, are actually deaf for frequencies higher than about 40 kHz, the main frequency region of the ultrasonic calls (Ehret, 1975a, 1976b, 1977a). We are testing now, whether sound production in mice that are not congenitally deaf is influenced by hearing. Hearing in general and hearing species-specific sounds in particular have been shown already to have one influence on vocalizations of adults (Berlin et al., 1969; Fox, 1971; Winter et al., 1973). Sounds can be elicited much easier in hearing mammals with social experience than in deaf or deprived ones. Thus the effect of hearing on vocal behavior seems to be one of causing calls to be more readily and frequently emitted. Further experiments will show whether the quality of the emitted sound can be influenced (see Green, 1975b). Another open question is whether a vocal repertoire which has developed quite normally without auditory feedback will be used in the appropriate behavioral contexts. C.

Do EXTERNAL STIMULI AND BEHAVIORAL CONTEXTS INFLUENCETHE DEVELOPMENT OF VOCALIZATIONS?

During the ontogeny of an animal, the time of the development of the vocal repertoire, animals are exposed to an increasing number of different behavioral contexts which are accompanied by a variety of environmental stimuli. On the other hand, stimuli and situations closely related to the nest, to maternal care,

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and to littermates disappear. This poses the question of whether there are context-specific and/or stimulus-specific releasers for certain vocalizations. A necessary condition for a theory of context- or stimulus-specific vocalizations is that the complete neural mechanisms and motor patterns for vocalizations are latently present in the nervous system and are just “waiting” to be released. The vocalizations would just be reflexive. This is true at least for the first time an animal is confronted with a certain stimulus or context and vocalizes specifically. After the onset of hearing and after experience with special behavioral contexts and stimuli the neural mechanisms and as a result the motor patterns for sound production could be modified; this would become evident as a variation of the vocal output. A number of investigations present evidence that behavioral contexts and external stimuli play a decisive role in eliciting vocalizations. For example, only female rock hyraxes during labor emit the hiccup, cough, and hoarse moan (Fourie, 1977). Kittens and cats produce the “mew” call when expecting food (K. A. Brown et al., 1978). Infant guinea pigs emit a “tweet” only when stimulated by their mother at the anogenital region in order to make them urinate and defecate (Berryman, 1976). Adult nonestrus female house mice emit a defensive call when a male tries to mount (Ehret, 1975a). Adult male vervet monkeys emit stimulus-specific alarm calls such as the “chutter” which is associated with man or snake but not with other potential enemies or predators (Struhsaker, 1967). This list of examples of context or stimulus-specific vocalizations could certainly be enlarged. On the other hand, many vocalizations are emitted in more than one behavioral context or to several stimuli. Examples are the clicks of shrews which are emitted by the young when displaced from the nest, by adults when exploring a strange situation, and during courtship of the males (Gould, 1969); the 22-kHz ultrasound of male adult rats in agonistic and sexual encounters (Sales, 1972a,b; Geyer and BarField, 1978; Adler and Anisko, 1979; Corrigan and Flannelly, 1979); ultrasonic calls of many rodent pups on isolation, handling, and temperature stress (compare Figs. 7 and 8, also Noirot, 1972; Sales and Smith, 1978); the grunts of pigs that are, among other things, vocalizations of greeting, tactile stimulation, and frustration (Kiley, 1972); the pant-hoot of chimpanzees which is given in many situations such as listening to a distant group of conspecifies, rejoining the group, eating prey, and when in the nest at night (Marler and Tenaza, 1977). From all these examples it is clear that vocalizations of young and adult mammals can, but need not, be context- or stimulus-specific. Thus a common developmental strategy for establishing a fixed relationship between a particular context or stimulus on the one hand and a specific vocalization on the other does not exist. There is no one-to-one correspondence between the development of the environment of the young and the development of their vocalizations. Nevertheless, the largest changes in the vocal repertoire usually occur just when typical

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behavioral contexts and stimuli of infant life (e.g., being nursed and groomed by the mother, close tactile contact with littermates) are being replaced by contexts and stimuli typical for the adults (compare Figs. 2-12). This time, during which interactions with conspecifics take on a new quality, is sometimes called the period of socialization (Elliot and Scott, 1961; Fox, 1966). Again there are only few quantitative data on possible causal relationships between the occurrence or disappearance of calls in the vocal repertoire and contexts and stimuli. Many calls are named after the situations in which they can be recorded. Mostly, however, stimuli or stimulus combinations were not quantitatively measured and the whole behavioral context was not well controlled. Probably best understood are the circumstances under which the ultrasound of young and adult murid and critecid rodents is produced. Ultrasound production by rodent pups can readily be elicited by three different stimulus situations: low temperature, tactile stimuli like handling, and isolation. The rate of production of ultrasound depends on the degree of deviation of the body temperature from normal and on the state of the development of temperature regulation (Okon, 1970a, 1972; Allin and Banks, 1971; Brooks and Banks, 1973; de Ghett, 1974, 1977; Geyer, 1979). Ultrasound on temperature stress ceases when full temperature regulation is achieved. The rate of ultrasound elicited by handling decreases from birth and disappears when the sensory systems (seeing and hearing) are functioning and motor control has developed enough for rapid and wellcoordinated body movements to be possible (Folt, 1965; Okon, 1970b, 1972; Altman and Sudrashan, 1975; Sales and Smith, 1978). Finally isolation is represented by lack of body contact with the mother and/or littermates and by a lack of familiar olfactory cues (Oswalt and Meier, 1975; Sales and Smith, 1978; Hofer and Shair, 1978; Conely and Bell, 1978). In most of these studies it was suggested that the amount of stress produced by the stimuli (or by the lack of appropriate stimuli) changes during development and causes a corresponding change in parameters, predominantly rate of ultrasound production. Adult rodents, especially males, emit ultrasound during sexual behavior (Sales, 1972b; Whitney et al., 1973, 1974; McIntosh et al., 1978). Most data exist for laboratory mice and rats; the latter use the same two kinds of ultrasound not only in sexual but also in agonistic encounters (Sales, 1972a; Corrigan and Flannelly, 1979). Thus these ultrasounds in rats are not expected to be stimulusspecific. They are elicited by the complex stimulus “female” or special aspects of it such as olfactory cues (Barfield and Geyer, 1975) and by the complex stimulus “aggressive male” and, after experience, by certain aspects of it (Corrigan and Flannelly, 1979). Similarly, ultrasound production to female urine can be conditioned in adult male mice after previous experience with females (Dizinno et al., 1978). These examples show that the actual repertoire of sounds a mammal can produce is influenced by external stimuli and contexts less than the frequency with which one particular call in the repertoire is used. During development one

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call type may be produced in response to an increasing number of different stimuli and behavioral contexts. Mechanisms for this convergence of stimuli and contexts on the releasing mechanism of one call, which has been described for many other calls of species mentioned so far, have not been investigated. We have seen that the vocal repertoire of mammals (except man) itself seems to be inherited (Section IV,B) and influenced only by the maturation of the central nervous system and the vocal tract (Section IV,A). As demonstrated in this section, the situations leading to the occurrence of one call type can change and increase or decrease in number. This means that the neural mechanisms triggering the different vocalizations are subject to changes during the ontogeny. These mechanisms can be influenced by sensory input like hearing as already discussed, so that, e.g., the threshold level is decreased or increased. Further, during the development an increasing number of stimulus parameters can converge on one mechanism triggering one particular call. Convergence of stimuli can also be reversed so that one stimulus or one behavioral context gives rise to a series of call types from one repertoire. Such series of different calls are usually not heard from neonates but occur later in development when the repertoire has broadened. Call series are produced, e.g., by dogs (Cohen and Fox, 1976) and some felidae (Peters, 1978), when group members are separated, by rock hyrax in situations of aggressive or defensive threat (Fourie, 1977), by pigs in frustration situations (Kiley, 1972), and by stumptail macaques during weaning (Chevalier-Skolnikoff, 1974). Although behavioral contexts and stimuli for call series have not been well defined, mechanisms of divergence from one stimulus or one behavioral context to different calls seem to develop. It must be emphasized that we should consider only call series here-although for many mammals different calls were recorded in the same situation-because we can be more confident then that actually one stimulus or behavioral context elicited the series of different calls. The appearance of call series late in the ontogeny of a mammal may be related to maturation processes of the nervous system, which allow a higher complexity of vocal output. At least mechanisms for an orderly triggering of motor patterns of the different call types have to be present. This section has tried to explain some developmental characteristics of a vocal repertoire in relation to external stimuli and behavioral contexts. In the following section an alternative approach via emotional factors within an animal will be taken and finally both will be combined.

D. DOESAROUSALINFLUENCE THE DEVELOPMENT OF VOCALIZATIONS? In an interesting article Bell (1974; see also Bell, 1979) hypothesized that the ultrasonic calls of young and adult rodents reflect states of arousal and produce arousal in animals nearby. At the moment, we shall consider arousal in the

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sender only. Whether arousal can be arousal producing will be discussed in Section V. Bell (1974) argued that cold stress and handling in mouse pups could be the basis for different states of arousal, which would then determine the kind of ultrasound emitted. Similarly he attributed the two kinds of ultrasound from adult rodents to different states of arousal, high during fighting and copulation and low after fighting and before and after copulation. He suggested that “changes in acoustic parameters of the vocalizations may reflect simply the energy in emitting the signals.” Kiley (1972), from her study of vocalizations of ungulates, concluded that many vocalizations are controlled by the level of excitement and the momentary stimulus interest of the animal. Also Fourie (1977) found in the rock hyrax that the level of excitement and of stimulus interest is decisive for the type of sound emitted. Cohen and Fox (1976) speak of an “emotional language” of the dog and suggest that the gradations between vocalizations may give an exact picture of the degree of arousal, motivation, and intention in a given behavioral context. The findings of these authors seem to be in close agreement with Bell’s hypothesis. However, these authors also found that at least a few calls were related to situations or stimuli rather than to an obvious state of arousal. If we consider arousal or excitement as a one-dimensional quantity* varying only on an intensity scale, we may a priori state that arousal certainly cannot be the only factor responsible for or an adequate measure of the probability of the occurrence of a particular vocalization from a given repertoire. The vocal repertoire of mouse pups, for example, is composed of pure ultrasounds, broadband harmonically structured calls, narrowband harmonically structured calls, and narrowband noisy clicks (Figs. 8 and 9). These sounds differ not only in their physical characteristics but also in the situations in which they can be elicited so that for all calls together any ranking on an arousal scale would be arbitrary. Also for all the other mammals the state of arousal alone does not seem to be a sufficient explanation for the great variety of the vocal repertoires. If one considers only calls which occur typically during sexual behavior, or others typical of mother-infant interactions, or of threat behavior, it does not seem logical to attribute consistently different arousal levels to these vocalizations unless these different degrees of arousal are independently measured by endocrinological or neurophysiological methods. One would have to assume sex-specific states of arousal in connection with calls produced only or predominantly by either sex. Similarly, the loss of a vocalization during the ontogeny would mean that a certain level of arousal will no longer be reached, and the addition of a new call type would be due to an additional state of arousal then occurring in the animal. In addition to the difficulties of linking vocalizations directly to different states of 2A discussion of problems with and limitations of the arousal concept can be found in Hinde (1970).

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arousal or excitement, there are many studies which clearly show that the production of certain calls is stimulus or context dependent. Some examples have already been given in Section IV,C. Further ones are the production of ultrasonic calls by rat pups on special odor cues (Conely and Bell, 1978), the bark of pigs in a startle situation (Kiley, 1972), tooth-chatter of collared lemmings on touching them or blowing on them (Brooks and Banks, 1973), and laughter in infant chimpanzees during play (Marler and Tenaza, 1977). Arousal obviously is not the only determinant of a mammal’s vocal repertoire, and just an intensity scale of states of arousal cannot alone explain the ontogeny of the vocal behavior. However, the degree of arousal or excitement in an animal certainly contributes, together with external stimuli and the behavioral contexts, to eliciting a particular vocalization from the repertoire. If one considers arousal as reflecting the general level of activity of the nervous system, then arousal can be used as a baseline to which further activity via internal (e.g., hormonal) and external stimuli and behavioral contexts is added. The specificity of vocalizations would then depend on the stimuli and the behavioral context; however, whether a certain vocalization is produced in the presence of adequate releasers or not would depend on the general arousal of the animal at that moment. Strong stimuli, for example, may trigger a call despite a low general level of arousal, and, conversely, only weak stimuli may be necessary when the animal is already very excited. Such a concept of synergism of nonspecific arousal and context-specific parameters in eliciting certain vocalizations is supported by many observations of vocal behavior. In particular, the gradation from one call type into another can often be explained by a shift in the degree of arousal while the external stimulus complex remains very much the same. Similarly, series of alternating calls given in one behavioral context may just reflect oscillations in the state of arousal. Thus the chutter of guinea pigs produced in a mildly aversive context changes into whines when the stimuli responsible for aversion continue (Berryman, 1976). During aggressive interactions in tasmanian devils the gradation from whines to whine-growls, growls, and screeches apparently parallels the levels of excitation of the animals which can otherwise be measured by movement patterns (Eisenberg et al., 1975). An increasing level of excitement of rock hyraxes during aggressive encounters is expressed by call series starting with grunts, then shifting to growls, and terminating in high-frequency snarls (Fourie, 1977). Schott (1975) reported that squirrel monkeys cackled on the sight of a dog, barked when the dog remained visible, increased cackling when the dog approached, and finally shrieked when they briefly attacked the intruding dog. These examples demonstrate that mammals can shift from one call to another, if the stimuli or behavioral contexts are prolonged. Such a shift can be attributed to a shift in the level of arousal or excitement. It is interesting to note that such shifts between call types were rarely found in

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the young. In infants the state of arousal seems to be expressed in the rate of sound production rather than by using different calls. This finding may once more indicate that young mammals are not capable of producing such a great variety of calls because the neural mechanisms necessary to do so have not yet developed. Thus they may be physically unable to shift from one call to another. However, a context-related explanation is also possible. Series of different calls often occur during agonistic interactions and are related to threat and aggression. Since neonates and infants before the period of socialization usually do not participate in agonistic encounters, they are not exposed to appropriate contextspecific stimuli so that there might be no “reason” to emit such calls and call series. Again, the dichotomy of explanations for changes in the vocal repertoire during the ontogeny of a mammal becomes obvious. One line of reasoning considers maturation processes while the other considers a development of behavioral contexts and stimulus exposure. The developing mammal has no choice; it is certainly exposed to both influences. Our experiments have to show which influence in which case is of greater importance.

v.

CHARACTERISTICS AND COMMON TENDENCIES IN THE DEVELOPMENT OF SOUND COMMUNICATION

Up to this point we have been concerned only with the ontogeny of the vocal behavior of the infant mammal, the sender. As already mentioned in Section I, the sender is only one part of a communicationsystem. Except for mammals such as bats, which use echoes of their own calls to obtain information and to adjust their own behavior, we cannot speak of sound communication until we have measured the response of a potential receiver. Receivers for the calls of the young are mostly conspecifics. In this section we shall concentrate therefore on conspecific responses to the sound signals of the developing young. A.

CAN INFANT MAMMALS HEARA N D DISCRIMINATE SOUNDS OF THEIRLITTERMATES?

Figures 2-8 and 12 show that adults normally hear but they also show that neonates of many species do not hear. A logical consequence of this fact is that sound communication among littermates in the bat Antrozous (normally twins are born), the dog, the rat, and the house mouse is not possible during the first days of life. In addition, in newborn kittens the thresholds for sound-evoked potentials in brain centers are so high during the first 4 days (Brugge et al., 1978; Mair er a [ . , 1978) that sound communication seems to be impossible. Further mammals in which functional deafness at birth and for the first postnatal days has

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been shown are the opossum (Larsell e t a / . , 1944), the rabbit (Anggard, 1965), the mongolian gerbil (Fink et a/., 1972), and the golden hamster (Pujol and Abonnenc, 1977). There is almost no information about sound communication among the young of the mentioned species for the time after inception of hearing. This is also true for species such as the guinea pig and sheep, which can hear at birth and thus could communicate by sound from birth. The reason for this lack of data may simply be the general unimportance of sound communication among littermates in mammals. From a functional point of view, young littermates cannot contribute very much to the needs of the neonatal sender and, as far as I know, there are no data pointing out a selective pressure during evolution in favor of establishing a system of sound communication among littermates. It has been shown for puppies (Fredericson, 1952) and for rat pups (Hofer and Shair, 1978) that littermates can mutually prevent themselves from isolation by exchanging tactile stimuli. The action of the mother, however, in placing all littermates together in one nest will mostly be more effective than the uncoordinated efforts of neonates to regain body contact. Neonates are usually protected in the nest or are closely attached to the mother so that communication via tactile and olfactory stimuli normally is ensured and obviously is sufficient. Only for human babies has it been shown that they hear, discriminate, and respond to baby cries. Simner (1971) and Sagi and Hoffman (1976) found in their studies of contagious crying that 2- to 3-day-old babies started crying on newborn cries significantly more often than on cries of older babies or synthesized cries. This kind of communication among babies can have the effect of amplifying the distress signal of the youngest and probably most helpless one of a group and thus can contribute to call the caretaker’s attention.

B . Do INFANTMAMMALS REACTTO SOUNDS OF

THE

ADULTS?

Sound communication between the young and their parents or other adults with the adults as the sender and the young as the receiver could be more important. However, only few experimental data are available which show that sound signals of the adults have a direct influence on the behavior of the young. Obviously, this kind of communication is impossible as long as the young are deaf. Brown (1976) demonstrated that the young of Antrozous pullidus responded to the directive calls of their mothers after they started hearing (Fig. 2). They changed their vocalization from the isolation to the orientation call and started crawling toward the mother. Similarly, Gould (1971) showed for two other bats (Epresicus and Myoris) that the young-after onset of hearingchanged their call rate when the mothers began emitting ultrasound in response to their isolation calls. In these bats the ultrasonic calls of the mother seem to be important in guiding the lost infant back to the mother. The only other studies known to the author deal with signal discrimination in

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wolf pups and influences of adult human speech on the behavior of babies. Wolf pups aged 5-8 weeks and reared in isolation from adult conspecifics from week 5 onward were tested for their vocalizations in response to natural wolf howls, human howls, wolf pup calls, and noise (Shalter et al., 1977). The rate of vocalizations and the resistance against habituation to repeated presentations were significantly greater for wolf howls than for other stimuli. This shows that vocalization of wolf pups is stimulated more by sounds from adult conspecifics than from other sources. They obviously have mechanisms within their nervous system adapted to respond preferentially to the howling calls of the conspecifics. Babies will stop crying significantly more often in response to the sound of the human voice than to other sounds from the age of 2 weeks onward (Wolff, 1969). Even 1-day-old babies react to human speech by coordinating their movements with the rhythm of the speech. This coordination of body movements did not depend on the language used (Condon and Sander, 1974). Thus babies seem to be predisposed to react to certain cues common to all human languages. It is interesting to note that general attributes of human languages like phonation, pronunciation, and syntax are nonfunctional when communicating with babies. Important are more basic parameters such as pitch, intensity, and rhythm. These three examples all show a predisposition of the young to respond to vocalizations of conspecific adults. Most probably this could experimentally be confirmed for many more mammals. We may suggest that as long as the receivers are very young and their nervous systems are still developing the structure of the vocalizations of the adults used for communication with their young should not be complicated. The repetition of a simple call element whose main intensity is concentrated in the frequency range of best hearing of the young would be most suitable. Series of FM calls of adult bats, series of wolf howls, and the repetition of a single syllable when speaking to a baby agree with this suggestion. In general, sounds used for communication between adults and their young (adults = sender, young = receiver) should have little variability and a high repetition rate so that they can be easily distinguished and recognized by the developing sensory and nervous system of the young.

c.

WHICH FEATURES OF INFANT CALLS DO ADULTS RESFQNDTO?

We have seen that sound communication among newborns is either impossible or otherwise has not been demonstrated, and that information transfer from adults to their young seems to have only occasional importance. Therefore, if sound is to contribute significantly to communication between young and adults, then the young must be the senders and the adults the receivers. Since infant vocalizations change in physical parameters and in frequency of occurrence during ontogeny we have to ask whether adults can recognize these changes and can discriminate several call types in the vocal repertoires of the

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young. Behavioral data on pure tone frequency and intensity discrimination are available for several mammals (see Ehret, 1977b), but they help very little in deciding whether or not a mother does, in fact, discriminate different calls of her young. Calls usually have a complex frequency structure which varies for one call type within and between individuals. Similarly, variations in duration and repetition rate of the calls occur. These parameters are normally held constant in discrimination experiments with pure tones. In addition, the experimental tests are designed such that the animals have to use only short-term memory when discriminating slightly different sound stimuli. When using long-term memory, discrimination capacity would be very much worse or the discrimination task could not be learned at all (e.g., Thompson, 1959). In the natural situation, a mother usually does not hear a sequence of two or three alternating call types, but hears different calls at different times. Thus, when she perceives a call she has to know what type it is in order to respond adequately. High discrimination scores for complex sound stimuli in mammals were obtained in tests using short-term memory. For example, chinchillas (Kuhl and Miller, 1975; Burdick and Miller, 1975) and squirrel monkeys (Waters and Wilson, 1976) discriminate speech sounds in a way very similar to man, and squirrel monkeys discriminate many variants of isolation peeps of their young (Symmes and Newman, 1974). In experiments in which synthetic calls had to be attributed to one call type, however, animals generalized over a wide range of call parameters. Smith (1975, 1976) showed that female house mice primed to retrieve pups respond to several models of infant calls. The fundamental frequency of the pure ultrasounds could be varied by 30 kHz, frequency sweeps could be included or not, and the call duration could be varied from 80 to 15 msec, and the females still responded to the calls. B. Haack and G. Ehret (unpublished) tested the response of lactating female house mice to models of infant calls in choice experiments. The females discriminated equally well playbacks of natural ultrasonic calls and series of white noise pulses of bandwidth 40-60 kHz from 20-kHz pure tones, but did not discriminate noise pulses with a bandwidth of 30-60 kHz from 20-kHz pure tones. Pygmy marmosets respond to synthesized models of their closed mouth trills and accept quite a range of variations of center frequency, frequency range, frequency modulation, and duration (Snowdon and Pola, 1978). These experiments show that when adult mammals are not conditioned to discriminate or have no immediate comparison they generalize over a much broader spectrum of variation of sound parameters. This statement is based on few experimental data and may be applied only to those mammals which do not learn to recognize individuals by their specific sounds signals. There is evidence from bats (see Brown, 1976; Porter, 1979) and elephant seals (Petrinovich, 1974) that uniparous mothers can discriminate the isolation calls of their own infant from those of other infants and thus recognize their

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young by its calls. Based simply on the number of discriminations to be done and the variability involved it is easier for a uniparous female to discriminate the isolation calls of her single infant from those of other infants than for multiparous mothers to discriminate the spectrum of variability of isolation calls of their own litter from another spectrum of variability from other litters. The situation for the female becomes even more complicated when we think of the development of call parameters during ontogeny of the young (Sections IV, A,C, and D). Recognition mechanisms within mothers would have to be adjusted continuously to the momentary pattern of vocalization of their young. Such an adjustment to the developing isolation call was in fact found in the bat Antrozous (Brown, 1976), in which mothers respond only to calls of infants close to the age of their own. In this case the response of a female is related to the age of the calling infant and not to the individual itself, which is recognized by olfactory cues. Gould (197513) found that vocalization of the normal isolation call is essential for nursing success of infant Eptesicus bats. Mothers ignored infants that produced abnormal calls after their laryngeal nerves were squeezed with cold forceps. The females obviously recognized the abnormal physical structure of the calls and stopped maternal responses. This shows that maternal behavior can depend predominantly on sound communication, and that disturbances such as “wrong” signals which are not “understood” can have fatal consequences. Many of us know from our own experience with mammals such as dogs and horses that they can learn to recognize individual persons by their voices. Such learning requires recognition of special sound features and attribution of these features to a special individual. The use of such mechanisms in connection with recognition of infant calls has only been found in species that normally have only one or two infants at a time. At this point, a discussion of the adaptive value of individual recognition by sound would be useful, but would go beyond the limits of this article. A response to nonspecific and general features of a call type makes good sense when the stimulus is very variable, which is true, e.g., for the ultrasounds of rodent pups (Noirot and Pye, 1969; Sales and Smith, 1978). Apparently there is no basis for the evolution of a high specificity of feature detection when there is a very variable stimulus and no selective pressure for discrimination. In rodents the rate and probability of occurrences of the ultrasonic calls are most decisive for eliciting maternal responses (see de Ghett, 1977); the calls seem not to convey specific information about the sender, but, according to the second part of Bell’s (1974) theory, may produce arousal in the receivers. The higher the call rate the higher may be the arousal produced and the higher the probability of a maternal response. One conclusion may be drawn from all these observations, namely, that it cannot be predicted from the auditory capacity of a mammal whether or not it will discriminate and recognize variants of one infant call or of different call

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types. Obviously different systems of sound communication with respect to specifity of information transfer have evolved. D.

DOESADULTRESPONSIVENESS PARALLEL THE DEVELOPMENT VOCALBmAvroR OF THE YOUNG?

OF

Experimental studies to answer this question are rather time consuming because the time course of the behavior of sender and receiver and their relationship has to be investigated. However, some data are available for bats, cats, and rodents. Gould (1971) showed that the behavior of Eptesicus and Myotis mothers toward their infant changed with age. When a newborn bat was placed away from its mother it emitted isolation calls. The mother normally approached the infant while emitting ultrasound, and when she reached her infant she guided it to the nipple. Mothers of older infants responded to the infant calls with ultrasounds, then the infant oriented, and while both were calling antiphonally the infant crawled toward its mother. It seems that with improvement of hearing, and vocal and motor behavior of the young, the maternal response changes from an active approach to the infant to a more passive guiding of the infant back to her nipple by sound. Haskins (1977) in a study of maternal behavior of lactating cats found that these responded to isolation calls of their kittens with orientation, approach to the sound source, retrieving, vocalization, and shifts of their lactating position. Two parameters changed significantly over the observation period of 5 weeks; the number of vocalizations of the females in response to kitten calls increased and the females’ retrieving response decreased. These data are similar to those for the bats. Vocalizations of young infants elicit active searching and a high probability of retrieval, while vocalizations of older infants are responded to by vocalizations which may help the infant to find its way back to the mother and the rest of the litter. Such a change in maternal behavior makes sense with regard to the improvement of hearing and orientation capability and of motor control of the young. The mother may just stay at a safe place and “‘call” the older young back. Noirot (1 964a,b) demonstrated that maternal behavior of lactating and virgin house mice decreased with the age of pups. In particular retrieval of a lost pup older than 13 days occurred only rarely. The experiments with the inexperienced virgin females showed that the decrease in maternal behavior must be due to a decrease in appropriate stimuli from the pups. Since the rate of ultrasound emitted by mouse pups to isolation and mild temperature stress decreases to almost zero by day 13 (Noirot, 1966; Okon, 1970a; Bell et ul., 1972; Ehret, 1975a), the decrease in maternal behavior follows the decrease in ultrasound production and may be directly related to that. Such a decrease in ultrasound production with age

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was also measured in rat pups (Allin and Banks, 1971; Sales and Smith, 1978), Peromyscus (Smith, 1972), Apodemus (Sales and Smith, 1978), collared lemmings (Brooks and Banks, 1973), mongolian gerbils (de Ghett, 1974), and Microtus (de Ghett, 1977). Moreover, Noirot and Pye (1969) found that in addition to the rate the sound pressure, duration, bandwidth, and sound energy per time unit decreased in the ultrasound of mouse pups. The strong correlation between the rate and the total energy of ultrasounds and the occurrence of maternal response behavior, especially retrieving pups, suggests that ultrasound in rodents is, in fact, a decisive stimulus for initiating maternal response. Thus the occurrence and probability of any maternal behavior toward a lost pup seem to be controlled by the ultrasound production of the pup. However, the kind of maternal response behavior may be influenced by other age-dependent cues from the pups. In the case of bats and cats, the mothers must have some knowledge of the developmental state of their young in order to respond by approach and retrieval of newborns or by vocalizations to older young. The vocalizations of the young themselves may include information about age (as shown for Anrrozous bats; Brown, 1976) or other cues such as size or the development of motor behavior of the young could be recognized by the mothers. OF ADULTRESPONSE BEHAVIOR E. NONACOUSTICDETERMINANTS

The response behavior of adults is even more difficult to measure and to control than the vocal behavior of the young because of the larger number of internal and external stimuli they are exposed to and their extended sensory capacities. Whether or not and how a mother will respond to a call of her pup can depend on, among other factors, ( a ) her internal state (hormonal level, hunger, thirst, etc.), ( b ) her arousal, being asleep or awake, ( c ) her momentary activity, ( d ) her experience with young, ( e ) the presence or absence of other than sound stimuli from the young, and (f, the presence or absence of external stimuli independent of the young. Therefore, a mechanistic description of a certain call type eliciting a certain response will in most cases be too simple and inadequate. One has to test, or, if possible, exclude interference of the factors mentioned above with the sound stimuli of the young. In many cases only a factorial analysis may help to discover behavior of the adults which originally is related to the vocalizations of the young. The following examples demonstrate this. Probably most experimental data on the influence of nonacoustic factors on the responsiveness of females to infant sound exist for rodents. Haack (1978) tested the response latency of female house mice to a calling pup placed in a Y-maze. The cage with the mother and the rest of the pups was attached to one arm of the maze and the mother could investigate the maze for at least 12 hr prior to the test. The latency from the first ultrasonic call of the pup in the maze to the moment

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when the mother entered the corresponding arm of the maze was measured in three different situations with regard to the behavior of the mother when the test started: ( a ) the female was awake (eyes open), lying on the pups and nursing and/or grooming them ( N = 85 observations); ( h ) the female was active in the cage, feeding, drinking, rearing, grooming herself, etc. ( n = 60); ( c )the female was lying on the pups sleeping (eyes closed, FI = 53). The females reacted significantly more frequently within the first 20 sec after the first call of the pup when they were awake and lying on the pups than when they were awake in the cage ( p < 0.025). Not a single female asleep on the pups reacted within the observation period of 80 sec. This result shows that the momentary activity and the state of arousal have to be considered when testing maternal responsiveness to infant calls. It has been demonstrated that other stimuli, e.g., olfactory from the young, can influence the probability of response to ultrasound of the pups. Smotherman rt (11. (1974) showed that ultrasounds of rat and mouse pups had the effect of guiding the mother into the “right” arm of a Y-maze only if there were also olfactory stimuli of the pups present in the maze. The females did not show preferences if they had the choice between an empty arm and playbacks of ultrasound in the other arm. Our own experiments (B. Haack and G. Ehret, unpublished) showed that specific olfactory cues of mouse pups are not necessary to make females ready to use ultrasound as a directional cue for finding the lost pup, general olfactory stimuli of the housing of the female or of the female herself are adequate. Without familiar olfactory cues in a maze exploring behavior seems to dominate maternal behavior. Allin and Banks (1972) did not find maternal retrieving responses toward calling rat pups in virgin male and female rats, although they did orient to the calling pup. Only lactating females left the nest to retrieve the lost pup. Smith (1976), however, showed that virgin but primed female house mice respond to ultrasounds of pups with oriented searching behavior. All these results from rodents show how important stimuli other than auditory can be in changing the response behavior of females to the calls of pups. Therefore only careful control of the factors mentioned can ensure that observed communication is really based on sound stimuli, and that, if no response could be measured, communication by sound could not be found under different circumstances. Thus data do not allow excluding statements, but once communicative effects have been demonstrated one can try to reduce the stimulus configuration to the minimum required to elicit a response. These conclusions derived from experiments on rodents also apply to other mammals. The dependency of maternal responses on stimuli other than sound of the young (compare, however, Section V,C) shows that sound communication between young and adults cannot be isolated from other communication channels; on the contrary, the developing sound communication in mammals is an

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expression of one part of the developing interaction between parents and their young.

VI. CONCLUSIONS While Fig. 1 was a starting point for our discussion, we can now use it as a summary. It turns out that the development of the vocal behavior of the sender, maturation processes, changes of the vocal repertoire, of behavioral contexts, and stimuli have been subjects of many studies and are better understood than the response behavior of the receiver. We can be fairly certain that the afferent side of the acoustic system of the adults is capable of hearing and discriminating the vocalizations of the young at least when they are close to the sender. The mechanisms, however, that make them respond, the influence of other than sound stimuli on this response, and the development of response behavior along with the ontogeny of vocal behavior of the sender are still in need of further research. Communicative significance has been demorxtrated for “isolationtype” calls, but there are many other vocalizations of infants and juveniles which may affect the behavior of the adults. Questions about the comparative rank and importance of sound communication in the communication systems of different species of mammals and the dependence on habitat and ecology cannot be answered yet. We d o not know either whether the relative rank and importance of sound communication compared with other communication forms within one species increases or decreases during development. We did not discuss the ontogeny of vocal behavior with respect to the changing environment in which the young are living. Short-distance communication plays the predominant role when the young are still in the “closed” environment of a burrow, a hole, or a nest, or are carried around by their mothers. When independent, long-distance communication may also become important and vocal signals are certainly evolved to fit the requirements of the habitat. The study of aspects of the development of sound communication in mammals as demonstrated in Fig. 1 is a relatively new field of research in which major progress has been made since 1970. On the basis of what we already know, we can expect exciting times for the future.

VII. SUMMARY The postnatal development of sound communication in mammals has been discussed on the basis of the development of components of the sound communication system. The time courses of the development of vocal behavior and, as far

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as is known, of hearing in the young of several species (the bat Antrozous, the cat, puma, tiger, jaguar, lion, guinea pig, rat, house mouse, stumptail macaque, chimpanzee, and man) are demonstrated. The newborn of some species such as guinea pigs and man can already hear at birth, whereas other more altricial species such as rat pups start hearing several days after birth. All newborn infants emit at least one call type, the “isolation call,” which is produced in response to distressful stimuli and when isolated from mother and littermates. During ontogeny, the vocal repertoire enlarges for most species. Many species have vocalizations typical for a certain age. Maturation of the vocal tract, of motor control of the larynx, and of nervous centers of the brain has been shown to influence the development of call structure and repertoire. The development of a normal adult repertoire seems to be innate and independent of hearing species-specific sound (except for man). In one case only (Japanese macaques) learning has been shown to influence vocal behavior. During ontogeny external stimuli and behavioral contexts change. The relationship between external stimuli and contexts and the production of certain calls is discussed in detail. Although the state of arousal in the sender influences the probability and rate of sound production arousal-specific call types have not been observed. Sound communication among young littermates has not yet been demonstrated and is actually impossible in newborns which are unable to hear. Only a few cases have been investigated (bats, wolves, man) in which adults are senders and the young are receivers. Sound communication with young as senders and adults (mothers) as receivers is most important and several examples are discussed. The afferent side of the auditory systems of adults most probably is able to discriminate the different species-specific types of vocalizations. However, from the capability for feature detection it cannot be predicted whether a mother will actually respond to different calls of her young. Multiparous females seem not to be able to recognize their own young by sound. In some cases, however, uniparous females can recognize their young individually or at least their age by age-specific vocal “signatures. ” The rate and probability of occurrence of isolation calls seem to be the decisive parameters for eliciting maternal behavior in multiparous females. Maternal behavior changes during the ontogeny of the young. Development of maternal behavior can, to a certain extent, be related to a corresponding development of vocal behavior of the young. However, nonauditory influences on maternal behavior also have to be considered. Thus sound communication is always only one part of the total communication system between young and adults. The role and importance of sound in this system have to be determined individually for every species.

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Acknowledgments Investigations of the author which contributed data to this article were supported by the Deutsche Forschungsgemeinschaft, Eh 53/1/36. I thank Dr. H. Mark1 and A. J. M. Moffat for reading the manuscript.

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ADVANCES IN THE STUDY OF BEHAVIOR VOL. II

Ontogeny and Phylogeny of Paradoxical Reward Effects' ABRAMAMSEI.A N D MARKSTANTON DEPARTMENT OF PSYCHOLOGY THE UNIVERSITY OF TEXAS AT AUSTIN AUSTIN. TEXAS

I. Introduction . . . . . 11. Paradoxical Effect rcement . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . A . A Little History: Why "Paradoxical"? . . . . . ............ B. The Paradoxical Effects . . . . . . , . , , , , , . . . . . . . . . . . . , , , , . . . . . , , , , . , 111. Frustration Theory as One Mechanism for the Paradoxical Effects. . . . . . . . . IV. The Comparative Analysis of Learning. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . A . Emphasis on Behavioral Process . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . B. Systematic Variation ....................... C. Species Differences i ......................... V. Toward an Ontogenetic Analysis of Paradoxical Effects A . The PREE and MREE . . . . . . . . . . . . , , . . . . . . . . . . . , . , , . . . . . . . . . . . , B. Successive Negative Contrast (SNC) and Patterned Alternation (PA). . . . .... C. The Overtraining Extinction Effect (OEE) . . . . . . . . VI. Comments on the Neural Substrate of Paradoxical Effects . . . . . . . . . . . . . . . VII. Concluding Considerations: Implications for Behavior and Behavior Theory A . Ontogeny of Appetitive Behavior . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . B. Ontogeny of Reward Learning: Difficulties for Theory . . . . . . . . . . . . . . , C. Concluding Comments . . . . . . . . . ... ........ References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

I.

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INTRODUCTION

Among behavioral and neuroscientists there is a broad segment of opinion suggesting that a fuller explanation of behavior will involve causal mechanisms derived from three levels of investigation: proximal, developmental, and evolutionary. 'The work from our laboratory was supported by NSF Grant BMS74-19696 and by Grant R01MH-30778 from NIMH. 227

Copyright @ 1980 by Academic Res. Inc All nghts of reproduction in any form reserved

ISBN 0-12-004511-7

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Proximal mechanisms are mechanisms that operate to affect behavior over a relatively short time course. Such mechanisms, actual or hypothetical, are the determinants of present behavior in the context of the immediate environment. Hinde (1966, p. 4) has suggested that in this level of analysis “we need not be chary of using the word ‘cause’ in its everyday sense.” Some of these proximal mechanisms have a historical basis, in the sense that associations formed at any stage of development may be cued and activated by contemporary determinants. Proximal mechanisms are organized in our thinking by terms such as sensoryperceptual factors, associative or learned factors, and motivational-emotional factors. At a less abstract level present behavior in the immediate environment can be related to neural and hormonal systems. The fact that differences exist in the operation of proximal mechanisms among different individuals, and even in the same individual at different points in the life span, brings us to the second broad area of investigation, development. Here questions about the historical basis for both associative and nonassociative factors in the lifetime of the individual are brought into sharper relief: How have genetic endowment, maturation, and early experience interacted to determine the nature and operation of the proximal mechanisms which determine the behavior of the adult? Is the individual’s machinery age dependent and, if so, by what developmental principles can this age dependence be understood? Evolution, which may be generally defined as the interaction of natural selection with phylogenetic history, may also play a part in the history of the individual. Heredity and differential reproduction adapt the species to changing ecological contingencies. Adaptation, in turn, alters the environment. Proximal mechanisms may be modified by natural selection at all stages of phylogeny and ontogeny . In this sense, also, are applications of evolutionary principles involved in the understanding of individual behavior: evolution explains differences among species and genetic principles partially explain differences in endowment among individuals of the same species. The problem of accounting for behavior is, then, admittedly very complex. The number of research problems and theoretical issues contained at each level of explaining behavior are sufficient to occupy a great many investigators crossing many disciplines. It is not surprising, then, that these three levels of mechanism which share, at least in theory, complex interrelationships, are usually in practice studied separately, and often independently. This independence leads to methodological and philosophical differences in approach to the study of behavior: as an approach, the ethologist’s interest in evolution and adaptation, with its emphasis on ecology, genetic transmission, and species comparisons, seems very remote from that of, say, the sensory physiologist, whose object of study, the properties of sensory neurons, leads to a choice of subjects (model systems, preparations) and stimuli based on laboratory convenience and amenability to experimental control.

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This usual independence of approach should not, however, be overstated. There are an increasing number of cases in which it has been profitable to combine considerations from at least two levels of mechanism in the study of behavior. Investigators interested mainly in developmental mechanisms have made species comparisons to understand development better (e.g., Kendler and Kendler, 1975; Rosenblatt, I97 1); and sensory physiologists have studied perception by making appropriate developmental (e.g., Hubel and Wiesel, 1959) and comparative (Pettigrew, 1980) manipulations. To those whose major interest is in the mechanisms of proximal causation, species and age comparisons can be very illuminating. To students of brain and behavior, for example, the develop ing species or organism can serve as a preparation or model system for studying the relationships between behavioral and neural changes (e.g., Altman et al., 1973; Fibiger et al., 1970). Some investigators who pursue proximal causation at the level of behavior theory, for example in the study of learning and memory, have found consideration of species and age differences just as illuminating as other investigators whose main interest is in brain correlates. In the case of learning, the theoretical advantages of making phyletic comparisons have been argued cogently by Bitterman (1 975). In this article, we will argue that the study of ontogeny provides similar theoretical advantages and is complementary to the study of phylogeny in this regard. A summary of our present approach might take the form of identifying stages in the biopsychological study of related behavioral effects; and it might be termed a modified empirical construct approach. As we see it the stages are:

I . Observe and describe a number of apparently related effects; 2. Develop a conceptualization of these effects in terms of empirical constructs; 3. Study these effects phylogenetically and ontogenetically for their presence or absence, and particularly for order of their appearance; 4. Study the appearance and order of appearance of these effects in relation to the presence or absence of portions of, or activities of, the neural substrate; 5 . Relate the findings from 3 and 4 to 2, i.e., to a conceptualization in terms of empirical constructs. The particular behavioral phenomena we have chosen to address in this context are the paradoxical effects ofreinforcement. There are many such effects, and we list a larger set of them in Table I, but we restrict our discussion to four of these effects that are of the between-subjects variety: the Partial Reinforcement Extinction Effect (PREE), the Magnitude of Reinforcement Extinction Effect (MREE), the Successive Negative Contrast (SNC), and the Overtraining Extinction Effect (OEE). We will deal also with another effect, Single Patterned Alter-

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nation ( P A ) , which is not strictly speaking a paradoxical effect but, as we shall see, is bound theoretically to such effects, We have begun an ontogenetic study of these phenomena in the laboratory rat that stresses very early development. And we have decided to study these effects first because (a) they have been studied extensively in a number of species by Bitterman, Gonzalez, and others, and (6)they have, at one time or another, all been deduced from the same sets of theoretical premises, specifically in treatments of the role of appetitive nonreinforcement (nonreward) on behavior (e.g., Amsel, 1962, 1967; Capaldi, 1967). The remainder of this article follows the five stages we have just outlined. Section I1 provides some theoretical background and describes the effects; Section 111 summarizes the frustration theory view of the role of appetitive nonreward in all these effects; Sections IV and V provide data from some phylogenetic, and our recent ontogenetic, experiments on the development of paradoxical effects; Section VI discusses some of our findings in relation to the neural substrate; and Section VII reflects on the implications of this work for behavioral theory.

n. A.

PARADOXICAL

EFFECTS OF REINFORCEMENT

A LITTLEHISTORY: WHY“PARADOXICAL”?

There are two senses in which the effects we have listed are paradoxical. The first, and simplest, sense is that in each case more produces less, and less produces more. The PREE is a case in which the lesser density of reward leads to greater resistance to (more trials to) extinction. In SNC and MREE greater magnitude of reward produces “abnormally” low levels of performance when reward is reduced or less resistance to extinction, respectively. An inverse relationship between number of acquisition trials and trials to extinction defines the OEE. In the within-subjects cases (Table I), to give some examples, the Partial and Magnitude of Reinforcement Acquisition Effects describe cases in which certain lesser percentages and magnitudes, respectively, of reward to one of two discriminanda result in relatively greater, rather than lesser, levels of performance. And Operant Behavioral Contrast describes the finding that reducing the value of reinforcement of one of two discriminative stimuli ( S - ) increases performance to the other ( S + ) . Even patterned (single) alternation produces paradoxical effects in the sense that, early in training, a reward produces better performance on the next trial while a nonreward produces poorer performance, and after some amount of training reward and nonreward have the opposite effects on the next trial (e.g., Tyler et al., 1953). The other sense in which these (and other) effects are paradoxical is more

23 1

PARADOXICAL REWARD EFFECTS

TABLE I PARAIH)XI(.AI. EFFECTS OF APPETI'TIVE REINFORCEMENT" Between-subjects effects

Within-subjects effects"

Partial Reinforcement Acquisition Effect (Haggard. 1959; Goodrich, 1959; Wagner, 1961) Partial Reinforcement Extinction Effect (Humphreys. 1939a.b. 1940, 1943) Magnitude of Reinforcement Extinction Effect (Hulse, 1958; Armus, 1959) Overtraining Extinction Effect (North and Stimmel, 1960) Successive Negative Contrast (Elliot, 1928: Crespi, 1942)

Partial Reinforcement Acquisition Effect (Henderson, 1966; Amsel ef a / . 1966) Magnitude of Reinforcement Acquisition Effect (MacKinnon, 1965) Simultaneous Negative Contrast (Bower. 1961) Operant Behavioral Contrast (Reynolds, 1961, 1963) Peak Shift (Hanson, 1959; Honig e t a / . , 1959) Pavlovian Positive Induction (Pavlov, 1927) The Overtraining Reversal Effect (Reid, 1953; Pubols, 1956)

"The references provided in each case are the early, seminal ones. For more recent references and more detailed discussion of these effects see Amsel (1967. 1971), Capaldi (1967). Gonzalez and Champlin (1974). Mackintosh (1974), and Rashotte (1979). "The within-subjects effects are all demonstrated in the context of discrimination learning and differential conditioning

theoretical. The starting point is associationistic psychology, and more particularly that branch of associationism known as Learning Theory. All learning theories have had to deal with the fact of decreasing incremental changes in performance with successive reinforcements, and of decreasing decremental changes in performance with successive nonreinforcements. More specifically, changes in the probability or associative strength of a learned response in a nonchoice situation are often expressed in a simple linear equation of the general form

Where A is the asymptote or limit to which probability can grow, /3 is a parameter reflecting rate of growth to asymptote, and Ap,, is the increment in probability on a given trial, which obviously gets successively smaller as learning proceeds. The use of stochastic or linear models to describe the course of learning was brought into prominence by Estes (1950) and Bush and Mosteller (1951) and was subsequently elaborated by them and by other mathematically oriented psychologists. For example, Bush and Mosteller (1955) devised mathematical accounts of a variety of learning phenomena based on a linear model with assumptions

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borrowed from Hull's (1943) theory; Lovejoy (1965) used a linear-model approach to develop a theory of attention; and more recently Rescorla and Wagner (1972) have used such a model, with simple but important modifications, to provide an account in associative terms of stimulus selection and attentional factors in Pavlovian conditioning. One of the characteristic simplifying assumptions of such linear-model theorizing is that decremental and incremental effects are conceptualized as governed by the same mechanisms, a Guthrian view. This is the case whether such effects are regarded as changes in response probability (Bush and Mosteller, 1955; Estes, 1950), or as changes in associative strength (Rescorla and Wagner, 1972). According to such models a decrement (inhibition) is the simple inverse of an increment (excitation); extinction curves are of the same form as acquisition curves; and reductions in performance, associative strength, or response probability with decreases in reinforcement density or magnitude are to levels appropriate to those values of reinforcement. In short, linear models of learning describe simple monotonic relationships in both learning and extinction, and make no provision for what we call paradoxical effects of reinforcement. In this sense, then, the word paradoxical represents the departures from what is expected on the basis of simple linear-operator models of basic or classical learning theories. To take the most recent case as an example, the Rescorla-Wagner model, with all its successes in other respects, cannot account for any single paradoxical effect, neither those which we will elaborate here nor any of several others (see Table I). An earlier case in point is the basic equation for growth of habit strength in Hull's ( 1943) theory

SHR= M - Me-'" In this equation the rate (i) and limit of growth ( M ) parameters play the same role as in all the linear models that were to follow. While habit strength in Hull's theory does not decrease in extinction, as does associative strength in the Rescorla-Wagner model, total inhibitory strength does subtract from excitatory strength and the rate of growth of inhibitory strength in extinction can be taken as a direct indicant of the strength of association formed in acquisition. Indeed, Hull (1 943, p. 118) considered resistance to extinction one of a number of measures of habit strength: The strength of the habit is manifested indirectly by various measurable aspects of action: (1) reaction amplitude or magnitude (A), (2) reaction latency (t), (3) resistance to experimental extinction (n), and (4) probability (p) of occurrence, i.e., percent of appropriate stimulations which evoke the associated reaction.

In this regard Hull's 1943 theory suffered from the same limitations as its linear-model successors. Spence (1960) pointed this out in the context of an early systematic discussion of the partial reinforcement acquisition effect (PRAE), a

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discovery by Haggard (1959) and Goodrich (1959) that rats trained under a 50% schedule of reward reached higher asymptotes of running speed than those under 100% reward. To reiterate, none of these classical associationistic theories can account for the PRAE or for any of the other effects we will describe as paradoxical. B.

THEPARADOXICAL EFFECTS

Even before Hull’s Principles was published there was already evidence from learning experiments that at least one extinction effect was not in accord with his view of habit measurement. Soon there were other findings that pointed to an absence of the expected direct relation between habit strength and performance reflecting resistance to extinction. Reinforcement manipulations which would presumably yield weaker habit strength were followed by stronger rather than weaker resistance to extinction. Perhaps the most seminal paradoxical effect of reinforcement to be discovered was the finding of Humphreys ( 1939a) that random interspersal of reinforcement and nonreinforcement in human eyeblink conditioning yielded inferior performance in acquisition but greatly increased resistance to extinction. The partial reiilforceinent extinction effect (PREE), as this effect came to be known, was shown by Humphreys (1943), as it had been shown in a different context by Skinner (1938), to occur in appetitive (reward) learning in rats as well as in defense conditioning in humans, and much of the later work on this and other effects has been done in the context of reward learning. The PREE, or “Humphreys Paradox” as the effect has been called (Kimble, 1961, p. 287), became a major problem for investigation in learning theory, inspiring a vast amount of research, several theories, and many applications. Broad reviews exist elsewhere (Lewis, 1960; Robbins, 1970). Another paradoxical effect of appetitive reinforcement, first reported by North and Stimmel (1960) in rats, was the finding that giving a large number ( N , in Hull’s equation) of reinforcements in acquisition results in faster extinction than giving a smaller number. This phenomenon has been termed the overtraining extinction effect (OEE) and has held up under a variety of conditions (see Mackintosh, 1974, pp. 423-426, for a summary). It is not in line with that portion of Hull’s equation that makes habit strength a direct function of N , at least not if strength of habit is inferred from resistance to extinction. At about the same time, it also was shown in rats that a large magnitude of reward in acquisition results in faster extinction than a small reward magnitude (Hulse, 1958; Wagner, 1961). The magnitude of reward extinction eflecr (MREE), as it has been termed, has since been confirmed in several experiments (e.g., Gonzalez and Bitterman, 1969; Ison and Cook, 1964; Traupmann, 1972). Again an extinction measure of performance seems to contradict Hull’s view that habit strength (SHR)is a direct function of reinforcement magnitude ( w ) .

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As early as 1928, Elliott showed that when rats were trained to learn a more complex maze, and their incentive was changed in mid-course from bran mash to sunflower seed, their performance (number of errors) deteriorated to a level below that of a control group rewarded with sunflower seeds throughout. Crespi’s (1942) more influential demonstration of what has come to be known as successive negative contrast (SNC) or, as Crespi termed it, the depression efect, dealt with contrast in terms of speeds in a straight alley rather than errors in a maze. It was as damaging to the 1943 Hullian view, and the later linear-model views, as were the PREE, the OEE, and the MREE. The term SNC refers not to an extinction effect, but to the finding that a shift from a large to a small magnitude of reward causes a reduction in performance, not only to the level of performance of controls trained throughout on the lower magnitude of reward, but transiently to a level lower than the small-reward controls. This effect has been viewed quite reasonably by some (e.g., Gonzalez and Bitterman, 1969) to be different from the MREE only in degree: in the MREE the downward shift is to zero reward, and there is evidence for subzero extinction performance, or performance below a never-rewarded “operant” level; in the case of the SNC the downshift in reward is simply not to zero. To reemphasize the point, these effects, when they occur, represent changes in performance that are not in accord with decremental assumptions in Hull’s (1943) theory or in any of the simple linear models of learning that followed. It is noteworthy, however, that these paradoxical effects are much more robust in instrumental than in classical conditioning, especially in animals, and do not seem to occur in the “purer” forms of classical conditioning from which preparatory responding (in animals) and cognitive involvement (in humans) have been removed or minimized (Amsel, 1972b). Indeed, there are levels of functioning both in fish and reptiles (and presumably other lower animals) and in humansthese might be characterized as relatively “primitive” levels-in which the reward effects appear in the nonparadoxical form predicted in 1943 by Hull and the linear-model approaches. It does not seem unreasonable to think that such results are obtained when acquisition, extinction, and reduction in reward magnitude do not arouse mediating expectancies about reward or anticipatory goal responses (or cognitions) either in animals, because the mechanisms do not exist, or in humans, because they are not engaged. In Sections IV and V we will examine some of these nonparadoxical cases.

111.

FRUSTRATION THEORY AS ONEMECHANISM FOR THE PARADOXICAL EFFECTS

In a series of theoretical papers, Amsel(l958, 1962, 1967, 1971 , 1972a,b) has developed an account of a variety of effects, including the various acquisition and

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extinction effects related to appetitive continuous and partial reinforcement and discrimination learning, and discriminative versus nondiscriminative contrast effects. A major assumption of this account is that in instrumental (and perhaps Pavlovian) but not in simple classical conditioning (see Amsel, 1972b), response diminution, including extinction, consists not of a decrement in the associative strength or response probability established in acquisition, but rather of the learning of a new association based on the frustrative properties of nonreward. These properties are aversive, and they produce escape and avoidance responses that are incompatible with the appetitive approach response established in acquisition (for extensive evidence see Daly, 1974). This is an "active" characterization of the effects of nonreward, or reduced or delayed reward, the response decrement reflecting learning of a new competing response tendency rather than unlearning of the old. More specifically, the theory assumes that an anticipation or expectancy of reward (TR-SR) is established and comes to control the goal approach response in instrumental learning. (As we shall see, it is a mediating mechanism of this kind that may be absent in the learning of fish and turtles, humans operating relatively noncognitively, and "precognitive " infant rats.) Once rH-sR is established and mediates approach responding, nonreward unconditionally elicits an aversive reaction termed primary frustration (RF).This reaction has drive properties (Amsel and Roussel, 1952); its reduction can reinforce escape responses (Daly, 1974); and it has feedback stimulus (sF) properties which can cue, guide, and direct behavior (Amsel and Ward, 1954). These feedback, drive-stimulus properties are analogous to the stimulus aftereffects of nonreward (Capaldi, 1967; Sheffield, 1949) or memories of nonreward (Capaldi, 1972) postulated in sequential theory, and are particularly important in any analysis in which reward expectancy or anticipation is not thought to play a major role in learning. With repeated nonrewarded trials, primary frustration can serve as a US for the conditioning of anticipatory or conditioned frustration (TF-SF) which, when established to accompanying cues (CSs) provides its own feedback stimulation that can evoke goal-avoidance responses (RAvd). It is these sFconnected avoidance tendencies that constitute the new learning that occurs in expectancy-mediated extinction, or indeed, in any situation in which reward is reduced or delayed. The frustration theory account of the paradoxical reward effects rests on the assumption that the conditioning of the avoidance tendency in extinction, contrast, or other effects of relative reward reduction depends on the magnitude of primary frustration (RF) which in turn depends on the discrepancy between the anticipated (r R-s R) and the realized reward. Factors that increase the strength or value of the expected reward will, by increasing the magnitude of RF when reward is absent, lead to enhanced avoidance of the goal and, consequently, to more rapid extinction or, in general, to greater reward-reduction effects. In this way, the larger number of training trials or reward magnitude in acquisition will

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produce faster extinction than fewer training trials or smaller rewards (the OEE and MREE, respectively). Successive negative contrast may be thought of as a less drastic version of the MREE, the downshift in reward being to a low reward magnitude rather than to zero. A theoretically consistent account of the partial reinforcement extinction effect follows from an additional assumption of the theory, that of counterconditioning, specifically the counterconditioning of feedback stimuli from conditioned frustration (S p) to approach, rather than avoidance, of the goal area in the face of anticipated frustration. This is assumed to occur on a partial reinforcement schedule in which rewards and nonrewards are interspersed during acquisition. Both rR-sRand rF+F gain strength under such a schedule, but, given that the approach tendency is dominant, sF acquires some association with the approach response. If these mechanisms operate to retard extinction it is because in partially reinforced animals continued approach is a response to feedback cues from anticipatory frustration (sF-RApp)whereas continuously reinforced animals, experiencing frustration for the first time in extinction, learn an avoidance tendency (sF-RA“~) unopposed by the counterconditioned approach tendency. With this particular theoretical integration of the paradoxical effects of reinforcement as a set of guiding principles or heuristic, we have begun to chart the course of development in infant rats of these effects and of their underlying processes. As we have already noted, many comparative investigations of these effects, mainly by M . E. Bitterman, R . C. Gonzalez, and their co-workers are already in existence. And these studies are comparative in the phylogenetic sense; they look for the presence or absence of these effects in fish, reptiles, and birds, as well as in mammals. Our recent ontogenetic work in this area owes much, not only to the earlier work of these investigators with a number of species, but also to discussions, particularly by Bitterman (1960, 1965, 1975), of methodological problems inherent in comparative analyses. From the viewpoint of methodological and theoretical analysis it may turn out that in ontogenetic and in phylogenetic analysis the problems are similar, although perhaps somewhat less severe in the former. In the next sections we will look at some examples of comparative studies of paradoxical effects from the phylogenetic and ontogenetic perspectives. But first, we will provide a brief review of some problems encountered in comparative analysis as explicated by Bitterman and others (Bitterman, 1960, 1975; Sutherland and Mackintosh, 1971).

IV.

THECOMPARATIVE ANALYSIS OF LEARNING

The essential features of the comparative study of learning are: ( u ) emphasis on “process, ( h ) “systematic variation” and “functional analysis” as a solu”

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tion to the control problems that are inherent in cross-species (and, in our case, cross-age) comparisons, and ( c ) characterization of species (and, in our case, age) differences through the study of behavioral phenomena that can be taken to reflect the operation of underlying processes. A. EMPHASIS ON BEHAVIORAL PROCESS From the point of view of theoretical analysis, emphasis on process is perhaps the most important distinguishing feature of the comparative analysis of learning. It should be noted, however, that this emphasis works in both directions: a comparative approach based on considerations of learning theory yields comparative observations and information that is perhaps more powerful than would be available from behavioral comparisons not guided by theoretical considerations. This distinction between investigation of behavioral process and investigation of behavior cannot be overemphasized. Characterization of behavior is an empirical matter while characterization of process is necessarily theoretical. Often the same behavioral effect can be understood in terms of a number of theoretical processes and, conversely, the manifestation of the same process may be inferred from a variety of behavioral effects. As an example of the former, the overtraining reversal effect (ORE)-faster reversal following extended discrimination training-has been taken to reflect the operation both of attentional (Sutherland and Mackintosh, 197 1) and frustrative (Amsel, 1962) processes. Similar considerations are familiar to physiological investigators. For example, in attempting to assess the effects of brain lesions on memory, one must be aware that the lesion may also produce sensorimotor or motivational changes that result in behavior indicative of “forgetting. By virtue of its theoretical nature, any analysis at the level of behavioral processes is cast in terms that are abstract and general, the concern being to provide an account of the functional properties of molar laws of behavior, rather than the specifics of stimulus, response, response topography, and so on, that occur in a given situation. In this regard, questions of process are quite distinct, in our view, from questions of “belongingness” and “species adaptiveness, determinants of behavior long recognized (Thorndike, 1911) but not studied intensively until recently (Hinde and Stevenson-Hinde, 1973; Seligman and Hager, 1972). It is one thing to ask which stimuli and which responses are more likely than others to enter into an associative relationship (Garcia and Koelling, 1966), or which reinforcers are more likely than others to strengthen or weaken a particular response (Shettleworth, 1978), and quite another thing to ask if the functional relationships derived from these novel experimental observations reflect, on the whole, the operation of new or essentially the same processes. Taste aversion learning provides, perhaps, the best illustration of this point. In view of the fact that the conditioning of taste aversions occurs rapidly and with very long ”

”

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CS-US intervals, some investigators (e.g., Kalat and Rozin, 1972) used their failure to obtain “blocking” in this system to argue that taste aversion learning is a more “primitive” learning system, involving more rudimentary processes, than other learning systems. After a large amount of systematic research, however, it appears that the same processes seem to operate in taste aversion learning as in Pavlovian conditioning in general (Domjan, this volume) and that the faster conditioning and extended CS-US interval can be regarded as extremes in these two dimensions. We are not arguing that differences between various behavioral systems do not exist or that such differences are unworthy of study; on the contrary, we have used the example of conditioning of taste aversion to point to the distinction between questions of belongingness or preparedness and questions of process, and to emphasize the point that results appearing to suggest radical difference in kind may not reflect actual differences in process. So much depends on the level of abstraction with which one views the phenomena, as well as on the amount of systematic research and the overall pattern of data available for examination. B.

SYSTEMATIC VARIATION

The major control problem in any comparative analysis is the changes or divergences that occur across species (or across ages within a species). In the case of comparisons of learning across species, for example, it is impossible to equate for level of motivation induced by deprivation procedures or for the reinforcing value of a goal event, to mention just two of many relevant factors. Bitterman (1965, 1975) has proposed systematic variation as a partial solution to this control problem. There is little we can add to Bitterman’s well-known discussion of this research strategy: the essence of it is that any conclusion about a difference in behavior (and in process) among species or ages in development should not depend on the application of any one set of values of a parameter. For any species or for any age level in ontogeny it should be possible, for example, to determine an effective range of reward conditions that produce diff#Vencesin performance and, presumably, in learning. For another species or age, the range may be different. In the case of paradoxical effects, for example, the conclusion that an effect exists at one level of phylogenetic or ontogenetic development but not at others should be reached only after extensive systematic variation of a number of relevant parameters has been accomplished. It goes without saying that “complete” systematic variation is an ideal, and that most investigators, including ourselves, are likely to suggest developmental transitional stages and divergences after very little systematic variation of parameters has been undertaken. These suggestions can properly be regarded as working, hypotheses-and nothing more.

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DIFFERENCES IN PARADOXICAL EFFECTS C. SPECIES In fish and turtles, four paradoxical effects shown in adult rats (and also in birds)-successive negative contrast (SNC), the magnitude of reward extinction effect (MREE), the overtraining extinction effect (OEE), and the partial reinforcement extinction effect (PEE)--have failed to appear, except in a few cases under conditions of highly massed trials. Consider the following experiment on SNC by Lowes and Bitterman (1967). Goldfish were trained to strike an illuminated target in order to receive Tubifex worms as a reward. Training was given at the rate of one trial a day for a 63-day period. Group 4 received a 4-worm reward and Group 40 a 40-worm reward on each trial throughout the training period, while Groups 4-40 and 40-4 had their reward magnitudes shifted approximately midway through training from 4 to 40 worms and from 40 to 4 worms, respectively. The group mean log target striking latencies are plotted as a function of three-trial blocks in Fig. 1 . The results show a clear reward-magnitude effect in the preshift phase of the experiment. In the postshift phase, Group 40-4 nevertheless failed to increase its latency of responding (decrease its speed) even to the level of Group 4, much less above that level. Group 4-40, on the other hand, improved its performance to the level of Group 40. This absence of incentive contrast in fish cannot easily be attributed to a lack of discriminability of the reward magnitudes. 2.20

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With regard to the MREE, we turn to an experiment by Gonzalez et a!. (1972). Three groups of goldfish were given one trial a day in an aquatic runway for a total of 24 acquisition and 39 extinction trials. The groups differed in terms of reward magnitude during acquisition, the different magnitudes being 1,4, or 40 Tubifex worms. As Fig. 2 shows, extinction performance was directly related to acquisition performance; there was no MREE. In an experiment providing information on the OEE in fish (Gonzalez et al., 1967b), trials per session (10 vs 20) was varied factorially with reward magnitude (1 vs 10 Tubifex worms) during acquisition of a target-striking response. After 12 training sessions, the four groups were extinguished. The results (Fig. 3) give no evidence of the OEE; persistence (resistance to extinction) was directly related to the number of acquisition trials. This absence of paradoxical extinction appears also to characterize the behavior of turtles. In a single study, Pert and Bitterman (1970) have tried and failed to demonstrate SNC, MREE, or PREE in turtles (Chrysemys picru picta). The one exception to the generalization that these three effects fail to appear in any form in fish and turtles is that while neither fish nor turtles show the PREE in widely spaced trials (Gonzalez et al., 1965; Longo and Bitterman, 1960; Shutz and Bitterman, 1969), the effect can apparently be demonstrated in massed trials in goldfish (Gonzalez and Bitterman, 1967) and turtles (Murrillo et al., 1951). On the basis of results such as these Bitterman has said that the fish and turtle are “Hullian animals,”* meaning that their performance in relation to reward reduction or omission (extinction) is not out of line with the theory of simple ’Personal communication. An exact quote (Bitterman, 1960, p. 708) is: “We might. . . conclude that contemporary S-R theory is appropriate at the level of the fish, although new processes of learning come into operation at the level of the rat.”

24 1

PARADOXICAL REWARD EFFECTS

learning proposed by Hull in his Principles ofBehavior (1943). The argument is that, in the fish and turtle, reinforcement (reward) has a direct effect on the association (the greater number of rewards resulting in greater associative strength), but that these animals do not learn “about reward,” which is to say they do not form anticipations or expectancies about reward or nonreward. As there seems to be some agreement that birds and mammals share a common ancestry in the class Reptilia dating back about 250 million years (Colben, 19SS), it could be the case that the ability to learn about rewards is a system in vertebrate evolution. There also appear to be cases in which adult humans operate as “Hullian animals. In one of his last articles Spence ( 1966) summarized and interpreted a series of experiments from his laboratory and elsewhere having to d o with cognitive and drive factors in human eyelid conditioning. He sought to integrate findings from a series of experiments in eyelid conditioning in which a “masking” procedure had been employed. In the masking situation, the conditioning of the eyeblink response is imbedded in a larger set of experimental manipulations designed to reduce the influence of cognitive (expectacy) factors and particularly to minimize awareness of the transition from acquisition to extinction. A task devised by Estes and Straughan (1954) was used to mask the intent of the investigation. Subjects were told to guess which of two side lights would come on next when a center signal light appeared, and to press a right or left button to ”

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ABRAM AMSEL A N D M A R K STANTON

so signify. The “cover story” was that the experiment had to do with the effects of distraction on their performance on this task, and that distracting stimuli in the form of a tone and an air puff to their eye would be given between pressing the button and lighting of one of the side lamps. Of course the tone and the air puff were the CS and US, respectively, and the guessing task was designed to minimize cognitive involvement in the conditioning. Under these masking conditions, Spence and his students found that extinction following continuous reinforcement is very greatly retarded and is very much like the rate found in experiments with lower animals; under the masking conditions the partial reinforcement extinction effect is absent in humans as it often is in animal experiments on classical aversive conditioning (see Spence, 1966; Wagner ef al., 1967). For our present purposes, these findings suggest that there is a level of adult human functioning, corresponding perhaps to functioning at lower phylogenetic and ontogenetic levels, in which learning and extinction (reaction to reinforcement change) can proceed without benefit of cognitive mediation (goal anticipation). This point, which is reminiscent of our earlier quote from Bitterman (1960), has also been made by Amsel (1972b) in the context of a distinction between pure classical and preparatory Pavlovian conditioning, and by Wickelgren (1979) who has very recently pointed out that the Thorndike-Hull S-R associative theorizing may turn out to be an important and appropriate model for learning at noncognitive levels. Our developmental work suggests that transitions between nonparadoxical and paradoxical effects of reward from one infant-rat age to another may be the ontogenetic counterpart of ( a ) the transitions between the fish-turtle and the bird-mammal stages phylogenetically, and (b) the transitions between masked and unmasked extinction effects in adult human eyeblink conditioning. The implication in the latter case is that the fish-like infant becomes the adult but remains the fish-like infant at the same time. It would be interesting to show, in this regard, that extinction in infant human eyeblink conditioning has the characteristics of extinction under masked conditions in adults.

V. TOWARDAN ONTOGENETIC ANALYSIS OF PARADOXICAL EFFECTS We are now ready to summarize some of our recent work on the ontogeny of paradoxical effects in the rat. In general, our strategy has been to start with juvenile- and weanling-age rats and to work with younger and younger animals, concentrating finally on the age range 11 to 14 days. In our presentation, we will combine the treatments of some of these effects because in many cases it was convenient to study two or more of them in the same experiment. Within each

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subsection we will present data from experiments over the last 4 or 5 years more or less in the order in which these experiments were performed. At the end of this section we will provide a tabular status report of the ages at which the various paradoxical effects have first been observed in our experiments. A.

THEPREE AND MREE

Our earliest work in this area dealt with the ontogeny of the PREE. As a first approximation to answering questions about the age at which persistence resulting from PRF treatments can first be acquired and retained, we reported differences in PREE between young rats whose runway training started at 30 days of age and weanling rats whose training started at day 18 (Chen and Amsel, 1975). Extinction of running after CRF training was very slow and gradual in the weanling rats, but extinction in the older, but still young, rats was more like the adult pattern, abrupt and negatively accelerated. A comparison of extinction performance following CRF and PRF acquisition at both ages showed a very durable P E E , in the sense that it could be demonstrated following a 45-day vacation period and a phase of CRF reacquisition. In experiments that followed we restricted the training to narrower age ranges and studied younger pups. In the first of these (Burdette et al., 1976), there were four age groups, and at each age original training was restricted to a 2.5-day period, followed by a 2-day extinction period which began 12 hr after terminal acquisition. These experiments revealed a very clear PREE when the CRF and PRF treatments were given as early as in the 18- to 21-day range. In a second experiment, another group was added at each age to equate the PRF and CRF groups for rewards rather than trials. This rewards-equated group is designated PRF-R. Using only the two extreme age groups, trained at 18-21 or 35-38 days, the result was the same: while persistence was not different between PRF and PRF-R conditions at either age, a clear PREE emerged in comparisons between the two PRF groups and the CRF group at both ages. In two experiments we looked for the magnitude of reward extinction effect (MREE) at various ages. In the first of these (Burdette er af., 1976, Experiment 3) rats were trained at 18-21 or at 36-39 days of age under CRF conditions with either a 45- or 300-mg food pellet as reward. The MREE was shown to operate in preweanling and juvenile rats as it does in adults: larger reward in CRF acquisition led to faster extinction at both ages. It was also the case that preweanling rats were more persistent following CRF training than juveniles at both reward levels. In a second experiment (Chen and Amsel, cited in Amsel, 1979) PRF or CRF acquisition were combined factorially with 45- or 300-mg reward at three ages: preweanling age (17-20 days), and at 30-33 and 55-58 days of age. (At preweanling age an intermediate level of reward, 97 mg, was also included.) Our data show that at all ages, the size of the PREE was greater following training

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with large than with small reward (Fig. 4), and that at all ages the effect is attributable to a direct relation between CRF reward size and rate of extinction, the MREE. To examine more closely the development of the PREE over the preweanling age range. we (Amsel and Chen, 1976, Experiment 1) included three groups spanning 17 to 2 1 days of age at the start of training along with three older groups for comparison. The older groups started at days 28, 35, and 65. Training was restricted to a 2-day period. A clear PREE was present at all ages. There was an inverse relationship between resistance to extinction and age, particularly after PRF training (Fig. 5 ) . In a second experiment retention of persistence over 45 days was demonstrated at three different ages, including the youngest group, trained at 17- 18 days. These experiments confirmed that rats trained in a runway at preweanling, weanling, and juvenile ages show the PREE and W E E in an immediate extinction test, that the PREE is, if anything, greater in preweanlings than in the older rats, and that it is retained into young adulthood. The very interesting questions that arise from an ontogenetic perspective are: ( a )Is there a transitional age range for the PREE, the MRE,E, and other paradoxical effects? (b) What is the order of their first occurrence? (c) Do the approximate ages of first appearance of these effects correspond to periods during which other significant behavioral and physiological changes are occurring? In most of our recent experiments, we have settled on the range I 1 to 14 days as an apparently

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FIG.5 . Acquisition and extinction of a running response in the rat as a function of age (in days) and reward schedule (CRFvs PRF). From Amsel and Chen (1976).

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ABRAM AMSEL A N D MARK STANTON

important one for the appearance of the PREE, and we have moved from this finding to the investigation of other ages and effects. Because rat pups cannot be weaned much, if any, earlier than 16 days of age we needed to develop a procedure that would enable us to study reward-schedule effects in a seminatural setting. The general procedure is as follows: Pups are culled to litters of eight at 3 days of age, are separated from their mothers at times appropriate to deprivation conditions, and are placed in a plastic chamber maintained at 33°C (the average temperature in an undisturbed nest). Experimental training is in a clear Plexiglas alley (usually 32 cm long and 8 cm wide) also maintained at 33°C. Approximately 20 min prior to the first trial, a lactating dam receives an injection of a general anesthetic producing a surgical level of anesthesia and blocking milk release (Lincoln et al., 1973; Wakerley and Lincoln, 1971). Preliminary training in these experiments consists of one or more “priming” trials in which each pup is placed either in the goal chamber or directly against the dam and allowed to attach to a nipple and suckle for a short period of time. At the end of this time the pup is gently detached from the nipple, carried by hand to the opposite end of the alley, and allowed to approach the dam. On reward (R) trials the dam is positioned on her side at the end of the alley and the pup is permitted to attach to a nipple, usually for 15 to 30 sec. On nonreward (N) trials, the dam is removed from the alley or the pup is prevented from reaching her. Using such a procedure we were able to demonstrate appetitive learning and 5-trial patterned alternations of acquisition and extinction of an approach (“crawling”) response in 10-day-old rat pups (Amsel et al., 1976). In this experiment, the dam was removed from the goalbox on N trials. Because of the possibility of differential distance cues related to the presence and absence, respectively, of the dam on R and N trials (the “homing” factor), we changed the apparatus and the procedure in later experiments so that the dam was in the goal box on all trials but was inaccessible to the pup on N trials. (In later experiments we also added an exhaust fan to the chamber in which the dam was placed.) This was accomplished with an apparatus in which the anesthetized dam was in the rear portion of the goalbox and could be made accessible or inaccessible to the pup by a door that bisected the box. The most important feature of the procedure was that there was no possible differential stimulation from the mother’s presence or absence while the pup was in the runway and the approach response was being measured (Amsel et al., 1977). Using this changed procedure we repeated the 5-trial ALT experiment of Amsel et al. (1976) and manipulated two factors-presence/absence of the dam on N trials, and 0- versus 15-sec detention in the goalbox on N trials. There was no effect in acquisition attributable to either factor. In extinction, where the dam was either present but inaccessible on all trials or absent on all trials, and where detention in the goal box was 0 or 15 sec, approach responding extinguished in

247

PARADOXICAL REWARD EFFECTS

all groups, the No-Detention groups being somewhat less resistant to extinction than the Detention group, and the Dam-Present groups extinguishing more slowly than the Dam-Absent groups. The procedure in this experiment eliminates any nonassociative interpretation of acquisition, patterned alternation, and extinction in 11-day-old rats, lending confidence that we are dealing with a true form of learning maintained by the reinforcing properties of suckling/contact. A later experiment (Amsel et al., 1977, Experiment 3) showed that simple contact with a male or female conspecific can also serve as a reinforcer for 1 1-day-old PUPS. It was a recent series of three experiments (Let2 er al., 1978) that led to the conclusion that the period between 1 1 and 14 days of age is transitional for the PREE in the rat. In one of these experiments (see Fig. 6 for results) the reinforcer was either 30 sec of dry suckling or 5 sec of milk from an anesthetized dam induced to lactate by oxytocin injection. While the most interesting extinction effect for our purposes was the occurrence of a PREE in 14- but not 1 1-day-olds, another interesting result was that, at both ages and reinforcement schedules, the Milk groups extinguished more slowly than No-Milk groups and, in fact, the 1 1-day-old Milk groups showed little evidence of extinction. If suckling with and ACQUISITION

EXTINCTION I

7 -

14-DAY-OLDS n

l6

b

t

g,,t W

w n (I)

5 1 11-DAY-OLDS

2

4

6

8

10

12

2

4

6

8

BLOCKS OF TWO TRIALS

FIG. 6. Acquisition and extinction of an approach response in a runway in infant rats as a function of age, reward schedule, and reward magnitude (“milk” = nutritive suckling, “no milk” = dry suckling, on an anesthetized dam). See text for details. From Letz e t a / . (1978).

24 8

ABRAM AMSEL AND MARK STANTON

without milk can be regarded as two reward magnitudes, which seems reasonable on the basis of the acquisition data, then the MREE might have been expected to occur in the CRF groups. It was not observed at either age. As we have seen, this effect is found in rats as young as preweanling age, 17-20 days, when the reward is dry food rather than milk (Burdette et al., 1976, Experiment 3; Chen and Amsel, cited in Amsel, 1979). In other recent work in our laboratory (Chen and Amsel, 1980a) we have again found evidence of the PREE in preweanling rats given acquisition and extinction between 14 and 15 days of age. In one experiment we used as the reinforcer a restrained unanesthetized lactating female rat that was given periodic ip injections of the hormone oxytocin to stimulate milk release. Nonreinforcement was absence of the dam. There were 28 training trials, CRF or PRF, and 20 trials of extinction. There was also a nonreinforcement (NRF) control. Subjects in the PRF groups were more persistent in extinction than those in the CRF group. The NRF group showed no significant acquisition or “extinction. ” In another experiment using a similar procedure where reward was an anesfherized lactating (oxytocin-injected) female we found that a PREE in pups trained for 40 trials between 14 and 15 days was retained over a 13-day interval. In a third experiment (Chen and Amsel, 198Ob), we showed a PREE in rats trained at 12-13 or 1 1-12 days, with extinction on day 13, but not in pups trained between 10 and 11 days, with extinction on day 11 or day 13. We have now made PRF-CRF extinction comparisons under a variety of different conditions, including a very recent experiment involving 120 acquisition trials (Stanton et al., 1980), and we have been unable to induce persistence in 1 1-day-old rats, but have been able to do so in rats 1 to 3 days older. In the case of the MREE, we have shown this effect in preweanlings but not in 14-dayolds. In mature rats the strength of the PREE and MREE depends on a number of training variables-number of acquisition trials, trial spacing, deprivation level, reward magnitude, and others. Our failure to demonstrate a PREE at day 11 or MREE at day 14 may therefore reflect, in Bitterman’s terms, too narrow a range of systematic variation. On the other hand, it may possibly reflect true transitional periods in development of the PREE and MREE. There are many observations to suggest that in several other respects the 10- 15 day age range does include important transitional periods. Infant rats spend at least 12 hr each day attached to a nipple but receive milk in discrete episodes following the milk ejection reflex triggered by the release of the neurohypophysial hormone, oxytocin (Wakerley and Lincoln, 1971). These brief, intermittent episodes of milk release are separated by 5-15 min of non-milk suckling. Two changes in the suckling behavior have been reported in rat pups 12-14 days of age (Hall et a[., 1975): ( a ) a sharp increase in the number of pups detaching from a nipple and scrambling for another immediately after milk ejection (see also Drewett et al., 1974), and ( b ) an inverse relation between duration of food

PARADOXICAL REWARD EFFECTS

249

deprivation and latency to attach to a nipple beginning at this age, but not at younger ages. At around 14 days of age pups first open their eyes, gain the ability to thermoregulate, begin to leave the nest, and begin to meet their nutritional needs in ways other than suckling (Bolles and Woods, 1964). In addition, this age range includes the age at which the maternal pheromone is first reported to appear (Holinka and Carlson, 1976; Leon, 1974; Leon and Moltz, 1972). It seems to be the case, then, that the mechanisms responsible for maintaining the mother-infant bond undergo a change at about 2 weeks of age. Up to about 2 weeks of age, suckling, even during the long no-milk intervals, and contact with the mother may be viewed as involving a kind of built-in persistence essential for survival. This suggests the possibility that as eating and drinking come more and more under direct instrumental control of the pup, externally imposed differential-reward schedules and magnitudes may become more and more effective determinants of learned persistence, and of the MREE. B.

SUCCESSIVE NEGATIVE CONTRAST (SNC) ALTERNATION (PA)

AND

PATTERNED

Information on the ontogeny of SNC has been sparse. In one experiment (Sayheed and Wolach, 1972), SNC was not found in "immature" (45-day-old) rats even though training was conducted in such a way that they reached maturity at the end of the experiment. The rewards used, however, were not different enough to produce SNC in the adult ( 1 10-day) control condition. Another study (Roberts, 1966) has shown significant contrast in adult (180-day) but not in immature (25-day) rats following 21 preshift trials given at the rate of one trial a day. Here, too, maturation was confounded with learning; the immature rats were 46 days old at the time of the shift. In any case, neither of these studies used animals young enough to be in the age range we have identified as transitional for the PREE. In one experiment, we (Stanton and Amsel, 1980) examined the effects of downshifts in reward in 11- and 14-day-old rat pups under conditions that were similar to those which produce the PREE (Letz et al., 1978). The major difference between the procedures of Letz et a/. and those used in this and other recent experiments in our laboratory is that while Letz et al. used a nutritive suckling condition involving injections of oxytocin to induce milk release, we have recently changed to an oral cannulation procedure in which light cream is injected as reward while pups suckle on an anesthetized dam. The cannulation technique. which offers several advantages, such as control over the timing and amount of milk delivery, was adapted from Hall and Rosenblatt (1977). The cannula, a piece of PE-I0 tubing, has a flanged end which rests securely on the tongue, exits at the ventral surface of the jaw, is pulled through a small fold of skin behind the head and secured there with two heat-flanged washers.

250

ABRAM AMSEL AND MARK STANTON

Our main experiment on SNC is a 2 x 2 x 3 factorial design, the factors being age (1 1 vs 14 days), deprivation (16 vs 24 hr), and groups. The groups, representing reward manipulations, are as follows: Large reward control (M-M), small and downshifted group (M-M).Large reward reward control (suckling/milk, designated “M”) consisted of 30 sec of suckling on the anesthetized dam plus infusion of 0.03 ml commercially available “Half and Half” at room temperature. The infusion, which took about 5 sec, reliably elicited the “stretch reflex” (Lincoln et al., 1973; Vorherr et al., 1967). Small reward (Sucklingho-milk, designated “M”)consisted of 30 sec of suckling on the anesthetized dam with no diet infused. Figure 7 presents the results from each age-deprivation condition in a separate panel. There were clear and highly significant effects in acquisition of both reward level and deprivation; but at neither age nor deprivation condition was there any evidence of SNC. In each case, the performance of the downshifted group declined to the level of the dry suckling controls but not below. This suggests that preweanling rats do not possess the processes responsible for the expressions of SNC. In a second experiment, we sought to produce an SNC effect by running older subjects: 16-day-olds were run under the 24-hr deprivation condition. We chose 16-day-olds because they are still young enough for the sucklingho-milk condition to be an effective lower level of reward. The results were the same: there was no evidence of SNC at 16 days of age; but again, at age 16 days, shifts in levels from high to low reward produced significant shifts in performance appropriate to the low-reward level. The failure to find SNC over the age range 11 to 16 days could have a number of explanations, and it is necessary to summarize these as a lead-in to the rationale for our work on the ontogeny of patterned (single) alternation. As you will recall, an explanation offered for failure to obtain SNC in goldfish (Lowes and Bitterman, 1967)-0ne that could apply equally here-is that instrumental performance in this species (at this age, in our case) is not governed by the incentive (or “reward expectancy”) mechanisms that have been advanced to explain SNC in adults. Instead, the level of learned performance in pups aged 11-16 days reflects the direct reinforcing action of the reward on an S-R association, and the reinforcing action is directly related to the magnitude of the reward. Lowered reward anticipation (or increased frustration) is not a factor at this age. In brief, as Bitterman has said of goldfish and turtlesand as we said of humans undergoing classical conditioning without cognitive involvement-the 11- to 16-day-old rat pup acts like a “Hullian” animal, whose performance, reflecting habit strength, is directly related to magnitude of reinforcement, not to incentive motivation. A second interpretation of these results is in terms of the sequential hypothesis of incentive contrast (Capaldi, 1967; MacKintosh, 1974). The guiding principle

(M-a),

25 1

PARADOXICAL REWARD EFFECTS

Preshift

Post Shill

Preshift

Postshift

-

?

4

6

2

4

2

4

M-M M-M

6

2

4

Blocks of Four Trials

FIG. 7. Effect of reward reduction on performance in a runway as &functionof deprivation period (16 vs 24 hr) and age (1 1 vs 14 days). Group M-M was shifted from suckling/rnilk to sucklingho-mi&. _The other groups were not shifted, Group M-M receiv-

ing suckling/milk and Group M-M receiving suckling/no-milk in both phases. From Stanton and Amsel (1980). here is that instrumental responding on Trial N + 1 is conditioned to the stimulus trace (or memory) of the reward outcome on Trial N. In the usual contrast experiment the inferior performance of the shifted animals in the postshift phase is the result of generalization decrement: the feedback stimulus from large reward on Trial N, that controls the response on Trial N + 1, is replaced by a feedback stimulus from small reward. A sequential interpretation of the failure to observe SNC in our infant rats would be that this failure reflects their inability to discriminate the aftereffects of suckling/milk from sucklingho-milk. A similar explanation has been offered by Mackintosh (1971) for the absence of SNC in goldfish. A third interpretation of these results derives from frustration theory (Amsel, 1958, 1967), which, you will recall, accounts for SNC in terms of an aversive state (primary frustration, RF),that occurs unconditionally when expected reward exceeds realized reward, and the conditioned form of that state, anticipatory frustration (fF-sF), that arouses an avoidance tendency. This avoidance tendency, added to other possible decremental consequences of reduced reward, produces

25 2

ABRAM AMSEL AND MARK STANTON

the below-baseline performance in downshifted animals. On such a theory, the absence of SNC in preweanling rats reflects ( a ) absent (or weak) RF, ( b )absent (or weak) rF-sF, (c) an absent (or weaker-than-in-adults)connection between sF and avoidance, or ( d ) some combination of these. In another experiment, this time using only 14-day-old pups, we tried again to produce SNC and, at the same time, to provide some evidence for or against these various interpretations. First, we increased the number of trials, both preshift and postshift. Increasing the number of preshift trials, we reasoned, should increase the strength of the reward expectancy (rH-sR)and hence of primary frustration (RF)following the downshift. It should also increase the effectiveness of generalization decrement when the downshift occurs. The number of postshift trials was increased for similar reasons. It is possible that rF is conditioned very slowly at this age and requires more trials to be effective. We further tested the hypothesis that frustrative processes are weak at this age by extinguishing the low- and high-reward control groups (Groups M-Mand M-M) at the end of the postshift phase to see if the MREE would appear. (As you recall, we had not found it in earlier experiments with fewer trials at this age.) Finally-and this is important-we assessed the role of carryover (and the discriminability of the large- and small-reward magnitudes) by including a group that was trained on a patterned (single) alternation (PA) schedule. This schedule consisted of regular, single alternations of the large (sucklinglmilk) and small (sucklinglno-milk) rewards used in the SNC condition. When adult rats are run on this schedule, they acquire a tendency to run fast on large and slow on small-reward trials. The most popular interpretation of this result, particularly in massed-trials conditions (Mackintosh, 1974), is that animals learn to respond discriminatively based on the previous trial outcome, the S + being some trace or memory of the previous small reward and the S- of the previous large reward. Performance on a singlealternation schedule, then, should tell us whether or not sequential processes (Capaldi, 1967) are operating in our 14-day-old rats. Subjects were divided into four groups, the usual three SNC groups, M-M, fi-m, and M-M ( N = 12lgroup from 12 litters) and a group run on an alternation schedule, Group PA-M-fi ( N = 8 from at least 5 litters). Subjects in Group PA-M-fi received suckling/milk reward on odd-numbered trials and suckling/ no-milk reward on even-numbered trials. Training was carried out in a single day in three sessions of 40 trials each (120 trials total). The intersession interval was 5-6 hr. For all groups, the intertrial interval was 8 sec. For the three SNC groups, the first session and a half (60 trials) served as the acquisition phase. The postshift phase was 30 trials long, consisting of the second half of session two and the first 10 trials of session three. At that point, extinction began and continued for the remaining 30 trials of session three. Only Groups M-M and ~ -were M extinguished. Group M-M was terminated at the end of the postshift phase. Group PA-M-a received patterned alternation training for all 120 trials of

253

PARADOXICAL REWARD EFFECTS

the experiment. The deprivation interval was 24 hr. The large-reward was 0.03 ml Half-and-Half within a 30-sec suckling period; the small reward was 30 sec dry suckling. Figure 8 summarizes the results. Performance of the three SNC groups over all phases of the experiment is in panels A, B, and C, and performance of Group PA-M-M is in panel D. As in earlier experiments, there was a magnitude-ofreward effect in acquisition, pups approached milk reward significantly faster than dry suckling reward. Group M-M rapidly declined to the level of M-M performance but not below; there was no SNC. In extinction, there was the suggestion of an MREE which would seem to fall in line with the failure to find this effect with fewer trials at this age (Letz et al., 1978, Experiment 2), on the one hand, and, on the other hand, that it is clearly present in preweanlings (Burdette et al., 1976). The important finding of this experiment, in our view, is the presence of patterned responding to single alternations of reward magnitudes in the absence of SNC in 14-day-old rat pups, despite extended preshift training in which they manifested a very large reward-magnitude effect in acquisition. A 30

. -g

Acquisition

I

10

b.+.

-

’.O

10 -

0

I

I

I

I

1

I

L

FIG.8. A comparison of-SN_C and patterned alternation in 14-day-old rats. The two control groups, M-M and M-M,are rewarded with nutritive and dry suckling, r e v tively, in acquisition (A, B) and this is followed by extinction (C). The-shifted group shows the effects of a reduction from nutritive to dry suckling (Group M-M, A, B). The PA results are shown in (D). From Stanton and Amsel (1980).

254

ABRAM AMSEL AND MARK STANTON

In one of another set of experiments (Chen et al., 1980) involving different feeding systems-ating of dry food and drinking milk out of a cup-adult subjects showed the classic Crespi-&man depression (contrast) effect with dry food as reward, while weanling rats (17 to 24 days old) showed no evidence of SNC with these dry food pellets. In another experiment comparing pups 25-26 and 35-36 days old using food pellet rewards, the 35- to 36-day-olds showed a strong SNC effect and the 25- to 26-day-olds showed a small and marginal SNC effect. When milk taken from a cup was the reward at three ages, 25- to 26-dayolds showed clear SNC, there was a suggestion of SNC in 20- to 21-day-olds, but none in the 16- to 17-day-olds. The large reward was 0.3 ml, the small reward 0.02 ml. A further experiment attempting to produce contrast effects in pups 16-17 days old under massed-trial conditions, and also to determine the effects of magnitude of reward on extinction in 16- to 17-day-olds, failed to show either SNC or the MREE.

FIG. 9. A comparison of patterned (single) alternationin a runway at 11 and 14 days of age. Reward (or odd-numbered trials) was nutritive suckling. Nonreward (on evennumbered trials) was goalbox confinement without access to the dam. From Stanton e t a / . (1980).

255

PARADOXICAL REWARD EFFECTS

We have been able to demonstrate PA not only at 14 days of age, but even at 1 1 (Stanton rt al., 1980). Three conditions have been employed: ( a ) suckling with milk delivery alternated with nonreward (no contact with dam); ( b ) suckling without milk delivery (dry suckling) alternated with nonreward; and (c) alternation of milk-suckling and dry suckling. The apparatus, general methods, and procedures of the experiments were the same as in the previous ones. The results of these experiments can be summarized briefly: all three alternating reward conditions resulted in patterning in both 14- and 1 I-day-olds. In every experiment, plots of blocks of R against N trials, and trial-by-trial plots of average speeds over the last 10 trials, showed this effect. The data from the first experiment are shown as an example in Fig. 9. A series of control conditions were also run for comparison. One group (CRF) was rewarded on every trial for 120 trials. Another group (PRF) received 120 trials on a 50% reward schedule such that the outcome of Trial N had no predictive value for Trial N 1. As expected, no suggestion of patterned alternation in running speeds appeared in either of these groups. These experiments show that infant rats, I 1 and 14 days of age, can learn patterned responding on the basis of single alternations of various combinations of reward, reduced reward, and nonreward. This learning is most efficient when milk-suckling is alternated with no-suckling nonreward, but occurs as well when dry suckling and nonreward or milk- and dry-suckling reward are alternated. Taken together, these experiments indicate that neither milk-delivery-related nor suckling-contact-related cues are necessary for patterning but that either is sufficient. It seems reasonable, then, to summarize the conditions that have produced patterning in these experiments as any that create a reward discrepancy.

+

C. THEOVERTRAINING EXTINCTION EFFECT(OEE) Our investigations of the OEE are not as far along as is our work on the ontogeny of the other reward effects, but our work on this phenomenon also suggests that a theoretically meaningful transitional period can be determined. We have completed three experiments (Stanton and Amsel, 1980). In the first experiment, we investigated the OEE at 14-15 days of age, and we used the cannulation technique with nutritive suckling on an anesthetized dam as the reward. One group received 85, the other group 25 acquisition trials. We reasoned that if frustrative processes are weak or absent at this age, as is suggested by our data on SNC, the OEE should not be observed. The methods were generally the same as in the SNC work. The apparatus was the same one used in our investigations of contrast and patterning. The entire experiment took six sessions, three sessions per day for 2 days. Group 85 received 20 acquisition trials in each of the sessions from one through four and 5 acquisition trials at the beginning of session five. At this point, extinction began

256

ABRAM AMSEL A N D MARK STANTON

without signal or delay and continued for 25 trials. An additional 30 extinction trials were given in session 6. Group 25 was treated like Group 85 except that it received handling during the first three sessions rather than acquisition training. The IT1 was about 90 sec. In an attempt to equate groups for deprivation, subjects were taken at the end of these sessions to another room and “postfed” at the nipple in a plastic cage bearing no auditory, tactile, or thermal resemblance to the goalbox. Group 85 subjects were fed one reward (0.03 ml) and Group 25 subjects were fed one reward plus the amount received by the Group 85 subjects during the training session. The results can be summarized briefly: There was a significant asymptotic difference, the group given 85 acquisition trials reaching higher speeds than the one given 25 trials. This difference remained throughout the extinction phase: there was no evidence of the OEE. In a second experiment we tested animals 60-70 days of age in a runway using the same spacing and distribution of trials as were used in the first experiment. The reward was a single 190-mg Noyes food pellet. The straight runway was 103 cm, instead of 38 cm, long, and was made of wood instead of Plexiglas. The acquisition results were very similar to those of the first experiment. The greater number of trials resulted in greater asymptotic speeds. In extinction an OEE showed up in each of three measures, and, of course, in an overall speed measure. The number, distribution, and spacing of training trials that failed to produce an OEE at 14-15 days was sufficient to do so at 60-70 days. It is possible, however, that the other procedural differences, not developmental differences, between the two experiments account for their respective outcomes. To avoid this problem in a third experiment, we compared the performance of preweanling (18- to 19-day-old) and weanling (25- to 26-day-old) rats in the same apparatus and with the same reward, milk in a cup. (The experimental design was the same one used in the previous experiments.) Our use of these ages and this reward was based on the experiments of Chen el al. (1980) showing SNC under these conditions. You will recall that in these experiments, where reward consists of milk in a cup, SNC appears at 25-26 days, being absent at younger ages. Our investigations of the ontogeny of the MREE showed that by 18-19 days this effect also occurs (Amsel and Chen, 1976; Burdette et al., 1976; Letz et al., 1978; Stanton and Amsel, 1980). On the basis of these data, we expected to find the OEE at 25-26 days but not at 18-19 days. The apparatus was the same one used in the second experiment except that the food trough was replaced by a stainless-steel cup. Reward consisted of 0.10 ml commercial Half-and-Half in the cup. In all other respects, the procedure in this experiment was the same as in the second experiment. As in the previous experiments, the 85-trial subjects ran significantly faster than the 25-trial subjects. This was true at both ages. A summary of the extinction data is as follows: while there was some evidence of the OEE at 25 days, it was not strong, and a clear “reverse-OEE” was found at 18 days.

257

PARADOXICAL REWARD EFFECTS

CURRENT PATTERN O F

TABLE I1 REWARDEFFECTS AT VARIOUS ACES

RESULrS ON

Reward effect Age (days) I1

14-20 21-25

25 + Adult

PA

PREE

MREE

SNC

OEE

Yes Yes

No Yes Yes Yes Yes

No No Yes Yes Yes

No No No Yes Yes

-

-

Yes

No

-

Yes Yes

Table I1 provides an idealized summary of our results on the ontogeny of paradoxical effects, showing the approximate age at which we have first seen each effect in our experiments. Our basis for identifying the “transitional” ages is stronger for some effects than for others. Even in our strongest case (the PREE), however, a greater degree of systematic variation could produce a different result. It would therefore be wise to regard this summary as an interim report, and we offer the following admonitions: ( a )It would be wiser to think in terms of ease of producing an effect at a particular age than in terms of an absolute age at which an effect first appears. ( h ) The order of appearance in ontogeny of an effect, as we present this order on the basis of a small number of experiments, should, as we have urged previously, be taken as nothing more than a working hypothesis.

ON VI. COMMENTS

THE

NEURAL SUBSTRATE OF PARADOXICAL

EFFECTS Because, in the alaicial rat, rapid postnatal behavioral and physiological development occur in parallel, the rat’s behavioral ontogeny is particularly open to physiological interpretations. Toward this end, a thorough developmental psychobiology (biopsychology) is a necessary long-run strategy, a fact attested to by the exponential increase in the amount of work we see in these fields. In the short run, however, a simpler strategy is available: combine what is known of the physiological basis of behavior in adults with data on neural development and see if this leads to any understanding of ontogenetic trends in behavior. This shortrun strategy has obvious dangers. First, since many neural changes occur simultaneously during development we must either designate one (or some) of these changes as particularly salient while ignoring the others, a very risky undertaking; if we consider all (or many) of the changes simultaneously we are back quickly to the long-run strategy. Second, the techniques employed in deriving the

258

ABRAM AMSEL AND MARK STANTON

adult “reference data” often are not the kind that can provide information that meshes with the developmental data. For example, among the neural developments that occur in ontogeny are changes in the organization, orientation, or afferent-efferent relations of the gross anatomical structures. The common techniques of adult physiology-lesions, stimulation, and recordingdo not address the effects of these changes. Third, the short-run strategy adopts, but does not test, the assumption that adult brain-behavior relationships apply as well to infants, that as a portion of the brain achieves adult-like status a corresponding adult-like behavior will be possible. That these examples have been taken from ontogenetic development should not provide comfort to comparative investigators; the problems described in these examples are, if anything, worse in phylogeny (Nauta and Karten, 1970). In spite of these and other dangers, the short-run strategy has value, at least as a preliminary heuristic. it is in this spirit that we offer a selective review of what is known so far of the biopsychology of the paradoxical effects, and search for convergences and divergences between data on physiological and behavioral development. It has been over four decades since Papez (1937) made his now classical proposal of a limbic substrate for emotion. An account of the paradoxical effects in terms of frustration makes it natural to look to the limbic system for their neural substrate. There is now much evidence for limbic involvement in the paradoxical effects. For example, sensitivity to reward changes has been disrupted by lesions of the amygdala (Schwartzbaum, 1960), and SNC has been eliminated by lesions of cingulate cortex (Gurowitz et al., 1970), and by administration of the minor tranquilizers (Rosen et a l . , 1967; Rosen and Tessel, 1970) which alter the electrical activity of limbic structures (Guerrero-Figueroa et al., 1973). The component of the limbic circuit which we emphasize in this discussion is the septohippocampal system. The postnatal development of the dentate gyms of the hippocampus has been studied extensively (Altman and Bayer, 1975). In the rat 90%of the granule cells develop postnatally. Differentiation increases rapidly at about 12-14 days and reaches adult levels at 25-30 days. This has led some writers (Altman et al., 1973; Douglas, 1975) to propose that hippocampal development plays a critical role in the ontogeny of “behavioral inhibition. These writers, however, differ somewhat in the way in which they characterize inhibition. Altman er al. adhere to a response inhibition view in the simple descriptive sense of peripheral response suppression. Douglas’ (1975) view is that the hippocampus is the substrate of Pavlovian internal inhibition, which is not equivalent to simple response suppression because response suppression may simply involve the competition of two excitatory tendencies, one appetitive, the other aversive. Pavlovian inhibition would operate equally to counteract excitatory tendencies of both kinds (see also Amsel, 1972b). Both parties base their views largely on studies of habituation to novel environments, spontaneous alternation, ”

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and passive avoidance learning. In all of these situations, performance decrements are found both in hippocampally damaged adult rats and in intact infant rats, the maturation of adult-like performance at 25-30 days coinciding with that of the hippocampus. It is ako noteworthy that the development of behavioral responsiveness to cholinergic drugs in the rat also coincides with that of the hippocampus (Campbell er al., 1969). Douglas ( 1975) has documented the evidence that, in adults, drug treatments which alter cholinergic function exert their behavioral effects via their action on the hippocampus, and therefore describes the system which is developing as the “hippocampal-cholinergic inhibitory system” (1975, p. 338). There is a third view on the nature of the behavioral inhibition subserved by the hippocampus. While it does not specifically address a psychobiological theory of behavioral maturation, it brings our work into line with such theories because it is based on a physiological analysis of the PREE in the context of the concept of conditioned frustration. This third view is that of Jeffrey Gray (1975, 1976, 1977) and his colleagues (Gray et al., 1978). According to Gray (1977), the septohippocampal system is an important component of the ‘‘behavioral inhibition system, a system responsible for halting ongoing behavior and increasing attention to the environment in the presence of cues associated with punishment, frustrative nonreward, or novelty. Gray’s theory also considers the septohippocampal system the substrate of mantained responding in the face of such cues (or habituation to their descriptive effect) under conditions in which such responding is the “best alternative” for the organism. [In this respect the system appears to act as the neural substrate for general persistence (Amsel, 1972a).] Gray’s is a more specific and detailed account of the functioning of the septohippocampal system than the response-braking idea (e.g., Altman ef al., 1973), and while the counterconditioning (habituation) aspect resembles Douglas’ (1972) Pavlovian inhibition view, these two positions differ in at least three respects. First, as it is based on two-process learning theory Gray’s position draws a distinction between inhibition of Pavlovian and of instrumental responding (Gray et ul., 1979). This could correspond to what we have referred to, respectively, as unmediated and mediated inhibition (after Amsel, 1972b). Contrary to Douglas (1972, 1975), Gray’s view is that instrunientul “inhibition” is subserved by the septohippocampal system. Second, according to Gray this is a system that suppresses, and builds persistence in, responses that have aversive outcomes (punishment or nonreward). Finally, Gray’s position must be distinguished from the others on the basis of the central position he gives to the role of the hippocampal theta rhythm. As Gray sees it, the relation between hippocampal theta and the operation of the septohippocampal system is as follows: Frequencies of theta associated with voluntary behavior (and the absence of reflexive behavior or fixed action patterns) lie above 8 Hz;those associated with reflexive behavior (and the absence ”

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of voluntary behavior) lie below 7 Hz; and theta frequencies in the 7 to 8 Hz range (specifically 7.7 Hz) occur when the behavioral inhibition system (specifically conditioned frustration) is active. The evidence relating this frequency of theta to conditioned frustration is quite convincing and includes the following: ( a ) 7.7 Hz theta occurs in response to nonreward in the goalbox of a runway (Gray and Ball, 1970). (b) Artificially driving theta (by medial septal stimulation) on 50% of the trials in a goalbox in which rats are always rewarded makes them more persistent than nonstimulated CRF controls (produces a “PREE”); 7.7 Hz theta-driving in extinction reduces persistence (Gray, 1972). ( c )Eliminating theta in PRF animals, either by overdriving with high-frequency septal stimulation in acquisition (Gray et d.,1972a), or by medial septal (Gray et a f . , 1972b), or full septal (Henke, 1974, 1977) lesions in both acquisition and extinction eliminates the PREE. Thus, all three techniques-recording, stimulation, and lesioning4onverge to suggest the same conclusion. Gray’s results have been corroborated in our laboratory by Glazer. He has shown that persistence in instrumental responding can be increased by inducing 7.5-8.5 Hz theta through pharmacological means, instrumental conditioning of theta, or electrical means (Glazer, 1972, 1974a, b, respectively). The effect on the P E E of blocking theta consists of an increase in resistence to extinction in the CRF animals coupled with a decrease in the PRF animals, a pattern that suggests interference with conditioned frustration. Essentially the same effect occurs in adult rats when maturation of the dentate gryus is disrupted by neonatal X-irradiation (Brunner et al., 1974), in rats treated with antianxiety drugs (Gray, 1977), and in rats subjected to noradrenaline depletion in the dorsal bundle by injection of 6-hydroxydopamine (e.g., Gray et al., 1979; Mason and Iversen, 1978; Owens et al., 1977). Gray has argued that all of these agents exert their effects by acting on the 7.7 Hz theta rhythm, the hippocampal activity that he proposes as the substrate for frustrative inhibition and for the counterconditioning mechanism in persistence. (Mason and Fibiger, 1978, take a different view-that the dorsal bundle extinction effect, as it is called by them, affects attentional mechanisms in acquisition, and that persistence increases for that reason.) In support of this position, Gray e? a f . (1979) present data on the effects of various drugs on the “theta-driving curve. This curve is obtained by plotting the current threshold for driving theta as a function of the stimulation frequency applied to the septal pacemaker cells. In the normal rat, this curve is V-shaped with the minimum threshold lying right at 7.7 Hz. Both the minor tranquilizers and 6-OHDA selectively raise the driving threshold at 7.7 Hz, producing a flatter (rather than a biphasic) theta-driving curve. The model presented in Fig. 10 summarizes Gray’s thinking and may be regarded as a hypothetical neural circuit for conditioned frustration. A number of other views on the functional significance of the hippocampal theta rhythm exist (see Isaacson and Pribram, 1975), and it seems likely that in its broad spectrum ”

PARADOXICAL REWARD EFFECTS

' inh;bits nonreworded behavtor

I fimbrio [counterconditioning1

26 1

' I '

*

Lot sept

Locus

FIG. 10. Hypothetical neural circuit of conditioned frustration and nonreward persistence. Signals predicting a nonreward response enter the medial septum (Med. sept.) and travel to the hippocampus via the theta producing fibers of the dorsal fornix. The hippocampus then either inhibits nonrewarded behavior or causes such behavior to persist by sending signals via the fimbria to the lateral septum (Lat. sept.), which inhibits the activities of the medial septum. The entire septohippocampal system is innervated by noradrenergic fibers of the dorsal bundle which originate in the locus coeruleus. The effects of antianxiety (antifrustration) drugs and of dorsal bundle lesions on persistence are thus explained. From Gray et nl. (1978).

conditioned frustration is, at best, just one of the many concomitants of theta. Nevertheless, there appears to be a plain empirical relation between frustrative suppression, the PREE, and hippocampal theta in adult rats, and this suggests the question: Do 1 1 -day-old rat pups, which show no evidence of the P E E , also fail to show hippocampal theta? Existing evidence (Vanderwolf et al., 1975) is that the age of first appearance of hippocampal theta in the rat is in the 12- to 14-day range, precisely the period that we have identified as transitional for the PREE. The fact that theta can be recorded at this age indicates the onset of at least some rudimentary functioning of the hippocampus. There is, interestingly enough, parallel evidence that the corticosterone level, which Levine and others (e.g., Coover er a l . , 1971) have shown to be elevated in appetitive extinction, and have taken to represent a physiological response to frustrative nonreward (Levine el a f . , 1972), is virtually absent in the rat between 6 and 12 days of age, and shows a significant rise at day 14 that continues until it peaks at day 24 (Henning, 1978). McEwen et al. (1975) have surveyed evidence for an interrelation between this steroid hormone and hippocampal function and in a recent report (Micco et al., 1979) have implicated corticosterone in nonreward persistence (Fig. 10). In addition to the work of Gray's group on the PREE, there exist lesion studies with adult rats which implicate the septohippocampal system in the other paradoxical effects of reward. Hippocampal lesions eliminate SNC (Franchina and Brown, 1971), and septa1 lesions appear to abolish the MREE (Wolfe

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et al., 1966). In the runway, hippocampal damage either eliminates (Franchina and Brown, 1970; Brunner et al., 1974, Experiment 3) or delays (Brunner et al., 1974, Experiment 2) the appearance of patterned alternation. In a Skinner box go/no-go paradigm, hippocampectomy eliminates patterning at an 80-sec IT1 (Walker et al., 1972), enhances it at an 8-sec IT1 (Means et al., 1970), and delays it at a 5-sec IT1 (Warburton, 1969). Cholinergic antagonists also impair PA in normal rats in this situation (Warburton, 1972). It is worth considering, therefore, how our data as a whole relate to the issue of hippocampal-cholinergic maturation and the ontogeny of inhibition. This involves two considerations: the degree of resemblance of the infant rats in our appetitive learning situation to adults with impaired hippocampal-cholinergic function, and the nature of the inhibition involved-response-braking, Pavlovian, or frustrative. With regard to the resemblance issue, the answer depends on the paradoxical effect in question and on whether, to go back to an earlier point, one chooses to speak in relative or absolute terms. In relative terms, our data indicate that inhibition increases with age. Extinction following both CRF and PRF training becomes more rapid with age (Fig. 5) and the appearance of some of the continuous-reward paradoxical effects (OEE and SNC) does coincide with the “completion” of hippocampal maturation. In absolute terms, however, we have documented instances of response inhibition, which in adults depends on hippocampal-cholinergic function, at ages (1 1 and 14 days) which clearly precede the proliferation of granule cells in the dentate gyrus: Acquisition and retention of the PREE are shown in the preweanling period; the MREE, which appears at 18-22 days, antedates hippocampal maturation; and patterned alternation, where response inhibition is very clear, is present even at 11 days of age (Fig. 9).3 Clearly, a deficit in, or absence of, response-braking (Altman et al., 1973) does not fit the performance of these 1 1-day-olds. They have no trouble “slamming on the brakes” after initiating responses on nonrewarded trials. A conclusion on the matter of whether the inhibition deficit is of a Pavlovian or frustrative nature is more difficult. It is of course possible that instrumental response suppression represents the summation of both kinds of “inhibition. What our data show is not an absence of inhibition in the hippocampally immature rat, but rather the absence of paradoxical inhibition. While preweanlings do not show SNC, their performance does decline with reward reduction to the level of the low-reward controls. Similarly, our failure to find the MREE until about 18 days of age, or the OEE until even later, does not reflect an absence of inhibition (in this case, extinction). Extinction is quite clearly present, but its ”

’While it is true that hippocampal lesions do not abolish PA in all situations (see above references)and that there is even evidence for a noncholinergic system mediating PA (Warbunon, 1969)-in the runway apparatus and with the training parameters (ITI, number of trials) we have employed, our 1 I to 1Cday-old rats bear a much closer resemblance to intact adults that to adults with hippocampal lesions in their ability to pattern on a single-alternation schedule.

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strength is directly, rather than inversely, related to acquisition reward factors. It is just not of the paradoxical sort. Possibly this nonparadoxical inhibition is present at birth. A recent report purports to show the reversal of an appetitive discrimination at 1 day of age (Johanson and Hall, 1979). Two recent reports (Campbell and Raskin, 1978; Smith and Spear, 1978) may be important in understanding the apparent contradiction between our findings and those on which the views of Altman and Douglas are based. These reports stress the importance of “nest cues” as a factor in the learning and/or motivation of infant rats. Campbell and Raskin (1978) point out that evidence for the Jacksonian principle of caudal-rostra1 (noradrenergic/excitatory-cholinergic/ inhibitory) brain development may depend on the testing situation used. They found that the peak in activity of rats at day 15, previously thought to reflect noradrenergidexcitatory maturation occurring in advance of cholinergicl inhibitory maturation (Fibiger el a / . , 1970), could be eliminated by testing the animals in the presence of nest cues. Their conclusion was that novel environments are particularly activating to young rats, and that activity measures in these environments are inappropriate to investigations of the Hughlings Jackson principle. Smith and Spear (1978) showed that the ability of 16-day-old rats to display inhibition in passive avoidance and spontaneous alternation tasks, precisely the situations that are the source of Altman’s and Douglas’ views, was dramatically affected by the presence of nest stimuli. When shavings from the nest were present, performance on all these tasks was adult-like. When clean shavings or no shavings were present, however, the classic inhibition deficit was found. If one assumes that an anesthetized dam constitutes a nest environment stimulus, as Smith and Spear do, our findings of simple response inhibition (but not necessarily paradoxical effects) in rats in the 1 1- to I6-day age range provide additional support for the idea that infants will be shown to have greater inhibitory capacity when they are tested in an environment that is not strongly arousing. Perhaps the rudimentary functioning of the hippocampus, suggested by the appearance of theta at 12-14 days, has behavioral impact in situations of low but not high arousal. Such an assumption would reconcile our data with the failures of others to find inhibition at this age.

VII.

A.

CONCLUDING CONSIDERATIONS: IMPLICATIONSFOR BEHAVIOR A N D BEHAVIOR THEORY

ONTOGENY OF APPETITIVE BEHAVIOR

While the main thrust of this article concerns theoretical considerations related to the ontogeny of learning and the paradoxical effects of appetitive reward, our work has some bearing on the ontogeny of appetitive behavior. Evidence has accumulated (Hall and Rosenblatt, 1977, 1978; Hall et a / . ,

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1975, 1977) which points to the development, between 10 and 20 days of age in the rat, of “the ability to pair the physiological consequences of suckling with the suckling behavior itself” (Hall and Rosenblatt, 1978, p. 424). The evidence comes from studies of nipple attachment and detachment. Attachment comes increasingly under the control of nutritive deprivation during this developmental period (Hall et al., 1977). Nipple detachment and termination of suckling appear at 10 days of age to be due to stomach fill per se (Hall and Rosenblatt, 1978), whereas at 20 days of age, detachment occurs before the stomach is full and depends very much on the nutritive value of what is ingested. What appears to be occurring is an increase with age in the ability to inhibit attachment and suckling in the absence of hunger. That suckling in the absence, as well as in the presence, of milk delivery reinforces approach and attachment in deprived 11- and 14-day-old infant rats is consistent with investigations of suckling behavior (Blass et al., 1977; Hall and Rosenblatt, 1977; Hall ef a l . , 1977). Our finding (Fig. 7) that deprivation increases approach speeds at 14 days but not at 1 1 days of age also is consistent with one of the aforementioned findings-that the incentive properties of suckling are becoming more deprivation-related over this age range. Deprivation increases approach speeds whether sucklinglmilk or sucklingho-milk is the reward. Another of our findings relevant to the work on the ontogeny of appetitive behavior is that, with deprivation held constant, suckling/milk appears to be a larger reward than sucklingho-milk, even at 11 days of age. This is true both between-subjects, as in our studies involving CRF acquisition (Figs. 6 , 7 , and 81, and within-subjects, as in our studies of patterned alternation (Fig. 9; Stanton ef a/., 1980). Whereas this finding does not contradict the suckling work in any direct empirical sense, as this work is derived from a consummatory rather than an instrumental response measure, it is contradictory to a possible implication of the suckling work that, at 11 days of age, dry-suckling and suckling for milk are about equally r e ~ a r d i n g .These ~ young animals seem more sensitive to the nutritive consequences of their instrumental behavior than they are to the consequences of suckling itself. This may mean that instrumental response measures are more sensitive than consummatory measures to motivational reward differences, possibly because the latter are more difficult to inhibit (Hall and Rosenblatt, 1978, p. 424; Martin and Alberts, 1979) or that milk intake has a rewarding effect on appetitive behavior at an earlier age than satiation suppresses 4This conclusion was drawn in a recent report by Kenny ef a / . (1979) who tested preferences for nutritive and dry suckling in a Y-maze. Our ability to demonstrate differential effects of these events at 1 1 days is attributable to our testing procedure and training parameters. In our patterned alternation procedure-which most resembles their preference test in that it provides a within-subjects assessment of nutritive and dry suckling-we employed an 8-sec IT1 and 120 trials. On the basis of unpublished data from our laboratory, we believe that had we used a 30-sec IT1 and only 60 trials, as Kenny e t a / . did, our results would agree with theirs.

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it. Whether this facilitating effect of milk intake depends on the gastric consequences of milk ingestion or on some other mechanism remains to be determined. €3. ONTOGENY OF REWARDLEARNING: DIFFICULTIES FOR THEORY The developmental data we have presented pose a problem for accounts of instrumental learning that attribute PA on the one hand, and the PREE, SNC, MREE, and OEE on the other, to the same mechanisms. The basic discrepancy that emerges out of our preliminary ontogenetic work can be summarized as follows: reward effects which involve intermittent reward (patterning, the PREE) develop sooner than those involving continuous reward (the MREE, SNC, the OEE). One can get patterned alternation at an earlier age than the PREE, and, the PREE, in turn, at an earlier age than SNC, the MREE, and the OEE. The appearance of PA at an earlier age than other paradoxical effects indicates that the failure of these young animals to respond in an adult-like manner to incentive reductions cannot be attributed to the absence of sequential (e.g., memorial) processes (Capaldi, 1972). This finding is noteworthy because of the emphasis these processes have been given by Mackintosh ( I 974) and others in explanations of the paradoxical effects of instrumental reward such as SNC. Earlier experiments with adult rats (e.g., Amsel et al., 1969; Surridge and Amsel, 1966) had failed to show patterned alternation under conditions (24-hr ITI) that are nevertheless capable of yielding SNC, the PREE, the OEE, the MREE, and other instrumental reward effects (but see Capaldi and Spivey, 1964, for the opposite results). Our earlier results seemed to show that sequential processes are not necessary for the Occurrence of these effects. Our finding that infant rats show PA but do not show SNC or a clear OEE or MREE seems to permit the stronger statement that sequential processes are not sufSiciertt to account for these effects either. If sequential interpretations of incentive reduction hinge on a “correlation between successive contrast and alternation learning” (Mackintosh, 1974, p. 401), our experiments showing alternation learning in 1 1 - and 14-day-olds suggest that this correlation is limited, at best. This dissociation of patterned alternation and these other paradoxical effects appears also to be characteristic of the behavior of ‘‘lower” organisms. Fish and turtles do not show the MREE, SNC, OEE, or a spaced-trials PREE. They do, however, show a massed-trials PREE and, with sufficient training, fish show patterned alternation (Gonzalez, 1972). The dissociation of the PREE and the continuous reward paradoxical effects (MREE, SNC, OEE) in the preweanling period also poses problems for Frustration Theory. One solution to the problem suggested by Bitterman (1975) for instrumental learning in nonmammalian species (e.g., fish and turtles) has been to make the distinction between the “massed-trials P E E ” reflecting reward-

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aftereffect mechanisms, and the “spaced-trials PREE, reflecting frustration mechanisms, and to attribute incentive-shift phenomena to “spaced-trial (i.e., frustration) mechanisms. Accordingly, a P E E - S N C dissociation in the 14- to 16-day age range may indicate the presence of sequential processes at this age and that the PREE obtained at this age is of the massed-trial variety and not dependent on frustrative processes. By this reasoning, the persistence we have demonstrated so far in rats 12-16 days of age is a sequential-processes PREE, and our failure to find SNC, the MREE, and the OEE in this age range is due to the absence of the required frustrative processes. There is another possible hypothesis to explain the apparent ontogenetic dissociation of S N C , the MREE, and OEE on the one hand, and the PREE on the other, within the context of frustration theory. It is that, while frustration may be conditioned in 14-day-old rats, its response-suppressive properties are weak. (See our earlier reference to the marginal presence of hippocampal theta and the corticosterone response at this age.) It would follow from such an hypothesis that phenomena requiring very great (paradoxical) suppression (SNC, MREE, and OEE) do not for this reason appear at this age. In the case of ?he PREE, however, where persistence requires the counterconditioning of $-SF to approach, the weaker response suppressive effects of TF-SF would not rule out and might even facilitate such counterconditioning. It is in this case a matter only of counterconditioning to weaker stimuli. ”

”

C. CONCLUDING COMMENTS As we pointed out earlier, the biopsychological study of paradoxical effects can bring together learning theory, brain physiology and neuroanatomy, and the phylogenetic and ontogenetic study of behavior. This article was an attempt to move in this direction. To paraphrase an earlier statement: We have begun to show that there is an ontogenetic level that appears to correspond to lower phylogenetic levels and perhaps even to a lower level of adult human functioning. At this level, learning, extinction, and other reactions to reinforcement change occur without benefit of goal anticipation (cognitive mediation). Our developmental work suggests that transitions between nonparadoxical and paradoxical effects of reward from one infant-rat age to another may be the ontogenetic counterpart of ( a ) the transition between the fish-turtle and birdmammal stages phylogenetically, and ( b )the transitions between, for example, masked and unmasked extinction effects in adult human eyeblink conditioning. Our review of the literature of brain function over the period of our developmental stages has shown that there are concurrent changes in brain neurophysiology and neuroanatomy, particularly in the limbic system-specifically in the moststudied structure, the hippocampus-which has been identified as an organ of

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inhibition. frustration, and anticipation (memory), all of which are involved in what we have called paradoxical functioning.

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ADVANCES

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M THE STUDY OF BEHAVIOR VOL.

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Ingestional Aversion Learning: Unique and General Processes' MICHAELDOMJAN DEPARTMENT OF PSYCHOLOGY UNIVERSITY OF TEXAS AT AUSTIN AUSTIN, TEXAS

I. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . ...... . .. . . . . . . . . .... A. Taste-Aversion Experiments and Expectations Based on Associative Interpretations . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . B. Aspects of Taste-Aversion Learning That Cannor Be Attributed to Sensitization Effects of Poisoning . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . C. The Role of Neophobia and Poison-Enhanced Neophobia in Ingestional Aversions . . , . . , , . . , . . . . . . . . . . , , . . . . . . . . . . . . . . . . , . , . . . . . . . . . . . 111. Poison-Avoidance Learning and the Complexity of the Ingestive Sequence . A . The Role of Ingestion in Taste-Aversion Learning. . . . . B. The Role of Ingestion in Odor-Aversion Learning . . . . . . . . . . . . . . . . . . . C. Learned Aversions to Nongustatory Orosensory Stimuli . . . . . . . . . . D. Ingestion as a Source of Stimuli That Mediate Conditioned Aversion Nongustatory Cues E. Ingestion as a Dete F. Ingestion and Poison-Avoidance Learning: Overvie .......... 11. The Associative-Nonassociative Controversy

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C. Proximal Unconditioned Stimulus Reexposure .

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Ingestional Aversion Learning , . . . . . . , , , . . . . . . . . . . . . . , . . . . . . . . . . . . . . .......... References . . . . . . . . . . .

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B. Interpretations of the Selective Association Effect . . . . .

'Preparation of this manuscript was supported by Grant MH 30788-01 (from the U . S . Public Health Service) and BNS 77-01552 (from the U.S. National Science Foundation). 215

Copyright 0 1980 by Academic Ress. Lnc. All nghrr of reproduction in any fonn reserved. ISBN 0-12-004511-7

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I.

INTRODUCTION

Poisons play an important role in the organization of plant and animal life. Although nonliving matter can be poisonous, many of the poisons that are of ecological importance are “secondary substances” synthesized by plants to govem their relationship to other plants and animals (Whittaker and Feeny, 1971). Certain of the higher plants, for example, synthesize poisons which inhibit the germination and growth of seeds of other plants which would otherwise provide competition for space and mineral resources. Others produce substances toxic to animals. Since plants are the basic food source for the animal kingdom, the presence of poisons in plants has provided evolutionary pressure for the development of mechanisms that protect animals against toxins, Some animals have evolved mechanisms for detoxifying certain poisons. Others sequester the poisonous substances so as not to experience the toxic effects. Detoxification and sequestration mechanisms provide animals with access to poisonous food avoided by other animals. In certain cases, the presence of a specific poison has even come to act as an attractant which guides animals with detoxifying or sequestering mechanisms to the poisonous plant (Whittaker and Feeny, 1971). Although sequestering poisons achieves some of the same effects as the detoxifying mechanisms, sequestration has the additional advantage of making the animals unpalatable to their predators. For example, monarch butterflies readily feed on milkweed containing cardiac glycoside poisons that do not affect them but are toxic to blue jays that feed on the monarchs (Brower et al., 1967). In addition to detoxification and sequestration mechanisms that protect animals from the effects of poisons, many animals have evolved a learning mechanism whereby they come to avoid eating substances that have made them sick on previous occasions. This learning mechanism of poison avoidance is potentially the most versatile of the three poison-protection mechanisms because it can provide a defense against just about any substance that produces postingestional malaise (Gamzu, 1977). Therefore, this mechanism is very important for omnivorous species, which select their diet from a wide variety of substances whose availability is constantly changing. Of the various defenses against poisoning, psychologists are most interested in this learning mechanism of poison avoidance. Current psychological research on poison-avoidance learning developed from several applied research programs started as a result of problems encountered during World War 11. Two of these programs involved attempts to develop effective rodent control techniques in the United States and the United Kingdom. In the course of this work it soon became apparent that rats avoided poisoned bait if they had previously experienced aversive postingestional effects after eating such bait (Richter, 1953; Rzoska, 1953). Thus, successful rodent population

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control through the use of poisoned foods requires poisoned bait that kills rats the first time it is eaten. A third research program involved investigating the behavioral effects of exposure to ionizing radiation. The results of greatest interest to psychologists were obtained with irradiation used as an unconditioned stimulus in a learning paradigm. Rats learned aversions to the taste of a relatively novel saccharin solution, for example, when ingestion of the saccharin was followed by exposure to y-radiation (Garcia et a / . , 1955). The two rodent control programs did not stimulate much systematic scholarly research on poison-avoidance behavior, although they formed the basis of a rather interesting agricultural application in which poison-avoidance behavior in mice was shown to be of potential benefit to farmers of Douglas fir in northern California (Tevis, 1956). Once Douglas fir is logged in certain areas of northern California, the region becomes invaded by tan oak because conditions are not favorable for the growth of conifers. Attempts to seed denuded areas with Douglas fir often failed because forest mice consumed the seeds. Extermination of the mice is not effective because nonpoisoned mice from neighboring areas quickly invade the exterminated territory. The problem can be solved, however, by adding a nonlethal poison to the Douglas fir seeds so that mice learn to avoid eating Douglas fir seeds without being killed or leaving the area (Tevis, 1956). In contrast to the rodent control programs, early demonstrations that rats acquire taste aversions as a result of exposure to ionizing radiation after experiencing the taste have stimulated much further research. This work was at first pursued primarily by John Garcia and his colleagues and later attracted the attention of James Smith, Paul Rozin, Marvin Nachman, Sam Revusky, and others. Through the efforts of these investigators and their intellectual descendents, the taste-aversion learning paradigm has become one of the most popular procedures for the investigation of learning (Barker e t a / . , 1977; Milgram e t a / . , 1977). A recent bibliography of reports relevant to this area listed 632 titles (Riley and Clarke, 1977). The current interest in taste-aversion learning developed in response to two landmark discoveries published in 1966. One of these (Garcia et a / . , 1966) involved the observation that rats will learn an aversion to a taste experienced before an aversive drug treatment or radiation exposure even if the interval between the taste and the consequent malaise is more than an hour. This phenomenon has come to be called the long-delay learning effect. The second major discovery (Garcia and Koelling, 1966) was that for rats taste stimuli are much more readily associated with toxicosis than are audiovisual cues, whereas audiovisual cues are much more readily associated with peripheral pain produced by footshock than are taste cues. This variation of the conditionability of tastes and audiovisual cues as a function of the use of toxicosis and footshock could not be attributed to differences in the salience or intensity of the individual events. Therefore, the experiment demonstrated that the strength of conditioning is

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greatly influenced by the combination of conditioned and unconditioned stimuli used. This phenomenon has come to be called the selective association or cueconsequence specificity effect. The long-delay learning and the cue-consequence specificity effects attracted a great deal of attention to the taste-aversion learning paradigm because they were unlike any other phenomena previously observed in conditioning laboratories. The reaction of some investigators to the uniqueness of these phenomena was to challenge interpretations of them as instances of associative learning (e.g., Bitterman, 1976; McLaurin, 1964; McLaurin and Scarborough, 1963). This approach to the long-delay learning and cue-consequence specificity effects makes it unnecessary to try to incorporate these findings into theories of learning. Another approach to the uniqueness of taste-aversion learning phenomena has been to use these effects to argue that previously formulated laws of learning are not generally applicable and that the pursuit of general laws of learning is an ill-fated venture (e.g., Hinde and Stevenson-Hinde, 1973; Rozin and Kalat, 1971; Seligman, 1970; Seligman and Hager, 1972; Shettleworth, 1972a). This approach contends that each instance of learning is best understood as an evolutionary adaptation to a particular challenge to survival and that learning mechanisms that evolve to deal with one such challenge may not necessarily have much in common with mechanisms that evolve to cope with other situations. The thesis of the present article is that neither of the above reactions to the findings of taste-aversion experiments is justified. Taste-aversion learning is indeed an associative process, and many aspects of it fail to challenge the existence of general laws of learning. Since there have been numerous detailed reviews of these issues in recent yeas (e.g., Logue, 1979; Revusky, 1977b; Spiker, 1977; Testa and Ternes, 1977), the present article will not attempt to be comprehensive. Rather, it will focus on several aspects of the research that my colleagues and I have conducted in the past decade that are relevant to these questions. Most of the experiments to be described were performed with laboratory rats. There is some reason to believe that the food selection behavior of rats is similar to that of other omnivores such as man (Rozin, 1976). However, it is unlikely that ingestional aversion learning in rats is representative of aversion learning in the feeding system of disparate animals such as insects and cephalopods.

II. THEASSOCIATIVE-NONASSOCIATIVE CONTROVERSY One of the recurring controversies involving research on ingestional aversions has been whether or not the enduring aversion to a taste which results from postingestional malaise following taste exposure represents an association between the flavor and the aversive postingestional event. The argument against an associative interpretation of ingestional aversions has taken three different forms.

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First, it was suggested that results of taste-aversion experiments do not conform to expectations based on an associative interpretation (McLaurin, 1964; McLaurin and Scarborough, 1963). Then, it was suggested that critical tasteaversion experiments failed to include important control groups to rule out nonassociative interpretations (Bitterman, 1975, 1976). Finally, it was suggested that certain nonassociative processes are activated by tastes and aversive interoceptive stimulation, and these processes may obscure evidence of the operation of associative mechanisms in the acquisition of ingestional aversions (Mitchell, 1978; Mitchell et al., 1977). I will discuss each of these criticisms in turn. A N D EXPECTATIONS BASEDON A. TASTE-AVERSION EXPERIMENTS ASSOCIATIVE INTERPRETATIONS

I . Early Experinierits Investigators of taste-aversion learning have been concerned from the beginning of this field of research with demonstrating the associative basis of ingestional aversion. In one of the early experiments, for example, Garcia and Kimeldorf (1957) investigated the importance for aversion learning of the temporal relationship between drinking saccharin and exposure to y-radiation. Four groups of rats were exposed to radiation for 4 hr, and a fifth group served as nonirradiated controls. The manipulation of interest was when a highly palatable saccharin solution was made available in relation to the radiation exposure. One group had the saccharin available for 2 hr just preceding the 4-hr exposure period. Other groups had the saccharin available during either the first or last 2 hr of irradiation, while the last irradiated group had saccharin available for 2 hr just after irradiation. These treatments are analogous to trace, simultaneous, and backward conditioning sequences often tested in classical conditioning (Kimble, 1961, pp. 47-48). Groups having the saccharin solution available during exposure to irradiation (simultaneous conditioning) learned stronger aversions to saccharin than subjects that had saccharin available just before irradiation (trace conditioning), although the trace conditioning group also learned an aversion to saccharin. In contrast, subjects having the saccharin solution available just after irradiation (backward conditioning) failed to learn a taste aversion. Garcia and Kimeldorf interpreted their results as demonstrating the role of associative mechanisms in aversion learning because the groups that received exposure to both saccharin and radiation did not all acquire equivalent aversions to saccharin. Rather, aversion learning required that the saccharin and radiation exposure occur in certain temporal arrangements. Simultaneous exposure to saccharin and radiation produced the strongest aversions, and no aversion was evident in subjects given saccharin to drink after radiation exposure. In contrast to Garcia and his colleagues, several other investigators expressed

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doubts about a learning interpretation of radiation-induced aversions. McLaurin and Scarborough (1963) pointed out that the trace conditioning procedures used by Garcia and his colleagues to condition taste aversions with ionizing radiation may have allowed delays between exposure to the taste and subsequent irradiation on the order of several minutes, delays which, on the basis of work in other learning preparations, would not be expected to support associative learning (Kimble, 1961, pp. 155-160). For example, in the Garcia and Kimeldorf (1957) experiment, subjects in the trace conditioning group received access to saccharin for 2 hr prior to irradiation. No data concerning temporal drinking patterns during the 2-hr period are presented. However, since subjects were water deprived, they probably drank to satiation long before the end of the 2-hr period, thus introducing a delay between taste and subsequent irradiation. Troubled by this possibility, McLaurin and Scarborough (1963) sought to determine the effects of various delays between exposure to a taste and subsequent irradiation. If taste aversions reflect an association between taste and radiation distress, then progressive delays between exposure to a taste and subsequent irradiation should result in progressive decrements in taste-aversion learning. McLaurin and Scarborough (1 963) assessed the saccharin aversion learning of rats exposed to X-irradiation 0, 25, or 50 min after a 10-min period of access to saccharin. Aversions were measured in saccharin-water preference tests conducted soon after conditioning. Contrary to predictions from a learning interpretation, progressive delays between exposure to saccharin and radiation did not weaken the taste aversions observed. Even the group exposed to radiation 50 min after drinking saccharin, an interval unprecedented for usual demonstrations of associative learning, acquired a strong aversion. McLaurin ( 1964) repeated the McLaurin-Scarborough experiment with groups of rats exposed to X-irradiation 3,60, 120, and 180 min after access to saccharin. The saccharin preference of subjects was tested immediately after irradiation. As in the previous experiment, all irradiated subjects acquired aversions to saccharin with no differences among the 60-, 120-, and 180-min delay groups. Introducing delays between the taste and X-irradiation again did not have the expected decremental effect on taste-aversion learning. Further evidence against a learning interpretation of the radiation-induced taste-aversion effect was obtained in a group that had not been given saccharin prior to X-irradiation but also evidenced an aversion to saccharin during the postirradiation test.

2.

Establishing the Delay Gradient

In contrast to the findings of McLaurin and Scarborough, numerous other investigators have found orderly decrements in taste-aversion learning as a function of the delay between access to a flavor and subsequent toxicosis. In the first such demonstration Garcia et a f . (1966) used apomorphine hydrochloride injections (7 mgkg, ip) as the US instead of X-irradiation and compared groups of

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rats injected with the toxin 30, 45, 75, 120, and 180 min after access to saccharin. Five conditioning trials were conducted, and subjects were tested for their response to saccharin 3 days after the last conditioning trial. Increasing the delay between access to saccharin and the apomorphine injections during conditioning attenuated the learning of saccharin aversions, and no aversions were learned in groups in which the apomorphine injections were delayed 120 or 180 min. The basic finding of Garcia et (11. (1966) that delays between taste and toxicosis result in orderly decrements in taste aversion learning have since been replicated by numerous other investigators (e.g., Kalat and Rozin, 1971; Nachman, 1970; Revusky, 1968; Smith and Roll, 1967; Wright er al., 1971). Furthermore, the difference in results between these experiments and the experiments of McLaurin and Scarborough cannot be explained in terms of the unconditioned stimulus used, since at least two of these studies also used X-irradiation (Revusky, 1968; Smith and Roll, 1967). The inconsistency between the experiments of McLaurin and Scarborough and the subsequent studies was resolved by a series of experiments that showed that rats can learn aversions to flavors experienced immediately after exposure to X-irradiation, presumably because the aversive effects of radiation last for a considerable time after radiation exposure (McLaurin et af., 1964; Morris and Smith, 1964; Scarborough et al., 1964; Smith et al., 1965; see also review by Smith, 1971). In the experiments of McLaurin and Scarborough all subjects were tested for saccharin aversions soon after exposure to X-irradiation. Thus, groups with various delays between taste and toxicosis, as well as subjects not given saccharin before irradiation, had equal opportunity to associate saccharin given during the postexposure test with the prolonged aversive aftereffects of irradiation. This aversion learning motivated by the aversive aftereffects of X rays was probably responsible for the lack of differences among groups. The other studies of the effects of delay between taste and toxicosis avoided this technical problem by testing for taste aversions at least 24 hr after toxicosis, by which time the aversive aftereffects of the irradiation or toxins used were probably no longer present. The finding that taste-aversion learning is a decreasing function of the interval between taste exposure and the aversive postingestional events is important evidence of the role of associative processes in ingestional aversion learning. Since all of the groups in a delay of reinforcement experiment have the same exposure to the CS flavor and the US malaise, the gradient of aversion learning observed cannot be attributed to the individual experience of these events. For example, in the first successful delay experiment (Garcia et al., 1966), the aversion learning observed in groups that had been injected with apomorphine 30, 45, or 7 0 min after taste exposure could not be attributed merely to previous exposure to saccharin and apomorphine because groups that were exposed to these two events separated by 120 and 180 min did not learn aversions. Rather, the pairing or opportunity to associate the flavor and malaise was necessary for aversion learn-

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ing. [A nonassociative interpretation of the delay gradient was recently proposed by Mitchell et a / . (1977). This possibility is discussed in Section II,C,3.]

3 . Other Similarities between Taste-Aversion and Other Types of Learning

McLaurin and Scarborough (1963) were concerned with just one characteristic of associative learning: that less learning is evident as the delay between the conditioned and unconditioned stimuli is increased. However, there are many other phenomena that are also commonly observed in cases of associative learning, and one might ask whether or not these relationships are likewise observed with taste-aversion learning. This evidence overwhelmingly favors an associative interpretation of aversion learning. The details of this argument have been presented elsewhere (Logue, 1979; Revusky, 1977b; Spiker, 1977; Testa and Temes, 1977). Briefly, the following phenomena observed in many instances of associative learning can be also observed in taste-aversion learning. Aversion learning is an increasing function of the intensity of the taste CS (e.g., Nowlis, 1974) and the drug or radiation US (e.g., Nachman and Ashe, 1973). The taste aversion is extinguished if subjects experience the flavor without aversive consequences after conditioning (Garcia et a l . , 1955). Repeated exposure to the flavor CS without aversive consequences before conditioning reduces the degree of aversion that is learned (e.g., Revusky and Bedarf, 1967), and preconditioning exposure to the unconditioned stimulus also interferes with subsequent aversion learning (see Randich and LoLordo, 1979, for a review). Aversions learned to one flavored solution generalize to other similar flavors (Nachman, 1963), and there is a gradient of generalization such that subjects conditioned to avoid one taste do not avoid all other novel flavors (Domjan, 1975; Nachman, 1963). Aversion learning to one taste is disrupted if during conditioning subjects are exposed to other stimuli that were previously conditioned with the aversive US (e.g., Gillan and Domjan, 1977; Willner, 1978), and aversion learning is also disrupted when the taste of interest is not the best predictor of malaise (Luongo, 1976). Phenomena such as conditioned inhibition and sensory preconditioning also do not differentiate taste-aversion learning from other types of learning (Best, 1975; Lavin, 1976; Taukulis and Revusky, 1975).

B. ASPECTSOF TASTE-AVERSION LEARNING THATCANNOT BE ATTRIBUTED TO SENSITIZATION EFFECTS OF POISONING The second type of criticism made against associative interpretations of ingestional aversion learning has been that many of the widely cited experiments in the field failed to include control groups to rule out sensitization effects of poisoning (Bitterman, 1975; Mitchell et a l . , 1977). According to this argument the taste aversions observed in these experiments may have reflected merely the fact that

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the subjects were previously poisoned and not the fact that the subjects associated the taste with the poisoning experience. There has been a great deal of discussion about whether or not certain experiments had proper control groups for sensitization effects (Bitterman, 1976; Garcia, 1978; Garcia et al., 1976; Mitchell, 1977; Revusky, 1977a, 1978; Smith, 1978). Regardless of what control groups were or were not included in these experiments, there are a number of aspects of ingestional aversion learning that are contrary to predictions of a sensitization interpretation. One widely accepted criterion for the identification of associative mechanisms is the demonstration of stimulus discrimination (Gormezano, 1966). In a discrimination procedure, one stimulus (the c s + ) is paired with the US on some trials, and another stimulus (the CS-) is presented without the US on other trials. Complete discrimination is said to exist if the conditioned response occurs in response to the CS+ but does not occur in response to the CS- . If taste aversions develop through nonassociative mechanisms, equal aversions would be expected in response to both the CS+ and CS- flavors. However, this is not what is observed. Discrimination procedures typically yield differential aversions in the taste-aversion paradigm (e.g., Gillan and Domjan, 1977; Rozin, 1969). Another finding contrary to a sensitization interpretation is that animals that have one flavored solution paired with toxicosis do not subsequently avoid all other novel flavors (e.g., Domjan, 1975; Nachman, 1963). If the taste aversions were only a response to prior toxicosis, the aversions would not be specific to the flavor that was paired with toxicosis. There is some evidence that animals that learn an aversion to one novel fluid may subsequently avoid other very different novel flavors ( e . g . , Best and Batson, 1977). However, these observations also appear to be mediated by associative mechanisms because the nonspecific avoidance of novel flavors is attenuated by extinction of the aversion to the drug-paired taste (Best and Batson, 1977). It appears that if animals learn an aversion to one novel flavor, this conditioned aversion may generalize to other flavors along the dimension of flavor novelty. If ingestional aversions were due to nonassociative effects of poisoning, then animals that are exposed only to the toxin US or to the US unpaired with a flavor CS should evidence as strong aversions to a novel flavor later as animals that are treated with the aversive US after drinking the flavored solution. Such control groups have been included in many experiments, and the outcome is never as predicted by sensitization. Poison injections unpaired with a novel taste rarely suppress the intake of novel solutions during tests conducted 1 day or more later (e.g., Domjan, 1975; Mitchell er al., 1977; Monroe and Barker, 1979). When such a suppression is observed, it is transitory and disappears as subjects recover their baseline water intake levels from the toxicosis (Best and Batson, 1977; Carroll et al., 1975). Another line of investigation that fails to substantiate claims that enduring

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flavor aversions result from mere exposure to the toxin US concerns the effects of repeated exposure to the toxin US prior to taste-aversion conditioning. If exposure to the toxin US alone produces an enduring suppression in the intake of novel solutions, then subjects that receive repeated exposure to the toxin US before conditioning should be suppressed in their intake of the CS flavor during the conditioning trial. However, such suppressions are typically not observed (e.g., Braveman, 1975a; Cannon etal., 1975; Goudie etal., 1975a; Revusky et a / . , 1976). A related set of evidence is provided by experiments in which subjects receive exposure to the toxin US shortly (within several hours) before the usual pairing of the flavor CS with a consequent toxin US. Such a proximal US preexposure treatment increases the total toxicosis subjects experience on the aversion conditioning day. Therefore, if ingestional aversions reflected the nonassociative effects of toxicosis, then proximal US preexposure would be expected to facilitate aversion performance. However, contrary to this prediction, proximal US preexposure has been found to disrupt taste-aversion conditioning (Best and Domjan, 1979; Domjan, 1978; Domjan and Best, 1977).

C. THEROLEOF NEOPHOBIA AND POISON-ENHANCED NEOPHOBIA IN INGESTIONAL AVERSIONS The third type of criticism against associative interpretations of ingestional aversion learning is that evidence of associative mechanisms has been obscured by the possible occurrence of taste neophobia and poison-enhanced neophobia in taste-aversion experiments (Mitchell et al., 1975, 1977). Animals typically ingest very little of novel substances, and under certain circumstances this flavor neophobia can be increased by a prior poisoning experience (see Corey, 1978; Domjan, 1977a, for reviews). Therefore, the avoidance of novel solutions after a taste-toxicosis conditioning trial may in part reflect nonassociative neophobia and enhanced neophobia processes. One possible approach to determining the role of flavor neophobia and enhanced neophobia in ingestional aversion learning is to test control groups that would permit evaluation of the contribution of these processes. However, given the unending disputes that exist concerning the adequacy of various control procedures (Bitterman, 1975, 1976; Garcia, 1978; Garcia et al., 1976; Mitchell, 1977, 1978; Revusky, 1977a, 1978; Smith, 19781, it is unlikely that any set of control procedures would satisfy all investigators. Another, perhaps more fruitful, approach to this problem is to investigate the circumstances in which flavor neophobia and enhanced neophobia phenomena are prominent. Once these situations have been identified, it becomes much easier to decide whether or not particular taste-aversion conditioning procedures are likely to permit the flavor neophobia and enhanced neophobia to occur.

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I . Flavor Neophobia The degree of aversion or neophobia nonpoisoned subjects display to a novel solution no doubt depends on its taste. Some tastes are simply more distinctive from the animal’s customary diet than other flavors and will therefore evoke a greater aversion when first presented. It is difficult to quantify or manipulate distinctiveness. However, the concentration of flavored solutions usually covaries with novelty. For animals raised on ordinary laboratory chow and tap water, increasing concentrations of a solution will be increasingly distinctive from their customary fluid and will therefore evoke greater neophobia. The relationship between taste concentration and neophobia is illustrated by one of our experiments with aqueous solutions of saccharin (Domjan and Gillan, 1976). Laboratory rats were first adapted to a daily 23.5-hr deprivation schedule. They then received access to a saccharin solution for 30 min each day. This saccharin drinking period was always followed by access to water for 30 min so that the animals could satisfy their daily fluid needs even if they chose to drink very little saccharin. Each group of rats was tested with a different concentration of saccharin. Figure 1 shows the amount of saccharin each group drank during the daily test sessions. Subjects initially showed strong aversions to the 0.5, 1.0, 2.0,and 3.0% saccharin solutions. In contrast, the animals drank substantial amounts of the 0.15% saccharin from the first day. The initial aversions that were evident with the concentrated saccharin solutions were no doubt in part a response to

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FIG. 1 . Amount ingested by independent groups of rats given access to 0.15,0.5, 1 .O, 2.0, and 3.0%saccharin for 30 min daily. The saccharin drinking period was always followed by access to water for 30 min. Water intakes are not shown. Redrawn from Domjan and Gillan (1976).

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their novelty; subjects increased their intakes as they were repeatedly tested and received exposure to the flavors. The smallest increase in consumption with repeated testing occurred with the 0.15% saccharin solution, indicating that this solution initially elicited very little neophobia. The intakes of 0.5 and 1.0% saccharin eventually matched the intake of 0.15% saccharin. However, the intakes of the 2.0 and 3.0% solutions never reached this level. The difference in the asymptotic levels of drinking achieved with these solutions may be interpreted as indicating that the response to the 2.0and 3.0% solutions was not completely determined by their novelty. Results such as those presented in Fig. 1 suggest that complications arising from flavor neophobia can be minimized in taste-aversion experiments by using weak taste solutions that elicit minimal neophobia (Smith, 1978). This has been the common practice. Probably more experiments have been performed with 0.1 and 0.15% saccharin than with any other solution (see Riley and Clarke, 1977, for a bibliography).

2 . Poison-Enhanced Neophobia Even more important than the role of neophobia in taste-aversion conditioning experiments is the possible contribution of poison-enhanced neophobia. That is, the aversion that subjects display after a taste-conditioning trial may not be due to the association of the taste with the toxicosis but may reflect a nonspecific increase in their aversion to novel tastes caused by the poisoning experience. Such an interpretation is not applicable to many taste-aversion experiments because of the reasons listed in Section II,A, 2. A detailed study of the circumstances that lead to poison-enhanced neophobia also makes this interpretation untenable for many experiments (see Domjan, 1977a, for a review). There is no doubt that animals poisoned after exposure to one novel taste subsequently avoid a variety of other novel flavors. This phenomenon has been well known to rodent control professionals for a long time and was one of the findings of early research on poison-avoidance learning (Richter, 1953; Rzoska, 1953).Recent research indicates that there are two mechanisms that contribute to this phenomenon. One of these does not involve an association between taste and poisoning (Domjan, 1977b) and the other mechanism requires the integrity of such associations (Best and Batson, 1977; Domjan, 1975). a. Nonassociative Mechanisms of Poison-EnhancedNeophobia. If subjects are tested before they have fully recovered from the effects of toxicosis, their flavor neophobia will be increased (Domjan, 1977b). In one of our experiments that illustrates this phenomenon, Sprague-Dawley rats were first adapted to a daily 23.5-hrwater deprivation schedule. Independent groups of subjects then received drinking tests with a 0.5% saccharin solution and water starting 30 min after the injection of 0-3.0 meqkg lithium chloride. The water and saccharin tests were conducted 6 days apart in a counterbalanced order.

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The amount of each solution subjects drank during the 60-min drinking tests is shown in Fig. 2. Generally, subjects consumed more water than saccharin, and increasing doses of lithium did not produce progressive decrements in water intake. However, a dose-related suppression in the intake of the saccharin solution occurred. We have found such a suppression in the intake of all novel solutions we tested (various concentrations of saccharin, 3% vinegar, and 5% casein hydrolyzate) whenever the drinking test was conducted shortly after the toxin injection. However, we did not find such a suppression of drinking with highly familiar solutions. Subjects reared with access to tap water, saccharin, or vinegar did not suppress their intake of these solutions in test sessions conducted shortly after the injection of less than 3.0 meq/kg lithium (Domjan, 3977b). It is quite likely that complete suppression of all ingestive behavior would occur with higher drug doses. The suppression of intake illustrated in Fig. 2 is not only specific to novelflavored solutions but is also limited to a relatively short period after drug treatment. In another of our experiments (Domjan, 1977b), independent groups of rats were given a 60-min drinking test with a novel 1 .O% solution of saccharin starting 10 to 120 min after the injection of 1.8 meq/kg lithium. The control group received injections of physiological saline. The amount of saccharin each group drank during these test sessions is displayed in Fig. 3. Progressively less suppression of drinking occurred with subjects whose drinking test was delayed longer after the drug injection. In fact, the intakes of subjects tested 90 and 120 min after drug treatment were not significantly less than the intakes of the control 2 5-

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group. Thus, the enhanced neophobia reaction was not an enduring response to the toxin drug treatment but dissipated quickly as the animals were allowed to recover from the toxicosis. Other investigators who used more severe deprivation schedules than what we typically employ observed enhanced neophobia reactions 24 and 48 hr after toxicosis treatment (Best and Batson, 1977; Carroll et al., 1975). However, even in these cases the enhanced neophobia response decayed if sufficient time passed to allow the baseline water intakes of the subjects to recover from the effects of the toxin. The transient nature of the enhanced neophobia effects that are observed as a direct result of toxicosis make it difficult to attribute enduring conditioned aversions to the same nonassociative mechanisms. Conditioned taste aversions are evident many days after the toxin administration. In one experiment, for example, conditioned aversions were observed in subjects tested 90 days after the taste-toxin pairing (Dragoin et af., 1973). b . Associative Mechanisms in Poison-Enhanced Neophobia. In certain circumstances, a poisoning experience can result in a lasting avoidance of novel flavored solutions that have not been paired with the toxicosis. In one of our experiments on this phenomenon, we found that animals that are first conditioned to avoid a weak saccharin solution subsequently also avoid a solution of casein hydrolyzate (Domjan, 1975). This is an example of enhanced neophobia because the generalized avoidance response occurs only if the casein solution is novel. However, the enhanced neophobia is not a direct effect of poisoning but is rather mediated by the aversion which subjects first learn to the saccharin solution. The casein aversion is evident only as long as subjects retain their conditioned aversion to saccharin. This important aspect of the phenomenon is illustrated in Fig. 4.

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All of the animals that provided data for Fig. 4 were first conditioned to avoid saccharin. However, before being tested for their intake of a novel casein solution, half of the subjects were given extensive access to saccharin in the absence of toxicosis. Figure 4 shows that this extinction procedure was effective in reducing the aversion that subjects had to the saccharin flavor. However, the extinction procedure for saccharin also substantially reduced the subjects' avoidance of the casein solution. Even though the extinction and control groups had the identical prior experience with toxicosis, only the control group evidenced enhanced neophobia for casein. This outcome, as well as the fact that an enhanced neophobia for casein is not observed if the prior toxicosis is not paired with exposure to saccharin, suggests that the enhanced neophobia effect is mediated by associative mechanisms. In our experiments on the associative poison-enhanced neophobia phenomenon, we did not find increased avoidance of all novel solutions following the pairing of a specific taste with toxicosis. For example, animals that had toxicosis paired with saccharin rarely if ever, showed increased avoidance of a novel vinegar solution. In a related series of experiments, Best and Batson (1977) found that animals that received access to a coffee solution paired with toxicosis subsequently showed enhanced neophobia to the taste of vinegar and the taste of casein. Based on these results, Best and Batson suggested that a conditioned aversion to one solution may generalize to other flavors along a dimension of novelty. However, their results are also an example of the associative poisonenhanced neophobia effect because the enhanced neophobia to vinegar and casein was not evident if the subjects' conditioned aversions to the coffee flavor were extinguished. The results of the experiments by Domjan (1975) and Best and Batson ( 1 977) are important because they indicate that associative mechanisms can be involved in enhanced neophobia effects. Therefore, one must not dismiss the possible SACCHARIN TEST

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FIG. 4. Saccharin and casein consumption of animals that initially had the taste of saccharin paired with lithium. Following the saccharin conditioning, the extinction group received extensive access to saccharin in the absence of toxicosis whereas the control group did not. From Domjan (1975).

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involvement of associative mechanisms merely because enhanced neophobia is observed after poisoning experiences. More sophisticated tests procedures are required before such a conclusion can be reached.

3 , Interruption of the Attenuation of Neophobia: A Nonassociative Explanation of the Delay Gradient in Taste-Aversion Learning Mitchell et al. (1977) recently suggested another nonassociative role of poisoning in taste-aversion experiments, the interruption of the attenuation of neophobia. The avoidance of novel flavored solutions is reduced as subjects have increasing exposure to the flavor (e.g., Domjan, 1976). However, the attenuation of flavor neophobia is also a function of the passage of time without aversive consequences following a taste exposure. Evidence of this is provided by experiments in which animals are exposed to a flavored solution on two occasions, with the interval between these two presentations systematically varied. Subjects drink more during the second exposure to the solution as a direct function of the interval between the two presentations (Nachman and Jones, 1974). This increased intake as a function of the passage of time is not attributable to increased thirst and is prominent only with novel-flavored solutions (Nachman and Jones, 1974). Therefore, the phenomenon appears to reflect the gradual loss of neophobia as a function of time after the first exposure to the taste solution. The attenuation of neophobia that occurs with the passage of time can be interrupted by the introduction of another novel taste (Green and Parker, 1975). Based on this observation, and related results from the study of other response systems, Mitchell et al. (1977) suggested that the administration of the toxin US in taste-aversion experiments may also interrupt the attenuation of neophobia that occurs after the taste presentation. In a delay of reinforcement experiment, this interruption would occur later in the process of the attenuation of neophobia for groups that receive longer delays between exposure to the taste and administration of the toxin. Mitchell et al. suggest that subjects that are conditioned with a long CS-US interval may drink more of the taste solution during later test sessions because the US was administered for them after they had already experienced a substantial loss of neophobia. Thus, this interruption by the US of the attenuation of neophobia which occurs with time predicts that a gradient of intake will be observed as a function of the CS-US interval during later tests with the flavor CS. The reinterpretation of the delay gradient offered by Mitchell et al. is rather interesting and creative. However, it would be difficult-perhaps impossible-to prove that an example of a flavor aversion was a result of the interruption by the US of the attenuation of neophobia. All of the results of such a mechanism could equally well be attributed to a weak association between the taste and the US. For example, the interruption hypothesis predicts a delay gradient as a function of the CS-US interval, which is exactly what is predicted by associative mechanisms.

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The interruption mechanism also predicts that the aversion resulting from the interruption of neophobia loss will be specific to the flavor that was followed by the toxin US. An associative interpretation also makes this prediction. The interruption hypothesis predicts more of an aversion following a CS-US trial with stronger flavor CSs because such CSs elicit more neophobia. The same prediction is derived from associative accounts because stronger associations between CS and US are predicted with more intense CSs. The interruption hypothesis predicts stronger aversions with more intense USs because such USs can presumably better disrupt the attenuation of neophobia. Associative mechanisms can also explain this result because stronger associations occur with more intense uss. Although all of the predictions of the interruption hypothesis can also be explained by associative mechanisms, this does not mean that the two processes are indistinguishable. There are some predictions of associative mechanisms that cannot be explained by the interruption hypothesis. The most important and obvious of these is that the interruption hypothesis does not predict taste aversions that are stronger than the initial reaction of an animal to an edible substance. If the attenuation of neophobia is interrupted, then the subjects will respond to a flavored solution as they did on their first encounter. In contrast, the associative hypothesis predicts that as a result of the pairing of a flavor with a toxin it should be possible to produce stronger aversions than what are evident the first time an animal ingests the flavored solution. This is in fact the case in the preponderance of experiments on taste-aversion learning (e.g., Garcia et a l . , 1966) and is also observed in delay experiments in which the toxin US is administered 30 min or more after taste exposure (e.g., Garcia et nl., 1972; Nachman, 1970; Rozin, 1969; Wright et a l . , 1971). The interruption hypothesis also cannot explain cases in which subjects drink less of a flavored solution after the CS-US pairing than do animals that did not have previous exposure to the CS flavor (e.g., Carroll el al., 1975). 4 . Role of Nonassociative Mechaiiisms in Ingesrional Aversions: Overview

There is no doubt that omnivores suppress their intake of novel flavored substances and that this neophobia can be aggravated by poisoning experiences (Domjan, 1977a). However, these facts do not necessarily imply that ingestional aversions are governed by nonassociative mechanisms. The various arguments presented also do not prove that ingestional aversions are always the result of associations between novel flavors and toxicosis. Rather, ingestional aversions appear to be a joint function of both nonassociative and associative processes. In some situations one type of mechanism predominates, in other cases the other processes predominate, and in still other instances both types of mechanisms may contribute to the observed results. We now know enough about the mechanisms

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of neophobia and poison-enhanced neophobia to examine the circumstances in which a particular ingestional aversion is observed and make an educated judgment about the possible involvement of nonassociative processes. If a highly unfamiliar taste solution is used and the aversion is measured before the subjects have fully recovered from the toxicosis, then it is highly likely that the aversion will have a large nonassociative component. In contrast, if a low concentration palatable solution serves as the CS and subjects show a profound aversion long after they have recovered from toxicosis, it is unlikely that nonassociative processes will be involved. Obviously, appropriate control groups will also help in making these decisions.

III. POISON-AVOIDANCE LEARNING A N D THE COMPLEXITY OF THE INGESTIVE SEQUENCE Because animals that suffer some type of malaise after ingesting a novelflavored substance quickly learn a profound aversion specific to the flavor of what they ate, it is tempting to think about this phenomenon as involving only the taste stimulus and the aversive postingestional event. Such an analysis of the taste-aversion paradigm follows the model of Pavlovian conditioning and is analogous to the analysis of other simple conditioning situations such as Pavlovian salivary conditioning (Pavlov, 1927) and fear conditioning (Kamin, 1965). However, closer examination of the typical taste-aversion conditioning situation reveals that in addition to having toxicosis follow exposure to a taste, the subjects also approach and orient toward the source of the ingestible material, take the material in their mouths, manipulate it with the tongue, and swallow it. The tactile and orosensory stimulation involved in this consummatory sequence may also have an important role in ingestional-aversion learning. The ingestion also occurs in a specific location and in the presence of specific olfactory cues, and these stimuli may be likewise involved in the aversion that is learned. A. THEROLEOF INGESTION IN TASTE-AVERSION LEARNING In the typical taste-aversion conditioning procedure subjects receive exposure to the taste CS by ingesting a flavored solution or food. Investigation of the importance of ingestion in aversion conditioning requires exposing subjects to the flavor CS in ways that either do not require ingestive behaviors or that require modified modes of ingestion. We chose the first of these approaches and studied how rats learned aversions when they were exposed to the flavor CS during conditioning in a passive manner not involving ingestive behaviors. Learning under these circumstances was then compared to the aversion learning that results

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from toxicosis following the ingestion of the flavored CS solution in the typical manner. In our first experiment (Domjan and Wilson, 1972a, Experiment 1) passive exposure to the flavor CS during conditioning was achieved by paralyzing the subjects with curare and rinsing the taste solution over the tongue before the injection of lithium chloride. The animals were then tested for their saccharin preference after complete recovery from both the paralysis and the lithium. We found that subjects conditioned under the influence of curare learned much weaker aversions to saccharin than animals that were allowed to drink the saccharin solution in the customary manner before toxicosis. Thus, the absence of ingestive behaviors during conditioning was accompanied by attenuation of taste-aversion learning. However, these results are somewhat difficult to interpret because curare paralysis is a multifaceted treatment. The results of our curare experiment were confirmed in a second study which involved less drastic procedures to achieve passive taste exposure than the curarization technique (Domjan and Wilson, 1972a, Experiment 2). In this experiment all of the subjects had a cheek cannula inserted which allowed infusion of the taste solution directly into the oral cavity. Instead of being paralyzed, the animals remained in the normal state and were held manually during the taste presentations. By varying the rate of infusion of the flavored solution and the state of thirst of the animals, we could manipulate the extent to which they swallowed the infused fluid. The taste presentation lasted for 2 min for all subjects. The amount animals swallowed, and the percentage of the 2-min taste presentation during which they were observed to make drinking jaw movements, are summarized in Fig. 5 for the various groups. The animals were first adapted to drinking their entire daily fluid requirements in a 25-min period of access to water each day. On the conditioning day, Group WF-Li was first allowed access to water for 25 min so that it would not be thirsty. To discourage Group WF-Li further from swallowing the saccharin solution during conditioning, the taste fluid was infused into the oral cavity at a very high rate (46m l h i n ) . Twenty-five minutes after the end of the taste presentation the subjects were injected with lithium. Figure 5 shows that the method of taste exposure for Group WF-Li was highly effective in minimizing ingestion of the saccharin CS. The subjects swallowed a negligible amount and were seldom observed making ingestive jaw movements. Group DF-Li received the same rapid oral infusion of saccharin during conditioning as Group WF-Li except that for these animals the saccharin exposure was conducted while they were water deprived. The higher level of thirst in this group resulted in their drinking considerably more of the saccharin solution than had Group WF-Li. Group DS-Li received a slow (3 ml/min) oral infusion of saccharin while water deprived, and Group FI was allowed to ingest the saccharin solution freely from a

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drinking tube for 2 min during the conditioning trial. These last two groups drank the greatest amount of the flavor CS. All of the water deprived groups (DF-Li, DS-Li, and n)were allowed to drink water for 25 min after the taste exposure so that their level of hydration would match that of Group WF-Li when the lithium was administered 25 min later. On the first and second days after the conditioning trial, each subject received a preference test in which the saccharin solution and tap water were simultaneously available for 30 min. The results of these test sessions are summarized in Fig. 6. All of the groups that had ingested considerable amounts of saccharin during the conditioning trial (Groups DF-Li, DS-Li, and Fl) subsequently showed strong aversions to the saccharin flavor. In contrast, subjects that had not swallowed the flavor CS during conditioning (Group WF-Li) had substantially higher preferences for the saccharin taste. In fact, the saccharin preferences of these subjects were very similar to the preferences of animals that had been conditioned while paralyzed with curare in the previous experiment. These results confirm that aversion learning is attenuated if subjects do not engage in the various mastication movements that are normally involved in ingestion.

FIG.5 . Amount of 0.2% saccharin ingested and percentage of time animals were observed drinking under various taste presentation procedures. Group WF-Li was not water deprived and received a fast oral infusion of saccharin. Groups DF-Li and DS-Li were water deprived and received a fast and a slow oral infusion of saccharin, respectively. Group FI was water deprived and was allowed to drink the saccharin from a drinking tube. From Domjan and Wilson (1972a).

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FIG. 6 . Saccharin preference of independent groups of rats injected with lithium chloride following the various taste presentation procedures depicted in Fig. 5. Group Na was not injected with the drug and indicates response to saccharin in the absence of aversion conditioning. From Domjan and Wilson (1972a).

The reduced taste aversion performance observed in animals that received passive exposure to the taste before toxicosis may reflect an attention decrement. Perhaps subjects that do not ingest a flavored solution pay less attention to its taste. The attenuated aversion performance can also be explained in terms of a stimulus generalization decrement from conditioning to testing. The test procedure for all subjects in the above experiments involved ingestion. Perhaps flavored solutions have different sensory properties when they are ingested as compared to when the solution is passed over the tongue in the absence of ingestive behaviors. Such a difference may have contributed to the weaker aversions of subjects that were conditioned in the absence of ingestion. This possibility could be evaluated by devising a test of taste-aversion learning which also does not involve having the subject drink the CS flavor. If stimulus generalization decrements occur between ingestion and no-ingestion situations, ingestionconditioned rats should evidence weaker aversions in tests that d o not involve eating and drinking than animals conditioned with passive taste exposure. Our subsequent experiments were motivated by these ideas. Although noningestion tests of flavor-aversion learning could be devised, our approach was to investigate these issues by conditioning aversions to olfactory stimuli with toxicosis. It seemed to us easier and more direct to devise odor-aversion test procedures that d o not involve ingestion.

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THEROLEOF INGESTION

IN

ODOR-AVERSION LEARNING

Animals that experience toxicosis after exposure to a novel odor can learn an aversion to the odor as a result (e.g., Garcia and Koelling, 1967; Lorden et al., 1970). We created an ingestion context for this odor-aversion learning by allowing animals to drink water in the presence of the CS odor (Domjan, 1973). However, we wanted to make sure that proximity to the drinking spout would not also bring the animals closer to the source of the odor. Therefore, odor exposure was accomplished during conditioning by placing the animals in plastic pails with tightly fitted lids, with the CS odor provided by spreading Mentholatum cream on the inside surface of the lids. The drinking spout was inserted about 5 cm above the floor of the pails when it was needed. The standard conditioning procedure involved placing the subjects in the odor-exposure chambers for 7 min, injecting them with lithium, and returning them to the home cage. This procedure resulted in the suppression of drinking in the presence of the CS odor during subsequent test sessions (Domjan, 1973). The drinking suppression was due to an association between the CS odor and the aversive effects of lithium because the aversion was not observed if subjects were tested in the absence of the odor or if they were injected with lithium in the absence of the odor and later tested with the odor present (Domjan, 1973). In some ways the effects of ingestion on odor-aversion learning (Domjan, 1973) were very similar to the effects of ingestion on taste-aversion learning described in the previous section. Animals that were allowed to drink water during the odor-conditioning trial evidenced much greater suppression of water intake during later test sessions in the presence of the CS odor than animals that were not given the opportunity to ingest anything during conditioning. Thus, ingestion facilitated odor-aversion learning, just as it facilitated taste-aversion learning in the earlier experiments. Because evidence of aversion learning was inferred from the suppression of water intake, one might be tempted to conclude that the enhanced aversions of animals that also drank water during conditioning reflected a learned aversion to water. However, there is no evidence for this possibility because animals that were allowed to drink water during odoraversion conditioning subsequently drank just as much water in the absence of the CS odor as subjects that received odor-aversion conditioning without ingestion (Domjan, 1973, Experiment 2). In an effort to specify better the test conditions in which the facilitative effects of ingestion on odor-aversion learning are evident, we constructed a special odor-testing chamber. A top view of this apparatus is provided in Fig. 7. Subjects were placed in area A and could explore compartments B and C when the guillotine doors D and E leading to these compartments were raised. Compartment B was odorized with Mentholatum. Using this test apparatus, we could assess the strength of an odor aversion in both ingestion and noningestion contexts. For ingestion tests, drinking spouts were inserted into compartments B and

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c=

A

I.

c!

FIG.7 . Top view of odor-choice test apparatus. Arrows indicate exhaust fans; see text for further details. From Domjan (1973). C at points F and G, and the response to the CS odor was inferred from how much animals drank from the fluid available in compartment B in comparison to the total fluid intake in both compartments. For noningestion tests, the two test compartments were both empty and the amount of time subjects spent exploring compartment B was measured as a percentage of the total time spent in exploration of both compartments. In one of our experiments using the special odor test apparatus, we compared the odor-aversion performance of three groups of subjects (Domjan, 1973, Experiment 4). During conditioning, Group Ingestion was allowed to drink water in the presence of the odor of Mentholatum before being injected with lithium chloride. Group No-Ingestion was exposed to the CS odor in the absence of fluids before the toxin injection, and subjects in Group Control received either ingestion or no-ingestion exposure to the CS odor followed by treatment with physiological saline. The aversion performance of these three groups was then assessed using three test procedures. In one of the tests, no fluids were available in the odor test apparatus, and the percentage of time subjects spent exploring the odorized compartment was measured. In another test session, a highly familiar 0.2% saccharin solution was available in both compartments of the test chamber and the percentage of intake in the odorized compartment was measured. In the third type of test session, access to tap water was made available in each test compartment.

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FIG. 8. Mean percentage preference for the conditioned stimulus odor for independent groups that during conditioning received exposure to the CS odor in the presence of access to tap water (ingestion) or without water (no-ingestion). Control subjects were not injected with lithium during conditioning. The animals were tested for their odor preference in the absence of edibles, and with access to saccharin (SACC) or water in the odor-choice apparatus. For the test without fluids, the numbers above the bars indicate mean total seconds spent exploring both test compartments. For the tests with saccharin and water, the numbers indicate mean total milliliters ingested in the test compartments. From Domjan (1973).

Preference for the Mentholaturn odor as measured by exploration, saccharin intake, and water intake is summarized in Fig. 8. During the exploration test without fluids, both the Ingestion and the No-Ingestion poisoned groups evidenced an aversion to the CS odor in comparison to the control subjects. However, the aversion performance in this test session was not facilitated by ingestion during conditioning. Similar results were obtained in the test session with saccharin available in the test compartments. Again both poisoned groups evidenced an aversion to the Mentholatum odor in comparison to controls, but there was no significant difference between the Ingestion and No-Ingestion groups. The facilitatory effect of ingestion during conditioningwas evident only when subjects

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were tested for their preference for drinking water in the presence of the CS odor. In this case Group Ingestion displayed significantly lower odor preferences than Group No-Ingestion. The results displayed in Fig. 8 confirm that ingestion during conditioning can facilitate odor aversion performance and help to specify the test conditions in which this effect is evident. The fact that enhanced aversions were not observed when subjects were tested for their preference to drink saccharin in the presence of the CS odor indicates that drinking measures of odor preference are not sufficient for observation of the phenomenon. Ingestion was necessary for the enhanced aversions to occur, since Groups Ingestion and No-Ingestion performed comparably in the exploration test. However, the nature of the ingested fluid was also important. More specifically, subjects had to be tested with the same drinking fluid that they drank during the conditioning exposure to the CS odor. As was noted above, the enhanced odor aversions of Group Ingestion could not be attributed to a learned aversion to the taste of water. Why is it, then, that the enhanced aversions were only evident in water-drinking measures of odor preference? An answer is suggested by analysis of the various stimuli that animals experienced when they drank water in the presence of the CS odor. The sensory experience of animals in Group Ingestion during conditioning can be conceptualized as consisting of three components: the CS odor, the taste of water, and a configural stimulus consisting of taste and odor. Our suggestion is that animals in Group Ingestion learned an aversion to both the odor component and the odor-taste configural stimulus (Domjan, 1973). Presumably the odortaste configuration becomes altered when subjects are tested with a taste that is different from what they experience during the conditioning trial. Therefore, the aversions manifest by Group Ingestion in the tests without fluids and with saccharin reflected only their conditioned aversions to the odor stimulus. In contrast, the aversions manifest in the water-drinking test also reflected a conditioned aversion to the odor-taste configural stimulus. This enhanced aversion was not evident with Group No-Ingestion because for these subjects the odor-water configuration had not been paired with poisoning during the conditioning trial. The present analysis of the effects of ingestion on odor-aversion learning in terms of the conditioning of configural stimuli that result from the ingestion context can be extended to the effects of ingestion on taste-aversion learning. Ingestion may also promote the perception of a configural stimulus in tasteaversion experiments. However, it is not entirely clear what the components of this configuration are. Nongustatory orosensory stimulation (the tactile sensations of the food in the mouth, for example) may constitute one of the components, and the taste of the ingested material may provide another component. Animals in the usual taste-aversion experiment may learn an aversion not only to the taste of what they ingest but also to the configuration created by taste and the

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orosensory stimulation involved in eating. Changing these orosensory stimuli would then result in weaker aversions. Such a mechanism could explain the attenuated aversions observed in animals tested for their preference for saccharin after they had passive exposure to this flavor paired with toxicosis (Domjan and Wilson, 1972a). C.

AVERSIONS TO NONGUSTATORY OROSENSORY LEARNED STIMULI

Experiments in which different methods of taste presentation are compared (e.g., Domjan and Wilson, 1972a) indicate that alteration of the orosensory stimuli normally involved in mastication and swallowing can modify tasteaversion performance. More direct evidence of the involvement of orosensory stimuli in ingestional aversion learning is provided by experiments in which different orosensory stimuli rather than different taste cues signal the presence or absenc.: of toxicosis. In one such experiment (Nachman, 1970), animals were adapted to drinking room temperature distilled water (27'C) for 10 min each day. During the conditioning trial, the distilled water was warmed to 43"C, and independent groups were injected with lithium chloride at various intervals after drinking the warm water. Subsequent drinking tests with the warm water indicated that the animals learned an aversion to this orosensory stimulus if the toxicosis was induced within 15 min after the first exposure to the warm water. Aversions have also been conditioned to the orosensory stimuli involved in drinking distilled water from a small-diameter drinking spout as compared to a large-diameter spout (Nachman et al., 1977). D.

INGESTION AS A SOURCE OF STIMULI THATMEDIATE CONDITIONED AVERSIONSTO NONGUSTATORY CUES

Animals typically experience a rich array of stimuli in the course of ingestion, including the taste, olfactory, and tactile properties of the edible, the orosensory stimuli involved in mastication and swallowing, and the visual, auditory, and spatial context in which the eating takes place. There is some evidence that in certain situations the taste stimuli encountered during ingestion may facilitate the association of nongustatory cues with toxicosis. In one of the first experiments of this type, Morrison and Collyer (1974) initially trained rats to press a response lever for water reward in a dark experimental chamber. On conditioning days the experimental chamber was illuminated by a 15-W light. One group of animals continued to receive water reward for pressing the lever, whereas for another group the reward was changed to a 0.1% saccharin solution. At the end of the 60-min bar-pressing session, each subject was injected with

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lithium chloride. Three such conditioning sessions were conducted at 3-day intervals. Subjects were then tested for lever-pressing without either water or saccharin reward in the presence of the CS light and in darkness. Evidence of aversion learning to the illumination of the experimental chamber was provided by differential suppression of lever pressing during the extinction test. Subjects that received saccharin reward on conditioning days responded much less frequently during the extinction test than animals that had always been rewarded with water. Furthermore, the water-rewarded group did not appear to have learned an aversion to the light because its rate of responding was not different from that of a third group of subjects that had received the same procedures but had never been injected with lithium. Galef and Osborne (1978) recently also observed the conditioning of visual aversions mediated by taste using procedures that more closely approximate events outside the laboratory. They presented rats with gelatin capsules that were either 100% clear or 50% blue and 50% clear and were always filled with powdered laboratory chow. On the conditioning day, ingestion of the distinctive (50% blue) capsules was followed by treatment with lithium chloride. For some of the animals, the capsules were unflavored during conditioning, whereas for others the capsules were filled with powdered chow flavored with quinine or sucrose. All of the animals were then tested for their willingness to ingest the 50% blue capsules filled only with unadulterated chow. Subjects for which the distinctive capsules had been flavored with quinine or sucrose during conditioning subsequently evidenced stronger aversions to the 50% blue capsules than animals that had received unflavored capsules paired with lithium. Thus, the taste of quinine and sucrose facilitated the learning of an aversion to the visual features of the distinctive capsules. In related experiments with rats, Martin and Ellinwood (1974) found that access to 0.1% saccharin facilitates the conditioning of an aversion to the gray side of a black-gray shuttle box. More recently, Rusiniak et al. (1979) and Durlach and Rescorla (1980) observed that the presence of a distinctive taste facilitates the conditioning of an aversion to olfactory cues with lithium. Such potentiation effects have been also found in research with pigeons. Clarke et al. (1979) and Westbrook et al. (1980) reported that pigeons learn stronger aversions to visual aspects of a drinking solution if the drinking fluid also has a salient taste. The above examples of the facilitation of aversions to nongustatory cues by distinctive tastes are unexpected on the basis of research in other conditioning paradigms. Tastes are much more easily associated with toxicosis than are nongustatory cues (see Section IV). The presence of an easily conditioned stimulus usually reduces the association of other less salient stimuli with the US (Pavlov, 1927; Kamin, 1969). In fact, such overshadowing has also been observed with

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taste stimuli. Best er al. (1973) found weaker aversion conditioning of spatial cues with toxicosis when animals drank a novel-flavored solution in the distinctive environment. Similarly, Revusky and Parker (1976) found that animals form weaker aversions to a distinctive water cup if during conditioning they are allowed to drink a novel sucrose solution from the cup instead of familiar tap water. In a related experiment, Braveman (1975b) found that guinea pigs are less likely to learn an aversion to the color of their water if the water has an added novel flavor. It is not clear at the present time why in certain situations tastes facilitate the conditioning of aversions to nongustatory stimuli, whereas in other cases the opposite outcome is observed. The procedures involved in these widely disparate outcomes are very different and have yet to be analyzed. Whether one or the other effect is observed may depend on the relative rates of aversion conditioning of the taste and nongustatory stimuli and whether or not an association is established between the cues before each cue becomes associated with the toxicosis (cf. Durlach and Rescorla, 1980). OF SELECTIVE ASSOCIATIONS E. INGESTIONAS A DETERMINANT In the experiments described in Section I I I , D , tastes encountered during the course of ingestion facilitated aversion conditioning to nongustatory stimuli paired with toxicosis. In other situations, ingestion has been reported to facilitate aversion learning to nongustatory cues even in the absence of specific taste mediation (Shettleworth, 1972b). Furthermore, in these experiments the presence and absence of ingestion appeared to determine which of several stimuli were selected for association with the aversive US. These observations were made with baby chicks. The unconditioned stimulus was provided by shock to the feet or beak, and auditory and visual cues served as conditioned stimuli. In some cases the auditory and visual cues were encountered during the course of the ingestion of water. In other cases, the conditioning was carried out in the absence of ingestive responses. Whether or not ingestion was permitted in the situation turned out to be very important for the results observed. When water was available during conditioning and testing, the chicks evidenced stronger learned aversions to the visual cues than to the auditory stimuli. In contrast, when water was not available during conditioning and testing, the animals evidenced stronger aversions to the auditory cues paired with shock than to the visual stimuli. Thus, the presence or absence of ingestion determined which stimulus had predominant control over the aversion performance. This result probably reflected the conditioning of different associations in the ingestion and noingestion situations. However, it is also possible that the ingestion and noingestion tests were differentially sensitive to the conditioned aversiveness of the visual and auditory stimuli.

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F. INGESTION A N D POISON-AVOIDANCE LEARNING: OVERVIEW The ingestion of a novel food with toxic consequences is a very complex experience involving not only the taste of what is consumed but also its odor, its visual and tactile properties, and the orosensory stimuli involved in mastication and swallowing. The research reviewed above suggests that many aspects of this complex experience can be involved in the ingestional aversion that is learned. Animals may learn aversions not only to the taste of what they eat but also to the olfactory and visual features of the food, to the orosensory cues involved in the ingestion, and to the configuration of various combinations of these stimuli. In some situations the flavor of the ingested substance can also mediate the conditioning of aversions to nongustatory aspects of what is eaten, and in other cases the ingestive sequence can modulate which of the various stimuli in the situation will become associated with the aversive consequence. Thus, instances of ingestional aversion learning in laboratory and natural settings can reflect several associative components acting in concert to motivate the aversion performance. Rather than relying solely on the taste of edibles to guide their food selection, animals can make use of the full range of stimulation experienced during the course of eating.

Iv. A.

THESELECTIVITY OF ASSOCIATIONSIN INGESTIONAI, AVERSIONLEARNING

DEMONSTRATIONS OF SELECTIVE ASSOCIATIONS

The research reviewed in the previous section shows that many of the various stimuli that are encountered during the course of ingestion can become associated with toxic postingestional consequences. However, these findings should not be interpreted as indicating that animals can learn aversions equally well to all of the various stimuli that are paired with toxicosis. In fact, one of the most important aspects of ingestional aversion learning is that there is a selectivity in the associations. I . Dijfeerentiul Effectiveness of Various Coriditiorzed Stimuli

Early experiments on aversion conditioning with toxicosis, particularly toxicosis induced by radiation exposure, followed the Pavlovian tradition and attempted to demonstrate that all of the various stimuli animals can experience could be conditioned equally easily. In one of these experiments, for example, aversions to spatial cues were successfully conditioned with radiation exposure in rats (Garcia et n l . , 1957). However, it soon became evident in this line of research that the conditioning of aversions to spatial cues with radiation expo-

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sure requires more conditioning trials and higher radiation intensities than tasteaversion conditioning (Garcia et al., 1961). Consistent with this observation, Rozin (1969) found that the introduction of a 0.5-hrdelay between CS and US greatly interferes with the association of nongustatory cues with toxicosis but does not preclude taste aversion learning. In contrast to the successful demonstrations of spatial aversion learning motivated by toxicosis previously described, spatial aversions are typically not found in poison-avoidance learning experiments. Several investigators have found that while rats learn to avoid the taste of poisoned bait, they do not learn to avoid the location of the poisoned bait (Hargrave and Bolles, 1971; Rozin, 1967; Tevis, 1956). In these experiments it may be that the taste of the poisoned bait overshadowed (Kamin, 1969) the cues provided by location. However, attempts to condition aversions to auditory, spatial, and visual cues in the absence of concurrently available distinctive gustatory stimuli using toxicosis have also provided negative results (Domjan and Wilson, 1972b; Garcia and Koelling, 1967; Garcia er al., 1968). The fact that nongustatory cues are not as easily associated with toxicosis as novel taste stimuli is not necessarily inconsistent with traditional concepts of Pavlovian conditioning. Differences in the ease of conditioning of various potential CSs is expected if these stimuli differ in intensity, salience, or novelty. Furthermore, the fact that some stimuli are not as easily conditioned as another class of cues is not sufficient evidence for the existence of selective associations. Categories of stimuli that are not optimal in aversion conditioning with toxicosis may be equally ineffective in conditioning with other types of unconditioned stimuli. 2 . Cue-Consequence Specificity

Evidence for the selectivity of association in aversion conditioning is provided by experiments in which the conditionability of different categories of stimuli is found to depend on the type of unconditioned stimulus used (Schwartz, 1974; LoLordo, 1979). The first experiment of this type was the classic study reported by Garcia and Koelling (1966). Rats in this experiment were allowed to drink from a specially outfitted drinking tube that provided a flavored solution (sweet or salty) and an audiovisual stimulus (light from a 5-W bulb and sound from a clicking relay) each time the animal licked. Ingestion in this situation was paired with exposure to radiation, lithium toxicosis, or shock to the feet. Several conditioning trials were conducted, and the animals’ rates of drinking were then observed when licks produced either the taste stimulus alone or the audiovisual cue alone. Following conditioning with radiation exposure and lithium toxicosis, the rats were slower to lick in tests with the taste cue than in tests with the audiovisual stimulus, In contrast, following pairing of the audiovisual stimulus

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with footshock, the animals were slower to drink in tests with the audiovisual cue than in tests with the taste stimulus. Thus, the relative aversion subjects evidenced to the gustatory and audiovisual stimuli depended on the type of unconditioned stimulus they had been exposed to during the training trials. In the Garcia-Koelling experiment the distinctive taste and audiovisual stimuli were both present during the conditioning trials. Therefore, it is possible that the two types of conditioned stimuli did not become conditioned equally with each unconditioned stimulus because the presence of one of the CSs somehow interfered with strong conditioning of the other. Thus, the selective association effect observed by Garcia and Koelling may have been mediated by a stimulus competition process. The possibility of competition between CSs was ruled out by procedures used in a subsequent study (Garcia er nf., 1968). In this experiment taste and nongustatory conditioned stimuli were paired with radiation illness and footshock in independent groups so that none of the subjects experienced both types of conditioned stimuli at the same time. The gustatory stimulus was provided by coating food pellets with either powdered sugar or flour, and the nongustatory stimulus was provided by the size of the pellets. Subjects for which the unconditioned stimulus was paired with a distinctive flavor always received food pellets of the same size, and subjects for which the US was paired with a distinctive size (large or small) always received pellets of the same flavor. Tests conducted after the five conditioning trials revealed that stronger aversions were conditioned to size than to taste when the unconditioned stimulus was footshock. In contrast, stronger aversions were conditioned to the taste than to the size of the food pellets when the unconditioned stimulus was radiation exposure. Thus, this experiment yielded the same type of selectivity in aversion performance as a function of the unconditioned stimulus as had been observed by Garcia and Koelling (1966). These results show that subjects do not have to have both taste and nongustatory stimuli present on conditioning trials to show selectivity in aversion performance. The experiment by Garcia et al. (1968) ruled out the possibility of explaining the selectivity in aversion performance in terms of stimulus competition mechanisms. However, it introduced another problem in the comparison of the associability of taste and nongustatory cues. Taste stimuli were presented by allowing the animals to ingest food pellets. Thus, the subjects did not receive exposure to the flavor until they approached a food pellet, picked it up, and inserted it into the mouth. In contrast, the size conditioned stimulus did not require the same sequence of events. The subjects may have been able to either see or feel with their whiskers the size of the food pellets before they picked them up. Therefore, ingestion was not necessary in order for the rats to come in contact with this CS. This difference in the way in which the subjects experienced the

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taste and nongustatory stimuli may have introduced differences in the temporal relationship of each CS to the unconditioned stimuli used. Garcia and his colleagues were not unmindful of the confounding that is introduced by presenting taste and nongustatory conditioned stimuli to animals in different ways. That is why in their first experiment (Garcia and Koelling, 1966) both the taste and audiovisual CSs were presented contingent on licking a drinking tube. Differences in the method of CS presentation can also be minimized by presenting both taste and nongustatory cues without requiring licking or ingestive responses, the way that audiovisual stimuli are usually received. The presentation of audiovisual stimuli without requiring ingestion does not involve special problems. Taste stimuli can be presented without approach and drinking responses by infusing the fluid directly into the oral cavity of nondeprived rats through a fistula (Domjan and Wilson, 1972a). We used such an approach in two replications of the selective association design (Domjan and Wilson, 1972b). One of our experiments (Domjan and Wilson, 1972b, Experiment 2) was modeled after the study by Garcia et al. (1968) and investigated the selectivity of associations with taste and nongustatory CSs presented individually during conditioning. The rats first had an oral fistula implanted with one end secured to the inside surface of the cheek and the other end exiting at the back of the neck. The fistula permitted the presentation of taste solutions while the animals moved about freely. After recovery from the operation, access to water was restricted to 35 min each day. Once the animals were adapted to the deprivation schedule, three conditioning trials were conducted on successive days, each scheduled after the daily 35-min access to water. For three groups of subjects, the oral infusion of a 0.2% saccharin solution at 1 ml/sec served as the conditioned stimulus, and for the other three groups the CS was an irregularly pulsed buzzer which added 20 dB to the 50-dB (SPD) background noise. Each CS was presented for 35 sec. Immediately after the saccharin infusion, the subjects received a 10-ml oral infusion of tap water to help terminate the saccharin flavor. One taste CS group was then injected with lithium chloride, another received exposure to electric shock, and the third group served as a control and received only an injection of physiological saline. The buzzer CS groups were similarly conditioned with lithium, shock, or saline injection after the buzzer presentations. In addition to receiving one of the conditioned stimuli immediately before the unconditioned stimuli during the training trials, each subject was also exposed to the alternative conditioned stimulus (buzzer for the saccharin-conditioned rats and saccharin for the buzzer-conditioned rats) 1.5-2.5 hr after each conditioning trial. This aspect of the procedure allowed us to evaluate the nonassociative effects of the unconditioned stimuli used. After the conditioning trials, each subject was tested for its preference for the saccharin and buzzer stimuli. During the saccharin preference test, the animals had simultaneous access to two drinking tubes, one filled with saccharin and the other filled with tap water. During the

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FIG. 9. (A) Saccharin preference of rats exposed to saccharin in Conditioning with lithium, shock, or saline. (B) Buzzer-water preference of rats exposed to the buzzer in conditioning with lithium, shock, or saline. From Domjan and Wilson (3972b).

buzzer preference test, both drinking tubes were filled with tap water. However, drinking from one of the tubes always produced the sound of the buzzer. Preference for the stimulus (saccharin or buzzer) that served as the CS in conditioning with lithium treatment, shock, and saline injection is summarized in Fig. 9 for the six groups of animals. The results were very similar to what Garcia and his colleagues found. Lithium-conditioned subjects acquired significant aversions to the taste of saccharin whereas shock-conditioned animals did not show such aversions. In contrast, shock-conditioned animals learned strong aversions to the buzzer CS whereas lithium-injected rats did not. Preference for the stimulus (saccharin or buzzer) that did not serve as the CS for a particular subject but was presented after each conditioning trial is not shown in the figure. However, the three groups conditioned with the buzzer as the CS did not differ in their preference for saccharin, and the three groups conditioned with saccharin as the CS did not differ in their preference for the buzzer. This aspect of the findings, overlooked by some readers (e.g., Bitterman, 1976), shows that the aversions observed resulted from associative processes. If lithium had produced an aversion to saccharin in the absence of an association between these events, then animals that had the buzzer CS paired with lithium should have also shown an aversion to saccharin. Similarly, if shock had produced an aversion to the buzzer without an association, then animals that had the saccharin CS paired with shock should have also shown an aversion to the buzzer.

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INTERPRETATIONS OF THE SELECTIVE ASSOC~ATION EFFECT

I . Anatomical Convergence of Sensory Pathways Garcia and his associates (Garcia and Ervin, 1968; Garcia et al., 1974) have suggested that the cue-consequence specificity observed in aversion learning reflects the anatomical organization of the sensory pathways conveying information about the conditioned and unconditioned stimuli. The clearest evidence cited in support of this hypothesis is provided by the organization of the somatic and visceral neuropils in the medulla oblongata of the tiger salamander (Herrick, 1948). The somatic neuropil receives input from both the auditory system and from the cutaneous receptors, and the visceral neuropil receives fibers from the gustatory system and visceral receptors. Such separation of the exteroceptive and interoceptive sensory systems is assumed to be the basis for selective associations involving stimuli in these systems. Unfortunately, selective associations have not been investigated in the tiger salamander. Furthermore, as others have pointed out (Nachman et al., 1977), it is not known how anatomical convergence leads to facilitation of' conditioning. Behavioral evidence for selective associations has been provided by experiments with mammals. In these species the neural projections of sensory systems which provide exteroceptive information are not as limited as in the salamander. However, both gustatory and visceral receptors in mammals send fibers to the nucleus of the fasciculus solitarius (e.g., Morest, 1967), and this convergence may be the basis for the selectivity of taste-toxicosis associations. If selective associationsresult from the convergence of sensory pathways relaying information about the conditioned and unconditioned stimuli, then certain lesions should selectively disrupt the learning of taste-toxicosis associations and other lesions should selectively disrupt the learning of audiovisual-shock association. This prediction has been only partially confirmed. Some lesions, such as in the lateral septum and the ventral hippocampus, have been found to disrupt the learning of noise-shock associations without disrupting taste-aversion learning. However, lesions have not been reported which interfere with taste-aversion learning but do not disrupt noise-shock association (Gaston, 1979; McGowan et al., 1972). 2 . Adaptive Specializations of Learning

Another interpretation of the selective association effect in aversion learning states that the mechanisms controlling the learning of taste-toxicosis and audiovisual-shock associations are the product of an evolutionary selection process which has made these two types of learning ideally suited to protect the animal from such challenges to survival as food poisoning and external sources of injury (Rozin and Kalat, 1971; Seligman, 1970; Seligman and Hager, 1972). This interpretation is rather unspecific because it does not detail what aspect of

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the conditioning process is altered by evolution to facilitate certain associations and hinder other types of learning. The selection process may act on attentional mechanisms, memory mechanisms, or various aspects of the association process to promote selective associations. In any event, one possible outcome of evolution is that selective associations reflect the operation of unique learning processes in the association of different classes of conditioned and unconditioned stimuli (Rozin and Kalat, 1971). Although this is a possibility, such a conclusion is not required by what we know about selective associations so far. Selective associations may result from mechanisms, described below, that are applicable to a variety of conditioning situations. 3 . The Development of Learning Sets

One approach to explaining instances of selective associations in terms of general principles of learning has stressed the possible involvement of learning sets (e.g., Testa and Ternes, 1977). During the lifetime of the organism, stimuli arising from ingestion are followed by postingestional consequences every time the animal eats. The postingestional events usually involve various digestive processes and thirst and hunger reduction rather than toxicosis. Nevertheless, this repeated pairing of orosensory stimulation with visceral events may lead to the development of a learning set which then facilitates the learning of associations between novel tastes and toxicosis. A comparable argument is made to explain the rapid learning of associations between exteroceptive (e.g., audiovisual) stimuli and cutaneous pain. Because exteroceptive stimuli are often followed by other exteroceptive cues in the normal life of the animal, a learning set is assumed to develop which facilitates the learning of an association between a novel exteroceptive stimulus and cutaneous pain. The learning set interpretation of selective association can be investigated by modifying the normal feeding history of the animal and seeing if this changes the selective association effect. In an application of this strategy, Lucy Sullivan (cited in Testa and Ternes, 1977) raised rats in an environment in which visual cues were made predictive of ingestive consequences and taste stimuli were irrelevant. This training facilitated the conditioning of aversions to visual cues with toxicosis. However, the animals were equally able to form associations between taste cues and toxicosis. Attempts such as that of Lucy Sullivan to establish an artificial learning set demonstrate that learning sets can be involved in selective associations. However, such demonstrations do not prove that learning sets contribute to the phenomenon under normal rearing conditions. Another approach to investigating the learning set interpretation involves exploration of the selective association effect in very young animals that have had limited feeding experiences. Using this approach, Gemberling et al. (1980) recently found what may be a selective association effect in 5-day-old rats. Six groups of pups were used. For three of

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the groups, the conditioned stimulus was provided by the infusion of a 0.5% solution of sodium saccharin through an oral fistula. For the remaining three groups a tactile conditioned stimulus was presented by placing the animals in a small enclosure lined with either terrycloth or smooth cardboard. Animals in each CS condition received one of three possible unconditioned stimuli: a 1% body weight injection of 0.30 M lithium chloride, a 1% body weight injection of 0.15 M sodium chloride, or cutaneous shock. The shock US consisted of a series of five shocks (1-sec, 1-mA, constant current) administered at 1-min intervals during the 5-min CS through two metal electrodes placed on either side of the body near the hind legs of the animals. Twelve hours after conditioning, the pups were tested for their aversion to their respective conditioned stimuli. For the animals that had saccharin infusion as the conditioned stimulus, the aversion test involved a 5-min oral infusion of the saccharin solution, and the amount ingested was calculated from the weightgain the animals showed following the infusion. For animals that had the tactile conditioned stimuli, the aversion test was conducted in a chamber identical to that used in conditioning except that half of the chamber was fully lined with terrycloth and the other half was lined with smooth cardboard. (For half of these animals, terrycloth served as the CS and for the remaining animals the cardboard served as the CS.)At the beginning of each preference test, the pup was placed so that the midline of its body coincided with the junction of the two textures at the center of the chamber. The amount of time spent on each texture during the 5-min test was measured for each animal. The results of the aversion tests are displayed in Fig. 10. The lithiumconditioned pups drank significantly less saccharin during the test session than the saline-injected controls. However, such an aversion was not observed for the shock-conditioned animals. In contrast, the shocked pups showed a significant aversion to the texture-conditioned stimulus in comparison to the saline-injected controls, but no such aversion was evident among the lithium-conditioned rats. This pattern of results is identical to what is observed with adult animals in experiments employing audiovisual instead of tactile stimuli as the exteroceptive conditioned stimulus. The fact that the same kinds of selective aversions observed in adults are evident as early as 5 days of age suggests that an extensive history of ingestion and experiences with exteroceptive cues is not necessary for the phenomenon. Thus, these results are contrary to the learning set interpretation of selective associations. In a subsequent experiment, Gail Gemberling investigated selective associations in 1-day-old rats in an effort to further reduce the possible contribution of a history of ingestive and exteroceptive experiences. The conditioning procedure was the same as what we had used with the 5-day-old rats except that the conditioned stimuli (0.5% saccharin for some rats and terrycloth or smooth cardboard for the remaining subjects) were presented for 10 min, and the shock

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FIG. 10. Saccharin intakes (corrected for body weight) of 5-day-old rats exposed to saccharin in conditioning with lithium (Li), shock, or saline (Na), and preference for the CS texture (cardboard for some and tenycloth for others) in 5-day-old rats exposed to this texture i n conditioning with lithium, shock, or saline. From Gemberling ri al. (1980).

unconditioned stimulus consisted of 10 1-sec shocks delivered at 1-min intervals during the 10-min CS. Following conditioning with lithium, control injection of physiological saline, or shock, the pups were returned to their mothers until they were 5 days old. Tests for aversion to the saccharin and tactile conditioned stimuli were conducted at 5 days of age in the same manner as in the previous experiment except that the test sessions lasted 10 instead of 5 min. Results of the postconditioning test sessions are presented in Fig. 1 1 . The lithium-conditioned pups drank significantly less saccharin than both the salineinjected controls and the shock-conditioned animals, which did not differ from one another. In contrast to the pups conditioned at 5 days of age in the preceding experiment, the rats conditioned at 1 day of age and tested at 5 days of age responded differently to the two textures (terrycloth and cardboard) used as the exteroceptive conditioned stimuli. Therefore, the data are presented separately for these textures. There were no significant differences among the three groups of pups that had been conditioned with terrycloth as the CS. In contrast, significant group differences were apparent among the groups for which the smooth cardboard served as the conditioned stimulus. Shock-conditioned animals showed a significantly lower preference for the cardboard CS than the salineinjected controls or the lithium-conditioned rats. Furthermore, these latter two groups did not differ from one another. The findings with saccharin and cardboard as conditioned stimuli in aversion learning in the 1-day-old rats are similar to what was observed with the 5-day-old animals and are similar to selective association effects observed in adult rats. It is

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FIG.11. Saccharin intakes (corrected for body weight) of rats exposed to saccharin in conditioning with lithium (Li), shock (Sh), or saline (Na), and preference for the CS texture (cardboard for some and terrycloth for others) in rats exposed to this texture in conditioning with lithium, shock, or saline. The animals received one conditioning trial when they were 1 day old and were tested when they reached 5 days of age. From Gemberling (unpublished). not clear at the present time why terrycloth was not an effective conditioned stimulus for the 1-day-olds. Perhaps terrycloth is not sufficiently different from the tactile sensations of the nest to allow 1-day-old rats to differentiate it from the nest cues. Alternatively, returning the pups to the nest for 4 days between conditioning and testing may have resuIted in extinction of the conditioned aversions to the terrycloth stimulus. In any event, given the young age of the animals at conditioning, it is very unlikely that the results observed were due to the development of learning sets based on extensive ingestive and other experiences. The experiments with 5- and 1-day-old rats are exciting because they minimize the contribution of extensive life experiences to the behavioral effects observed. However, it is important to point out that these investigations are only preliminary. We have performed experiments that show that the aversions in rats con-

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ditioned at 1 day of age i n fact reflect associative processes. However, we have yet to determine the contribution of other variables, discussed below, to the selective associations learned shortly after birth. 4.

Event Covariation

One of the most interesting beliavioral interpretations of selective associations is based on the suggestion that the rate of conditioning is directly related to how similar the conditioned and unconditioned stimuli are in terms of their spatial location and temporal-intensity characteristics (Testa, 1974). According to this hypothesis, tastes are easily associated with toxicosis because both tastes and malaise tend to be prolonged and are slow to begin and end. Correspondingly, brief audiovisual cues are presumably easily associated with discrete footshock because of the similarity of the durations and onset and termination characteristics of these stimuli. In contrast, tastes and footshock and audiovisual cues and toxicosis are not readily associated because these pairs of stimuli have very different intensity and time course characteristics. The selectivity of associations observed in aversion learning is compatible with the event covariation hypothesis but was not predicted by this idea. However, the hypothesis has been the impetus for several other findings. One of these involved a comparison of the effectiveness of various combinations of visual conditioned stimuli in association with different types of air blast as unconditioned stimuli in rats (Testa, 1975). The visual conditioned stimulus was either pulsed and emanated from the ceiling or was presented in a wave form emanating from the floor. The air blast unconditioned stimulus was also either pulsed and originated from the ceiling or was presented in a wave form and originated from the floor. Various groups received different combinations of these stimuli in conditioning. Stronger aversions to the visual CS resulted in cases in which the conditioned and unconditioned stimuli had a similar temporal distribution and originated from the same location as compared to cases in which the temporal distribution and location of the CS and US were different. These results are exactly as predicted by the event covariation hypothesis. However, as the author noted, it is unclear whether the results reflected associative changes or sensitization effects because the appropriate control groups were not included in the experiment. More convincing evidence for the event covariation hypothesis was provided by a series of second-order conditioning experiments by Rescorla and Furrow (1 977). Two of these experiments investigated the development of second-order associations between different combinations of visual and auditory stimuli in rats. These studies showed that an association develops more rapidly between stimuli of the same modality (both auditory or both visual stimuli) than it does between stimuli of different modalities (auditory-visual associations or visualauditory associations). The third experiment provided similar evidence of selec-

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tivity in the development of second-order associations in pigeons. All of the stimuli in this last experiment were visual. Two of them were color stimuli (blue and green), whereas the other two were orientation cues (horizontal and vertical lines). Associations developed more rapidly if both of the stimuli were of the same type (color or orientation) as compared to cases in which one of the stimuli was color and the other was orientation. Similar results were recently reported with the association of stimuli presented in the same or different locations (Rescoda and Cunningham, 1979). 5 . Differential Time Course of CS Traces

This explanation (Krane and Wagner, 1975) is similar to the event covariation hypothesis in that it emphasizes the importance of the temporal characteristics of the stimuli involved in selective association experiments. Another important factor in this explanation is the delay between exposure to the conditioned stimulus and the onset of unconditioned stimulus effects. It is assumed that the trace of taste stimuli is considerably longer than the trace of audiovisual cues. Therefore, when a taste is paired with an immediate brief electric shock, it is quite likely that the trace of the flavor persists after the unconditioned stimulus. This reduces the extent to which the taste serves as a signal for shock and therefore little conditioning occurs. Audiovisual-shock conditioning, in contrast, is robust because in this case the trace of the CS does not linger beyond the unconditioned stimulus to reduce the signaling relationship between CS and US. The poor associability of audiovisual cues with toxicosis is explained by the fact that toxicosis is usually delayed in its onset and therefore may not occur while the trace of the audiovisual CS still exists. The delayed onset of toxicosis does not similarly interfere with conditioning of taste stimuli because the trace of taste cues presumably persists long enough to overlap with the toxicosis. Evidence consistent with the differential CS trace hypothesis was provided by Krane and Wagner (1975) in an experiment that compared the effectiveness of brief footshock in conditioning aversions to an audiovisual stimulus and the taste of 0.7% saccharin. Independent groups were shocked 5 , 30, and 210 sec after exposure to these conditioned stimuli. Subsequent test sessions revealed that aversion learning to the audiovisual stimulus was best at the 5-sec CS-US delay, and learning progressively decreased with longer delay intervals. In contrast, the strongest saccharin aversion learning occurred when the shock US was delayed 210 sec, and no conditioning was evident with the 5-sec delay interval. The inverse relationship observed between conditioning of the audiovisual CS and the CS-US interval presumably occurred because with longer CS-US intervals the trace of the CS did not persist to coincide with the unconditioned stimulus. The direct relationship between conditioning of the taste CS and the CS-US interval presumably reflected the long trace of the flavor CS, which persisted beyond

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the US in groups conditioned with a short CS-US interval and lasted long enough to overlap with the US in groups conditioned with a long CS-US interval. Although the results presented by Krane and Wagner (1975) are good evidence for the differential time course of the trace of audiovisual and flavor conditioned stimuli, others (e.g., Hankins et al., 1976) have pointed out that these results may have limited applicability to the selective association effects reported with toxicosis and shock (e.g., Domjan and Wilson, 1972b; Garcia and Koelling, 1966). Krane and Wagner used a much more concentrated saccharin solution than had been used in the earlier selective association experiments, and therefore the aversions observed may have been in part controlled by the odor of the saccharin. It is also not clear to what extent the shock-conditioned aversions to saccharin were similar to saccharin aversions conditioned by toxicosis. The shock-conditioned aversions may have been weaker than typical toxicosisinduced aversions and may have been much more limited to the conditioning situation. Thus, it remains to be seen whether or not the original selective association effect observed in conditioning with shock and toxicosis can be eliminated by sufficiently delaying the shock unconditioned stimulus for the taste-conditioned groups. 6. Differeniiul Orientdon Produced by Unconditioned Stimuli

Another interesting behavioral interpretation of the selective association effect attributes the phenomenon to differential orientations caused by the different unconditioned stimuli (Rescorla and Holland, 1976). This interpretation assumes that footshock causes animals to attend especially to audiovisual stimuli, and toxicosis causes animals to attend especially to taste stimuli. This differential attention to one or the other type of conditioned stimulus is then assumed to be responsible for the rapid association of these stimuli. Differential orientations evoked by the unconditioned stimuli are most likely to determine which CS becomes conditioned on the next trial. Therefore, such a mechanism would appear to be of limited applicability to situations in which selective associations are observed following a single conditioning trial. Although the classic demonstrations of the selective association effect involved multiple trials (Domjan and Wilson, 1972b; Garcia and Koelling, 1966; Garcia et a / . , 1968), recent experiments on selective associations in infant rats were performed with a single conditioning trial (see Section IV,B,3). The differential orientations evoked by the unconditioned stimuli would also have to be long lasting to account for selective associations because such effects are usually demonstrated with intertrial intervals of 24 hr or more (Domjan and Wilson, 1972b; Garcia and Koelling, 1966; Garcia et a / . , 1968). Rescorla and Holland (1976) suggested an experimental design for precluding the operation of differential orientation mechanisms in selective association

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experiments. Basically, the strategy involves exposing subjects to both of the unconditioned stimuli. One unconditioned stimulus is to be paired with the conditioned stimuli, and the other unconditioned stimulus is to be presented during the intertrial interval. For example, one group of subjects might receive an auditory-taste compound CS paired with toxicosis and have the footshock unconditioned stimulus presented during the intertrial intervals. Another group might receive the auditory-taste CS paired with footshock and have toxicosis administered at some other time. Presumably because both of the unconditioned stimuli are presented to both groups, any differences in aversion performance between them could not be attributed to nonassociative orientation effects of the unconditioned stimuli. This experimental design has been used with success in demonstrationsof selective association effects in second-orderconditioning (Rescorla and Furrow, 1977; Rescorla and Cunningham, 1979). However, the experimental design remains to be tested in connection with the taste-toxicosis audiovisual-shock selective association effect.

7. Differential Sensitivity of Response Measures Another possibility that must be considered is that the differential aversions evident in conditioning with toxicosis and footshock reflect differential sensitivity of the response measures employed (e.g., LoLordo, 1979; Rescorla and Holland, 1976; Testa and Ternes, 1977). The tests used to measure taste-shock and audiovisual-toxicosis associations may not be as sensitive as the tests used to measure taste-toxicosis and audiovisual-shock associations. It is always possible that a particular failure to observe learning reflects insensitivity of the test procedure used rather than the absence of learning. The discovery of test procedures that show strong evidence of taste-shock and audiovisual-toxicosis learning would indicate that a selective association effect does not exist with these CSs and USs. However, such evidence would not completely dispose of the phenomenon originally identified by Garcia and Koelling. Garcia and Koelling (1966), Garcia et al. (1968), and Domjan and Wilson (1972b) all used the same response measures in assessing the conditioning of various CSs with footshock and toxicosis. In most cases this involved the suppression of ingestion. Even if the results obtained did not reflect selective association effects, it remains to be explained why the same response measure was more sensitive to taste-toxicosis and audiovisual-shock associations than it was to taste-shock and audiovisual-toxicosis associations. For a complete theory of behavior, it is just as important to explain such selective performance effects as it is to explain selective association effects.

8. Dixerential Innate Reactions to the Conditioned Stimuli Selective association effects are commonly interpreted as reflecting different rates of acquisition of different associations. However, the initial strength of the

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different indicant responses may not be equivalent. For example, it may be that the innate reaction to taste stimuli involves some of the same responses that are conditioned by toxicosis, and the innate response to audiovisual cues involves some of the same responses that are conditioned by footshock. Evidence of taste-toxicosis and audiovisual-shock associations may appear quickly because in these cases less learning is required to bring the conditioned response above threshold. This kind of reasoning, originally contemplated by Konorski (1948, 1967), was recently discussed in detail by LoLordo (1979). There is no evidence in toxicosis and shock conditioning to preclude such an interpretation.

c.

THEUNIQUENESS OF SELECTIVE ASSOCIATIONSIN THE FEEDING SYSTEM

The observation that ingestion-related stimuli are favored in associations with toxicosis and that audiovisual cues are favored in associations with peripheral pain is one of the important facts that have been used to argue that learning in the feeding system has certain unique properties. The experiment by Garcia and Koelling ( 1966) was the first striking demonstration of selective associations. Because much of the work of Garcia and his colleagues involved the feeding systems, it was tempting to conclude that the results represented special properties of conditioning in this system. This conclusion, however, was probably premature. First, the cue-consequence relationship Garcia and Koelling ( 1966) discovered involved both toxicosis conditioning and conditioning with shock, and the selective association effect was as true of fear conditioning with shock as it was of taste-aversion conditioning with toxicosis. That is, tastes were found to be much less effective in conditioning with footshock than were audiovisual cues. Thus, if the selective associations found with toxicosis are used to argue for the uniqueness of conditioning with toxicosis, a similar argument should be made for the uniqueness of fear conditioning with footshock. The cue-consequence specificity Garcia and Koelling (1966) first identified also cannot be used to argue for the uniqueness of learning in the feeding system because similar selective association effects have been observed since then in other situations. For example, Testa (1975) observed that if the unconditioned stimulus was an air blast from the ceiling, a visual stimulus from the ceiling became better conditioned than a visual stimulus from the floor. In contrast, if the unconditioned stimulus was an air blast from the floor, the visual stimulus from the floor became conditioned more readily. In other examples of selective association effects, Rescorla and Furrow (1977) observed that stimuli that were similar in modality or visual characteristics became more readily associated with one another in a variety of second-order conditioning procedures than stimuli that were less similar, and Rescorla and Cunningham (1979) found that stimuli presented in the same location became more readily associated than stimuli pre-

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sented in different locations. Finally, LoLordo and his associates (reviewed in LoLordo, 1979) have found that in pigeons auditory stimuli become more readily conditioned in shock-avoidance experiments than visual cues and visual stimuli are favored over auditory cues in conditioning with food reward. The various examples of cue-consequencerelationships that have been discovered since the original work of Garcia and Koelling (1966) suggest that the selective association effects observed in conditioning with toxicosis are not unique. Rather, it appears that selective associations and cue-consequence relationships are but another common characteristic of associative learning. As the mechanisms that contribute to such effects become better understood, other examples of selective associations will no doubt be discovered.

ON INGESTIONAL AVERSION LEARNING V. LIMITATIONS

Although the mechanisms of selective associations in aversion learning have not been fully characterized yet, there is no dispute that taste stimuli are favored in conditioning with toxicosis in omnivores such as the rat. There is also no dispute that taste aversions can be learned in one trial even if there is a long delay (more than an hour) between the taste exposure and the subsequent toxicosis. These characteristics of the phenomenon have encouraged the view that ingestional aversion learning is a primitive type of conditioning which occurs automatically when taste exposure is paired with postingestional malaise. The implication is that animals will learn aversions to tastes paired with toxicosis even if a causal inference between ingestion and toxicosis cannot be easily drawn. This view is perhaps best exemplified by the title of an article by Kalat and Rozin (1972), “You can lead a rat to poison but you can’t make him think.” Recent research suggests that it may be incorrect to view taste-aversion leaming as a primitive type of conditioning that is immune to the influence of informational variables. Stated in the language of Kalat and Rozin, it appears that rats can be made to think when they are led to poison. Several lines of investigation have shown that aversion learning is disrupted by experiences that reduce the extent to which a causal inference can be made between the target conditioned stimulus flavor and toxicosis. One type of evidence involves the effect of repeated exposure to the CS flavor in the absence of toxicosis before the conditioning trial. A food that is repeatedly ingested without aversive effects in nature is not likely to be the cause of malaise experienced later. As expected on the basis of this consideration, extensive exposure to the CS flavor in the absence of toxicosis before the conditioning trial severely disrupts taste-aversion learning. Similarly, extensive exposure to the toxin unconditioned stimulus alone before the conditioning trial also interferes with aversion learning. Preconditioning US exposures in the absence of taste also reduce the extent to which a causal in-

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ference can be made between taste and toxicosis. Because these two phenomena have been discussed extensively elsewhere (e.g., Domjan 1977a; Randich and LoLordo, 1979), they will not be treated further here. The CS preexposure and US preexposure phenomena noted disrupt aversion learning because of special experiences several days or more before the actual taste-aversion conditioning trial. Other research has shown that events closer to conditioning can also disrupt aversion learning. These events similarly reduce the extent to which a causal inference can be made between the target conditioned stimulus flavor and toxicosis. One of these types of experiments has shown that the presentation of several novel flavors during the conditioning trial reduces aversion learning to the target flavor. The second type of experiment has shown that aversion learning is disrupted if stimuli are introduced during conditioning that are better predictors of toxicosis than the target conditioned stimulus flavor. Finally, conditioning is similarly disrupted if in addition to receiving toxicosis after taste exposure, the animals are also injected with the toxin within several hours before access to the flavor. These phenomena are discussed in greater detail below. IN TASTE-AVERSION LEARNING A. OVERSHADOWING

It is a common observation in conditioning experiments that learning is disrupted if in addition to the target conditioned stimulus the animals are also exposed to other novel stimuli during the conditioning trial (e.g., Kamin, 1969). Pavlov (1927) referred to this effect as overshadowing. Overshadowing is also characteristic of taste-aversion learning. In one demonstration of the effect, Revusky (1971) conditioned an aversion to 0.2% saccharin in several groups of rats by allowing the animals to drink 2 ml of saccharin 75 min before the injection of lithium chloride. Fifteen minutes after the saccharin exposure, independent groups of animals were allowed to drink 5 ml of a novel 0.5, 1.5, or 4.5% solution of vinegar. Tests of saccharin conditioning conducted later showed that aversion learning was disrupted by the presentation of the vinegar flavor during the conditioning trial, and the extent of this disruption was directly related to the concentration of the vinegar solution. This latter aspect of the results is probably related to the fact that the more concentrated vinegar solutions were more novel to the subjects (Kalat, 1974). Consistent with this view, Revusky, Lavin, and Pschirrer (reported in Revusky and Garcia, 1970) found that the overshadowing of one flavor by another in taste aversion conditioning is greater if the overshadowing flavor is more novel. The experiments conducted by Revusky and his colleagues involved presenting one overshadowing novel flavor during the conditioning trial in addition to the target conditioned stimulus flavor. In a related experiment, Kalat and Rozin (197 1) investigated the effects of presenting three flavored solutions in addition

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to the target flavor during conditioning. Although the animals learned an aversion to the target stimulus when they also tasted three other substances during conditioning, the aversion learning was attenuated by exposure to the nontarget flavors. This effect was especially evident in Experiments 2B and 2C. The authors analyzed their data in terms of the absolute amount of the target flavor ingested during the postconditioning test session. However, the test session consisted of a choice between the target flavor and plain water. Intakes of the CS flavor in the overshadowing groups of Experiments 2B and 2C were 21 and 51% of total intake during the test session. In contrast, the corresponding values for the subjects not exposed to overshadowing flavors during conditioning were 4 and 5%, respectively. B.

RELATIVEVALIDITYOF CONDITIONED STIMULI

Another common observation in conditioning experiments is that the conditioning of one stimulus is disrupted by the presence of other conditioned stimuli that are better predictors of the unconditioned stimulus (see reviews by Rescorla and Wagner, 1972; Wagner, 1969). This research shows that the relative validity of cues as predictors of the US influences the rate of their conditioning. One of the important paradigms used in these investigations involves the prior conditioning of the interfering stimuli; another important paradigm involves the concurrent conditioning of the interfering cues.

I.

Prior Conditioning of Interfering Stimuli: The Blocking Effect

In this procedure one conditioned stimulus is first paired with the unconditioned stimulus until learning is well established. This conditioned stimulus is then presented during the conditioning of a novel stimulus, and conditioning of the novel stimulus is thereby severely disrupted. This blocking of conditioning by the presentation of a previously conditioned stimulus has been observed in several situations, including fear conditioning (Kamin, 1969) and foodreinforced discrimination learning (Miles, 1970). Explanations of the blocking effect have invoked cognitive mechanisms such as attention (Mackintosh, 1971, 1975; Sutherland and Mackintosh, 1971), expectancy (Rescorla and Wagner, 1972), and processing in short-term memory (Kamin, 1969; Terry and Wagner, 1975; Wagner et al., 1973; Wagner and Terry, 1975). Because of this, demonstrations of the blocking effect in taste-aversion learning have been considered important evidence for the involvement of cognitive mechanisms in tastetoxicosis conditioning as well. Some of the early efforts to demonstrate the blocking effect in taste-aversion learning were unsuccessful, and this failure was used to argue that taste-aversion learning is not influenced by cognitive processes (Kalat and Rozin, 1972). However, the phenomenon has been repeatedly demonstrated in other research. In

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some of these experiments, exteroceptive cues served as the blocking stimuli (e.g., Batson and Best, 1979; Braveman, 1979; Rudy er a / . , 1977; Willner, 1978). During the first phase of these studies, the animals were injected with lithium after placement in a distinctive environment for several trials. After this exteroceptive conditioning, the animals had the taste of saccharin paired with lithium. Saccharin aversion learning was attenuated for subjects that were exposed to the drug-conditioned spatial cues during the saccharin conditioning trial. Blocking may be more difficult to demonstrate when a taste solution rather than spatial cues serves as the blocking stimulus. The animals have to be exposed to the initially conditioned taste for this flavor to block the conditioning of a novel taste solution. However, the subjects will learn an aversion to the blocking flavor in the first phase of the experiment, and this will limit their voluntary contacts with the blocking stimulus during conditioning of the novel taste solution. In the first successful demonstration of blocking with taste stimuli, Revusky (197 1) facilitated exposure to the blocking taste stimulus during conditioning of the novel flavor by conducting conditioning after 2 days of water deprivation. Another approach to the problem is to expose subjects to tastes during the conditioning trials by infusing the flavored solutions directly into the oral cavity through a chronic fistula. This is the method we used in our experiments on blocking in the taste-aversion system (Domjan and Gemberling, unpublished; Gillan and Domjan, 1977). Most of our blocking experiments consisted of two phases. During the first phase, all subjects received differential conditioning in which the oral infusion of flavor D (the drug-predictive taste) was repeatedly paired with the injection of lithium chloride, and the oral infusion of flavor ND (the non-drug-predictive taste) was repeatedly presented without toxicosis. Solutions of vinegar and sodium chloride served as taste stimuli during this phase of the experiment and were assigned as flavors D and ND in a counterbalanced fashion. Following the initial differential conditioning, all animals had the taste of 0.5% saccharin paired with lithium malaise. In one of our experiments, one group of animals received an oral infusion of flavor D immediately before the saccharin conditioning trial, and another group was exposed to flavor ND immediately before saccharin conditioning. Several days after the saccharin conditioning trial, subjects were tested for their intake of the saccharin solution in a one-bottle test. The results of this test session are displayed in Fig. 12. As is evident from the figure, animals exposed to the drug-predictive flavor immediately before saccharin conditioning (Group D) learned a much weaker aversion to the saccharin flavor than animals for which the lithium was not expected during saccharin conditioning (Group ND). Group D drank more than twice as much saccharin during the test session as Group ND. In other experiments (Gillan and Domjan, 1977), we have found that exposure to flavor ND does not influence taste-aversion learning. That is, Group ND

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MINUTES

FIG.12. Mean cumulative intake of saccharin following aversion conditioning. For Group D, the lithium injection during the saccharin conditioning trial was announced by exposure to a flavor that was previously paired with drug treatment on several occassions. For Group ND, the lithium injection during the saccharin conditioning trial was preceded by a stimulus that had never before been followed by drug treatment. From Gillan and Domjan ( 1977). acquires as strong an aversion to saccharin as animals that do not receive any flavor in addition. to saccharin during the saccharin conditioning trial. Furthermore, the blocking of conditioning, which is produced by exposure to the previously conditioned flavor D, is related to the drug-conditioned properties of flavor D because extinction of these properties also attenuates the extent to which flavor D blocks saccharin aversion learning. Finally, for the drug-predictive flavor D to block saccharin conditioning, it has to be presented within an hour of the saccharin conditioning trial. If saccharin conditioning is conducted more than an hour after subjects are exposed to the drug-predictive flavor D, an interference with aversion learning does not occur (Domjan and Gemberling, 1980).

2. Concurrent Conditioning of Interfering Stimuli In the standard blocking experiment, the blocking stimulus is conditioned first. Aversion learning to a novel conditioned stimulus is then disrupted by the presence of the blocking stimulus because the blocking stimulus is a better predictor

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of the unconditioned stimulus than is the novel cue. Another experimental design for investigating how conditioning is influenced by the relative validity of the conditioned stimuli in the situation was introduced by Wagner er al. (1968). Repeated conditioning trials were administered, and the target conditioned stimulus (A) was paired with the unconditioned stimulus on 50% of the trials. In one group, the animals were exposed to a second CS (B) in addition to stimulus A on all reinforced trials (AB+) and a third stimulus (C) was presented with stimulus A on all nonreinforced trials (AC-). Thus, this group received an equal number of AB+ and AC- trials. The comparison group also had stimulus A paired with the unconditioned stimulus on 50% of the trials. However, in this case stimuli B and C occurred equally often on reinforced and nonreinforced trials ( A B k / A C k ) . It is important to note that in procedure AB+-/AC*, stimulus A is as good a predictor of the unconditioned stimulus as are stimuli B and C because each of these cues is paired with the US 50% of the time. In contrast, in procedure AB+/AC- , stimulus A is a less effective predictor of the US than is stimulus B because stimulus A is reinforced only 50% of the time whereas the US is presented every time stimulus B occurs. If conditioning is influenced by the extent to which one CS is more or less predictive of the US than other CSs in the situation. then procedure AB +/AC- should produce less conditioning of stimulus A than procedure ABdACzk. This outcome was observed by Wagner er a / . (1968) in both instrumental and classical conditioning situations with auditory and visual cues serving as conditioned stimuli. Much less research has been done in taste-aversion learning with the concurrent conditioning of interfering stimuli than with the prior conditioning of interfering cues in the blocking design. However, it appears that results comparable to those of Wagner et al. (1968) can also be observed in taste-aversion learning. Luongo (1976) compared the conditioning of stimulus A in procedures AB+I AC- and AB+-/AC* with tastes serving as stimuli A, B , and C and toxicosis serving as the unconditioned stimulus. Stimulus A was the flavor of 0.16% saccharin, and the tastes of cinnamon and wintergreen extract dissolved in water were assigned as stimuli B and C in a counterbalanced fashion. The compound stimuli AB and AC were made by adding the cinnamon and wintergreen extracts to the saccharin solution so that the resultant fluids consisted of 1% extract. In Experiment 1 subjects received 11 trials paired with lithium toxicosis and 1 I nonreinforced trials; in Experiments 2 and 3, 16 reinforced and 16 nonreinforced trials were administered. Following this training with the flavor mixtures, subjects were tested for their intake of the saccharin solution unadulterated with cinnamon or wintergreen. Animals that received the conditioning procedure AB+/AC- learned significantly weaker aversions to the saccharin solution in each experiment than subjects that received procedure AB?/AC+. This outcome was observed even though the saccharin solution was paired with toxicosis an

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equal number of times for both groups. Thus it appears that as in the research of Wagner et a!. (1968), taste-aversion learning is influenced by the extent to which the flavor CS is a good predictor of toxicosis relative to other tastes in the situation. C, PROXIMAL UNCONDITIONED STIMULUS PREEXPOSURE Another procedure that reduces the extent to which a causal relationship between taste and toxicosis can be inferred involves injecting the subjects with the toxin not only shortly after the taste exposure but also shortly before the taste presentation. Such proximal unconditioned stimulus preexposure has been found to reduce eyelid conditioning in rabbits (Terry, 1976). Recent experiments by Michael Best and me indicate that a similar interference effect occurs in tasteaversion learning (Best and Domjan, 1979; Domjan, 1978; Domjan and Best, 1977). The proximal US preexposure effect is illustrated by one of our experiments that compared the saccharin aversion learning of seven groups of rats (Best and Domjan, 1979, Experiment I). During the saccharin conditioning trial, all animals were given access to a 0.15% saccharin solution for 20 min or until they drank 3 ml, whichever occurred first. Forty minutes after the beginning of the saccharin presentation, each subject received a conditioning injection of 1.8 meq/kg lithium chloride. This was the only drug injection given to subjects in Group TAC (Taste-Aversion Control). The other groups not only received the conditioning injection but were also injected with lithium 90 min, 360 min, or 1 day before the saccharin conditioning trial. For three of the groups, the preexposure drug injection dose was 1.8 meq/kg, whereas for the other three groups the preexposure dose was 3.0 meqkg. Several days after the conditioning trial, subjects were given a 20-min onebottle test with the saccharin solution. The mean saccharin intake of each group is summarized in Fig. 13. The nonpreexposed Group TAC learned the strongest aversion to saccharin. Lithium preexposure 1 day before the conditioning trial did not produce a significant attenuation in saccharin aversion learning with either the 1.8 or 3 .O meq preexposure dose. In contrast, significant attenuations in conditioning were observed in both of the groups that were preexposed to lithium 90 min before the conditioning trial and in animals that received a 3.0 meq lithium injection 360 min before conditioning. However, the lower preexposure drug dose did not produce a significant interference effect when administered 360 min before the conditioning trial. The results described above indicate that a single drug injection administered before conditioning interferes with aversion learning only if the US preexposure occurs within a relatively short period before the conditioning trial. Drug treatment 1 day or more before conditioning does not disrupt aversion learning. However, the time course of the interference effect is related to the drug dose: the

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1

OJ,

i

90min

360rnin

1 Day

PREEXPOSURE INTERVAL

FIG. 13. Mean saccharin test intakes for independent groups of rats that received either a 1.8 or a 3.0 meq/kg lithium injection 90 min, 360 min, or 1 day before saccharin conditioning. The dashed horizontal line represents the mean intake of Group TAC which

received saccharin conditioning in the absence of lithium preexposure. From Best and Domjan (1979).

interference effects of a higher preexposure dose persist longer than the disruptive effects of low drug doses. Other experiments have identified many characteristics of the proximal US preexposure effect and have shown that the phenomenon occurs in a wide variety of situations. Proximal US preexposure disrupts aversion learning even if the preexposure US treatment is otherwise effective in producing a “backward” conditioned saccharin aversion (Domjan and Best, 1977). The phenomenon also occurs whether or not the conditioning drug treatment is administered before or after exposure to the CS flavor during the training trial (Domjan, 1978). The interference effect is also evident when subjects are tested for their conditioned taste aversions while they are under the influence of the drug US (Best and Domjan, 1979), and proximal US preexposure disrupts conditioning even if the preexposure drug injection is paired with a novel flavor (Best and Domjan, 1979). In all of our published research on the proximal US preexposure effect, both the preexposure drug injection and the conditioning drug injection administered later consisted of lithium chloride. However, one drug administered shortly before a taste-aversion conditioning trial can also interfere with aversion conditioning induced by other drugs or treatments. We have observed that proximal preexposure to lithium disrupts taste-aversion conditioning induced by rotational stimulation (Domjan, unpublished). Others have reported that proximal preexposure to atropine disrupts taste aversions conditioned by lithium and radiation

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exposure (Deutsch, 1978; Gould and Yatvin, 1972; 1973); preexposure to pimozine disrupts conditioning with amphetamine (Grupp, 1977); proximal preexposure to antihistamine disrupts conditioning with irradiation (Levy et al., 1974); preexposure to dexamethasone disrupts conditioning with lithium (Hennessy et al., 1976); and preexposure to a-methltyrosine disrupts amphetamine conditioning (Goudie et al., 1975b). These effects may be in part due to the fact that the preexposure drug treatments create some malaise which reduces the causal inference that can be made between the taste experience and the subsequent conditioning drug treatment. Consistent with this suggestion, Deutsch ( 1978) found that atropine interferes with taste-aversion learning produced by lithium if the atropine is injected shortly before the conditioning trial but does not disrupt learning if the atropine is given between the taste exposure and the lithium injection during conditioning. Similarly, Sessions (1975) reported that the interference effects of antihistamine on radiation-induced aversion conditioning reported by Levy er al. (1974) do not occur if the antihistamine is injected between the taste exposure and irradiation rather than before the taste exposure during conditioning.

A CONTINUING SEARCH FOR GENERAL AND VI. CONCLUSION: U N I Q U E CHARACTERISTICS OF INGESTIONALAVERSION LEARNING

The taste-aversion learning paradigm has become a prominent field of investigation because some of the characteristics of this type of learning at first appeared to be unique, and this brought into question the advisability of trying to identify general laws of learning. The attack on the generality of the laws of learning had two aspects. One was the suggestion that different types of mechanisms may be involved in the various examples of learning that are exhibited by a given species. The other was the suggestion that the laws of learning discovered with one species may not be applicable to other types of animals. Because the research reviewed in the present chapter did not compare and contrast learning in different types of animals, the discussion does not permit reaching a conclusion about the generality of the laws of learning among various species. However, we can say something about the generality of learning mechanisms across various types of conditioning procedures for at least one type of animal, the omnivorous mammal as exemplified by the rat. For this type of organism, some of the characteristics of taste-aversion learning that were initially considered to be unique, such as the stimulus selectivity effect, have since been identified in other conditioning preparations. There are also few instances of conditioning phenomena observed in other conditioning preparations that have not been also observed in taste-aversion learning after sufficient exploration. These developments suggest that the pursuit of general theories of learning may not be as ill-fated a venture as some have suggested. Furthermore, the use of

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examples from taste-aversion learning to argue against the generality of the laws of learning is no longer very convincing. Although ingestional aversion learning appears to have many characteristics in common with other types of conditioning, it is probably an overstatement to suggest that this type of learning is entirely lacking in unique features. There are at least two aspects of ingestional aversion learning that may turn out to be unique. First, the conditioning situation involves having animals experience the conditioned stimuli during the course of ingestion, and this provides a complex array of covarying and interrelated stimuli including the visual, olfactory, taste, and tactile properties of the food as well as the orosensory stimuli involved in mastication and swallowing. These numerous sensations that accompany ingestion contrast with the simple auditory and visual conditioned stimuli used in other conditioning preparations and play an important role in ingestional aversion learning. The other characteristic of ingestional aversion learning that may turn out to be unique is that aversions are learned in one trial even if the toxicosis is not induced until several hours after ingestion of the target edible. Ingestional aversion learning may have some unique features because the stimuli involved in this type of conditioning have certain characteristics that are very different from the characteristics of stimuli involved in other types of learning. The unique characteristics of ingestional stimuli may lead to unique conditioning phenomena which are nevertheless governed by generally applicable laws of learning (cf. Krane and Wagner, 1974). Alternatively, the unique phenomena observed in ingestional aversion learning may result from the operation of unique learning processes (cf. Rozin and Kalat, 1971). Whether unique learning processes or unique stimulus features are responsible for the unusual aspects of ingestional aversion learning is central to theoretical evaluations of this type of learning. Research on the importance and role of the complex of ingestive sensations for aversion learning is still in its infancy. For example, very little is known about the mechanisms of the modulation of selective associations by ingestion-related events in the systems in which these effects were discovered. We also do not know if comparable phenomena exist in other situations. Therefore it is premature to speculate whether these effects reflect unique aspects of the stimuli involved or unique learning mechanisms. In contrast to the paucity of research on the importance of the complex of ingestive sensations, there has been a great deal of empirical work and theoretical speculation concerning the mechanisms of long-delay ingestional-aversion learning (see, for example, reviews by Best and Barker, 1977; Garcia and Ervin, 1968; Kalat, 1977; Revusky and Garcia, 1970; Revusky, 1977c; Rozin and Kalat, 1971). Furthermore, this research suggests that long-delay ingestionalaversion learning may be the result of a unique learning process and not the result of unique properties of ingestional stimuli. Two types of evidence support this conclusion. First, long-delay learning of the sort found in ingestional condition-

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ing with toxicosis is rarely found in other conditioning preparations. Second, long-delay ingestional aversion learning is not limited to taste cues encountered during ingestion. The most systematic attempt to discover long-delay learning effects in other learning preparations has been carried out by Revusky and his colleagues and has been motivated by the concurrent interference theory proposed by Revusky (for reviews, see Revusky, 1971, 1977~).The basic tenet of the concurrent interference theory is that long-delay learning will occur in situations in which there is minimal concurrent interference with the association of the events of interest, the conditioned and unconditioned stimuli in Pavlovian conditioning experiments. Concurrent interference is said to occur when either the CS or the US of interest becomes associated with other stimuli in the situation. In the typical long-delay taste-aversion learning experiment, subjects are exposed to only one novel flavor, followed by the toxin US several hours later. There is little opportunity for concurrent interference in such a procedure because there are no prominent stimuli other than the toxin with which the novel taste can become associated. Similarly, there are no prominent stimuli other than the novel taste that can become easily associated with the toxin US. (The various nongustatory stimuli animals are likely to encounter during the delay interval are not easily associated with toxicosis.) In contrast to conditioning with toxicosis, there are many opportunities for concurrent interference in conditioning with cutaneous shock. Most situations involve a continually changing array of audiovisual and tactile cues as the animal moves about, and all of these stimuli can be easily associated with shock to provide concurrent interference for the conditioning of an aversion to the conditioned stimulus of interest. The long-delay learning effect in taste-aversion conditioning is predicted by the concurrent interference theory from the fact that there is a limited number of stimuli that can be easily conditioned with toxicosis. Revusky (1971, 1977c) has referred to this selectivity of association as a relevance principle, and has suggested that long-delay learning should be evident in all situations that involve relevance principles. He further suggested that in addition to the taste-toxicosis relevance principle, there is also situational relevance. According to the situational relevance principle, events that occur in an experimental chamber are not very likely to become associated with events that occur outside the experimental chamber (such as in the home cage), and vice versa. The concurrent interference theory, together with the principle of situational relevance, predicts that animals will associate events that occur in the same experimental chamber with one another even if a long delay separates the events. What is required is that the animals be removed from the experimental chamber during the delay interval. Consistent with this prediction, several experiments have demonstrated learning with a long delay introduced between the discriminative stimulus and reinforcement and between the response and reinforcement in

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runway and T-maze situations when animals spend the delay interval outside the experimental chamber (see Revusky, 1977c, for a review). However, the delay interval was never as long in these experiments as the intervals that can support long-delay taste-aversion learning. For example, in one intertrial association experiment (Pschirrer, 1972), the delay interval was about 15 min, and in a delay of reinforcement experiment the longest delay interval tested was 60 min (Lett, 1975). Furthermore, a conditioning effect was often not evident in these studies until extensive training had been provided. Learning was not evident with a 60-min delay between response and reinforcement in the T-maze until the rats received more than 30 rewarded trials (Lett, 1975). In a black-white discrimination experiment with about a 4-min delay between discriminative stimulus and reinforcement (Revusky, 1974), learning was not evident until subjects received more than 300 trials. In contrast to the above efforts to obtain learning with long delays between a response or discriminative stimulus and reinforcement, one-trial long-delay learning of positive affective responses is possible if special procedures are employed. In one experiment (D’Amato and Buckiewicz, 1980), Cebus monkeys were first tested for their baseline side preference in a T-maze. During conditioning, they were confined to the nonpreferred arm for 1 min, than placed in a holding cage for the delay interval (30 min), and finally returned to the start area of the T-maze to receive the food reward. This procedure increased their preference for the arm of the T-maze that had been paired with food. One-trial spatial preference learning has been also obtained in rats with as long as a 2 hr CS-US interval when the CS exposure during conditioning was 40 min and the animals received the sucrose US in a novel waste basket instead of the T-maze or the home cage (D’Amato, 1980). These are intriguing findings. However, further empirical and theoretical analysis of these procedures is needed before a detailed comparison with long-delay taste-aversion learning can be made. The fact that long-delay associations are not easy to demonstrate in situations that do not involve poison avoidance is not conclusive evidence that unique learning processes are involved. In many demonstrations of long-delay learning distinctive tastes were used to signal toxicosis. Because taste stimuli have temporal-intensity patterns that are very different from the temporal-intensity characteristics of other types of stimuli, it is possible that long-delay tasteaversion learning reflects these unique stimulus features and not the operation of unique learning processes (cf. Krane and Wagner, 1974; Testa, 1974). However, long-delay ingestional aversion learning has also been observed in situations in which distinctive visual cues signal toxicosis (e.g., Braveman, 1977; Martin and Bellingham, 1979; Wilcoxon, 1977). The visual cues in these studies did not have the temporal-intensity pattern characteristic of tastes. Therefore, the unique stimulus features of taste cannot be used to explain long-delay visual aversion learning.

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Much has yet to be discovered concerning the mechanisms of long-delay visual-aversion learning. For example, we do not know whether all visual cues can become readily associated with toxicosis or only visual features of ingested foods. We also do not know whether the mechanisms of visual-aversion learning are the same as the mechanisms of taste-aversion learning. It will be exciting to witness the resolution of these issues in the coming years and to see whether long-delay poison-avoidance learning in fact turns out to be mediated by unique conditioning mechanisms. References Barker, L . M., Best, M. R., and Domjan, M. (eds.). 1977. “Learning Mechanisms in Food Selection.” Baylor Univ. Press, Waco, Texas. Batson, I . D.. and Best, P. J. 1979. Drug-preexposure effects in flavor-aversion learning: Associative interference by conditioned environmental stimuli. J . Exp. Psychol. Anim. Behav. Proc. 5 , 273-283. Best, M. R. 1975. Conditioned and latent inhibition in taste-aversion learning: Clarifying the role of learned safety. J. Exp. Psychol. Anim. Behav. Proc. 1 , 97-1 13. Best, M. R., and Barker, L. M. 1977. The nature of “learned safety” and its role in the delay of reinforcement gradient. In “Learning Mechanisms in Food Selection” (L. M. Barker, M. R. Best, and M. Domjan, eds.), pp. 295-317. Baylor Univ. Press, Waco, Texas. Best, M. R.,and Batson, J. D. 1977. Enhancing the expression of flavor neophobia: Some effects of the ingestion-illness contingency. J . Exp. Psychol. Anim. Behav. Proc. 3, 132-143. Best, M. R., and Domjan, M. 1979. Characteristics of the lithium-mediated proximal US pmxposure effect in flavor-aversion conditioning. Anim. Learn. Behav. 7 , 433-440. Best, P. J., Best, M. R., and Mickley, G. A. 1973. Conditioned aversion to distinct environmental stimuli resulting from gastrointestinal distress. J . Comp. Physiol. Psycho/. 85, 250-257. Bitteman, M. E. 1975. The comparative analysis of learning. Science 188, 699-709. Bitterman, M. E. 1976. Flavor aversion studies. Science 192, 266-267. Braveman, N. S. 1975a. Formation of taste aversions in rats following prior exposure to sickness. Learn. Motiv. 6 , 512-534. Braveman, N. S. 1975b. Relative salience of gustatory and visual cues in the formation of poisonbased food aversions by guinea pigs (Cavia porcellus). Behav. Bio. 14, 189-199. Braveman, N. S . 1977. Visually guided avoidance of poisonous foods in mammals. In “Learning Mechanisms in Food Selection” (L. M. Barker, M. R . Best, and M. Domjan, eds.), pp. 455-473. Baylor Univ. Press, Waco, Texas. Braveman, N. S. 1979. The role of blocking and compensatory conditioning in the treatment preexposure effect. Psychopharmacologia 61, 177- 189. Brower, L. P., Brower, J. V. Z., and Corvino, J. M. 1967. Plant poisons in a terrestrial food chain. Proc. Narl. Acad. Sci. U.S.A. 57, 893-898. Cannon, D. S., Berman, R. F., Baker, T.B., and Atkinson, C. A. 1975. Effects of preconditioning unconditioned stimulus experience on learned taste aversions. J. Exp. Psychol. h i m . B e h v . Proc. 1, 270-284. Carroll, M. E., Dinc, H. I., Levy, C. J., and Smith, J. C. 1975. Demonstrations of neophobia and enhanced neophobia in the albino rat. J . Comp. Physiol. Psyrhol. 89, 457-467. Clarke, J. C., Westbrook, R. F., and Irwin, J. 1979. Potentiation instead of overshadowing in the pigeon. Behav. Neural B i d . 25, 18-29. Corey, D. T. 1978. The determinants of exploration and neophobia. Neurosci. Biohehav. Rev. 2, 235-253.

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D’Amato. M. R. 1980. Paper presented at the Binghamton Symposium on Memory Mechanisms in Animal Behavior. State University of New York at Binghamton, June 10-12. D’Amato. M. R.. and Buckiewicz. J . 1980. Long-delay, one-trial conditioned preference and retention in monkeys (Cebus apella). h i m . Learn. Behav., in press. Deutsch. R. 1978. Effects of atropine on conditioned taste aversion. Pharmacol. Biochem. Behav. 8, 685-694. Domjan, M. 1973. Role of ingestion in odor-toxicosis learning in the rat. J . Comp. Phvsid. Psychol. 84, 507-52 1. Donijan, M. 1975. Poison-induced neophobia: Role of stimulus generalization of conditioned taste aversions. Anim. Learn. Behav. 3, 205-21 1 . Domjan, M. 1976. Determinants of the enhancement of flavored-water intake by prior exposure. J. Exp. P.rvchol. Anini. Behm. Proc. 2 , 17-27. Domjan, M. 1977a. Attenuation and enhancement of neophobia for edible substances. h i “Learning Mechanisms in Food Selection” (L. M. Barker, M. R. Best, and M. Domjan, eds.), pp. 151-180. Baylor Univ. Press, Waco, Texas. Domjan, M. 1977b. Selective suppression of drinking during a limited period following aversive drug treatment in rats. J . Exp. Psychol. Anim. Behav. Proc. 3, 66-76. Domjan, M. 1978. Effects of proximal unconditioned stimulus preexposure on ingestional aversions learned as a result of taste presentation following drug treatment. Ai7in7. L m m . Behuv. 6, 133- 142. Domjan, M.. and Best, M. R. 1977. Paradoxical effects of proximal unconditioned stimulus preexposure: Interference with and conditioning of a taste aversion. J. Exp. Psycho/. Anim. Behav. Proc. 3 , 310-321. Domjan, M., and Gemberling, G. A. Effects of expected vs. unexpected proximal US preexposure on taste-aversion learning. Anirn. Learn. Behar.. 8, 204-210. Domjan, M., and Gillan, D. J . 1976. Role of novelty in the aversion for increasingly concentrated saccharin solutions. Physiol. Behav. 16, 537-542. Domjan, M., and Wilson, N. E. 1972a. Contribution of ingestive behaviors to taste-aversion learning in the rat. J. Con7p. P h y i o l . Psychol. 80, 403-412. Domjan, M., and Wilson, N. E. 1972b. Specificity of cue to consequence in aversion learning in the rat. Psychoti. Sci. 26, 143-145. Dragoin, W.. Hughes, G., Devine, M., and Bently, J. 1973. Long-term retention of conditioned taste aversions: Effects of gustatory interference. Psychol. Rep. 33, 51 1-514. Durlach, P. J., and Rescorla, R. A. 1980. Potentiation rather than overshadowing in flavor-aversion learning: An analysis in terms of within-compound associations. J . Exp. Psycho/. h i m . Behav. Proc. 6 , 175-187. Galef, B. G . , Jr., and Osbome, B. 1978. Novel taste facilitation of the association of visual cues with toxicosis in rats. J. Comp. Physiol. Psycho/. 92, 907-916. Gamzu, E. 1977. The multifaceted nature of taste-aversion-inducing agents: Is there a single common factor‘? I n “Learning Mechanisms in Food Selection” (L. M. Barker, M. R . Best, and M. Domjan, eds.), pp. 477-510. Baylor Univ. Press, Waco, Texas. Garcia, J. 1978. Mitchell, Scott. and Mitchell are not supported by their own data. Anini. Leorn. be ha^ 6, I 16. Garcia, J , , and Ervin, F. R. 1968. Gustatory-visceral and telereceptor-cutaneous conditioning: Adaptation in internal and external milieus. Commun. Behuv. Biol. 1 (Pan A), 389-415. Garcia, J.. and Kimeldorf. D. J. 1957. Temporal relationship within the conditioning of a saccharin aversion through radiation exposure. J. Comp. Phy,siol. Psychol. 50, 180-183. Garcia, J . . and Koelling, R. A. 1966. Relation of cue to consequence in avoidance learning. Psychon. Sci. 4, 123- 124. Garcia, J., and Koelling. R. A. 1967. A comparison of aversions induced by X-rays. toxins, and drugs in the rat. Rudiar. Res. Suppl. 7, 439-450.

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ADVANCES IN THE STUDY OF BEHAVIOR VOL. I I

The Functional Organization of Phases of Memory Consolidation R . J . ANDREW ETHOLOGY AND NEUROPHYSIOLOGY GROUP SCHOOL OF BIOLOGICAL SCIENCES UNIVERSITY OF SUSSEX BRIGHTON, UNITED KINGDOM

I Phases of Memory in Higher Vertebrates: Evidence from Amnestic Agents A. One or More Phases of Memory Formation'?

I1 111 1V V

VI

,

...

B. Amnesia: Disruption of Consolidation or of Retri C. Sequential Dependence of Phases of Memory . . Human Memory . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Models of Memory Formation . . . Previous Studies of Memory, Using Pecking in the Chick ............... Hormones and Other Enhancing Agents in the Chick: Opposition to Amnestic Agents . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . A . The Enhancement of Normal Memory in the Chick.. . . . . . . . . . . . . . . . . B. Phases of Memory in the Chick. . . . . . . . . . . . . . . . .......... C. Testosterone and Retrieval Processes ............................. Conclusion: General Implications . . . . . . . . . . References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

338 339

344 345 341 348 350 352 354 357 359 36 1 363

There is little agreement as to the functional properties and interrelation of different phases of memory formation; their possible number, and even the existence of genuinely different phases, have been matters for dispute. A major difficulty in the interpretation of mammalian studies, as will be seen, is the considerable variation in estimates of even the most basic property of such hypothetical phases: their duration in time. Much of this variation is undoubtedly due to differences of species or strain, and to differences in task or in testing procedure, and it is clearly necessary to standardize all of these to a far greater extent than in the past, if separate studies are to be collated and interpreted fully. One instance in which this has to some extent been done is that of a task based on the inhibition of spontaneous pecking in the domestic chick. A comprehensive and well-supported model of memory formation already exists (Gibbs and Ng, 337

Copyright @ 1980 by Academic Ress. Inc. All rights of reprnduction in any form resewed ISBN 0-12-a)4511-7

338

R. J . ANDREW

1977), based on this task; it convincingly defines a series of phases in memory formation, which are sequentially dependent, so that the disruption of one causes subsequent phases to fail to establish. In this article, I examine some of the main issues raised by studies of memory formation in mammals in the light of evidence from the chick. Recent work in my laboratory has demonstrated brief sharply timed transitions between phases, which can be defined not only by time courses of susceptibility to, or survival under, amnestic agents, but also by changes in the vulnerability of the trace to interference from subsequently established traces. Earlier work on the effects of testosterone on attention had suggested that these might depend upon increased stability of information in a short-term memory store. Effects of the hormone on the different phases of consolidation were therefore sought: almost all (and not just the earliest) proved to be affected. However, the timings of most of the main transitions are unaffected; this, and the character of the changes themselves, suggests that the hormone is acting upon a mechanism external to the stores in which the consolidating trace is held; I argue that this mechanism may be important in retrieving and sustaining information. I.

PHASES OF MEMORY IN HIGHER VERTEBRATES: EVIDENCE FROM AMNESTIC AGENTS

The main measures with which I will deal here, and in the later sections devoted to work on memory in the chick, are the persistence in time, following a brief and precisely timed learning event, of ( a ) susceptibility to various agents or manipulations, and ( b ) forgetting subsequent to the application of the agent or manipulation, or in its continuing presence. Estimates of these time courses vary greatly, and are certainly affected by variables such as intensity of the agent, and sensitivity of the test, as well as varying between strain and species (McGaugh and Herz, 1972). Thus by increasing test sensitivity a considerable extension of the period of susceptibility to electroconvulsive shock (ECS)can be obtained (McGaugh and Dawson, 1971), while susceptibility to ECS can be extended from much less than 5 sec after training to more than 30 min by increasing the intensity of current and shifting its site of application on the cortex (Gold et al., 1973b). Indeed, some authors (e.g., McGaugh and Gold, 1974) have taken the robust view that variability is so great and of such a type (i.e., it is sensitive to intensity of agent or to effectiveness of reinforcer) that either no useful conclusion can be drawn from such evidence as to the duration of memory processes, or a single process of consolidation must underlie memory formation, with traces becoming progressively more resistant to disruption. It is certainly impossible to use such evidence to prove or disprove any of the models of memory formation considered later. However, there do seem to be

MEMORY CONSOLIDATION

339

typical values for both susceptibility and survival which differ between agents, and some at least of the markedly discrepant values can be given special explanations. My aim in this section will be to show what likely hypotheses are raised by the existing evidence, and then to turn, in later sections, to a large body of data from the chick in which time courses involving widely different types of manipulations, but all based on the same standard test, can be compared. It will be convenient to divide this section into three parts: ( a ) how many phases of memory formation are there likely to be; ( h )do the usual amnestic agents act by disturbing consolidation or by making subsequent retrieval impossible; and ( c ) are memory phases sequential, in the sense that information can reach a later phase only by passage through the immediately previous one? A.

O N E OR

MOREPHASES

OF

MEMORY FORMATION?

The amnestic agents commonly in use are often (and perhaps rightly) assumed to have obvious central consequences which ensure that their main central effects should be on distinct phases of memory formation. Electroconvulsive shock (ECS) is assumed to disrupt patterns of neuronal firing (e.g., Kesner, 1973); the induction (or reversal) of changes at synapses such as might normally provide the first basis of storage following neural activity has also been suggested (Flood et al., 1977). Anesthetics and similar agents should interfere with the processing of information, while protein synthesis inhibitors should block the final establishment of structural changes. In fact, as might be expected of such powerful agents, both ECS and protein synthesis inhibitors have other effects which could affect memory formation. Thus, for example, ECS depresses protein synthesis significantly, if only moderately (Dunn, 1971); inhibition of protein synthesis may inhibit tyrosine hydroxylase and thereby depress monoamine systems (Flexner ef al., 1973; Flexner and Goodman, 1975). It is perhaps not likely that the main effects of these agents are to be explained in these ways; thus inhibition of tyrosine hydroxylase alone does not produce amnesia (Squire et a/., 1974), while the production of amnesia correlates well with the attainment of high levels of inhibition of protein synthesis (McGaugh and Gold, 1974). However, it is clearly impossible to assume that each group of agents always acts by the most obvious route and only by that route. The duration of susceptibility to ECS is typically no more than 30 sec to 1 min after learning, and is often less (Table I). However, even without obvious special conditions (see following), times as long as 6 hr have been reported (Kopp et al., 1966), and McGaugh and Herz (1972) note that the more extended periods of susceptibility tend to be found in studies in which more sensitive test procedures were used. The classical position, that susceptibility to ECS defines an initial very short phase in which memory is sustained by neural activity alone, is thus

TABLE I DURATIONOF SUSCEPTIBILITY TO AND SURVIVAL OF AMNESIC AGENTS"~

Agent I . ECS At 8 sec At 20 sec

Animal Mouse

Rat

Reference

Still susceptible

No longer susceptible

17 19 19

0 min

11 15 12

30 min 6hr

30 min

5 sec

10 sec

10 sec

30 sec

15-30 sec

60 sec

Surviving

Lost

5 rnin

< I hr Ihr

6 hr

1-2 hr?

8 High punishment

LOW punishment 23 18 Test

Short Long Subconvulsive Convulsive 2. ECS

Chick

20 16

Several seconds Ihr 15 min 0-10 sec

30 sec

3 0 4 0 sec 50 sec

+ special conditions

Inhibition of protein synthesis Deprivation of REM sleep

Mouse

11

9 hr (duration of inhibition)

17

3hr 2 days

9

6 hr

3. Anesthetics

Ether

Mouse

14

I

Rat

2 21

5 min 24 min 24 hr 5 min

15 min 24 min

10 min

30 rnin

Halothane Sodium pentobarbital NO

co

2

Concussion

Chick

7 27 21

Rat Mouse Mouse Man

25 26

Chick

6

Mouse

4

5

0 20 min 10 min

0 30 min 30 min

1.5 hr 40 min 20 min 15 min 60 min

4. Convulsant ether

Flurothyl

5. Protein synthesis inhibitors Cycloheximide

Anisomycin Acetoxycycloheximide

Mouse

Chick Chick Mouse

24 23 Low punishment High punishment 3 13 13

3

4 min, 64 min, 24 hr. according to dose 6hr 3 hr

10-20 min 20 min

0

10

Puromycin Puromycin on cortex

3 10

11-60 days

30-45 min 30-45 min 30 min

6hr 1 min

6hr

24 hr

3hr

6hr

3hr 5h r 15 min 10-20 hr

6hr 5hr 3hr c 20hr

“The latest times at which there was susceptibility or survival are given, together with the fmt at which there was not. The studies considered here were chosen because they gave relatively clear timings of susceptibility or survival. They were: 1. Abt eral. (1961); 2. Alpem and Kimble (1967); 3. Barondes and Cohen (1968); 4. Bohdanecky eral. (1%8); 5. Bovet er al. (1966); 6. Cherkin (1969); 7. Cherkin and Lee-Teng (1965); 8. Choroverand Schiller (1965); 9. Fishbeinetal. (1971); 10. Flexnerera/. (1%7); 11.Floodetal. (1977); 12.GellerandJarvik(1968); 13.GibbsandNg(1977); 14. Herz(1969); 15.Kopp era/. (1966); 16. Lee-Teng(1970); 17. Linden etal. (1975); 18. McGaugh and Dawson(l971); 19. McGaugh and Landfield (1970); 20. Miller and Springer (1971); 21. Pearlman et al. (l%l); 22. Quartermain and McEwen (1970); 23. Quartermain eral. (1%5); 24. Squire and Barondes (1972); 25. Taber and Banuazizi (1966) 26. Weissman (1%7); 27. Zinkin er al. (1976). “High punishment” and “low punishment” refer to levels of footshock during training; it will be Seen that high footshock reduces the duration of susceptibility but extends that of survival. Flurothyl, as a convulsant ether, is considered separately from anesthetics. Fuller information on the chick is given in Table 111.

342

R . J . ANDREW

under challenge, and can be maintained, with some danger of circularity of argument, only by assuming that unusually long susceptibility times either represent secondary effects of ECS or have some other special explanation. There is in fact good evidence that considerable extension of susceptibility can result from manipulations such as deprivation of paradoxical sleep or sustained inhibition of protein synthesis (Table I), and that susceptibility is sustained only until a little after the end of the resulting special state (Fishbein et al., 1971; Flood et al., 1977); however, whatever the nature of this state, it seems unlikely that a trace could be sustained continuously for many hours or even days by neural activity alone. One explanation which avoids this problem is that of “reminder” or “reactivation” effects, which are discussed later: briefly, by presenting stimuli associated with training, the trace set up at training can be made once again vulnerable to amnestic agents, which would otherwise be quite ineffective. Since procedures such as handling are very likely to occur both at training and at any subsequent manipulation (such as administration of ECS) any aberrantly long period of susceptibility might be argued to be explicable in this way. Two remaining groups of amnestic agents, anesthetics and protein synthesis inhibitors, have been held to define two further phases of memory formation (Booth, 1970). A variety of anesthetics have yielded rather similar values for duration of susceptibility, between 10 and 30 min, although here too there are exceptional much larger values (Table I). It seems very likely that there is a real difference between these agents and ECS. It is less certain that any difference has as yet been established between anesthetics and protein synthesis inhibitors. The very extended periods of susceptibility to puromycin applied to the cortex (to 60 days: Flexner et a l . , 1967) are probably best considered entirely separately. Puromycin is known to cause potent central changes such as the release of abnormal peptides, in addition to inhibition of protein synthesis (review, Cohen, 1970). Deutsch (1971), using cholinergic agonists and antagonists, has demonstrated systematic changes in susceptibility (and retention) over weeks after learning, so that much longer term changes than those considered in this article may well be important; how far puromycin effects are of this type, rather than depending on reminder or similar effects, remains to be seen. Duration of survival offers another means of distinguishing different groups of amnestic agents (Table I); for obvious reasons, there is little or no such information for anesthetics. Memory often survives ECS for up to l hr. Protein synthesis inhibitors, on the other hand, rather typically allow survival for 3-5 hr; puromycin on the cortex is again aberrant (Table I). It is worth noting that the hypothesis that all amnestic agents act on the same process of consolidation, which becomes more resistant to disruption as it proceeds, would predict that the most potent agents would have the longest periods of susceptibility and the shortest periods of survival. In fact, both seem to be longer in the case of inhibitors of protein synthesis than in that of ECS (Table I). The value of comparison is reduced here

343

MEMORY CONSOLIDATION

by the wide variety of conditions under which the data were obtained; however, a similar relationship will be shown later to hold in the chick for a variety of agents applied under identical conditions. Estimates of duration of susceptibility after learning to agents that enhance learning suggest that this is typically possible for 15-30 min (Table 11). This agrees well with similar estimates for susceptibility to anesthetics and to protein synthesis inhibitors, and supports the hypothesis that a phase of lability of the trace is replaced by a more permanent state, perhaps half an hour after learning. Estimates of susceptibility to enhancing agents suggest a rather similar course of events after reminder (Table 11). The same agents oppose amnesia due to ECS and to protein synthesis inhibitors: here susceptibility tends to be for longer periods (e.g., 1-3 hr, Table 11). If genuine, this difference may be compared to the extension of susceptibility to ECS during the period of action of anisomycin which has already been noted; unlike the latter, it cannot be due to synergism between two agents with basically TABLE I1 OF SUSCEPTIEII.ITY .TO ENHANCING AGENTS"~' DURATION

Agent

Animal

Reference

Mouse

6 2 13 3 12 9, 1 1

Measure of enhancement

Not Susceptible susceptible

I . After learning

Strychnine Amphetamine Vasopressin Strychnine

Flurothyl Pentylentetrazol Physostigmine Corticosteroids ACTH. norepinephrine Brain stimulation 2. After reminder Brain stimulation Strychnine

7 8

2 hr Opposition to ECS Opposition to CXM 3 hr Opposition to ECS I hr Increased use of redundant cues 0 I hr Improved learning 30 min Improved learning 4-16 min Improved learning 15 min Improved learning 15-25 min Improved learning Improved learning 150 min 0 improved learning

Rat

5

Improved learning

30min

60min

Rat Rat

5 9

Improved learning Improved learning

30min 15 min

60min 30min

Rat Mouse Rat Chick Mouse Mouse Mouse Rat

4

10 1

3 hr

6 hr

2 hr

30 min 210 min 2 hr

"The latest times at which there was susceptibility to enhancement are given, together with the first at which there was not. The studies considered here were chosen because they gave relatively clear timings. They were: 1 . Alpern and Mariott (1973); 2. Barondes and Cohen (1968); 3. Brennan and Gordon (1977); 4. Cherkin er al. (1975); 5 . Devietti ef a/. (1977); 6. Duncan and Hunt (1972); 7. Flood et al. (1978); 8. Gold and van Buskirk (1976);9. Gordon(1977); 10. KrivanekandMcGaugh(1968); 1 I . McGaugh(l966); 12. McGaughandKrivanek ( 1970); 13. Pfeifer and Bookin ( 1978). 'Brain stimulation was in the midbrain reticular formation.

344

R . J . ANDREW

similar effects. It suggests instead an unusual persistence of a labile phase from which transition to a more permanent state remains possible. The chick data, which will be presented later, also indicate a transition to a more permanent state (which in this case can be accurately timed) at about 30 min, with another important transition, this time gradual, over 40-90 min. Indeed, it could be argued that in this respect at least, consistency between studies done in different species and under different conditions is at least as obvious as the variability, which is undoubtedly also present. DISRUPTION OF CONSOLIDATION OR OF RETRIEVAL? B. AMNESIA: There has been some confusion of terms in this controversy, which remains an active one. Interference with retrieval has sometimes been taken to mean disturbance of mechanisms responsible for retrieval, and sometimes interference with the establishment of stored information allowing the retrieval of a particular trace (see Spear, 1973, who distinguishes ‘‘retrieval processes” and the “effectiveness of retrieval”). Here we will be concerned only with the second (which might very well be a consequence of the first, induced at an appropriate time during memory formation). It should be noted that where clear gradients of susceptibility subsequent to learning have been demonstrated, amnesia cannot be due to a disturbance of retrieval mechanisms, which clearly continue to be effective at test despite the administration of the agent. Consolidation is sometimes held to have occurred once the transition from the (hypothetical) initial phase based on neural activity has occurred (e.g., Lewis et al., 1969). Alternatively, it may be used of all phases up to the final transition to “permanent” memory (e.g., Cherkin, 1969, 1972). I have used the term in this second sense. The main lines of evidence whose interpretation is in dispute are recovery from amnesia, and the reappearance of susceptibilityto amnestic agents after ‘‘reminder” of training. Recovery suggests that a trace may be unavailable without being lost. A subsidiary dispute centers around the significance of failure to demonstrate recovery, since it is always possible to argue that another approach might have produced evidence of some retention despite amnesia. Gold (Gold and King, 1974; Gold et af., 1973a) has argued that the demonstration of recovery and of reminder commonly requires the provision of further information in a form that amounts to retraining. This is certainly often tme of reminder procedures, while even spontaneous recovery commonly is demonstrated after repeated testing. Gold and other theorists (e.g., Cherkin, 1969; Mah and Albert, 1973), who argue that amnestic agents interfere with consolidation, explain evidence of some survival of memory after apparently complete amnesia as due to “weak” or “subthreshold ’ ’ traces. Miller and Springer (1974) rightly emphasize that the strength of a trace is only

MEMORY CONSOLIDATION

345

apparently a simple concept: it might involve more information, greater redundancy of the same information, or increased availability of information. It seems likely that, when pressed to a conclusion, the distinction between effects on consolidation and retrieval has meaning only if a memory trace depends on information held in two different types of store: one representing the main body of information, and the other holding information necessary for the retrieval of the main trace. Such a distinction cannot be justified by the available animal evidence, although Weiskrantz ( 1966) has argued strongly for defects of retrieval information in human amnesia; it does provide a framework within which the processing and retrieval of information can be discussed more clearly. Lewis (1976) has emphasized the probable importance of an early phase of memory in which such processing occurs, and has argued (Lewis er ul., 1969) that the reason why familiarization with the training apparatus markedly attenuates the effectiveness of ECS given just after training is that such familiarization greatly abbreviates the processing needed before an organized trace can be stored. Another phenomenon, which is commonly taken to show that amnestic agents can act on availability for retrieval (i.e., on the storage of information for use in retrieval) is that of “reminder” or “reactivation.” Many studies have shown that the presentation of the reinforcer used in training (e.g., footshock, Springer and Miller, 1972), or conditioned stimuli (e.g., tone, Misanin ef ul., 1968) or specific features of the training apparatus or problem (Bregman et d.,1976; Meyer, 1972) may render a memory once again susceptible to amnestic agents (ECS in the examples previously given), even many hours or days after learning. Reminder may also allow enhancement (preceding and Table 11). Amnesia following reactivation, coupled with the application of an amnestic agent, is commonly interpreted as due to a disruption of subsequent retrieval. It does seem most likely that it is retrieval information that is affected, but vulnerability of the main trace cannot be excluded, until the phenomenon is much better understood.

c.

SEQUENTIAL

DEPENDENCE OF PHASES

OF

MEMORY

If, as seems probable, consolidation is divisible into two or more phases, dependent on differing neuronal states (and so sensitive to different amnestic agents), then the simplest way in which they might be related is that of strict sequential dependence. This would mean that each phase was dependent on the previous one for its formation, and could not be set up from any other source. Such phases could well be successive states of the same populations of neurons, with each state providing conditions necessary for the initiation of the next; they need not (although they could) represent functionally different stores, as far as their role in the handling and accessibility of information.

346

R . J . ANDREW

If the whole of a phase were sensitive to a particular amnestic agent, then survival in the presence of that agent would be likely to be shorter than susceptibility to it (Fig. 1A and B). On the whole (Table I) reported survival times are longer than reported duration of susceptibility; this is also true for the chick over a wider range of agents (see following). This can be accommodated without giving up serial dependency, either by extending the overlap between phases until the first phase ends after the end of the second phase (Fig. lC), or by confining sensitivity to the beginning of each phase (Gibbs and Ng, 1977; Fig. 1D).The latter alternative is the only one adequately to explain the data for the chick; it also agrees with the data already presented. However, it remains perfectly possible to argue that memory formation may involve functionally different stores which operate in parallel. Kesner (1973) has argued for a specific model of which this is true. An initial store, which depends

FIG.1. A number of ways are shown in which duration of susceptibility to a particular agent might be greater than (A and B), less than (C and D), or equal and coupled to (El and &) the duration of survival in the presence of the agent. The period for which the trace is sensitive to the agent is shown by hatching; in A-C, it is assumed that the whole of one phase is sensitive, as might be the case if the agent affected the process by which the trace was held, while in D and E, only a period of formation is sensitive. The duration of susceptibility is shown as slightly shorter than the true period of sensitivity, in order to allow for a delay between administration of the agent and the beginning of effective central action. In general, where the whole of each stage is sensitive (A-C), survival times should be longer than susceptibility times. This is not true of the arrangement shown in C, which is, however, an unlikely one. When only the initial part of each phase is sensitive (D) it is more likely that susceptibilitytimes will be longer. The special case shown in E is suggested when susceptibility and survival times are the same, and respond similarly to manipulation.

MEMORY CONSOLIDATION

347

upon neural activity, establishes traces separately in short-term, and in long-term memory. Such establishment is believed to be very rapid, particularly in the case of short-term memory, so that ECS (which is assumed to affect only neural activity) will not prevent short-term memory from establishing, unless it is given as training ends. If short-term memory establishes but not long-term, then survival will be observed up to a point at which traces are normally lost from short-term memory. This argument depends on the assumption that ECS does not produce effects which persist for some time, and so might block some process necessary for subsequent passage from one phase of memory to the next. However, there is other evidence consistent with parallel processing: Kesner and Conner ( 1974) found that stimulation of the hippocampus immediately after training resulted in memory which appeared to decay over 3-4 min, whereas stimulation of the midbrain reticular formation produced immediate apparent amnesia, with evidence of memory appearing after a few minutes. They argue that in the first case long-term, and in the second short-term memory is disrupted, and that (if so) the two are clearly capable of independent establishment.

II. HUMANMEMORY One of the few safe comparisons that can be made between human and animal studies of memory is the susceptibility gradient of amnesia for events preceding concussion in man. Retrograde amnesia can extend up to 30 min before concussion (Weissman, 1967) which, perhaps by coincidence, agrees well with animal estimates for agents like anesthetics. There is little evidence from studies of verbal memory and little current support from theorists in this area for decay over time as a process of fundamental importance in normal human forgetting (e.g., Crowder, 1976). This is perhaps to be expected, since if reminder effects in animals d o represent a reactivation of a memory trace, almost all human verbal memory tasks are likely to involve repeated reactivation (and so interruption of any decay processes), as material is manipulated in memory. Equally important is the fact that so much closely comparable verbal material is held in human memory that ability accurately to retrieve is likely to be of crucial importance. Therefore, it is worth mentioning one phenomenon in verbal memory which does seem to have a predictable time course, which is measured in minutes, even if it cannot as yet be easily explained. When retention scores for verbal items are compared in paired-associate tests for items that produced a marked, or little or no galvanic skin response, scores are initially poor for the first and then improve, whereas the reverse is true for the latter (Walker, 1958; Kleinsmith and Kaplan,

348

R . J . ANDREW

1963). The crossover is at about 15 to 20 min after learning, and a stable state is reached by about 45 min. A variety of types of explanation have been suggested, of which perhaps the most interesting is that a marked GSR indicates high degree of processing (Kahneman, 1973); it is probable that correlation between serial position in the list and GSR is not important (Kleinsmith and Kaplan, 1974). For our purposes the chief point of importance is the suggestion of a shift from dominance of one type of store or process to another somewhere between 15 and 45 min after learning the list. There is good evidence for decay in initial very short-term stores: thus loss seems to be very marked over 1 sec or less for both visual stimuli (iconic store: Sperling, 1960, 1967) and auditory stimuli (echoic store: Darwin el al., 1972; Howell and Darwin, 1977). These times are perhaps comparable with susceptibility to ECS in animals that are very familiar with the apparatus in which learning has just occurred (see previously). If all visual information passes through a store or stores with such rapid decay, then it must be possible to establish a very complex trace very rapidly, since human memory for complex scenes is remarkably capacious and retentive (e.g., Standing et al., 1970) even in normal subjects who lack eidetic imagery (e.g., Haber and Haber, 1964). An alternative might be parallel processing of the sort suggested by Kesner on animal evidence (see previously). The next store or system following the very short-term stores that have just been considered seems to have limited capacity. Baddeley (Baddeley and Hitch, 1974; Baddeley er al., 1975) has suggested that this system may function as a working memory with a “central processor” of limited capacity, and associated buffer stores (e.g., for verbal material) which may have only brief retention in time. One way of combining such a system, for which there is much evidence, with the possibility of entry to permanent memory of a very detailed description of a briefly perceived but complex visual stimulus would clearly be parallel entry to working memory and to a long-term store. Working memory could then have the establishment of means of retrieval as one role.

III. MODELSOF MEMORY FORMATION It may be helpful at this point to summarize the main types of model that are serious contenders at present. A single trace with progressively increasing resistance to disruption does not seem usefully to cope with the evidence already reviewed. On the whole, there is little theoretical interest in such a model. One current model (that of Gold and McGaugh, 1975) has been termed “single-trace”; it is nevertheless a two-phase model. It assumes that after a trace is set up, it will decay and be lost, unless “nonspecific” (i.e,. not holding specific information about learning) modulating

MEMORY CONSOLIDATION

349

processes cause its storage. Effectively, this amounts to a labile phase and a permanent phase of meory. The nonspecific modulating processes that, on this model, determine whether storage occurs themselves would often arise at the time of learning: thus they would be initiated by appropriate reinforcement at learning. The way is clearly open to postulate increased information content in these processes (e.g., how far was reinforcement contingent on a stimulus or response involved in learning), and thereby bring the model nearer to models involving parallel stores. However, as formulated, central agents such as hormones (see following), concomitants of increased arousal, and aftereffects of reinforcement are argued to be critical in modulation of storage. Models with two or more phases which are sequentially dependent have the advantage that they are reasonably straightforward (in theory) to test, as long as relatively precise timings can be assigned to each phase. In the next section, the model of this sort developed by Gibbs and Ng (1977) for the chick will be examined in more detail. Parallel stores have been postulated in order to account for temporary survival of memory after, or in the presence of, an amnestic agent (see preceding). It may well prove to be the case that a store whose contents do not automatically consolidate, and which operates in parallel to the stores leading to permanent memory, is responsible for holding information required only in the short term; however, once such a parallel store is postulated testable predictions about the duration of survival and susceptibility become extremely hard to frame. It is necessary to make a variety of firm assumptions (e.g., which store will provide information at retrieval, when will information pass from the parallel store to the stores leading to permanent memory, which store is affected at a particular time by a particular amnestic agent), none of which can be justified by experimental evidence. Better justification for considering a parallel store of some sort comes from human evidence for a working memory with limited capacity. If information used in retrieval is really established separately from the trace proper in animals, then this too would argue for a parallel memory system of some sort. The best strategy seems to be to push a strictly sequential multiphase model to its limits, giving as precise temporal and physiological properties as possible to each successive phase. Only if a real inadequacy can be demonstrated in such a model is it sensible to assume in addition a parallel store. Information processing is clearly important in the establishment of a trace: Lewis (1976) has argued that the duration of the early phase susceptible to ECS may be dependent on the extent to which this is required. It is therefore crucial to be able to define stages of memory formation from evidence based on the handling of information, and to compare this with evidence from amnestic agents. A beginning to such work has been made in the chick work to be reviewed later.

350

R. I . ANDREW

Iv.

PREVIOUS STUDIES OF

MEMORY, USING PECKING CHICK

IN THE

Cherkin and Lee-Teng (1 965) introduced inhibition of spontaneous pecking in the young domestic chick as a result of an,unpleasant taste associated with the pecking target, as a simple standard passive avoidance task. It has the advantage that it requires no preliminary training, so that there is no ambiguity as to the point in time at which relevant learning occurred. Cherkin ( 1 969) replaced the original ill-tasting substance (n-propanol) by a new one, methyl anthranilate, which then became standard. Gibbs (Gibbs and Barnett, 1976; review, Gibbs and Ng, 1977) changed the target from a microminiature lamp to a metal or colored bead, so that at retention test discrimination between a bead of the color used in avoidance training (“aversive”) and a bead of another color (“neutral”) could be tested. She also housed her chicks in pairs (Mark and Watts, 1971; Watts and Mark, 1971), a change which proved to have a marked effect on some time courses (Gibbs and Ng, 1977), and gave a pretraining session using metal beads (two trials with a small bead and one with a large one), so as to reduce the proportion of birds, whose training is disturbed by fear of the bead. The timing and character of pretraining sometimes has important effects on memory formation, and will be considered further in later sections. Cherkin (1970) has argued that amnesia for this task, when induced by flurothyl (a convulsant ether, given as the vapor), probably involves disruption of consolidation, on the grounds that there is no recovery of memory even after 9 days (and good retention in control trained animals). Flurothyl amnesia was also resistant to “reminder” by presentation of a target coated with a dilute solution of methyl anthranilate in water (Cherkin, 1972), which was not in itself capable of producing permanent inhibition of pecking. It is worth noting that this evidence of permanent and complete amnesia was obtained with chicks whose training was not preceded by any pretraining with similar targets. Different results might be obtained in chicks allowed “familarization ” (see previously) before training. Much shorter, and more clearly defined susceptibility after training was obtained for enhancement (Cherkin er a [ . , 1975). The effectiveness of training was reduced by using dilute methyl anthranilate; the enhancing agent, flurothyl, this time in very low concentration, was effective only to 16 min. Gibbs and Ng (1977) define three sequentially dependent phases of memory (“short-term memory,” “labile memory,” and “long-term memory”), on the basis of work by Gibbs and her colleagues (see Mark and Watts, 1971 ;Watts and Mark, 197 l), using three groups of amnestic agents, administered systematically or by freehand injection bilaterally into the forebrain. Although the present article will not consider the sort of physiological mechanisms that may be involved in such phases, it may be helpful to note that the first group (glutamate, 1

35 1

MEMORY CONSOLIDATION

or 2 m M KCl) is argued to interfere with hyperpolarization, the second group (ouabain, ethacrynic acid) is sodium pump inhibitors, and the third group [anisomycin, cycloheximide (CXM), and a-arninoisobutyrate (AIB)] interferes with protein synthesis or with the uptake of amino acids necessary for synthesis. All of the agents were applied over a wide range of times relative to training, so as to establish a time course of susceptibility from a point sufficiently far before training as to render the agent ineffective, to a corresponding point after training. Since all agents were effective at some time after as well as before learning, direct effects on learning can be excluded as important in subsequent performance; since all agents ceased to be effective at relatively clearly defined times in relation to training, but well before retention tests, direct effects at test are also unlikely to be important. Duration of both susceptibility and survival is relatively standard for each group of agents (Table 111). This is particularly clear for inhibitors of protein synthesis (Group 111), where both anisomycin and cyclohexirnide gave similar TABLE Ill THREEGROUPS OF AMNESTIC AGENTSI N Agent I

I1

Ill

llla

Task'

LiCl Ouabain

B B B

Ouabain (high dose) Ouabain Ouabain Ethacrynic acid CXM CXM Anisomycin AIB

B AW PF B B PF B B

KCI

THE

CHICK""'

Susceptibility (-10)

(-10) (-30)

- 5 to +2.5 ( + 5 ) - 5 to ?+2.5 (+5) - 1 5 to + 5 ( + l o )

+

(+ 10) further loss

?

+ 10

to +30 ( + 30)

-5 (I - 10"

(-15) (-45) (-45) (-10)

Survival

- 5 t 0 +5(+10) -30 to +20 (+30, ?45) - 10'' -30 to +20 (+30,?45) - 5 to +2.5/5 ( + l o )

O? +5 10/15,

+ 10" + 10" + 10 +30

+60" +30 +30

(+5)

(+ 15) (

+60190)

( + 120)

(+60) ( + 60/90)

"The data are taken from Gibbs and Ng (1977). and are for chicks of mixed sex. housed in pairs (and so not in an altered physiological state due to isolation stress), and untreated with hormones. The doses for which data are shown are 20 pl 2 mM KCI, 20 p1 154 mM LiCI, 0.4 pg ouabain, 0.6 p g ouabain (high dose), 1 .O pg ethacrynic acid, 20 pg cycloheximide (CXM), 20 p g anisomycin, 20 pl 250 m M a-aminoisobutyrate (AIB). All were given bilaterally intracranially. "Times before training are shown as negative. Limiting times at which the agent was no longer effective, or loss was complete are shown in parentheses. "B, Standard bead with methyl anthranilate task (test); AW, aversive wheat task learn to avoid aversive tasting red wheat in 30 sec exposure; PF, pebble floor: learn to discriminate food grain from stuck down pebbles in C 5 min exposure. Measured from beginning of task. 'Measured from end of task.

'

352

R.

J . ANDREW

values, which in the case of cycloheximide varied little over a wide range of doses (20-300 pg: Watts and Marks, 1971; Gibbs and Ng, 1977). Further, AIB (Gibbs and Ng, 1977) and L-proline (Gibbs et al., 1977), which are believed to interfere with specific protein synthesis by a different route, namely, by competing for transport with amino acids normally used in synthesis, also yield similar survival times. Their periods of susceptibility are the same as those of Group I (glutamate, KCl), which Gibbs and Ng (1977) explain by postulating that amino acids needed for subsequent synthesis are taken up during the phase of formation defined by Group 1 agents. The two Group I1 agents, ouabain and ethacrynic acid, also yield almost coincident estimates of susceptibility and survival, although here there is some hint that survival times are somewhat sensitive to concentration of ouabain (Table 111). However, there is no suggestion of overlap with Group I11 times. Group I shows rather more variation in survival time, since 2 mM KCl yields either no survival or survival over 1 or 2 min, while LiCl allows some survival for at least 5 min. Times for Group I and Group I1 are sufficiently close (particularly considering that the resolution interval is in general itself 5 min) to suggest that the two groups might perhaps be acting on the same phase of memory but by slightly different routes. However, the most obvious possibility, namely, that Group I has a longer latency, can be excluded since, as Gibbs and Ng (1977) point out, they have a very brief duration of action as estimated from the time course of susceptibility before training. It thus seems very probable that the two groups of agents act on different phases of memory. A striking feature of the data is that for each group of agents (with the possible exception of Group I) duration of survival consistently exceeds that of susceptibility. This can be explained, as already noted (Fig. ID), with sequentially dependent phases, if amnestic agents act only at the beginning of each phase, presumably during its formation (Gibbs and Ng, 1977; Fig. 3A). However, this hypothesis leaves open the physiological basis for that part of each phase that is not sensitive, and thereby weakens the argument that the trace itself is represented, at least at the beginning of each phase, by a neuronal state sensitive to one of the three groups of amnestic agents. Instead, it could be that mechanisms involved in the establishment of each phase (e.g., in transfer of information from one store to another) are sensitive. The sequential dependence of successive phases would remain the same in both cases. V.

HORMONES A N D OTHER ENHANCING AGENTS IN OPPoSITION TO AMNESTIC AGENTS

THE

CHICK:

For some time (Murphy and Miller, 1955; De Wied, 1964) hormones such as ACTH have been known to affect the acquisition and extinction of avoidance tasks. Later work showed that the effects are not specific to avoidance training: they can be obtained with either food or access to a sexual partner as reward

MEMORY CONSOLIDATION

353

(Bohus er al., 1977). Recent, not necessarily contradictory interpretations of the effects of MSH, and ACTH or ACTH analogs have included “improvement of selective attention” (Sandman and Kastin, 1977) and improvement of retrieval andlor consolidation processes (van Wimersma Greidanus and de Wied, 1976; van Wimersma Greidanus er al., 1978). Gold and Van Buskirk (1976) showed that epinephrine and ACTH apparently could promote consolidation when given immediately after learning. In the case of steroid hormones, Flood ef af. (1978) have demonstrated enhancement of retention by corticosteroids given after training in poorly trained mice, and Gold and McGaugh (1 975) suggested more generally that hormones such as ACTH, vasopressin, and epinephrine might promote storage. Comparable effects in the chick are suggested by the marked extension of time courses of survival of amnestic agents when chicks were stressed by isolation, rather than being housed in pairs (Gibbs and Ng, 1977, and following). Here, I will be concerned chiefly with effects of testosterone on memory formation, although it should be noted that this is only one (albeit the most effective, except for estradiol, see Section V , A) of the steroid hormones that are effective in this way. Enhancement of memory formation can be demonstrated in the chick both by opposition to amnestic agents and by effects on normal memory formation; in this section, I will consider only the first type of effect. Testosterone (given as the free steroid, in dimethylacetamide, typically 10 pg/40 gm male chick) extends both susceptibility to and survival under ouabain. In our hands (Andrew and Stephenson, 1981) the two times are the same, both in control and in testosterone-treated chicks: in the first the times are greater than 5 and less than 10 min, and in the second greater than 15 and less than 20 min. There is some discrepancy with the times already noted for controls in another laboratory (Gibbs and Ng, 1977), of 5-10 min for susceptibility and greater than 10 min for survival, and the reason for this is not yet known.’ However, it is clear that survival and susceptibility are coupled in their response to testosterone, even if this coupling may be relaxed under other circumstances. If ouabain is acting directly on the trace, then such coupling of the durations of susceptibility and survival suggests that the ouabain-sensitive period is very brief, and is postponed by testosterone (Fig. 1E). An alternative possibility, which would be consistent with the data, is that it is not the trace itself, but a mechanism responsible for transfer of the trace from one store to another, which is sensitive to ouabain. Testosterone also extends survival in the presence of CXM (Gibbs er al., 1981). The survival time is determined by the time, not from training, but from injection; testosterone remains effective for between 4.5 and 5.5 hr according to ‘Slight differences in overall timing are not unexpected in a measure sensitive to hormonal state. It may be that survival is slightly longer than susceptibility in all three cases: it would be expected to be longer by the time required for ouabain to begin to act (Fig. l ) , for example. Given a resolution interval of 5 min a slight difference might be revealed only when a test fell at a crucial point.

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dose. A similar estimate of duration of effectiveness is obtained from tests using enhancement of normal learning, such as are described in Section V,A. The processes underlying the loss of effectiveness are discussed elsewhere (Gibbs et al., 1981); here, it is important only because it allows the demonstration of an unusual state, in which the trace surviving the inhibition of protein synthesis can be sustained or held available for many hours, and yet is not permanently stored. Thus, a second injection of testosterone prolongs the lifetime of the trace, as long as it is given before the end of effectiveness of the first. A.

THEENHANCEMENT OF NORMAL MEMORY IN THE CHICK

Messent (1973) observed that, when first exposure to, and pecks at a target (a colored bead mounted on a wire) occurred after the administration of testosterone, such pretraining interfered with avoidance training, using a similar target coated with methyl anthranilate and given immediately afterward; without pretraining testosterone had no effect on behavior. Control animals never showed any interference with avoidance training. Andrew et al. (1981) confirmed the effect, and showed that interference occurred only when a bead identical in appearance with that used at training, was also used in pretraining. Testosterone was found to be effective only if given within a certain minimum time of pretraining. Its timing in relation to training, on the other hand, was not important: if it was not given in time to affect the consolidation of pretraining, then its presence at training (or testing) did not change behavior. Although I will deal here only with testosterone, it should be noted that it has been possible using this test to construct dosage curves for a wide range of of steroids (Rainey, unpublished): the two most effective proved to be testosterone and estradiol (threshold dosages la0 and 10 nglchick, respectively). The marked specifity of the interference between traces of training and pretraining suggested that this test might offer a way of studying the course of consolidation under conditions more normal than in the presence of amnestic agents, It also promised to allow the study of transfer of information, rather than changes in the physiological state of a trace. The basic procedure was to vary systematically the interval between pretraining and training. A somewhat similar approach has been taken by Spear and his colleagues (Spear et al., 1972; Spear, 1973), using interference between initial passive avoidance training and subsequent active avoidance training. If the two training trials are separated only by 1 min, interference with the second task is marked; with a longer interval ( 1 hr) interference is only slight. However, even with such longer intervals, there may be an effect on the long-term survival or availability of learning based on the second trial. With 1 hr between the training trials, active avoidance is remembered well at a test 1 hr subsequently, but shows considerable interference from passive avoidance 24 hr later (Gordon and Spear, 1973). In the chick experiments (Clifton et al., 1981) testosterone was given before

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pretraining, since it was essential that it should have begun to act at the time of pretraining, if short intervals between pretraining and training were to be studied. Birds with differing intervals between pretraining and training fell into three groupings. Over the time range 10 sec to 2 min, pretraining dominated, in that birds (when tested 3 hr after training) tended to peck aversive type beads as much as neutral beads. From 3 to 25 min, training dominated at test and the aversive bead was not pecked, while at times of 30 min or greater, pretraining again dominated. Control groups withheld pecks in consequence of training whatever the interval between pretraining and training. The range of 10 sec to 2 min is of particular interest, since it suggests that once testosterone has begun to act, it affects the ability of the pretraining trace in the first few seconds of its life to compete with the establishment of subsequent training trace. The reasons why there should be three periods in the formation of a trace under enhancement by testosterone in which its competitive ability should differ so much are still a matter for speculation. The most reasonable working hypothesis seems to be the following. The outcome of the interaction, which the data indicate must occur between traces relating to the same stimulus, is assumed to depend upon the relative stability of the two traces. The first phase would be explained if information initially were to be held in a very short-term store, in which it decays very rapidly (as in the case of the human iconic or echoic stores), and from which it enters a store, within which traces are given increased stability by testosterone. As a result, the training trace, with only a brief time in which to enter, would be at a double disadvantage. Clearly, if this is so, loss of the training trace should be immediate with no period of survival: this is confirmed by the absence of any measurable inhibition of pecking 2 rnin after training (which is as close as testing can reasonably be taken without being greatly affected by direct aftereffects of training such as lingering taste in the mouth). The transition at between 2 and 3 rnin corresponds roughly but not perfectly with the end of susceptibility to Group I amnestic agents (between 2.5 and 5 min); it may be that these agents act on the store that has just been postulated (store 2 in Fig. 2B). The training trace may be given advantage during the second period in the life of the pretraining trace, because transfer from store 1 to the next store is a one-way traffic. As a result, the entering trace is likely to be at an advantage, since its basis remains secure during interaction. The third transition may indicate the point at which the pretraining trace changes state and becomes permanent, in the sense of becoming capable of resisting subsequent interaction with the training trace. This is not true of control birds, and it must therefore be assumed that the effects of testosterone during consolidation in some way give continuing advantage to the pretraining trace, once it passes into a permanent state. There are at least two points in time at which such a change in state might

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I

I

I

I

I

60

30rnin STM

A

I11 ,;'/L,

=- _J _L

- -/.;'*/:;'

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LM

,,

:'- -- -

I

I

I

I

10

20

30

40

,

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FIG. 2. The sequentially dependent stages of consolidation postulated by Gibbs-Ng model. ES, Stage sensitive to ECS; STM,short-term memory; LM, labile memory; LTM, long-term memory. The periods of establishment of each phase, when the trace is sensitive to a particular group of amnestic agents, are indicated by hatching. The agents effective in each case are shown by Roman numerals: I, Group I (agents such as 2 mM KCI);11, Group 11 (ouabain and ethacrynic acid); 111, Group I11 (protein synthesis inhibitors). (B) Part B incorporates the sharply defined transition suggested by evidence from trace interaction experiments at 2/3 and 25/30 min. Points of sensitivity to amnestic agents are shown in the same way as in A. Since in the case of the transition between established short-term memory (3) and the next stage, it is possible that it is the transfer mechanism that is sensitive to ouabain; this is indicated by hatching in the m o w . The same convention is used for the transfer to long-term memory, which is shown as sensitive to sotalol (S). The stages of memory are numbered in order to provide a simple means of reference, without any undesired implications; they are equivalent to the following stages of A: 1, ES; 2, formation of STM, here an entirely separate stage; 3, established STM; 4, formation of LM, if this is present as a sensitive period;5 , established LM; 6, LTM. LTM is not shown as divided, although processes of structural change presumably continue through this time, and there is probably a shift of retrieval to LTM as stage 5 ends. A period of preparation for stage 6 is tentatively indicated as the place of action of protein synthesis inhibitors (111). The main sites of action of testosterone are indicated by T. They include the stabilization of traces in stage 2, the postponement in time of the transition from stage 3 to the next stage, the prolongation of stage 5 (when stage 6 is blocked), and late effects on the consolidation of the trace in stage 6. This last effect (measurable as increased effectiveness of the permanent trace in competition with subsequently established traces) can be obtained after the transition at 25/30 min. It may be due to an effect on stage 5 , if the contents of stage 5 continue to transfer to, or interact with, stage 6; alternatively, it may represent a direct effect on stage 6.

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occur. The most obvious is a little less than 30 min after the setting up of the pretraining trace. This corresponds closely with a very sharp end of susceptibility to sotalol (a P-adrenergic antagonist) which has its maximum effect in the chick 25 min after avoidance training, falling to little or no effect at 30 min (Stephenson and Andrew, in preparation). However, it is also possible that the crucial change in state occurs at a later gradual transition to permanent memory. It is necessary to assume in addition that, as long as they do not interact in the earliest phases of consolidation of the pretraining trace, the two traces consolidate independently until the training trace reaches this final transition, and that the training trace (presumably because associated with reinforcement) consolidates more effectively. It might then be that when 30 or more min separate pretraining and training the training trace has already become more stable than the pretraining trace when interaction begins (P. Clifton, personal communication). It is not at present possible to resolve this question; on balance the first explanation seems the more likely, since it is not clear that the second would be expected to yield the same crossover point in competitive advantage in all of a large group of chicks as would be needed to generate the sharp transition observed. The independent evidence of a sharp transition between 25 and 30 rnin also favors the first alternative. The technique of opposing two traces has provided further evidence about the handling of information in the successive phases of memory formation. Store 1 proves to have unusual properties (Andrew et al., 1981). If a blue bead is used in pretraining, in chicks that have been treated with testosterone, then it normally does not have any effect on subsequent avoidance training using a red bead. However, when the interval between pretraining and training is 1 or 2 min, there is full interference despite the difference in color; the transition to the normal lack of interference is sharp, occurring as the interval between pretraining and training is lengthened to 2-3 min (Clifton, unpublished). This result agrees well with the hypothesis that when the pretraining trace is still in store 1, the training trace is not allowed to establish at all. It also suggests that information handling in this phase of memory has a limited processing capacity, much as in human working memory.

B. PHASESOF MEMORYI N

THE

CHICK

It is now possible to pull together the various lines of evidence that help to define phases of memory in the chick. The main features of the Gibbs-Ng model (Fig. 2A) are confirmed by the new evidence which has been reviewed here. It will be easiest to consider the changes and extensions of the model that have been postulated here by taking each stage in turn (Fig. 2B). Little is known of the first stage, which is included because of evidence

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(Lee-Teng and Sherman, 1966; Lee-Teng, 1970) that susceptibility to ECS extends in the chick to about 30 sec. Gibbs and Ng (1977) also found it necessary to postulate a stage prior to that sensitive to Group I amnestic age-nts in order to explain temporary survival of such agents (e.g., Benowitz and Speny, 1973). On the Gibbs-Ng model stage 2 is the period of formation of short-term memory (sensitive to Group I agents). Its end coincides quite well with that of the period in which the resident pretraining trace' is able, when stabilized by testosterone, to exclude the training trace; it seems best therefore to distinguish it as a period spent in a store with special functional properties. Stage 3 (established short-term memory on the Gibbs-Ng model) ends with a probably brief period of transfer or change of state (here indicated as 4); either a mechanism necessary for transfer or the trace itself as it establishes in the next phase is sensitive to Group LI agents during this period. Testosterone postpones the transfer or change of state. Stage 5 (established labile memory), it is here argued, is divided into two periods by a sharply timed transfer that introduces the trace into long-term memory (stage 6), but does not terminate stage 5. This transfer probably occurs a little less than 30 min after learning: it can be detected both as the point at which the trace becomes more resistant to displacement or change, and as the time immediately after which sensitivity to the &antagonist sotalol suddenly ceases. Like the transition between stages 2 and 3, its timing is not affected by testosterone. The end of stage 5 is probably revealed by the progressive loss of the pace, which can be observed when the establishment of long-term memory is blocked. In chicks unaffected by testosterone or other hormones, all agents bringing about such blockage (CXM,anisomycin, AIB, Gibbs and Ng, 1977; sotalol, Stephenson, unpublished) yield roughly similar survival times, with progressive loss between 30 and 60 to 90 min. The timing of the end of stage 5 is affected by testosterone little, if at all, under one set of circumstances: when establishment of the training trace in long-term memory is prevented by the prior establishment there of the pretraining trace, rendered more effective by testosterone, the training trace once again shows progressive loss between 30 and 60 to 90 min (Clifton et al., 1981). One special feature of this last case deserves emphasis. It will be remembered that it requires that pretraining (in the presence of testosterone) and training be separated by 30 min or more. Training results in a trace reaching and entering state 5 ; with an appropriate interval between pretraining and training the pretraining trace is then still present in that stage (as well as in long-term memory, stage 6), and is presumably displaced or reshaped by the training trace. From then until the end of the life of the training trace in stage 5 , it is evidently retrieved at test in preference to the pretraining trace, which is simultaneouslyresident in long-term

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memory. The simultaneous presence of two contradictory traces in different stages of memory is of particular interest in that it shows that parallel storage without final permanent consolidation is possible, albeit so far demonstrated only under rather special circumstances. The timing of the end of stage 5 is affected by testosterone under one set of conditions, namely, when the establishment of long-term memory is blocked by Group I11 agents. In the presence of such a blockage, testosterone extends survival of the trace, presumably in stage 5 , for as long as it (testosterone) remains effective. Why this might be is considered in Section V,C.

C. TESTOSTERONE A N D RETRIEVALPROCESSES Testosterone has been shown to affect almost every stage of memory formation; it is not obvious what sort of direct action on the neuronal basis of the trace could explain this, and it seems worthwhile to examine alternative explanations. The effects of testosterone are broadly comparable in each stage that is affected: stabilization of the trace against interference in stage 2, extension of its life in stage 3, and under some circumstances at least in stage 5 also, and finally increased effectiveness in competition after permanent storage in long-term memory. Despite these extensive changes the times of establishment of stage 3 from stage 2, and of stage 6 from stage 5 , remain unchanged. This is consistent with an action of testosterone not directly on the trace itself, but indirectly through a mechanism that can intervene in each successive stage of consolidation. The effects of testosterone upon attention, as shown in search tests and tests of distractibility (Andrew and Rogers, 1972; Andrew, 1972, 1976), also have some basic features in common with the effects just discussed. Chicks treated with testosterone are much more likely to sustain attention on a particular type of stimulus during search, and are more likely to return to a previous point of attention after distraction. Both types of effect can most readily be explained by increased stability of information held in a short-term store. The increased stability of the consolidating trace in stage 2 is a comparable effect, operating over a similar time scale. The most important difference is that in search and distraction tests, the chick is commonly responding to familiar stimuli (e.g., familiar types of food, position and appearance of the food dish in a familiar runway). If in these tests also, testosterone acts by stabilizing a memory trace, then this trace is likely usually to be one retrieved from permanent memory. This difference, however, may not be a crucial one. The reminiscence experiments, which were discussed earlier, provide strong evidence that once retrieved, traces (or the information used in the retrieval of traces) are subject to the same enhancing (and disrupting) agents as during consolidation. It is not unreasonable

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therefore to suppose that testosterone might sustain retrieved traces, as well as ones consolidating for the first time; how this might occur in either instance is of course the basic issue to be resolved. The only mechanisms that are known to have access to all (or almost all2) phases of consolidation are those concerned with retrieval. Too little is known of the processes of retrieval to allow any unambiguous prediction as to the consequences of such access: it might not affect the character or stability of the trace at all, or it might weaken it rather than stabilize it. The hypothesis set out below begins with the premise that retrieval mechanisms can hold a consolidating trace stable. Its main attraction is that it provides a theoretical framework within which a variety of different effects can be explained, and from which a wide range of testable predictions about the nature of both consolidation and retrieval can be made. It must initially be assumed that when a trace is retrieved, so that its information content is held directly and readily accessible, this involves sustained access to the store in which the trace is then held; this would be long-term memory, except in the case of a consolidating trace. The alternative, here assumed not to be true, is that access is brief, and results in all of the information being duplicated in another bulk store, in which it remains while it is held accessible; in the meantime the trace proper persists in its original state. Testosterone is assumed to increase the time for which a trace is held available, once retrieved. An effect of this sort on traces retrieved from long-term memory provides the most satisfactory explanation for the changes produced by testosterone in search tests and tests of distractibility (see preceding). In the case of a trace based on a salient experience, such as the experiences with beads dealt with here, it seems reasonable to suppose that for some time after the experience, the consolidating trace would be held readily available. It is here assumed that this involves the same mechanisms as are responsible for retrieval from longterm memory, and that testosterone has the same effect of prolonging the time for which the trace is sustained in an available state. Those events that can be precisely timed during consolidation fall into two categories: those whose timing is changed by testosterone, and those that are unaffected by testosterone. The latter (the transitions at 2/3, and at 25/30 min) show that the overall timing of consolidation is unaffected by changes in the mechanism on which testosterone acts. The challenge for the present hypothesis is thus to explain why two other timings should be markedly changed by testosterone. It is important to remember *In both chick (Cherkin, 1971) and mouse (Irwin el al., 1968) there may be brief periods during consolidation, when a trace appears to be difficult to retrieve. Further study of the timing of such periods may shed light on the way in which retrieval mechanisms establish contact with consolidating traces.

MEMORY CONSOLIDATION

36 1

that the evidence for survival in a particular phase of consolidation is usually really evidence that retrieval takes place from that phase. This is particularly clear for survival in stage 5 , where it has been shown that retrieval continues for some time to be from stage 5 , even though a comparable trace has been already established in stage 6. Here, then, it seems reasonable to suppose that “the end of stage 5” actually represents the time at which retrieval mechanisms shift from stage 5 to 6. Indefinite extension of stage 5 (or retrieval from stage 5 ) due to testosterone occurs only if the establishment of long-term memory is blocked: this suggests that the shift does not occur if no trace is available to the retrieval mechanism in the next stage. This is perhaps not unexpected, but if it can be confirmed, it is the first direct evidence that bears on the way in which retrieval mechanisms may determine in which store to search. The retrieval mechanisms then must be assumed to sustain the trace in stage 5 for as long as testosterone continues to affect them; in the absence of testosterone or a similar agent, access to the trace by the retrieval mechanisms is apparently no longer stable enough, so long after learning, to allow the trace to be sustained. The extension of stage 3 by testosterone is more difficult to explain on the present hypothesis. It suggests some special intervention of retrieval mechanisms in a particular early stage of consolidation. The only obvious reason for this is the selection of those features of the trace that are subsequently to serve in its retrieval. Recently we have found that the duration of stage 3 does indeed coincide with the time for which reclassification of the properties of a stimulus, as coded in a trace, can occur (Clifton and Andrew, unpublished). Further study of the effects of testosterone on stage 3 should therefore provide one means of testing the present hypothesis. The final effect that must be considered here is the increased effectiveness of the fully consolidated pretraining trace in competition with subsequent training, which results when consolidation is affected by testosterone. Too little is known of the causes of this increase in effectiveness to say whether it can be explained by the present hypothesis (or some other one). Two main types of explanation are possible: changes in the stability of the trace, and changes in the way it is classified for retrieval, such that interaction with a subsequent trace relating to the same stimulus is made more likely. Further work should show which is correct, and it may then be possible to decide whether this effect too could be caused by a change in the role played by retrieval mechanisms during consolidation.

VI. CONCLUSION: GENERAL IMPLICATIONS The answers to some of the questions posed in the first section of this article are now somewhat clearer, at least for the chick. All of the new evidence is in

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agreement with the most important feature of the Gibbs-Ng model, namely, the sequential dependence of successive stages of consolidation. It now seems likely that at least one of the transitions (that between stages 2 and 3) involves a shift of the trace between stores that differ in their capacity to handle information. The way is now open to characterize other stages in the same way, and to begin comparison with work on human memory (e.g., comparison of stage 2 and human working memory). Some of the transitions are surprisingly sharply timed, suggesting that there may be points during consolidation when the relative timing of two or more events is crucial. The properties of transitions such as that at stage 4 suggest points of manipulation by mechanisms external to the stores in which the trace is held. Some features of a parallel store may also be present: thus stage 5 may hold information which is different from that held at the same time in stage 6, and which is not finally consolidated. The main value of the work on chicks lies in the detail and the preciseness of the temporal structure, which has been established for consolidation. It seems unlikely that consolidation in the chick (or birds in general) differs radically from consolidation in other vertebrates, and in particular in mammals. It is impossible at present to tell how much of the variability in times of survival of, and susceptibility to particular amnestic agents would disappear, if a systematic body of data were available for a particular strain of mouse or rat, studied in a standard physiological state. Certainly even the data reviewed earlier are at least compatible with consolidation processes organized as in the chick, but with timings varying between strains and with variables such as levels of circulating hormones. One feature that may be to some extent peculiar to the chick experiments is the lack of experience of the chicks: nothing in their brief past experience is likely to be closely comparable with any aspect of the bead presentations. It may be that this makes the process of organization and consolidation of the trace much clearer, and perhaps more protracted, since they are starting from scratch. The most fundamental questions raised by the chick data are those of the possible relations between memory and attention. The effects of testosterone on consolidation and on attention suggest, as a hypothesis that deserves further pursuit, the possibility that this and perhaps other hormones act on mechanisms that select, manipulate, and sustain information in short-term stores. Such a hypothesis is not entirely novel: current explanations of the effects of hormones on retention include effects on “selective attention” (Sandman and Kastin, 1977), and the promotion of retrieval, or retrieval and consolidation (Gold and McGaugh, 1975). These different approaches could be reconciled by effects on retrieval mechanisms such as have been suggested here for testosterone. This hypothesis depends on the assumption that the same mechanisms, which select and maintain information within stores, are crucial not only in retrieval but in

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consolidation and in attention. If this is true, then studies of the kind discussed here may eventually turn into studies of thinking in animals.

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Cherkin, A. 1970. Retrograde amnesia: Impaired memory consolidation or impaired retrieval? Commun. Behav. Biol. SA, 183-190. Cherkin, A. 1971. Biphasic time course of performance after one-trial avoidance training in the chick. Commun. Behav. Biol. 5,379-381. Cherkin, A. 1972. Retrograde amnesia in the chick: Resistance to the reminder effect. Physiol. Behav. 8, 949-955. Cherkin, A,, and Lee-Teng, E. 1965. Intenuption by halothane of memory consolidation in chicks. Fed. Proc. Fed. Am. SOC. Exp. Biol. 24, 328. Cherkin, A,, Meinecke, R . O., and Garman, M. W. 1975. Retrograde enhancement of memory by mild flurothyl treatment in the chick. Physiol. Behav. 14, 151-158. Chorover, S. L., and Schiller, P. H. 1965. Short-term retrograde amnesia in rats. J . Comp. Physiol. Psychol. 59, 73-78. Clifton, P. G . , Andrew, R. J., and Gibbs, M. E. 1981. Interference between memory traces in successive phases of consolidation (in preparation). Cohen, H. D. 1970. Learning, memory and metabolic hormones. In “Molecular Mechanisms in Memory and Learning” ( G . Ungar, ed.), pp. 59-70. Plenum, New York. Crowder, R. G. 1976. “Principles of Learning and Memory.” Erlbaum, Hillsdale, New Jersey. Darwin, C. J., Turvey, M. T., and Crowder, R . G . 1972. An auditory analogue of the Sperling partial report procedure: Evidence for brief auditory storage. Cog. Psychol. 3, 255-267. Deutsch, J. A. 1971. The cholinergic synapse and the site of memory. Science 174, 788-794. Devietti, T. L.,Conger, G. L., and Kirkpatrick, B. R. 1977. Comparison of the enhancement gradients of the mesencephalic reticular formation after training or memory reactivation. Physiol. Behuv. 19, 549-554. DeWied, D. 1964. Influence of anterior pituitary on avoidance learning and escape behavior. Am. J . Physiol. Un,255-259. Duncan, N., and Hunt, E. 1972. Reduction of ECS produced retrograde amnesia by post-trial introduction of strychnine. Physiol. Behav. 9, 295-300. Dunn, A. 1971. Brain protein synthesis after electroshock. Brain Res. 35, 254-259. Fishbein, W., McGaugh, J. L., and Swarz, J. R. 1971. Retrograde amnesia: ECS effects after termination of rapid eye movement sleep deprivation. Science 172, 80-82. Flexner, J. B., and Flexner, L. B. 1968. Studies on memory: The long survival of peptidylpuromycin in mouse brain. Proc. Natl. Acad. Sci. U.S.A. 60, 923. Flexner, L. B., and Goodman, R. H. 1975. Studies on memory: Inhibition of protein synthesis also inhibits catecholamine synthesis. Proc. Narl. Acad. Sci. U.S.A. 72, 4660-4663. Flexner, L. B., Flexner, J. B., and Roberts, R. B. 1967. Memory in mice analysed with antibiotics. Science 155, 1377-1383. Flexner, L. B., Serota, R. G., and Goodman, R. H. 1973. Cycloheximide and acetoxycycloheximide: inhibition of tyrosine hydroxylase and amnestic effects. Proc. Narl. Acad. Sci. U.S.A. 70, 354-356. Flood, J. F., Bennett, E. L., Orme, A. E., and Jarvik, M. E. 1977. Protein synthesis dependent gradient of ECS retrograde amnesia. Behav. B i d . 21, 307-328. Flood, J. F., Vidal, D., Bennett, E. I., Orme, A. E., Vasquez, S., and Jarvik, M. E. 1978. Memory facilitatingand anti-amnesic effects of corticosteroids. Pharmacol. Eiochem. Behav. 8, 81-87. Geller, A., and Jarvik, M. E. 1968. The time relations of ECS-induced amnesia. Psychol. Sci. 12, 169-1 70. Gibbs, M.E., and Barnett, J. M. 1976. Drug effects on successive discrimination learning in young chickens. Brain Res. Bull. 1, 295-299. Gibbs, M. E., and Ng, K. T. 1977. Psychobiology of memory: Towards a model of memory formation. Biobehav. Rev. 1, 113-136. Gibbs, M. E., Ng, K. T., and Richdale, A. L. 1977. L-Proline inhibition of long-term memory formation. Neurosci. Lett. 6 , 355-360.

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McGaugh, J. L., and Gold, P. E. 1974. Conceptual and neurobiological issues in studies of treatments affecting memory storage. Psychol. Learn. Moriw. 8, 233-264. McGaugh, J. L., and Herz, M. J. 1972. “Memory Consolidation.” Albion, San Francisco. McGaugh, J. L., and Krivanek, J. 1970. Strychnine effects on discrimination learning in mice: Effects of dose and time of administration. Physiol. Behav. 5 , 1437-1442. McGaugh, J . L., and Landfield, P. W. 1970. Delayed development of amnesia following electroconvulsive shock. Physiol. Behav. 5 , 1109-1 113. Mah, C. J . , and Albert. D. J . 1973. Electroconvulsive shock-induced retrograde amnesia: An analysis of the variation in the length of the amnesia gradient. Behav. Biol. 9, 517-540. Mark, R. F., and Watts, M. E. 1971. Drug inhibition of memory formation in chickens. I. Long-term memory. Pror. R. Sor. London E 178, 439-454. Messent, P. R. 1973. Distractibility and persistence in chicks. Ph.D. Thesis, University of Sussex. Meyer, D. R . 1972. Access to engrams. Am. Psycho/. 27, 124-133. Miller, R. R., and Springer, A. D. 1971. Temporal course of amnesia in rats after electroconvulsive shock. Physiol. B e h v . 6, 229-233. Miller, R . R., and Springer, A. D. 1974. Implications of recovery from experimental amnesia. Psycho/. Rev. 81, 470-473. Misanin, J. R., Miller, R. R., and Lewis, D. J. 1968. Retrograde amnesia produced by electroconvulsive shock after reactivation of a consolidated memory trace. Sciend 160, 554-555. Murphy, J . V., and Miller, R. E. 1955. The effect of adrenocorticotrophic hormone (ACTH) on avoidance conditioning in the rat. J . Comp. Physiol. Psychol. 48, 47-49. Pearlman, C. A., Sharpless, S. K.,and Jarvik, M. E. 1961. Retrograde amnesia produced by anesthetic and convulsant agents. J . Comp. Phvsiol. Psyrhol. 54, 109-1 12. Pfeifer, W. D., and Bookin, H. B. 1978. Vasopressin antagonizes retrograde amnesia in rats following electroconvulsive shock. Pharmacol. Biochem. Behav. 9, 261-263. Quartermain, D., and McEwen, B. S. 1970. Temporal characteristics of amnesia induced by protein synthesis inhibitors: Determination by shock level. Nature (London) 228, 677-678. Quartermain, D., Paolino, R. M., and Miller, N. E. 1965. A brief temporal gradient of retrograde amnesia independent of situational change. Science 149, 11 16-1 118. Sandman, C. A., and Kastin, A. J. 1977. Pituitary peptide influences on attention and memory. In “Neurobiology of Sleep and Memory” (R.R. Drucker-Colin and J. L. McGaugh, eds.), pp. 347-360. Academic Press, New York. Spear, N. E. 1973. Retrieval of memory in animals. Psychol. Rev. 80, 163-194. Spear, N. E., Gordon, W. C., and Chiszar, D. A. 1972. Interaction between memories in the rat: Effect of degree of prior conflicting learning on forgetting after short intervals. J . Comp. Physiol. Psychol. 78, 47 1-477, Sperling, G . 1960. The information available in brief visual presentations. Psychol. Monogr. 74. Sperling, G . 1967. Successive approximations to a model for short-term memory. Acra Psychol. 27, 285-292. Springer, A. D., and Miller, R. R. 1972. Retrieval failure induced by electroconvulsive shock: Reversal with dissimilar training and recovery agents. Science 177, 628-630. Squire, L. R., and Barondes, S. H. 1972. Variable decay of memory and its recovery in cycloheximide-treated mice. Proc. Narl. Acad. Sci. U.S.A. 69, 1416-1470, Squire, L. R . , Kuczenski, R., and Barondes, S. H. 1974. Tyrosine hydroxylase inhibition by cycloheximide and anisomycin is not responsible for their amnesic effect. Brain Res. 82, 241-248. Standing, L., Conezio, J., and Haber, R. N. 1970. Perception and memory for pictures: Single-trial learning of 2560 visual stimuli. Psychol. Sci. 19, 73-74. Stephenson, R. M., and Andrew, R. I. 1981. Amnesia induced by specific fi-antagonists in the chick (in preparation).

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Taber, R . J., and Banuazizi, A . 1966. CO,-induced retrograde amnesia in a one-trial learning situation. Psychophannucolo,?~(Berlin) 9, 382-391 . Van Wimersma Greidanus, T. B., and de Wied, D. 1976. Modulation of passive-avoidance behaviour of rats by intracerebroventricular administration of antivasopressin serum. Behav. B i d . 18, 325-333. van Wimersrna Greidanus, T. B.. Van Dijk, A. M. A,, De Rotte, A. A., Goedemans. J. H. J., Croiset, G., and Thody, A. J . 1978. Involvement of ACTH and MSH in active and passive avoidance behaviour. Brain Res. Bull. 3, 227-230. Walker, E. L. 1958. Action decrement and its relation to learning. Psycho/. Rev. 65, 139-142. Watts, M.E., and Mark, R. F. 1971. Drug inhibition of memory formation in chickens. Il. Shortterm memory. Proc. R. Soc. London B 178, 455-464. Weiskrantz, L. 1966. Experimental studies of amnesia. In "Amnesia" (C. M. Whitty and 0. L. Zangwill, eds.), pp. 1-35. Appleton, New York. Weissman, A. 1967. Drugs and retrograde amnesia. Int. Rev. Neurohiol. 10, 167-198. and Deweer. B . 1976. Retroactive and proactive effects of anaesthesia Zinkin, S., Lecanuet, J.-P., on following in chicks. Physiol. Behav. 16, 185-189.

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Index

A Adaptation among Phocidae and Oteriidae convergent evolution of social structures, 136-138 divergence in geographical distribution, 135-I36 divergence in rearing methods, 133-135 divergences in ways of life, 133 to predation, among Pinnipeds. 128-129 selective association effect and, 308-309 Aggressive behavior, male. hormonal control of, 33-37 Amnesia, memory phases and, 344-345 Anolis carolinensis

behavioral ecology of, 44-45 character displacement in, 48-51 dewlap as species-isolating mechanism, 45-48 behavioral repertoire of, 6-10 biological bases of species-typical behavior patterns in hormonal control of female sexual receptivity, 10-17 hormonal control of male aggressive and sexual behavior, 33-37 neuroendocrine control of male reproductive behavior and gonadotropin secretion, 37-44 sociosexual control of seasonal gonadal recrudescence, 25-33 stimulus control of male mounting behavior, 17-25 natural history of, 3-6 Anolis sagrei, character displacement in, 48-51 Anosmia, effect on suckling, 100-105 Appetitive behavior, ontogeny of, paradoxical reward effects and, 263-265

369

Arousal, development of vocalizations and, 205-208 Associations, selectivity of demonstrations of, 303-307 ingestion as determinant of, 302 interpretations of, 308-317 uniqueness of, 317-318 Aversion learning, see Ingestional aversion learning

B Behavioral context, development of vocalizations and, 202-205 Bird song, 143-144 geographical variation in, 159-160 microgeographical, 160-170 repertoires, 144-145 contribution to survival and reproduction, 146-159 Blocking effect, in ingestional aversion learning, 320-322

C Carnivora, development of vocal behavior and hearing in, 185-189 Cat, development of vocal behavior and hearing in, 185-187 Character displacement, in Anolis carolinensis and Anolis sagrei, 48-51 Chick, memory in normal, 354-357 phases of, 357-359 previous studies of, 350-352 testosterone and, 359-361 Chimpanzee, development of vocal behavior and hearing in, 195-196 Chiroptera, development of vocal behavior and hearing in, 183-185

370

INDEX

Common seal, social plasticity in, 125 Communication, see Bird song; Sound communication Competition, between males, bird song and, 148-154 Crocodilians, reproductive cycle of, 59-6 I

D Dewlap, as species-isolating mechanism, 45-48 Dialects, in bird songs, functions of, 168-170 Discrimination maternal, in ewes, 97 of sound, by infant mammals, 208-209 Dog. development of vocal behavior and hearing in, 187-189

E Elephant seal, social plasticity in, 125 Event covariation, selective association effect and, 313-314 Ewe, maternal behavior in, see Maternal behavior Extinction effects, paradoxical reward effect and magnitude of reward and, 243-249 overtraining and, 255-257 partial reinforcement and, 243-249

Hearing development of vocalizations and, 200-202 of infant mammals, 208-209 time courses of development of, 183 in Carnivora, 185-189 in Chiroptera, 183-185 in primates, 194-198 in rodents, 189-194 Hormonal control of maternal behavior, in primiparous ewes, 111-112 of postparturient maternal responsiveness, 84-87 of species-typical behavior female sexual receptivity, 10-17 male aggressive and sexual behavior, 33-37 Hormones induction of maternal behavior with, 79-80 in nulliparous ewes, I 1 1-1 12 manipulations of, effect on maternal behavior in ewe, 105-106 retrieval processes and, 352-354, 359-361 House mouse, development of vocal behavior and hearing in, 192-194 Human, development of vocal behavior and hearing in, 196-198

F

Felidae, development of vocal behavior and hearing in, 185-187 Frustration theory, as mechanism for paradoxical reward effects, 234-236

G Genetic isolation, microgeographic variation in bird songs and, 165-167 Geographical distribution, divergences among Phocidae- and Oteriidae in, 135-136 Gonadal recrudescence, sociosexual control of, 25-33 Gonadotropin secretion, neuroendocrine control of, 37-44 a e y seal, social plasticity in, 124-125 Guinea pig, development of vocal behavior and hearing in, 189-190

H Habitat, sex ratio and, among Pinnipeds, 123 Habituation, bird song repertoires and, 152-154

I Imitation, of bird songs extent and accuracy of, 160-161 site of, 161-165 Ingestional aversion learning, 276-278 associative-nonassociativecontroversy and, 278-279 aspects which cannot be attributed to sensitization effects of poisoning and, 282284 expectations based on associative interpretations, 279-282 role of neophobia and poison-enhanced neophobia in aversions, 284-292 complexity of ingestive sequence in, 292,303 conditioned aversions to nongustatory cues and, 300-302 nongustatory orosensory stimuli and, 300 odor-aversion learning and, 296-300 selective associations and, 302 taste-aversion learning and, 292-295 future directions in, 326-330

37 I

INDEX limitations on, 318-319 overshadowing, 3 19-320 proximal unconditioned stimulus preexposure, 324-326 relative validity of conditioned stimuli, 320-324 selectivity of associations in demonstrations of, 303-307 interpretations of, 308-317 uniqueness of, 317-318

L Learning aversive, ingestional, see Ingestional aversion learning paradoxical reward effects and, 236-237 behavioral process and, 237-238 species differences and, 239-242 systematic variation and, 238 Learning sets, selective association effect and, 309-313 Lizards, parthenogenetic, reproductive cycle of, 61-65

suckling behavior, 100-106 research prospects in, 113-1 15 Memory, 337-338 hormones and other enhancing agents and, 352-354 normal memory and, 354-357 phases of memory and, 357-359 testosterone and retrieval processes and, 359-361 human, 347-348 models of formation of, 348-349 phases in higher vertebrates, 338-339 amnesia and, 344-345 number of, 339-344 sequential dependence of, 345-347 previous studies of, 350-352 Mimicry, in bird songs, 155-158 Monogamy, among Rnnipeds, I3 I - 133 Mortality, sex ratio and, among Pinnipeds, 129-130 Mounting behavior, male, stimulus control of, 17-25 Mouse, development of vocal behavior and hearing in, 192-194

N M Magnitude of reward extinction effect, paradoxical reward effect and, 243-249 Mammals, sound communication in, see Sound communication Maternal behavior, 76-77 in inexperienced ewes, 108, 112-1 13 in parturition in primiparous and multiparous ewes, 108-1 1 1 role of hormones in primiparous ewes, 111-112 influence of endocrine state of ewe on, 77-79, 87-88 fading of postpartum maternal responsiveness in absence of neonate and, 83-87 induction of maternal behavior in nonpregnant ewes, 79-82 influence of newborn lamb on development of, 88-89, 98-99 characteristics of neonate and, 89-93 information provided by neonate and maintenance of maternal behavior, 93-97 mother-young relationships beyond postpartum period in sheep, 99, 107-108 recognition of young, 106-107

Neonate absence of, fading of postpartum maternal responsiveness in, 83-87 influence on development of maternal behavior in ewes, 88-89, 98-99 characteristics of neonate and, 89-93 information provided by neonate and maintenance of, 93-97 Neophobia, role in ingestional aversions, 284292 Neuroendocrine control, of species-typical behavior, male reproductive behavior and gonadotropin secretion, 37-44

0

Odor-aversion learning, role of ingestion in, 2%-300 Orientation, differential, selective association effect and, 315-316 Overshadowing, in taste-aversion learning, 3 19-320 Overtraining extinction effect, paradoxical reward effect and, 255-257

372

INDEX

P Paradoxical reward effects, 227-234 comparative analysis of learning and, 236-

Primates, development of vocal behavior and hearing in. 194-198

R

237

behavioral process and, 237-238 species differences and, 239-242 systemic variation and, 238 frustration theory as mechanism for, 234-236 implications for behavior and behavior theory ontogeny of appetitive behavior and, 263265

ontogeny of reward leaming and, 265-266 neural substrate of, 257-263 ontogenetic analysis of, 242-243 overtraining extinction effect and, 255-257 partial reinforcement extinction effect and magnitude of reward extinction effect and, 243-249 successive negative contrast and patterned alternation and, 249-255 Partial reinforcement extinction effect, paradoxical reward effect and, 243-249 Patterned alternation, paradoxical reward effect and, 249-255 Physiological state, maternal behavior and, 80-82

Pinnipeds adaptive strategies among convergent evolution of social structures, 136- 138

divergence in geographical distribution, 135-136

divergence in rearing methods, 133-135 divergences in ways of life, 133 social structures of adaptation to Arctic predation, 128- 129 convergent evolution of, 136-138 ecological determinism of, 125-128 effect of sex ratio on sexual dimorphism, 130-131

effect of sex ratio on sexual maturity and mortality, 129- 130 monogamy and polygyny, 131-133 sex ratio and habitat, 123 social plasticity, 123-125 Poison-avoidancelearning, see lngestional aversion leaming Polygyny, among Pinnipeds. 131-133 Predation, adaptation to, among Rnnipeds, 128- 129

Rat, development of vocal behavior and hearing in, 190-191 Rearing methods, divergences among Phocidae and Oteriidae in, 133-135 Recognition of neighbors and kin, bird song and, 154-155 of young, 106-107 Reinforcement, see Paradoxical reward effects Reproduction bird song and, 146-159 male behavior, neuroendocrine control of, 37-44

Reproductive cycle of Anolis carolinensis, see Anolis carolinensis of crocodilians, 59-61 of parthenogenetic lizards, 61-65 of snakes, 5 1-57 of turtles, 57-59 Reproductive isolation, bird song mimicry and, 157- 158

Reward, see Paradoxical reward effects Rodents, development of vocal behavior and hearing in, 189-194

S Sensory pathways, anatomical convergence of, selective association effect and, 308 Sex ratio, among Pinnipeds habitat and, 123 sexual dimorphism and, 130-131 sexual maturity and mortality and, 129-130 Sexual behavior choice, bird song and, 146-148 female receptivity, hormonal control of, 10-17

male, hormonal control of, 33-37 Sexual dimorphism, sex ratio and, among Pinnipeds, 130-131 Sexual maturity, sex ratio and, among Pinnipeds, 129-130 Snakes, reproductive cycle of, 5 1-57 Social structures, of Rnnipeds adaptation to Arctic predation, 128- 129 convergent evolution of, 136-138 ecological determinism of, 125-128

373

INDEX effect of sex ratio on sexual dimorphism, 130-13 1 effect of sex ratio on sexual maturity and mortality, 129-130 monogamy and polygyny, 13 1- 133 sex ratio and habitat, 123 social plasticity, 123-125 Sociosexual control, of species-typical behavior, seasonal gonadal recrudescence, 25-33 Sound communication, 179- 18 1, see also Bird song characteristics and tendencies of development of, 208 adult responsiveness to infant calls, 210213 adult responsiveness and vocal behavior of young, 213-214 infant hearing and discrimination, 208-209 infant responsiveness to adults, 209-2 10 nonacoustic determinants of adult response, 214-216 components of systems, 181-183 development of vocal behavior, 198-199 arousal and, 205-208 external stimuli and behavioral contexts and, 202-205 hearing and, 200-202 physical characteristics of vocal output and, 199-200 time courses of development of, 183 in Carnivora, 185-189 in Chiroptera, 183-185 in primates, 194-198 in rodents, 189-194 Species differences. in paradoxical reward effects, 239-242 Species isolation, dewlap as mechanism for, 45-48 Species-typical behavior hormonal control of female sexual receptivity, 10-17

male aggressive and sexual behavior, 33-37 neuroendocrine control of, male reproductive behavior and gonadotropin secretion, 37-44 sociosexual control of, seasonal gonadal recrudesence, 25-33 stimulus control of, male mounting behavior, 17-25 Stimulus(i) external, development of vocalizations and, 202-205 interfering, in ingestional aversion learning, 320- 324 Stimulus control, of species-typical behavior, male mounting behavior, 17-25 Stumptail macaque, development of vocal behavior and hearing in, 194-195 Successive negative contrast, paradoxical reward effect and, 249-255 Suckling behavior, 100-106 Survival, bird song and, 146-159 Systematic variation, in paradoxical reward effects. 238

T Taste aversion, see Ingestional aversion learning Territoriality, bird song mimicry and, 156 Testosterone, retrieval processes and, 359-36 I Turtles, reproductive cycle of, 57-59

V Vocalization, see Bird song; Sound communication

W Weddell seal, social plasticity in, 123-124

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Contents of Previous Volumes

Volume 1

Volume 3

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

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

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

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

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

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

Physiological and Psychological Aspects of Selective Perception GABRIEL HORN

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

Current Problems in Bird Orientation KLAUS SCHMIDT-KOENIG

Author IndexSubject Index

Habitat Selection in Birds P. H. KLOPFER and J . P. HAILMAN

Volume 4

Author IndexSubject Index

Volume 2

Constraints on Learning SARA J . SHETTLEWORTH

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

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

Breeding Behavior of the Blowfly V. G. DETHIER

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

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

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

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

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

Author 1ndexJubjec.r Index

Author IndexSubjert Index

315

316

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

Functional Analysis of Masculine Copulatory Behavior in the Rat BENJAMIN D. SACHS and RONALD J . BARFIELD Sexual Receptivity and Attractiveness in the Female Rhesus Monkey ERIC B. KEVERNE Prenatal Parent-Young Interactions in Birds and Their Long-Term Effects MONICA IMPEKOVEN

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

Life History of Male Japanese Monkeys YUKIMARU SUGIYAMA

Auihor Index-Subjeci Index

H.PHILIP ZEIGLER

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

Feeding Behavior of the Pigeon Subject Index

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

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

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

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

Ethological Aspects of Chemical Communication in Ants BERT HOLLDOBLER

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

Filial Responsiveness to Olfactory Cues in the Laboratory Rat MICHAEL LEON

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

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

Subject index

Subject index

CONTENTS OF PREVIOUS VOLUMES

377

Volume 9

Volume 10

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

Learning, Change, and Evolution: An Enquiry into the Teleonomy of Learning H. C. PLOTKIN and F. 1. ODLING-SMEE

Feeding: An Ecological Approach F. REED HAINSWORTH and LARRY L WOLF

Social Behavior, Group Structure, and the Control of Sex Reversal in Hermaphroditic Fish DOUGLAS Y. SHAPIRO

Progress and Prospects in Ring Dove Research: A Personal View MEI-FANG CHENG Sexual Selection and Its Component Parts, Somatic and Genital Selection, as lllustrated by Man and the Great Apes R. V. SHORT Socioecology of Five Sympatric Monkey Species in the Kibale Forest, Uganda THOMAS T. STRUHSAKER and LYSA LELAND Ontogenesis and Phylogenesis: Mutual Constraints GASTON RICHARD Subjecr Index

Mammalian Social Odors: A Critical Review RlCHARD E. BROWN The Development of Friendly Approach Behavior in the Cat: A Study of Kitten-Mother Relations and the Cognitive Development of the Kitten from Birth to Eight Weeks MILDRED MOELK Progress in the Study of Maternal Behavior in the Rat: Hormonal, Nonhormonal, Sensory. and Developmental Aspects JAY S. ROSENBLATT, HAROLD I. SIEGEL, and ANNE D. MAYER Subjec,! Index

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