Advances in the Study of Behavior, Volume 14

Advances in

THE STUDY OF BEHAVIOR VOLUME 14

Contributors to This Volume JAMES R. ANDERSON MARTHA K. MCCLINTOCK

HANUS PAPOUSEK MECHTHILD PAPOUSEK HOWARD TOPOFF MICHEL VANCASSEL

Advances in

THE STUDY OF BEHAVIOR Edited by

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

COLINBEER Institute of Animal Behavior Rutgers University Newark, New Jersey MARIE-CLAIRE BUSNEL Laboratoire de Physiologie Acoustique Institut National de la Recherche Agronomique Jouy en Josas (78350), France PETER J. B. SLATEU Ethology and Neurophysiology Group School of Biological Sciences The University of Sussex Brighton, England

VOLUME 14 1984

ACADEMIC PRESS, INC. (Harcourt Brace Jovanovich, Publishers)

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ISBN 0-12-004514-1 PRINTED IN THE UNITED STATES OF AMERICA 84 85 86 87

9 8 7 6 5 4 3 2 I

Contents

Contributors . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Preface . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Announcement . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

vii ix xi

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

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

.. ..... . .. .. . 111. Behavioral Units of Analysis: Robustness and Redefinitions . . . . . IV. New Individual Behaviors . . . . . , . . . . . . . . . . . . . . . . . . . . . . . . . . 11. The Social Pattern of Mating in Groups and Pairs

V. The Social Structure of Mating: Selection within and of Groups. . VI. Classic Mating Behaviors in a Social Context. . . . . . . . . . . . . , . . . VII. Panogamy . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

2 3 8 13 20 32 39 42

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

I. II. 111. IV. V.

Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . The Development of Parental Behavior. . . . . . . . . . . . . . . . . . . . . . The Adaptive Radiation of Parental Behavior. . . . . . . . . . . . . . . . . Relationship between Development and Adaptive Radiation . . . . . The Study of Parental Behavior: Illustration of Which Theories? . References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . V

51 52 58 63 74 78

vi

CONTENTS

Social Organization of Raiding and Emigrations in Army Ants HOWARD TOPOFF I. 11. I11 . IV . V. VI .

Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Phylogeny and Systematics . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Nomadic Behavior and Brood-Stimulation Theory . . . . . . . . . . . . . Behavioral Ecology of Chemical Communication . . . . . . . . . . . . . . Empirical Tests of Brood-Stimulation Theory . . . . . . . . . . . . . . . . . Conclusion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

81 83 85 88 99 120 123

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

I . Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 11. Some Fundamental Principles of Cognitive Integration . . . . . . . . . 111. The Relevance of Dyadic Interactions: Concluding Remarks . . . . . References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

127 130 157 159

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

I. 11. I11. IV . V. Vl . VII . VII1 . IX . X.

/tidf..r .

introduction . . . . . . . . . . . ....................... Where Do Primates Sleep'. . . . . . . . . . . . . . . . ........... Sleeping Sites as a Limiting Resource . . . . . . . . . . . . . . . . . . . . . . . Sharing and Competition for Sleeping Sites . . . . . . . . . . . . . . . . . . Characteristics of Sleeping Sites . . . . . . . . . . . . . . . . . . . . . . . . . . . Traditional Sleeping Sites and Security . . . . . . . . . . . . . . . . . . . . . . Arrival, Sleeping Postures, and Nighttime Activity . . . . . . . . . . . . Social Aspects of Sleeping . . . . . . . . . . . . . . . . . . . . . . . . . . . . Awakening and Leaving the Sleeping Site . . Concluding Comments . . . . . . . . ..... References . . . . . . . . . . . . .......................

.................................................................... Cot7icwr.r of Previous Vnl~rmes ..................................................

166 166 170 174 177 188 194 201 208 215 216

231 235

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

JAMES R. ANDERSON, Department of Psychology, University of Stirling, Stirling FK9 4LA, Scotland (165) MARTHA K. MCCLINTOCK, Department of Behavioral Sciences, University of Chicago, Chicago, Illinois 60637 ( I ) HANUS PAPOUSEK, Developmental Psychobiology, Max-Planck Institute for Research in Psychiatry, 0-8000 Munich-40, Federal Republic of Germany (127) MECHTHILD PAPOUSEK, Developmental Psychobiology, Max-Planck Institute for Research in Psychiatry, 0-8000 Munich-40, Federal Republic of Germany (127) HOWARD TOPOFF, Department of Psychology, Hunter College of the City University of New York, New York, New York 10021, and The American Museum of Natural History, New York, New York 10024 (81) MICHEL VANCASSEL, Laboratoire d Ethologie, LA 373 CNRS, Universite'de Rennes I , 35042 Rennes Cedex, France (51)

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

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s Dr. Peter J. B. Slater of England has been invited to be an Editor and we are pleased that he has accepted the position beginning with this volume. With his appointment we continue to have an English representative. We hope, therefore, to maintain the international representation among both our readers and contributors established by earlier volumes.

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ADVANCES IN THE STUDY OF BEHAVIOR, VOL. 14

Group Mating in the Domestic Rat as a Context for Sexual Selection: Consequences for the Analysis of Sexual Behavior and Neuroendocrine Responses MARTHAK. MCCLINTOCK DEPARTMENT OF BEHAVIORAL SCIENCES UNIVERSITY OF CHICAGO CHICAGO. ILLINOIS

I. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 11. The Social Pattern of Mating in Groups and Pairs . . . . . . . . . . . . . . . . . . . . . A. The Sequence of Copulation . . . . . . . . . . . . . . . . . . . . . . . . . 111. Behavioral Units of Analysis: Robustness and Redefinitions A. The Ejaculatory Series . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

A.

B. C.

Male Rece Female So Female Intercep

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

2 3 3 7 8 8 10 13 13 13 19 19

V.

VI.

The Social Structure of Mating: Selection within and of Groups A. Intrasexual Selection: Competition. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . B. Intersexual Selection: Mate Choice . . . . . . . . . . . . . . . . . . . . . . . . . . . . . C. Cooperation. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . D. Sexual Selection at the Group Level.. . . . . . . . . . . . . . . . . . . . . . . . . , . Classic Mating Behaviors in a Social Context.. . . . . . . . . . . . . . . . . . . . . . . . A. Multiple Intromissions and Multiple Ejaculations. . . . . . . . . . . . . . . . . . B. Male Postejaculatory Quiescence. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . C. Sensory Regulation of Copulation .............

. . . . . . . . . ............................ ..................... References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . , . , 1

20 21 26 28 30 32 32 33 34 38 39 39 40 42

Copyright Q 1984 by Academic Press. Inc. All rights of reproduction in any form reserved ISBN 0-12-0345 14-1

MARTHA K . MCCLINTOCK

I.

INTRODUCTION

In the rat (Rattus nonpegicus), behavior and neuroendocrine function are reciprocally linked in the control of reproduction. Species-typical mating behavior is the product of underlying neuroendocrine mechanisms. In turn, the neuroendocrine events necessary for ovulation, ejaculation, sperm transport, and implantation are triggered or modulated by specific patterns of copulatory behavior. There are many aspects of this reciprocal relationship that are puzzling, if not paradoxical. Some of the confusion may stem from a focus limited to the study of rats mating in pairs. Although domestic rats are sometimes bred in pairs, it is not the social context which most breeders generally use. More commonly, rats have been selected for high reproductive output when they mate in groups (Charles River Breeding Laboratories, Inc., In lirt.). Therefore, the study of rats in groups may resolve some of the seemingly paradoxical aspects of behavior and neuroendocrine function. Domestic rats are clearly adapted to group living. Even when there is room for dispersal in a cage, they often huddle together in a corner (see Fig. 1). They can recognize individuals and establish a variety of social relationships within the group, including dominance (Barnett, 1975). Therefore, given that a group is one of the social contexts in which the mating system of the Sprague-Dawley strain has been selected, it is likely that social relationships are an important factor in determining the individual’s pattern of copulation. Thus, an analysis of the social control of copulation will be an integral part of understanding the reciprocal relationship between individual behavior and neuroendocrine function. The breeding practices of some breeders have inadvertently imposed sexual selection at both the individual and the group level. At the individual level, mating in a group presents the opportunity for two forms of sexual selection: competition and mate choice. Females are subjected only to this level of sexual selection. Although a female conceives in a group along with several other females, she does not remain with these same females throughout her reproductive lifespan. Her reproductive performance can be monitored on an individual basis because the maternity of her litters is obviously always known. Therefore, if a female conceives and delivers a full set of healthy pups, she is eventually returned to the breeding colony and placed with the first available group. Maies. on the other hand, are selected at both the individual and the group level. Sexual selection is imposed at the group level when males are kept together as a group throughout their reproductive lives and remain in the breeding colony or get discarded solely on the basis of their reproductive output as a group. Presumably, discarding the entire group is more cost effective than determining which member, if any, is responsible for a decrease in the number of offspring sired by the group as a whole. Nonetheless, this does have the effect of

GROUP MATING IN THE DOMESTIC RAT

3

FIG. 1. A huddle or pile-up of domestic rats living in a group cage.

group selecting males for reproductive performance (albeit in a weak form; Arnold and Wade, personal communication). It is this sex difference in the breeding practices that represents a form of sexual selection at the group level. The purposes of this article are therefore twofold. The first is to use the social context of group mating to reevaluate the units of behavior that are appropriate for the study of mating behavior and neuroendocrine function in the Norway rat. The second purpose is to evaluate the ways that sexual selection at both the individual and the group level is mediated by copulatory behavior, which in turn triggers the neuroendocrine mechanisms required for successful reproduction in the domestic strain.

11. THE SOCIALPATTERNOF MATINGIN GROUPSAND PAIRS A.

THE SEQUENCE OF COPULATION

When rats mate in pairs, the sequence of copulatory events obviously must be the same for the male and female (see Fig. 2). The male mounts the female many times when she is in estrus, achieving an intromission during most mounts. The male thrusts rapidly during an intromission, then dismounts and immediately grooms his penis. The pair then separates and each rat may briefly explore the environment, eat or drink before coming together again for another mount and

4

MARTHA K . MCCLINTOCK

PAIR

I11

[

Interintromission Interval

’ Ejaculatory Series

1

Postejaculatory Interval PEI

intromission. After several intromissions, the male ejaculates and becomes quiescent. He usually sits or lies on the ground, urinates and emits a 22-kHz ultrasonic call. After a while, the pair resumes mating and begins the next ejaculatory series. The pair may have as many as seven ejaculatory series before the copulatory sessions ends. This pattern of copulation is remarkably stereotyped whether a pair mates in the small enclosure of a standard laboratory testing cage ( I ’ X 2’) or in a larger seminatural environment containing a burrow system. Wild rats also mate in a similar pattern (McClintock and Adler, 1978). The pattern of copulation is strikingly different when rats mate in groups. Females and males change partners repeatedly in the midst of copulation in a

5

GROUP MATING IN THE DOMESTIC RAT

mating system termed panogamy (see Section VI1,A). Therefore, males and females do not experience the same sequence of copulatory events as they must when they mate in a pair (see Fig. 3). Social interactions during copulation create a sex difference in the pattern of copulation. Although these interactions are complex, they result in a pattern of copulation that is elegantly coordinated with the neuroendocrine mechanisms of successful reproduction from both the male and the female perspectives (McClintock and Anisko, 1982; McClintock et al., 1982a,b).

c

9,

111

91

PE I

d*

PEI

* 0

INTROMISSION EJACULATION

FIG. 3. A schematic of the sequence of copulation during group mating at a 2:3 sex ratio. The male and female sharing a copulatory event are connected by a horizontal line. To see the sequence of copulation from the perspective of one of the individuals, follow down that individual’s column. The time line only indicates the order of events, not the intervals between them. (Reprinted from McClintock et al., 1982a.)

6

MARTHA K. MCCLINTOCK

During group mating at sex ratios ranging from 2:l-2:4, males change partners after an intromission. Their intromissions are spread evenly (not randomly) among the estrous females of the group. That is, they are significantly more likely to mate with a different female than would be expected if the sequence of partners were random (see Fig. 3; McClintock er a / . , 1982a). In contrast, females are not likely to change partners between successive intromissions. However. after an ejaculation, they usually do change partners and resume mating with the other male (McClintock er a / . , 1982a,b; Thor and Flannelly, 1979). Males and females both take turns during group mating in a way that is consonant with the pattern of changing partners. They do this at different points in the copulatory sequence. Males take turns between themselves after they have ejaculated (when there are two males in the group). Thercfore, there is only one male mating with the estrous females of the group at a given time (see Fig. 3). After a male has ejaculated and returned to his resting spot, the other male usually approaches him to within one body length. The approaching male ignores solicitations from the females until he has made his approach and only then begins to mate, copulating until he ejaculates, whereupon the first male resumes mating. Therefore, each male has one or two complete ejaculatory series during the postejaculatory quiescent period of the other male. Females also take turns mating more frequently than randomly expected; that is, they are less likely to mate twice in a row than they would in a random sequence (see Fig. 3). However, in contrast to the males, females take turns after receiving an intromission; there is no alternation pattern after receiving an ejaculation. In general, it appears that the social pattern of copulation results more from turn-taking within a sex than it does from active attempts to change mating partners. Female rats tend to solicit and mate with whichever male is available. They seldom approach the male that is “out-of-turn.” Likewise, males tend to follow the closest soliciting female. There are exceptions to this generalization. For example, 78% of all cases in which a male mated out-of-turn resulted from a female soliciting a male that was sitting in his resting place (McClintock er a / . , 1982a). As will be discussed in Section V,B, exceptions such as these provide evidence for mate choice and sexual selection. Nonetheless, turn-taking within a sex is striking, particularly because it is observed at a variety of sex ratios (2: 1 , 2:2, and 2:4; McClintock er al., 1982a). Female turn-taking has also been observed at sex ratios of 1:5 (Tiefer, 1969) and 1:2 (Krames and Mastromatteo, 1973). However, male turn-taking may not be as stable when more than two males are in a group (e.g., 3:4). Furthermore, it is not observed among males that have not been living together prior to mating (Thor and Carr, 1979) and may well not be as striking when there is more space in which to monopolize females.

GROUP MATING IN THE DOMESTIC RAT

7

AND ITS PATTERNOF COPULATION B. TEMPORAL FUNCTIONS NEUROENDOCRINE

Rats must have several intromissions during copulation in order to trigger the males’ ejaculation and the females’ progestational state. Both the male and the female neuroendocrine systems are exquisitely sensitive to the timing of intromissions so that there are optimal intervals for triggering both of these neuroendocrine events. Surprisingly, the optimal intervals for the two sexes are not the same. From the male perspective, a 3-min interval is the most efficient for achieving ejaculation (Larsson, 1956; Bermant, 1964; Bermant et al., 1969). When intervals are either shorter or longer, more intromissions are needed to reach his ejaculatory threshold. From the female perspective, however, the optimal intervals for inducing a progestational state are substantially longer. Females are more likely to enter the progestational state when intromissions are spaced at 10 to 15 min (Edmonds et al., 1972). When intromissions are paced at these long intervals, males may never ejaculate (Larsson, 1956). When rats mate in pairs, intromissions are paced at 1-min intervals (Beach, 1956; Dewsbury, 1967a), a temporal pattern that is not optimal for triggering either ejaculation or the progestational state. Furthermore, it is not even a compromise between the two optimal intervals. When rats mate in groups, copulation is timed in a pattern that does match the optimal patterns for triggering ejaculation and the progestational state (McClintock and Anisko, 1982). This is because males and females can take turns mating and change partners so that the sequence and timing of copulation is no longer the same for males and females (compare Figs. 2 and 3). Intervals between intromissions are significantly shorter for males than they are for the females (see Fig. 4). Furthermore, there is a sex difference in temporal dependence of the rate of copulation. Males pace intromissions at a relatively constant rate that does not change markedly with the passage of time. Females pace intromissions at a slower rate and this rate decreases as time passes since the previous intromission. Furthermore, the intervals that are optimal for triggering neuroendocrine events are slightly more probable than other intervals. This is particularly true when the animals do change partners and the timing of their behavior is not as constrained by the temporal preferences of their original partner (see Fig. 5). A male is more likely to mate at intervals of approximately 3 min and also at 1 to 1.5 min than he is to mate at other intervals (see Fig. 6). The 3-min interval is optimal for reaching ejaculatory threshold. It is also the interval at which spinally transected males have spontaneous erections (Hart,1968), possibly reflecting the temporal pattern of the spinal mechanisms of male sexual behavior. The shorter interval (1- 1.5 min) may reflect the temporal parameters of CNS control of the initiation of copulation in males. It corresponds to the interval between mounts

MARTHA K . MCCLINTOCK

- 99 --- dd

0

10

20

30

40

50

60

70

80

90

100

110

Time t Interintromission I n t e rvals (min )

FIG. 4.Sex differences in the rate of copulation during group mating. In log survivor analysis. a cumulative distribution of intervals is plotted on a log scale. This method is used because the steepness of the slope of the survivor plot at time f is proportional to the probability of a behavioral event at time f since the previous event, and hence to the rate of behavior (Fagen and Young, 1978; Lee, 1982). (Figure redrawn from McClintock and Anisko, 1982.)

when a male mates with a tethered female that is prevented from affecting the pace of copulation (Larsson, 1973). It is also the length of mount bouts when males are prevented from intromitting (Sachs and Barfield, 1970; Lodder and Zeilmaker, 1976). Females, on the other hand, are particularly likely to mate at 10- to 15-min intervals (see arrow in Fig. 5). These intervals were found to be effective in inducing the progestational state necessary for implantation (Edmonds et a/., 1972j. Furthermore, intromissions paced at 6-min intervals were slightly lcss effective for inducing a progestational state; these intervals are relatively less common during group mating. Therefore, the pattern of group mating is well coordinated with both the temporal requirements of the neuroendocrine rellexes that are triggered by copulation and with its neural mechanisms. 111.

BEHAVIORAL UNITS OF ANALYSIS: ROBUSTNESS AND REDEFINITIONS

THEEJACULATORY SERIES The ejaculatory series is one of the fundamental units of analysis for mating behavior in the rat. In the male, the ejaculatory series has been used to quantify sexual motivation and to document its endocrine and neural mechanisms (Beach, A.

9

GROUP MATING IN THE DOMESTIC RAT

1956; Caggiula et al., 1973; Dewsbury, 1968a; Hart, 1968; Sachs and Barfield, 1976). In the female, it has been used as an independent variable to quantify her receptivity and assess the neuroendocrine consequences of copulation (Adler, 1969; Chester and Zucker, 1970; Connor and Davis, 1980; Lanier et al., 1979; Thor and Can, 1979). During group mating, the ejaculatory series is a robust unit of analysis for male sexual behavior. Males begin with an intromission and continue mating, usually without interruption, until they ejaculate. Furthermore, the males take turns mating, alternating at the end of an ejaculatory series, indicating that the behavioral unit is also robust at the social level of analysis. However, from the female perspective, the ejaculatory series has no meaning as a unit of analysis. In startling contrast with the sequence of copulation from the male perspective, females do not experience a regular sequence of mounts, intromissions, and ejaculations. The total number of copulatory events had by females in the group is the same as the males’; it must be. But the sequence from the female perspective is completely different (see Fig. 3 and compare the sequence of events in the male and female columns). The variance in the number of intromissions before ejaculation is five times greater than that of the male’s (McClintock and Anisko, 1982; see Section IV,B for a discussion of female units of analysis that are robust). This suggests that several tacit assumptions underlying the analysis of female

100

d

-different

50

1

I 0

% 10

, 20

30

40

50

60

Time t Interintromission Intervals (min )

FIG.5. The effect of changing partners on the rate of copulation. Note that intervals between intromissions > 3.5 min are not likely when males change partners and mate with a different female. From the female perspective 10- to 15-min intervals are particularly likely when females change partners. (Figure redrawn from McClintock et al., 1982a.)

10

MARTHA K. MCCLINTOCK

10

'

0

1

2

3

1

I

4

5

Time t

interintromission i n t e r v a l s ( m i n )

FIG 6. Distribution of intervals between intromissions of a single male (2BS) during group mating. Notc that 1- and 2.5- to 3-min interval\ are particularly likely. (Figure redrawn from McClintock and Anisko, 1982.)

sexual behavior should be reassessed. For example, it is often assumed that the intromissions must occur prior to ejaculation in order to induce sperm transport. Nonetheless, most females in a group become pregnant even when they do not receive stimulation in the ordered pattern of an ejaculatory series, suggesting that sperm transport may also be triggered during an ejaculation or afterward. Another example is the literature on mechanisms of sperm competition and its role in sexual selection. To date, controlled studies of sperm competition have assessed paternity only when the ejaculations from competing males were separated by complete ejaculatory series (Dewsbury and Hartung, 1980). In order to fully understand sperm competition in a biologically meaningful context, the types of copulatory sequences should be expanded to include those that occur during group mating (e.g., two ejaculations in a row without intervening intromissions). B.

THE OFTIMALPACEFOR TRIGGERING EJACULATION

1 . The Optimul Intervul befiveen Intromissions

Larsson (19.56, 19.59)quantified the optimum copulatory interval for bringing male rats to ejaculation. He enforced different copulatory intervals by using a partition to keep the male and female separate until a predetermined time had elapsed. Several different investigators have used this technique and identified the optimum interval as approximately 3 min. These findings have been used to build a model of the time course of net excitation relative to the ejaculatory threshold (Sachs and Barfield, 1976).

GROUP MATING IN THE DOMESTIC RAT

11

A similar relationship is found between the pacing and number of preejaculatory intromissions even when the pace of mating is not artificially controlled (see Fig. 7A). In our studies, the probability of intervals of different lengths was biased by giving males (both domestic and wild) the opportunity to mate with either a wild or a domestic female. Furthermore, pairs were tested in both standard testing cages and a seminatural environment. Long intervals are more likely when the female is of the wild strain and also when mating takes place in a large seminatural environment. A bias toward short intervals occurs when the male is paired with a domestic or a wild postpartum female (McClintock, unpublished observations) and also by mating in a small standard testing cage. Data from these various conditions demonstrate a relationship between the pacing and number of preejaculatory intromissions that is almost identical to that reported by Larsson (1956). Other investigators have manipulated the interval between intromissions using a variety of techniques and failed to alter the number of preejaculatory intromissions (Beach et al., 1956; Bermant, 1964; Caggiula, 1972; Dewsbury, 1968b; Sachs and Barfield, 1974). If anything, lengthening the interval decreased rather than increased the number of preejaculatory intromissions (Beach et al., 1955; Caggiula and Vlahoulis, 1974; Larsson, 1963). This suggests that some experimental treatments, such as shock, may change more than the interval between intromissions; they undoubtedly alter the ejaculatory threshold as well, obscuring its relationship to the pace of copulation. 2.

The Cost of Ejaculation

During group mating, intromissions are not likely to be paced at intervals greater than 3-3.5 min. In fact, almost every analysis of male sexual behavior, including the effect of dominance and changing partners, indicated that intervals greater than 3.5 min were not likely to occur (McClintock et al., 1982a; see Fig. 5 and 12 for examples of inflection points in a log survivor curve). In other words, intervals that are greater than the optimal value for triggering ejaculation are less likely to occur under almost every social circumstance. This suggests that intervals longer than 3.5 min are particularly costly. The “cost” of a particular interval between intromissions can be measured in terms of the time it takes to reach ejaculation [sometimes called the ejaculatory latency (Dewsbury, 1967b)l. Figure 7B plots the cost (in time to reach ejaculation) as a function of the interval between intromissions and is based on the ejaculatory threshold curve in Fig. 7A. It is immediately obvious that variation in intervals up to the optimum length have little effect on the cost of ejaculation. Up to the optimal interval, an increase in the time between intromissions is compensated by reaching ejaculation after fewer intromissions (see Fig. 7B). However, when intervals are longer than the optimum, the cost climbs exponentially as intervals become longer. It is these longer intervals that are rare from the male’s

12

MARTHA K . MCCLINTOCK

A

L 1.0

2.0

3.0

4.0

5.0

S.0

7.0

8.0

TIME t INTERINTROMISSION INTERVALS (min)

B

z 0

I-

<

1.0

2.0

3.0

4.0

5.0

6.0

7.0

8.0

TIME t

I NTERlNTROMlSSlON INTERVALS (min )

FIG. 7. Effect of intervals between intromissions on the number of preejaculatory intromissions (A) and the cost in time of reaching an ejaculation (B). Males were paired with a domestic female mating in small (DS,) or large (DS,) cage or with a wild female in a large cage mating at cycling (WS,) or a postpartum estrus (W-PPS,). (Figures drawn from data presented in McClintock and Adler, 1978; McClintock, unpublished.)

GROUP MATING IN THE DOMESTIC RAT

13

perspective during group mating, particularly when he can take advantage of the opportunity to change partners and avoid the costly constraints imposed by the female’s preference to mate at the longer intervals (see Fig. 5).

IV.

NEWINDIVIDUAL BEHAVIORS

New individual behaviors are revealed during group mating which are not readily observed during pair mating in a traditional testing environment. A.

MALERECEPTIVITY

The male, like the female, has three components to his sexual behavior: receptivity, attractivity, and active sexual behavior or proceptivity. [This term was coined by Beach (1976) to describe the active component of female sexual behavior. It is also appropriate for a description of the male’s behavior as well.] Because proceptivity is the most salient component of the male’s behavior in a traditional testing environment, particularly when highly trained stud males are used, most research has focused on the environmental and neuroendocrine mechanisms of this component. However, during group mating the males’s receptivity is also important. A male does not always respond to a solicitation. He may have just ejaculated and be in a refractory state or be in the midst of pursuing another female or fighting with another male (Barfield and Sachs, 1968; McClintock et al., 1982b). It would be possible to quantify a male’s receptivity by calculating a receptivity quotient (number of mounts/total number of solicitations received X 100). This method is comparable to the method for quantifying female receptivity (lordosis quotient: number of lordosis responses/total number of mounts received X 100; Beach, 1944; Gerall and McCrady, 1970). B . FEMALESOLICITATION

1. The Role of the Female in Pacing Copulation An environment that is more complex and larger than the standard testing cage gives female rats the opportunity to solicit the male and actively regulate the timing of copulation (McClintock and Adler, 1978). This behavior is even more salient during group mating when females take turns soliciting the males (McClintock and Anisko, 1982). Female solicitation has three main components: the approach, the orientation to the male, and the runaway (see Fig. 8). The female usually begins a solicitation by approaching the male with either an estrous run or walk. This gait is jerkier than the gait of a social approach or the gait of a nonestrous female. Once

MARTHA K . MCCLINTOCK

-

______FULL SOLICITATIONS

PARTIAL SOLICITATIONS touchback

(2 runby

INTERCEPTION

FIG.8. Examples of the variety of female solicitations and interceptions.

the female is within one body length of the male, she orients herself to him, usually holding a head-on or 90" position for a few seconds. If he is not responsive. she may groom him, crawl over his head or present her genital area for grooming. Finally, the female turns away and runs directly away from the male either with a dart-hop gait or the stiff-legged run of an estrous female. All three components of solicitation are not necessary to elicit a mount from the male: Partial solicitations can be equally effective (see Fig. 8). If a female is already within a body length of the male and oriented away from him, she may substitute a touchback for the approach and orientation before the run away. Or, a female can simply run by the male at 90" to stimulate a chase and mount. Therefore. the solicitation should not be considered a fixed action pattern. There is a large variety of ways in which females can modify the basic form of the behavior to accommodate the particular situation [see Fig. 8 and McClintock and Adler ( 1978) for a more detailed description].

GROUP MATING IN THE DOMESTIC RAT

15

However, the female cannot solicit in a small barren cage. There she is essentially kept continuously in the orientation phase of her solicitation and is effectively prevented from regulating her contact with the male. The male usually responds to any movement that she makes as if it were part of an active solicitation. Therefore, studying female solicitation and proceptive behavior in a small cage is akin to studying swimming behavior in a bathtub or ballroom dancing at a disco; it cannot be done. Only the reflexive components of the behavior, such as the dart-hop gait, can be measured in this restrictive environment. The behaviors that make up a female solicitation were noted anecdotally by other investigators before their function or importance for the pacing of copulation were recognized (Beach, 1944, 1967; Hardy and Debold, 1972; Larsson, 1956; Stone, 1922; Tiefer, 1969; Timmermans, 1978; Zucker and Wade, 1968). It was also known that a female could pace her contact with a male if he was restrained in some way and she was given operant control over access to him (Bermant, 1961; Bermant and Westbrook, 1966; Drewett, 1973; Fitzpatrick et al., 1971; French et al., 1972; Krieger et al., 1976; Law and Gerbrandt, 1967; Meyerson and Lindstrom, 1973; Peirce and Nuttall, 1961; Rodgers, 1970). Under operant conditions, estrous females prefer sexually active males and return to them faster if they are only mounted than they do when they received an intromission. Nonetheless, the integral role of active female sexual behavior in the pacing of copulation has been quantified only recently and data on its neuroendocrine mechanisms are sparse in comparison with the wealth of data on the reflexive component (e.g., the lordosis reflex and the dart-hop gait). Female rats can use solicitation to pace the timing of intromissions during mating in a pair and thereby alter the number of intromissions that a male has before he ejaculates. This was first demonstrated by observing both SpragueDawley and wild rats mating in a complex seminatural environment designed to incorporate features of the rat’s burrow system (Calhoun, 1962; Lore and Flannelly, 1978; see Fig. 9). Both strains have multiple intromissions and multiple ejaculations during mating. Furthermore, the form of female solicitation appears to be identical in the two strains. However, the total amount of copulation and its timing are not the same: Wild pairs have more preejaculatory intromissions, mate at longer intervals between intromissions, and have fewer ejaculations than domestic pairs do. The role of the female can be demonstrated by creating mixed strain pairs. When this was done (McClintock and Adler, 1978), mating tests showed that domestic males mate more slowly with wild females and have just as many preejaculatory intromissions as the wild male does when he is paired with a wild female. Furthermore, when a wild male is paired with a domestic female, he mates quickly in the domestic pattern and has only one-third the number of preejaculatory intromissions. Therefore, although it had been assumed that the number of preejaculatory intromissions during pair mating was due to charac-

16

MARTHA K. MCCLINTOCK

FIG.9. A seminatural environmcnt built in the laboratory to approximate the complexity of a rats burrow system. (Reprinted from McClintock. 1981 .)

teristics of the male, it is in fact largely determined by the strain of the female with which he mates. The female's contribution to the pacing of mating is also demonstrated by contrasting the pattern of mating in a complex environment that permits female solicitation with mating in a small cage that attenuates her contribution. A difference between such environments contributes three times the variance in the pacing of mating, and almost twice the variance in the amount of mating, as the male's strain contributes (McClintock and Adler, 1978).

17

GROUP MATING IN THE DOMESTIC RAT

This point is extremely important for interpreting the results of earlier studies that purport to study the female’s active sexual behavior and its mechanisms. For example, Price (1980) did not find that the female’s strain affected either the pacing of mating or the number of preejaculatory intromissions. However, his testing environment was simple and relatively barren. Furthermore, before meeting the male, the female was only given 5 min to explore the environment and immediately thereafter began copulation [instead of adapting to both for 4 days (McClintock and Adler, 1978)]. Therefore, the environment and experimental design prevented the females from soliciting intromissions and contributing to the timing of mating. In fact, even though the square footage of the environment was large, the timing of copulation was virtually identical to the timing of mating in a small traditional testing environment (see Fig. lo), strongly suggesting that the female’s contribution was indeed attenuated by the testing environment and the absence of the opportunity to adapt to it. 2 . The Function of Solicitation We have hypothesized that female rats use solicitations to pace the timing of intromissions and ejaculations in order to obtain sperm and to meet the neuroendocrine requirements for triggering a progestational state (McClintock and Adler, 1978). Diamond (1970) has referred to these requirements as a “vaginal code” because there are stable species differences that may well serve as a

A

I

n

t

l6

n

Standard

Large

Seminatural

Stanaard

Large

( M 8 A 78)

( P 80)

( M B A 78)

( M B A ‘78)

(P.’80)

TEST1NG ENVl RONMENT

Seminatural ( M 8 A ‘78)

TESTING ENVIRONMENT

FIG. 10. Effect of testing environment on pattern of copulation. Copulatory behavior in a large but barren environment (Price, 1980) is more similar to behavior in a small testing cage (McClintock and Adler, 1978) than it is to behavior in a large complex environment (McCIintock and Adler, 1978). In each test, Sprague-Dawley females were paired with either a domestic (open columns) or a wild male (filled columns).

18

MARTHA K . MCCLINTOCK

reproductive isolating mechanism. We have also hypothesized that female rats use solicitations to alter the length of their own postejaculatory quiescence and regulate sperm transport (Geyer and Barfield, 1980; McClintock et al., 1982a,b). During pair mating, there is virtually a one-to-one correspondence between a solicitation and an intromission. in group mating, although only one-half of the solicitations result in an intromission, the correlation between the total number of solicitations made and intromissions received is highly significant across individuals ( r = 0.92). Furthermore, once a female stops soliciting, she usually receives only a few additional intromissions (McClintock and Anisko, 1982). Gilman et 01. (1979) demonstrated that the opportunity to pace intromissions allows females to become progestational with fewer intromissions than when they cannot control the pace of copulation. Although the study was done in a small testing cage, the females had an escape compartment and could therefore regulate the pace of mating. This finding is substantiated by Erskine and Baurn’s (1982) observation that a female ends estrus more quickly if she can pace her contacts with a male. presumably having fulfilled her neuroendocrine requirements more efficiently. Again, the environment was not large, but it did have a barrier with an opening sized for easy passage by the female, but small enough to prevent the male from entering the female’s compartment. During group mating, each female received at least three ejaculations regardless of the total number of intromissions that she received (McClintock and Anisko, 1982). This suggests that females are also capable of differentially soliciting intromissions and ejaculations, perhaps utilizing ultrasonic calls from the male (see Section VI,C,2). 3. Methods for Quantihing Female Proceptivr Behavior Taken together, these studies indicate that there is an active component to the female rat’s sexual behavior (termed proceptivity; Beach, 1976) which is normally manifested by solicitation. However, the natural variation in the form of solicitation and the ability of females to adapt their behavior to artificial environments indicates that the essential element of solicitation is its regulatory aspect rather than its fonn. Little is known about the mechanisms of active sexual behavior in the female rat because most investigators have focused on only one of the simplest and most reflexive components of the behavior, the dart-hop gait. While it is true that dart-hopping can be part of a solicitation, it is not necessary nor does it reflect its pacing reliably. It is primarily a gait, and most probably integrated on a spinal or subcortical level, whereas the pacing and diversity which are the essential aspects of solicitation are undoubtedly the result of more encephalized controls. Approaches are a much better index of female active sexual behavior or proceptivity [but should be used cautiously; not all approaches are part of a

GROUP MATING IN THE DOMESTIC RAT

19

solicitation (McClintock and Anisko, 1982); gait and orientation are the best features to distinguish a social from a sexual approach]. Progesterone appears to play a more central role in the regulation of approaches (Fadem et af., 1979; MadlafouSek and Hliiiak, 1978) than it does in the regulation of lordosis (Davidson et al., 1968; Weick et al., 1971). Furthermore, the apparent sex differences in the neuropharmacology of mating behavior (Caggiula et al., 1979) may simply be an artifact of comparing the neural mechanism of the male’s active component (mounting) to the female’s receptive component (lordosis reflex and dart-hop gait). The more appropriate basis of comparison would be the neuropharmacology of solicitation, which is the behavior that is comparable to active sexual behavior of the male. C . FEMALEINTERCEFTION During group mating, a female can intercept the male when he is chasing another female and induce him to follow her instead of his original partner (see Fig. 8). This is a social form of solicitation that can only be seen when several estrous females are mating in a group. The behavior is similar in form to a run-by solicitation. Its function also is similar and mediates competition between the females for the opportunity to mate with the male (see an expanded discussion of the use of interceptions in female competition in Sections V,A,2 and V,B,2). QUIESCENCE D. FEMALEPOSTEJACULATORY

Female postejaculatory quiescence ensures time for the transport of sperm to fertilize her ova and reduces her risk of entering a progestational state without having been fertilized (Adler and Zoloth, 1970; McClintock et al., 1982b). The latter could happen if she consistently resumed mating and disrupted the ejaculatory plug before enough sperm had been transported into the uterus (Matthews and Adler, 1977). Like the male, the female goes through three phases of postejaculatory quiescence (see Fig. 11; McClintock et al., 1982b). First, she remains stationary. During this time her EEG has a sleeplike pattern (Kurtz, 1975), although she is more responsive than the male. Second, she begins to interact with other members of the group, approaching them only socially. She begins the last phase with a solicitation, and solicits repeatedly until she gets an intromission. During pair mating, the female’s posture is slightly different after an ejaculation from what it is after an intromission (Dewsbury, 1967b; Diakow and Dewsbury, 1978). However, her quiescence is eclipsed by the male’s refractory period because it is longer than hers, making him the rate-controlling agent in the interaction after an ejaculation. In complex environments, some of the female’s quiescent behavior can be

20

MARTHA K. MCCLINTOCK

Stationary

Interactive

I

Median

E

1

0

5

5 20

50

Sexual ( p =0.007)

Ip =0.0501

( p = 0.1081

Duration ( m i n ) 15

10

70

20

40

-1 85

95

100

% Sperm Transported FIG. 1 1 . Sex differences in the length of the different phases of postejaculatory quiescence. The time since ejaculation is plotted on the x axis along with the percentage of sperm trunsportcd at that time. (Reprinted from McCIintock et n l . , 1982b.)

seen. After ejaculation, the female returns to her own resting place and remains motionless for a while (McClintock and Adler, 1978). This corresponds temporally to the longer delays for performance of an operant response for contact with a male after receiving an ejaculation (Bermant, 1961; Fitzpatrick et ul., 1971; Krieger et ol., 1976; Peirce and Nuttall, 1961). However, even in a complex environment, the duration of the female's sexual inactivity must be the same as the male's and therefore it cannot be measured independently of his. It can only be quantified when there are other males in the group that have not just ejaculated and are sexually active. Under these conditions, it becomes possible to demonstrate that the female has her own postejaculatory quiescence that is similar to but shorter than the male's (see Fig. 11; McClintock et ol., 1982b).

V.

THESOCIAL STRUCTURE OF MATING:SEL>ECTION WITHIN AND OF GROUPS

Domestic rats have been artificially selected for a high reproductive rate in social groups where they have the opportunity for competition, mate choice, and cooperation during copulation. Because different aspects of copulation trigger a variety of neuroendocrine mechanisms required for successful reproduction, these neuroendocrine events can be used to define the appropriate units of behavior which are the currency for sexual selection and cooperation during group

GROUP MATING IN THE DOMESTIC RAT

21

mating. In other words, the amount and timing of copulatory behavior can be conceptualized as a central mechanism through which competition, mate choice, and cooperation are expressed in this species. As in many animal and human groups (Masters, 1978), rats have both common and conflicting interests with the other members of the group. In the following discussion, it will be striking that both competition and cooperation can be mediated by the very same aspect of copulatory behavior, and their consequences may be manifested in the same neuroendocrine systems. That is, a single feature of the rat’s copulatory behavior, such as a large number of preejaculatory intromissions, may serve both cooperative and competitive functions. Therefore, it is important to recognize that these aspects of the social structure of mating are neither independent nor are they diametrically opposed (Mayr, 1958). A.

INTRASEXUAL SELECTION: COMPETITION

1. Male-Male Competition

a. The Pattern and Cost of Copulation. When several male rats live together in a group, a dominance relationship is established among them that is indicated by postures, odors, ultrasounds, and the pattern of wins and losses in fights and displacements (Barnett, 1975; Carr et al., 1976; Krames et al., 1969; Lehman and Adams, 1977; Sales, 1972; Timmermans, 1978; Thor, 1979). However, if the males have been living together, as is the case during domestic breeding, agonistic encounters do not usually occur during copulation (Barnett, 1958, 1975; Calhoun, 1962; McClintock et al., 1982a; Robitaille and Bouvet, 1976; Telle, 1966; Thor, 1979). Even males that have been together for just a short time avoid interfering with each other during copulation (Dewsbury and Hartung, 1980; Price, 1980). Direct competition during copulation is usually observed only when males are placed in a small cage with a single female and first meet under these conditions (Thor and Carr, 1979; Thor and Flannelly, 1979). Although agonistic dominance does not affect the average pace of copulation (Dewsbuly and Hartung, 1980; Price, 1980; McClintock et al., 1982a), it does affect some temporal features that alter the cost of ejaculation. Dominant and subordinate males mate at the same pace when there are 3.5 min or less between intromissions (McClintock et al., 1982a; see Fig. 12). Any variation among these short intervals would not appreciably affect the total time that it takes to ejaculate (see Section III,B,2). However, subordinate males do have significantly more of the long costly intervals (I11 > 3.5 min) that significantly increase the number of preejaculatory intromissions and the time required to ejaculate. This difference is the result of losing fights or nudges when a clear turn-taking pattern has not been established. In this instance, the dominant male is more

22

MARTHA K . MCCLINTOCK

likely than the subordinate to resume mating after an agonistic encounter. This finding is corroborated by anecdotal reports that fights between males disrupt copulation temporarily (Price, 1980) and indicates that dominance affects the timing of male sexual behavior primarily when the cost of ejaculation is high. Even though subordinate males have intervals between intromissions that are the same or longer than the dominant's, subordinates ejaculate after fewer preejaculatory intromissions (McClintock et al., 1982a). It therefore appears that subordinate males have a lower ejaculatory threshold than the dominant's [as defined by Freeman and McFarland (1974): ejaculation is reached after fewer intromissions even when the pace of intromissions predicts that the number of preejaculatory intromissions should be the same or higher]. Lowered ejaculatory thresholds have been reported in stressed males that have been subjected to electric shock (Eleach el a / . , 1956; Caggiula and Vlahoulis, 1974), suggesting that subordinate males may ejaculate more quickly because they are stressed socially. This hypothesis is supported by the observation that subordinate males mate in the pattern of a dominant male if the dominant male is removed and the subordinate is left to copulate alone (Thor and Carr, 1979). Lower ejaculatory thresholds may have several advantages for subordinate males and may represent a successful mating strategy when they must mate in a group with a more dominant male. The reduced number of preejaculatory intromissions compensates for the increased probability of long intervals between

1

0

5

10

15

Time t Interintromission I n t e r v a l s ( m i n )

FIG. 12 Seventy-two percent of intervals between intromissions are the same for dominant and subordinate males. However. dominant males have significantly fewer of the costly long intervals (> 3.5 min). (Figure redrawn from McClintock e t a / . , 1982a.)

GROUP MATING IN THE DOMESTIC RAT

23

them, making the cost of a subordinate’s ejaculation comparable to the dominant’s. Furthermore, the subordinate male will be less likely to waste energy by delivering more intromissions than females actually need. They also will be more likely to have ejaculated before the dominant male begins the sexual phase of his postejaculatory quiescence (McClintock et al., 1982b), thus reducing the possibility of any direct confrontation during copulation. b. Paternity. When more than one male mates with a female, the paternity is affected by a variety of factors including the total number of ejaculations that each male delivers, the order in which they are delivered (Lanier et al., 1979), and intrauterine sperm competition (Sharma and Hays, 1975). It is interesting that dominance status does not affect the total number of ejaculations delivered by dominant and subordinate males to the females of an adapted group. However, dominance does affect the way in which these ejaculations are distributed among the females. Dominant males give slightly more ejaculations than subordinate males to most of the females in the group, and have lower variance in the number of ejaculations given to an individual female (McClintock et al., 1982b). This is an effective strategy for increasing the chances of paternity that is used when the cost of ejaculation is relatively low (Short, 1979). However, subordinate males have a different strategy: They give almost all of their ejaculations to a few females and therefore have a high variance in the number of ejaculations per female. This is the strategy that is used by rams during continuous mating in multifemale groups (Synnott et al., 1981) and may reflect the higher cost of finding a female to the subordinate male (a cost that is also increased by female choice; see Section V,B,2). Therefore, it is expected that dominant males have a slight advantage in siring the litters of many females, whereas subordinates have a major advantage with a few females: two different strategies for achieving a similar end. The pattern described above may occur only when the males have been living together in a mating group. If the testing procedure creates overt aggression between males, the dominant male has a greater total number of ejaculations than the subordinate (2:l sex ratio; Thor and Carr, 1979). Males only have to be adapted to each other briefly for them to have the same number of ejaculations (2:l sex ratio; Price, 1980). The order in which dominant and subordinate males give a female ejaculations may also affect paternity differentially (Dewsbury and Baumgardner, 1981 ; Levine, 1967; Parker, 1970). Dominant males are more likely to give a female her last ejaculation in adapted multifemale groups (McClintock et al., 1982a) and in groups with a 2:l sex ratio (Thor and Carr, 1979). Being the last to ejaculate is correlated with siring more of the litter (Lanier et al., 1979). However, primacy of the last ejaculation may simply reflect a correlation with delivering more ejaculations. Furthermore, conflicting reports make it difficult to interpret the effect of the order of copulation on paternity. Dewsbury and Hartung

24

MARTHA K . MCCLlNTOCK

(1980) did not find that being the first to deliver an ejaculation conferred any advantage, although Gartner and co-workers (198 1) found that delivering the first intromission did. It will not be possible to sort out the order effects of ejaculations until there are studies that consider all of the relevant variables simultaneously: sperm count as a function of number of previous ejaculations; delivery of intromissions and ejaculations in the pattern that females normally receive them during group mating (McClintock and Anisko, 1982); male dominance (measured independently of mating performance; Dewsbury, 1981a, 1982a); and the sex ratio at the time of mating (McClintock et al., 1982a). During postejaculatory quiescence, dominant and subordinate males also behave differently in ways that could affect their paternity differentially. This is the time when sperm transport can be disrupted by the resumption of mating (Adler and Zoloth, 1970). The dominant male resumes mating sooner and more quickly after an ejaculation than the subordinate (McClintock et al., 1982a). While this would seem to increase the risk of disrupting the transport of his own sperm, mating is not usually resumed with the same female that received his preceding ejaculation because females have their own postejaculatory quiescence (McClintock er nl., 1982b). In addition, because the males alternate ejaculatory series, resuming mating quickly gives the dominant male a greater opportunity to disrupt the transport of the subordinate male’s sperm. Again, the subordinate male has a different strategy. He rarely resumes mating at a time when he could disrupt the transport of the dominant male’s sperm.

t

1

2

3

4

5

6

7

a

9

E jic~lalton

Intromission

Preceding Ejaculation

Fiti. 13. Interceptions are significantly more likely at the penultimate intromission before ejaculation 0, 5 0.05; note that time runs backward along the x-axis. indicating the intromissions that precede ejaculation). (Figure drawn from data presented in McClintock et ul., 1982a.)

GROUP MATING IN THE DOMESTIC RAT

1st

2nd

3rd

25

4th

QUARTILE Total ## of Ejaculations

FIG.14. In multifemale Groups A (open column) and B (filled column), female interceptions were restricted to early ejaculatory series (first two quartiles) when the male’s sperm count is likely to be high. (Figure redrawn from McClintock, unpublished data.)

Therefore he avoids confrontation with the dominant male and cannot benefit from this form of male competition (McClintock et al., 1982a; Thor and Flannelly, 1979). On the other hand, by delaying mating, subordinates rarely risk interrupting the transport of their own sperm by copulating when it could be disrupted. 2 . Female-Female Competition Interceptions are a form of female competition that is based on female solicitation. When the male is following a female (during the runaway component), another female may run between them and sometimes induce the male to follow and copulate with her instead of with his original partner (see Figs. 8 and 13; McClintock et al., 1982a; Tiefer, 1969). This form of female-female competition is most common when the male is about to ejaculate (see Fig. 13). In addition, it is restricted to early ejaculations (see Fig. 14) when the male’s sperm count is most likely to be high (man, Johnson et al., 1980; goats, Fielden and Berker, 1964; sheep, Synnott et al., 1981; house mice, Huber et al., 1980; rats, Matthews, personal communication; Pessah and Kochvah, 1975). Therefore, female rats compete at a time when it appears that they are more likely to be inseminated and produce a full litter.

26

M A R T H A K . MCCLINTOCK

The timing of female competition suggests that male rats benefit from a sexual selection strategy that is the inverse of that emphasized in other species (Cox and LeBoeuf, 1977): males inciting competition among females. As the male approaches ejaculation, something about his behavior incites females to compete for the opportunity to mate with him and receive his ejaculation. However, this form of female competition is restricted to the portion of the mating session when the males’ fertilizing capacity is high, most likely because his behavior is different before his first ejaculation than after the fourth or fifth. Female competition may also affect the sex ratio of her litter under some conditions. If a female receives her first ejaculation early in estrus, the sex ratio of her litter will be biased toward males. However, if she receives her first ejaculation late in estrus, the litter will have a female bias (Hedricks and McClintock, 1982). Thus, females that are dominant (in that they compete successfully for an ejaculation early in the copulatory session) may be more likely to have male offspring. The female’s behavior during the male’s postejaculatory quiescence can also have a competitive effect indirectly on the probability of being inseminated successfully. If females in the group repeatedly solicit a male and induce him to resume mating with the female that received his ejaculation early, before the time required for complete sperm transport has elapsed, the sperm transport in that female could be disrupted. Males rarely mate with the female that received his ejaculation when transport of their sperm could be disrupted. However, when they did so, i t was only after they had been induced to resume mating by solicitations from the other females of the group (McClintock et al., 1982b). B.

ISTERSEXUAI.

I.

Male ChoiL‘e

SELECTION: MATE CHOICE

Usually, during group mating, a male rat simply mates with the female that is closest and soliciting him. Nonetheless, copulation has a cost, and a male can choose, to some extent, which female will benefit from his efforts (see Section III,B,2; Dewsbury, 1982b; McClintock ef ai., 1982a). In contrast to pair mating (McClintock and Adler, 1978), only one-half of solicitations during group mating elicit copulation (McClintock and Anisko, 1982), indicating that a male does not always respond to a female solicitation. This is most striking when two females solicit the same male simultaneously or when one female intercepts another. At these times, the male has the opportunity to choose the female that he will follow and mate. Mate choice by males could be based on the female’s individual odor (Carr et d.,1962; Krames and Mastromatteo, 1973; Thor and Flannelly, 1977; see Section VI,C) or ultrasounds (see Section VI,C,2) as well as the type or gait of her solicitation (McClintock and Adler, 1978; see Section IV,A).

GROUP MATING IN THE DOMESTIC RAT

27

The number of male approaches tends to correlate with the total amount of copulation experienced by an individual male (McClintock and Anisko, 1982). Nonetheless, male approaches do not determine which female he mates with nor the total amount of copulation that a female receives either during pair or group mating (McClintock and Adler, 1978; McClintock and Anisko, 1982). Therefore, during group mating (2:2-2:4), male mate choice is mediated by his differential response to female solicitations (his receptivity), rather than by his approaches or proceptivity. 2 . Female Choice Female rats can discriminate individual males and their dominance and reproductive status on the basis of the male’s behavior, odors, and ultrasounds (Barnett, 1975; Carr and Caul, 1962; Carr et al., 1979; Krames, 1970; Krames et al., 1969; Mackay-Sim and Laing, 1980; Sales, 1972). Nonetheless, before the male ejaculates, females do not show a marked preference for mating with a particular male. In other words, when a male is mounting and intromitting, females solicit whichever male happens to be mating at the time and only rarely approach the male that is “out-of-turn.” This pattern corresponds to the absence of a strong mate preference under operant testing conditions (Bolles et al., 1968) and the decrease in olfactory responsiveness as mating continues (Krames and Mastromatteo, 1973). The female’s mate choice is most salient during postejaculatory quiescence (McClintock et al., 1982a,b), perhaps reflecting the discriminative ability demonstrated by operant studies (Law and Gerbrandt, 1967; French er al., 1972). After a minimum duration of quiescence, female rats truncate their postejaculatory quiescence if they have received an ejaculation from a subordinate male. If they receive an ejaculation from a dominant male, their postejaculatory quiescence is significantly longer. The parallel between the time course of the female’s postejaculatory behavior and the time course of sperm transport suggests that the female may be affecting the paternity of her litter. The minimum duration of quiescence would ensure some sperm transport and reduce the risk of pseudopregnancy. The shorter quiescence following a subordinate male’s ejaculation could increase the probability that transport of the subordinate male’s sperm will be interrupted (McClintock et al., 1982a). Her longer postejaculatory quiescence after a dominant male’s ejaculation suggests that she is essentially protecting the transport of the dominant male’s sperm and may bias the paternity of her litter in his favor. It is important to note, however, that the female’s postejaculatory behavior is timed in a way that could ensure multiple paternity of her litter (McClintock et a l . , 1982b) and that female mate preferences are likely to affect only the proportion of her litter sired by the dominant male. Multiple paternity has been documented in a variety of female mammals (Birdsall and Nash, 1973; Hanken and Sherman, 1981; Weir and Rowlands, 1973) including rats (Dewsbury and Har-

28

MARTHA K . MCCLINTOCK

tung, 1980; Lanker et a / . , 1979; Gartner et al., 1981) and is an effective strategy when male dominance status is not particularly stable or necessarily a good predictor of traits that would be desirable when the offspring reach reproductivc age. Paternity may be biased toward the male that is dominant at the moment, but the female may “hedge her bets” and ensure that some of her offspring will be sired by other males as well. In addition, litters of mixed paternity are larger (Gartner er al., 198 I ) , which could increase the female’s reproductive potential, particularly during domestic breeding when resources are not a limiting factor. The rat. therefore, has a mating system in which female choice of males operates within the copulatory session. Females solicit males in a way that could differentially affect paternity. This is characteristic of a promiscuous system (Trivers, 1972) and emphasizes the importance of social dynamics within the group at the time of mating. C.

COOPERATION

When rats mate in groups. males cooperate with other males and females cooperate with other females during copulation. That is, they “invest resources in a common interest shared by other group members” (Chase, 1980); they do not interfere with one another even though they have the opportunity; and they behave in ways that facilitate the mating of other animals in the group. This is not meant to imply that the cooperative behavior is intentional (Allee, 1938) nor to say that it is altruistic (Masters, 1978). Nor must the individuals of the group be genetically related in order to benefit by cooperative behavior (Packer and Pusey, 1982; Thor, 1979). It is simply that under some conditions, the mating behavior of individuals is more efficient during mating in a group and short-term compromises are often outweighed by long-term benefits. This, in turn, suggests that group mating would result in increased fitness, a hypothesis that awaits a direct test. I.

Mule Coopercitiori

Males who live with other males mate morc efficiently, reducing the cost of ejaculation (Thor, 1980). Furthermore, when a single male mates with several different females, he risks wasting his ejaculations and mating effort. Female rats must have intromissions to trigger sperm transport and the progestational state necessary for implantation. Nonetheless, in multifemale groups, a male is not likely to ejaculate with the same female that received his preejaculatory intromissions. Therefore, his sperm might be wasted because it is not transported and there is no progestational state to support implantation. In addition, the effort of his preejaculatory intromissions may also be wasted in females that do not also receive his ejaculation (see the social pattern of copulation schematized in Fig. 3). This potential for wasted effort is reduced when males mate together in a

GROUP MATING IN THE DOMESTIC RAT

29

group. If a male rat (Male 1) permits another male rat (Male 2) to mate during his postejaculatory quiescence, instead of attacking him as he would an intruder (Thor and Flannelly, 1979), Male 2 is likely to provide the additional intromissions that are needed by the female that received Male 1’s ejaculation. Male 2 will also benefit; if he does not interfere with Male 1’s copulation, he can rely on Male 1’s preejaculatory intromissions to prime the female with which he himself ejaculates. Therefore, during group mating, males have the common goal of triggering sperm transport mechanisms and the progestational state in the females of their group and will mutually benefit by cooperating with each other in achieving this end. In groups with two males, males cooperate by taking turns mating. They extend their postejaculatory quiescence beyond the length typical for single males if the other male is copulating (McClintock et al., 1982b). That is, they wait until the other male has ejaculated and they have approached him before they respond to solicitations and resume copulation. The females are as likely to receive intromissions from the other male as they are to receive them from the ejaculator (McClintock et al., 1982a). In this way, the males’ copulatory behavior is mutually beneficial, at least in the short term. Cooperative behavior is also beneficial in a long-term perspective. During domestic breeding, the male’s reproductive success depends on his ability to mate successfully on several nights in succession. A male that monopolizes the group of females on the first night risks behavioral exhaustion (from which it takes a week to recover; Beach and Jordan, 1956) and emptying his seminal vesicles (which takes more than a day to replenish; Pessah and Kochva, 1975; Robb et al., 1978). Males that share copulation with other males will be less exhausted, more likely to recover by the next night, and thus more likely to be sexually active and fertile on successive nights when additional females will be in heat. They thereby have more offspring when totaled over the entire opportunity for reproduction. Avoiding direct competition is also advantageous if more than two males are present. Males that stop and fight with each other are distracted from pursuit of the female, are less likely to mate with her, giving other males an uncontested opportunity to mate (Arnold, 1978; Price, 1980; Robitaille and Bouvet, 1976). Avoiding direct confrontation has been termed competitive mutualism or a gambler’s strategy; individuals cooperate at least for the opportunity to compete. The behavioral mechanism of male cooperation in the form of turn-taking may rely on differences in ejaculatory threshold. When domestic and wild males mate together in a group, “there is a tendency for the males to become desynchronized in sexual activity, one male copulating while another [is] experiencing postejaculatory quiescence” (Price, 1980). Wild and domestic males, like dominant and subordinate males, have different ejaculatory thresholds. Because one reaches ejaculation before the other, they soon begin to alternate ejaculatory series and stabilize in a turn-taking pattern. Male turn-taking is not just restricted to mating

30

MARTHA K. MCCLINTOCK

and may also have a basis in a broader social context: one male explores, eats and drinks while the other rests in a burrow (Ziporyn. personal communication). 2 . Fern& Cooperation Females that mate in groups have the common goal of increasing the number of intromissions and ejaculations received from the males, that is, increasing the males’ reproductive investment. Females will not be able to transport sperm or support implantation without the stimulation from intromissions. By taking turns mating (instead of monopolizing the male), females provide males with different partners, perhaps creating a form of “stimulus novelty” that is known to increase the amount of male copulation (Larsson, 1956; see Section VI,D on the Coolidge Effect). By mating together, females may also decrease the chance of inadvertent injury during male competition (Robitaille and Bouvet, 1976; Thor and Flannelly, 1979; Cox and LeBoeuf, 1977).

D.

SEXUAL SELECTION AT

THE

GROUPLEVEL

The history of the Sprague-Dawley rat as domesticated and bred by the Charles River Breeding Laboratories raises the intriguing question of sexual selection at the group level. The preceding sections have detailed the ways in which sexual selection at the individual level may be mediated by the effects of copulatory behavior on neuroendocrine function. However, because the Charles River breeding practices happen to keep or discard males on the basis of the performance of their group, sexual selection is also being imposed artificially on males at the group level. The question then is: How is artificial selection at the group level manifested in relationships between behavior and neuroendocrine function’? In parallel with their breeding history of artificial selection at the group level, the behavior of males that have lived together in a group is more cooperative than would be expected on the basis of the level of aggression noted among unfamiliar males that are placed in groups just to mate (Thor and Flannelly, 1979; see Section V,C, 1 for the detailed discussion). Because groups of males are kept or discarded on the basis of the net reproductive output of their group, males would profit by cooperating during copulation even if they sire fewer offspring themselves (provided they live in a group with males that are more capable of increasing the group’s reproductive output). Although their individual lifetime fitness may be lower if they cooperate, their chances of being represented in future generations and having more offspring in those generations will be increased (Vehrencamp, 1979). Therefore, male cooperation during copulation is consistent with a history of group selection in which individuals temporarily sacrifice the personal component of inclusive fitness but gain through the future component.

GROUP MATING IN THE DOMESTIC RAT

31

Proposing group selection as an evolutionary mechanism for male cooperation is not meant to exclude concurrent selection for this behavior at other levels. Because group and individual selection may operate in the same direction (Hamilton, 1975; Wade, 1977, 1978; Wimsatt, 1980), male cooperation may also result from individual as well as group selection. Kin selection also may be operating, if males in a group are genetically related (Hamilton, 1964). Conversely, the fact that individual selection operates in the form of dominance relationships does not preclude the contribution of group and kin selection. In fact, kin selection would increase tolerance for a decrease in the personal fitness of the subordinate males. This problem has been discussed elegantly by VehrenAl

FITNESS W

I

a

b

C

\

FITNESS

GROUP SIZE

FIG. 15. Fitness of dominant (Wa) and subordinate (Ww) males as a function of group size in both related (A) and unrelated (B) groups. In related groups, the optimum group size preferred by a dominant (b) is affected by the skew of the group (a) # (b). When Wci = Ww = W at (c), groups without skew are likely to form.

32

MARTHA K . MCCLINTOCK

camp (1980). A schematic of some possible relationships between these variables during group mating is presented in Fig. 15. Nonetheless, the exact relationship between these three levels of selection (individual, kin, and group) and the skew introduced by dominance relationships in groups of rats must be described empirically.

VI.

CLASSICMATINGBEHAVIORS IN A SOCIAL CONTEXT

There are many features of the Norway rat’s mating behavior which are quite robust during pair mating but lack an obvious function. In the following sections, several of these behavior patterns will be discussed in the context of group mating, a context in which the Sprague-Dawley strain was domesticated. These discussions are intended to suggest putative functions for the behaviors and the mechanisms through which they evolved. A.

MULTIPLE INTROMISSIONS

AND

MULTIPLE EJACULATIONS

During pair mating, male rats can have as many as eight or nine ejaculations. However, female rate can become pregnant and bear a full litter after receiving only one ejaculatory series (Adler, 1969). Therefore, it has been suggested that the multiple ejaculatory pattern is merely a laboratory artifact without an essential function in the rat’s mating system (Zucker and Wade, 1968). Nonetheless, during mating in a multifemale-multimale group, the multiple ejaculatory pattern does serve several important functions. First, the capacity for multiple ejaculations permits males to inseminate more than one female (see Section 11,A). Females regulate the number of ejaculations that they receive if they mate in an environment where they can contribute to the pace of copulation (McClintock and Adler, 1978; McClintock, 1981). Therefore, the number of ejaculatory series had by a male is determined by the number of estrous females and the sex ratio of his group. When several females are in estrus, the number of ejaculatory series per male is increased; when one female mates with two males, the number of ejaculatory series per male is half that in pairs (Dewsbury and Hartung, 1980; McClintock et ul., 1982a; Price, 1980). In small or barren cages that do not allow the female to affect the pace of copulation, this relationship breaks down (Tiefer, 1969). Second, in multimale groups, a male that can give a fernale several ejaculations will sire a greater proportion of her offspring than one that gives her only one ejaculation (Lanier et ul., 1979). Therefore, multiple ejaculations enable a male to compete with other males in his group through sperm competition (Arnold, 1976; Parker, 1970). It has been demonstrated in pairs that both intromissions and ejaculations trigger the progestational response that is necessary to compensate for a short luteal phase (Adler, 1969; Beach and Rabedeau, 1959; Clemens, 1969; Land and

GROUP MATING IN THE DOMESTIC RAT

33

McGill, 1967; Taleisnik et al., 1966; Terkel and Sawyer, 1978). They also trigger sperm transport mechanisms (Adler, 1969), interrupt sperm transport by dislodging or removing the plug (Adler and Zoloth, 1970; Chester and Zucker, 1970; Mosig and Dewsbury, 1970), and may clean the vaginal tract in preparation for deposition of the plug (Dewsbury, 1982b). From the male perspective, the multiple ejaculatory pattern cannot be dissociated from the multiple intromission pattern; each male must have several intromissions before he can ejaculate. Therefore, the consequences of multiple ejaculations are always correlated with the consequences of multiple intromissions. However, during group mating, intromissions and ejaculations do not occur together in an ejaculatory series from the female perspective. A female may receive two ejaculations in a row before she receives many intromissions or she may receive 20 intromissions before getting her first ejaculation (McClintock and Anisko, 1982; Tiefer, 1969). This behavioral dissociation from the female perspective suggests that the neuroendocrine consequences of intromissions and ejaculations must be reevaluated given the copulatory patterns that the female actually experiences during group mating. For example, older females (Davis et al., 1977) and females in postpartum estrus (Davis and Connor, 1980) require several ejaculatory series to become pregnant in comparison with younger cycling females that need only one. However, it is not known whether it is multiple intromissions or multiple ejaculations that are critical. Sexual interference among males is another area in which there is not enough independent information about the neuroendocrine consequences of intromissions and ejaculations. Males can compete by interrupting transport of each others’ sperm (Dewsbury and Hartung, 1980; Thor and Flannelly, 1979), but to date, relative paternity has been measured only when females receive ejaculations along with intromissions of a complete series. Therefore, ejaculations from each male were always separated by the time and stimulation of multiple intromissions. During group mating, successive ejaculations rarely occur in this pattern (McClintock and Anisko, 1982). It happens only if the physical and social environment permits a male to sequester a female (Robitaille and Bouvet, 1976) and mate exclusively with her until he ejaculates. What, then, is the nature of sperm competition when a female receives ejaculations from two males without any intervening intromissions? Can sperm transport be triggered successfully by intromissions that occur after as well as before an ejaculation?

B . MALEPOSTEJACULATORY QUIESCENCE After ejaculating, a male rat becomes quiescent. His activity is reduced (Beach and Whalen, 1959; Dewsbury, 1967b, 1972; Larsson, 1956) and hippocampal theta activity becomes desynchronized (Kurtz and Adler, 1973). Artificial manipulation of the male during pair mating has permitted division of the male’s postejaculatory quiescence into absolute and relative refractory periods (Beach

34

MARTHA K. MCCLINTOCK

and Ilolz-Tucker, 1949; Sachs and Barfield, 1976). During the absolute refractory period. the male cannot be induced to resume mating. However, during the relative refractory period, the sudden introduction of a strange partner, a change in cages, or an electric shock can induce him to resume mating. During group mating, the male’s refractory periods are manifested spontaneously in his social interactions. After ejaculation he is immobile and does not respond at all to the behavior of other group members (McClintock et a/. , 1982b; Price, 1980). Then, he enters an interactive phase when he begins to move about his environment interacting socially, eating, fighting, and exploring. However, he does not respond to solicitations until he enters the sexual phase of his quiescence whereupon he almost immediately mounts and has an intromission. lmmediately after ejaculating, the male returns to his resting place during pair mating (McClintock and Adler, 1978; McIntosh et al., 1979). Once there, he alternately urinates profusely and emits an ultrasonic call (Anisko er ul., 1979; McIntosh et a/.. 1979). During group mating, it is clear that the pools of urine are deposited at the male’s and not the female’s resting place: Females have their own resting spots (McClintock and Adler, 1978; McClintock et al., 1982b). It is possible that these pools of urine are olfactory signals that coordinate male turntaking during group mating. For example, after a male has ejaculated and returned to his resting spot, he is approached briefly by other males. It is known that the odor of male urine keeps other males at a distance (Gawienowski et al., 1976). Therefore, the approaching male may be more likely to keep at a distance after sniffing the resting male’s urine. This hypothesis is also consistent with the fact that males are less likely to approach each other late in the mating session when the resting place is heavily marked with the urine of previous ejaculatory series. During pair mating, when postejaculatory quiescence is artificially prolonged by the experimenter, the intervals between intromissions are shorter when mating first resumes (Beach and Whalen, 1959; Dewsbury and Bolce, 1970). A similar correlation occurs during group mating when the males’ postejaculatory quiescence is prolonged by male turn-taking; very short intervals between intromissions are common (McClintock and Anisko, 1982).

C. SENSORY REGCLATIONOF COPULATION Stone (1922, 1923) and Beach (1942) have shown that blind, deaf, or anosmic rats can still copulate successfully despite their sensory deficits. Both investigators concluded that none of these sensory modalities was essential for copulation in this species. Nonetheless, subsequent studies have shown that copulating rats do have distinctive displays, emit ultrasounds, and mark their environment with urine and secretions. Furthermore, other rats can detect these signals. Because the original tests of the effects of sensory deficits were conducted during pair mating in a small testing cage, it is possible that the simplicity of the

GROUP MATING IN THE DOMESTIC RAT

35

social and physical environment made multiple sensory signals superfluous. During the intricacies of group mating in a complex environment, sensory signals may play a more subtle role mediating mate choice, competition, and cooperation. I.

Olfactory Preferences

The literature on olfactory preferences is fraught with apparent contradictions, especially when they are considered in the context of pair mating. However, many, if not all of these are resolved when the data are reinterpreted in the social context of group mating. Both male and female rats prefer the odor of a partner that has not mated recently over the odor of one that has just copulated until ejaculation (Carr ef al., 1966; Krames and Mastromatteo, 1973). During group mating these odor preferences may mediate mate choice when there are several available partners. The male’s preference would make him more likely to give his partner her first ejaculation and therefore be less likely to waste his ejaculation when there is the risk of sperm competition from another male. The female’s preference would increase her likelihood of mating with a partner that still has a high sperm count, reducing her risk of pseudopregnancy. Males do not show any olfactory preferences or avoid their partner’s odor if they are tested before they ejaculate (Krames and Mastromatteo, 1973). However, when they are tested 2 min after their first ejaculation, males do avoid their partner’s odor, preferring the odor of a novel female, (Carr et al., 1970). After this, once the male begins a second ejaculatory series, his olfactory preferences disappear again (Krames and Mastromatteo, 1973). After later ejaculations, a preference for odors of a novel female reappears briefly, but is markedly attenuated (Carr et al., 1970). Thus, a male avoids the odor of his partner only during testing when his sperm is being transported. At this time, he runs the risk of inhibiting transport of his own sperm if he resumes mating with the same female. During group mating, the temporary olfactory preference for a different partner might reduce this risk. Furthermore, his preference for a novel partner is strongest when the risk of interfering with sperm transport is highest, that is, after early ejaculations when the sperm count of his ejaculate is high; it is not maintained when sperm count is likely to have dropped. A male rat responds to the female’s individual odor, not the odor of his own ejaculate; he avoids the odor of the individual female that received his ejaculation even when her odor sample is collected before mating begins (Krames and Mastromatteo, 1973). Males whose experience has been limited to monogamous or pair mating do not have any marked olfactory preference (2:l sex ratio, Carr et al., 1970). Olfactory preferences develop only if males have already had experience mating with several females (22 sex ratio, Krames and Mastromatteo, 1973; 5:2 sex

36

MARTHA K . MCCLINTOCK

ratio, Carr er a / . , 1970). This suggests that olfactory preferences are learned during group mating when males are no longer limited to mating with a female that is temporarily unreceptive because of her own postejaculatory quiescence and have the opportunity to continue mating with females that are still sexually active (McClintock et al.. 1982b). The male’s olfactory preferences may even reflect state-dependent learning, both because they are learned only in the presence of testosterone (Can et al., 1965) and because they are expressed only during his postejaculatory quiescence. In contrast to males, female rats that have only experienced monogamous mating prefer the odor of their partner over that of a stranger. This has been cited as evidence for “feminine fidelity” (1:l sex ratio, Carr et a/., 1979). However, if female rats have group mating experience, their “fidelity” vanishes (2:2 sex ratio, Krames and Mastromatteo, 1973). This suggests that female rats are not necessarily monogamous; they simply prefer a male that they know is a good mater over an unknown male. Female’s olfactory preferences are also different than the male’s once mating begins. Females do not have olfactory preferences immediately after receiving an ejaculation (with either pair- or group-mating experience; Krames er af.,1967; Krames and Mastromatteo, 1973). This is not surprising given that neither her chances for having a full litter nor the paternity of her offspring is affected by identity of the male that disrupts sperm transport. However, the identity of the male that gives her the ejaculation is critical; his dominance status affects the timing of her postejaculatory behavior during group mating. Because the urine of stressed and subordinate males has distinctive odors (Mackay-Sim and Laing, 1980; Krames e f crl., 1969) and because males mark their postejaculatory resting place with copious amounts of urine (see Section VI,B), a female could use this olfactory signal to determine the dominance status of a male that gave her an ejaculation. She could then use this olfactory information to alter the length of her own postejaculatory quiescence in order to reduce the proportion of her litter sired by a stressed or subordinate male (see Section V,B,2).

2.

Ultrusounds

Rats emit a variety of ultrasounds during copulation (Sales and Pye, 1974). Most research on the function of ultrasounds has focused on their role during pair mating. and not group mating. Nevertheless, it is likely that ultrasounds modulate the intricate social interactions of group mating when dominance relationships and individual differences are an integral part of successful copulation. After a male ejaculates. he becomes quiescent, returns to his resting place, and emits a 22-kHz call (Barfield and Geyer, 1972). Originally it was hypothesized that the male’s call inhibits female solicitations after an ejaculation and reduces the chance that the male will be induced to resume mating and interfere with transport of his own sperm (Barfield and Geyer, 1972). Because the female has

GROUP MATING IN THE DOMESTIC RAT

37

her own quiescence, ultrasonic calls are indeed grossly correlated with quiescence and with distance maintenance during pair mating (Geyer and Barfield, 1980). However, a detailed analysis of pair mating revealed that ultrasound is not the primary cause of female quiescence; females are as likely to solicit the male when he is calling as when he is not (Anisko et al., 1977). Furthermore, when mating involves several females, the females that do not receive an ejaculation continue to solicit the male during the time that he would be calling (McClintock et al., 1982b). The only quiescent female is the one that receives his ejaculation (McClintock et al., 1982b), indicating that stimulation from the male’s ejaculation is more critical for producing female quiescence than his postejaculatory call. Nonetheless, during group mating, the male’s 22-kHz call may indeed modify the female’s postejaculatory behavior. When females mate with more than one male, they resume mating more quickly if the ejaculation was from a subordinate male than they do when it was from a dominant male (see Section V,B,2). Because subordinate males are more likely to emit the 22-kHz call during an agonistic encounter or have experienced learned helplessness (Sales, 1972; Altenor et al., in preparation, cited in Adler and Anisko, 1979), it is possible that their postejaculatory ultrasonic calls are also longer or more frequent than the dominant’s. If so, females could use this auditory information to alter the length of their postejaculatory quiescence on the basis of the dominance status of the male whose sperm they were transporting. The ultrasonic signal might act in association with olfactory signals from the males postejaculatory urination (see Sections V,B,2 and VI,C, l), an association that has been reported in a variety of species and contexts (Floody ef al., 1977). Because the male’s 22-kHz call also reduces the probability of aggression from other males (Sales, 1972; Lore et al., 1976; Lehman and Adams, 1977; Adler and Anisko, 1979), it is also possible that it facilitates cooperation among males during group mating by mediating their turn-taking pattern (see Section V,C,l). The call is a reliable signal that the male is “in a socially withdrawn state” (Anisko et al., 1977) and is therefore not likely to interfere with the copulation of familiar males. It also might reduce the callers risk of being attacked once the other male becomes active and resumes mating. During copulation, male rats also emit a series of ultrasonic chirps with rapid changes in pitch (40-70 kHz, Sales, 1979) often called the 50-kHz call (Barfield et al., 1979). Because calls from a tethered or restrained male increase darting and hopping in females (McIntosh et al., 1978; Geyer et al., 1978a), it has been hypothesized that the primary function of the 50-kHz call is to stimulate the female to solicit the male. However, when a pair is copulating spontaneously, without artificial constraints sucy as tethering, 50-kHz calls by the male usually occur after the female has already begun her solicitation and during the runaway component when the male is chasing her (McClintock and Cogswell, un-

38

MARTHA K . MCCLINTOCK

published observations; Sales, 1972). Therefore, although 50-kHz calling may indeed facilitate darting, which occurs as part of the runaway component of solicitation, it does not appear to regulate the initiation of solicitation during pair mating. Nonetheless. during group mating, the 50-kHz call may also facilitate female approaches. The male is likely to emit the cafl as he approaches ejaculation (McClintock and Cogswell; unpublished observations, Barfield e f al., 1979). This is the time that female interceptions are most likely (McClintock et a / . , 1982b; see Fig. 13). This temporal correlation suggests that females may respond to the male’s 50-kHz call when he is chasing another female, and they may use this information to time their interceptions and receive his ejaculation. This hypothesis is also consonant with the observation that 50-kHz chirping declines with successive ejaculations (McClintock and Cogswell, unpublished observations; Geyer et a / . , 1978b) in parallel with the decline in female interceptions during group mating (see Fig. 14). D.

T H E COOLILXE EFFECT

A new partner can sometimes induce a male to resume copulation even after he has reached satiation with his original partner (Fisher, 1962; Wilson et al., 1963). This phenomenon has been termed the Coolidge Effect, in honor of an apocryphal story about President Coolidge and his cogent remark about a rooster mating in a barnyard full of hens (Bermant, 1976). It has been hypothesized that the function of the male’s behavior in the Coolidge Effect is to enable him to inseminate more than one female and increase his fitness (Daly and Wilson, 1978; Barash. 1979). Traditionally, the Coolidge Effect has been quantified by allowing a male to continue mating in a small cage with a single female until he stops copulating for a specified time period. Then a novel female is placed in his cage to test whether he will resume copulation. This classic protocol has yielded results that are somewhat less than robust [see the review by Dewsbury (1981b)l. Furthermore, the protocol does not incorporate the putative function of the male’s behavior since his new partner is introduced only after is is satiated and not likely to inseminate her because his sperm supply is depleted (Huber et al., 1980; Johnson et L J I . , 1980; Matthews, personal communication; Pessah and Kochva, 1975). Group mating may be closer to the contest in which the behavioral and neural mechanisms underlying the Coolidge Effect evolved. When there is more than one estrous female in the group (2:2 and 2:4), male copulatory behavior is increased so that a male has twice the number of ejaculations that he would have mating in a pair and four times the number mating in groups with a 2: 1 sex ratio (McClintock er al., 1982a). The Coolidge Effect may have been robust in these particular groups because the males were familiar with their various partners and

GROUP MATING IN THE DOMESTIC RAT

39

the environment allowed the female to pace copulation (kames, 1971; McClintock and Adler, 1978). A similar increase in the number of ejaculations has been reported when a single male mates sequentially with several females (Beach and Jordan, 1956; Fisher, 1962; Fowler and Whalen, 1961; Hsiao, 1965; Zucker and Wade, 1968; contra Tiefer, 1969). During group mating, males do not mate exclusively with one female until sexual exhaustion and then switch partners. They switch partners within an ejaculatory series and throughout the entire copulatory session (McClintock et al., 1982a; Tiefer, 1969; Zucker and Wade, 1968; k a m e s and Mastromatteo, 1973). This suggests that future investigation of the Coolidge Effect would profit by using testing procedures that more closely approximate the social pattern of group mating (McClintock, 1981). Under these conditions, the mechanisms that produce the Coolidge Effect may be more salient and replicable than the testing procedure which is restricted to the classic empirical definition of the phenomenon.

VII.

A.

PANOGAMY

DERIVATION AND DEFINITION

Domestic rats mating in groups are more than polygamous. In a polygamous mating system only one of the sexes has several mates (i.e., polyandry or polygyny), but in domestic rats, both males and females have several partners. Furthermore, in polygamous mating, copulation does not occur simultaneously with all partners: Copulation is completed with one partner and then resumes with another, often at a different place and time, whereas rats change partners repeatedly in the midst of copulation, even before there is an ejaculation. Promiscuity (“indefinite polyandry joined with indefinite polygyny”; Spencer, 1906) and polybrachygamy (multiple indiscriminate matings; Selander, 1972), are also inadequate terms for the same reasons. Furthermore, both terms have the connotation of randomness or disorder and fail to describe the rat on these grounds. When rats mate in a group, copulation is not at all disorderly but rather is socially coordinated among all members of the group in a nonrandom pattern. In turn, this pattern is elegantly coordinated with the neuroendocrine reflexes required for successful reproduction and can mediate cooperation, competition, and mate choice. Panogamy is therefore proposed here as a term to accurately describe mating systems that are like the behavior of domestic rats mating in a group. Its derivation is Greek: I T ~ V(pan: of the whole, altogether), yap00 (gamos: marriage), and an allusion to the Greek nature god, Pan, a guardian of flocks noted for his satyric escapades (cf. Synnott et al., 1981).

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MARTHA K . MCCLINTOCK

The essential feature of panogamous mating is copulation with more than one partner in a mating period. Therefore, in nonhermaphrodites, the male must have multiple intromissions before ejaculation or have multiple ejaculations. Both sexes have multiple partners and sex differences in the pattern of copulation are therefore likely. Furthermore, social structure will affect not only mate choice, but also the amount, distribution, and timing of copulation itself. The mating behavior of some other mammals is concordant with panogamy. Female sheep (Synnott er a f . , 1981), rhesus monkeys (Macaca mulatta, Kaufmann, 1965; Wilson et al., 1982). chimpanzees (Pan troglodytes schweinfurthii, Tutin. 1975), and Barbary macaques (Macaca sylvanus L., Taub, 1980) solicit copulation with more than one male during a single mating period. Furthermore, males in these species may also mate with several partners on a single day if there is more than one female in heat. Female colonial nesting birds are reported to have a high incidence of breeding synchrony; if so, males could mate with several females. In addition, each female may mate with several males [pukeko, Porphyrio p . melanotus (Craig, 1980); noisy miner, Manorina melanocephulu (Dow, 1979); acorn woodpecker, Melunerpes~ormicivorus(Stacey, 1979)], suggesting that panogamy may occur in avian species as well. B.

WILDNORWAYRATS Group mating has been imposed artificially on Norway rats (Rams nor-

vegic74s) by the breeding practices of some commercial laboratories. After artifi-

cial selection over hundreds of generations, domestic rats mate panogamously in a pattern that is well coordinated with the neuroendocrine systems of both sexes. Did commercial breeders create a panogamous system artificially or did they find that panogamy or group mating was an efficient breeding protocol because it was based on an established mating system used by wild rats? The difference between social behavior of wild and domestic males suggests that some feature of group mating may be the result of artificial selection. Wild males are usually observed chasing an estrous female as a pack [termed a rush (Robitaille and Bouvet, 1976)l rather than turn-taking. This may be because a rush of males is dramatic and more readily observed at night in the field than turn-taking would be. Nonetheless, the striking difference between this and the behavior of domestic males suggests that turn-taking only occurs when there are two familiar males mating together (cf. Barnett et al., 1979) and may have rcsultcd from artificial sexual selection at the group level during domestic breeding. On the other hand, the wild strain has a greater sex difference in the preferred pattern of copulation than the domestic strain does, suggesting that wild rats can have a panogamous mating system. For example, wild males prefer to mate at even shorter intervals than domestic males do; wild females prefer to mate at

GROUP MATING IN THE DOMESTIC RAT

41

longer intervals than domestic females do (see Fig. 16; McClintock and Adler, 1978). Since panogamous mating permits sex differences in the pattern of copulation, wild rats may be panogamous under some conditions. There is a paucity of good field work on wild Norway rats, making it difficult to do more than speculate about the answer to the question. Furthermore, wild rats are found in such a variety of habitats and group structures that it is clear that

Wild

d Dom d

Wild

9

WiIddDomd Wild

9

W i l d d Dom d Wild

IJ

Wild

6 Dom d

Dorn Q

Wildd Domd Dorn

Wild

d

0

Dom d

Dom 0

FIG. 16. The pattern of copulation is affected more by the strain of the female than it is by the strain of the male. In addition, domestication has had the opposite effect on the two sexes. For example, domestication has shortened the interval between intromissions for females and lengthened it for males, indicating that sex differences are likely to be greater in the wild strain. (Figure drawn from data presented in McClintock and Adler 1978).

42

MARTHA K . MCCLINTOCK

there is no single social or mating system that characterizes the species. Nonetheless. it is generally acknowledged that wild Norway rats are “contact animals” (Barnett, 1958; Heidiger. 1950; see Fig. I ) . Although wild rats have been found living alone or in pairs, it is more common to find them in large burrows, in groups ranging from 7 to 100 or more individuals (Calhoun, 1962; Telle, 1966; Steiniger. 1950). Furthermore. Calhoun t 1962) observed that wild rats produce substantially more litters when they live in multifemale groups than they do living alone or in pairs. He also attributed dominance to a group of males living with femaleh, not to individuals. An estrous female in the field is usually mounted by several different males during a single night (Barnett, 1958; Calhoun, 1962; Robitaille and Bouvet, 1976; Steiniger, 1950: Telle, 1966). It is also likely that there will be several females in heat if the group is large because females outnumber males among adults of reproductive age (Calhoun, 1962: Davis, 1951; Leslie et ul., 1951). Furthermore, several females often occupy the same territory or burrow and attract males from surrounding areas when they are in heat; a sex ratio of 2 - 3 5 - 8 is common (Calhoun, 1962; Davis, 1955; Schein, personal communication). Therefore, it is possible that multimale-multifemale mating may occur in the wild, particularly if there is any tendency for females to come into heat on the same night (McClintock, 1978, 1983), creating the social context for a panogamous mating system. Acknowledgments

I am indebted to S . Arnold and M. Wade for invaluable discussions of group selection. to F. Beach and the editors for their occasionally delightful critiques of an earlier draft. and to T. Larson Butler, K. Rebtifo. and T. Ziporyn for their help with manuscript and figure preparation. This work was supported hy grant5 from the National Science Foundation (BNS 80- 19496) and the Public Health Seivice (PHS 5 R23AG024OX). References Adler, S . T. (1969). Effects of the male’s copulatory behaviour on successful pregnancy 01 the female rat. J . Comp. Physiol. Phwhoi. 69, 613-622. Adler. N. T . . and .4nisko. J . (1979). The behavior of communicating: A n analysis of the 22 kHz call of rats (Ruttrrs non~eyicrrs).Am. Zoo/. 19, 493-508. Adler, N. T.. and Zoloth. S . R . (1970). Copulatory behavior can inhibit pregnancy in female rats. Science 168, 1488. Allte. W . C. (1938). .‘Cooperation Among Animals.” Schuman. Ncw York. Anisko. J . J . , Adler. N. T . . and Suer. S . (1979). Pattern of post-ejaculatory urination and sociosexual behavior in the rat. Beha\,. Neirrul. Biol. 26(2). 169-176. Anisko. J . J . . Suer. S. F McClintock. M. K . . and Adler. N. T. ( 1977). The relationship between 22 kHr ultrasonic signals and sociosexual behavior in the rat. J . Comp. Physiol. Psycho/. 92, 82 I - 829. Arnold. S. (19761. Sexual behavior. sexual interferences and sexual defense in the salamanders Ainhy,tomu tiyrinirm and Plethodoti jordani. Z. Tierpsychol. 42, 247-300.

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McClintock. M. K., and Adler, N. T. (1978). The role of the female during copulation in wild and domestic Norway rats (Rotrus noncqicrrs). Behmioirr 67, 67-96. McClintock. M. K . , and Anisko, J . J . (1982). Group mating among Norway rats. I. Sex differences in the pattern of copulation. Anim. Behar. 30(2), 398-409. McCIintock, M. K . , Anisko. J . J . , and Adler, N. T. (1982a). Group mating among Norway rats. 11. The Social dynamics of copulation: Competition. cooperation, and mate choice. Anim. Behuv. 30, 410-425. McClintock. M. K . , Toner, J . P., Adler, N. T., and Anisko. J . J . (198%). Postejaculatory quiescence in female and male rats: Consequences for sperm transport during group mating. J . Comp. PhIsiol. Psychol. 96, 268-277. Mclntosh, T . K., Barfield, R. J . , and Geyer, L. A. (1978). Ultrasonic vocalizations facilitate sexual behaviour of female rats. Nature (London) 272, 163-164. Mclntosh. T . K . , Davis, P. G.. and Barfield. R. J. (1979). Urine marking and sexual behavior in the rat (Rartus tior\*rqicrts). Bekav. Neural Biol. 26, 161- 168. Mackay-Sim. A , . and Laing. D. G. (1980). Discrimination of odors from stressed rats by nonstressed rats. Physiol. Behuv. 24, 699-704. Madlafoukk, J.. and Hliiiak, 2 . (1978). Sexual behaviour of the female laboratory rat: Inventory, patterning, and measurement. Behaviour 63(3-4). 129- 174. Masters, R. (1978). Of marmots and men: Animal behavior and human altruism. I n “Altruism, Sympathy and Helping: Psychological and Sociological Principles” (L. Wispe, ed.), pp. 59-77. Academic Press. New York. Matthews, M . , and Adler. N . T . (1977). Facilitative and inhibitory influences of reproductive behavior on sperm transport in rats. J . Camp. Physiol. Psychol. 91, 727-741. Mayr, E. (1958). Behavior and systematics. In “Behavior and Evolution” (A. Roe and G. G. Simpson. eds.). pp. 341-362. Yale University Press, New Haven, Connecticut. Meyerson. B. J . . and Lindstrom, L. H . (1973). Sexual motivation in the female rat. Actu Physiol. Scund. Sicppl. 389, 1-80. Mosig. D. W., and Drwsbury. D. A. (1970). The behavior of rats during copulation as a function of prior copulatory experience. Psychon. Sci. 21(3). 141- 143. Packer. C.. and Pusey. A. E. (1982). Cooperation and competition within coalitions of male lions: Kin selection or game theory’? Nature (London) 296(5859), 740-742. Parker. G. A . (1970). Sperm competition and its evolutionary consequences in the insects. Biol. Rev. 45, 525-568. Peirce, J . T . , and Nuttall, R. L. (1961). Self paced sexual behavior in the female rat. J . Comnp. Physiol. Psychol. 54, 3 10-31 3. Pessah. H.. and Kochva, E. (1975). The secretory activity of the seminal vesicles in the rat after copulation. Biol. Reprod. 13, 557 560. Price. E. 0. (1980). Sexual behavior and reproductive competition in male wild and domestic Numay rats. . h i m . Behur, 28, 657-667. Robb, G . W.. Amann, R. P.. and Killian. G . J . (1978). Spcrm production and cpididymal sperm reserves of pubertal and adult rats. J . Reprod. Fertil. 54, 103-107. Robitaille. J . A , . and Bouvet. J. (1976). Field observations on the social behaviour of the Norway rat. Ratrus nonsericus (Berkenhout). Biol. Bchuv. 1, 289-308. Rodgers, C. H . (1970). Timing of sexual behavior in the female rat. Endocrinology 86, 1181. Sachs. B . D.. and Barfield. R. J. (1970). Temporal patterning of sexual behavior in the male rat. J . Comp. P h s i o l . P.\)c.hol. 73, 359-364. Sachb. B. D.. and Barfield. R . J. (1974). Copulatory behavior of male rats given intermittent electric shocks: Theoretical implications. J . Comp. Physiol. Pswhol. 86, 607-615. Sachs. H . I).. and Barfield. R. J . (1976). Functional analysis of masculine copulatory behavior in the rat Adv. Studv Behail. 7 , 91-154.

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Sales (nee Sewell), G. D. (1972). Ultrasound and aggressive behavior in rats and other small mammals. Anim. Behav. 20, 88-100. Sales, G. D. (1979). Strain differences in the ultrasonic behavior of rats (Rafrus norveqicus). Am. Zool. 19, 513-527. Sales, G. D., and Pye, D. (1974). “Ultrasonic Communication by Animals.” Wiley, New York. Selander, R. K. (1972). Sexual selection and dimorphism in birds. In “Sexual Selection and the Descent of Man” (B. Campbell, ed.). Aldine, Chicago. Sharma, 0. P., and Hays, R. L. (1975). Heterospermic insemination and its effect on the offspring ratio in rats. J . Reprod. Fertil. 45, 533-535. Short, R. V. (1979). Sexual selection and its component parts, somatic and genital selection, as illustrated in man and the great apes. Adv. Study Behav. 9, 131-158. Spencer, H. (1906)( “Principles of Sociology,” Vol. 1, 3rd ed., p. 654. Appleton, New York. Stacey, P. B. (1979). Kinship, promiscuity and communal breeding in the Acorn Woodpecker. Behav. Ecol. Sociobiol. 6, 53-66. Steiniger, von F. (1950). Beitrag zur Soziologie und sonstigen Biologie der Wanderratte. Z . Tierpsychol. 7, 356-379. Stone, C. P. (1922). The congenital sexual behaviour of the young male albino rat. J . Comp. Psychol. 2, 95-153. Stone, C. P. (1923). Further study of the sensory functions in the activation of sexual behavior in the young albino rat. J . Comp. Physiol. 3, 469-473. Synnott, A. L., Fulberson, W. J., and Lindsay, D. R. (1981). Sperm output by rams and distribution amongst ewes under conditions of continual mating. J . Reprod. F e d . 61, 355-361. Taleisnik, S., Caligaris, L., and Astrada, J. J. (1966). Effect of copulation on the release of pituitary gonadotrophins in male and female rats. Endocrinology 79, 49. Taub, D. M. (1980). Female choice and mating strategies among wild Barbary macaques (Macaca sylvunus L . ) . In “The Macaques: Studies in Ecology, Behavior, and Evolution” (D. G. Lindburg, ed.), pp. 287-344. Van Nostrand Reinhold, New York. Telle, H. J. (1966). Beitrag zur Kenntnis der Verhaltenweise von Ratten, vergleichend dargestellt bei Rattus norveqicus und Rattus r a m s . Z . Angew. Zool. 53, 129-196. Terkel, J., and Sawyer, C . H. (1978). Male copulatory behavior triggers nightly prolactin surges resulting in successful pregnancy in rats. Horm. Behuv. 11, 304-309. Thor, D. H. (1979). Olfactory perception and inclusive fitness. Physiol. Psychol. 7(3), 303-306. Thor, D. H. (1980). Isolation and copulatory behavior of the male laboratory rat. Physiol. Behav. 25, 63-61. Thor, D. H., and Cam, W. J. (1979). Sex and aggression: Competitive mating strategy in the male rat. Behav. Neural Biol. 26, 261-265. Thor, D. H., and Flannelly, K. J. (1977). Social-olfactory experiences and initiation of copulation in the virgin male rat. Physiol. Behav. 19, 411-417. Thor, D. H., and Flannelly, K. J. (1979). Copulation and intermale aggression in rats. J . Comp. Physiol. Psychol. 93, 223-228. Tiefer, L. (1969). Copulatory behaviour of male Ratrus norveqicus in a multiple-female exhaustion test. Anim. Behav. 17, 718-721. Timmermans, P. J. A. (1978). Social Behavior in the Rat. Unpublished doctoral dissertation. The Catholic University of Nijmegen, The Netherlands. Trivers, R. L. (1972). Parental investment and sexual selection. In “Sexual Selection and the Descent of Man” (B. Campbell, ed.). Aldine, Chicago. Tutin, C. E. G. (1975). Exceptions to promiscuity in a feral chimpanzee community. In “Contemporary Primatology.” Karger, Basel. Vehrencamp, S. L. (1979). The roles of individual, kin and group selection in the evolution of sociality. In “Handbook of Behavioral Neurobiology: Social Behavior and Communication” (P. Marler and J. C. Vandenbergh, eds.), Vol. 3. Plenum, New York.

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Vehrencanip. S. L. (1980). To skew or not to skeu. Proc. I n r . Omithol. Crtngr. 17th pp. 869-874. Ventura. W . P., and Freund. M. (1969).An in 1,itr.ostudy of the effects of rat semen and accessory gland secretions on female reproductive tract of rats. Fed. Proc. 28, 637. Wade. M. J . (1977). An experimental study of group selection. Evolution 31, 134-154. Wade. M J . (l97X). A critical review ofthe models of group selection. Q. Rev. B i d . 53, 101-1 14. Weick. R. F.. Smith. E. R . Domininguez. R . , Dhariwal. A. P. S., and Davidson, J . M. (1971). Mechanisn of stimulatory feedback effect of estradiol on the pituitary. Endocrinology 88, 293-301 Weir. B . J . , and Roulands, J. W . (1973). Reproductive strategies of mammals. Annu. Rev. Ecol. S v s f . 1, 139-163. Wilcoz. J . R.. Kuehn. R. E., and Beach, F. A. (1963). Modification in the sexual behavior of male rats produced by changing the stimulus female. J . Comp. Physrol. Psxchol. 56, 636-644. Wilson. M . E . , Gordon, T. P . . and Chikdzawa, D. (1982). Female mating relationships in rhesus monkeys. Am. J . Primoinl. 2, 21-27. Winisatt. W . ( 1980). Randomness and percewed-randomness in evolutionary biology. Synthesc 43, 287-329. Zuckcr. I . . and Wade. A . (1968). Sexual preferences of male rats. J. Comp. Physiol. Psycho/. 66, 816-819.

ADVANCES IN THE STUDY OF BEHAVIOR. VOL. 14

Plasticity and Adaptive Radiation of Dermapteran Parental Behavior: Results and Perspectives MICHELVANCASSEL LABORATOIRE ETHOLOGIE LA

373 CNRS

UNIVERSITE DE RENNES I, CAMPUS DE BEAULIEU RENNES CEDEX, FRANCE

I. Introduction . . . . ............................................ 11. The Development of Parental Behavior . . . . . . . . . . . . ......... A. Ethological Approach.. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . B. Physiological Correlations of Parental B C. Hormones and Control of Parental Beha .................. 111. The Adaptive Radiation of Parental Behavior A. Interspecific Comparisons. . . . . . . . . . . . B. Intraspecific Comparison: The Case of Forficulu auriculal-ia . . . . . . . . IV. Relationship between Development and Adaptive Radiation . . . . . . . . . . . . . A. Conditions for the Development of Parental Behavior in Forjicula auricularia . .......................................... B. Outline for no ........................... ... V. The Study of Parental Behavior: Illustration of Which Theories? . . . . . . . . . A. Which Conception of Behavior? ............................... B. Behavior Considered as Systems Dynamics ...................... References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

I.

51 52 52

58 60 63 63 71 74 74 75 78

INTRODUCTION

The aim of this article is to describe the relationships between phenotypic plasticity through development and intra- and interspecific radiation specifically in regard to dermapteran parental behavior. The preference for the terms development and radiation rather than ontogeny and evolution is really only a pretext for the remarks which follow. First, ontogeny generally means the processes of behavioral elaboration in one individual from conception until adulthood, whereas this article will concern mainly adults, and specifically, dynamics of their reproductive cycle. Second, the great majority of studies on behavioral ontogeny concern “higher” animals, 51

Copyright 0 1984 by Academic Press, Inc All nghts of reproducuon in any fwm reserved ISBN 0-12-0045 14-1

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MlCHEL VANCASSEL

mainly mammals, where mother-infant relationships imply a type of social bond (psychosocial level) that is not found in insects (biosocial level) (Schneirla and Rosenblatt, 1961; Tavolga, 1970). Radiation refers here to the variations in parental behavior observed within the limited and fairly uniform evolutionary branch of the Dermaptera, particularly to variants that are revealed at the intraspecific level. This section will therefore be guided by the question of behavioral transformations linked with speciation, in particular Darwinian behavioral adaptations “arising from the conventional Darwinian mechanism of selection upon genetic variation” (Gould and Lewontin, 1979). The limited question of relations between development and adaptive radiation in behavior falls within the much wider one concerning parallels between ontogeny and phylogeny. To outline the issues very briefly, it should be said that the discredit into which recapitulation theories have fallen, reducing ontogeny to a consequence of phylogeny, is far from sufficient to rule out mutual constraints between phylogeny and ontogeny (Gould, 1977), even though such constraints are mentioned too rarely when behavior (Richard, 1979)-and particularly insect behavior (Topoff, 1 9 7 2 t i s considered. This question cannot be investigated, on a methodological level, without referring simultaneously to ethological, physiological, ecological, and comparative data. Not surprisingly, the study of behavior has the interdisciplinary status of “synthetic science” as soon as it is defined in a broad sense as “a very complex process of functional interaction between the organism and its environment” (Kuo, 1970). An attempt is made below, first, to describe the development of dermapteran parental behavior, then to examine this process within the context of intra- and interspecific adaptive radiation, and, last, to discuss the theoretical implications of this epigenetic approach.

11. A.

THEDEVELOPMENT OF PARENTAL BEHAVIOR

ETHOL.OGICAL APPROACH

The first experimental study on Forjicula n u r i c h r i a parental behavior was published in 1929 by Weyrauch. Besides specifying the different stages of the parental phase, Weyrauch analyzed the conditions underlying the expression of the capacity of the female to care for eggs, and by using dummies he showed the necessity for eggs to be smooth and round. He obtained the continuation of care by renewing the eggs after hatching and the disappearance of care by prematurely and abruptly removing the eggs. However, considering instinct as a sequence of reflexes precisely aimed ( “Auf ein bestimmtes Ziel gerichtete Reflexflogen,” p. 544). he interpreted his results in complex and abstract terms, in which the

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instinct to care for eggs was opposed to the instinct to consume eggs. He accounted for the changes in the female’s behavioral tendencies by distinguishing central manifestations, which can be more or less important, but are always present, from the motor manifestations of these two instincts which appear only when central manifestations reach above a certain level. Studying this behavior in the species Labiduru ripariu, Vancassel (1973a) showed, in a preliminary investigation, that the imaginal life of females is composed of a regular succession of two very contrasting behavioral phases: during the first phase, the female eats, mates, and, because earwigs are nocturnal, spends the days in temporary shelters. During the second phase, the female fasts, isolates herself in a closed subterranean nest where she lays eggs, and then cares for her eggs and nymphs. During this parental phase, four important moments when the female’s behavioral tendencies change can be recognized: first, simultaneously with burrowing, the female becomes able to care for eggs and no longer eats them. Then, while tending her eggs, the female becomes able to accept the presence of newly hatched nymphs without attacking and eating them. After the nymphs have hatched, the female loses her readiness to care for eggs and her usual oophagy reappears. Last, the female loses her readiness to accept nymphs at the end of the parental cycle, after rapid nymphal dispersal (Vancassel, 1973b). The emergence of parental responsiveness appears as the effect of sexual behavior, which occurs when a particular physiological state is reached by the female at the end of vitellogenesis. Parental responsiveness is also associated with important changes in the female’s physiological state, characterized by the beginning of a long fast (Vancassel, 1973~).The maintenance of this parental state depends both on this new physiological condition and on the presence of eggs. The continuation of this state leads, in turn, to the initiation of the female’s ability to accept nymphs, and besides, prepares her for the hatching of the eggs. Hatching, in removing the eggs, induces the disappearance of care for eggs; by causing the emergence of nymphs, hatching enables the ability to accept nymphs to be expressed and maintained. Last, dispersal of the nymphs and the resumption of feeding lead in turn to the disappearance of the tendency to accept nymphs, and therefore to the end of the parental cycle. Vitellogenesis, accompanied by the resumption of feeding, is the first phase of the next parental cycle (Vancassel, 1977). The parental sequence in the female is, therefore, a succession of interactions between physiological and behavioral conditions as well as between these and environmental stimuli (male, eggs, nymphs). The diagrammatic representation of these interactions (Fig. 1) is equivalent to the reconstitution of the parental cycle as a whole. Also, it is obvious that the sequence detailed above is elaborated step by step: each stage is prepared by the immediately preceding one and leads in turn to the following stage. Therefore we believe we are justified in

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MICHEL VANCASSEL

__---

__---------FEEDING

r-.--

I

1 /BURROW OPENING, -EGGSCOPULATION EGG LAYING=+EGGS

W S l T l V E REACTION TOWARD N Y M P H S

I

I -

FIG.1 . Development of the parental cycle. Solid lines, positive relations; broken lines, negative relations. (After Vancassel, 1977.) concluding, as did Rosenblatt and Lehrman (1963) at the end of their study of rat parental behavior, that ‘‘the successive phases of the maternal behavior cycle are related to one another through the development of these interrelationships. This identical conclusion concerning behaviors with the same biological outcomes but for species from different phylogenetic levels is probably linked to the similarity of methods. When starting to study parental behavior in Lubiduru riparia, i deliberately adopted methods simiiar to those followed in the papers, now considered classic, on reproductive behavior in the rat (Rosenblatt and Lehrman, 1963), dove (Lehrman, 1964), and canary (Hinde, 1965). This method is summarized by the following: “The processes underlying the organization of the behavior of an animal at any developmental age, or at any stage of a cyclically-varying pattern, appear to us to be best illuminated by analysing the ways in which that age (or stage) has arisen from preceding ones, and the ways in which that age (or stage) influences or gives rise to succeeding ones” (Rosenblatt and Lehrman. 1963, p. 9) and “however narrow the problem may be, it is essential to remember that development involves a nexus of causal relations, with action, reaction and interaction, both within the organism and between organism and environment, at every stage” (Hinde, 1966, p. 425). Agreeing with an epigenetic conception of behavior, Kuo (1970) wrote, “In the total response behavior of the organism [where] the overt or gross movement is merely an integral part, [the notion of] behavior gradients [corresponds to] the differentiations of intensity and extensity among the different parts of body” (p. 189). Here the analysis of the development of parental behavior leads us to infer the existence of numerous physiological mechanisms regulating behavior and suggests strongly that ovarian physiology, taken in its wide sense (alternating feeding and fasting, vitellogenesis, implied neuroendocrine regulation, etc.), constitutes one of those “behavior gradients.” Concretely it can be said that ”

PLASTICITY AND RADIATION OF PARENTAL BEHAVIOR

55

these regulating mechanisms are activated each time that, by experimentally manipulating the female’s external and/or internal conditions, one of the pivotal events described above (Fig. 1) is suppressed, advanced, or delayed. It must be noted also that, in this perspective, “the question of intervening variables in the physiological sense or the question of motivation ceases to exist for they are parts of the pattern of behavior gradients.” Simultaneously, “we are inclined to think that under the concept of behavior gradients, physiology will become meaningless unless it is merged with and becomes part and parcel of the science of behavior” (Kuo, 1970). Hinde and Stevenson (1971) adopted a similar attitude when they stressed an interest in the causal analysis of behavior and recommended abandoning notions such as drive. Where classic ethological analysis only infers the existence of regulatory mechanisms in behavior, causal analysis aims to decipher these mechanisms.

CORRELATIONS OF PARENTAL BEHAVIOR B . PHYSIOLOGICAL Earwig ovarian physiology, marked by a succession of active vitellogenesis phases and resting phases, the latter corresponding to the parental period, has not failed to interest insect physiologists, and particularly endocrinologists. Lhoste (1957) introduced the notion of a “physiological state predisposing Forficula auriculariu females to care for eggs” thus allowing a reinterpretation of Weyrauch’s data. In recent years, many physiological correlates of the parental phase have been described in Labidura riparia. First Caussanel (1974) described different aspects of the corpus allatum (CA) and pars intercerebralis (PI) during vitellogenesis and the period of ovarian nondevelopment. The volume of the CA is large during vitellegenesis and very small while eggs are tented. The neurosecretion rate (A cells) of the PI is high during vitell%enesis and low during care of eggs. Rouland (1979) described synchronous fluctuations of hemolymphatic vitellogenine during the reproductive cycle. Caussanel and Dresco-Derouet (1972) established that the period of care is marked by a low rate of oxygen consumption (QR = 1.11) compared with the vitellogenesis phase (QR = 0.80). Last, the levels of hemolymphaticjuvenile hormone (JH3) and ecdysteroids complete the picture: They are high at the beginning of vitellogenesis, but the levels of these two types of hormones fall during the nesting phase (Caussanel et al., 1979; Caussanel and Karlinsky, 198 1; Baehr et al., 1982). However, in spite of their obvious interest, these studies, aiming at a better understanding of the mechanisms regulating vitellogenesis, do no more than demonstrate physiological correlations of parental behavior. Although the physiological mechanisms are well documented, their relationships with behavior including action, reaction, and interaction still need to be investigated.

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MICHEL VANCASSEL

1

3

5 7 9 Day after laying

11

13

FIG.2 . Levels of hernolymphatic juvenile hormone during the parental phase in Labiduro ripcrricz. (0) Controls; (0) isolated females; ( + ) females with food:).( fed controls. l h e single diamond ( + ) pools observations from I I females having clearly neglected their eggs (two consecutive daily observations, following the sixth day after laying ). Surgery (taking samples of hernolymph and ovaries and controlling effective feeding) was performed beheen the seventh and thirteenth days after laying, based on the pools observations from 9 females with food who did not female. The single square neglect their eggs before the surgery. These females had not eaten at all in spite of the presence of food (“fed controls”) before the surgery on the seventh and ninth days after laying. Each of the other points pools observations of 8 to 12 females operated the same days. (After Strambi ef a / . , 1983.)

(m)

BEHAVIOR C . HORMONESA N D CONTROLOF PARENTAL Pierre‘s work (1979) written from this perspective showed that the female’s parental predisposition to remain in the nest is significantly prolonged after the eggs have hatched if the corpora allata have been removed. As we have seen (Section I,A), under conditions allowing the normal manifestation of the parental sequence, the maintenance of the female’s tendency to care for eggs is dependent both on the female fasting and the presence of eggs. Regular introduction of food into the burrow induces the female, when she eats, to abandon her eggs; parental tendencies disappear in spite of the presence of eggs. Removing the eggs for 48 hr the day after they are laid induces a similar disappearance of parental behavior, although the female continues to fast (Van-

PLASTICITY AND RADIATION OF PARENTAL BEHAVIOR

57

cassel, 1974). By radiotagging juvenile hormone and radioimmunoassays (Strambi et al., 1983) the variations in the titers of this hormone can be followed for the three situations described (Fig. 2): ( I ) control females: presence of eggs and fasting; (2) isolated females: eggs removed and fasting; and (3) females with food: presence of eggs and food. Simultaneous measurements of the ovary characterize different stages of vitellogenesis (Fig. 3). As expected, control females and females with food that do not eat do not show any ovarian development, and the levels of their circulating juvenile hormone remain very low during the entire undisturbed phase of their caring for eggs. In contrast, females that eat show, concurrently with neglect of their eggs (Fig. 2), an increase in vitellogenetic activity associated with a high level of circulating juvenile hormone. Similarly, females isolated from their eggs (over 60% of them lose their readiness to care for eggs after 48 hr and 100%after 72 hr) exhibit, after a similar delay, transitory vitellogenetic activity, as well as transitory high levels of circulating juvenile hormone. The change in vitellogenetic activity following removal of the eggs seems to be linked with the rapid disappearance of the reserves in the females that continue to fast. It is well known that in Labidura riparia vitellogenesis is interrupted very quickly follow-

-

11c!

'

1

3

5

7

9

Day after laying

11

13

FIG.3. Ovarian development during the parental phase. (0)Controls; (I?) isolated females; ( + ) females with food; (H) fed controls. (Same conditions as for Fig. 2). Ovarian development is measured here by the ratio of apparent surfaces of the ovocyte and of the trophocyte. During nearly all vitellogenesis, the trophocyte remains the same size, whereas the ovocyte grows enormously. (After Strambi et al., 1983.)

58

MlCHEL VANCASSEL

ing an alimentary deficiency. The necessity for fasting and for the presence of eggs to maintain parental care is thus verified: these results indicate, besides, that the presence of eggs intervenes in ovarian physiology by inhibiting it. In contrast, feeding, by stimulating the premature recovery of vitellogenesis, interrupts care of the eggs in spite of their presence. In paraphrasing Hinde and Stevenson ( 197 1 ) we can say: “nous voici loin maintenant de la simple pulsion B soigner les oeufs . . . Les changenients de comportements paraissent dipendre d’interactions complexes entre les stimulus externes et les facteurs internes a I’Cchelle de I’organisme et du systhme nerveux.”

111.

THEADAPTIVE RADIATIONOF PARENTAL BEHAVIOR

Although taxonomists have cataloged over 1700 (Sakai, 1982) living species of Dermaptera, the natural history of only about 20 of them is known. However. this small sample includes representatives of most of the families of this group, from those considered to be the most primitive (Diplatyidue) to those considered to be the most evolved (Forficulidae), so that Chopard (1949) and later Beier ( 1959) considered maternal behavior to be a characteristic of this group. If the structural homogeneity and the ancient origins of this insect order, attested by the Jurassic fossil gpecies Protodiphr?,sfortis. are taken into account, all the species now living can be considered to have derived from a common ancestor and there is a good chance that parental behavior has a single phylogenetic origin. From the point of view of comparative studies, this situation is favorable: The advantage o f working on related species largely compensates for the small variation in form due to rather limited evolutionary radiation. A.

INTERSPECIFIC COMPARISONS

Two types of interspecific differences appear as soon as a comparative study is undertaken. One concerns the mechanisms regulating identical behavioral forms such as the onset of the behavioral ability to care for eggs. For some species such as Lubiduru ripuria. the effect of sexual behavior upon the internal conditions prevailing at the end of vitellogenesis elicits, as we have seen above (Section [ , A ) , the appearance of the ability to care for eggs. However, for other species, such as Forficuh auricularia, sexual behavior plays no part in this process. These earwigs undergo a classical diapause: in this case exposure to cold establishes the parental tendencies. Nevertheless, in spite of their obvious evolutionary interest. and although they seem to constitute adaptations of species to their environment.’ without any data we are, for the time being, totally unequipped to ‘Thc species that present the Lubidirru ripuria type of regulation are all mediterranean or tropical, whereas those presenting the Forjliculo artricrrlaria type live in temperate regions or under a subalpine climate.

PLASTICITY AND RADIATION OF PARENTAL BEHAVIOR

59

deal with differences of this type. Other differences which concern the form of the parental cycle can, in some cases, be analyzed. For example, the second part of the parental cycle, when the female stays in contact with her nymphs, takes more different forms than the care-for-eggs phase which hardly varies from one species to another. Thus reproductive strategies can be divided into three main categories: 1. The Lubiduru riparia type where a rapid dispersal of nymph is related to the occurrence of several successive parental cycles by the same female. In the field this leads to a reproductive strategy characterized by several cohorts and at least two generations a year. 2. At the other extreme, nymphs of species such as Anechuru bipuncrutu remain with their one brood-producing female for several instars, and even until their imaginal molt if the female survives long enough. There is only one cohort and therefore only one generation a year. 3. Species such as Forficulu uuriculuriu adopt a mixed and intermediate solution. Some females for each population remain with their nymphs and undergo only one parental cycle, whereas others (not so many), after being isolated (usually after the first nymphal molt), lay and care for a second brood. This reproductive strategy is characterized by the presence of two cohorts but only one generation a year. Differences at the ovarian level can be related to these behavioral differences. Only Lubiduru riparia females have a germarium (continuous production of ovocytes) that remains active during all their imaginal life, whereas the ovary of Anechuru bipuncrutu females is empty after their one and only batch of eggs has been laid (functional castrates). Forficulu uuriculuriu females, although they do not possess a germarium, do have the possibility of laying several successive batches of eggs. Finally, these three species live in different environments with important climatic differences (Fig. 4): Lubiduru riparia is a Mediterranean species, Forficulu uuriculuriu is from a temperate climate, and Anechuru bipuncrata is from a subalpine climate. The 10 species it has been possible to study in the laboratory all fit in with one or another of the three strategies of these species: They present the ovarian characteristics and live under the climatic conditions that seem to be linked with each of them in nature (Vancassel and ForastC, 1980a). This comparative survey reveals the limits of the parallel and apparently complimentary differentiation of the ovarian organization and physiology and parental behavior in relation to environmental factors. Nevertheless, beyond this statement, analyses on this interspecific level only lead to conjunctures on the mechanisms of this adaptive radiation of behavior. Intraspecific comparison of populations from different environments can prove very profitable in pursuit of our objective.

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-J

F M A M J J A S O N D

(A);

FIG.4 . Average monthly temperatures for Lnbiditra riparia, ”Camargue” For~fi’rulacturicrtlrrrici “Pack” ( 0 ): Forfcula arrriculariri “Font Romeu,” Cheliduru prennii.[j ( = Atzrchrtrci hipum~attr)(0). (After Vancassel and Foraste. 19802.)

B.

INTRASPECIFICCOMPARISON: THE CASEOF F O R ~ I C U L A ALIRICULARIA

I. Di’ereiit

Forficula Populuticrns; Their Characteristics

Forficula auricdaria is distributed widely over Europe (Van Heerdt, 1946).2 The characteristics of the population called “Pace,” taken as representative here, coincide completely with those described for other populations from France (Lhoste, 1957) or Germany (Weyrauch. 1929). Similar characteristics have been described for different North American populations (Fulton, 1924; Crumb, 194 1; Lamb and Wellington, 1975; Lamb, 1976a). In Europe, the blanket-like distribution of FO$C14/U ciuricularia is interrupted where there are mountains since this species never seems to colonize above 1800-2000 m high (Weyrauch, 1929; Van Heerdt, 1946). At its range limits, Farficitln ciiiricularin develops particular marginal populations: Two of them have been followed for several years. The first one, called “Font Romeu” is from the Pyrenees. just above 1600 m. and is sympatric with the typical mountain species Chelitlirra pyenaica. The second one called “Les Combes” is from -Of European origin. Forficwtn rrttric.i~/urinwas introduced by man into many countries. In North America it is found in regions as different, from a cliniatic point of view. as British Columbia (Lamb, 1975) and Quebec (Vickery rr a / . . 1974). The success of this species under highly contrasted ecolosgical conditions could be the framework for a very interesting natural experiment.

PLASTICITY AND RADIATION OF PARENTAL BEHAVIOR

61

the Alps, just above 1800 m, and is sympatric with Anechuru bipunctutu. These two populations undergo similar subalpine climates, characterized by a long winter snow-cover and a short summer with a low mean temperature (Fig. 4) mainly due to cool nights. Everything indicates that these populations produce only one brood and only one cohort a year. For example, “Font Romeu” nymphs, hatching at the beginning of April, become adult (imaginal molt) only during the second half of August. This population is then composed strictly of young adults, whereas at Pack at that time, the population is composed of adults from the first cohort and third and fourth instar nymphs from the second cohort. This Anechuru bipunctutu-type reproductive strategy can be correlated with the ovarian organization of Font Romeu and Les Combes females, which is nearer to that of mountain species. In Forficulidue only the basal ovocyte develops during each vitellogenesis. In these species, the number of ovocytes per ovariole, fixed at the imaginal molt, determines the possible number of egg batches. The study of the ovarioles of Pack and Font Romeu females at the imaginal molt, i.e., before any trace of ovocytary degeneration, shows that Pact females have significantly more ovocytes (Table I). Moreover, the number of eggs in the first batch (each ovariole develops a single egg) is significantly different between these two types of populations; consequently, the first brood in Font Rorneu and Les Combes populations consists of significantly more eggs (Fig. 5). Last, genetic determination of these differences is probable, since they persist between daughter populations born and bred under identical conditions in the lab (Table 11). This last point led us to an attempt at reconstructing the selective processes that established these interpopulation differences. 2.

Origin of the Different Reproductive Strategies

It would be interesting to know, to begin with, if the adopted reproductive strategies are direct consequences of the different ovarian organizations. The ovarian structure of Font Romeu females is undeniably correlated with a reduced TABLE I NUMBER OF TROPHOCYTES PER OVARIOLE IN Forfiicula auricu/aria“.b

Font Romeu Pace

Number of ovarioles

Mean number of trophocytes per ovariole

SD

229 185

3.12 5.27

1.12 I .42

“In the dermapteran follicles each ovocyte is associated with a single trophocyte so that the number of stained nuclei of trophocytes per ovariole corresponds exactly to the number of ovocytes in it. (After Vancassel and ForastC, 1980a.) bStudents’s r test, p 6 0.001.

62

MICHEL VANCASSEL

Pace

ll

30

L

0

Number of eggs

FIG. 5 . Number of eggs in the first batch (= number of ovarioles) in Pace and Font Roincu Forficula auriculciria populations.

number of broods. The relationship between strategies and effective fecundity of females must now be studied in each population. The notion of maximum egg production must be introduced here: It is observed, empirically, by isolating females after their first brood has hatched and feeding them with an optimal diet of carrots and pollen in excess of their need (Lamb and Wellington, 1974; TABLE I1 N U M B ~OKk E G G S lk FiKsr BATCH( N U M B ~ ROl- O V A K l O L t S ) AND S t C O N D B A l C H ( N U M B ~ ~OKF OVtXYrES PER O V A R I O L E ) O F PACE A N D FONT ROhlEU DAUGHTER POPIJLATIONS HATCHt.1) AND BREDIN THE LABORATORY UNDER IDENTICAL. CONDITIONS birst batch ( B , ) Population

Mean

SD

Font Romeu (17 = 62,

59.9

12.8

Second bdtch Sign test" p

< 0.oO01; s***

Median test /J

Pace (I'

< 0.001; s**

51.8

9.3

p = 0.23: NS

(B?)

Mean

SD

25.7

13.3

Median test p < 0.01; s* 39.5 10.4

46)

oFor the sign test. the difference between 8 , and BZ of each female was considered only when it exceeded 10 eggs (to be compared with data from Pace and Font Romeu mother populations; Fig. 5 shows the number of eggs in the first batch and Table I the number of ovacytes per ovariole).

PLASTICITY AND RADIATION OF PARENTAL BEHAVIOR

TABLE 111 MAXIMUM EGG PRODUCT~ONI N PACE Pace Mean

AND

63

FONT R O M E U ~ Font Romeu

SD

Mean

SD ~

First batch Second batch Frequency of second batch

41.3 44 4415 1

11.9 10.4 (86%)

65.1 28.3 25/49

10.5 9.3 (51%)

“Females isolated after the first brood hatched and then fed with pollen.

Vancassel and ForastC, 1980b). The results for both types of populations, studied simultaneously, are as follows: Nearly all the Pace females can produce a second batch with as many eggs as in the first one, whereas significantly fewer Font Romeu females can produce a second batch and these have fewer eggs than in the first batch (Table 111). These observations agree with a significant reduction of the second Font Romeu cohort; however, there is no parallel between this reduced second cohort in the lab and its complete absence in the field, just as there is no correlation between the nearly constant Pack second batch in the lab and the rate of second batches really laid in the field. To account for this discrepancy between maximum egg production and effective fecundity in the field, female ovarian characteristics as well as different interfering parameters (such as the presence of first brood nymphs) must be taken into account for Font Romeu and Pack populations. In fact, this means studying the development of parental behavior, particularly the phase that follows the hatching of the first batch of eggs. IV.

A.

RELATIONSHIP BETWEEN DEVELOPMENT AND ADAPTIVE RADIATION

CONDITIONS FOR THE DEVELOPMENT OF PARENTAL BEHAVIOR IN FORFICULA AURICVLARIA

It has been known for a long time that female Forficula auricularia remain with their nymphs a long time (Fulton, 1924; Weyrauch, 1929; Crumb et al., 1941; Lhoste, 1957; Lamb, 1976b). In this species, which is nocturnal like all known Dermaptera, the day is spent in shelter or in the closed burrow in the case of a female engaged in a parental cycle. Feeding occurs at night. The first days after hatching only the female leaves the burrow. She brings back food and shares it with the nymphs (Fulton, 1924; Lamb, 1976b). She returns to the nest before daytime. Later, the nymphs feed themselves outside the burrow, follow-

64

MICHEL VANCASSEL

ing an identical rhythm to the female's, and returning to the burrow after each feeding bout. Lamb (1976a) adds to this a description of nymphal dispersal, a phenomenon very variable in intensity and in temporal distribution from one brood to another, but not to be neglected. He also describes the dispersal of females heralding a second oviposition, that is, at the end of the second vitellogenesis. Under his observational conditions, this behavior occurs in about 50% of the females. Both nymphs and females disperse during the nocturnal feeding phase. They fail to return to the brood chamber but adopt a new shelter. The second batch of eggs is laid almost exclusively by these dispersing females. In the few cases where a female deposits eggs in the nest among nymphs of its first brood. the eggs disappear rapidly (the nymphs eat the eggs). These observations indicate easily measurable parameters: nymphal dispersal, female dispersal. rate and delay of second oviposition. Thanks to longitudinal studies under controlled conditions, the dynamics of parental behavior can now be analyzed in terms of the influence of the following different factors upon these parameters: effects of the presence of nymphs, the quality of food, and of climatic conditions. The interactions between different factors and/or different parameters can thus be appreciated.

I.

Ii!f!uence of the Presence of Nxmphs

The importance of the presence of nymphs on the subsequent development of the female has already been stressed in an interspecific context (Vancassel and Foraste, 1980b). Here, details of the effect in Forficula auriculuria will be discussed, first by comparing it with the ovarian differences between Pact and Font Romeu females.

w

K

W

n.

2hr

I '-

I

I t , , , Night

_ . )

FIG.6. Nycthemcral temperature conditions for studying the development of parental behavior in Fotj6cula aurirularia. (Conditions I imitate Pack summer conditions; conditions I1 imitate Font Romeu summer conditions.)

65

PLASTICITY AND RADIATION OF PARENTAL BEHAVIOR

TABLE IV INFLUENCE OF THE PRESENCE OF THE FIRSTBATCHOF NYMPHS ON OF THE SECOND BATCH Pack Average delay before second oviposition” -

+

LL LL

33.1 32.6

SD = 7.5 SD = 5

THE

PRODUCTION

Font Romeu Frequency of second batches 18/23 8/23

(78%) (34%)

Average delay before second oviposition” 40.3 SD 49.3 SD

= =

7.4 10

Frequency of second batches 11/25 3/29

(44%) (6%)

“Delay before second ovipositlon is measured in days after the day the first batch hatches

After laying a first batch of eggs, the females from the two populations no longer differ in the number of functional ovarioles but mainly in the average number of ovocytes per ovariole, which is greater for Pack. This has been established by direct examination (many ovarioles are already inactive in Font Romeu females but not in Pack females) as well as by examination of the average number of second hatch eggs (Table 111). Under identical temperature (condition I, Fig. 6) and food conditions (pollen + carrots in excess), the frequency of second batches and the delay (counted from the day the first brood hatches) are compared for females from both population in the two following situations: (1) females isolated after hatching; (2) females left with their nymphs. The results obtained for isolated females are similar to those presented in Table 111. The differences between populations for these two situations can be imputed only to ovarian differences. Pack females have a quicker vitellogenesis and a shorter delay than Font Romeu females. The effect of the presence of nymphs is shown in both populations by the marked decline in the number of batches (Table IV). Further observations will help specify the reasons for this effect.

2. Influence of the Quality of the Food In an experiment with only the Pack population, Bourez (in preparation) examined the effects of the presence of nymphs and the quality of food. He set up the four following situations: (1) females isolated after hatching + normal food (carrot pollen, in excess) (IN); (2) females left with their nymphs + normal food (LN); (3) females isolated + poor food (carrot in excess without pollen) (In); and (4) females left with their nymphs poor food (Ln). At the same time, he examined the stage of development of the experimental females by measuring their ovocytes during vitellogenesis in regular samples from the four groups (six individual observations for each group every 6 days) (Table V and Fig. 7).

+

+

66

MICHEL VANCASSEL

Delay before recond oviposition' Number of fenidles ob\ened

Number of s x o n d batches

Frequency of second batches

IN LN

25 25

25 I2

100 48

1n Ln

25

14

iY

3

56 10

X2

15

Mean 23.8

< 0.001

u test

11 p < 0.001

30.9 40.3 44.3

I7

SD 3.6

< 0.005 9.2 8.2 4.7

'zl;en~aleseither iwlated after their first lot of eggs has hatched ( I ) or left with their larvee (13 and eithcr fed with pollen f N ) or not ( n ) . hAfter Botirez (1983). 'Delay as in Table IV.

The effect of poor food is e\:en more marked than that of the presence of nymphs. However, it is quite normal that both the number of second broods decreases and the delay before the second oviposition increases every time one or the other of these factors is introduced. The comparison between the two groups of isolated females (IN and In) shows that shortage in second batches is correlated with slower vitellogenesis. A careful examination of the average delay in laying and average ovarian development shows that in the group of isolated poorly fed females (In), only the females that undergo the quickest vitellogenesis lay (Fig. 7). This indicates that ovarian development, although necessary, is not sufficient for a second batch to be laid. The speed of vitellogenesis, that is, the intensity of ovarian physiology. must be taken into account when the regulation of oviposition behavior and probably associated behavior (development of the readiness to care for eggs) are considered. Comparison between the two experimental groups IN and LN is also instructive. The groups differ in both the frequency and the delay in laying the second batch (Table V). The difference in the delay in laying can be attributed directly to the slowing down of vitellogenesis in the LN group. The difference in the frequency of egg laying does not mean however that 52% of LN females do not lay. In fact, observations of ovaries on days 25, 31, and 37 show that the proportion of females presenting ovocytes at the beginning of vitellogenesis increases until all do so on day 37. This means that all these females laid eggs between day 20 and day 37 and started their third vitellogenesis. Contrary to group In females, nearly all the LN females laid eggs. The significant divergence between the rates of batches observed for the two groups In and LN is simply due to the fact that only the LN females that isolate themselves before laying keep

67

PLASTICITY AND RADIATION OF PARENTAL BEHAVIOR

their eggs and start a new parental phase. Eggs laid by females in their initial nest are eaten very rapidly by the first batch nymphs (Lamb, 1976a). As it turns out, the observation “absence of laying” concerns, for this LN group, females that do not abandon their burrow before laying (10 cases out of 13) (Table V). To conclude, according to feeding conditions and therefore ovarian development, three different effects must be considered: first, the almost total suppression of vitellogenesis (Ln), second, the inhibition of laying (some of the In females), and third, the inhibition of dispersal in the females before laying the second batch of eggs (LN). 3 . Female-Nymphs Interactions

Continuing his study of the development of parental behavior, Bourez showed an obvious attraction to the nymphs by the female. He found that the attraction of the female fluctuates mainly in relation to the presence of nymphs and not in relation to her ovarian development. Ten and 20 days after the nymphs have hatched, Ln females are much more attracted than IN females, but no more than LN females which, moreover, exhibit intense ovarian activity similar to that of IN females. The importance of this phenomenon of attraction by the female under the particular conditions of nymphal dispersal will be discussed (Section IV,A,4).

60..--Follicular

surface at---.-+-z-*

,to

- -0

t

0 0

/

0)

0

50-

/

Lc L u 2)

-3

/

40-

0

E 30. P

i 20.

4-

(I)

Q

210.

0 0

0

/

/

0

/

68

MlCHEL VANCASSEI.

4. Itijluenc-e of Climcitic Corditions

Font Romeu females experience significantly lower average temperatures (Fig. 4). During the reproductive period, between April and August, these average temperatures are lowered by the cool nights at high altitude. This leads to important nycthemeral variations in temperatures. The influence of this characteristic has been studied by comparing two groups of Pact! females bred under very highly contrasted conditions of nycthemeral temperature variations (Fig. 6). When the first brood hatched, each female and her nymphs were put into a 900cm2 arena having the central initial nest, as well as four fixed shelters and four feeding places with pollen and carrot in excess. all placed at equal distances from the initial nest. Food w3s renewed every day, and the nymphs outside the initial nest were counted and then taken away. Thus, without disturbing the family group. both nymphal and female dispersal behavior can be measured. Condition I1 means that a lower average temperature and a general slowing down of nymphal and female development can be expected (Herter, 1965). Although the results confirm this expectation, nevertheless, there was no

-I%

I1431 1391 1391) _i_.

117,41

2

-

120.31

122.81

B n

FIG. 8. lnfluence of nocturnal temperature conditions on nymphal dispersal and development. ( A ) Nymphal dispersal in percentageidaylbatch; (B) nymphal development in percentage of batches where molts 1, 2. and 3 wcre observed: (MI) imaginal molt. (0) Average delay before laying the second batch of eggs; in brackets. "range" of the rates of nymphal dispersa1;batch at different times of the second egg-laying phase.

PLASTICITY AND RADIATION OF PARENTAL BEHAVIOR

69

TABLE VI DISTRIBUTION OF LARVAEAFTER LARVAE AND FEMALELEFTBURROW SIMULTANEOUSLY"

Distribution Observed (12 cases: 12 females and 37 larvae) Theoretical (four available shelters)

Larvae with female

Larvae not with females

31

6

10

21

ux2 = 23; p < 0.001.

desynchronization between nymphal development (measured by molts) and female development (measured by the delay before the second oviposition) (Fig. 8). The lesser dispersal of nymphs under condition I1 constitutes the greatest apparent difference between the two groups. For their part, the dispersing females of this group I1 leave their burrow for less time before laying than those of group I (situation 11: 3.1 days; SD = 2.9; situation I: 9.8 days; SD = 6.4; U test, two tailedp < 0.05). If to these two points is added the fact that the nymphs dispersing from the nest the same night as the female show a high tendancy to follow her (Table VI), it can be expected that the dispersing group I1 females have more chances of laying eggs in the presence of some nymphs than dispersing group I females. A lower rate of success for this second brood, when realized outside the initial nest, is to be expected under condition 11. In fact, the loss of females' eggs because of the intervention of nymphs is recorded once out of eight in group I and four times out of eight in group I1 (Fisher test: p = 0.14, N.S.). In spite of these nonsignificant data, this possible effect of nymphs on the survival of the second brood, and, therefore on the size of the second cohort, deserves further study. Moreover, in this experiment, the measure of nymphal dispersal for each brood enables us to quantitatively evaluate the influence of the presence of nymphs on development and female behavior. According to previous results (Sections IV,A,1 and 2), it is to be expected that there will be fewer nymphs with females that lay a second time when they abandon their first burrow (dispersing females) than with nondispersing females. This expectation, confirmed in both groups, may in turn depend upon two factors: a smaller initial number of nymphs and a greater nymphal dispersion. Of these two new correlations, only the second one is found to be significant here. That suggests that in this experiment, previous nymphal dispersal leads mainly to fewer nymphs with dispersing females (Table VII). In spite of these results, this experiment does not verify completely the initial

70

MICHEL VANCASSEL

TABLE VII C O K KA~~ II O ~ WB E T U L ~ NL ~ R V A DISPLRSION I A N D IHL: O B S ~ R V ~ TOF I OA NSLCONDBATCH

ot. EGGS ( F E M A L t

Conditions I Second brood observed I1 = 8

Not observed 11 = 1s

Conditions 11 Second brood observed n =8

Not observed It =

DISPtRSION)

Remaining larvae

Dispersed larvae

Mean

SD

Mean

SD

Mean

SD

30

11.3

7.4

10.6

37.4

9.8

Initial number

S: U test onetailed 0.05 40.6 10 9

S: U

tebt onetailed 0.024 1.5 2.6

42. I

10.9

22.4

5.7

28.1

9

11.3

S: U test onetailed 0.05 32.1 7.1

6.2

C, test onetailed 0.05 2.3 3.9

N.S.

N.S.

S:

34.4

1.7

11

hypothesis according to which low nocturnal temperatures and marked daynight differences should lead to a lower success of second broods. Although the data show a very weak tendency in that direction (lot I: 7/23, lot 11: 4/19), the difference is not significant. Although the sample may be too small, the many effects involved and the complexity of the development of parental behavior suggest other reasons for this that are open to experimental control; below are the two most likely. First it must be stressed that the average number of first brood nymphs, at the beginning, is significantly lower in group I1 (condition I: 40.5; SD = 10.6; condition 11: 31.4; SD = 8.7; p < 0.005, U test, two tailed); this situation, accepted above because it could only have an unfavorable influence on the verification of the general hypothesis, can, however, weigh more heavily than expected (Table VII). Moreover, the experimental set-up does not take into account possible interactions between temperature and feeding behavior, whereas the importance of the quality of food on the production of the second brood has now been demonstrated (Section IV,A,2). In addition, Van Heerdt (1946) showed that locomotor speed of Forficula auricztlaria increases linearly from 1-2 cm/sec at 1°C to 7.5 cm/sec at 35°C. Therefore, we believe that at least the intensity of feeding behavior can be influenced to some extent by temperature. Obviously presentation of food, concentrated at four points during this experiment so as to present optimal foraging conditions with a minimum of movement,

71

PLASTICITY AND RADIATION OF PARENTAL BEHAVIOR I

could mask this depressant effect of temperature; it would be interesting to establish time budgets under more natural conditions of food distribution and accessibility.

B. OUTLINEFOR I.

A

SCENARIO

fntraspecific Radiation of Behavior

Although still incomplete, the above data show that the production of one or two broods is affected by a group of interactions involving at least climatic conditions, feeding conditions, nymphal dispersion, and behavioral tendencies of the female (dispersing behavior and oviposition). Whether a second cohort is produced appears here to be essentially a question of phenotypic plasticity and consists of a “physiological adaptation” in the sense given by Gould and Lewontin (1979). This adaptation is nothing other than the product of the development of parental behavior. However, the difference between the Pact and Font Romeu populations also shows the importance of the differences in ovarian organization for realizing either of these two strategies. This stock effect, probably of genetic origin, makes these strategies look like Darwinian adaptations. How did these adaptations come about? To try to answer this question, let us consider how the two types of ovarian structures may be maintained: first for the Pact population and for many populations which seem to reproduce and retain the same solution. Lamb (1976a) suggests an answer by showing that, for the populations he studied (which seem to be comparable to the Pack population from all points of view), differential survival between the two cohorts is so important that at least 50% of the hibernating adults, which will assume reproduction the following year, come from this second cohort; although, to begin with, the latter was much smaller. He also established (1975) that predation by birds can be an important factor for this differential survival of the two cohorts. Under such conditions, females with an ovarian structure allowing the production of a second batch of eggs of maximum size (i.e., up to as many as in the first one) will have a selective advantage over females with an ovarian structure inducing them to produce only one brood, even with more eggs. The problem is simpler for the Font Romeu population because through the combined effect of ovarian structure and development of the first parental phase the second cohort completely disappears. Let us now consider how a Font Romeu type of ovarian structure can evolve. The results above indicate that even for Pack-type females the second cohort would most probably be reduced to zero under Font Romeu subalpine conditions. In that case, the effect of the differential survival between the two cohorts no longer plays any part. On the contrary, the females which, through their ovarian

72

MICHEL VANCASSEL

constitution, would be the best prepared to lay a single batch (reduced number of ovocytes par ovariole) and simultaneously lay the most eggs the first time (more ovarioles). would obtain a selective advantage. Under such conditions, a Packtype population would undergo a selective pressure that would lead to a reduction in the number of ovocytes per ovariole and an increase in the number of ovarioles; this would lead to a Font Romeu type of ovarian organization. Although this chain of events has not yet been completely established, there are enough points in its favor for its most interesting aspects and consequences to be discussed. First. it reminds us that the selection pressures which act on populations emerge from the development of parental behavior, that is, from interactions between behavioral phenotypes and particular ecological conditions, and not only from ecological conditions alone. These simultaneous evolutionary processes of reproductive strategies, of behavior itself, and of ovarian structures are highly complex: Many parameters intervene in the development of parental behavior (Section 11). The selective pressures that emerge are also multiple: Even if up to now only two morphological aspects (number of ovarioles and number of ovocytes) have been discussed, the related physiological (ovarian endocrinology) and behavioral (behavioral tendencies) aspects must not be neglected. The evolution of a new ovarian type does not imply the suppression of the influence of behavioral development in determining the type of reproduction adopted: It must not be forgotten, for the transformation Pack type + Font Romeu type that has been proposed, that all tendency to produce two broods has not been abolished in the Font Romeu population. On the contrary, under conditions leading to a rapid dispersion of the first brood nymphs (Tables 111 and IV), nearly 50% of the Font Romeu females are able to produce a second batch of eggs. This means that the development of behavior still plays an important role in repressing the second cohort in the Font Romeu population. The one brood reproduction of this population should be understood both as Darwinian adaptation. compared to the Pace population. and as a phenotypical variation or physiological adaptation, compared to its full potentialities. Last, this selective process, modulated by the development of behavior, affects and modifies parental behavior itself. Of course this evolution remains limited in our intraspecific comparison. That is a disadvantage of the necessity of remaining within the limits of true homologies (Atz, 1970) if such phenomena are to be analyzed in detail. However, under identical conditions, females from the two populations show different rates and delays before their second oviposition (Tables I11 and IV). This implies differences in the regulation of their parental behavior. Taking into consideration what is now known about hormone--behavior interactions occurring during this phase, it may be that, for these two types of Fw-jicuku auricdnrin, the modulating mechanisms of parental be-

PLASTICITY AND RADIATION OF PARENTAL BEHAVIOR

73

havior are the same and follow the same pathways but at different speeds and/or different intensities. 2 . Interspecific Evolution of Behavior Can this hypothetical schema be applied to the wider interspecific differences known in Dermaptera? The suppression of the tendency to care for eggs during vitellogenesis, analyzed above in Lubiduru ripuriu, is also well known in Forficulu uuriculuriu (Weyrauch, 1929). However, this behavioral regulation is completely absent in Anechuru bipunctutu females: After their young hatch, these females remain indefinitely prepared to care for eggs, even after a long absence of stimulation. Now it appears that these Anechuru bipunctutu females have an empty, inactive ovary after laying their single batch of eggs. Just after their imaginal molt, the ovarioles of these females often have a second ovocyte, but it aborts quickly. This could mean that this species is derived from forms having had the capacity to produce more than one batch of eggs. The precisely defined mountain distribution of Anechuru bipunctutu and its taxonomic relationship to F o t j h l u suggest that the ovarian characteristics of Anechuru bipunctutu could have evolved following a process of the type proposed for the different Forficulu uuriculuriu populations. This change, more pronounced here as the females are reduced to a state of functional castrates after laying their single batch of eggs, would prevent any resumption of ovarian and endocrine activity linked to vitellogenesis and secondarily of hormone-dependent behavioral regulation such as loss of the tendency to care for eggs. It must be stressed that with such an ovarian organization, the one brood reproductive strategy of Anechuru bipunctutu appears as a precisely defined Darwinian adaptation without any possible change due to phenotypical plasticity. Can the intervention of such evolutionary processes now be considered as affecting species from dermapteran families other than Forfculidue? Nothing can be usefully said at that level now. The most we can do is to argue that the different dermapteran families are effectively phylogenetically related. The fact is that Lubiduru ripuriu (Lubiduridue) presents two behavioral peculiarities that are difficult to explain. The first is that females bring food back to the nest, fleetingly but repeatedly, during the very rapid nymphal dispersal (Vancassel, 1973b). The second is the sensitivity of females to the experimental presence of nymphs; this lengthens the duration of the positive reaction to nymphs (Section I). It is difficult to understand how such characteristics could evolve because nymphal dispersal decreases or even negates their survival value. The behavior of providing food (by the female) and the regulation of behavior linked to the presence of nymphs could have become established originally in the most primitive species (Pygidicrunidue and Diplutydue) and could then have been maintained or even developed secondarily in Forficulidue. However, in species evolving the ability to produce a number of batches of eggs (Lubiduridue),these

73

MICHEL VANCASSEL

characteristics. without any survival value, would only be relics and even byproducts of structural constraints (Gould and Lewontin, 1979). The phylogeny proposed by Popham ( 1965) giving Labiduridae an intermediate status in the dermapteran (considered until then a5 very primitive), supports this hypothesis. Naturally. it is very important to have a better knowledge of the development of parental behavior in species from families retaining the more primitive characteristics of this group.

V.

THE STUDYOF PARENTAL BEHAVIOR: ILLUSTRATION OF WHICHTHEORIES’?

In any experimental research, the problems studied and the subsequent interpretation of the data are never naively and completely objective. Indeed, they alnay5 imply, more or less explicitly, obvious and “scientific” theoretical frameworks. An essential part of the interest of any research is to be found, however, in the presentation and discussion of these theoretical aspects. A large part of the confidence placed in interpretations depends on the coherence of the theory to which they are linked. A.

WHICHCONCEP~ION OF BEHAVIOR‘?

The study of the development of behavior has never been neutral or without biases. In fact, the results of this type of research can only be expressed in terms of multiple interactions within the organism studied and between the organism and its environment (Lehrman, 1953, 1964; Hinde, 1965, 1966). This leads to a very particular approach involving a series of questions which were for a long time some of the most important in ethology. First of all, this type of approach and the subsequent conclusions lead to interpreting behavior as a “superphenotype” produced by interactions between the living organism, which already belongs to this phenotypic world, and its environment. This constitutes a first disagreement with the classic ethological conception of behavior-organ, which relies on the species-specific character of behavior. The same procedure leads to acknowledging that there is no isomorphism between genes and behavior, that the genome cannot therefore be considered a “blueprint,” and that there is no possibility of separating the innate and acquired in behavior (Lehrman, 1970). This conception can only refer to a nonreductionist definition of genetic determination which takes into account the fact that genetic methodology can only compare differences without applying to the ”traits” themselves and does not attribute an elusive integrating and organizing power to the genome (Waddington, 1968a; Weiss, 1974). Because this epigenetic approach was applied, notions such as instinct and motivation were

PLASTICITY AND RADIATION OF PARENTAL BEHAVIOR

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abandoned. Therefore, all this is not new, but it must be stressed that since Schneirla’s pioneer studies on Eciton (1938, 1957), the extension of this approach to insect behavior has been highly limited. For too many biologists, including ethologists, invertebrates still typify the world of stereotypy, assumed to be produced by genetic programs, and insects are still too often conceived as “automates gknktiques” (Langaney, 1979). B.

BEHAVIOR CONSIDERED AS SYSTEMSDYNAMICS

It is probably now useful to assume a theoretical position similar to that of Weiss, who defined behavior as system dynamics. He emphasized the opposition between machine and system: “This is exactly the opposite of a machine, in which the structure of the product depends crucially on strictly predefined operations of the parts. In the system, the structure of the whole determines the operation of the parts; in the machine, the operation of the parts determines the outcome” (Weiss, 1969, p. 13). Are not the behavior-hormone interactions we are beginning to grasp in Labidura riparia the concrete form of the integrated functioning of this system? Differences in parental behavior regulation from one species to another have been noted. Among these, appearance of the tendency to care for eggs depends on sexual behavior in Labidura riparia and on an exposure to cold in Forficulidue. Is not the existence in related species of a similar regulation following different patterns evidence of a transformation and of a radiation of the postulated system(s)? In this systems formulation, causal analysis of behavior is the characterization of the relational structure of the system studied. The development of behavior corresponds to the working of this relational structure, and the evolution of behavior refers to a modification of this relational structure. If experimental research allows a systems interpretation of behavior to be considered, theoretical research, as for example Delattre’s essay-with such an evocative title-“Systeme, structure, fonction, tvolution” (1971), in which the relations between these different concepts are analyzed, is of considerable help in the study of these difficult questions. It is this type of contribution which helped me in formulating the question of possible relations between phenotypic plasticity and Darwinian adaptation in the specific case of insect behavior. The results presented here suggest strongly that the development of behavior itself, while producing a “physiological adaptation,” also maps the selection pressure the system will undergo. As behavior is affected by the transformations it participates in producing, it assumes the roles of both object of evolution and “motor of evolution” (Piaget, 1976), but it appears better seen as the actor of evolution by analogy with the relationship between an actor and his character. This view cautions against any conception of natural selection that would identify it with a strictly external force, independent of the organism. We refer

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MICHEL VANCASSEL

instead to the notion of “process of natural selection” defined by Waddington ( 1968b) to his genetic assimilation model, and more generally to his representation of an evolutionary system (1959) where he distinguishes four partly overlapping and interacting subsystems: “the exploitive system, (‘set of processes by which animals choose and often modify one particular habitat out of the range of environmental possibilities open to them’). the epigenetic system, the natural selection system and the genetic system” (Waddington, 1975, p. 58). In particular in this conception “we have to think in terms of circular and not merely unidirectional causal sequences. At any particular moment in the evolutionary history of an organism, the state of each of the four main subsystems has been partially determined by the action of each of the other subsystems. The intensity of natural selective forces is dependent on the condition of the exploitive system, on the flexibilities and stabilities which have been built into the epigenetic system, and so on” (Waddington, 1975). To be exact, the essential part of the results presented here concerning parental behavior is situated at the intersections between the first three subsystems defined by Waddington. If the “genetic system” has not been approached in this study on parental behavior, it must be admitted that the conclusions and conceptions presented above contain a certain number of requirements concerning its organization and working: Among the models proposed by geneticists, which models seem to answer best these requirements? In their critique of what they call “the adaptationist program,” Gould and Lewontin (1979) stress the need to analyze “the organisms as integrated wholes” in order to grasp the “constraints” which, according to them, “delimit the pathways of change,” rather than to proceed “by breaking an organism into unitary ‘traits’ and proposing an adaptive story for each considered separately” (p. 581). This proposition, which seems implicitly contained in Waddington’s illustration of the natural selection process and of an evolutionary system. also seems applied to the analysis according to which the development of parental behavior participates in modeling selective pressures undergone by dermapteran populations. In a way, it is a complement to these ideas on the origin of selective pressures, though he does not discuss them. that Wright (1980) reexamines how these selective pressures act and on what. He contrasts “genic selection,” with the gene as unit, with “organismic selection,” with the individual within a population as unit. First, Wright’s genetic system model embraces many aspects such as pleiotropy or population heterogeneity (heterallelism) which, at a first approximation, cannot only adapt but also participate, and thus contribute to explaining the phenomena described above concerning Dermaptera. The organization of the individual in a coordinated system can no doubt be assumed better within the framework of a “universal pleiotropy” than within that of a simpler and linear, even polygenic, genetic determination of “traits. Also, the analysis sketched for Forficiicufa auricularia is situated from the start at a population level and is ”

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allowed by taking into account their range of variation (without, however, needing its exhaustion). Another important point, Wright reminds us is that the supporters of genic selection are mainly sociobiological theoreticians. Although there is no question of discussing further the form(s) of neo-Darwinism implied in this theoretical current, so important today, one must remember that when these theoreticians (Dawkins, 1976; Maynard Smith, 1978) consider evolution of behavior, they stress its genetic determination and thereby tend to emphasize an innatist and instinctivist conception of behavior which seemed to have been abandoned since the 1960s. Is this convergence between some conceptions of behavior (innate or epigenetic) and some conceptions of natural selection (genic or organismic) purely accidental or does it correspond to the old epistemologic split between reductionism and holism (Weiss, 1974)? In ethology, this split seems to reappear in the way the four questions distinguished in the study of behavior (cause, ontogeny, function, evolution) are broached between those who consider it possible to study these questions separately and those who try to study the relationships between these questions. With Lehrman (1970) “I think it is not an affront to any theory to point out that there are some questions that it cannot answer because it has not asked them.” After all, the question of evolution of behavior is sufficiently delicate by itself for one to consider broaching it by itself to begin with, and thus complying with the parsimony principle (evolution of an isolated and genetically determined trait). The problem remains to know whether the cost of this parsimony, by evacuating the relationships between the four questions mentioned above-r in other words what Morin (1980) would call the “complexitk vivante”-is not merely producing answers poorly relevant to this complexity (Devereux, 1980). I have tried here to explore in the subject of humble insects the problem of relationship between development and evolution of behavior. In spite of the requirements implied from the start (simultaneous analyses of the ecological, physiological, behavioral, and comparative aspects), I think that this approach, considered by Tinbergen as far back as 1963, remains possible.

Acknowledgments

I would like to thank Guy Bourez, Maryvonne Foraste, and Colette and Alain Strambi for allowing me to quote from their unpublished works and my other friends and colleagues-Ann Cloarec, Jean Yves Gautier, Jacques Gervet, Jean Gingras, Georges Le Masne, Jean Sibastien Pierre, Gaston Richard, Michel Veuille, Jean Marie Vidal-whose helpful comments improved earlier drafts. I also thank Colin Beer, Jane Brockman, Marie-Claire Busnel, Jay S. Rosenblatt, and Peter Slater for critically reviewing the article. I am especially grateful to Ann Cloarec for translating this paper and to Jay S . Rosenblatt for reviewing and correcting the manuscript. All the interpretations and conclusions presented in this final version remain, however, my entire responsibility as some suggestions were not taken into account.

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References Atz. J . W. (1970). The application of the Idea of Homology to Behavior. In “Development and

Evolution of Behavior (Essays in Memory of T. C. Schneirla)” (L. Aronson, E. Tobach, D. Lehrman, and I. Rosenblatt, eds.), pp. 53-74. Freeman. San Francisco. Baehr. J. C . , Cassier, P.. Caussanel. C., and Porcheron, P. (1982). Activity of Corpora allatu, endocrine balance and reproduction in female Labiduru riparia (Dermapteres). Cell Tissue Res. 225, 267-282. Beier. M. ( 1959). “Klassen und Ordnungen des Tierreichs: Ornung Dermaptera,” pp. 455-585. Ceest and Portig, Leipzig. Bourez. G . (1983). Les rapports femelle-larves au cours du cycle parental de Forficula uurirulariu (Insecte Dermaptere). These 3e Cycle. Universite de Rennes (in preparation). Caussanel. C. (1974). Cycles reproducteurs de la femelle de Labidura riparia (Insecte, Dermdpttrc) et leurs contrdles neuroendocrines. These, Universite Paris VI. Caussanel, C.. and Dresco-Derouet, L. (1972). Respiration de la femelle de Labidura riparia (Insecte Derniaptere) avant la ponte et pendant la p6riode de soins aux oeufs. C.R. Acud. Sri. Paris 274, 1 179- 1 182. Caussanel, C., and Karkinsky, A. (1981). Les soins matemels d’un Perce-Oreille. Recherche 125, 1004-1007. Caussanel, C., Baehr. J. C., Cassier. P., Dray, F., and Porcheron, P. (1979). Correlations humorales et ultrastructurales au cours de la vitellogenese et de la p6riode de soins aux oeufs chez Labidura riparia (Insecte, Dermaptere). C.R. Acad. Sci. Paris 228, 513-516. Chopard. L. (1949). Ordre des Dermaptkres. In “Trait6 de Zoologic. Tome 9” (P. P. Grasse ed.), pp, 774-770. Masson, Paris. Crumb. S . E.. Eide, P. M., and Bonn, A. E. (1941). The European Earwig. Tech. Bull. U.S. Depl. ARric. 766, 1-76. Ddwkins. R . (1976). “The Selfish Gene.” Oxford University Press. Delattre. P. (1971). “Systeme, Structure. Fonction, Evolution: Essai d’Analyse EpistCmologique.” Maloine. Paris. Dcvereux. G . (1980). ”De I‘angoisse a la methode dans Ics sciences du comportement.” Flammarion. Paris. Fulton. B. B. (1924). Some habits of Earwigs. Ann. Ent. Soc. Am. 17, 357-367. Could. S. J . (1977). “Ontogeny and Phylogeny.” Belknap, Cambridge, Mass. Gould, S J and Lewontin, R. C. (1979). The Spandrels of San Marco and the Panglossian paradigm: A critique of the aciaptationist programme. Proc. R . Soc. London Ser. B 205, 58 1-598. Herter. K. ( 1965). Verglcichende Beobachtungen und Betrachtungen uber die Fortpflanzungsbiologie der Ohrwurmer. 2. Naturforsch. 20b, 365-375. Hinde. R. A. (1965). Interaction of internal and external factors in integration of canary reproduction. In ”Sex and Behavior” (F. A. Beach, ed.), pp. 381-415. Wiley, New York. Hinde, R. A. (1966). “Animdi Behavior: A synthesis of Ethology and Comparative Psychology.” McGraw-Hill. New York. Hinde. R . A , , and Stevenson, J. G . (1971). Les mothations animales et humaines. Recherche 12, 443-456. Kuo. %.-Y. (1970). The need of coordinated efforts in development studies. In “Development and Evolution of Behavior” (Essays in Memory of T. C. Schneirla). (L. Aronson, E. Tobach. D. Lehrman. and I. Rosenblatt, eds.), pp. 53-74. Freeman. San Francisco. Lamh. R . J. (1975). Effects of dispersion. travel and environmental hererogeneity on populations of the earwig Fofic.ula auricularia (Dermaptera: Forfculidae). Can. J . Zoo!. 53, 1855- 1867.

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Lamb, R. J . (1976a). Dispersal by nesting earwigs, Forficula auricularia (Dermaptera: Forficulidae). Can. Entomol. 108, 213-216. Lamb, R. J. (1976b). Parental behavior in the Dermaptera with special reference to Forficula auricularia (Dermaptera: Forficulidae). Can. Entomol. 108, 609-619. Lamb, R. J., and Wellington, W. G . (1974). Techniques for studying the behavior and ecology of the european earwig Forficula auricularia. Can. Enromol. 106, 881-888. Lamb, R. J., and Wellington, W. G. (1975). Life history and population characteristics of the european earwig Forficula auricularia (Dermaptera, Forficulidae), at Vancouver, British Columbia. Can. Entomol. 107, 919-824. Langaney, A. (1979). “Le. Sexe et I’Innovation.” Seuil, Paris. Lehrman, D. S . (1953). A critique of Konrad Lorenz’s theory of Instinctive Behavior. Q . Rev. Biol. 28, 337-363. Lehrman, D. S . (1964). The reproductive behavior of Ring Doves. Sci. Am. 1-8. Lehrman, D. S. (1970). Semantic and conceptual issues in the nature-nurture problem. In “Development and Evolution of Behavior” (Essays in Memory of T. C. Schneirla) (L. Aronson, E. Tobach, D. Lehrman, and J. Rosenblatt, eds.), pp. 17-52. Freeman, San Francisco. Lhoste, J. (1957). Donnees anatomiques et histophysiologiques sur Forficula auricularia L. Arch. Zool. Exp. Gen. 95, 75-252. Maynard Smith, J. (1978). L’Cvolution du comportement. Pour la Science 13, 148-158. Morin, E. (1980). “La mtthode, 2: La Vie de la Vie.” Seuil, Paris. Piaget, J. (1976). “Le comportement moteur de I’Cvolution.” Gallimard, Paris. Pierre, J. S. (1979). Effet de I’allatectomie sur la fin du cycle parental chez Labidura riparia Pallas. (Dermaprerae, Labiduridae). Biol. Behav. 4, 219-226. Popham, E. J. (1965). The functional morphology of the reproductive organs of the common earwig (Forficula auricularia) and other Deimaptera with reference to the natural classification of the order. J . Zool. 146, 1-43. Richard, G . (1979). Ontogenesis and phylogenesis: mutual contraints. Adv. Study Behav. 9, 229-278. Rosenblatt, J. S . , and Lehrman, D. S. (1963). Maternal behavior of the laboratory rat. In “Maternal Behavior in Mammals” (H. L. Rheingold, ed.), pp. 8-57. Wiley, New York. Rouland, C. (1979). Proteinhie et vitellogCnine au cours des cycles reproducteurs de la femelle de Labidura riparia (Insecte, DermaptCre). Thtse 3e Cycle, UniversitC Paris VI. Sakai, S. (1982). A new proposed classification of the Dermpatera with special reference to the check list of the Dermpatera of the world. Bull. Daito. Bunka. Univ. 20, 1-108. Schneirla, T. C. (1938). A theory of army-ant behavior based upon the analysis of activities in a representative species. J . Comp. Psychol. 25, 51-90. Schneirla, T. C . (1957). Theoretical consideration of cyclic processes in Doryline ants. Proc. Am. Philos. Sac. 101, 106-133. Schneirla, T. C., and Rosenblatt, J. C. (1961). Behavioral organization and genesis of the social bond in insects and mammals. Ann. J . Orthopsychiat. 31, 223-253. Strambi, A., Strambi, C., Vancassel, M., and ForastC, M. (1983). Normal and experimentally induced changes in hormonal hemolymph titres during parental behaviour of Labidura riparia (in preparation). Tavolga, W. N. (1970). Levels of interaction in animal communication. In “Development and Evolution of Behavior” (Essays in Memory of T. C. Schneirla) (L. Aronson, E. Tobach, D. Lehnnan, and J. Rosenblatt, eds.), pp. 281-302. Freeman, San Francisco. Tinbergen, N. (1963). On aims and methods of Ethology. Z . Tierpsychol. 20, 4, 410-433. Topoff, H. (1972). Theoretical issues concerning the evolution and development of behavior in social insects. Am. Zool. 12, 385-394.

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Vancasael, M. ( 1973a). Elements pour I'analyse du cycle parental du Forficule Labidura ripuriu (Derni.. Lahiduridae). Rev. Cornp. An. 7, 53-62. Vancashel. M. (1973b). La fin du cycle parental de Labiditra ripuriu (Denn. Lubiduridaej. Terre Vie 27, 481-490. . entre les comportementc sexuel et parental chez Lubicfura riparia. Vancassel, M. ( 1 9 7 3 ~ )Rapport Ann. Soc. Enf. Fr. ( N . S . ) 9(2), 44-455. Vancassel, M. ( 1974). Etude du cycle parental chez Labidura ripuriu (Insecte, Dermaptere). These, Univcrsite de Rennes. Vancassel. M. (1977). Le developpement du cycle parental de Lobidura ripariu. B i d . Behav. 2,

SI-64 Vancassel. M.. and Foraste, M. (198Oaj. Le comprtcment parental des Dermapteres. Reprod. Nutr. Dev, 20(3B1 759-770. Vancasscl. M., and ForastE, M. (1980b). Importance des contacts entre la femelle et les larves chez quelques Dermapteres. B i d . Beha\*. 5 , 269-280. Van Heerdt. P. F. (1936). "Eenige physiologische en oecologische problemen bij Forficula auriculuria L." ( N . V. Drukkerij and P. Den Boer. eds.). Utrccht. Vickery. V . R., Johnstone, D. K.. and Mc Kevan, E. (1974). The orthopteroid insects of Quebec and the atlantic provinces of Canada. Mem. Lyman. E n f . Mus. Res. Lab. I , 1-204. Waddington. C. H. ( 1959). Evolutionary adaptation. In "Evolution after Darwin-University of Chicago Centennial." pp. 381-402. Univ. of Chicago Press, Chicago. Illinois. Waddington. C. H . (1968a). Thc basic ideas of biology. In "Towards a Theoretical Biology, I: Prolegomena" (C. H, Waddington. ed.), pp. 1-32. Edinburgh Univ. Press, Edinburgh. Waddington. C. H. (1968b). Does evolution depend on random search? In "Towards a Theoretical Biology, I: Prolegomena" (C. H. Waddington. ed.), pp. 1 1 1 - 1 19. Edinburgh Univ. Press. Edinburgh. Waddington, C. H. (1975). "The Evolution of an Evolutionist." Edinburgh Univ. Press, Edinburgh. Wei55. P. A . (19691. Thc living system: Determinism stratified. In "Beyond Redustionism" (A. Koestler. and J . R. Smythies, eds.). pp. 3-55. Hutchinson. London. Weiss. P. A . (1971). "L'Archipel Scientifique. Etude sur les fondements et les perspectives de la science." Maloine. Paris. Weyrauch. W. K . ( 1939). Experimentelle Analyse der Brutpflege der Ohrwurrnes Forfcula uu. 49, 553-558. ric.uluriu L. B i ~ l Zenirulbl. Wright. S. ( 19x0). Genic and organismic selection. Evolrtfion 34, 825-843.

ADVANCES IN THE STUDY OF BEHAVIOR, VOL. 14

Social Organization of Raiding and Emigrations in Army Ants HOWARDTOPOFF DEPARTMENT OF PSYCHOLOGY HUNTER COLLEGE OF THE CITY UNIVERSITY OF NEW YORK AND THE AMERICAN MUSEUM OF NATURAL HISTORY

NEW YORK, NEW YORK

I. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 11. Phylogeny and Systematics . . . . . . . . . . . . . . . . . . . . ............... 111. Nomadic Behavior and Brood-Stimulation Theory. .....................

IV.

V.

VI.

Behavioral Ecology of Chemical Communication ...................... A. Laboratory Studies of Trail Following .............. B. Ecological Aspects of Mass Recruitme C. Multiple Use of the Mass Recruitment System .................... Empirical Tests of Brood-Stimulation Theory ......................... A. Callow Excitation and the Onset of Nomadism.. . . . . . . . . . . . . . . . . . . B. Larval Stimulation and Nomadic-Phase Length. . . . . . . . . . . . . . . . . . . . C. Between-Phase versus Intraphase Differences in Behavior D. Food Location and the Direction of Emigrations. . . . . . . . . . . . . . . . . . . E. Food Abundance and the Frequency of Emigrations Conclusion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . ....... References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .......

85 88 88 94 98 99 99 102 107 120 123

I. INTRODUCTION The designation army ants is an appropriate analogy for a group of ant species that carry out attacks en masse, move about in orderly columns, and periodically change nesting sites. Indeed, so pervasive was the use of military metaphors in the description of army ant behavior by nineteenth century naturalists that even so prominent a scientist as William Morton Wheeler referred to them as the Huns and Tartars of the insect world. In his classic book “Ants-Their Structure, Development, and Behavior,” Wheeler (1910)provided an exhaustive review of published information about army ant behavior and ecology, and he concluded this section of his book with the following plea for more research: 81

Copyright 0 1984 by Academic Press, Inc. All rights of reproduction in any form reserved. ISBN 0-12-004514-1

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HOWARD TOPOFF

In conclu\ion. attention may be called to certain problems that are suggested by our prewnt meager knowledge of the Dorylinae. Besides the investigation of the species with a view to obtaining all the phases and thus clearing up the taxonomy, wc are in great need of a fuller insight into the domestic economy of these singular insects. As yct no one has been able to observe the methods of rearing the brood and thc mating of sexual forms, which must. of course. take place without a true marriage flight. Nor has it been possible to plot the territory covered by the annual migrations of any of the species, to determine the time spent in the bivouacs or in the presumably more permanent breeding nests. or the precise relations which these nomadic ants bear to their myrmecophiles. . . . Another problem of more theoretical interest is prcscntcd by the Dicthadiigynes, which are so unlike typical female ants.

In 1932. Wheeler’s appeal piqued the curiosity of T. C . Schneirla, a comparative psychologist at the American Museum of Natural History. By emphasizing studies of behavioral ontogeny , Schneirla sought to explicate similarities and differences in the mechanisms underlying social organization in diverse animal species. In preparing for his first field trip to study the genus Eciton in Central America, Schneirla recognized the opportunity for extending our knowledge of these notorious social insects beyond the fragmentary and anthropomorphic observations of the earlier naturalists. It is interesting to note that army ant emigrations was not one of the problems raised by Wheeler as requiring additional study. And why should it? After all, almost everyone agreed that nomadism was a sporadic event, triggered either by the colony’s need for food or by the exposure of the nest to adverse weather conditions. And yet it was this very problem that Schneirla seized, primarily because it provided an opportunity to demonstrate how adaptive group integration is achieved by interactions among colony members and between the colony and-its physical and biotic environment. Central to Schneirla’s research were two discoveries that resulted from systematically following colonies over long periods of time. The first was that emigrations in some army ant species are not random, episodic events. Instead, each colony has a behavioral cycle that consists of alternating nomadic and statary phases. The second discovery, which came to be known as brood-stimulnticirz theory, was that changes in overall colony activity between the two phases are caused by comparable changes in the intensity of stimulation arising from the colony’s developing brood. During his 35 years of field and laboratory research. Schneirla studied worker polymorphism, bivouac formation, male and queen reproductive biology, colony division, and many other aspects of army ant behavior and ecology. But it was brood-stimulation theory that remained his principal theoretical contribution to the development of social organization in army ants. Since Schneirla’s death in 1968, researchers from many laboratories have expanded our knowledge of army ant behavior, and readers desiring a comprehensive review of this work may consult both Schneirla’s (1971) monograph,

RAIDING AND EMIGRATIONS IN ANTS

83

and the more updated summary by Gotwald (1982). The principal goal of my own research program was to perfect the ability to conduct controlled manipulations on colonies of army ants, both in the field and in the laboratory. To do this we switched the emphasis away from tropical colonies of Eciton and concentrated instead on colonies of Neivamyrmex nigrescens in the southwestern United States. The impetus for this change was simply colony size. Eciton hamatum and Eciton burchelli, the most ubiquitous neotropical species, have colonies containing hundreds of thousands of individuals. Neivamyrmex nigrescens, by contrast, is a small ant (size range of individuals = 2.5-5.0 mm), and has colony sizes ranging from 10,000 to about 100,000 individuals. With N . nigrescens, therefore, it became feasible to monitor the food intake of undisturbed colonies, and even to collect enough fresh (nonarmy ant) brood to artificially supplement the booty intake of colonies in the field. Equally important was our ability to collect entire colonies of N . nigrescens, house them in laboratory nests with transparent covers, and directly observe spatial arrangements and behavioral interactions inside the colony. By interconnecting a series of nesting boxes and foraging arenas with 100 m of lucite tubing, these laboratory colonies of army ants were able to conduct species-typical predatory raids and emigrations from one nest box to another. Eventually, we succeeded in rearing laboratory colonies through complete nomadic-statary cycles, and we could even manipulate the length of each phase by altering such variables as room temperature. In this article, I shall summarize the results of our field and laboratory research on the relationship between food supply and emigrations, on chemical communication and orientation, and on other behavioral processes that relate to broodstimulation theory. The goal of these studies is to understand how processes occurring inside the nest interact with factors in the colony's external environment in influencing differences in colony behavior between the nomadic and statary phases, as well as behavioral variations within each phase. To begin, however, let us place army ants in perspective by briefly reviewing their evolution and taxonomic status.

11. PHYLOGENY AND SYSTEMATICS Army ants comprise approximately 300 species of tropical and subtropical ants whose behavior is uniquely characterized by the combination of group predation and nomadism. It is commonly recognized that group raiding evolved as an adaptation for feeding on large arthropods and other social 'insects (Schneirla, 1971; Wilson, 1958). Because social insect colonies are more widely dispersed than other types of prey, nomadism allows army ants to periodically shift their foraging field to exploit these new food sources. During the past 10 years, considerable evidence has been gathered showing that these two patterns of

84

HOWARD TOPOFF

Gt\;t:KA Ecitoninae

ANL)

NL~MBER OF

Number of species

Dorylinae

Number of species

Dorylini

Ecitonin I ECi/Otl

TABLE I ECITONINAE AkL3 DOKYLINAt"

SPECIES Oi-

12

Ld>idus Yomcitnyrrnc~.~ Nei vurnyrinrs Chelioniymiecini Cheliontymiex

I17

Total

I45

8 3

Dot:v/rrs

54

Aenictini Aenic/ir.s

50

5 I04

:'From Rettenmeyer e r crl. ( 1983).

"legionary" behavior have evolved independently on several occasions in the primitive ant subfamily Ponerinae (Wilson, 1958; Gotwald and Brown, 1966). Although once viewed as a monophyletic group, all species of army ants are currently organized into two subfamilies (Table I). The Old World species comprise the subfamily Dorylinae (the subfamily name formerly applied to all army ants), whereas the New World species are now placed in a separate group, the Ecitoninae (Snelling, 1981). This systematic arrangement more accurately reflects the evidence for polyphyly that is based on the morphological studies of Brown (1954), Gotwald (1969), and Gotwald and Kupiec (1975). The Dorylinae are divided into two tribes. The Acnictinini, composed of the single genus Aerzirtus, is represented by 34 species in Asia, New Guinea, and Queensland, and by about 15 additional species in Africa (Wilson, 1964). The Dorylini, also with a single genus (Doylus). is represented by 50 species in Africa, but only 4 species in Asia. In the New World Ecitoninae, Watkins (1976) recognizes 147 species distributed among five genera within two tribes (Ecitonini, Cheliomyrmicini). Included in the Ecitonini are Eciton, perhaps the most thoroughly studied army ant genus, and Neivamyrmex, the genus containing the only species ( N . nigrescerzs) that extends into temperate regions of both north and south America. The fact that army ants have a single, wingless queen, coupled with the finding that new colonies result from colony fission, signifies that geographical dispersal has always been relatively slow. In a recent review of the origins and dispersal of army ants, Gotwald ( 1977, 1979) attempted to incorporate current evidence from studies of continental drift. For example, it is believed that evolution proceeded in isolation in Africa during the greater part of Tertiary time. Arabo-Africa was separated from Eurasia by the Tethys Sea from the late Cretaceous to the Miocene. Africa and Asia were broadly connected from the late Oligocene to sometime within the Pliocene. South America was even more isolated in the Tertiary and remained so until the Panama Bridge was established

85

RAIDING AND EMIGRATIONS IN ANTS

at the end of the Tertiary (Patterson and Pascual, 1972, cited by Gotwald, 1977). Ant distribution patterns tend to confirm both the Eurasian-African connection and the isolation of South America, because there is not a single species shared between South America and Africa, but there is considerable sharing of species groups between the Ethopian and Oriental regions (Brown, 1973). Eurasia and North America were periodically connected during much of the Tertiary by a north Pacific bridge that sometimes resulted in considerable faunal exchange. Thus, the geological and zoogeographical evidence to date suggests that the following about army ant dispersal (Gotwald, 1977, 1979). 1. Aenictus arose in tropical Laurasia in the early Tertiary and dispersed into Africa sometime between the late Oligocene and the late Pliocene; dispersal of Aenictus to North America was not possible (as the north Pacific bridge favored animal groups adapted to much cooler climates. 2. Dorylus evolved in Africa in the early Tertiary, but did not disperse to Asia until late in the Tertiary (before the connection narrowed and became arid). 3. The Ecitonini and Cheliomyrmicini arose in tropical South America, diversified during a long period of isoIation, and did not disperse to North America until the end of the Tertiary.

AND BROOD-STIMULATION THEORY 111. NOMADICBEHAVIOR

The two behavioral characteristics of army ants, group predation and nomadism, were well known to many of the early naturalists, and they usually postulated food exhaustion as the proximate cause of the ants' periodic emigrations (Heape, 1931; Fraenkel, 1932). Accordingly, a colony of armt ants would conduct daily raids from a single nesting site until they had depleted the food supply in the area around the bivouac. Thus, emigrations were thought to be sporadic TABLE I1 ESTIMATESOF PREYC A ~ U RFOR E Eciton hamatum NOMADIC AND STATARY PHASE"

DURING THE

Total prey Colony phase

Raid strength

Daily number prey carriers

Number

Biomass (mg)

Statary Statary Nomadic Nomadic

Weak Strong Weak Strong

2000-5000 10,000-35,000 5000- 10,000 25,000-60,000

3000-7600 15,200-53,200 7600- 15,200 38,000-91,000

1070-2680 5400- 19,000 2700-5400 13,400-32,200

UFrom Rettenmeyer et ul. (1983).

86

HOWARD TOPOFF

instead of cyclic (Vosseler, 1905). This "random drift" hypothesis was tested by Schneirla during the first years of his field research in Panama (Schneirla, 1933, 1934), in which he concentrated on the two most surface-adapted army ant species, Eciton hnmatirm and E . burchelli. By the end of his first field expedition. Schneirla had already concluded that both species of Ecifon exhibit regular cycles of activity, with each cycle consisting of distinct nomadic and statary phases. The nomadic phase, which lasts for 16-18 days in E . hnmarum and 12-17 days in E . burchelli, is one of high colony activity, in which large daily predatory raids (Table 11) are followed by an emigration to a new temporary nest or bivouac. The nomadic phase is followed by a statary interval lasting almost 3 weeks, and which is characterized by a lower intensity of raiding and the absence of emigrations (Schneirla, 1957; Rettenmeyer, 1963). Specter

ECJton

horndurn

J

Newomyrmex; nqescens

Brood

Caiiow5

/ pE:

collow~

Pre-

,Popae

Larvae-.-.

Queen

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

Contracted

__--

------rPhySOposlric

-

t ?I

. . . . Pupae . . . . . . . . . . . . . . . (Naked)-- . Embryos Larvae

[

E9g*

______

] ............ ..... Controcled ?

F I G I . Relationship between brood development and cyclic behavior in army ants. For Eciton and h'eivcimyrme.r, the nomadic phase is initiated by callow eclosion and main-

tained by stimulation from developing larvae. Pupation of the larvae reduces the level of arousal. and the colony becomes statary. Early in the statary phase. the queen becomes physogastric and lays a new batch of eggs. The sequence is similar for Aenicrus, except that the nomadic phase begins several days after callow eclosion. (From Schneirla, 1971.)

87

RAIDING AND EMIGRATIONS IN ANTS

TABLE 111 BOOTYINTAKEFOR Neivamyrmex nigrescens Statary day

Intake (8)

Time (hr)

I‘ 2 3 4 6 7 8 9 10 1I t 12 13 14 15d 16 17 18

2.77 0.00 0.00 0.00 0.00 0.00 1.00 0.00 0.41 0.00 4.18 0.63 0.68 4.29 0.93 11.72 7.92 9.71

3.00 5.00 1.00 0.00 0.00 0.00 0.00 0.00 2.00 0.00 5.00 1.00 1.00 6.00 1.00 7.00 6.00 7.75

Total

43.26

46.75

5

DURING

Intakeltime (gW

Nomadic day

0.93 0.00 0.01

2

-

4d

1 3d

-

5c

-

6 7d 8 9 10 1lC 12 13d

0.00 -

0.20 0.84 0.63 0.68 0.71 0.93 1.67 1.32 1.25 0.93

COMPLETECYCLE",^

Intake (g)

Time (hr)

9.50 9.50 9.00 10.00 9.00 10.50

Intakeltime &/day)

25.99 12.73 8.22 16.20 12.73 24.95 16.20 6.11 21.07 13.79 15.91 0.00 16.20

10.50 10.25 9.50 9.00 0.00 10.00

2.69 1.34 0.91 1.62 1.41 2.38 I .62 0.68 2.06 1.45 1.77 1.62

189.70

116.75

1.62

10.00

“From Mirenda (1978). bThe statory phase began on July 18, 1976. The nomadic phase began on August 5 , 1976 ‘Booty intake based on counts and estimates. dBooty intake on these days based on estimates only.

According to Schneirla’s theory of brood stimulation, the behavioral cycle in both Eciton species is regulated by stimulative interactions between the large developing broods and the adult worker ants (Fig. 1). At the start of a nomadic phase, a mature pupal brood completes its development and emerges from cocoons as lightly pigmented callow workers. The callows are highly excitatory to the adult population. This sudden and intensive social stimulation, originating through callow-adult interactions and transmitted throughout the bivouac by communication among the mature adults, starts the colony off on a new nomadic phase. As the callows mature, however, their chemotactual excitatory effects decline, but nomadic activities in the colony are now maintained by equivalent stimulation imparted to the adults by a brood of developing larvae, hatched from eggs laid by the queen shortly after the onset of the previous statary phase. Later, as this maturing larval brood ceases feeding prior to pupation, the adult worker population receives only minimal stimulation, and the colony lapses into the statary phase. The queen then lays a new batch of eggs which hatch into larvae at

88

HOWARD TOPOFF

the same time that the present pupal brood ecloses into callows. The callows initiate a new nomadic phase, and the cycle is repeated. The army ant genus Neivamvrme.r differs from Eciton in several key respects. First, unlike species of Eciton which are essentially neotropical, Neivamyrmex extends well into temperate zones (from about 45” N to 45” S). Second, in tropical habitats nomadic colonies of Eciton species typically commence raiding at dawn and begin their emigrations in late afternoon or evening. In the arid environments of the southwestern United States, Neivumyrmex emerges from its subterranean nest only after sunset. Third, while colonies of the dominant Eciton species may contain several hundred-thousand individuals, the colony size range for Neivamyrmex is only 10,000 to 100,000 ants. Finally, whereas the nomadic-statary cycle of tropical Eciton continues virtually uninterrupted throughout the year, colonies of Neivamvrniex in temperate habitats cease cyclic behavior with the onset of colder temperatures in the fall, and remain dormant until springtime. Between April and October, however, these colonies of Neivnmyrme-r exhibit the typical cyclical pattern of behavior in which nomadic phases of intensive foraging (Table 111) and frequent emigrations are followed by statary intervals with reduced raiding and no change of bivouac (Schneirla, 1958).

ECOLOGYOF CHEMICAL COMMUNICATION IV . BEHAVIORAL A.

LABORATORY STUDIESOF TRAILFOLLOWING

In addition to the behavioral processes of group predation and nomadic emigrations. army ant workers share an important morphological characteristic-the absence of multifaceted compound eyes. At best, as in the genera Eciton and Neivumyrmex, each eye is reduced to a single, ocellus-like structure. At the other extreme are species of the Old World genus Aenictus, in which the receptors are reduced to an area of lighter pigmentation on both sides of the head. Although these receptors respond to changes in illumination intensity, it is doubtful whether they can function in image perception. As a result of this sensory deficit, it is not surprising that both raiding and emigration behavior in army ants are based on a process of recruitment that relies heavily on chemical and tactile cues. In studies of communication among ants, the term “recruitment” subsumes qualitatively distinct social interactions that have the common effect of assembling nestmates for food retrieval, colony defense, nest construction. or emigration. In patterns of recruitment thought to be primitive, such as social carrying and tandem running. tactile interactions between individuals predominate (Wil1974; Moglich and Holldobler, 1974). In most son, 1959; Holldobler et d., derivative patterns, however, orientation to a deposited chemical trail becomes

RAIDING AND EMIGRATIONS IN ANTS

89

increasingly important (Wilson, 1962; Szlep and Jacobi, 1967; Holldobler, 1978; Topoff and Mirenda, 1978a,b). In army ants, raiding and emigrations were thought to be conducted on a relatively nonvolatile chemical trail deposited from the hindgut of the workers (Blum and Portocarrero, 1964; Watkins, 1964; Torgerson and Akre, 1970; Topoff et ul., 1972a,b). Although this trail substance (consisting of fecal material) fits the requirements for the ants’ exploratory behavior, it was commonly believed that active recruitment should involve a more volatile chemical that is deposited only as long as the stimulus source (food, predator, new nest) is present. The first behavioral evidence for a unique recruitment trail was provided by Chadab and Rettenmeyer’s (1975) field study of Eciton, in which they demonstrated that the trail deposited by an aroused recruiting worker is sufficient to elicit mass recruitment. Because of the difficulty of working with Eciton in the field, however, the level of recruitment was low and the phenomenon not always reproducible. As a result of our ability to house colonies of the smaller army ant Neivumyrmex nigrescens in laboratory nests, we were able to conduct behavioral tests under more carefully controlled conditions. Colonies of N . nigrescens were maintained in shallow observation nests (30.0 X 30.0 X 0.5 cm). The nest was connected to plastic feeding boxes by interlocking sections of lucite tubing (3 .O-cm diameter) filled halfway with white sand. To minimize disturbance to the ants (which are nocturnal), all tests were conducted at night, under red illumination. To determine whether a single worker of N . nigrescens could indeed initiate mass recruitment, we utilized a single nest that was connected to two consecutive food boxes (Fig. 2). Midway between the nest and food box 1, a short (10 cm) tubular runway was connected perpendicularly. A second piece of tubing (2 m long) was cut in half lengthwise, thus creating a runway open on the top. The lower end of this runway was attached to an open box, and the upper end slid tightly over the short tube. Both the short and long perpendicular runways were lined with a 3-cm wide strip of chromatography paper. Finally, a door that opened vertically was inserted at the junction between the short and long runways . At the start of the experimental test, the door was removed and the nest opened. As is usual, the ants quickly established columns throughout all runways and boxes. After 10 min of exploratory activity, the door was placed in position and the ants in the longer perpendicular runway removed by aspiration. A wire mesh cube containing 20 pupae of the ant Truchymyrmex arizonensis was placed in food box 1, and a cork inserted into the front (i.e., nestward end) of the food box. The mesh was large enough for workers of N . nigrescens to enter and contact the food. The cork, in turn, prevented ants aroused by the booty from recruiting other individuals out of the nest. As soon as several army ants had entered the booty basket and contacted the food, the basket was lifted out of the

90

HOWARD TOPOFF

FIG.2. Apparatus used to distinguish between army ants’ response to exploratory and recruitment trails. Numbers and arrows indicate positions and directions of monitored ant traffic. (From Topoff et a / . . 1980a.)

food box and transferred to the empty box at the lower end of the perpendicular runways. At this time we started recording ant traffic (utilizing an eight-channel event recorder) at two positions: (1) near the nest exit, and (2) midway down the short perpendicular runway (see Fig. 2). Only one army ant was permitted to leave the booty basket and run toward the moveable door. All other ants were aspirated as soon as they left the mesh basket. As soon as the first recruiting ant reached the door, the door was removed and the ant allowed to enter the main ant column. After opening the door, we continued to record ant traffic at the same two positions for an additional 8 min. As a control test, we repeated the above procedure, but used a booty basket that contained no food. Thus any ant leaving the basket should still be in an exploratory phase and should not recruit nestmates. A comparison of recruitment behavior between the experimental and control tests is shown in Fig. 3 (Topoff et af., 1980a). Within each test condition, the arrow indicates the time of door opening. In the experimental series, there was an abrupt increase in the number of ants leaving the nest within 5 min after the door was opened (position I ) . Furthermore, the graph of position 2 shows that most of this outbound ant traffic moved into the perpendicular runway. In the control test

91

RAIDING AND EMIGRATIONS IN ANTS

50

-I"

W n

150

-

/--.

3

z

100 -

50

I

.

,./-

_.-.-.-.-._. _._.-.-. -~.-.--*'

F

i

100 1501

1

I

I

I

I

1

I

I

I

1

2

3

4

5

6

7

8

1 9

1

I 0

1

I 1

I

1

2

1

I 3

1

I 4

TIME (MIN)

FIG. 3. Magnitude of recruitment elicited by recruiting ant (lower graphs), exploring ant (middle graphs), and by new terrain (upper graphs). Arrows indicate times when door (Fig. 2) was removed for each test condition. (A) Control-no trail, position 2; (B) control-no trail, position 1; (C) control-exploratory, position 2; (D) control-exploratory, position 1; (E) experimental, position 2; (F) experimental, position 1. (From Topoff et al., 1980a.)

92

HOWARD TOPOFF

(labeled “exploratory” in Fig. 3), by contrast, no significant increase in ant traffic occurred. Having demonstrated that mass chemical recruitment could be initiated by allowing one aroused ant to contact nestmates, we next conducted a test to determine whether the trail deposited by a recruiting worker was by itself sufficient to arouse nestmates to mass recruitment. Procedures for this experiment were similar to those described above, in that only one food-aroused army ant was allowed to leave the booty basket and run toward the door. In this experiment, however, the recruiting ant was aspirated at the same time that the door was removed. As a result. ants from the main column passing through the door would encounter only the trail deposited by the recently removed ant. This experiment also utilized a single (exploratory) control condition, in which the

Ic

1

1

I

I

7

.

I

I

3

4

5

I

1

I

6

7

8

I

I

9

1

0

TIME (MIN)

FIG.4. Level of recruitment elicited by chemical trail deposited by recruiting ant (solid line), and by trail deposited by exploring ant (dotted line). Arrows indicate times when door was opened for each test consition. (A) Position 3: (B) position 2; (C) position 1. (From Topoff et a / ., 1980a. )

RAIDING AND EMIGRATIONS IN ANTS

93

aspirated ant came from an empty booty basket. In both the experimental and control tests, traffic away from the nest was monitored at an additional position (no. 3 in Fig. 2), in front of food box 1 . The magnitude of mass recruitment elicited by contact only with a chemical trail deposited by a food-aroused ant is shown in Fig. 4. Within 4 min after the door was opened, there was an abrupt increase in ant traffic out of the nest. And as in the previous experiment, most of this outbound traffic promptly made a 90" turn and entered the perpendicular runways. Recordings from position 3 show, however, that many of the recruited ants by-passed the runways and continued running toward food box I . The significance of this phenomenon, which we have termed recruitment overrun, will be discussed below. Finally, there was again no increase in traffic out of the nest during the control test. In our laboratory studies of recruitment behavior, we have repeatedly noticed that recruiting ants behave quite differently from those in an exploratory phase. In particular, food-aroused ants run faster and with an erratic up-and-down movement. We quantified these behavioral differences by photographing ants at 64 frames per sec, before and after they contacted food. The mean running speed for 11 ants moving toward food was 3.4 cm/sec (range 3.2-3.7 cmlsec). After contacting food, the mean running speed increased to 4.6 cm/sec (range 4.4-4.8 cmisec). This was accompanied by a corresponding increase in the amplitude of antenna1 and head movements. In addition, our analysis of the films showed that ants do not always promptly pick up booty and return to their bivouac. Instead, they may run back and forth over a distance of several centimeters, contacting almost every ant encountered in their path. It is during this back and forth movement that the ants exhibit the most vigorous vertical displacement of the appendages. A similar type of looping movement occurs during recruitment to food in Eciton (Chadab and Rettenmeyer, 1975), the weaver ant Oecophyllu Zonginoda (Holldobler and Wilson, 1978), and the fire ant (Wilson, 1962). The mechanical interactions between recruiters and nestmates undoubtedly serves to arouse nestmates to trail following, in much the same way as occurs during the related communicatory process of group recruitment (Moglich and Holldobler, 1975; Dlussky et al., 1978). Finally, recent morphological investigations by Holldobler and Engel (1978) have provided new insight into the chemical basis of recruitment in army ants. Both Eciton and Neivamyrmex have large pygidial glands (located in the dorsal part of the gaster, and opening onto the ant's surface at the seventh abdominal tergite, which is called thepygidiurn). In both the army ant genera, the gland's reservoir opens directly above the anus at the tip of the gaster. The dorsal membrane near the exits of the reservoir is modified into a brushlike structure. Because our filmed analysis of Neivamyrmex shows that recruiting ants often bend theirgasters to form a 90"angle with the substrate, the pygidial gland is indeed a leading candidate as the source of the army ant recruitment pheromone.

94

HOWARD TOPOFF

Colony 77N-IA

Prey species

Combined

Nests Percentage of Nests Percentage of Ncsts Percentage of raided total raided total raided total 18

5 0 5 0 0 ?

4 1 2 I 1

0 I 6 9 Total

Colony 77N-5

58

31.0 8.6 0.0 8.6 0.0 0.0 3.3 6.9

26 16 20 13 5 2 II

6.9 3.3 I .7

2 0 I

1.7 0.0

1 1

1.7

0

10.3 15.5

I8 24

1

18.4 11.3 14.2 9.2 3.5 1.4 7.8 0.7 I .'I 0.0 0.7 0.7 0.7 0.0 11.8 17.9

I41

44 21 20 18

5 2 13

5 6 2 2

1 I

I 24 33

22.1 10.5 10.1 9.0

2.5 I .0 6.5 2.5 3.0 I .o I .0 1 .0 0.5 0.5 12.1 16.6

199

"From Mircnda er ol. ( 19801

B . ECOLOGICAL ASPECTSOF MASS RECRUITMENT Although the chemical identification and glandular location of pheromones still play an important role in studies of social insect communication, there has recently been an increase in emphasis on elucidating patterns of recruitment behavior that contribute to ecologically adaptive strategies of foraging (HiilIdobler. 1978). For example, all species of Eciron, as well as Lnbidus praedator and Nomamynex esenbecki are specialized predators of social wasps. Although attacked colonies frequently lose all of their brood, most adult wasps survive and quickly reestablish a nest. The importance and frequency of army ant attacks are evidenced by an array of defensive behaviors by the wasps, some of which are elicited only by the presence of army ants (Chadab-Crepet and Rettenmeyer, 1982). Neivarnyrmex nigrescens. a considerably smaller army ant, preys predominantly upon the brood of other (non-Eciron) ant species. Some of these prey, including the formicine Camporlofirsfesfinafusand the myrmicine species ,Yovomessor cockerelli, Pheidole desertorurn, and Trcichymyrrnex arizonensis respond to the presence of army ants by removing their own brood and abandoning their nest (Droual and Topoff, 1981; LaMon and Topoff, 1981). In many

95

RAIDTNG A N D EMIGRATIONS IN ANTS

cases, the panic alarm exhibited by the prey species is again specific for army ant predators (Tables IV and V). Because of the patterns of defensive behavior exhibited by prey species, the success of army ant predation depends upon their ability to have a critical striking force continuously available for recruitment to all potential prey sites. One way army ants accomplish this is by recruiting nestmates when they first emerge from the bivouac at dusk, long before a booty aupply is located. This phenomenon was documented in the laboratory by connecting the nest to two consecutive food boxes, placed 4 and 8 m away from the nest, respectively. At the start of the test, one door was placed 10 cm from the nest exit and a second placed at the far end of the first food box. Baseline traffic in and out of the nest was recorded for 5 TABLE V RESPONSES OF THREESPECIES OF Camponotus

TO THE

PRESENCE OF ARMYANTSO Speciesb

Treatment Interspecific contact 1 Neivamyrmex nigrescens 50 Neivamyrmex nigrescens Sustained N . nigrescens contact in arena and nest 10 Neivamyrmex texanus 10 Trachymyrmex arizonensis 10 Pheidole desertorum 10 Pogonomyrmex occidenralis 10 Camponotus festinatus 10 Campanotus ocreatus 10 Cumponotus vicinus Abiotic disturbances Physical arousal of individual workers Mechanical disturbance of nest Olfactory tests Live Neivamyrmex nigrescens, screen enclosure in arena or nest Neivamyrmex nigrescens body odors on filter paper Freshly killed N. nigrescens in arena Neivamyrmex nigrescens trail substance Methylene chloride or acetone extracts of N nigrescens

Camponotus festinatus

Camponotus ocreatus

Camponotus vicinus

E E

X

(018) (414)

X R

(018) (414)

(212) (414) (012) (012) (013) (012)

R R

(2/2) (414) (012) (012) (013) (012) (0/2)

NC E

x x X

(7110) (616)

(414) (012) (012) (014)

NC

R R R

x x X

x

x x X

x x

X X

(0/2) (0/2)

NC

X

(012)

NC

X X

(016) (016)

X X

(016) (016)

X X

(016) (0/6)

X

(0/4)

X

(014)

X

(014)

x x x

(0/2) (012) (012)

x x x

(012) (012) (012)

x

x

x

(012) (012) (012)

X

(014)

X

(014)

X

(014)

OFrom LaMon and Topoff (1981). b X , No response; R, recruitment; E, nest evacuation; NC, not conducted. Ratios represent number of responses as indicated per number of replications.

96

HOWARD TOPOFF

min, after which the first door was opened. This allowed the ants to enter the runway and the first food box. After recording ant traffic for an additional 20 min. we also removed the door at the exit from food box 1. Bidirectional ant traffic at the nest exit was then monitored for an additional 25 min. Before the first door was removed, traffic was equally light in and out of the nest (Fig. 5 ) . Within 1 min after opening the first door, a surge of ants exiting from the nest occurred. Typical of the mass recruitment process, this initial outbound traffic was accompanied by a decrease in the number of ants returning to the nest. After approximately 10 min, however, outbound traffic subsided and returning traffic increased. When ant traffic had stabilized, we then opened the second door, thus giving the ants access to a new runway and food box. This was followed by a second (although smaller) surge of ants out of the nest. Additional support for the notion that army ants can recruit to a new substrate can be gleaned by referring to the topmost portion of Fig. 3 (the no-trail control condition). In this control test (as in the experimental condition), the ants were allowed to leave their laboratory nest and explore at1 boxes and runways. After 10 min, the door was closed, and all ants removed from the perpendicular runways (see Fig. 2 ) . While the door was closed, the long runway was lined with a new strip of chromatography paper. Baseline data for ant traffic was recorded for 9 min, the door was then opened, and traffic recorded for an additional 5.5 min. During the baseline phase of this test, ant traffic out of the nest was

200 w,

i

150

r

100

50

~,5

10

15

20

1

~~

25

30

35

40

45

~

50

TIME (MINI

FIG.5 . Magnitude of recruitment elicited by allowing army ant workers to encmntcr substrate containing no chemical trails. Arrow at left indicates time when nest door was opened. Arrow at right indicates time when door at far end of food box was opened. Solid line represents movement away from nest; Dotted line represents movement toward nest. (From Topoff rt d., 1980a.)

97

RAIDING AND EMIGRATIONS IN ANTS

A

U

0

a y1

m

5 z

200

1w

1

3

5

7

9

11

13

15

17

TIME (MIN)

FIG. 6. Comparison of recruitment to food (solid line) from direction of nest (B) and from terminal box (A) in opposite direction (dotted line). Arrows indicate time when food was introduced. Eventual increase in traffic away from food in (B) represents workers returning to the nest with booty. The corresponding increase in (A) is caused by recruitment overrun. (From Topoff et al., 1980a.)

relatively high. As a result, no obvious increase was recorded at the nest after the door was opened. Nevertheless, the increase in the number of ants moving into the perpendicular runway shows that recruitment indeed occurred shortly after the ants encountered the clean substrate. For N . nigrescens, the recruitment to new foraging areas plays an important role in generating the multibranched trail system that ensures the availability of a large striking force within easy reach of any booty site that is eventually located. When a suitable ant or termite nest is found, the ensuing mass recruitment to this food source clearly takes precedence over the recruitment to new substrate. In the field, this is evidenced by the fact that ants in columns adjacent to the booty site promptly reverse direction and “drain” into the column containing the successful raiding front. An additional adaptation of army ant foraging is the ants’ tendency to recruit many more individuals than are capable of actually participating in the raid. In some instances, the limiting factor is the size of the entrance to the prey nest. This phenomenon, which we have termed recruitment overrun, does not produce a chaotic situation in which the excess ants simply mill around outside of the

98

HOWARD TOPOFF

raided nest. Instead, the raided site becomes the base of operation from which a new trail system arises. Thus, many of the recruited workers soon run right past the raided nest, and become part of the ant column that is extending the newly developed trails. To demonstrate recruitment overrun in the laboratory, a feeding box was placed 1 1 m from the nest. An empty terminal box was placed an additional 1 1 m beyond the food box. The ants were thus able to leave the nest and establish an unbroken exploratory trail through the food box and into the terminal box. Baseline traffic toward and away from the food box was then monitored for 5 min at two positions ( I ni to the left and right of the food box). One hundred termites were then placed in the food box, and bidirectional traffic recorded for an additional 11 min. Shortly after the introduction of the termites, the number of ants moving toward the food box increased from both directions (Fig. 6). Recruitment from the nest was appreciably stronger, which probably reflects the fact that more ants are available for recruitment from the nest than from the terminal box. After several minutes, the number of ants moving away from the food increased, as these booty-laden ants returned to the nest. Note however, that there was also an eventual increase in ant traffic away from the food box (Fig. 6A). This was not due to ants carrying booty into the terminal box (because all booty-laden ants always return to their bivouac), but to recruitment overrun. In other words, many of the ants that were recruited from the nest did not stop after reaching the food site; instead, they continued through the food box and into the next runway leading to the terminal box. C.

MULTIPLEUSE OF

THE

MASS RECRUITMENT SYSTEM

Although many studies of ants have focused on recruitment to food, relatively few have examined the communicative basis for exploring new terrain and for changing nesting sites. Both the weaver ant (Holldobler and Wilson, 1977a,b, 1978) and the fire ant (Wilson, 1962) have been reported to recruit to new substrate and to shift nest location under adverse conditions. Within each of these species, it is significant that the same pattern of recruitment (including the same pheromone) is utilized for all three behavioral processes. Although army ants also recruit to food and to new terrain, species such as Ecitun hamatum, E . Burc,helli, and N . nigrescens are among those unique forms which possess a regularly occurring nomadic phase in which colonies frequently emigrate to new bivouacs (Schneirla, 1957. 1958, 1971; Rettenmeyer, 1963). We are now confident that the recruitment pheromone of army ants is qualitatively different from that of the exploratory trail. But because we do not yet know the glandular source of the recruitment chemical, we can’t rule out the possibility that different chemicals are utilized for recruitment to food, new terrain, and new nesting sites.

RAIDING AND EMIGRATIONS IN ANTS

99

Nevertheless, some indirect evidence suggests that army ants, like Oecophylla, use the same recruitment process in all three behavioral contexts. After establishing a multibranched trail system, the exploratory behavior of N . nigrescens is characterized by bidirectional ant traffic, with approximately equal numbers of workers running toward and away from the nest. Regardless of the behavioral context, recruitment is preceded by an increase in arousal of varying numbers of individuals, which run back and forth in a highly excited manner. The resulting recruitment always leads to an essentially unidirectional movement of the ant column, with the distance between individuals reduced to a minimum. Although recruitment from the nest to new terrain and to food are very similar processes, recruitment to new nesting sites during emigrations is unique in that it involves the queen, newly eclosed callows (at least early in the nomadic phase), and the brood-carrying workers. In our earlier laboratory studies of Neivamyrmex (Topoff and Mirenda, 1978a,b), we reported that the spatial organization of colonies is such that emigrations can result simply from an increase in the duration of mass recruitment. Thus, during foraging, the callows, brood, and queen are sequestered toward the center of the nest, and therefore buffered from the increased level of arousal that accompanies recruitment. When a new nest is located, however, recruitment from the nest continues until workers near the brood, queen, and callows become exposed to general excitation, and join in the exodus. The behavior of the queen and callows poses no particular problem for our analysis, because they remain quite passive in the nest until activated by mechanical interactions from aroused nestmates. One remaining problem, however, is the mechanism responsible for the adult workers picking up the larval brood prior to leaving the bivouac. Thus, although the overall exodus from the nest during an emigration may be due to a process of mass recruitment essentially the same as is used for foraging, we remain open to the possibility that emigrations are organized by the utilization of one or more additional pheromones that elicit brood-carrying behavior.

TESTSOF BROOD-STIMULATION THEORY V. EMPIRICAL A.

AND CALLOWEXCITATION

THE

ONSETOF NOMADISM

According to Schneirla’s theory of brood stimulation, the onset of each nomadic phase is caused by intense social stimulation abruptly released into the colony by the eclosion of a mature pupal brood into lightly pigmented callow workers. Schneirla based his theory primarily upon field observations of those species of Eciton, Neivamyrmex, and the Old World genus Aenictus that exhibit distinct behavioral cycles (Schneirla, 1957, 1958, 1971; Schneirla and Reyes,

100

HOWARD TOPOFF

1966, 1969). In the African driver ant Dorylus, however, emigrations are episodic, with single changes of bivouac separated by intervals ranging from less than 1 week to more than 2 months. Nevenheless, field studies by Raignier and van Boven (1955) showed a strongly positive correlation between brood condition and emigrations, marked by the emergence of a large population of callows near the time of each prolonged exodus. In species exhibiting regular behavioral cycles of activity, a population of newly hatched larvae is present in the nest during the period of eclosion. Schneirla maintained that stimulation from these larvae is not a significant factor in colony arousal until nomadic day 4 or 5 (when callow excitation has subsided). His downgrading of larval stimulation at the start of the nomadic phase was based on the untested assumption that small larvae, sequestered in a single mass deep within the nest, could not have a major stimulative effect on the large adult population. The first empirical test of callow stimulation was conducted by Topoff et al. (1980b), again utilizing our ability to collect and manipulate intact colonies of N . nigrescens. Our goal was to artificially create a colony that had mature pupae (.just prior to eclosion) but no larval brood. Because it was too difficult to physically separate the tiny, newly hatched larvae from the adult workers, we used an indirect procedure in which a larval brood from a nomadic day-7 colony was removed and replaced with a pupal brood from an early statary colony. We reasoned that if the queen of this “synthetic” colony maintained her egg-laying cycle, the introduced pupal brood would eclose into callows about 7 days before her next brood of eggs hatched into larvae (see Fig. 7 for an illustration of this rationale). Both colonies were collected in the field at the appropriate stages of their behavioral cycles and placed in a cold room (at 4°C) for 2 hr. When the ants were inactive, the brood of each colony was removed by aspiration. The pupal brood (consisting of approximately 3OOO individuals) was then introduced into the nomadic colony (which was culled to contain about 6000 adult workers). The colony was promptly releascd back into the field, where its activities were monitored for 23 days. The artificially created colony moved into the first subterranean bivouac encountered after its release. After 3 days at this site, the colony made two consecutive nightly shifts (distinguished from a real emigration by the absence of prior raiding). Because many of the adult workers were transporting pupae, these shifts revealed that the introduced brood had indeed been accepted by the host colony. For the next 12 days, the colony stayed in the same underground site and behaved like a typical statary colony (i.e., with nights of either brief raids or no above-ground activity). The first strong raid, characterized by an extensive trail system and heavy booty capture, occurred on the next night. And on the following night, the predatory raid was followed by a full-scale emigration. Samples of

RAIDING AND EMIGRATIONS IN ANTS

101

FIG.7. Behavioral cycle of Neivamyrmex nigrescens. Approximate duration of events is shown outside of numbered, phase-day circle. Note that periods of callow eclosion and larval hatching overlap during transition from statary to nomadic phase. Temporal separation of eclosion and hatching caused by brood substitution is depicted inside the phase-day circle. By switching the broods on nomadic day 7, callows would emerge in the nest about 1 week before the next larval brood. (From Topoff et al., 1980b.)

workers taken at hourly intervals throughout the emigration revealed the presence of callows, deeply pigmented pupae (just prior to eclosion), and eggs. Significantly, no newly hatched larvae were present in the emigration column. Although no emigration occurred on the second nomadic night, the colony did emigrate on nomadic nights 3 and 4. And once again, our aspirated samples contained callows and eggs, but no larvae. Thus, the onset of nomadism in the absence of small larvae shows that callow-induced excitation is indeed sufficient for colony arousal during the first few nomadic days. Although the callows of N . nigrescens seem to be a principal source of stimulation, we are not so convinced as Schneirla that eclosion per se is the process that initiates nomadism. Our observations of pupal eclosion in four laboratory nest of N . nigrescens indicate that colony arousal is indeed high at this time (Topoff and Mirenda, 1978a,b). Each mature pupa is attended by up to four adult workers that excitedly scrape off the pupal skin. Throughout the period of eclosion, the adult ants avidly lick the most pupal skin and all parts of the body of the

102

HOWARD TOPOFF

newly exposed callow. a process strikingly analogous to that occurring during mammalian parturition (Schneirla and Rosenblatt, 1961). Our skepticism about the role of eclosion in initiating the nomadic phase stems from comparable observations of larval pupation. Indeed, this is also a period of increased arousal inside of the nest, as workers manipulate and lick both the shed larval skins and the emerging moist pupae. But despite this increased activity, pupation occurs at the start of the statary phase, when the level of raiding is low and no emigrations occur. A further complication stems from Schneirla's (1957) conclusion that newly emerged callows of Eciron are persistently active and feed voraciously in the hours following eclosion. Rettenmeyer (1963) observed samples from two colonies of E . hamartmi and reported that callows tend to remain inactive, clustered in large groups inside the nest. Our subsequent observations of callows of N . nigrescens (Topoff and Mirenda. 1978a,b) also show that newly eclosed individuals do not feed, and indeed form into tightly packed inactive clusters until stimulated by mature adult nestmates. Thus, although our study supports Schneirla's theory of callow-induced stimulation, the mechanism of that stimulation has yet to be elucidated. Furthermore, because the callows do not immediately feed, the primary adaptive value of the vigorous raiding at the transition from statary to nomadic phase is probably to ensure an adequate supply of food for the larvae. which d o commence feeding immediately after hatching.

B.

LARVALSTIMULATION AND NOMADIC-PHASE LENGTH

According to brood-stimulation theory, callow excitation subsides after the first few nomadic days, and comparable stimulation from the growing larvae keeps the colony at a high state of arousal until they cease feeding prior to pupation. The only experimental support for this notion came from a field study by Schneirla and Brown (1950). in which they demonstrated an abrupt reduction in nomadic activities after removing a portion of the larval brood. Additional support for the role of larval stimulation was provided by a more recent study (Mirenda and Topoff. 1980) demonstrating a significant correlation between larval growth and nomadic-phase length for N . nigrescens in two different habitats. When Schneirla extended the results of his studies on neotropical colonies of Eciton to nearctic populations of Neiwrnyme.r, his base of operation was the Southwestern Research Station. located 8 kni west of Portal, Arizona. At an altitude of 1600 rn, the study site is in an oak-juniper habitat (dominated by Arizona and Emory oak, alligator juniper, and Chihuahua pine). At this altitude, the modal length of the nomadic phase is 18 days (Table VI) and that of the statary phase is 19 days. The more recent study by Mirenda and Topoff (1980) was conducted instead in a desert-grassland habitat at an elevation of only 1250 m. This community receives about 287 mm of rain annually and has mixed

103

RAIDING AND EMIGRATIONS IN ANTS

TABLE VI NUMBEROF NOMADIC AND STATARY PHASES OF DIFFERENT LENGTHS FOR Neivarnyrmex nigrescensa Nomadic phase Desert

Oak woodland

Statary phase Desert

Oak woodland

Length (days) 10 11

12 13 14 15 16

17 18

19 20 21

"From Mirenda and Topoff (1980).

vegetational cover. For most of the year, shrubs such as mesquite, yucca, snakeweed, and morman tea dominate the landscape. Following the summer monsoon rains, however, grasses and a variety of annual flowering plants cover much of this valley bottomland. In this desert habitat, the modal length of the nomadic phase for N . nigrescens is only 13 days (Table VI), and that of the statary phase is 16 days. As shown in Fig. 8, these differences in phase length correlate with the fact that larvae from desert colonies of Neivumyrmex grow at a faster rate than those from colonies at higher elevations. This difference in growth rate, in turn, may be due to temperature differences between the two habitats. At 1600 m, the maximum and minimum temperatures average 29 and 13"C, respectively, during the summer months. In the desert study site, by contrast, the maximum and minimum temperatures for the same period average 33 and 18"C, respectively. The excellent relationship between larval growth and nomadic-phase length is clearly consistent with Schneirla's theory of larval stimulation. VERSUS INTRAPHASE DIFFERENCES IN C . BETWEEN-PHASE BEHAVIOR

Virtually all field and laboratory research conducted to date has verified that brood-stimulation theory remains a powerful conceptual tool for explaining differences in army ant behavior between the nomadic and statary phases. But Schneirla's attempt to apply the same theory to characteristics of raiding and

104

HOWARD TOPOFF

6.01

E -E

4‘5-

W

U

> a

3

3.0-

Y

0

0 W

L!

0

UJ 1.5-

0

I 2

i

6

0

Ib

12

1,4

I6

1’8

NOMADIC DAY

FIG. 8. Comparison of larval growth during the nomadic phase for two studies of N . tiigrescens. The maximum (large circles) and minimum (small circles) sizes of larvae are shown as a function of nomadic day. Larvae from desert-grassland habitat represented by solid circles. Larvae from cooler, oak-woodland habitat represented by open circles. (From Mirenda and Topoff. 1980.)

emigrations within phases gets only “mixed reviews.” For example, in studies of Ecitoiz burrhefli in Panama, Schneirla and Brown (1950) wrote that failures to emigrate during the nomadic phase were most likely between nomadic days 2 and 6 , the interval between the two periods of intensive brood stimulation: (1) from newly eclosed callows at the very beginning of the nomadic phase, and ( 2 ) from the larvae which present an increasingly potent stimulus as they mature. Table VII, summarizing the results of a recent field study of N . nigrescens (Mirenda and Topoff, 1980), shows, however, that failures to emigrate occur with about equal frequency at all points during the comadic phase. Indeed, similar results were obtained from Schneirla’s own field studies of Neivamyrmex in southeastern Arizona (Schneirla, 1958) and of Eciron burchelli in the rainy season (Schneirla and Brown, 1950). Only in the dry season did E . burchelli exhibit a reduction in the frequency of emigrations shortly after the onset of nomadism. It now seems clear that the location of food sources and the availability of suitable bivouac sites have an equally important effect on emigration failures during the nomadic phase. The interaction among the same complex of parameters also suggests why brood stimulation alone fails in its prediction of longer emigration distances as the nomadic phase progresses. Evidence from studies on Neivamyrmex by Mirenda (1978) and on Eciron by Rettenmeyer (1963) suggest instead that the

TABLE VII EMIGRATION FREQUENCY IN Neivamyrmex nigrescens A N D Eciton burchelli: SPECIES AND HABITATDIFFERENCESO

Species (season)

N . nigrescens (summer) N . nigrescens (summer) E. burchelli (dry) E . burchelli (rainy) E . burchelli (dry) E . burchelli (rainy)

Number of colonies

Nomadic days observed

Failures to emigrate

Nomadic day of failure

Source

6

94

11

2, 3, 5, 5 , 6, 9, 10, 11, 11, 12, 12

Mirenda (1978)

9

69

18

Schneirla (1958)

7

96

16

3

43

2,2,3,3,5,7,7,8,9,10,11,11,13, 15, 16, 20, 20, 20 2, 2, 3, 3, 3 , 3 , 4, 5, 6 , 6 , 7, 8, 9, 10, 12, 13 3, 4, 6, 9, 10

1

207

44

Not reported

1

120

51

Not reported

56

aFrom Mirenda and Topoff (1980). bFour of these failures occurred in a single colony subjected to an experimental reduction of the larval blood.

Schneirla and Brown (1950) Schneirla and Brown ( 1950) Teles da Silva ( 1977) Teles da Silva ( 1977)

I06

HOWARD TOPOFF

longest emigrations tend to occur in the middle of the nomadic phase. On the positive side, however, a recent study by Teles da Silva (1977) did confirm a systematic increase in the average distance of emigrations for three colonies of E . burchelli as a function of nomadic day. Clearly, additional comparative studies are needed to resolve this issue. Finally, Schneirla ( 1949, 197 1) also stated that raiding intensity (and therefore booty capture) should be larger at the end of the nomadic phase, as a result of the increasingly potent stimulus arising from the nearly mature larval brood. Similarly, raids should also be larger at the end of the statary phase, a result of stimulation from mature pupae and eclosing callows. Our field research with Neivamyrmrx confirmed only the build-up in raiding intensity at the end of the statary interval, but we were unable to document any systematic change in nomadic phase raid intensity or booty capture (Mirenda et al., 1980). Among colonies, however, we did find a positive correlation between colony size and raid intensity. Within each phase, larger colonies have more raid columns, cover more area, discover more prey sites, and gather more booty.

I

Bloltlgical

Hehaworal

Reoroducrion

1

-------

FIG. 9. Conceptualization of army ant behavioral cycle as resulting from dynamic interaction among colony individuals and between these individuals and their physical and biotic environment. (From Schneirla, 1957.)

RAIDING AND EMIGRATIONS IN ANTS

I07

I/ NI+FI=

6.4m

F1 +F2

= 10.4 m

F2+F3

= 4.9 m

F3 +NZ

= 10.4 m

N2-+F4 = 6.4m

FIG. 10. Arrangement of nest boxes, food boxes, and interconnecting runways that comprise “tube city.” Food box 3 is the critical junction, because ants must then select either nest box 2 or 3 as their next bivouac site. (From Topoff and Mirenda, 1980a.)

AND D. FOODLOCATION

THE

DIRECTION OF EMIGRATIONS

To Schneirla, the complex functioning of an army ant colony represents a level of social organization that emerges through interactions among all colony members and between these individuals and their physical and biotic environment (Fig, 9). Thus, although his primary contribution was in elucidating the relationship between brood development and nomadic behavior, I do not want to convey the impression that Schneirla was unaware of the role of food as an ecological parameter. After all, even at an early stage of his field research (Schneirla, 1938), he reported that colonies of Eciton emigrate along the heaviest raiding route of that day. Although this correlation was verified by Rettenmeyer’s (1963) subsequent field research, the large colony size and vast raiding area of Eciton make it difficult to conduct controlled studies on the relationship between food location and emigration direction. So once again Neivamyrmex nigrescens became the species of choice, enabling us to combine continuous observations in the field with controlled manipulations in the laboratory. For the laboratory phase of the study (Topoff and Mirenda, 1980a), we converted one room into a foraging and emigration area (Fig. lo). Colonies of Neivamyrmex were housed in large wooden boxed (each 1 m3) that were placed

Raiding tront reache5 N(iinadIc

day

5itc

N I Opcn

FS

N2

4 5

F4

2(100

F3 F5

I930 1x30 2030

7020 2006

2040 1015

1910

1946 2108

2033 20 I 0 I9Sl

7

FS

emigration

21ox 203 I 2055 2124 2049 2017 20711 2112

212%

-

2135

-

0f

N3

h

F4

Site of booty cache

Onset

th14

x

f 3 F4

2050 2021 1948 I935 2031

2044 2005

2040

1956

2056 201 0 2051 2118 2052 2015 2012 2107

2115

0

IS

10

F5

II 12 13

F3

2000 1930 I900 2000

2046

200s 2051

F4 F4

I900 1930

1938 1955

195-1 2010

1945 2016

2016 2029

2004 2026

14

F4

2000

2025

2051

2057

2111

2115

~~FIorn Topoff and Mirenda ( I980a)

19SX

214X

-

21 14 21 19

2105 2156

Emigration

Route of booty

I0

transport

N3

F4-N2- F3- N 3 F4-N2-F3-FZ-FI-NI FS-N3 FS-N3-F3-F2-F3-N3 F4-N2-F3-F2-FI-N I F5-N3-F3-F2-Fl-N I FS-N3 F3-FZ-FI-F2-F3-N2 F4-N2-F3-F2-FI-NI F4-N2-F3-F2-F1-N1 F4-N2

_..

N3

N3

.-

-

-

N3 I

I

N2 N2

I

-

NS N2 I

Aborted N2

RAIDING AND EMIGRATIONS IN ANTS

109

at window height outside the laboratory, thus exposing the nests to the die1 fluctuations in illumination, temperature, humidity, and barometric pressure. Each of the three nests was filled halfway with soil, rocks, and logs collected from the field. The rocks and logs were interspersed with soil, thus creating subterranean cavities for the ants to occupy. Because we constructed these cavities at varying depths, the ants were able to regulate brood development by shifting individuals into different vertical temperature zones. Substrate moisture was monitored continuously with a soil-suction meter, and was maintained at 3-5 centibars of pressure. After each emigration, the vacated nest box was emptied and refilled with new substrate materials. The three nestboxes were interconnected with 75 m of plastic: tubing (3-cm diameter) that was filled halfway with white sand. To simulate the field condition in which the ants typically raid over new substrate each night, the sand was redistributed by shaking the tubes each morning. Every third day the tubes were filled with new sand. Five small food boxes (30 X 15 X 15 cm) were interspersed with the tubular runways (as illustrated in Fig. 10). To determine the degree to which the route of an emigration is influenced by the location of food, two colonies were collected early in the nomadic phase and culled to contain about 6000 adults and 4000 larvae. To simplify the analysis of emigration behavior, the arrangement of the foraging tubes always provided the ants with only two alternative routes. Thus, each night’s raid out of N1 would lead the colony through F1 and F2, and into the crucial junction box, F3. From F3, the colonies always established simultaneous raids through W2 (to F4) and through N3 (to F5). By placing booty in either F4 or F5, it was relatively straightforward to determine whether emigrations occurred in the direction of food location. The only exceptions to this procedure occurred on nomadic day 11 for colony 2 (when food was placed in F3), and on nomadic day 10 for colony 4 (when food was omitted). Each night’s supply of food consisted of one batch of ant pupae weighing approximately 2 gm (the amount of food that a nomadic colony of this size ordinarily collects during a night of foraging). The relationship between emigrations and food location for two nomadic colonies of N . nigrescens is summarized in Tables VIII and IX. The tables include the times when the nest box (NI) was opened in the evening, the temporal progression of the raid column into F3 and beyond it through the two potential nest boxes, as well as the onset of the emigrations. For colony 2, no emigrations occurred on 5 of the 11 observation days in the laboratory. For colony 4, no emigrations occurred on 4 of 12 days. On these nights, the ants’ typical pattern of behavior was to transport the booty directly back to N1. On nights when emigrations occurred, they started within 33-104 min after the ants first reached the nest box into which they moved. Colony 2 emigrated in the direction of the booty on nomadic days 6,7, 10, and 14. On 3 of these days, the booty was removed from the food box and deposited in a subter-

Raiding front reachex Nomadic day

Food site

N I Open

F3

N2

N3

F4

6 7

F5 F4 F5 F4

I900 I930 2000 2015 1900 2030 I900 I930 2000 2030 2000 1900

1942 2008 2037 2044 I930 2105 I952 19.57 205 I 2105 2036 I 938

2007 202 I

I955 2016 2045 2121 I954 2 I30 2037 20 18 21 10 2129 20.58 I948

2029 2043

8 9 10 11

12 13 14 15 16 17

F5 FS F4 F4 F5 F4 F5

“From Topoff and Mirenda ( 1980a)

2052 21 10

I947 2121 2019 2028 21 18 2121 205 1 19.51

2117

2126 2011 2133 2044 2056 2142 2140 2118 2018

Onwt Of

of booty

Emigration

F5

emigration

cache

tO

2017 2058 2108 2142 2017 2147 20.55 2039 2135 2157 2122 2025

21 10 2125

SltC

N3 N3 __

-

-

2124 2235

N2 N2

2141 2215 2242 2215 21 16

N2 N2

N2 N2 N3

-

-

N3

N2

Route of booty transport

F5-N3 F4-N2-F3-N3 FS-N3-F3-F2-FI -N I F4-N2-F3-F2-FI -N I -

F5- N3- F3- N 2 FS-N3-F2-FI-N 1 F4-N2 F4-N2 FS-N3 F4-N2-F3-F2-FI -NI FS-N3-F3-N2

RAIDING AND EMIGRATIONS IN ANTS

111

ranean cache in the adjacent nest box (that subsequently became. the new bivouac). No cache formed on nomadic day 7; instead, the booty was being transported back to Nl when the workers were reversed by the emigration column. Colony 4 emigrated in the direction of booty location on nomadic days 6, 13, 14, and 15. Three of these emigrations were also preceded by the formation of a booty cache in the new nest adjacent to the food box. Of special significance, however, were the emigrations of colony 2 on nomadic days 4 and 11 and of colony 4 on nomadic days 7, 1 1 , and 17. These five emigrations took place toward nests that were in a direction opposite to that of the food. In these instances, the location of a suitable nest was clearly sufficient to elicit the full-scale emigrations. On most of these occasions (nomadic day 4 for colony 2; nomadic days 7, 11, and 17 for colony 4), the food was transported from the feeding box, through the adjacent nest box, back to F3, and then out of F3 toward the opposite nest box. The dissociation of emigrations from booty location was further evidenced by the emigration of colony 4 on nomadic day 10, when no food was administered. At the same time that the above laboratory stud was being conducted, we were also involved in conducting field observations on the relationship between food location, raiding, and subsequent emigrations (Mirenda et a l ., 1982). Colonies of N . nigrescens were located in the desert-grassland habitat and followed each night throughout their nomadic phase. For each colony, we recorded the number and location of raid, cache, and other potential nest sites explored by the ants. A raid site was defined as any hole in the ground that the ants entered and left with booty. A cache site was any location along the column that ants entered with booty and left empty-mouthed. The compass direction and distance from the old nest to each explored site was measured. Raid and emigration routes were sketched roughly as they developed and then recorded permanently the next morning on maps that incorporated the location of important sites on each column. Workers from six nomadic colonies typically formed and maintained surface columns, encountered prey, recruited nestmates to the raid sites, and brought booty back to the old nest before an emigration commenced. Indeed, some degree of raiding preceded 89% of the emigrations (n = 86) observed. For 77 nomadic emigrations, 53 (69%) began within 4 hr after the onset of raiding. Booty was brought back to the old nest before 47 of 56 emigrations (84%), and the emigration moved toward one or a group of raid sites 78% of the time (40 of 5 1 emigrations). The activity of colony 77N-1 on nomadic day 6 illustrates a typical series of events as seen at the periphery of the raid column and is illustrated in Fig. 11. The colony became active on the surface of 1900 hr (MST) as a column proceeded to the west. Over the next 2.5 hr, ants of this column discovered three raid sites and carried all booty back to the bivouac. At 1920 hr a second column

9

112

HOWARD TOPOFF

NES C 1

*-;fi -%

7

NEST 2

FIG. 1 I . Map of raid and emigration of colony 77N- 1 A on nomadic day 6 illustrating that army ants typically emigrate over a heavy raiding trail toward a cluster of booty sites. This colony raided from nest I , first to the west (where it located booty sites 1-3). then to the bouth (encountering food at sites 4 through 9). The colony finally emigrated under a bush near raid site 9. (From Mirenda er al., 1982.)

left the nest and headed south, locating prey at four more sites (nos. 4-7 in Fig. I I ) . Raiding continued on this column for the next 3 hr, during which all booty was again carried back to the nest. Between 2230 and 2300 hr, activity subsided, but another exodus from the nest began along the second column at 2310. Prey was then discovered at sites 8 and 9. At 2320 hr, workers began to explore a small hole at the base of an Ephedru (mormon tea) bush neat site 9. No booty was obtained at this site, but by 2340 hr the emigration had begun from nest 1 and proceeded directly to the hole (nest 2). Less typical, but important, was the activity of colony 77N-5 on nomadic day 11 (illustrated in Fig. 12). This colony began raiding in early evening and sent raid columns to the north, east, and west of the bivouac. The colony located 11 raid sites along these columns. After raiding for 2 hr and transporting all booty homeward, a branch of the east column split off to the south and entered a large rodent hole. Within 20 min, an emigration began from the old nest and proceeded directly into this hole (nest 2). Raid sites 12 through 23 were located well after the emigration had begun. In both cases shown in Figs. 11 and 12, no booty cache formed in or near the new nest site before the emigration. In all, caches formed prior to only 21% of the emigrations ( n = 33). Five of those caches formed in underground chambers to which the colony eventually emigrated. In two instances, the cache was formed on the surface within 3 m of the new bivouac. Ants depositing these caches did not carry any of the stored food into the new nest until workers carrying larvae in the emigration had passed the cache point. In other words, the ants forming these caches were apparently directed to the new nest (though only a few meters from it), but they did not direct nestmates to it.

RAIDING AND EMIGRATIONS IN ANTS

113

Of 86 emigrations 9 (11%) occurred with no prior raiding. All 9 instances occurred in situations when the colonies were probably having problems with their old nest, and these fall into three categories: (1) on nights following heavy rains when the study area was partially flooded, (2) following signs that the old nest was too small for the colony, and (3) on the last day of the nomadic phase when colonies may require nesting sites with special characteristics, suitable to house them for an entire statary phase. The results of these field and laboratory studies confirm that the location of prey colonies clearly influences the direction and distance of m y ant emigrations. On some occasions, colonies of Neivumyrmex may actually move into the prey species’ nest. But since these nests are obviously not always large enough to house an army any colony, it is more typical for army ants to bivouac in a subterranean nest in the vicinity of a cluster of raided sites. The fact that a particular area yields numerous prey colonies almost guarantees, the establishment of a network of army ant columns, and this, in turn, increases the probability that a suitable nesting site will be found. But the exceptions also show that

N

TSM

NES

FIG. 12. Map of raid and emigration of colony 77N-5 on nomadic day 11 illustrating that army ants can emigrate away from an area of previous heavy raiding. Early in the evening prey was discovered at sites 1-1 1. Later in the evening a raiding front branched off to the south and located hole in the ground which promptly became the next bivouac site. After the emigration, raid sites 12-23 were discovered. (From Mirenda et al., 1982.)

I14

HOWARD TOPOFF

raiding and emigrations can be completely dissociable behaviors, and that the location of a nesting site can elicit a level of recruitment sufficient to effect a fullscale emigration of an entire army ant colony. E.

FOODABUNDANCE AND

THE

FREQUENCY OF EMIGRATIONS

In the sense that the abundance and location of prey ant colonies influence the distance and direction of emigrations, food can be conceptualized as a rather static environmental factor in the life of army ants. But in another sense, the role of food can only be appreciated by considering the feedback relationships among food. brood, and adult individuals. Thus, the presence of booty outside of the bivouac is a potent source of colony arousal, as it typically stimulates mass chemical recruitment by successful foragers. But as Rettenmeyer (1963) first suggested, a large amount of food inside the nest may lower the level of larval and adult excitation. reduce (or even eliminate) foraging behavior, and thereby shift a nomadic colony into a statary mode. This concept of food, as a modifier of the interaction between the colony’s brood and adult population, is clearly consistent with Schneirla’s theory of brood stimulation. Although the nature of the stimuli that mediate brood excitation is not known, these stimuli clearly act as a primer pheromone by increasing the workers’ responsiveness to other classes of stimuli (such as prey or new nests), which in turn elicit specific patterns of recruitment. In the myrmicine ant Myrmica rubru, for example, it is well known that larvae can increase worker excitation and foraging (Brian, 1957, 1962; Brian and Hibble, 1963; Brian and Abbott. 1977). Perhaps the best empirical support for the interaction between food supply and brood stimulation comes from studies on the social organization of foraging in honey bees, in which workers can collect either protein-rich pollen or carbohydrate-rich nectar. Louveaux ( 1959) found that the amount of pollen gathered by an incipient colony is small, but increases as the larval population grows in size. In a subsequent study, he removed the queen from a mature colony and found that pollen collection was not affected until many of the larvae ceased feeding and pupated (Louveaux, 1958). Further evidence for larval stimulation of adult foraging was provided by Fukuda (1960; cited by Free, 1967), who showed that foraging workers from a recently divided colony collected very little pollen until the eggs laid by the newly mated queen hatched into larvae. Finally, Free (1967) demonstrated that adult worker foraging was influenced more by their direct access to the brood than by brood odor alone. Perhaps most significant was his additional finding that artificially feeding a honey bee colony with pollen resulted in a decrease in pollen collection and a corresponding increase in foraging for nectar. When Schneirla began his field research with surface-adapted species of Eciton in the tropics, he initially dismissed the role of food abundance as a

115

RAIDING AND EMIGRATIONS IN ANTS

Species

Time of dav 6 am

Ecifon bomotum

‘\I

4

12 pm

6 pm

12 am

6 am

--&--

Netvamyrmex nigrescens

Aenictus foeviceps

FIG.13. Daily schedule of nomadic activities for three genera of army ants. In Ecifon and Neivamyrmex, emigrations typically develop out of raiding columns. In Aenicfus, by contrast, emigrations may occur without prior raiding. This suggested to Schneirla that emigrations might be related to food abundance in the bivouac. Thin line, raiding; thick line, emigration, (From Schneirla, 1971.)

mediator of brood stimulation. But when he extended his studies to include comparisons with the Old World genus Aenictus, he noted that emigrations could begin at any time of the day or night (Fig. 13) and that they were not, as in Eciton, routinely correlated with raiding behavior. Thus, by the time of his last field study on Aenictus, he concluded that short-term variations in colony excitation may depend upon the “alimentary condition prevelant in the brood” and that emigrations are likely to begin shortly after food has run low (Schneirla and Reyes, 1969). The notion that food abundance within an army ant bivouac could significantly alter nomadic activities raises the intriguing possibility that nomadic colonies of Eciton, Neivamyrmex, and other groups that emigrate almost daily during the nomadic phase might not actually be able to secure enough booty to satiate their own larval brood. As a result, we began another series of laboratory and field studies, designed to determine whether artificially overfeeding a colony would lower the frequency of nomadic emigrations. For the laboratory study, we used four colonies of N . nigrescens, all collected early in the nomadic phase and culled to contain the same number of brood and adult individuals. Both colonies in group 1 (the underfed group) were given 0.5 g

116

HOWARD TOPOFF

of food each night, whereas the colonies in group 2 (overfed) were given 6.0 g of booty each night. For all colonies, the food was placed 22 m from the box containing that night’s bivouac (see Fig. 10). The results of this study showed that overfeeding a colony of N . nigrescens produces a marked reduction in the frequency of nomadic emigrations (Topoff and Mirenda, 1980a,b). Of the two overfed colonies, 77N-4 emigrated on only 3 of 12 nomadic days (Table X). Colony 77N-6 conducted only four emigrations during a 13-day nomadic period. By contrast, in the underfed group, colony 77N-7 emigrated on 8 of 11 nomadic days, and colony 77N-10 changed bivouac location eight times in I3 days. Thus for the two overfed colonies combined, emigrations occurred on 28% of the nomadic days, whereas the emigration frequency for the underfed colonies was 62% (x2 = 7.8, p = 0.01). In this laboratory study, colony arousal was reduced by artificially feeding the colonies early in the nomadic phase, after callow eclosion. The field study went one step further in that food augmentation began before the onset of the nomadic phase. The first colony used for this study contained approximately 80,000 adults and 50,000 larvae (a population at the high end of the range for N . nigr-mens in this desert habitat). It was found on July 11, 1980, late in its nomadic phase. On July 13, the colony settled into a kangaroo rat mound and became statary. For the next 13 nights the colony remained at the same location

Overfed Nomadic day

Colony 77N-4

Underfed Colony 77N-6

Colony 77N-7

Colony 77N- 10

RAIDING AND EMIGRATIONS IN ANTS

117

and staged either brief (1-3 hr) or no predatory raids. On statary day 17, the colony conducted a statary shift, which enabled us to observe that the pupae were deeply pigmented and callow eclosion had begun. Artificial feeding of the colony began on the next night, and we continued to supply food for 6 consecutive nights. Thus, during the period July 30-August 4, we administered 9.1, 34.7, 18.5, 32.6, 17.6, and 31.6 g of food, respectively. On average.,this represents about 1.2 times the amount of food that a colony of this size would normally gather on its own. Each evening during the period of food augmentation, a basal column appeared shortly after sunset (1800-1900 hr). On the days of heaviest feeding, when over 30 g of food were provided, the army ants required several hours to transport it back to their bivouac. The colony occasionally put out additional raiding columns later each night, but all captured booty was promptly taken back to the statary nest, and no emigration occurred. On the afternoon of August 5 , the study area received 14 mm of rain during the afternoon. The overcast sky, coupled with cool temperatures, enabled the colony to begin raiding earlier than usual. Thus, although we arrived at the site by 1800 hr, a long emigration was already in progress. Given the extraordinarily large size of the colony, we terminated food augmentation. The colony remained nomadic for the next 9 days, during which time it conducted six emigrations. To determine whether we had indeed delayed the onset of the nomadic phase, three types of evidence were analyzed: phase length, callow pigmentation, and larval size (Topoff et al., 1981). 1. Phase length. Because the colony was anchored temporally, July 13 was known to be the first statary day and August 5 the first nomadic day. Thus, the statary interval becomes 23 days. According to Mirenda and Topoff (1980), the range of statary-phase duration for N . nigrescens in the desert habitat is 15-19 days, with a modal length of 16 days. This suggests that the minimum delay in nomadic onset for our colony was 4 days. If we use Mirenda and Topoff's modal duration, the delay is calculated to be 7 days. 2. Callow pigmentation. Newly eclosed callows of N . nigrescens are yellow and acquire adult-like pigmentation between 7 and 12 days. Several hundred callows were collected from the colony during its first emigration on August 5, and compared with preserved samples collected daily from nomadic colonies in previous years. Although this visual comparison can not pinpoint the exact posteclosion day, our comparison indicated that callows from the overfed colony were 5-8 days old. 3. Larval size. Several hundred larvae were also collected during the first emigration. By visual inspection, we separated the 10 largest and 10 smallest individuals and measured them with the aid of a dissecting microscope (fitted with a micrometer). The mean length of the large group was 4. mm (range =

118

HOWARD TOPOFF

3.8-4.2 mm), as compared with a mean length of 1.5 mm (range = 1.3-1.7 mm) for the small group. When these data are compared with the graph of larval growth as a function of nomadic day (Fig. 8), they again correspond to a range of nomadic days between 4 and 6 . In sum, we were successful, through food augmentation. in delaying the onset of the nomadic phase in this large colony of N . nigrr.scrn.sby almost one week. For the next colony, which was considerably smaller. we did even better. The second colony used for food augmentation was collected during its last nomadic emigration and maintained in the laboratory until the pupal brood was fully pigmented. Prior to release in the field, the colony was culled to contain 4000 adults and 4000 pupae. By the next nomadic phase, approximately 4500 larvae were also present in the colony. This small colony size was chosen to increase our ability to significantly overfeed the workers, and because a laboratory colony of comparable size had previously been released without food supplementation and could therefore serve as an appropriate control. The nightly pattern of activity for this second colony is illustrated in Table XI. Because the colony was small, we were able to provide about five times more food than it would typically collect during a complete nomadic phase in the field. We were also able to monitor the time of onset and the duration of each night’s raid, in addition to the emigration frequency. The colony was released on statary day 15, and it promptly moved into a subterranean nest beneath the desert floor. The first raiding column appeared shortly after 2200 hr, at which time 9.0 g of booty were placed near the raid column. The workers removed this food in less than one hr, after which ail surface activity ceased. For the next 7 nights, the colony was either inactive on the surface or, at best, conducted only brief raids (each of which was followed by artificial feeding) but no emigrations. On August 15. we arrived at the study site after 2200 hr, and found the colony in an early stage of an emigration to a new site located 25 m to the northwest. We immediately provided 10.2 g of booty, placed 1 m from the old nest. This resulted in the recruitment of additional ants, both from the original nest and from the longer emigration column. All of the food was taken back to the old nest and the emigration was aborted. On August 19 (nomadic day I l ) , after not having been fed for 2 days, the colony conducted its only successful emigration. The move took the colony 19 m to the north, beneath an Ephedra bush. On August 25 we excavated the nest and forced it to shift its statary bivouac. This procedure verified that the colony’s brood was pupated. Thus, throughout a nomadic phase lasting 14 days, largescale overfeeding suppressed all but one emigration. During the 10 nights on which raiding occurred, the median time for raid onset was 2200 hr, and the median duration of each raid was 1.5 hr. The control colony, which was also released from the laboratory at the end of a

119

RAIDING AND EMIGRATIONS IN ANTS TABLE XI ACTIVITYSCHEDULE FOR ARTIFICIALLY FEDAND CONTROLCOLONIES OF Neivamyrmex nigrescens I N T H E FIELD^ Colony no. 2

Control colony

Activity

Date

Duration of raid

817

2215-2300

818

-

Occurrence of emigration

Activity

Food (8) Proposed provided phase day Date

9.0 -

819 8/10

2 130-0 120

811 1

-

-

8/12 8/13 8/14 8/15 8116 8/17

-

-

8/18 8/19 8/20 8/2 1 8/22 8/23 8/24 8125

1920-2210 0100-0235 2240-0145 2 140-22 10 2315-2350 0210-0305

7.5

6.9 -

10.2 9.3 8.5

-

-

2040-0330 2215-2305 2300-2350 2030-2110 -

-

8.0 10.0 9.5 -

-

-

Duration of raid

Omccurrence of Phase emigration day

-

S-15 S-16 N- 1 N-2 N-3 N-4 N-5 N-6 N-7 N-8 N-9

7115 7/16 1915-0515 7/17 1810-0340 7/ I8 20 10-0640 7/19 1845-0500 7120 1900-0400 7/21 2030-0515 7122 1940-0455 7/23 1850-0430 7/24 1800-0420 7/25 1820-0305

+ +

N-10 N-11 N-12 N-13 N-14 s-1 s-2 s-3

7/26 1745-0430 7/27 1830-0300 7/28 1840-0410 7/29 1920-0400 7/30 2010-0625 7/31 2015-0615

+ + + + +

-

+ + -

-

+ + -

S-16 S-17 N- 1 N-2 N-3 N-4 N-5 N-6 N-7 N-8 N-9 N-10 N-11 N-12 N-13 N-14 N-15

UFrorn Topoff et al. (1981). bEmigration started but reversed by feeding. See text for details. 'SS, Statary shift forced by excavation of bivouac.

statary phase, exhibited more typical patterns of nomadic behavior (Table XI). During a 15-day nomadic phase, the colony emigrated on 11 nights. Some degree of raiding occurred on every nomadic night. Finally, the median time of raid onset for this control colony was 1850 hr, and the median duration of raiding was 9.7 hr. In comparing the nomadic activities between the experimental and control colonies, it must be emphasized that a reduction in the frequency of emigrations is by itself not sufficient for inferring a relationship between food abundance and colony arousal. In all of our laboratory and field studies, supplemented food was always placed near a raiding front relatively close to the bivouac. In most cases, the army ants established few or even no additional raiding columns beyond the

120

HOWARD TOPOFF

feeding site. Thus, our procedure reduced the ants’ ability to locate a suitable nesting site, which is a prerequisite for a successful emigration. The case is made considerably stronger, however, by comparing the temporal aspects of raiding behavior between the two colonies. The experimental colony, for example, conducted no raids on 4 nomadic nights. By comparison, the complete absence of raiding (on stormless nights), while typical of statary colonies, has never been reported for a nomadic colony of N . nigrescens. Finally, when we compare both the time of raid onset and the duration of raiding for the two colonies, we can conclude that overfeeding can effectively shift the level of overall colony activity from a nomadic to a statary condition.

VI.

CONCLUSION

Practically all species of ants at some stage of their life cycle exhibit the same patterns of behavior that characterize army ants. For example, emigrations may occur at the beginning and end of the functional season, when a colony grows too large for the size of its nest, or if it is disturbed by the intrusion of other animals. And even more widespread (at least for species in temperate climates) is the increase in foraging for food in the spring, when the queen’s first batch of eggs hatches into actively feeding larvae. This is actually the pattern of reproductive activities for many species of army ants, which is undoubtedly why they lack distinct behavioral phases. What makes species such as Eciton hamatum, Eciton burchelli, Neivamyrmex nigrescens, and Aenictus laeviceps unique is the concordance of abrupt, large-scale, and persistent changes in raiding intensity, food capture, bivouac location, and emigration frequency. And it is only in these species that the queen becomes reproductively active in distinct cycles, resulting in the synchronous development of all brood stages. Thus it is easy to see why Schneirla devoted so much effort to developing brood-stimulation theory. Although the larvae of all ant species are a source of chemical and tactile stimulation to adult workers, the synchronous hatching of huge numbers of larvae in army ants produces an increase in activities sufficiently abrupt and sustained to generate a distinct nomadic phase. To Schneirla, the chemical and tactile communication between larvae and their adult sister workers is comparable to the interactions that occur between mother and young during the development of social bonds in mammals. Thus brood-stimulation theory was the vehicle by which Schneirla extended his analysis of the ontogeny of social behavior from vertebrates to social insects. Virtually all investigators agree that brood-stimulation theory was a breakthrough in increasing our understanding of army ant social organization. As I have described in this article, our studies of brood substitution, larval growth

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121

rates in different climatic habitats, and raiding intensity between phases have all yielded results consistent with Schneirla’s theory. Nevertheless, Schneirla was criticized for relying too heavily on brood stimulation and other behavioral processes occurring within the colony itself, at the expense of external environmental and ecological factors. Chief among these factors is food-its quality, location, and abundance. Actually, questions about the relationship between food supply and nomadic behavior became somewhat confused over the issue of ultimate versus proximate causation. On the one hand, Schneirla acknowledged the role of food in an evolutionary sense by concluding (Schneirla, 1944) that “the lack of food can at best be only a very indirect and secondary cause of insect migration-that is, lack of food operates selectively in the evolutionary process rather than directly and ontogenetically.” And in a subsequent paper (Schneirla, 1957), he reiterated that “an early stage in the evolution may have involved changes in colony nesting site enforced through depletion of food in the occupied zone. This is no longer true for any well-known doryline. Rather, the nomadic changes now seem due to stimulative colony arousal mechanisms based upon reproductive processes. Thus to Schneirla, the adaptive relationship between food and nomadism was attributable to fluctuations in the level of brood excitation, and the effect “is important of whether or not the brood, source of determinative stimulation, can feed at the time” (1957). Although colonies of Neivamyrmex, as we have shown, stage raids of much greater magnitude during the nomadic phase, raiding obviously also occurs on many statary days. We have no reason to believe that the process of group recruitment, involving a combination of an exploratory and recruitment trail, is in any way different between the two behavioral phases. Nomadic and statary raids are directed to the same target species, and the army ants explore many potential nesting sites. And yet it is extremely rare for an undisturbed statary colony of army ants to conduct a prolonged emigration. Clearly, the huge adult population of workers is in a different state of behavioral arousal in each phase, and the larval brood is unquestionably the source of a major portion of this arousal during the nomadic phase. But the aroused ants have to be channeled to appropriate bivouac sites. Both our field and laboratory studies 011 the location of raiding sites show that the nests of prey species (as well as the area around these nests) are often the focus for army ant emigrations and that mass chemical recruitment is the vehicle for colony exodus as well as for booty capture. The army ant trail system is dendritic, a pattern which increases the chances of locating a nesting site that can accommodate the large population of adult workers and brood. But the real possibility remains that failures to emigrate during nomadic days may be due as much to the lack of suitable nesting sites in a particular area as to a temporary reduction in the magnitude of brood excitation, In the field it is impossible to assess the suitability of underground sites as ”

122

HOWARD TOPOFF

potential army ant bivouacs. In the laboratory, however, colonies of N . nigrescens will pass through a complete nomadic phase (with intensive raiding) without a single emigration if no suitable alternative nest is provided. Finally, our studies on food augmentation show that the amount of food captured by an army ant colony plays a key role in influencing the level of overall excitation. By comparing the amount of booty gathered by colonies of N . nigrescerzs during the nomadic and statary phases, we have estimated that up to 77% of the food taken during the nomadic phase is for larval consumption. Thus larval satiation seems to be inversely correlated with larval stimulation of adult individuals. In both our field and laboratory studies, especially when we concentrated on small colonies of Neivamyrmex, overfeeding virtually eliminated nomadic emigrations. To a large extent, the lack of emigrations was caused by a decrease in raiding, which again shows that the two processes are typically closely linked. Even we were impressed by the degree to which overfeeding could increase the time of raid onset, decrease raid duration, and eliminate almost all emigrations. As a comparative psychologist, T. C. Schneirla did not promulgate simple, reductionistic explanations for social organization. The sense in which Schneirla viewed the army ant colony as an adaptive system is illustrated in Fig. 9, where adjustments of the colony to its environment are represented by both individual properties and by interrelationships among subgroups. Although the conceptual schema also emphasizes behavioral interactions within the colony, it does not ignore food and other ecological parameters. Perhaps most significant is that in his final summary of army ant behavior, Schneirla (1971) gives considerable attention to the relationship between nest-changing operations and ecological conditions. Thus, for surface-adapted species of Eciron, Schneirla notes that “successive stages of traffic developing through the raid determine the emigration route and the location of the new bivouac.” And in summing up his findings on the paleoarctic genus Aenictus, Schneirla makes the following acknowledgment of the relationship between food supply and brood stimulation: Members of a larval brood of Aetiicrrts, monomorphic and closely similar physiologically. tend to be disturbed at nearly the same time when food runs low in the bivouac and then begin a mass agitation which spreads readily through the cluster. The workers, also nionomorphic and capable of similar responses under equivalent conditions, rcspond to the wave of brood stimulation with excited larva-grasping responses throughout the cluster $0 that the colony soon launches an exodus with brood. Presumably, with food shortages of lesser degree. less intense comniunicative processes of the same type can initiate a new wave of raiding.

I think these statements show that Schneirla was on the verge of extending his research program along the lines that we have taken. During most of his career, he concentrated on behavioral interactions between brood and adult workers, on

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123

the role of the queen as pacemaker of brood production, and on the relationship between bivouac formation and cyclic colony behavior. By emphasizing the process of recruitment, raid site location, food supplies, and other factors whose primary influence takes place outside of the bivouac, we have extended, not replaced, Schneirla’s concept of army ant social organization.

Acknowledgments This research was supported by Grants BNS77-17366 and BNS80-04565 from the National Science Foundation and by Grant 1349 from the City University of New York.

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Schneirla, T. C. (1949). Army-ant life and behavior under dry-season conditions. Bull. Am. Mus. Nut. Hist. 94, 7-81. Schneirla, T. C. (1957). Theoretical consideration of cyclic processes in Doryline ants. Proc. Am. Phil. SOC. 101, 106-133. Schneirla, T. C. (1958). The behavior and biology of certain nearctic army ant. Last part of the functional season, southeastern Arizona. Insectes SOC. 5 , 215-255. Schneirla, T. C. (1971). “Army Ants: A study in Social Organization.” Freeman, San Francisco. Schneirla, T. C., and Brown, R. Z. (1950). Army-ant life and behavior under dry-season conditions, Vol. 4. Bull. Am. Mus. Nut. Hist. 95, 265-353. Schneirla, T. C., and Reyes, A. Y. (1966). Raiding and related behavior in two surface-adapted species of the Old World doryline ant. Aenictus. Anim. Behav. 14, 132-148. Schneirla, T. C., and Reyes, A. Y. (1969). Emigrations and related behavior in two surface-adapted species of the Old World doryline ant. Aenictus. Anim. Behav. 17, 87-103. Schneirla, T. C., and Rosenblatt, J. S . (1961). Behavioral organization and genesis of the social bond in insects and mammals. Am. J . Orthopsychiatry 31, 223-253. Snelling, R. R. (1981). Systematics of social hymenoptera. In “Social Insects” (H. R. Herrnann, ed.), Vol. 11, pp. 369-453. Academic Press, New York. Szlep, R., and Jacobi, T. (1967). The mechanism of recruitment to mass foraging in colonies of Monomorium venustum Smith, M . subopacum Em., Tapinoma israelis For., and T . simothi Ern. Insectes SOC. 14, 25-40. Teles da Silva, M. (1977). Behavior of the army ant Eciton burchelli Westwood (Hymenoptera: Formicidae) in the Belem region. 1. Nomadic-statary cycles. Anim. Behav. 25, 910-923. Topoff, H., and Mirenda, J. (1978a). Precocial behavior of callow workers of the army ant Neivamyrmex nigrescens: Importance of stimulation by adults during mass recruitment. Anim. Behav. 26, 698-706. Topoff, H., and Mirenda, I. (1978b). In search of the precocial ant. In “The development of behavior: Comparative and evolutionary aspects” ( G . Burghardt and M Bekoff, eds.), pp. 81-100. Garland, New York. Topoff, H., and Mirenda, J. (1980a). Army ants do not eat and run: Relationship between food supply and emigration behavior in Neivamyrmex nigrescens. Anim. Behav. 28, 1040- 1045. Topoff, H., and Mirenda, J . (1980b). Army ants on the move: Relation between food supply and emigration frequency. Science 207, 1099-1 100. Topoff, H., Boshes, M., and Trakimas, W. (1972a). A comparison of trail following between callow and adult workers of the army ant Neivamyrmex nigrescens. Anim. Behail. 20, 361-366. Topoff, H., Lawson, K., and Richards, P. (1972b). The development of trail-following behavior in the tropical army ant genus Eciton. Psyche 79, 357-364. Topoff, H., Mirenda, J., Droual, R., and Hemck, S. (1980a). Behavioural ecology of mass recruitment in the army ant Neivamyrmex nigrescens. Anim. Behav. 28, 779-789. Topoff, H . , Mirenda, J., Droual, R., and Herrick, S. (1980b). Onset of the nomadic phase in the army ant Neivamyrmex nigrescens: Distinguishing between callow and larval excitation by brood stimulation. Insectes Suc. 27, 175-179. Topoff, H., Rothstein, A., h j d a k , S . , and Dahlstrom, T. (1981). Statary behavior in nomadic colonies of army ants: The effects of overfeeding. Psyche 88, 151-161. Torgerson, R. L., and Akre, R. D. (1970). The persistence of army ant chemical trails and their significance in the ecitonine-ecitophile association (Formicidae: Eciton,ini). Melanderia 5 , 1-28. Vosseler, I. (1905). Die Ostafrikanische Treiberameise. Pflanzer 1, 289-302. Watkins, J. F. (1964). Laboratory experiments on the trail following of army ants of the genus Neivamyrmex. J . Kansan Entomol. SOC.37, 22-28.

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Watkins. J . F. (1976). "The Identification and Distribution of New World Army Ants (Dorylinae: Formicidae)." Baylor Univ. Press, Waco, Texas. Structure, Development, and Behavior." Columbia Univ. Wheeler. W. M. ( 1910). "Ants-Their Press, New York. Wilson. E. 0.f 19%). The beginnings of nomadic and group-predatory behavior in the ponerine ants. Evolution 12, 24-3 I . Wilson. E. 0. (1959). Communication by tandem running in the ant Cardiocondvlu. Psyche 66, 29-34. Wilson. E. 0. ( 1962). Chemical communication among workers of the fire ant. Anim. Eehav. 10, 134-164.

Wilson. E. 0 . (1964). The true army ants of the Indo-Australian area. Par. Insects 6, 427-483.

ADVANCES IN THE STUDY OF BEHAVIOR, VOL. 14

Learning and Cognition in the Everyday Life of Human Infants HANUSPAPOUSEK AND MECHTHILD PAPOUSEK DEVELOPMENTAL PSYCHOBIOLOGY

MAX-PLANCK INSTITUTE FOR RESEARCH IN PSYCHIATRY

MUNICH, FEDERAL

REPUBLIC OF GERMANY

I. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 11. Some Fundamental Principles of Cognitive Integration. . . . . . . . . . . . . . . . . . A. The Principle of Behavioral State . . . . . . . . . ..................... B. Principles of Attention and Perceptual Organization . . . . . . . . . . . . . . . C. Principles of Causality and Self-Awareness ...................... 111. The Relevance of Dyadic Interactions: Concluding Remarks . . . . . . . . . . . . . References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

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I. INTRODUCTION In this article, we discuss several topics from the area of infant research which have usually been approached as independent complex phenomena in numerous detailed studies. However, it is not our intention to review the present state of the art in each topic but rather to draw attention to one or more global aspects of these topics, namely, the problem of the support in everyday life contributing to the infant’s learning and cognitive abilities. In this case, the common denominator of topics to be discussed is their involvement in early postpartum interchanges between infants and their social environment. The given problem relates to our original clinical interest, and as it has grown out of confrontations of experimental data and naturalistic observations, it also relates to the lesson from biology that naturalistic observation stimulates formulation of hypotheses just as it validates experimental treatment of them and, by the way, reminds experimenters of major conceptual frames or major needs of better knowledge in human society. In developmental psychology, the significance of naturalistic Observation (and biological knowledge) for theoretical advance is best exemplified in Jean Piaget’s theory of cognitive development. At the same time, the confrontation of this theory with the behavioristic theory of learning, based almost exclusively on laboratory experiments, has demonstrated the value of a dialogue between natu127

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ralistic observers and laboratory experimenters. Not long ago, it would have been unusual to combine learning and cognition in one title. However, scientific advances have set aside incongruities, and students of behavior have acknowledged interactionistic syntheses of both theories just as they have gotten used to seeing social interactions where they used to see mere stimulus-response (S-R) models. The infant’s competence-a major issue of developmental research in the last decade-includes many more principles than that of conditioning to an extent that we have to be exclusive rather than inclusive while introducing them in this article. An aggregate term for all operations allowing the infant to integrate a global experience across sensory modalities, a global concept across many events. and an abstract verbal symbol across many concrete concepts has not yet been commonly accepted. Here we understand learning and cognition to be parts of integrative processes. and we find it convenient that these terms leave sufficient space for all sorts of learning and cognitive operations without prejudice. From observing the infant in his everyday naturalistic environment, we have learned that the development of integrative capacities can hardly be understood unless we pay more attention to the competence of his or her social environment, parents in particular, to support integrative development. In spite of the degree of infant competence and autonomy reported in research, the infant’s early interchanges with environment can lead to successful integration of experience only under very favorable conditions. Such conditions are rare unless the caretaking environment adjusts to the infant’s constraints in some supportive intervention as experimenters d o in order to be able to demonstrate learning in the infant. In contrast to detailed studies of the infant’s learning and cognition, the parent’s supportive competence has long been neglected in laboratory research. The dominating method of investigation was the use of questionnaires based upon the assumption that parents are consciously aware of supportive attitudes or interventions and for that reason able to report them verbally. Recent attention to naturalistic parent-infant interactions and the introduction of microanalytic methods in interactional research have led to a revisionist perspective that is increasingly psychobiological in nature. We now know that infants bring to the world propensities and capacities to orient, attend, process. and regulate information in ways that contribute to the development of integrative competence. We also begin to understand that the way in which parents naturally interact with infants to promote the same goals are determined not only by human culture but also by complex native behaviors. We shall devote particular attention to the earliest months of infancy. The younger the subject. the more evident, perhaps, the biological contribution to his behavior relative to the sociocultural influence. Also, by studying young infants, we increase our chance of identifying potential evolutionary pathways in the development of behavior. In this post-Darwinian century, the greatest challenge

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is to understand the most difficult evolutionary product-the process of human thought. Recent findings in anthropology and paleontology have stimulated a new interpretation of human evolution in which a greater role has been assigned to reproductive capacities and parental care of progeny than to the use of tools (Lovejoy, 1981). The evolution of human uniqueness is related to the process of thought and may have been influenced by the evolution of particular forms of parenting. In spite of its uniqueness, human parenting may still be based on native behaviors common to many other animal species. The above arguments require intensive research on interactional behaviors that may have relevance for the development of thought; moreover, they call for joint efforts in pursuing a comparative approach. For this reason in particular, we dare to present our views and experience despite the preliminary character of some of our arguments. Moreover, the needs of the present society to improve the quality while controlling the quantity of future progeny should also be kept in mind. Before turning to experimental findings derived from this new perspective on infant and parent, we shall first illustrate some typical methodological advances-applied in the infant experiment laboratory and in homelike laboratory settings-which have enriched this perspective. In many contemporary studies of perception and cognition in infants, develop-

FIG. 1 . The experimental arrangement. (A) An infant looks at the stimulus panel; (B) the infant looks away from the panel. Notice that the direction of the infant’s gaze is clearly evident on the TV monitor even in this degraded photographic reproduction. (In the actual experimental situation, the monitor and trial counter are located in the control room.)

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mental investigators observe infant looking. Figure 1 shows one way in which this is accomplished operationally at Bornstein’s laboratory. A baby sits in an infant seat looking at a display panel. A stimulus is projected over the baby’s head onto the panel and a television camera focuses through a hole in the panel at the baby. The video signal of the baby’s face and eyes is projected in real time for the mother to view and is recorded for later scoring purposes. As the baby looks at a stimulus, he or she signals visual interest to the person who is scoring it; if the baby’s gaze wanders from the stimulus, this too is evident to the scorer. Figure I shows such an arrangement with the baby in an observation room (A) and the investigator in an adjacent control room (B). In this study, preference of 3-month-old babies for smiling and neutral expressions of the same face were assessed. As can be seen, the baby’s leftward looking at the smiling face is evident as visual orienting on the T V monitor; the duration can easily be timed. Studies on parent-infant interaction follow a different tactic and involve microanalysis of social interaction. Unobtrusive, continuous audiovisual records replace former pencil-and-paper time sampling and complement direct observation in naturalistic settings. Film, television, and audiotapes-often in sophisticated combinations-permit investigators to reproduce an observation several times for purposes of control or supplementary evaluations, to extend the list of preselected items in additional analyses, and to apply subsequent microanalyses. Figure 2 shows an example of such an improvement. A mother-infant interaction illustrated with a simple photograph on the left (A) was videotaped with equipment combining the picture of this interaction with the digital display of time (in 0.01 sec) and oscillograms of vocalizations on the right (B). Frame-byframe analysis allows a detailed study of movement, sound, and their coordination. Figures in the next sections of this article will illustrate some further examples. In less than 1 decade, the application of objective recording and microanalysis ha\ reached such an extent that it may sound trivial to mention them. Yct in doing so we want to point out one nontrivial consequence. During the decade of microanalysis, we have learned to see new behavior in human parenting of which the parent is not aware. and which for that reason probably had also escaped the attention of observers relying on pencil-and-paper methods, questionnaires, and lists of a priori defined behavioral items. 11.

SOMEFUNDAMENTAL PRINCIPLES OF COGNITIVE INTEGRATION

OF BEHAVIORAL STATE T H PRINCIPLE ~ Even under strictly standardized laboratory conditions, students of infant behavior find a striking intraindividual variability in most items. Two sources of variability belong to typical attributes of infancy. One is the developmental

A.

FIG. 2. Analysis of naturalistic interactions with film and television techniques. (A) The photographic technique provides more details in the picture; (B) the TV technique allows an electronic display of time units (0.01 sec) and sound curves simultaneously with the picture.

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change in the system regulating a given item; this change may be particularly fast, nonlinear, individually different, and incongruent with chronological age. The other concerns the general organization of all such systems in an individual and is evident in changes of the general behavioral state. In contrast to adults, the infant’s behavioral state changes more frequently, for shorter periods of time, and less regularly (Sostek and Anders, 1981; Sterman, 1972; Stem et a l ., 1973; Stratton, 1982). The literature on methods, terminology, and topics in research on infant behavioral state is rich and has been recently reviewed in detail, for instance by Berg and Berg (1979), Prechtl and O’Brien (1982), Sostek and Anders (1981), Thonian and Tynan (1979) and Wolff (1981). The significance of behavioral state for our topic has not yet been studied sufficiently. The interest in infant behavioral state has been stimulated mainly by advances in the study of circadian sleep- wake cycles and by the introduction of neurophysiological recording methods (electroencephalography, electromyography, and electrooculography, for instance) expected to provide some leading variable for state quantification. Such methods are obtrusive in waking infants and for that reason may have inhibited interest in waking state. Furthermore, the primary interest in circadian cycles has probably drawn attention away from the infant’s interactions with the environment. Conversely, observers primarily interested in integrative development have paid attention principally to waking states and have conceptualized behavioral state frequently as state of arousal or consciousness dependent upon environmental stimulation. Thus at present, the lack of conceptual unity and the divergence in primary interests are considered as the main reasons for increasing diversity in terminology (Prechtl and O’Brien, 1982). Prechtl’s analysis of the vector space of behavioral state in newborns (Prechtl, 1974) shows that only four observable criteria--open eyes, regular respiration, gross movements, and vocalization-represent real vectors since their presence or absence reliably distinguishes states from one other. These four criteria are applicable over all five state categories suggested by Prechtl. Other additional criteria including neurophysiological measures, none of which has proved applicable as a leading variable, should be seen as mere state concomitants. Prechtl and O’Brien ( I 982) recommend restricting the concept of state to conditions that are stable over time (in the order of minutes), that concern larger sets of variables, and that show a cyclic organization. This recommendation can facilitate a consolidation in approaches to behavioral state, and it should be considered from this point of view since some consolidation is necessary if the growing mass of data is to produce fruitful theoretical syntheses. The interrelation between behavioral state and integrative processes initially attracted an increase in attention in the hope that both phenomena might be organized under one principal system, as was postulated clearly in the Pavlovian theory of the regulation of excitatory and inhibitory processes in the central

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nervous system. These hopes have been given up. The need for further research on these interrelations, however, remains urgent. As to the organization of waking states, for instance, most attention has been paid to alert waking with signs of infant interest in environmental events. Wolff (1973) considered alert waking as “self-sustaining” insofar as the adaptive sensorimotor action patterns, which can only operate as long as the infant is awake, also maintain the infant in a waking state. One of Wolff’s categories of waking states-“waking activity” with diffuse movements, open but unfocused eyes, and absence of crying or any obvious attention to external stimuli-was analyzed in more detail by Becker and Thoman (1982). They found it was temporally distributed with consistency across individual infants and across two conditions: mother present or absent. The authors suggest that “waking activity” is a sign of immature organization of states which decreases over the early months of life. It is probably subject to intrinsic control. Interestingly, Wolff (1965, 1973) also observed that one can extend the duration of alert waking for 15 min or more beyond the expected time by presenting the infant with “interesting spectacles or nonperemptory environmental events. The caretaker can, therefore, intervene and successfully influence the infant’s behavioral state. Vestibuloproprioceptive stimulation produced by lifting the infant upright is another intervention eliciting visual exploration significantly more than either bodily contact or presentation of high-pitched voice can do (Korner and Thoman, 1970, 1972). Although the question of similar interventions is relevant to both laboratory studies and everyday rearing situations in families, studies devoted to this question and using state criteria representing real state vectors (Prechtl and O’Brien, 1982) are difficult to find. One such team study was started at the Institute for the Care of Mother and Child in Prague in the mid-fifties. The Czech reports on this study have not received much publicity, however, for political reasons. Publication in Western countries gradually became possible only after the termination of the “cold war.” It took a year in the residential unit for longitudinal observations in healthy infants to find a complex arrangement corresponding to infant individual needs yet allowing multiple daily observations on a regular schedule (for a description see PapouSek, 1961a, 1967a). The smooth functioning of this arrangement for more than 20 years is convincing evidence, by itself, of a successful environmental control of behavioral state in infants. One detailed experimental study systematically varied the temporal relations between the cycles of feeding and sleep in a bifactorial design to find convenient schedules for demonstrating the dependence of learning on these varied temporal relations (Koch, 1962, 1968). PapouSek (196 la) first introduced systematic recording of both observable and polygraphic state criteria including all four vector criteria in experiments on infant learning and described mutual interdependence between behavioral state ”

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and the course of conditioning (see Section 11,3 for description of methods). Using extensive material gathered from 1956 to 1965, PapouSek analyzed learning parameters in four categories of waking state in infants up to 6 months of age. He found the highest percentage of 4287 correct instrumental headturns occurred when infants were in a waking state accompanied by vivid, well-coordinated movements and/or vocalization other than fussing or crying. Latencies were also shortest in the waking state. PapouSek stressed the significance of the amount and the pattern of motility as state criteria. Krafchuk et al. (1976, cited in Sameroff and Cavanagh, 1979) later reinforced this conclusion. They found an almost identical dependence of operant headturning on behavioral state in newborns. There was a much higher percentage of responses related to the waking state. with active motility than to quiet alertness. Conversely, the course of learning (PapouSek, 1967b, 1969) and problemsolving (PapouSek and Bernstein, 1969) was also observed to effect the ongoing behavioral state in different ways. These integrative processes elicited changes of two sorts (PapouSek, 1961a, 1967b, 1969): Halfway to the correct solution of a learning task, infants often increased general motility and intertrial responses and/or displayed fussy facial expressions or vocal sounds. During the first 2 months of age, an abrupt change occasionally occurred, and for a fraction of a minute to several minutes, the infant stayed motionless and voiceless; inattentive to environment; with unfocused, staring eyes; slow heart rate; and slow, regular respiration. With increasing stability of correct responses, the infants stabilized their general behavior and their waking level and showed well-coordinated movements. They often exhibited facial expressions or made sounds interpretable as signs of pleasure during the performance of correct responses. If‘ we take changes in motor and emotional behavior as either signs of displeasure during unsuccessful coping with learning tasks or signs of pleasure during successful coping, we can interpret them not only as signals of changes in behavioral state but also as signs of intrinsic motivation for coping with learning tasks. PapouSek and PapouSek (1979a) suggested that infants may be intrinsically

FIG. 3. The mcithcr checks the infant’s state trying gently to open the infant’s mouth.

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FIG.4.The mother checks the infant’s state trying gently to open the infant’s fist.

motivated for maintaining a certain level of informational input and processing just as they are motivated to feed and to fall asleep. They stressed the fundamental role of integrative processes in the organization of adaptive behaviors. From another point of view, similar concomitant changes during infant learning can serve the caretaker as evidence of how the infant processes the information delivered by the caretaker. This brings us to the question of the role of behavioral state in the infant’s everyday social interactions. According to the above laboratory evidence, caretakers could profit by knowledge of infant behavioral state; it could facilitate correct timing of rearing interventions. These would be based on evaluation of state cycles. The correct amount of stimulation would be based on feedback cues from the infant’s emotional behavior. We have been unable to find evidence of conscious monitoring of rearing interventions using such cues either in parental reports or in historical reviews on infant care (Bell and Harper, 1977; Peiper, 1958). However, while observing parental behavior in naturalistic settings, we have noticed interesting regularities. Thus, parents do not attempt to modify the infant’s behavioral state as long as the infant is in a sleep or alert waking state. On the contrary, they tend to intervene if the infant becomes drowsy, fussy, or starts crying. Interestingly, traditions, indirectly related to behavioral state, recommend soothing crying infants or lulling them to sleep. During the infant’s alert waking, parents tend to provide a variety of stimulation to convey of information, mediate environmental experience, or create a learning situation (see also Sections 142 and 3) or play. Deviation from alert waking in the infant causes parents to interrupt stimulation, change the mode of babytalk, and frequently to express verbally uncertainty about the further course of interaction. Parents ask the infant, for instance, whether he is tired, sleepy, hungry, uncomfortable, what he dislikes, etc. Two interesting patterns often accompany their words: Parents either try gently to open the infant’s mouth by pushing his chin downward (Fig. 3) or attempt to open the infant’s fist and to stretch his fingers (Fig. 4). Differences in resistance or in the responses elicited

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(rooting, sucking, gentle or firm grasp), which depend on the muscle tone and consequently vary with behavioral state, seem to be informative, according to the parental sequences which follow or their comments in babytalk. In these sequences. parents influence the infant’s state by soothing or arousing stimulation, as for example. by modulating babytalk (PapouSek and PapouSek, 198Ib), lifting the infant upright (Komer and Thoman, 1970), or laying him down in horizontal position for sleep. Put another way, parents unconsciously try to renew either alert waking or sleep in the infant. The position and gestures of the infant’s hands also vary with behavioral state and provide visual cues eliciting appropriate parental behavior (PapouSek and PapouSek, 1977). We prepared standard drawings of infants in which only two forms of visual cues varied: eyes open or closed, and hand position as in a hungry, an interacting, a passive, or a sleeping infant. These drawings were perceived by adults as changes of state (often without conscious awareness of the proper cues) and therefore could be used for investigating childless people. Kestermann ( 1982) tested several populations with the help of these standard drawings: 7- to 8 year-old girls, women without children, pregnant women, and mothers and fathers of 6-week-old babies. Subjects were asked to respond nonverbally to each stimulus drawing by offering a milk bottle, a pacifer, a toy, by preparing the ”infant” for sleep (by turning off the light), or else to signal with a press of a button their inability to decide. Appropriate responses confirmed the effectiveness of selected cues in all of the populations; the degree and latencies of responses appeared to depend on the amount of previous experience caring for babies. Results of those fathers who were regularly involved in care of a baby did not significantly differ from results of mothers. Thus, there is some evidence in everyday life that parents perceive cues signaling changes in the infant’s behavioral state and tend to favor alert waking or sleep. The fact that these parental tendencies escape conscious awareness, that they are present in women without children, and that they develop already in childhood suggests that innate determinants may have played a role to some extent in their evolution. B.

PRINCIPLES OF ATTENTION A N D PERCEPTUAL ORGANIZATION

The study of behavioral state leads directly to our next topic, viz., processes of attention, perception, thinking, and emotions. Psychophysiological research on attentional processes, orienting, habituation, and perception in individual sensory modalities has brought such a plethora of data on the neural mechanism and functioning that it has become very difficult to delineate global concepts of their cofunctioning in observable behaviors. Yet, such global concepts are valuable, for instance, to psychobiologists looking for behavioral universals, developmental continuities, and adaptive significance.

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Observers of naturalistic situations now frequently comment on the discrepancy between the infant’s everyday perceptual world and laboratory modeling of infant perception (Gibson, 1969). Laboratory stimuli are usually elementary, static, two-dimensional physical compositions, whereas everyday situations for the baby consist of dynamic events experienced holographically, simultaneously in several modalities, as related to self-perception, and interactive if they concern other living beings. This discrepancy alone justifies, first, attempts to verify the significance of laboratory conclusions for everyday life and, second, attempts to subject naturalistic observations to experimental analysis. In order to discriminate familiar from novel, to learn conditional associations or instrumental acts, to link such acts in meaningful sequences, to acquire new skills through imitation, or to construct abstract symbols into communication, the infant obviously has to use a fundamental set of cognitive operations that organize both perceptual input and adaptive behavioral responses. The existence of such mechanisms has been considered from various aspects. Bruner (1957) postulated that perception inherently involves categorization; Hunt (1965) speculated that cognitive functions intrinsically involve motivation; Gibson (1969) stressed the role of these mechanisms in perceptual learning. Based on extensive laboratory investigation, Bornstein (1981) has argued that the infant-while experiencing variety and instability in the material worldperceives structure and organization of various kinds. One kind of perceptual organization, equivalence classification, enables the infant to treat equivalently discriminably different stimuli based on their perceptual similarity; another kind, prototypicality, enables the infant to select particular stimuli from different equivalence classes or sensory domains as salient. Both organizational principles reflect biological structure and function and can be found in a wide variety of animal species; they are employed near the beginning of life and show developmental continuity. These types of perceptual organizations serve several functions: They attract attention and facilitate encoding and storing in memory. They also serve as reference points for perceptual judgement and afford meaning to incoming stimulation. In studies of the early development of color vision, Bomstein showed that 3- and 4-month-old human infants already partition the photic spectrum into equivalence classes of hue (Bornstein et al., 1976), preferentially attend to and habituate faster to prototypical colors than chromatic mixtures, remember prototypical colors better than color mixtures, and use prototypes effectively to anchor qualitative distinctions among hue categories (Bornstein, 1975, 1981). Similar evidence for the value of perceptual organization may be found in studies on pattern perception. Young infants prefer the principal orthogonals, i.e., vertical or horizontal, to obliques (Bornstein, 1978), and they detect very early vertical symmetry in patterns and prefer such patterns to horizontally symmetrical or asymmetrical ones (Bornstein, et al., 1978, 1981; Fisher et al., 1981).

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These studies document how valuable it can be to assess the organism’s cognitive capacities when interpreting the fundamental forms of its experience. In human naturalistic observations, adults in general reveal a strong concern whether and about what infants think. They already ask newborns many questions and answer them by playing the role of the newborn and thus creating the illusion of a dialogue (PapouSek and PapouSek, 1983; Rheingold and Adams, 1980). In doing so. they in fact respond to the infant’s facial expressions, type of vocalization, or visual behavior, and they interpret these behaviors as expressions of thought. Most generally, facial and vocal signs of increasing upset are interpreted as symptoms of difficult comprehension and problem solving, whereas signs of pleasure are interpreted as symptoms of successful solutions in this context. Yet even more astonishing may be the evidence in interactional microanalysis of the extent to which parental stimulation complies with the principles of perceptual organization functioning in the infant. In this part of our article, we provide examples of this in relation to visual and auditory perception. During interactions with younger infants, some parental tendencies facilitate infant visual perception in general. Parents regularly use two different eye-to-eye distances. One, “observational distance,” corresponds to their optimal reading distance of 40 to 50 cm and is used if they watch and treat an infant who is not attending to them. The other, “dialogue distance,” is shorter (22.5 cm average) and is used as soon as the infant shows interest in communicative interchange. In mothers, this distance regulation was found both in primiparas and multiparas on the first postpartum days (Schoetzau and PapouSek, 1977), often opposing the mothers’ belief that newborns cannot yet see anything. The newborn’s visual acuity is relatively poor, 8 min of arc (Lewis and Maurer, 1977) to 66 min of arc (Miranda, 1970) compared to 1 min of arc in adults. Therefore, it may be meaningful to reduce eye-to-eye distance from 45 to 22.5 cm during communicative interchanges with younger infants. Haynes et ul. (1965) suggested a similar short distance of 19 cm for visual stimulation with respect to the newborn’s poor accomodation; however, their finding has been questioned by Salapatek et ul. ( 1976). Their retinoscopic investigation showed that the refractive power of the lens depends on the infant’s behavioral state; this finding might throw a new light upon the parental use of arousing stimuli during communicative interchange. First, between 6 and 12 months of age, the infant’s visual acuity reaches the normal adult level of 1 min of arc (Fantz et a l ., 1962; Teller, 1973). Parents also seek a vertically parallel face-to-face position toward the infant, try to capture his or her gaze, and reward the attainment of eye-to-eye contact with lively greeting responses (PapouSek and PapouSek, 1977, 1981a) in addition to their general tendency to maintain alert waking in the infant with the help of

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FIG.5. The father seeks face-to-face position and tries to stay in the center of the infant’s visuaI field.

arousing stimulation mentioned in Section 11, A (Fig. 5). Vertically parallel facial orientations not only facilitate reading minute facial behaviors, but also represent an interesting parental counterpart to the organization of perception in the infant, as demonstrated by Bornstein et al. (1981). Such a congruence between laboratory models and naturalistic observations confirms that these models are not mere academic constructs and points to the adaptive significance of observed tendencies in human parental behavior. Parental interest in direct eye-to-eye contact and behavioral patterns supporting such contacts represent a unique component in human communication. Its adaptive significance may well be in directing the infant’s attention to the parent’s face as a prototype of many later interactional behaviors in a broader social environment and as a rich source of stimulation facilitating and nourishing the fundamental integrative processes near the beginning of postpartum life. Early experience in observing facial and visual behavior might also be relevant to later capacities to read feedback information of the thoughts and intentions of social partners-additional capacities of adaptive significance. Near the beginning of life, these capacities are mainly utilized by the parent, for instance, in response to visual behavior in the infant. The parent tends to carry out repetitive stimulation and to convey information while the infant keeps looking at him and tends to vary stimulation if the infant’s gaze wanders away. Conversely, the infant has an early chance to manipulate effectively the amount and quality of incoming parental stimulation with the help of visual behavior (PapouSek and PapouSek, 1979a). Such patterns of nonverbal communication seem to serve specific needs during early months of life but may still underlie later patterns and individual profiles of

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nonverbal communication reported by Montagner (198 1). However, the lack of evidence in both human and animal research allows conclusions neither on the detailed development of these capacities nor on their uniqueness in human development. The vocal interchange is so closely tied with observable facial behavior that it is difficult to treat visual and auditory modalities of parent-infant interaction separately. In fact, much of what has been said of the visual aspects is also true of the auditory ones. One major difference, unfortunately, is the different amounts of experimental evidence on perceptual organization. The principles of equivalence classification and prototypicality have not yet been sufficiently analyzed in the auditory modality, although categorical perception has been demonstrated in relation to speech phonemes (Aslin and Pisoni, 1980; Liberman et al., 1967) and shown to function near the beginning of life (Eimas, 1975). Interestingly, the close ties between visual and auditory perception were demonstrated by Kuhl and Meltzoff (1982) in the capacity of 18- to 20-week-old infants to detect correspondence between speech sounds and visual display of faces of talking persons. This phenomenon, analogous to lip reading in adults, confirms equivalence detection across two, biologically interrelated modalities of crucial importance for the evolution of language. According to the initial evidence, some spectral component rather than the temporal parameter is necessary for such equivalence detection. The authors suggest that both the detection of auditory-visual correspondence and vocal imitation, also observed in their experiments, have a common origin in the intermodal representation of speech, learned or inherent, and that, seen clinically, the bimodal delivery of speech by parents may facilitate language learning because infants are predisposed to represent speech this way. At least in one further feature of vocal sounds, i.e., in the rise time that is responsible for differences in products of both music and speech, categoric perception has been reported in adults (Cutting and Rosner, 1974) as well as in 2month-old infants (Jusczyk et al., 1977). However, already during the presyllabic phase of infancy many more features come into consideration. Starting with the fundamental vowel-like voicing, infants gradually improve the control of respiration and phonation and learn modulations of intensity, rhythm, melody, and timbre, which are necessary prerequisites for later production of speech and song (PapouSek and PapouSek, 1981b). As precursors of later speech prosody and also vocal musicality, the variations in these features may function as universal envelopes for relevant messages, understood across linguistic barriers between cultures or between adults and infants. Thus, for instance, the categorical signs of statements, invitations to dialogue, questions, warnings, or threats may be identified in prosodic envelopes of messages prior to speech development, ontogenetically and perhaps phylogenetically.

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In this respect, it seems to be adaptive that, during the presyllabic phase in which the infant practices the prosodic musicality very much like during the first task in the script for the acquisition of language, the parent provides the necessary counterpart in the form of baby talk. Baby talk, as such, i s categorically different from other forms of speech used in adult-to-adult dialogues in its higher average pitch (Ferguson, 1964), slower speed, and prolongated pauses between abbreviated, simplified, and repetitive segments (Garnica, 1977; Phillips, 1973; Snow, 1977). Before the first syllables appear in infant vocalization, parents strikingly exaggerate prosodic envelopes as if giving lessons on the nonverbal signs of the most important categories of messages. For instance, already in the first interchanges with the newborn, parents present frequent questions and answers, call or sooth the infant, and reject his fussy sounds, thus displaying striking prosodic contours typical for given interactional contexts (PapouSek and PapouSek, 1981b). Two typical examples of utterance classes and their prototypical denominators are given in Figs. 6 and 7. Figure 6 shows melodic contours effectively used by the mother to elicit infant vocalization. Within 3 min, the mother produced 37 utterances consisting of one to seven syllables, including 11 different semantic contents and yet representing almost equal amounts of information in melodic contours that, analyzed by computer as contours of the fundamental frequency, are shown in a cumulative graph (Fig. 6). Figure 7 includes the sonagram of a soothing melodic contour addressed to a 2-month-old fussy infant and a graph documenting repetitive presentation of sounds having this contour in various lexical contents in real time. Between 1 and 2 months of age, infants are able to discriminate melodic contours (Morse, 1972) and acoustic correlates of stress location (Spring and Dale, 1977); however, there is no laboratory evidence as yet that infants categorically perceive similar features and detect prototypes in them, Nevertheless,

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an early increase of interest in the rich material obtainable in everyday parent-infant interactions can safely be predicted, probably reaching a conclusion in line with that from studies of visual perception. i.e., that the infant's attention to and perceptual processing of meaningful environmental stimulation can be favorably influenced by parental engagement.

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C. PRINCIPLES OF CAUSALITY AND SELF-AWARENESS

Both the blind and the deaf can survive and share experience with the unimpaired, but experience cannot be shared with the loss of somatosensory perception. Probably for this reason the cultural heritage related to this sensory modality is relatively poor. Humans spend substantial amounts of time and energy learning new motor skills and compete for virtuosity, and yet the paucity of words in the everyday lexicon for the description of what they feel and organize internally is striking. The biological significance of somatosensory perception is evident in its early postconceptional functioning. Already the classical investigations of Hooker and Humphrey (reviewed by Humphrey, 1969) demonstrated the first exteroceptive reflexes in the trigeminal region before 9 weeks of gestational age and the first proprioceptive reflexes, the gastrocnemius stretch reflex, at 13 weeks. Those investigations were made in aborted fetuses in a terminal condition, whereas today, real-time ultrasound methods allow observations of fetuses in everyday naturalistic settings, i.e., of fetuses spontaneously moving under normal intrauterine conditions. The first results have already dramatically changed our knowledge, De Vries et al. (1982) observed the first spontaneous movements at 7.5 weeks of postmenstrual age, and by the age of 15 weeks, they recorded 16 movement patterns closely resembling those observed in newborn infants and 2 additional patterns causing either somersaults or rotations around the longitudinal axis. These findings substantially correct former impressions that early fetal behavior consists merely of reflexes rather than of spontaneously generated movement patterns. However, it remains unknown how the complex behaviors are perceived by fetuses. A reciprocal effect of excitation and inhibition can be observed prenatally from 18 weeks (Bergstrom and Bergstrom, 1963). Before 25 weeks, the primary somatosensory area in the brain cortex matures, followed by the visual and auditory areas, as measured by the development of cortical evoked responses (Hrbek et al., 1968; Weitzman and Graziani, 1968). By term, cortical areas are still relatively immature; however, the peripheral structures, from receptor cells up to the brainstem, are well differentiated and all leading subsystems are myelinated-somatosensory , haptic, visual, and auditory-and can initiate motor responses if stimulated (Berg and Berg, 1979; Carmichael, 1970; Hecox, 1975; Horsten and Winkelman, 1962). Thus by term, at the latest, but probably much earlier, new sensory avenues are open for the development of additional principles of perceptual organization and learning-the principles of cross-modal and serial processing of input from somatosensory organs, on the one hand, and exteroceptive organs, on the other, and the principles of causality and selfawareness.

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The categorization of information according to these principles is adaptively relevant not only for the exploration of one’s environment but above all for the differentiation between the self and “other.” In the one direction, the first steps can be taken toward the integration of causality concepts and in the other toward the concept of self. To better understand such steps, let us consider five logical examples of perceptual input and their interpretative meaning (in brackets): (1) no somatosensory sensation of movement in upper extremity with a sensation of tactile stimulation in it (“something from out there touched me”); (2) somatosensory sensation of movement in that extremity followed by tactile sensation of movement in fingers ( “ I moved hand and touched something out there”); (3) somatosensory sensation of movement in that extremity followed by simultaneous tactile sensations in fingers and nose (“while moving I touched myself’’); (4) no somatosensory sensation of movement with auditory sensation from environment (“something out there made noise”); (5) somatosensory sensation of movements followed by auditory sensation from environment ( “ I may have caused that noisc out there”). No matter how simple such playful consideration may seem, its experimental exploitation still has to wait for innovative methods. The last example under ( 3 , involving the principle of causality, deserves attention because, without much concern about perceptual organization, it has already been studied abundantly in studies on infant operant and instrumental learning. Here, however, we want to stress that all the above examples-in a very fundamental and universal waypotentially contribute to the development of awareness of causality and self. We cannot say how far an infant really is aware of them, but it might be even more important to know whether the given combinations of perceptual input have some intrinsic potency for activating integrative processes participating in input and processing of information. Estes (1981), for instance, sees motives as organized components of the cognitive system and stresses that having available in one’s repertoire various cognitive operations is not enought if motives cannot activate them in problem situations. We can again consider several categories of perceptual combinations that, in terms of adaption. might be crucial in activation of integrative operations: I . A stimulus but no other relevant change is perceived; the integrative system first responds with an increase in attention which then habituates again. 2 . A stimulus is perceived as followed with some relevant event; the integrative system responds with an increase in attention necessary to find out the further probability of this combination and may organize a learned response as in associative conditioning. 3 . Some relevant event is perceived as preceded by an act organized in the integrative system; the integrative system responds with increased attention, initiates repetition of the acts in question, and tests under which conditions some

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act can lead to that relevant event again as in instrumental conditioning, for instance. The complexity in each of the above categories can differ, requiring different operations such as cross-modal processing, detection of rules and construction of working hypotheses. The integrative process will, in no case, depend merely on the qualities of external stimulation, but will depend also on the organism’s state, phylogenetic or ontogenetic experience, and other ongoing activities. We can easily establish models for all three categories: only the kind of stimulation and/or response would be varied as in the designs of habituation experiments and associative or instrumental conditioning. Even then, these categories would in different degrees contribute to concepts of causality and self or would acquire the attribute of intentional acts. Similar organismic positions have been taken in interpretations of infant learning and cognition by recent reviewers (Lipsitt, 1982; Sameroff and Cavanagh, 1979), although not many of the studies reviewed had been designed from organismic perspectives. While the number of studies on infant learning has obviously decreased, the academic interest in the development of intentionality, self-awareness, or awareness of causality has increased, being nourished from new directions-psycholinguistics, in particular. Although speculative in character, the attempt to conceptualize the ontogenesis of speech acts (Bruner, 1975; Dore, 1975) cannot avoid infant autonomy and intentionality, the elements of which are seen in the core of instrumental acts as such. One of the few attempts to elaborate an experimental model of “voluntary acts” in infants was a part PapouSek’s studies on integration of head turns mentioned already in the section on behavioral state (Section 11,A; PapouSek, 1961a,b,c). Head turning as a motor act already functioning well in newborns can serve either as a response orienting telereceptors toward a novel stimulus, as an avoiding response, or as an instrumental act for obtaining a reinforcement. Head turning can easily be applied in all main types of conditioning as well as in habituation and preference studies (where, in fact, it has been used under the term visual behavior). In this model of voluntary acts, free-choice instrumental learning was combined with conditioning signals as in Konorski’s type of conditioning. PapouSek first investigated 4-month-old infants and later (PapouSek, 1967b) newborn infants as well. The sound of a metronome located at the midline for 10 sec 10 times per session with random intertrial intervals signaled a chance to obtain a portion of milk with a head turn to either side. Head turns were reinforced with sweetened milk from one side and with unsweetened milk from the other. When the infant turned five times consecutively to the same side, differential reinforcement was reversed to the other side. The capacity to learn an instrumental act, show a preference, and relocate the side of preferred reinforce-

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ment when reversed by the experimenter was considered as a sufficient representation of preverbal voluntary acts. In older infants, the two-part demonstration took I08 trials on the average, whereas in newborns it required 3.6 times this number of trials. The rationale for the decision to combine instrumental learning with conditioning signals and thus to limit the validity of the instrumental paradigm to the periods of time signaled with CS is to be seen in the intention to simulate everyday situations where instrumental acts usually are effective only within certain conditions (PapouSek, 1961a,b, 1967b). Comparing the experiments with instrumental head turning with preceding experiments using classical, associative conditioning of sucking responses, Pdpouiek (1961a) pointed out several substantial advantages of the head-turning method. It clearly had adaptive significance as a purposeful act with which the subject could obtain something relevant. One of the advantages was the possibility of demonstrating learning in newborns. In addition, PapouSek stressed a participation striking in a way of affective behaviors in instrumental, but not in associative, learning. infants became fussy during the initial difficulties in learning, but with the increased occurrence of well-coordinated behaviors, they exhibited smiles, and cooing as they approached the criterion of successful learning (PapouSek, 1961a,c, 1967a,b). The presence of behavior usually categorized as social, in nonsocial laboratory situations, raised the question of whether social behavior of this sort is not elicited as an outcome of integrative operations in both cases ( PapouSek and PapouSek, 1979a). A similar problem was viewed from another perspective by Watson (1972). He provided 8-week-old infants in family settings with a means of controlling the movement of a mobile over their cribs and was told by mothers of exuberant smiling and cooing occurring in infants after a few days of exposure. Watson proposed that the perception of the contingent relation between the infant’s responding and subsequently receiving stimulation is possibly the major initial influence in guiding the human infant to classify fellow members of the species as “social objects.” In fact, Watson (1967, 1972, 1979) and Watson and Ramey ( 1972), while analyzing different S-R aspects of contingency awareness, did not analyze social interactions but “social behaviors” related to the detection of contingency. It is arbitrary either to assume that social behaviors may be elicited with nonsocial stimuli (as in Watson’s interpretation) or to assume that integrative processes primarily are intrinsically connected with affective behavior (as suggested by PapouSek and PapouSek, 1979a) or hedonic equivalents and secondarily become tied to social interactions due to the high frequency of integrative operations that are elicited in social interactions. Perhaps for this very reason, social interactions have been favored during human evolution. The main point in relation to the processing of somatosensory input is the evidence in both PapouSek’s and Watson’s studies that important integrative

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operations involving affective and motivational regulations may be assumed in infant responses and that they may be crucial for the interpretation of early social communication, intentionality, and self-awareness, although they still require more attention in developmental neuroscience and in comparative approaches as well. One experimental approach to the role of integrative operations in the coordination of movements was exemplified in head turning designs (PapouSek, 1969; PapouSek and Bernstein, 1969) in which 4-month-old infants could control a visual stimulus (random blinking of color bulbs), applied in the midline, by certain patterns of head movements. Infants had to detect the rules of patterning without any instructions. They were able to detect and adaptively apply the following rules (PapouSek, 1969): (1) two head turns to the given side carried out consecutively and through at least 30”; (2) three such consecutive head turns; ( 3 ) regularly alternating turns to the left and to the right; (4) regularly alternating double head turns to the left and to the right. Thus, at the age of 4 months, the infants were also able to cope with simple numeric concepts, however, they were unable to cope with asymmetrical rules such as “two turns to one side or three turns to the other.” As noticed in that study, such a task was very difficult even to adults tested incidently. Inasmuch as head turns were recorded polygraphically, infant subjects provided clearly readible transcripts of the course of integration, for instance, in the gradual organization of dyads or triads, otherwise never observed in preexperimental records. Visual perception and discrimination of small numbers in infants of similar age were confirmed by Starkey and Cooper (1980). Recently, probably in connection with new techniques, the interest in intrinsic patterning within spontaneous motility has increased, beginning with intrauterine observation of fetuses with the help of real-time ultrasound recording (de Vries et al., 1982; Nijhuis el al., 1982) or with the rhythmic patterning in waking newborns (Robertson, 1982) and infants (Ashton, 1976; Thelen, 1979, 1981). They allow a better insight into the participation of different central programs during ontogeny and phylogeny, and they reveal a very early existence of complex spontaneous patterns where formerly only “primitive reflexes” or mere ‘‘random movements” used to be observed. In everyday situations, infant behaviors, no matter how random, elicit a strong interest. A living human caretaker is a prototype par excellence of an attentive, stimulating, and above all, responsive counterpart, offering plenty of interchanges that represent, at least hypothetically, support for the development awareness of causality and self-awareness. Parents may consciously use rewards and punishments for behavior modification under the influence of behavioristic recommendations. Here, however, we are more interested in tendencies that perhaps escape conscious parental awareness, but which may be closer to univer-

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sal behavior both across cultures and evolutionary periods. In order to outline a more complex picture of our approach, we give examples from ongoing, unpublished observations. In Fig. 8 we show such an example of a very common and regularly elicitable parental response accompanying the establishment of visual contact with the infant, the “greeting response.” Both pictures represent a laboratory situation in which one of the parents is asked to communicate with the infant via a mirror. Therefore, both engaged faces can be shown en face in one picture. Such greeting responses-a slight retroflexion of head, raised eyebrows, widely open eyes, and slightly open mouth-which, in less expressive forms, sporadically accompany baby talk, become more frequent with increasing probability of an eye-toeye contact and peak in frequency and intensity when the infant looks at the parent (PapouSek and PapouSek, 1977). At this moment, parents can hardly resist carrying out a greeting response if asked by the observer not to respond. Differentiated changes in baby talk based on prior infant vocalization, as shown in Figs. 6 and 7, can serve as another example of parental contingencies. As long as the infant’s vocal sounds arc quiet and pleasant, the parent tends to use quiet, tonal prosodic envelopes with terminal pitch rise and to pause for turntaking (Fig. 6). Conversely, the parent responds to fussy sounds and crying with stressed words of rejection and with a slowly falling pitch in soothing contours giving the infant no turns (Fig. 7) (PapouSek and PapouSek, 1981b). The above two examples represent relatively universal patterns of parental behavior which function already in the first postpartum interactions and with the firstborn child, both in mothers and in fathers, according to our observations. Next to such patterns, many other patterns that are more variable and are typical only of individual parents in certain interactional contexts easily become contingent and repetitive components of interactional sequences, at least with a temporary consistency. Altogether, parents tend to use simple repetitive patterns as if they were preprogrammed to use behaviors that the infant’s integrative system can process easily, classify, conceptualize, predict, and control according to the infant’s needs. In this sense, the infant has a counterpart also supporting the integration of causality awareness. It is a trivial experience that infants soon become capable of manipulating their parents. They know how to attract their attention, how to ask for food, lifting or rocking, etc. (see also Fig. 12). Many regularities and contingencies in parental behavior can be found only with the help of microanalysis because of their rapid occurrence. Seeing how many of them can occur within 1 min of interaction, one realizes the advantage of their being independent of conscious rational decisions. If they were not so, they would quickly wear down the parent. The delivery of numerous contingencies during everyday parent-infant interactions points to parental didactic capacities and their evolution (PapouSek and PapouSek, 1978, 1983). It seems probable that the principle of causality has not only been utiiized

FIG.8. Parental “greeting behavior” as a response to the achievement of eye-to-eye contact. All persons are sitting in front of a mirror. In (A) the father tries to captivate the infant’s sight via mirror. In (B) the father responds to the achievement of eye-to-eye contact.

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for learning studies in infancy research or for production of educational toys, but also favored in the evolution of parental support of the integrative development of progeny. Detecting causality and striving to verify its validity already represent a perspective-taking ability: in other words, a way toward integration of expectancies, goals, intentionality, and self-awareness (Bruner, 1974; Piaget, 1952). lnfancy research considers corresponding principles of integration more and more seriously and points to precursors of later concepts in younger and younger infants. Furthemiore, integrative capacities have become objects of investigation; for instance, those which are involved in imitation and self-recognition. The more groping and uncertain the first steps in this direction are necessarily, the more helpful reference to naturalistic observation may be. Let us. for instance, consider two of many observations of infants in mirror situations. Perceptual processing of contingency in the mirror image has been interpreted as a significant precursor of self-awareness. In one study (PapouSek and PapouSek, 1974). a combination of television playbacks and live images of

FIG. 9. The infant’s “biological mirror”: yawning. Both partners arc sitting in front of a mirror.

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self allowed us to separate three individual features of the mirror image: eye-toeye contact, contingency, and similarity. With this method, 5-month-old infants were found to respond first to eye-to-eye contact and only later, but increasingly, to contingency. In the other study (Field, 1979), 3-month-old infants from a twin population looked either at their mirror image or at co-twins and showed more gazing at the mirror image of self, but showed more smiling, vocalizing, and reaching toward co-twins. The contingency in mirror images of self is categorically different from contingencies in dyadic social interactions. The partner in everyday interactions always performs contingent behaviors with a delay, equal to the latency of his responding, whereas the mirror image of self “responds” with no such delay. Such a categorical difference may require differential processing of perceptual information and should be taken into account in interpretations of self-recognition. Interestingly, Nature provides the infant with a “biological mirror’’ as well as with a “biological echo” which may be easier to process, and which may have functioned prior to the invention of mirrors. They can be seen in the parental tendency to imitate infant behaviors, particularly those that are relevant to social communication. Parental imitation or matching usually appears in the first interactions with the newborn and, in our observations, always prior to the infant’s matching. Matching mostly concerns facial expressions and quiet vocal sounds (PapouSek and PapouSek, 1977, 1981b). Typical examples of both parents matching the infant’s facial expressions are shown in Figs. 9 and 10. In everyday interactions between mothers and 2-month-old infants, vocal matching occurred with average frequencies of 2.8/min when initiated by the mother and 2.4/min when initiated by the infant (PapouSek and PapouSek, 1982). Mothers mostly matched in pitch (84.5%) and less in phonetic structures (4.8%). Similarily, infants’ matching mostly concerned pitch (88.1%) and only seldom concerned phonetic structure (1.7%). Infant matching of pitch was reported to occur in onehit trials rather than as result of gradual tuning; it allowed the infant to hit the same tone or the same tone in a higher octave. Kessen et al. (1979) observed vocal imitation in 3- and 6-month-old infants and attempted in vain to influence it with lessons provided by mothers at home. Kuhl and Meltzoff (1982) observed imitation incidently during studies mentioned earlier in this article. The fact that parents imitate the infant in the same behavior in which imitation has been reported in infants and that they are first to imitate, causes problems in the interpretation of the infant’s capacity to imitate. The reports on vocal imitation seem to confirm the assumption of an innate central program in the infant as well as to prove that there are supportive environmental factors. Imitation of facial expressions and gestures has thus far been studied mainly in infants (Field et al., 1982; Gardner and Gardner, 1970; Jacobson, 1979; Maratos, 1973; Meltzoff, 1981; Meltzoff and Borton, 1979; Meltzoff and Moore, 1976), howev-

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F I G . 10. The infant's "biological mirror": pleasure and distress. Notice that in both A and 0 even the fathcr in the background matches his facial expression to that of the infant.

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er, the present position of research seems to be comparable with the position in vocal imitation. Further progress may lead to additional evidence that not only programs for learning, but also for teaching, have been selected during human evolution so as to function together harmoniously. In laboratory research, experimenters usually try to isolate phenomena in order to analyze their functioning with the help of techniques allowing exact measurements. This used to be difficult in observations of interactions. However, the present equipment for audiovisual recording has made it possible to combine unobtrusive recording with additional special analyses and in this way to overcome former difficulties. Social interactions are complex and can only be understood if the role of individual phenomena in the interactional context is known as well. Conversely, audiovisual recording often documents unexpected sequences clearly revealing phenomena otherwise difficult to demonstrate in the laboratory. Anecdotal but well-documented evidence, too, may help to direct further laboratory research. Let us demonstrate it with a few examples. The series of pictures in Fig. 11 shows incidental evidence of self-awareness and self-recognition, problems occupying experimenters for a long time. Provocative comparative data on self-recognition and its role in the emergence of mind in primates (Gallup, 1970, 1980, 1982) have nourished interest in human early ontogeny of self-awareness in particular (for review see Lewis and BrooksGunn, 1979). Figure 11 shows a 13-month-old girl interested in her mother’s necklace. Allowed to wear it for the first time, the baby crawls to a mirror on her own initiative to watch herself. Figure 12 is an example of a concise seriogram including substantial information based on photographic and sonagraphic analyses. It can be used as an economical substitute for an audiovisual record, in this case, of a playful interaction between a 6-month-old infant and his mother. The mother played a game in which her fingers “walked” through the air above the infant until they approached his shoulders and then suddenly turned to his armpits and tickled him there as the point of the game. This seriogram shows the infant asking for another repetition of this game, then the attentive state of expectation with cooperative stretching of arms, and finally an anticipatory laughter prior to the real point of game. The vocal appeal and the burst of laughter are shown sonagraphically on the right. The last example is taken from our ongoing observation on the preverbal use of phonetic and/or gestural signs as prototypical representations of general categories. In everyday interactions, parents tend to use the infant’s first repetitive syllables already as potential prototypical representations (Papouiek and Papouiek, 1981b). For instance, dogs and birds can be perceived by infants in different modalities and so frequently that signs for the dog or bird are particularly broad and omnipresent categories in the infant’s world in many cultures. Under the influence of parental mediation of experience with dogs and birds,

FIG 1 1 , Self-recognition in a 13-month-old infant. ( A ) The infant shows interest in the mother's necklace: ( B ) the mother allows the infant to wear the necklace; (C) on her own initiative. the infant crawls to a miror to watch herself.

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FIG. 12. A concise seriogram substituting for an audiovisual record of a playful interaction. (A) The infant asks for another repetition of a game in which the mother walks with fingers through the air above the infant until she approaches the armpits and surprises the infant with tickling. (B) shows the infant’s attentive state of expectation. In (C) picture, the infant’s anticipatory laughter precedes the actual point of the game. The vocal appeal and the burst of laughter of the infant are shown in sonagrams to the right of the pictures.

some particular signs become rather general too, for instance, the vocal imitations of barking or bird song or protowords “WOW” or “pee,” and arm movements symbolizing the use of wings as shown in Fig. 13. Both dogs and birds are richly represented in toys, drawings, decorations of baby rooms, etc. Infants often hear dogs and birds even if they cannot see them. The bird exceeds the dog in musicality, of course. If infants are shown novel objects, drawings, or sounds representing a bird and

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FIG. 13. An example of a preverbal sign and its boundaries: the bird. The syllable “pee” or the gesture of wing movements as shown in this figure are two very common signs for the bird. Several drawings in which the infant identified the bird show how broad the boundaries of this sign can be if the category of the bird is represented in the infant’s world richly enough.

recognize them, they usually respond with identifying signs on their own initiative, for instance, with the syllable “pee” or with the gesture of wing movement. Figure 13 shows such a gesture (A) and several pictures (B-E) illustrating the variety of drawings in which a preverbal 9-month-old girl identified birds, sometimes in very difficult artistic representations. 111. THERELEVANCEOF DYADICINTERACTIONS: CONCLUDING

REMARKS

The revival of naturalistic observations in science, in developmental approaches in particular, has inevitably led to the study of social interactions. The parent-infant interaction represents a specific interacting system in which the

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two partners critically differ in amount of knowledge and social awareness and thus constitute a didactic system (PapouSek and PapouSek, 1978, 1983). Didactic activities used to be considered as typical sociocultural phenomena and consciously performed interventions. Consequently, attempts to view them as biological phenomena have been rare (Liedtke, 1976), and little is known about precursors of human didactic behaviors in animal parenting. A better understanding of human parenting has revealed a primary model of didactics in nonconscious parental behaviors functioning as a perfect counterpart to the postpartum development of competence in learning and cognition in the infant. The contributions to better understanding have come from both experimental rcsearch and naturalistic observation. In most respects, these contributions have opened new ways and pointed to new problems rather than offered conclusions. However. the examples selected in this article reinforce the impression that on the one hand. the human infant is intrinsically motivated to learn and acquire knowledge, while on the other, the parent is intrinsically motivated to share knowledge with his progeny and to convey information to the infant in accordance with the developmental and momentary states of infant integrative ability (PapouSek and PapouSek, 1983). Like many products of Nature, the primary didactic capacities may be beautiful in their perfection, but also may be variable and fragile in individual cases. Above all, however, they are not yet fully understood. For instance, it is not yet known to what degree their variability influences infant integrative development. Ruddy and Bornstein ( 1982) investigated the predictability of cognitive differences at 12 months from infant and maternal behaviors at 4 months, and they showed that to a certain degree. cognitive differences are predictable and positively influenced by maternal stimulation at 4 months, specifically, by the encouraging of infant’s attention to objects. Realizing the delicate microstructure of parent-infant interaction, we can predict that its best functioning requires the dyadic form of interchanges, i.e., interchanges in which only one parent and one infant are engaged at one time. This prediction was confirmed by Bornstein and Ruddy (1983) in a comparison between singletons and twins. At 4 months, there were no differences in measures on information processing-rate and amount of habituation, and recognition memory-but mothers of twins encouraged attention to environmental objects, properties, and events less than half as often per child as mothers of singletons. At 12 months, twins used less than one-half as many words as singletons and performed worse on many items of the Bayley Scales of Infant Development. Thus, two signposts for further research become evident. One points to a comprehensive understanding of controls over early cognitive and linguistic deveiopment in children (Bornstein and Ruddy, 1983). The other aims at the clinical significance of interactional failures (PapouSek and PapouSek, 1979b).

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Both directions are parallel inasmuch as they view the infant in unity with the parent and consider the contribution of both principal sources of variance in early infancy-one that is biogenetic and the other that is experiential. This view necessitates a well-balanced distribution of attention to both laboratory and naturalistic observation.

Acknowledgments The following foundations have kindly supported our research: Die Deutsche Forschungsgemeinschaft and Die Stiftung Volkswagenwerk.

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ADVANCES IN THE STUDY OF BEHAVIOR. VOL. 14

Ethology and Ecology of Sleep in Monkeys and Apes JAMES R. ANDERSON DEPARTMENT OF PSYCHOLOGY UNIVERSITY OF STIRLING STIRLING, SCOTLAND

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Introduction . . . . . . . . . . . . . . , . . , . . . . . . .

. . .. . . . . .. . . . . . . ... .... ... . . . . . . . . . . . . A. How Many Sites? . .. . . . . . . . . . . . . . B. The Location of Sleeping Sites . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Sleeping Sites as a Limiting Resource . . . . . . . . . . . . . . . . . . . . . A. Distribution and Group Size . . . . . . . . . . . . .. . . . . . . . B. Ranging Patterns.. . . . . . . . . . . . . . . . . . . . . . . . . . . , . . . . . . . . . . . . . . . Sharing and Competition for Sleeping Sites. . . . . . . . . . . . . . . . . . . . . . . . . . . Characteristics of Sleeping Sites . . . . . . . . . . . . . . . . . . . . . -. . . . . . . . . . . . .. ... . . . . .. .. . . . A. Safety from Predators.. . . . . . . . . . , . . . . . . B. Comfort.. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . C. Sleeping Sites as Information Centers.. . . . . . . . . . , . , . . . . . . . . . . . . . Trdditional Sleeping Sites and Security . . . . . . . . . . . . . . . . . . . . . . . . . . . , . . A. Monkeys .......................... . .. ..... .... . s . ... .. .. .... B. Learning and Tradition in Nesting Habits C. Advantages of Highly Familiar Sites.. . . . . . . . . . . . . . . . . . . . . . . . , . . Amval. Sleeping Postures, and Nighttime Activity . . . . , . . . . . , . . . . . , , . . . ........ .... A. Arrival ..................... B. Postures.. . . . . . . . . . , , . , . . . . . . . . . . . . . . . . . . . . . , , . . . . . . . . . . . . . C. Nocturnal Activity.. . . . . . _ .. . . . . . . . . ... . . . . . _ . . . . . . . . . . . . . . . Social Aspects of Sleeping . . . . . , . . . . . . , . . . . , . . . . . . . . . . . . . . . .. .... .. .... A. The Group.. . . . . . . . . . . . . . . . . . . B. Subgrouping . . . . . . . . . . . . . , . . . . . .. . . . . . . . . . . . . . . . . .. .. ...... . . . C. Effects of Dominance.. . . . . . . . . . ................... D. Huddles and H e a t . . . . . . . . . . . . . . Awakening and Leaving the Sleeping Site.. . . . . . . . . . . . . . . . . . , . . . . . . . . A. Early Calling.. . . . . . . . . . . . , , . . . . . . . . .. . . . . . . . . _ . . . . . . . . . . . . B. Elimination . . . , . . . . . . . . . , . . . , . . . . . . . . . , . . . , . . . . . . . . . . . . C. Weather, Warming Up, and Departure . . . . . . . . . . . . . . . . . . . . . . D. Activity Budgets.. . . . . . , , . . , . . . . . . . . . . . . . . . . . . , . . . . . . . . . . . . . E. Social Aspects of Leaving . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Concluding Comments. . . . . , . . . . . . , . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . _ .. . . . . . . . . . . . . . . . . . _ _

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Field studies of primates commonly gather some information about the sleeping habits of the species under investigation. In reports, reference might be made to the numhcr of sleeping sites used, the presence or absence of preferred areas for slccpiny. and the time of day at which the subjects became alert and/or retired. It is less conimon for direct relationships between sleeping habits and aspect5 of the subjects' ecological circumstances to be expounded, e.g., effects of the availability of food, weather conditions. or competitors. Often the data on onc or morc o f the relevant variables are insufficient. Among the reasons for the ovcrall paucity of knowledge about ecological details of sleeping patterns are logistical problems in locating and monitoring nightly sleeping sites, poor visibility i n the dark. and an understandable bias toward studying daytime behavior since this is when most subsistcnce and social activities occur (Anderson and hlcGrcw. 1982). Whatever the function\ o f sleep (and there may be several, Meddis. 1982; Webb. 1970). it is t o be expected that organisms adjust their sleeping habits, within limits. to environmental conditions. Primates as a group show an impressive flexibility in their sleeping habits. complementing their successful radiation into disparate ecological niches. The present article comprehensively reviews the avaiiahle information on sleep in wild monkeys and apes: where they sleep, why certain locations might seem favorable or not, with whom the primates sleep, and what they do during the night and early morning. It will be seen that the securing of suitable sleeping sites can be a significant factor in the distribution and behavior o f primates and that sleeping habits themselves are modified within ovt.rall adaptive patterns of activity. The review is intended to help socioecologists formulate questions about sleeping habits and to help sleep researchers such as Meddis (1982) whose thcoretical progress has been slowed because "we have very little data concerning the sleep of animals in their natural habitat." Meddis continues: "The data may be available somewhere but it is not easily accessed. Naturalists appear to regard sleep as an unimportant phenomenon even though most mammalian species spend more than half of their life in this state." It will become apparent that o u r knowledge of this aspect of primate socioecology is indeed limited and lacking in careful study. Where appropriate, some studies of captive primates will also be considered; it will be argued that captive research could better contribute toward the understanding of sleeping habits than has been the case in the past. 11.

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SLEEP'?

l h c basic primate pattern of existence is an arboreal one. so it is not surprising that most primates sleep in trees. There are a few well-known cases of the

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adoption of cliffs and shallow caves as regular sleeping sites such as by Hamadryas baboons (Papio hamadryas) in Ethiopia and Saudi Arabia (Kummer, 1968a; Kummer et al., 1981; Kummer and Kurt, 1963), chacma baboons (Papio ursinus) in South Africa and Namibia (Anderson, 1982; Gow, 1973; Hall, 1962; Hamilton et al., 1976; Marais, 1969; Stolz and Saayman, 1970), and gelada baboons (Theropithecus gelada) in Ethiopia (Crook, 1966; Kawai, 1979). The habit of using cliffs or rocky outcrops as sleeping sites has been recorded for other groups too, including olive baboons (Papio anubis) in parts of Ghana (Booth, 1956), Sudan (Butler, 1966), Ethiopia (Crook and Aldrich-Blake, 1968; Dunbar and Dunbar, 1974), and Kenya (Harding, 1976); yellow baboons (Papio cynocephalus) in a part of the Serengeti Plain (Altmann and Altmann, 1970) and on the Somali coast (Messeri, 1978); Barbary macaques (Macaca sylvanus) in parts of Morocco (Alvarez and Hiraldo, 1975; Deag and Crook, 1971) and on Gibraltar (MacRoberts, 1970); Formosan rock macaques (Macaca cyclopsis) in Taiwan (Poirier and Davidson, 1979); a group of Japanese macaques (Macaca fuscata, Hayashi, 1969); and common langurs (Presbytis entellus) at the north of their distribution (Bishop, 1979; Boggess, 1980). Hamilton (1982) has recently surveyed the literature on baboons and gives the following decreasing order of preferred sleeping sites: cliffs, emergent trees, emergent trees above a closed canopy, and open woodland. He also includes illustrations of the different sorts of sleeping sites. Throughout India, many rhesus (Macaca mulatta) and bonnet (Macaca radiata) macaques, as well as common langurs living in and around towns or villages, sleep on rooftops and various other niches in buildings (Blaffer-Hrdy, 1977; Rahaman and Parthasarathy, 1969; Singh, 1969; Southwick and Siddiqi, 1967; Roonwal and Mohnot, 1977). The reasons for the adoption of particular sleeping sites will be dealt with in detail later, but generally the choices can be interpreted in terms of inaccessibility to potential predators and comfort.

A.

How MANYSITES?

The number of sleeping sites used by different groups of primates varies widely. Some groups have one area that they return to almost every evening whereas others use hundreds of sleeping sites. In assessing the variability, it appears that multimale, forest- or woodland-living groups accumulate the most sleeping sites. Such groups of howler monkeys (Alouatta, Chivers, 1969; Sekulic, 1982), rhesus macaques (Lindburg, 1971; Makwana, 1978), and Japanese macaques (Wada and Tokida, 1981) all slept in dozens of different areas; one forest group of rhesus appears to have used over 200 sites in a 9-month period (see Fig. 9 in Lindburg, 1971). Great apes, namely, chimpanzees (Pan troglodytes), gorillas (Gorilla gorilla), and orangutans (Pongopygmaeus) nest in many different locations throughout their home ranges (e.g., Casimir and Butenandt, 1973; Goodall, 1965; MacKinnon, 1974). There are exceptions: One

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troop of squirrel monkeys (Snirnirz oersted) habitually slept in one small area of the home range (Baldwin and Baldwin, 1972), and a woodland troop of olive baboons generally returned to the same area each night (Ransom, 1981). Possible reasons for variabitity in the number of sleeping sites used are considered later. Forest-living groups that defend territories (and generally contain only one adult male) and more open-country , semiterrestrial species generally have fewer sleeping sites, e.g., up to 11 in yellow-handed titi monkeys (Callicebus toryuatirs, Kinzey et a l . , 1977); 14 in cotton-top tamarins (Saguinus oedipus, Neyman, 1978); 26 in Kloss gibbons (Hylobates klossi, Whitten, 1982a); 14 in Hanuman langurs (Blaffer-Hrdy, 1977); 14 in olive baboons (Harding, 1976); 22 in chacma baboons (Hamilton et al., 1976); and 15 in yellow baboons (Hausfater and Meade. 1982). Many groups of the above-mentioned species have considerably fewer sites than the figure given; indeed, some olive, chacma, and Hamadryas groups reportedly used only 1-2 sleeping sites (DeVore and Hall, 1965; Hall, 1962; Saayman, 1971; Sigg and Stolba, 1981), as do some family groups of KIoss gibbons and the sympatric Mentawai langurs (Presbytis potenziani, Tilson and Tenaza, 1982). Also, the wide-ranging, open-country patas monkey (Erythrocebus paras) is an exception, sleeping in many different areas throughout its home range: One group used 15 different sites in only 28 days (Hall, 1965). Several factors probably influence the number of sleeping sites used by a group of primates, the most important general one possibly being availability. An abundance of suitable trees allows some forest primates to have many sites (above references and Aldrich-Blake, 1970; Booth, 1956; Horwich, 1972; Mizumi et al., 1976), although some specific requirements of the sites may reduce the number, as is discussed later. It has been suggested that where both predators and potential sleeping sites are numerous, it may be advantageous to the primates to vary where they sleep (Bert, 1973; Blaffer-Hrdy, 1977; Goodall, 1962). Blaffer-Hrdy also reported a possible alternative antipredator tactic adopted by one group of langurs: One particular sleeping site was used on over 90% of nights, possibly because its location-near a human settlement surrounded by forest-afforded the monkeys good protection from predators. The contrast between the pattern of unpredictable usage of many sleeping areas by forest rhesus and the regular roosting in a few fixed sites by urban troops may be due to the scarcity of areas free from disturbance in towns (Singh, 1969). Primates for whom traveling through the home range in search of food can result in substantiai energetic demands may benefit from having many potential sites throughout the range (see also Ransom, 1981). Jay (1963) pointed out that by having several sleeping sites langurs did not have to make long return journeys. and Rasmussen (1979) drew attention to the savings in energy accruing to a troop of yellow baboons with several sleeping sites. Hamilton (1982) has put forward the hypothesis that the frequency of use of less-suitable sites in a group’s home range will increase at times when increased foraging demands result in use

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of wider areas of the home range. The relationship between sleeping sites and ranging patterns will be returned to in Section 111. This general line of inquiry leads to the question of where in the home range sleeping sites are situated. B.

THELOCATION OF SLEEPING SITES From the preceding discussion it might be expected that a proportion of sleeping sites would be found near food sources. Forest primates, in particular, seem inclined to sleep in areas where they have been feeding in the late afternoon (e.g., Harrisson, 1969; Lindburg, 1971, 1977; MacKinnon, 1974: Mizumi ei al., 1976; Pook and Pook, 1981; Rodman, 1979; Roonwal and Mohnot, 1977), although at least two studies have failed to find evidence of the distribution of food influencing choice of sleeping places in forest primates-in both cases monogamous, territorial groups (Dawson, 1979; Gittins, 1982). In general, gorillas (Dixson, 1981; Schaller, 1963; Tutin and Fernandez, 1983) and woodlandliving chimpanzees (Izawa and Itani, 1966; van Lawick-Goodall, 1968) also sleep near their latest afternoon food source, although they may travel over a kilometer before nesting (Goodall, 1965). In Gombe National Park, Tanzania, chimpanzees frequently slept around the area in which they were provisioned with bananas, an illustration of the way in which sleeping (and ranging) patterns can be influenced by the availability of certain foods (van Lawick-Goodall, 1968). The tendency of orangutans (Davenport, 1967; MacKinnon, 1974), and to a lesser extent chimpanzees (Goodall, 1965), to continue feeding while in the nest might influence the choice of nesting trees on some occasions. The possibility that ranging patterns could be based around a core area of sleeping sites was considered by Chivers (1969) with regard to howler monkeys. Subsequent studies of howlers have tended to suggest that the location of sleeping sites depends more on the location of used food sources than vice-versa (Milton, 1980; Richard, 1970; Sekulic, 1982). An interesting suggestion by Mittermeier (1973) was that primates such as howlers might show seasonal alternation between the two patterns of ranging: A group might sleep near food trees in the wet season, thus reducing the likelihood that foraging could be seriously impeded by downpours (see Section IX). This intriguing hypothesis deserves further testing with other species. Rahaman and Parthasarathy (1969) indicated that bonnet macaques shifted their sleeping sites in order to remain near food sources in times of scarcity, and Hamilton (1982) mentions that a similar effect was seen in chacma baboons in the Okavango Swamp, Botswana. Sleeping sites are commonly situated inside the core area of a group’s home range, i.e., the most intensively used area, or within the boundaries of the defended “territory” of a group [e.g., squirrel monkeys, Baldwin and Baldwin, 1972; Hanuman langurs, Blaffer-Hrdy, 1977; Lowe’s guenons (Cercopithecus campbelli), Bourliere et al., 1970; moustached tamarins (Saguinus mystax), Castro and Soini, 1978; lar gibbons (Hylobates lar) and siamangs (Symphalangus synductylus), Chivers, 1972; red colobus (Colobus badius) and black-

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and-whitc colobus (Coluhirs guereza), Clutton-Brock, 1974; vervet monkeys (Cercopithecus crethiops). De Moor and Steffens, 1972; chacma baboons, Davidge. 1978b; capuchins (Cebus albifi-om), Defler, 1979; olive baboons, Harding, 1976; Hanuman langurs, Jay, 1965b; pygmy marmosets (Cebuella pygmfieu), Ramirez et al., 1978; St. Kitts vervets (Cercopithecus nethiops subueusf. Poirier, 1972; pygmy marmosets, Simonds, 1974; Soini, 1982; Hanuman langurs, Starin, 1978; Mentawai langurs, Tilson and Tenaza, 19761. Factors causing partial or full exceptions to this pattern (e.g., olive baboons, AldrichBlake er 111.. 1971; Geoffroy’s tamarins, Dawson, 1979; yellow-handed titi monkeys, Kinzey er 01.. 1977) require clarification. In some of the abovcmentioned cases. the core area containing the sleeping sites was situated quite centrally within the home range, whereas in others it was peripheral; this obviously depends on the surrounding terrain and vegetation. Since defended territories, and to a lesser extent core areas, are not often penetrated by neighboring groups, there may be some exclusivity of sleeping sites. However, sharing of a proportion of sleeping sites is fairly common (Section IV). The final variable to be considered here for its possible influence on the location of sleeping sites is water. Substantial water courses appear to be important for the occurrence of sleeping sites of talapoin monkeys (Miopithecus talapoin, Gautier-Hion. 1973), for antipredator reasons which are given later. Water for drinking was recognized as a possible factor influencing the choice of sleeping areas in rhesus macaques during the dry season (Lindburg, 1971, 1977) and in chacma and Guinea baboons (Fady. 1977; Gow, 1973; Stolz and Saayman, 1970). Sharman ( 1981 ) mentioned that Guinea baboons (Pupio papio) usually slept in tall kapok trees (Ceiba penfandru) 5 m from water, but this habit also was evident in the wet season when water was in plentiful supply. However, in the same hot savanna region of eastern Senegal, chimpanzees were possibly restricted in their choice of sleeping sites by having to range near the few water sources in the late dry season (Baldwin et al., 1982). It also seems possible that the sleeping area of a group of vervet monkeys was chosen to facilitate drinking from tree holes (adult females) or from neighboring groups’ water holes (adult males) during a dry season (Wrangham, 1981). Finally, an early suggestion by Aschemeier (1922), that gorillas in Gabon nested near streams because these areas were avoided by other animals due to mosquitos, does not seem to have been taken up by subsequent investigators. Other physical characteristics of sleeping sites are dealt with in Section V . 111.

A.

SLEEPING SITESAS

DISTRIBU‘TION AND

A

LIMITING RESOURCE

GROUPSIZE

Sleeping sites were recognized as a potential factor limiting the distribution of primates in the early stages of field research. Washburn and DeVore (1961)

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suggested that sleeping trees were as limiting as food and water in the savannah and open grassland habitats of yellow baboons in Kenya (see also Washburn and Hamburg, 1965). Altmann (1974) noted that areas of Amboseli in Kenya have abundant food but no baboons during the rains and suggested a lack of sleeping trees as one reason for the failure of baboons to exploit these areas. In a “thicket savanna” region of Uganda, restricted numbers of Acacia selberina trees, the only ones suitable as sleeping trees for olive baboons, probably limited the distribution of baboons (Patterson, 1973). In the Namib Desert, areas adequate in food may be devoid of chacma baboons if there is a lack of suitable sleeping cliffs (Hamilton et al., 1976); Stolz and Saayman (1970) also proposed that availability of sleeping cliffs influenced the distribution of chacmas in open regions of southern Africa. It is perhaps not surprising that more open-country species like baboons seem particularly limited by a lack of suitable places to sleep, but the effect may also be seen in some forest-living primates. Indeed, in reporting on spider monkeys (Ateles geoflroyyi), Carpenter (1935) was possibly the first to suggest that “favourable trees” constituted a factor regulating dispersal. The question arises as to whether trees used primarily for sleeping, rather than other activities, can be identified as a resource limiting the distribution of forest primates. There appear to be a few examples of this, involving species with well-defined habitat requirements for sleeping. Troops of talapoin monkeys use lianas and branches of trees overhanging water as sleeping sites (Gautier-Hion, 1970; Rowell, 1972b). Talapoin troops were absent in areas of inundated forest which had only small water courses whose associated vegetation did not match that of the talapoin “dormitories” (Gautier-Hion, 1973). Another example concerns the golden lion tamarin (Leontopithecus rosalia) of Brazil. Family groups of this small monkey sleep in holes in trees. Coimbra-Filho (1978) has drawn attention to the apparent decline in numbers of this species from areas of forest where mature trees containing suitable holes are selected for felling. One suggested intervention was to supply nest boxes in areas where the tall trees used for sleeping by these primates were removed. As regards Asian primates, Jay (1965b) emphasized sleeping places over food value of the vegetation as a likely factor regulating the distribution of Hanuman langurs in India, and Poirier (1969) mentioned an abundance of sleeping trees as being one characteristic of preferred habitats of Nilgiri langurs (Presbytisjohnii). A scarcity of large trees for safe sleeping was also held to be the primary factor limiting the distribution of the otherwise adaptable bonnet macaque (Macaca radiata) in southern India (Simonds, 1974). Where sleeping sites are scarce, group size rather than absolute occurrence of primates may be affected. The most dramatic example of this comes from comparisons of Hamadryas baboons in different areas of Ethiopia. In areas with plenty of sleeping cliffs, troops were relatively small, i.e., usually fewer than 80 members and as few as 14. In contrast, where cliffs constituted a sparse but

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ioculi.~abundant resource (Altmann. 1974), troops or ”sleeping aggregations” usually numbered several hundred baboons (Kummer, 1968a, b). Areas with an adequate supply of food but generally impoverished in sleeping sites lacked troops of chacma baboons but supported solitary individuals or pairs (Hamilton and Tilson. 1982). In forests, where there is generally no shortage of places to sleep, this factor is less likely to affect group size (see Aldrich-Blake, 1970). The possibility that restricted dormitory sites might influence the size of talapoin troops was suggested by Gautier-Hion (1973), but she gave no supporting data. B.

RANGINGPATTERNS

In addition to influencing the occurrence and group sizes of primates, sleeping sites can constrain how far primates travel each day and during their lives. The above-mentioned examples of sleeping sites being located near water sources implied an influence upon ranging patterns. Altmann ( 1974) included sleeping sites among the essential localized resources determining ranging patterns in open-country species. Thus, during the rainy season, many mammals extend their range into the open plains where food and water are abundant, whereas baboons show a comparatively modest extension of ranging, their ability to return to sleeping trees being a limiting factor (Altmann and Altmann, 1970). Hall (1965) contrasted the very large home ranges of patas monkeys with those of baboons and vervet monkeys, noting that patas had the fewest restrictions on where they slept. Similarly, Kummer et a/. (1981) noted that Hamadryas baboons in Saudi Arabia appeared more “nomadic” than Hamadryas in Ethiopia; the former are less selective in their choice of sleeping sites. The ability of the distribution of sleeping sites to restrict lengths of day ranges has been pointed out for some other baboons ( P . a ~ i i b i . Aldrich-Blake ~, et al., 1971; P . ursinus, DeVore and Hall. 1965). Anubis baboons spent over 507~of their waking hours within 200 ni of their sleeping cliff (Harding, 1976), although this might be partly cxplained by the fact that some important food plants grew on the cliffs. As might be expected, there is little evidence that the size of home ranges in forest-living, arboreal monkeys is influenced by the availability of sleeping trees per se. One troop of woodland-living red howler monkeys (Alouotm s e n i d u s ) had relatively few sleeping trees in its home range. This troop had a small home range but large day ranges compared to neighboring troops with more sleeping trees (Sekulic, 1982). Dawson (1979) found that day ranges of Geoffroy’s tamarins were longer if they returned to the sleeping tree they had used the previous night. However. other observers have recorded shorter day ranges when a group returned to the previous night’s site (e.g., see Fig. 4 in Davidge, 1978b; Hall, 1962). The fact that some groups of Hamadryas baboons have only one or a few sleeping sites may result in them being forced to make relatively long daily journeys (Sigg and Stolba, 1981). In all of these examples of sleeping sites

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influencing day ranges, the availability of food seems to be an obvious complicating factor. Some primate groups can be considered as “radial packs” or “refuging systems” (Hamilton and Watt, 1970), further illustrating the socioecological significance of sleeping sites in some cases. In the former system, members of a group forage as a unit with their ranging anchored around some core site (i.e., sleeping site). In refuging systems, the groups are usually larger at the central site but fragment for efficient foraging. Hamilton and Watt considered groups of rhesus macaques and chacma and gelada baboons as exemplifying radial pack systems, whereas hamadryas baboons constituted a refuging s j stem. Limited data on the extent of subdivision of groups during the day hampers this exercise for many primates, but taking the broad definition of refuging as “the rhythmical dispersal of groups of animals from and their return to a fixed point in space” (Hamilton and Watt, 1970, p. 263), there are many instances of primates refuging for much of the time, with sleeping sites being the fixed point. Groups of vervet monkeys (Booth, 1956; De Moor and Steffens, 1972; Dunbar, 1974; Hall, 1965; Harrison, 1983a, b; Kavanagh, 198I), olive baboons (Aldrich-Blake et al., 1971; Rowell, 1966), yellow baboons (Hall, 1965), and long-tailed macaques (Macaca fascicularis, Fittinghoff and Lindburg, 1980) have been reported to range into relatively open areas during the day, following this by returning almost always to particular sleeping areas each night, in all cases the sleeping area being a strip of riverine or gallery forest with tall trees. Hall felt that such areas constituted a home base for his study groups. Of course, by no means can all groups of the above species be considered to be radial packs or refuging systems; the different arrangements observed in different habitats attest to the range of adaptations achieved by some species. There are fewer accounts of refuging primates whose home range lies exclusively within a fairly homogenous woodland or forest habitat. Talapoin monkeys are one possible example, as discussed earlier. In contrast to some sympatric species, a group of blue monkeys (Cercopirhecus rnitis) often returned to the same sleeping area each night (Mizumi et al., 1976). A troop of squirrel monkeys in a Panamanian forest had one “traditional” sleeping area (Baldwin and Baldwin, 1972); anubis baboons at Gombe, Tanzania, also appeared to sleep in only one area (Nash, 1973; Ransom, 1981). For some groups, not only the size of the home range, but its shape, or “structure” (Hall, 1963), is likely to be affected by the distribution of sleeping sites. For example, Nagel (1973) contrasted the rectangular range of a canyonliving anubis group which had several sleeping sites with the egg-shaped range of another group with only one site. The distribution of sleeping sites along a river edge probably contributed to the elongated shape of the home range of a troop of long-tailed macaques (Aldrich-Blake, 1980). A talapoin troop’s day ranges formed a series of loops along the river edge, to which the troop returned each

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evening to sleep (Rowell, 1972b). In forests, ranging patterns may be influenced by the location of preferred sleeping areas (e.g.. Rudran, 1978), especially if particular features of the site are important, such as the presence of tall trees. Dawson ( 1979) suggested that thc distribution of suitable sleeping trees might influence travel pattcrns in Geoffroy's tamarins, but no data were prcsentcd. in summary, the availability and distribution of sleeping sites may determine, at least in part, whether primates occur in an area, the size of groups, and the size and shapc of day ranges and home ranges. Relationships of this type are more likely to be noticed in primates living in more open habitats. but some forest or woodland primates may also be affected by the distribution of sleeping sites. A clear overall picture of how sleeping sites combine with other potentially limiting resource$, e.g., food. water. to influence these aspects is still to emerge. All of the above examples concern monkeys. As yet there is little evidence that nesting sites per se exert an important limiting influence on occurrence, group size. or travel patterns in great apes. Studies of forest-living chimpanzees and gorillas have found (sometimes scasonal) preferences for nesting in certain vegetation typcs. but no strong evidence for the subjects deliberately traveling to those areas solely for the purpose of sleeping (e.g.. Anderson et al., 1983; Baldwin cr nl., 1981. 1982: Goodall, 1962, 1965; Suzuki, 1969; Tutin and Fernandez, 1983). However, Horn (1980) and Kano (1983) have suggested that ranging patterns of pygmy chimpanzees (Pan pnniscus) might be affected by their prcferences for ccrtain nesting areas: in one case thc preference bcing for primary forest. in the other case for secondary growth.

IV.

SHAKING A N D COMPETITION FOK SLEEPING SITES

As discussed above, sleeping sites are a limited resource for some primates. It is of interest how groups and individuals partition access to this resource. Altmann (1974) proposed that home ranges of groups of primates might overlap most at areas containing resources with a restricted spatial distribution. In accordance with this, there are numerous examples of primate groups sharing a common deeping site. Usually the groups sleep at the common site on different nights (e.g., olive baboons, Aldrich-Blake el a / ., I97 1; long-tailed macaques, Angst, 1975: Hanuman langurs, Blaffer-Hrdy, 1977; chacma baboons, Hall, 1962: bonnct macaques. Sugiyama, 1971); resource partitioning of this type reduces aggression between groups (Altmann and Altmann. 1970). In Hamadryas baboons, however. the extraordinary concentration of sleeping sites on a few large cliffs means that large aggregations of bands and one-male units form at thc cliffs often. though skirmishes between bands for access to the sleeping ledges are common (Kummer, 1968b). Sigg and Stolba (1981) stated that sleep-

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ing cliffs were more important than feeding and drinking sites in determining home range overlap in Hamadryas baboons. There are reports of other primates sometimes sharing a sleeping site with one or more neighboring groups of conspecifics on the same night (yellow baboons, Altmann and Altmann, 1970; Hanuman langurs, Blaffer-Hrdy, 1977; proboscis monkeys (Nusalis lurvatus), MacDonald, 1982; chacma baboons, Saayrnan, 1971) but in some cases the groups settled only after there were aggressive interactions between them. Goodall ef a f . (1979) report that when chimpanzees discovered fresh nests in the periphery of their home range, i.e., in areas of overlap with a neighboring community, the chimpanzees would closely inspect the nests and adult males might then aggressively destroy them. This behavior seems related to the general hostility reported between the communities at Gombe and has not been recorded in other areas. Direct competition over sleeping sites may result in the losers being supplanted and having to find an alternative site. Virtually all evening shifts by groups of yellow baboons were due to intergroup competition for sleeping groves (Altmann and Altmann, 1970). One dispute among chacmas resulted in a troop heading for another site in the dark (Saayman, 1971), and another ended with the subordinate troop being ousted and forced to sleep in scattered, less-suitable trees (Hamilton et al., 1976). Schaller (1963) reported that a group of mountain gorillas could be dislodged from a nesting site if another group approached closely. Poirier (1974) suggested that sleeping trees constituted a potential source of aggression in colobines. He gave no direct evidence in support, but BlafferHrdy (1977) reported conflicts between Hanuman langur groups arriving at the same sleeping site in the late afternoon. Anderson (1981) predicts that the frequency of encounters between primate groups will be influenced by the extent to which the groups share sleeping sites; quantitative data are required. In considering sleeping places as a resource over which competition might arise, Eisenberg et ul. (1972) suggested that animals could act in concert to secure sites. This may be seen when members of a troop combine against another troop in a dispute over access to a site or when members of a Hamadryas band combine against another band at a sleeping cliff. Within-group competition is also reported. Dittus (1977) observed toque macaques (Macacu sinica) to vie for positions before settling down to sleep at night; subordinates sometimes had to settle for less-safe positions. Conflicts over relative position in sleeping clusters occurred among howler monkeys in a high-altitude forest (Gaulin and Gaulin, 1982); individuals ending up at the periphery of a cluster were more likely to suffer discomfort from the low night temperatures. Interestingly, Tollman (1982) has presented evidence from captive vervets suggesting that body temperature fluctuates less with increasing social rank in the group. In such cases it seems likely that kin relations and alliances among group members play a role in

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shaping the social arrangements at sleeping sites, as discussed later. Aggression sometimes also breaks out between orangutan and chimpanzee mothers and their juvenile offspring when the juvenile attempts to sleep beside the mother in her nest (Clark, 1977; Horr, 1972). Van Lawick-Goodall (1971) reported a case of a dominant male chimpanzee usurping a nest which an adult female had recently completed. Clearly, competition for good sleeping places between or within groups depends on the abundance of this resource, thus the phenomenon seems less common between groups of forest-living primates than in more open-country groups. However, Tenaza (1975, 1976) witnessed territorial defense of sleeping trees by adult male Kloss gibbons. At the study area on Siberut Island, Indonesia, the best trees-emergent and free of lianas-were not very common. Adult males defended their trees by performing most of their morning choruses from the crown of sleeping trees, less than 0.5 km from neighboring males in their sleeping trees. This seems the clearest example of sleeping sites as a primary defendable resource in a forest primate. in forests, where sympatry among primate species tends to be most marked, different species may share the same sleeping areas. Some overnight associations probably arise through the chance meeting of two species near a food source or on a travel route (for example, orangutans with long-tailed macaques, Fittinghoff and Lindburg, 1980; Cercopithecrts Iowei with Cercopithecirs petaurista, Bourliere et c i l . , 1970). but other cases of interspecific association overnight are more robust. Since some species seen together during the day tend to segregate with their own kind at night (e.g., several species in Uganda, Haddow, 1952; geladas and Hamadryas, Kummer, 1968a; eight species in Uganda, Lumsden, 1951 ; six species in Bolivia, Pook and Pook, 198I ; Cercocebirs cilbigena and six species in Uganda, Waser, 1980), why some species persistently sleep in association is an intriguing question. Gautier-Hion and Gautier (1974) reported that groups of C. riictiraizs and C . pogorzias in northeastern Gabon were more likely to be found together than apart. Their sleeping sites were usually contiguous. with some overlap of the two species at night. In this case, nighttime association seems to be a simple extension of that during the day. However, Chivers (1973) stated that primate species in an area of Malaysia were most likely to associate at night. He suggested that the ability to detect predators might be enhanced through such association, in particular, siamangs (Syrnphcikingus sy&ct\.lus) would benefit by their proximity to the very sensitive leaf monkeys. Bernstein ( 1967b) also noted that the adult male of a pair of gibbons regularly slept among a troop of banded leaf monkeys (Preshytis melalophus). Baldwin and Baldwin ( 1 9 7 3 also felt that squirrel monkeys and howler monkeys (Alonotta tdlosa) might respond reciprocally to each other's alarm calls elicited by nocturnal predators. Responses to predators at sleeping sites are discussed later.

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In summary, where sleeping sites are a limited resource, primates may compete with conspecifics from other groups for access to them. Sites in areas of home range overlap are usually used by the different groups at different times. Members of the same group may also compete for the most favorable or favored places at a site. Finally, while some species form mixed groups during the day but separate at night, others continue to associate overnight or even come together before settling to sleep. The extent and function of these various patterns require further study. V.

CHARACTERISTICS OF SLEEPING SITES

Throughout this article, “good” and “suitable” sleeping sites have been mentioned in relation to the distribution and behavior of primates. It is appropriate to examine the characteristics of sleeping sites and to identify what constitutes good or suitable solutions to this requirement of primates. Three main factors will be considered, namely, security from predators, comfort, and the degree to which the surrounding environment can be monitored from the site. It will be seen that the relative importance of each of these aspects varies with the prevailing ecological conditions. A.

SAFETY FROM PREDATORS

Many of the predators of primates, e.g., felids and snakes, are mainly crepuscular or nocturnal hunters. For some of the smallest species of primate, nocturnal birds of prey (e.g., owls) may also pose a threat-. It has been suggested that most primates are diurnal in order to avoid nocturnal predators (Moynihan, 1976). According to Meddis (1979), sleep keeps an animal quiet and inconspicuous during the period of greatest danger from predators (see also Washburn and Hamburg, 1965), and sleep at night might thus have had survival value for primates. Once asleep, however, when awareness and muscle tonus are considerably reduced, primates are, in theory, very vulnerable to attack. To avoid contact with predators at night, they generally settle in a spot likely to give them an advantage in detecting and/or avoiding potential predators. As discussed below, different primates approach the need for security at night in different ways. The importance of safety at the sleeping site is most readily appreciated in cases where the primates actually overcome hazards or obstacles in order to reach their chosen sleeping places. For example, at Mt. Assirik, Senegal, Guinea baboons would leap up to reach otherwise inaccessible boughs of a sleeping tree, risking an unbroken fall of 20 m onto boulders below (Anderson and McGrew, 1983). Climbing on the precipitous cliff faces containing the sleeping ledges was regarded as a dangerous activity for Hamadryas baboons in Ethiopia (Kummer

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and Kurt. 1963). Some members of a troop of chacma baboons living in a marsh in Botswana swam to the dead Acacia trees in which they slept; others crossed on fallen logs and then climbed the sleeping trees (Hamilton, 1982). Neville (1968a) noted that one group of rhesus monkeys rarely climbed their tall sleeping trees (pines) during the day, possibly because of the amount of effort required. A common feature of the sleeping places mentioned above is that they were difficult, if not impossible, for potential predators to reach or scale. According to DeVore and Hall (1965), “[tlhe most general statement it is possible to make about baboon sleeping sites is that they seem to choose the safest places available to them” (p, 32). The “safety” principle applies widely among primates, and many primates are very selective about where they spend the night. The one sleeping area used by a troop of long-tailed macaques on Mauritius was very steep and thorny. probably making it the safest place in the troop’s home range (Sussman and Tattersall, 1981). Some trees used for feeding or daytime resting might never be used for sleeping (e.g., Sugiyama, 1971). Black-mantled tamarins (Saguinirs nigricollis) sometimes rested on dead, slanting trees, but never slept on such trees at night (Izawa, 1978). Chimpanzees often construct day nests on the ground during rests, but their night nests are always in trees, unless an individual is too sick to climb (van Lawick-Goodall, 1968). It is not clear whether the 8% of pygmy chimpanzees’ nests which were found on the ground (Kano, 1979) were day or night nests. Orangutans may rest on old nests during the day, but rarely sleep in them at night (e.g., Davenport, 1967), although it is conceivable that this is better understood in terms of comfort than safety (see below). 1.

Heighi

Many primates sleep in relatively tall trees, sometimes at a higher level in the canopy than they would be likely to be seen during the day (e.g., M .fascictcleris, Bemstein. 1968; Cercopithecus diana, Colobus polykomos, and Colobirs budius, Booth. 1956; Aloucirta seniculris, Braza et al., 1981 ; Symphalangus synductylus, Chivers, 1977; Alouatta, Coelho et al., 1976; Mucaca sinica, Fooden, 1979; various species of Papio, Hamilton, 1982; Presbytis entellus, Jay, 196%; Callicehirs torquutus, Kinzey et al., 1977; M. radiata, Koyama, 1973; several species in Uganda, Lunisden, 1951; M . rnukatta, Madwana, 1978;Alouattu palliata, Mendel. 1976; several species in Uganda, Mizumi et al., 1976; Presbytis geei, Mukherjee and Saha, 1974; M. radicita, Rahaman and Parthasarathy, 1969; Papio anubis, Rowell, 1966; Cercopithecus mitis, Rudran, 1978; Alouatta seniculus, Sekulic, 1982; Presbstis entellus, Starin, 1978; M. sylvanus, Taub, 1077; Hylobares klossi and Presbytis potenziani, Tilson and Tenaza, 1982); this is obviously the case for species that spend much of their waking time on the ground-almost invariably they sleep off the ground. Adult male gorillas are exceptional in that they often or usually sleep on the ground, probably because of

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their considerable weight. The precise location of the nest on the ground does not appear to give the gorilla any advantage in detecting predators (Donisthorpe, 1958; Goodall, 1979; Kawai and Mizuhara, 1959). Clearly, the higher up a tree a primate is, the less likely it is to be attacked by largely terrestrial predators. Often primates choose to sleep in trees with no very low branches (e.g., Anderson and McGrew, 1983; van Lawick-Goodall, 1968). Furthermore, chimpanzees frequently increase the functional height of their nests by constructing them over gulleys or streams (van Lawick-Goodall, 1968). 2 . Concealment Sleeping high up in trees is not the only way to obtain arboreal safety. Whereas some groups of primates are reported to prefer tall sleeping trees with few lianas or vines (e.g., Dawson, 1979; Gautier-Hion e t a l . , 1981; Tenaza, 1975) or even leaves (free-ranging M . arctoides, Estrada and Estrada, 1976; Colobus ubyssinicus, Haddow, 1952; Papio ursinus, Hamilton, 1982; M . rudiutu, Koyama, 1973; M.fascicularis, Kurland, 1973), others regularly sleep lower down among dense tangles of vegetation. Some groups show flexibility: Longtailed macaques (M. fascicularis) either retired high in emergent trees or lower down if protected by a screen of vines (Aldrich-Blake, 1980). Geoffroy’s tamarins (S. oedipus) slept at a mean height of 16 m in tall trees, or below 7 m in short trees with heavy tangles of vines (Dawson, 1979). Marmosets (Callithrin humeralifer) settled for the night at heights of up to 20 m, but usually only 5-6 m when they retired in dense undergrowth (Rylands, 1981). In general, primates sleeping in tall or emergent trees are 20-50 m from the ground, whereas those sleeping among thick foliage are considerably lower. Squirrel monkeys in Panama slept at a height of 6-11 m, well below the upper canopy of 18-25 m (Baldwin and Baldwin, 1972). Members of a group of pygmy marmosets (Cebuellapygmaea) sleep huddled together among leafy twigs and vines, usually between 7 and 10 m (Soini, 1982), or in holes 8-12 m from the ground (Ramirez et al., 1978). The smallest Old World monkey, the talapoin, sleeps at a height between 2 and 15 m (Gautier-Hion, 1970), below that of most other arboreal African monkeys. All of the sleeping sites of groups of Goeldi’s monkeys (Callimico goeldi) and titi monkeys (Callicebus moloch) were in dense thickets of vegetation (Pook and Pook, 1981; Robinson, 1979). As is clear from the foregoing discussion, it is generally smaller species that use concealment among dense vegetation for avoiding nocturnal predators, and in areas of sympatry, vertical stratification among species at night is often noticeable (e.g., Booth, 1956; Jolly, 1972).

3. Additional Attempts at Inaccessibility Another strategy used by many tree-sleeping primates to reduce the chance of being preyed upon during the night is to sleep out toward the terminal ends of

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branches. This seems to be most common in relatively large monkeys and hylobatids, i.e., some of those species which also sleep in relatively tall or high trees (e.g.. S~mphalangussyndactylus, Chivers, 1974: M . sinica; Dittus, 1977; Piipio papio, Dunbar and Nathan, 1972; M . sinica, Fooden, 1979; M . rudiata, Koyoma. 1973; Preshytis entellus, Starin, 1978; M . m i r l ~ t t n ,Vessey, 1973). One observer suggested that howler monkeys (Alolratta palliarfa) slept on such small-diameter branches that the position would have been impossible to maintain if the monkeys did not use their prehensile tails to anchor them (Mendel, 1976). Some small monkcys also sleep at the terminal ends of branches (e.g., Sriirniri .sciureits. DuMond. 1968). There are two obvious ways in which sleeping on terminal branches might reduce a predator’s chances of successful attack. First, vibrations caused by the approach of a predator aloog a bough could be detected and evasive action taken. Second, since predators are often considerably heavier than their potential prey, their weight might not be supported by thin branches which could support climbing and jumping monkeys (Jay, 1965a). Therefore, while chimpanzees sometimes appear t o take risks by nesting low in young trees or saplings (Anderson et a(., 1983; Baldwin. 1979; Kano, 1983), the risk might not be as great as it first seems. Additionally. the majority of chimpanzee nests have at least one “escape route,” i.e., a path out of the tree which does not necessitate the chimpanzee descending to the ground immediately below the sleeping tree (Anderson rt d.. 1983; Baldwin, 1979). A testable hypothesis from Altmann and Altmann (1970) is that baboons sleep as far along a branch as their weight will allow. Such an arrangement would result in adult males being nearest to the trunk and hence likely to be initially nearest to an approaching predator. In general, Guinea baboons appeared to sleep in the middle third of boughs; some slept at the terminal ends, but few slept in at the trunk (Anderson and McCrew, 1983). At Ishasha, Uganda, adult female baboons with infants tended to be farther from the trunk than did adult males (Rowell, 1972a). Clearly, quantitative information on overnight positioning of age and sex classes at the sleeping site would be of interest. A graphic example of bdbOOns seeking refuge on the outer ends of branches in their sleeping tree comes from Busse (1980), who recorded several attacks by leopards (Partthera prirdiis) on chacma baboons while the latter were in their sleeping trees. While the leopard was on a broad branch near the trunk of the tree, the baboons were out on the terminal ends of branches, harassing the predator. Small primates sleeping in dense tangles of vegetation are afforded similar types of protection as larger primates sleeping on outer branches, with crypsis and noise of an approaching predator (Harrison, 1983b) as additional aids. It might even be argued that small primates vulnerable to attack from owls would be safer sleeping closer to the trunk of a tree than on more-exposed, terminal twigs. A group of cotton-top tamarins slept in near the trunk; once they slept in

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crotches near the trunk while howler monkeys slept on outer forks of the same tree (Neyman, 1978). Dawson’s tamarins, however, slept away from the trunk (1979). Kinzey et al. (1977) reported that titi monkeys (Callicehus torquatus) obtained protection from aerial predators by always sleeping at spots with branches directly overhead. In contrast to the above examples of primates sleeping in the midst of dense vegetation, Nissen (1931) suggested that by constructing “open” nests (i.e., in a location in the tree which gave no overhead cover), chimpanzees in Guinea reduced the chances of a predator dropping on them from abdve. Baldwin et al. (1981) found there to be a greater proportion of open nests in savannah-living chimpanzees in Senegal than in forest-living chimpanzees in Equatorial Guinea. It is possible that this difference is associated with differences in the risk from nocturnal predators in the two areas. Gautier-Hion (1970, 1973) suggested that talapoin monkeys sleeping on thin lianas and branches could detect vibrations of any approaching predator and escape either by climbing higher or by plunging into the water below. Finally, some of the smallest monkeys, the Callitrichids, avoid nocturnal predators by sleeping in elevated holes in tree trunks (Leontopithecus rosnlia, Coimbra-Filho, 1978; Saguinus fuscicollis and S. geoffroyi, Moynihan, 1976; Callithrix hurneralifer, Rylands, 1981; Cebuella pygmaea, Ramirez et al., 1978), but the extent of this behavior is far from clear [compare above reports with, e.g., Dawson, 1979 (Saguiaus oedipus); Izawa, 1978 ( S . nigricollis); Soini, 1982 (Cebuella pygmaea)]. In general, primates are successful in avoiding being preyed upon during the night, but there are records of attacks and kills by predators at sleeping sites. In an area of Botswana, leopards frequently climbed 15 m up into the sleeping trees (Diospyros rnespiliforrnis) of chacma baboons and killed some of the monkeys (Busse, 1980). Altmann and Altmann (1970) once arrived at a sleeping tree in Amboseli to find a leopard therein with two dead baboons, and Pirta (1982) found strong evidence of a predator (possibly leopard) killing and dragging rhesus and langur monkeys from their sleeping trees in India; in this case, felling of large trees in the forest might have resulted in a scarcity of safe sleeping refuges. Blaffer-Hrdy (1977) reported that an adult female Hanuman langur lost part of her tail during the night in a presumed predatory attack; the group left very early the following morning. Finally, an adult male rhesus evidently was killed by a tiger while sunning low in a tree shortly after sunrise (Lindburg, 1971). Mortality through predation has a role in population regulation, and the availability of safe sleeping places can be seen to have a role in this regulation (see Dittus, 1980). It would be of interest to compare relative predation rates at night and during the day. Choosing a safe place to sleep at night thus seems to be a significant aspect of the behavior of primates. Although habits that normally confer safety at night may persist in primates for whom the threat from predators has been removed

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(e.g., small islands, Estrada and Estrada, 1976; Vessey, 1973; note also the

tendency of captive primates to continue to sleep in elevated locations), in some cases this aspect of sleeping behavior has been modified. For example, in areas of Saudi Arabia where potential predators are scarce, Hamadryas baboons have takcn to sleeping on easily accessible slopes. in contrast to conspecifics in Ethiopia who slept only on vertical cliff faces (Kummer et al., 1981). One section of a troop in Ethiopia slept on relatively flat ground near the sleeping cliff but had a stand of opuntia cactus as a protective screen (Kummer, 1968a; see Hall, 1963 for a similar example in chacmasj. Of course the threat from predators is removed in captivity. and many captive primates take readily to sleeping on the floor or ground of their cage or enclosure. The responses of primates to predators or othcr disturbances at the sleeping site are further discussed in Section V l . B.

COMFORT

I.

Weather

Many wild-living primates have to cope with cold, even freezing, temperatures for some of the time, and all are periodically exposed to winds and rain of varying severity. Primates have behavioral thermoregulatory responses for adapting to foul weather. Minimum temperatures usually occur between sunset and sunrise. therefore it might be asked to what extent primates incorporate heatconserving measures into their sleeping habits. Postural adjustments and “social” solutions are both used, and these are described later (Sections VII and VHI). Here, location of the sleeping site as it relates to being comfortable is considered. Primates sleeping behind dense screens of foliage or in tree holes thus obtain some protection from wind and rain. Captive Saguiizus geojfro!i were observed to return to their sleeping hole if rain was falling (Moynihan, 1976). In such cases, protection from weather conditions is clearly bound up with protection from predators. It is of interest in the present context to look for “purer” examples of sleeping sites providing shelter from harsh weather. Although Hamadryas baboons in Saudi Arabia slept on easily accessible slopes, they chose crevices between and underneath boulders, thus obtaining protection from the 10°C wind (Kummer ef al., 1981j . Hamadryas baboons sometimes also move to leeward slopes to avoid winds during the day (Kummer, 197I b). The relatively limited availability of sleeping sites for some groups of Ethiopian Hamadryas means that sleeping cliffs are probably not selected for the amount of protection they afford from wind. In the Transvaal, however, where temperatures sometimes dropped below lO”C, chacma baboons’ choice of sleeping cliffs was probably influenced by the direction of winds, especially during the cool months of

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July and August (Stolz and Saayman, 1970; see also Hall, 1962); these baboons sometimes sheltered from strong winds during the day too. A more southerly population of chacmas living at high altitude encounters temperatures of down to - 11°C (Anderson, 1982). These baboons also sleep on cliff faces, and Anderson points out that at night the baboons receive heat absorbed by the rock during the day, thus they may stay warmer than if they spent the night in trees. Hanuman langurs living within 50 km of Tibet frequently sleep on southerly exposed cliff faces above the forest canopy (Boggess, 1980), probably for the same reason as chacma baboons at Suikerbosrand, i.e., to obtain warmth from the rock during cold or freezing nights. This explanation may extend to other cases of cliffs being preferred to trees. It also seems possible that macaques and langurs sleeping on rooftops benefit from this “extra” source of heat during the night. Some cliffroosting baboons and langurs may also be able to protect themselves from rain by moving behind boulders or under overhanging rocks on the precipice; some macaques also apparently shelter or sleep in caves during rain (e.g., M. cyclopsis, Poirier and Davidson, 1979; M.fuscutu, Hayashi, 1969). There might seem to be little that most bough-sleeping primates in the tropics could do, in terms of locating a sleeping site, to reduce discomfort from inclement weather. Of course, the nearer to the equator, the less temperature varies in forests. Nevertheless, gibbons (Hylobutes ugilis) in Malaysia slept in trees on ridges in preference to trees in valleys, and Gittins (1982) related this to the relatively lower night temperatures in the valleys. (He also considered “acoustics” as a factor influencing choice of sleeping trees; see following section.) It is possible that variations in microclimate affect choice of sleeping sites in other forest primates in ways that are still to be clarified. Furthermore, while the range of ambient temperatures in tropical forest may be relatively narrow, strong winds and rain may still pose problems for primates both during the day and at night. The inhibitory effect of these conditions on primates’ movements is discussed later, but it may be noted here that strong wind appeared to disturb sleep more than did low temperatures (down to 14°C) in Guinea baboons in outside cages in Senegal (Bert et al., 1975). Carpenter (1940) felt that the sleeping trees of forest-living gibbons were well protected from strong winds and that changes in wind direction could influence choice of sleeping trees. Horr (1977) and MacKinnon (1974) have suggested that orangutans might choose nest trees to avoid serious wind sway or to be exposed to the evening sun. Goodall (1964) and Reynolds (1965) noted chimpanzees sometimes building rather low nests on windy evenings. One instance of reuse of a nest by a chimpanzee might have been caused by a strong wind making it difficult to build a new one (Goodall, 1962). Such observations remain largely unquantified. One report suggested that olive baboons in an area of Ugandan forest slept on the ground rather than in trees if heavy rain fell around sdnset (Lumsden, 1951), but this has not been confirmed for any other baboons; indeed, Anderson and

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McGrew ( 1983) and Goodall (1965) commented on the failure of Guinea baboons and chimpanzees to make obvious use of the trunk of their sleeping tree for shelter from wind or rain. Apparently. antipredator responses and/or traditional (,see below) avoidance of the trunk predominated. Chimpanzees, however, may move to the base of a large tree for shelter from heavy rain during the day (Nishida. 1980). Jones and Sabater Pi (1971) felt that some nests of lowland gorillas were strategically located to provide shelter from rain. Schaller (1963) recorded greater numbers of sheltered nests during periods of rain in the Virunga area, but other studies of the nests of mountain gorillas have not found strong evidence of nests being sheltered from rain (Casimir, 1979; Kawai and Mizuhard, 1959). Chimpanzees do not appear to construct nests to shelter them from rain (e.g., Goodall. 1965); in fact. one group of chimpanzees in Senegal made a greater proportion of open nests in the wet season (Baldwin e f al., 1981). It was suggested that using open nests reduced discomfort from dripping vegetation after a downpour and allowed better exposure to the early morning sun (see Section IX). Preliminary information on pygmy chimpanzees (Pan paniscus) (Kano, 1982). however. suggests that these apes may sometimes deliberately build sheltered nests. as orangutans have been reported to do (Davenport, 1967; MacKinnon. 1974). The role of learning and tradition in sleeping habits is discussed in detail in the following section. but one interesting difference in two reports from the same area is considered here since it pertains to obtaining shelter at night. Many Japanese monkeys live in regions characterized by heavy snowfalls in winter. Some groups of monkeys move to sleep in certain areas where they are likely to obtain some protection from snow. e . g . . into dense forest (Izawa, 1972) or onto leeward slopes where they can sun themselves in the late afternoon and after sunrise (Furuichi el CJ/. , 1982). In the Shiga Heights, deciduous trees are leafless in winter, whereas conifers retain their leaves. Monkeys slept in conifers during winter nights, possibly receiving some protection from cold winds and falling snow by screens of packed snow on the conifers' branches (Wada and Tokida, 1981) . However. Suzuki (1965) reported that in the same forest, monkeys slept in conifers on winter nights irtdess it was snowing. in which case they slept on branches of defoliated deciduous trees. According to Suzuki. by making this switch the monkeys avoided snowfalls from the higher branches of the conifers landing on them. Neither report gives much detail. but together they point toward an interesting possible difference in a comfort-achieving aspect of sleeping arrangements.

2.

Oriw Aspects of Conlforf .. 1 here are other aspects of "comfort" offered by a potential sleeping site that might influence whether it will be used by primates. Whitten (1982b,c) found that Kloss gibbons avoided sleeping in trees with an abundance of Myr-mecodia

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tuberosa epiphytes, probably due to the biting ants associated with these plants. Whether such avoidance characterizes other primates is not known. Rudran (1978) pointed out that primates might avoid sleeping in fruiting trees lest they be disturbed by nocturnal frugivores (e.g., bats). In support of this, Soini (1982) noted that pygmy marmosets tended not to sleep in feeding trees. In general, tree-hole-sleeping primates would seem the least vulnerable to being disturbed during the night. Van Lawick-Goodall (1968) suggested that chimpanzees sometimes did not sleep in food trees because of the seasonal lack of suitable leaves, but no general pattern of the use of food trees for sleeping has yet been identified for monkeys or great apes. Goodall (1962) noted that about half of the fibers of branches used by chimpanzees in the making of a nest break so that they do not spring back when bent over. This contributes to the ape’s comfort during the night, and the location of trees with appropriately fibrous wood may influence the location of sleeping sites (see Horr, 1977). The above examples suggest that primates may compare potential sites from the point of view of comfort before making their selection. However, comfort is probably secondary to other considerations such as safety in many cases, and it may be sacrificed. Neville (1968a) felt that rhesus monkeys might have left their sleeping trees early in the morning because they were not particularly comfortable. It seems likely that great apes sometimes abandon nests because they are not very comfortable (e.g., Davenport, 1967; Goodall, 1962). Nissen (1931) pointed out that a fresh nest was probably softer, warmer, and less noisy than an old nest. Tutin and Fernandez (1983) found that lowland gorillas built more nests off the ground in seasonally inundated areas of forest. They suggested that by doing so the gorillas would be less damp, which suggests that comfort might indeed be an influencing factor in gorillas’ nest-building behavior. Another potential variable to be considered is odor. The accumulation of excreta at the sleeping sites of many primates often causes noticeable odors (see Section IX). It has been suggested that primates might use this odor as a cue to switch sleeping sites (Carpenter, 1940; Hausfater and Meade, 1982). This behavior could be functional: Baboons at Amboseli in Kenya appear to regulate their use of sleeping sites so as to reduce the chances of becoming infested with intestinal parasites deposited in their own feces (Hausfater and Meade, 1982). Anderson and McGrew (1983) found no such pattern of use in Guinea baboons at Mt. Assirik, Senegal, but in this case the baboons virtually never came into contact with the ground (and feces) below the tall sleeping tree. In this context it is interesting to note that stump-tailed macaques on a small island habitually slept in one large tree with branches overhanging the water (Estrada and Estrada, 1976). It is conceivable that much of their excreta at the sleeping site was thus washed away; this effect was noted for long-tailed macaques sleeping in a riverside tree (Fittinghoff and Lindburg, 1980). This general line of inquiry deserves

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further attention in the field. Cliff-roosting baboons in the Transvaal have low parasite loads (Pettifer, cited in Anderson, 1982). It is not clear whether this result is due to climatic factors (favored by Anderson) or to an efficient pattern of usage/avoidance of the sleeping sites. Stolz and Saayman (1970) give data which appear to indicate Ies.~avoidance of a site after use by baboons in the Transvaal than that shown by baboons in Aniboseli. The extent to which baboons sleeping on cliff ledges soil the ledges or come into contact with their excreta is not clear from the literature. Nor is it certain that odor would deter primates from using a sleeping site. A group of langurs was not discouraged from using a regular sleeping site by the stench of rotting carcasses of cattle (Mohnot, 197 I ) . Finally, ectoparasites may be considered as a potential factor. Nagel (1973) predicted that ectoparasites would flourish on the concave sleeping ledges of baboons, but 1 knoa of no data bearing upon this. MacKinnon (1974) also stated that orangutans' use of a fresh nest each night would reduce the possibility of infestation by ectoparasites.

c.

SLEEPING

SITES AS INFORMATJON

CENTERS

Several investigators have commented that elevated sleeping sites enhance primates' ability to monitor visually and to respond to events in the environment (e.g.. Goodall. 1962: Kurland, 1973; MacKinnon, 1974; Starin, 1978). Of course. this feature of sleeping sites has been sacrificed to some extent by primates that sleep in tree holes or in low, thick vegetation. In some cases, dominant or other adult males of a group take up the highest positions at the sleeping site, from where they can best monitor the surroundings (e.g., Miopithecus tulapoiii, Gautier-Hion, 1973; Muruca rurliata, Rahaman and Parthasarathy, 1969). By sleeping in emergent trees, groups of howler monkeys in Guatemala perhaps increased their ability to detect and avoid approaching spider monkcys (Coelho et a/., 1976). A semiwild orangutan nested on a cliff which visually dominated the surrounding environment (Harrison, 1969). However, while it may be the case that sleeping positions above the surrounding vegetation improve the ability to respond early to potential predators or other disturbance, during the dark seems questionable (see Donisthorpe, 1958). Occasionally, an essential resource (e.g., an isolated water source, Sigg, 1980) might be spotted from a favorable sleeping spot, but probably a more important feature of many sleeping sites is that they enable primates to communicate with neighboring conspecifics. For example, the adult male of a group of territorial gibbons, siamangs. langurs, howler monkeys, or titi monkeys usually engages in loud calling before leaving the sleeping tree in the morning. These vocal displays help to maintain spacing between groups, and some authors have noted that sleepingisinging trees are particularly well suited to the purpose of intergroup vocal communication, i.e., favoring good sound transmission and

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reception above the main canopy (Chivers and Raemaekers, 1980; Gittins, 1982; Gittins and Raemaekers, 1980; Kinzey et al., 1977; Sekulic, 1982; Tilson and Tenaza, 1982). Where visibility permits, visual signals can be incorporated into displays performed at sleeping sites. A good example of a sleeping site functioning as a “watchtower” is given by Fittinghoff and Lindburg ( 1 980). Two troops of Macaca nemestrina each slept in a large tree on opposite banks of a river. The sleeping trees were leafless, which the authors felt increased the conspicuousness of the troops’ presence and their branch displays to each other. After one troop’s sleeping tree fell down in a flood, causing a shift of sleeping site, some males of the opposite group swam across the river and invaded the home range of the first group, which suggests that the displays in the former sleeping tree had been an effective deterrent. It is conceivable that other reports of the use of leafless trees for sleeping or the use of large single trees, as by langurs in one densely populated area (Blaffer-Hrdy, 19771, might be open to similar interpretation, either along with or instead of antipredator considerations. By sleeping in fairly conspicuous positions, any subgroups sleeping at some distance from the rest of the troop might also be better located and contacted at dawn, as reported for bonnet macaques (Simonds, 1974). For primate groups that regularly break up into foraging subgroups during the day and come together at a sleeping site before darkness (e.g., some chacma baboons, Anderson, 1982; long-tailed macaques, Angst, 1975; Fittinghoff and Lindburg, 1980; olive baboons, Crook and Aldrich-Blake, 1968; Hamadryas baboons, Kummer, 1968a; St. Kitts vervets, McGuire et al., 1974; Guinea baboons, Shaman, 1981), i.e., those groups approaching a “refuging system” (Hamilton and Watt, 1970), congregation at the sleeping site provides an opportunity for dissemination of information among members of the sleeping party. This is also the case for chimpanzees who irregularly unite and disperse in the evenings before nesting (Goodall, 1962, 1965). Direct information about the physical condition of other members becomes available. In addition, motivational cues relating to the state of some resource or part of the home range can be exchanged to influence the direction in which members of the sleeping party travel in the morning. This increased opportunity for the transfer of information at sleeping sites may also apply to groups displaying strong cohesion during the day, since even these groups may increase cohesion at the sleeping site (see below). The foregoing discussion has indicated the importance of sleeping sites for many groups of primates. How particular sleeping habits are maintained in the behavioral repertoire is not well understood. The following section examines the ways in which certain sleeping habits might become established in primate groups and considers possible advantages of having some highly familiar sleeping sites.

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VI. A.

THADITIONAL SLEEPING SITESAND SECURITY

MONK

The sleeping sites of many primates seem to qualify as “traditional” sites in that their use continues through many generations. Good data are scarce, but studies of baboons and hylobatids spanning 10 years or more (Altmann, 1980; Chivers and Raemaekers. 1980) indicate long-term. regular use of particular sites. Buxton ( 195 1 ) reported that groups of Ugandan primates had been using the same sleeping trees for at least 6 years and stated that “the habits of a family group may remain constant for a period longer than the life span of the individual” ( p . 32). One report suggests that Japanese macaques have been using certain ledges and caves for shelter for over 100 years (Hayashi, 1969). Of course. evidence for a significant “tradition” factor in the location of sleeping sites is weak if the number of potential sites is limited, although strong preferences for particular sites could stili be due at least partly to traditional preferences. Also, as the preceding discussion has shown, in many cases the selection of sites can be explained in terms of safety, comfort, and/or information. Nevertheless, some instances of selection seem difficult to interpret from these functional viewpoints. and in such cases tradition (see DeVore and Hall, 1965)appears to be in operation. Wild Barbary macaques had both tall oak trees and cedars available. but slept only in the batter (Taub, 1977). Tree-roosting chacnia baboon troops slept in Acocia but not Adansonia trees (Stolz and Saayman, 1970). Yellow baboons in Amboseli slept in fever trees (Acacia xanthlophoeci) but not umbrella trees (Acacia tortifis),although both were tall enough for sleeping i n and the baboons used the latter for food (Altmann, 1974). Harding ( 1976) noted that olive baboons in Kenya showed strong preferences for particular points along the sleeping cliff despite the cliff‘s apparent uniformity (see also Hall, 1962, chacnia baboons). “Attachment” to particular sleeping places is also seen in Hamadryas onemale units (Kumnier. 1968a) and bands (Sigg and Stolba, 1981) regularly sleeping o n the same ledges when the cliff is shared. Altmann (1980) recorded significant regularity in the frequency with which individual yellow baboons used parts of a sleeping grove over a prolonged period, and Struhsaker (1967a) noted that individual vervet monkeys were seen more often in some groves than others. Subgroups of bonnet macaques consistently slept in the same clumps of bamboo (Simonds. 1974). In such cases. however, dominance relations might partly account for the allocation of particular places. For traditional sleeping habits to arise. the behavior in question must be labile. The wide variety of sleeping sites used by often closely related groups of primates is in itself evidence of such lability. Neighboring populations of conspecifics may differ in choice of sleeping locations. e.g.. tree holes versus boughs for callitrichids. buildings versus trees for langurs and macaques, snow-

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shielded versus open trees for Japanese monkeys, cliffs versus trees versus ground for various species of baboon (see earlier discussion). Some groups of baboons show a persistent tendency to sleep on cliff faces despite the presence of apparently suitable trees (Crook and Aldrich-Blake, 1968; Dunbar and Dunbar, 1974; Hamilton, 1982; Harding, 1976; Kummer, 1968b; Nagel, 1973; Stolz and Saayman, 1970); vervets always slept in trees although cliff ledges were available (Dunbar and Dunbar, 1974). This type of site attachment may reflect the development of a tradition surrounding a group’s sleeping habits. In some of the baboon examples, however, choice of sleeping sites has remained flexible to the extent that groups may use both cliffs and trees (Crook and Aldrich-Blake, 1968; Dunbar and Dunbar, 1974; Nagel, 1973; Stolz and Saayman, 1970). On the basis of the impressive variability in choice of sleeping sites, Kummer (1971a) has suggested that this behavior pattern is subject to a broad range of adaptive modifications, in contrast to some other behavioral traits that are more strictly genetically constrained. Similarly, Bert (1973) assigns choice of sleeping places to a tradition factor of sleep, whereas “genetic” and “rapid action” factors subsume other aspects. From the evidence reviewed above, it is clear that many primates show longterm loyalty to particular sleeping sites. Such sites must become highly familiar to the users. Good knowledge of the relative locations of sleeping sites is evident from the primates’ ability to travel to the sites from various directions, either directly or circumventing obstacles en route, and often despite restricted visibility due to vegetation or topography. Other known sleeping sites may be passed before reaching the one chosen for that particular night (e.g., Altmann and Altmann, 1970; Dawson, 1979). Such behavior indicates that the primates possess a “mental map” of the home range (Altmann and Altmann, 1970; Sigg and Stolba, 1981) in which sleeping sites are represented. Clearly, social transmission of information about sleeping sites and other habits passes from mature group members to young in monkeys. According to Bert (1973), infants acquire knowledge of sleeping sites, and where to position themselves at the site, through their prolonged close association with their mothers. Knowledge of suitable sleeping places is seen as one benefit accruing to the infant through maternal care (Eisenberg et al., 1972; Poirier, 1969). As is discussed below, this social transmission of sleeping habits almost certainly extends to nest-building patterns in great apes. B.

AND TRADITION IN NESTING HABITSOF LEARNING GREATAPES

There are several lines of evidence indicating that great apes learn to build their night nests through social learning. The techniques involved in nest building are already well described (Bernstein, 1969; Yerkes and Yerkes, 1929) and so will only be reiterated here briefly. The basic elements are the bending or

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folding over of several pieces of vegetation (e.g., branches in trees, herbacious material on the ground), and keeping the material in place by standing or sitting on it. A lining of small twigs, leaves, or other material is often added before the ape eventually lies down on the platform that has been made. Adjustments may continue for several minutes before the nest is considered satisfactory, and time taken to complete a nest varies from less than 30 see to around 20 min. Some efforts by chimpanzees are abandoned before completion if insufficient material is at hand (van Lawick-Goodall, 1968). Imprecise descriptions have created some confusion about certain aspects of nesting behavior in great apes. For example, certain authors have commented that nests appear to contain quite complicated interweaving or intertwining of materials (Izawa and Jtani. 1966; Nissen, 1931; Reynolds and Reynolds, 1965; van Lawick-Goodall, 1968). However, there is no direct evidence of deliberate weaving motions by apes making nests (Davenport, 1967; Dixson, 1981; Haddow, 1958; Harrison, 1969; Schaller, 1961), although gorillas may twist the vegetation as they bend it over (Bolwig, 1959; Dixson, 1981). If the finished product appears well plaited, it is probably due to elements being crushed and forced into place by the strength and weight of the builder, rather than being neatly woven. Of course, this does not mean that learning is not involved in nest building. Another aspect of nesting that is not clear is the degree to which materials to be incorporated into the nest are transported to it. Reynolds and Reynolds (1965) reported that chimpanzees in Budongo Forest, Uganda, sometimes fetched small branches and twigs from neighboring trees and used them in the nest, but Goodall ( 1962) did not observe this in Tanzania. Kawai and Mizuhara (1959) observed no transported vegetation in the nests of mountain gorillas, and Schaller (1963) stated that it was rare. In contrast, it appears to be more common in orangutans (Harrisson. 1962; MacKinnon, 1954). Great apes born and reared in captivity with no opportunity to observe othcrs building nests do not do so themselves when given the opportunity. Bernstein ( 1962, 1967a) found that wild-born chimpanzees captive for over 30 years still made nests when presented with suitable materials, whereas no captive-born chimpanzees did so. despite manipulation of the materials. Lethmate (1977) recorded some elements of nest-making behavior in an isolation-reared orangutan. e.g.. arranging objects in a rough circle around himself and patting down inaterials with his hands, which suggests that nest building depends on an interplay between innate motor tendencies and learning. Bernstein (1969) gives a fuller description of the responses of captive great apes to nesting materials. Nest building has to be taught to rehabilitant chimpanzees (Brewer, 1978; Carter. 1981). Furthermore, the absence of a maternal nest-building model results in such youngsters being lazy about aspects of nest building when they do it. e.g., by making them on the ground rather than in trees (Harrisson, 1962).

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Baldwin et al. (1981) point out that the several years during which a young chimpanzee sleeps with its mother at night provide it with over 2000 “trials” during which the mother serves as a potential model of how to build a nest. They suggest a combination of stimulus enhancement, trial and error, and imitation as the mechanisms leading to sophisticated nest building. Infants begin to incorporate nest-building patterns into play in the second half of the first year of life (MacKinnon, 1974; Schaller, 1963; van Lawick-Goodall, 1968). The nests of juvenile gorillas may be quite crude compared to those of adults (Schaller, 1965), but a similar distinction does not seem to have been made for chimpanzees or orangutans. Given the evidence for a learning component in nest building, and the known propensity for “tradition drift” in other aspects of chimpanzees’ behavior (e.g., McGrew and Tutin, 1978), it is reasonable to look for evidence of traditions in the nesting behavior of great apes. Particular vegetation types (Anderson et al., 1983; Horn, 1980; Kano, 1983; Suzuki, 1969; Tutin and Fernandez, 1981), or specific areas near seasonal food sources (Goodall, 1962; MacKinnon, 1974; Schaller, 1963) may be strongly preferred as nesting sites, but it has not been established that they are chosen for traditional reasons rather than more functional ones such as safety, comfort, or, as MacKinnon suggests for orangutans, on good travel routes. Some evidence for the development of a traditional nesting habit was reported in chimpanzees by van Lawick-Goodall (1968). For the first 14 months of her study, van Lawick-Goodall saw no nests in any oil-palm trees (Elaeis guineensis), but these became increasingly common during the second year, suggesting the development of a “fashion” among the chimpanzees for nesting in these trees. Better examples are awaited. It can also be asked whether behavioral differences between populations might be due to cultural divergence between them. An obvious point for comparison has been the heights of nests. In an early report on mountain gorillas, Kawai and Mizuhara (1959) suggested that variations in heights of nests could be accounted for by differences in habitat, and there has been little subsequent evidence to contradict this. Dixson (1981) adds that variations in hunting pressure could influence the height at which nests are built. MacKinnon (1974) states that differences in the heights of trees in different sites at which orangutans have been studied can account for differences in nest heights. In the most thorough comparison of nesting variables in two populations of chimpanzees, Baldwin et al. (1981) found that nests in a savannah habitat in Senegal were built higher than those in a tropical forest in Rio Muni, despite the greater abundance of tall trees in the latter site. The difference was interpreted in terms of unequal danger from predators, and other differences-i.e., more nests in Senegal being open (see Section V), occurring in larger groups, more often being in a tree with another nest, and being in trees with broader girths-were interpretable in terms of environmental differences between the sites, rather than as cultural differences.

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A geographically intermediate population also living in rain forest built nests very similar to those of chimpanzees in Rio Muni (Anderson et al., 1983). Thus while the above evidence, and some to be discussed later, indicates that chimpanzees and other apes readily adapt their nest building to environmental conditions, the behavior appears quite stereotyped. and there is no good evidence of purely cultural differences having emerged.

c.

ADVANTAGES OF HIGHLYFAMILIAR

SITES

Several possible advantages to primates having regularly used, familiar sleeping sites have been proposed. Some are more speculative than others: If conditions are such that leatlessness of the sleeping tree is advantageous, then repeated use of certain trees may be advantageous by encouraging defoliation (see Kurland. 1973; Lumsden. 1951). Heavy use of a tree for sleeping may result in the most-used branches being worn smooth (Anderson and McGrew, 1983; Washburn, 1957). and if the tree is otherwise covered with thorns, the primates can sleep in relative comfort while scansorial predators may be deterred (Sharman, 1981). Habitual use of one area of flat ground for sleeping by Hamadryas baboons may eventually lead to the growth of a protective screen of opuntia cactus from seeds deposited in the baboons’ feces (Kummer. 1968a). Long-term use of a cave by Japanese macaques results in a build-up of feces, and by sitting o n the (dried‘?) feces as opposed to the bare floor (see Hayashi, 1969), the monkeys may obtain some degree of insulation. The layer of hair accumulating in the bottom of tree holes regularly used for sleeping by callitrichids (CoimbraFilho, 1978) probably also acts as an insulator. The potential transmission of information at communal sleeping sites has already been mentioned. Another possible advantage of a regular site might be that any group members that accidentally became separated from the main body of their group could rejoin it in the evening (Bert, 1973). Evidence for increased cohesion at sleeping sites is considered in the following section. Two reports concerning groups of stump-tailed macaques released in unfamiliar areas suggest a meehanisni through which preferences for particular sites might become established. Both groups adopted a sleeping site quite near the spot of their release and showed a continuing preference for this site. Bertrand ( 1969) suggested that the feeling of safety imparted by this first site caused the monkeys to persist in this safe choice. Estrada and Estrada (1976) felt that in their group the initial choice of site might have been determined by the proximity of il large fruiting tree, but a sort of “imprinting” to the first safe sleeping site might account for its continued use. That familiar sleeping sites impart a sense of security to their users is suggested by other lines of evidence. A troop of Nilgiri langurs in south India was forced to shift its home range due to deforestation, but in the early stages of the

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shift, the monkeys would return to their familiar sleeping area before dark (Poirier, 1968). Some monkeys flee to their sleeping places to escape threatening dogs or humans (Bernstein, 1968; Taub, 1977); this tendency led Braza et al. (1981) to use the term “night-refuge sites.” The only time olive baboons did not flee from domestic dogs was at a sleeping cliff (Harding, 1976), and Struhsaker (1967a) suggested that being highly familiar with the layout of a sleeping site could facilitate a vervet’s escape from nocturnal predators. Attacks on chacma baboons by lions within 1 km of the baboons’ sleeping grove resulted in a muchreduced day range the following day, confined within 200 m of the sleeping site, and during nocturnal attacks by leopards, the baboons remained in their sleeping trees (Busse, 1980). A solitary male yellow baboon continued to sleep in the favorite grove of his former group, until he joined another group with different sleeping groves (Altmann and Altmann, 1970). Flight distance is usually reduced at sleeping sites; diurnal primates are generally reluctant to travel in the dark (Altmann and Altmann, 1970; Hall, 1962; Hamilton, 1982; Harding, 1976; Kummer, 1968a, 1971b; MacKinnon, 1974; Schaller, 1963; Sharman, 1981; Washburn and DeVore, 1961). However, disturbance from humans, carnivores, other primates, or, in one case, elephants uprooting trees (Pirta and Singh, 1980) may result in primates evacuating the site, but more usually disturbance leads to them leaving very early the next morning (e.g., Bertrand, 1969; Blaffer-Hrdy, 1977; Kummer, 1968a; Nissen, 1931; Oates, 1977). Whether or not they respond with vocalizations to nearby predators (see following section), roosting primates virtually always remain at the sleeping site during an encounter at night. They appear to prefer to stay put in their sleeping places than risk moving away or onto flat ground in the dark where the danger might be even greater. Thus there are records of monkeys sleeping in proximity to potential predators, e.g., a tiger and its kill (Jay, 1965b), cobras (GautierHion, 1973) and pythons (Fittinghoff and Lindburg, 1980). In certain cases, following serious disturbance at a sleeping site, the primates avoid using the sleeping site for some period in the future. Fatal attacks by leopards at a sleeping grove resulted in a group of yellow baboons not sleeping at the grove for over 2 months, whereas they had used it on 13 of 57 nights before the killings (Altmann and Altmann, 1970). Hamilton (1982) also reports that sleeping sites were abandoned by chacma baboons for a time following nocturnal attacks by leopards. Rhesus monkeys abandoned a rooftop sleeping site after some members of the troop were trapped there by humans (Pirta and Singh, 1980). It would seem reasonable to suggest that the likelihood of a group deserting a sleeping site may depend upon the availability of alternative sites. The Amboseli baboons that deserted the grove after suffering from leopard attacks had several other groves. Chacma baboons that lost group members through leopard attacks in the sleeping trees (Busse, 1980) apparently continued to use the same trees; conceivably other, suitable sites were scarce. Similarly, despite

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the trapping of baboons at their sleeping cliffs, the primates continued to use the cliffs as before (e.g., Kummer. 1968a). Mohnot (1971) describes a remarkable case of loyalty to a particular sleeping site in Hanuman langurs at Jodhpur, western India. Despite the stench from rotting dead cows during a period of drought, the langurs continued to sleep at the site. Furthermore, even though 71 members of the 82-member troop died. probably from drinking contaminated water, and the carcasses were scavenged by crows and vultures, the 1 1 survivors continued to sleep in the vicinity of the skeletons of their friends and relatives; in fact. they tended to travel less far from the sleeping site than normal during this period. Apart from showing strong attachment to a highly familiar sleeping site, this example suggests that desertion may be less likely if there is no obvious external cause of upheaval to the monkeys.

A.

ARRIVAL

Generally speaking diurnal primates are in their sleeping positions by nightfall. though variation in time of arrival at the sleeping site appears marked compared to time of departure in the morning (Chalmers, 1968; Chivers and Raemaekers, 1980;Gibbons and Menzel, 1980; Gittins, 1982; but see Hall, 1962 and Kummer, 1968a for baboons). Some factors contributing to the variability within and between groups are known: Dull weather (Reynolds and Reynolds, 1965; Kowell, 1966), rain (Dawson, 1979; Izawa and Itani, 1966; MacKinnon, 1974j, or snow (Hall, 1963) may cause earlier than normal cessation of the the day's activities. A sudden storm was the only condition to prevent a free-ranging group of stump-tailed macaques from reaching their favorite sleeping tree (Estrdda and Estrada, 1976). in chimpanzees and orangutans, sickness may lead to the early construction of nests (Goodall, 1983; Harrisson, 1969). Seasonal differences in time of retiring are well documented. Chacma baboons (Hall, 19621, rhesus monkeys (Makwana, 1978), green monkeys (Harrison, 1983a), and chimpanzees (Nissen. 1931 ; van Lawick-Goodall, 1968) tended to retire later during the summer months with more daylight, and orangutans retired later in the dry months (MacKinnon, 1974). Agile gibbons retired early in the wet seasonaround 3 hr before dusk (Gittins, 1982). Rhesus monkeys in outdoor cages also retired early in freezing temperatures, but the start of their daily activity was not affected (Chernyshev, 197 I ). It seems likely that time of arrival at the sleeping site is influenced by foraging requirements. Sigg and Stolba (1981) recorded earlier arrivals at the sleeping cliff following relatively short day ranges in Hamadryas baboons. Whereas gibbons might retire between 1500 and 1600 hr, sympatric siamangs usually settle

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1-2 hr later (Chivers, 1972; MacKinnon, 1977); this difference has been interpreted in terms of the siamang’s 50% greater energy requirement (Gittins and Raemaekers, 1980). Interestingly, leaf monkeys and macaques tend to retire later than both gibbons and siamangs (Chivers, 1971b, 1973); this might be a result of competition for food (see Tilson and Tenaza, 1982) which the dominant apes win earlier in the day. MacKinnon and MacKinnon (1980) also point out the possibility of differences between sympatric species in time of retiring being related to optimal intake of foods of varying digestibility, rather than direct competition between the species. Lumsden (1951) and Haddow (1952) noted species differences in time of settling in the sleeping trees among African primates, and Kinzey and Wright (1982) mention a difference between two species of Cullicebus. However, a comparative perspective on times of retiring in relation to foraging requirements has not yet been taken with African or neotropical primates, though Dawson ( 1 979) noted that by retiring toward dusk, Geoffroy’s tamarins avoided direct competition for food with the night monkey, Aotus. Gittins (1982) has drawn attention to the possibility of differences in feeding requirements between age and sex classes within a group producing differences in times of settling down for the night. As in Gittins’s study of gibbons, juvenile orangutans are reported to continue feeding later and consequently to retire later than adults (Horr, 1972; MacKinnon, 1974). Infant chimpanzees may make several short journeys from the mother’s nest before eventually staying in it with her (Goodall, 1962). Time of retiring for the night may be delayed by bright moonlight (e.g., Miopithecus talapoin Rowell, 1972b). Altmann and Altmann (1970) found that yellow baboons tended to be slightly further from their sleeping trees toward dusk during periods of a full moon than during other lunar phases. They suggested that by avoiding the sleeping grove the baboons might be reducing the chance of an attack by a predator (leopard) in the moonlight. Another possibility is that a full moon simply allows diurnal primates to engage in daytime activities both later in the day and earlier in the morning through improving visibility (Anderson and McGrew, 1983). Nevertheless, that predators may constitute a problem for primates around the sleeping site is suggested by the often cautious approach to the site in the late afternoon. Attacks on baboons by leopards were frequently observed near sleeping sites by Hamilton (1982) and were only ever witnessed around sleeping sites by Busse (1980). The adult male of a group of patas monkeys (Erythrocebus patus) thoroughly reconnoiters the area before the group members settle into scattered trees for the night (Hall, 1967). Dawson (1979) suggested that the silent and often rapid approach to the sleeping tree by Geoffroy’s tamarins might help in avoiding the attention of predators, and Nissen (193 1) felt that chimpanzees were most alert as they began to construct their night nests. Stolz and Saayman (1970) also noted cautious and quiet approaches to the sleeping cliff by chacma baboons; this possibly resulted from competition

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between chacnia groups for access to the site. Hamadryas one-male units and bands also monitor the site and other subgroups intending to use the cliff from their customary “waiting areas.” which they usually reach between 1600 and 1700 hr (Kummer, 1968a; Sigg and Stolba, 1981). A group of humans setting up camp at a sleeping site of Hamadryas baboons caused the latter to move 500 m along the cliff before retiring (Kummer ef [ I / . , 1981). Why some primates frequently enter the sleeping site after dark is not clear (c.g.. Cer-copitherws ascanizts, Haddow, 1952: Miopithecus ralapoin, Rowell, 1972b). Possibly this represents an alternative antipredator tactic or an adaptation to other aspects of the environment. Some late arrivals at the sleeping site can reflect short-term adjustments to current ecological or social conditions. For example. red-tail monkeys sometimes retired late if afternoon foraging had been intempted by a downpour (Haddow, 1952). Mother-infant pairs of long-tailed macaques sometimes did not enter the Sleeping tree until after dark because they were frequently attacked by newly dominant males (Wheatley, 1982), and young adult rhesus males on the periphery of the group took up their sleeping positions at the edge of the group after dark (Vessey, 1973). Gibbons and Menzel(1980), studying captive tamarins (Saguinus fitscicollis), speculated that the maximum separation observed between the parents and the oldest offspring during progressions toward the nestbox reduced aggression between them. It also seems likely that some arrivals in the dark (e.g., Rowell, 1966) are due to “miscalculations” in the primates’ activity budgeting. Reynolds and Reynolds (1965) observed an adult male chimpanzee continuing to feed as darkness fell and found him in a crotch of the tree the following morning, suggesting that he had not bothered to make a nest. In the same vein, Dixson (1981) indicates that gorillas may forego building nests if they continue feeding until nightfall. Once in the vicinity of the sleeping site, primates may engage in a final bout of feeding or socializing before moving into their nighttime positions. Social behavior might continue after dark, with individuals shifting positions and changing partners. As might be expected, the amount of presleep activity around dusk is widely variable in primates, but sooner or later the sleeping party quiets down, and individuals fall asleep. B.

POSTCRES

The postures adopted for sleep are not random. They represent adaptations to problems of temperature and stability. For example, most primates sleep in a squatting or sitting position; several investigators have commented that sprawling is rare at night (Altmann and Altmann, 1970; Anderson and McGrew, 1983; Bertrand, 1969; DuMond. 1968; Kummer. I968a; Thorington, 1968; Vessey, 1973: Washburn. 1957). While a sitting posture is probably better than a lying one for moving quickly should the need arise (DuMond, 1968), the preference

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for sitting at night is better understood as a response to the cool night temperatures. Sprawling with the limbs dangling or outstretched is a heat-dissipating posture and is therefore commonly observed during the day (e.g., Bertrand, 1969; DuMond, 1968) or on warmer nights (Schultz, 1961). In the cooler night temperatures, body heat can be conserved to a certain extent by bringing the extremities in close to the body, which may be hunched (Altmann and Altmann, 1970; Carpenter, 1940; Whitten, 1982b). The hands and feet may be brought together, or “stacked,” in between the flexed legs (Anderson and McGrew, 1983; Wada and Tokida, 1981; Washburn, 1957). Gibbons may wrap their long arms around their tucked-up knees (Benchley, 1947; Ellefson, 1974). With the head lowered, these sitting postures result in the relatively thinly haired chest and inner surface of the limbs being covered. Also, primates may sit with their back to the wind or rain (Altmann and Altmann, 1970; Harrisson, 1962; Kummer, 1968a); the hair may be erected and postures are adopted to optimize runoff of water from the coat, rather than soaking into the skin (Anderson and McGrew, 1983; Starin, 1978). One chimpanzee sat up in his nest during a nighttime downpour, wrapped his arms around his drawn-up knees, and lowered his head between his knees in a manner similar to that observed in humans (Goodall, 1962). Huddling with other individuals as a heat-conserving behavior is discussed in the following section. In addition to helping conserve body heat, by flexing the spine and placing the arms low between the thighs a primate lowers its center of gravity (Wells, 1974), thereby increasing stability. The large body size of great apes may be the main reason for their adoption of lying postures for sleep, and ischial callosities are either absent or less pronounced in these primates than in Old World monkeys. Even so, great apes appear to conserve heat by drawing their limbs close into the body, while usually lying on their front or side (Goodall, 1965; Nissen, 1931). Schaller (1963) mentioned that supine sleeping postures were extremely rare in mountain gorillas, who were often exposed to freezing ground temperatures. Chimpanzees sometimes lie on their backs in their nests (Goodall, 1965; Izawa and Itani, 1966), but it is not clear how prevalent such a posture is during the night; it was rare in a study of captive chimpanzees (Freemon et al., 1970). With the weight resting on the ischial callosities and the soles of the feet, a “tripod” arrangement is achieved by Old World monkeys and hylobatids. Washburn’s (1957) argument that ischial callosities evolved in primates as the callosities enabled them to sleep sitting on branches seems reasonable. The generally smaller and lighter New World primates lack ischial callosities (Rose, 1973). Many of them crouch on all fours to sleep, and some use their prehensile tail as a brace or anchor during the night (e.g., Milton, 1980), which reduces the amount of energy expended in staying in place (Mendel, 1976). It seems likely that the tail aids balance during the night in some Old World monkeys too

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(Anderson and McGrew. 1983; Wells, 1974). Some primates prefer to sleep at forks of boughs, whereas others show no such preference; the data on this aspect of sleeping are too fragmentary for comparisons. Finally, particular postures may be either assumed or avoided to minimize discomfort from aches or wounds (Rahaman and Parthasarathy, 1969). It can be seen that a combination of physical and behavioral adaptations operate to maintain an individual's comfort and stability during the night, even during periods of muscular relaxation in sleep (Rose, 1973). Most perching primates appear to rely on balance to stay in their sleeping places. Although Kumnier (197 1 b) and Ellefson (1974) wrote that Hamadryas baboons and gibbons might make use of handholds, such reports are uncommon; perching seems to bc the most conimon way of maintaining stability. As noted earlier, the hands are often placed together between the legs, and Anderson and McGrew (1983) commented that Guinea baboons did not hold onto foliage while sleeping. Perhaps surprisingly, there are very few reports of falls from elevated sleeping positions: Busse (1980) reported that an adult female chacma fell out of a sleeping tree during a lightning storm. The baboon was severely stunned, but eventually recovered. Sharman (1981) found an adult female Guinea baboon dying at the foot of a sleeping tree, with injuries including a fractured skull. Rare accidents of this type illustrate the successful adaptation of most primates to problems of reaching a safe sleeping place and staying in it overnight. Although orangutans and chimpanzees may hold a lateral or overhanging bough while lying in their nests (e.g., Harrisson, 1962; Izawa and Itani, 1966), this is not universal (e.g.. Goodall, 1965) and is probably not necessary for maintaining position in the nest. Finally, the sleeping postures of the Geoffroy's tamarins studied by Dawson (1979) appeared to have an antipredator function. In a tight cluster with their heads lowered, the huddling tamarins looked much like the brown arboreal nest of some termites. This cxample is a reminder that tnany primates are well camouflaged by virtue of morphological adaptations including color. Combined with appropriate postures, such adaptations are undoubtedly useful in conditions of poor light when many predators are active.

C. NOCTURNAL ACTIVITY I . Gmrral Activity With some primates, activity during the night appears to be minimal: Individuals can usually be found at the same spot in the morning as they were left the previous night. often in precisely the same or similar postures (Altmann, 1980; Ellclson, 1974; Kinzey L't (11.. 1977; Neville, 1968a Rahaman and Parthasarathy, 1969; Richard, 1970; Riss and Goodall, 1976; Struhsaker, 1967b). Nocturnal

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silence and stillness in patas monkeys was considered by Hall (1966) to be to their advantage against predators. This probably applies to other species too. Even baboons can be inconspicuous in their sleeping trees when they quiet down (Altmann and Altmann, 1970; personal observations). The torpidity noted in several species of callitrichids during sleep (Hershkovitz, 1977) may guarantee inactivity and hence increase inconspicuousness; this would be in accordance with the view that sleep has evolved largely to reduce activity (e.g., Meddis, 1982). In a torpid state during sleep, tamarins may be quite unresponsive to an approaching human (Dawson, 1979). Great apes change postures during the night (MacKinnon, 1974; van Lawick-Goodall, 1968) and may even leave the nest, but this is apparently rare. By no means are all primates totally inactive during the night. Radiotelemetry of wild gelada baboons revealed considerable nocturnal movement (Kawai and Iwamoto, 1979). Most movements lasted less than 30 sec and probably reflected minor shifts of position. Captive Macaca cyclopsis changed postures 10 times per hour during the night (Kawai and Mito, 1973). DuMond (1968) felt that squirrel monkeys were more active during the first few hours of sleep than later. Freemon et al. (1970) found that in captive chimpanzees body movements were more frequent during later periods of rapid eye movement sleep. Bert (1970) has suggested that the various stages of sleep may be present to varying degrees in species according to their nighttime behavioral profiles, which in turn relate to their ecological circumstances and pressure from predators. The behavioral data are as yet too scant to assess this hypothesis. Some shifts of position during the night may result from disputes between individuals (Simonds, 1974). Vocalizations may occur in response to some disturbance in the environment or to other group members, weaning vocalizations being common in baboons (see Anderson and McGrew, 1983; Baldwin and Baldwin, 1976; Byme, 1981; Kummer, 1971b; Shaman, 1981; Stolz and Saayman, 1970). The extent of infant activity at night in the wild is not well documented, but in captivity it may be considerable (Cercopithecus petaurista, Todt et al., 1982).

2. Efsects of Moonlight Bright moonlight appears to increase sensitivity to environmental stimuli (Altmann and Altmann, 1970; Rowell, 1972a; van Lawick-Goodall, 1968), and several activities seem to occur more during moonlit nights (Chivers, 1974; Haddow, 1952; Harrison, 1969; Lumsden, 1951; Rowell, 1972a; Vessey, 1973). Even group movements and foraging have been recorded in moonlight (Fittinghoff and Lindburg, 1980; Izawa and Itani, 1966; Stolz and Saayman, 1970; van Lawick-Goodall, 1968), but such gross activity is rare. [Glander (1975) reported late-night traveling in a group of howler monkeys, but did not mention phase of the moon.] Bert et al. (1975) found no effect of lunar phase on

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electrophysiological characteristics of sleep in baboons held in outdoor cages in Senegal. Possibly the captive conditions masked any effects of the moon. Neville ( 1968a) reported town-dwelling rhesus monkeys to be much more active at night than their forest-living counterparts; parts of the town remained lit up at night. It may also be noted that nocturnal bushbabies (Gcilago zanziharicus) in Kenya gave long-distance calls more during nights of a full moon than at other lunar phases and, along with a congeneric species (G. crassicaudcitiis), traveled more during a full moon (Nash, 1982).

2. Sociul lrztcraction mid Sex Some nocturnal activity is social. e.g., grooming and copulation, which may also be more frequent during moonlight (Sharman, 1981; Stolz and Saayman, 1970). Interestingly, such observations suggest that consort relations may persist during the night (Vessey, 1973). Packer (1979) recorded 12 copulations by a single adult male olive baboon one night; the male's possessive behavior probably meant that he went short of sleep. Adult male Guinea baboons followed estrous females in the sleeping tree in the morning (Anderson and McGrew, 1983). Clearly. opportunity for nocturnal sexual behavior will be influenced by the social organization of the group, as will the frequency of changing social partners. Vessey (1973) reported that sleeping clusters of rhesus monkeys tended to last for only about 1 hr during a full moon before breaking up. Sleeping clusters and other social aspects of sleeping are discussed in more detail in the following section. Those primates that produce spacing calls in the morning may occasionally give them during the night too. Groups of chimpanzees nesting within vocal range of each other may exchange vocalizations frequently throughout the night (Izawa and Itani, 1966; van Lawick-Goodall, 1968) and chest-beats may be given by adult males of neighboring gorilla groups (Schaller, 1963).

4 . Alerting to Prrdutors Although they may be relatively safe in their sleeping places, some primates give alarm calls or other vocalizations in response to nocturnal predators in the vicinity (Altmann and Altmann, 1970; Byrne, 1981; Hamilton, 1982; Hamilton and Tilson, 1982: Stolz and Saayman, 1970; Tutin et al., 1981). At first this may seem strange since such noise might attract a predator's attention. However, Byrne ( 1981) points out (as did Washburn, 1957) that regular sleeping sites of primates are likely to be well known to local carnivores. Byrne suggests that a function of choruses of loud vocalizations from the safety of the sleeping site might be "self-advertisement," i.e., a vocal show of strength in numbers to discourage a would-be predator from waiting around to try an attack at dawn. Viewed in this way, "exchanges" of volleys between groups sleeping at d ent sites could be a form of competition. each group making as much noise as necessary to dissuade the predator (Byrne, 1982). Byrne and Tutin et al. (1981)

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propose a testable hypothesis, namely, that self-advertisment should be a tactic used only by large groups with a number of adult males; individuals sleeping in smaller groups would do better to rely on quiet inconspicuousness. Indeed this might be the reason why Bert et al. (1975) observed no response to sounds of predators in caged Guinea baboons in Senegal. Data from Tilson and Tenaza (1976) suggest that the presence or absence of infants in the group might be a determinant of whether adult males give alarm calls or remain silent. In support of the idea that nocturnal volleys might serve an antipredator function in this fashion is the fact that they appear to be most characteristic of baboons, in whom large adult males acting in concert might provide some defense against threatening predators; it is the adult males who give the loud “wahoo” barks (Byrne, 1981; Reynolds, 1963).

VIII.

SOCIALASPECTSOF SLEEPING

A. THEGROUP Nighttime is a time of increased group cohesion in many primates. For example, the three members of a group of titi monkeys were rarely in physical contact except in the sleeping tree (Kinzey et al., 1977); the longest grooming sessions occurred on the sleeping bough before the members of a family group settled down to sleep (Kinzey and Wright, 1982). Vessey (1973) stated that the area over which a rhesus monkey group was spread at night was less than half of that observed during the day, and Angst (1975) made a similar observation in longtailed macaques. A troop of yellow baboons was more compact at the sleeping grove around dusk than at any other time (Altmann and Altmann, 1970). Groups of St. Kitts vervets showed increased cohesion shortly before settling to sleep, forming “supragroups” (McGuire et al., 1974); apart from instances of group fission, individuals always slept with the group at night. In contrast, Struhsaker (1967a,b) observed sleeping subgroups of vervets in Amboseli to be sometimes widely dispersed. The possibility of reliable differences between various populations remains to be investigated. Jay (1963) noted that while very old langurs might lag behind the rest of the group and show little social activity by day, they always slept with the rest of the troop at night. Mountain gorilla groups are more compact at night than during daytime feeding (Schaller, 1963). Subgroups of chimpanzees may either join or break off at dusk (Goodall, 1965), with sleeping parties often being larger near some rich food source (Goodall, 1962). Sleeping parties of both Guinea baboons and chimpanzees at Mt. Assirik, Senegal, are larger in the wet season than the dry season (Anderson and McGrew, 1983; Baldwin et al., 1981), but the precise reasons are not known. In some clear-cut cases, the aggregation of primates into large sleeping parties

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is accounted for by the localized, restricted distribution of sleeping sites (e.g., Haniadryas baboons, Kummer, 1968a,b; Guinea baboons, Sharman, 1981). Simonds (1974) suggested that groups of arboreal primates were more likely to sleep spread over a relatively wide distance than were more terrestrial primates. In support of this, neither Chalmers (1968) nor Waser and Floody (1974) observed a difference between day and night in the spread of members of groups of mangabeys (Cercacehus),Aldrich-Blake ( 1980) reported wide nighttime dispersal in long-tailed macaques, and Klein and Klein (1975) found no evidence for spider monkeys (Ateles belzeburh) congregating before settling to sleep. Members of a family group of gibbons may spend the night spread over an area of several hundred square meters (Chivers, 1972; Ellefson, 1974; Gittins, 1982; but see Tenaza, 1976; for Kloss gibbons). Woodland-living olive baboons were also widely dispersed at night (Ransom, 1981). In contradiction of Sirnonds’s ( I 974) hypothesis regarding arboreality and night dispersal, at night highly arboreal callitrichids and Callicebus monkeys usually form into one huddle composed of the members of their respective family groups (e.g., Kinzey ef al., 1977; Mason, 1968; Neyman, 1978; Robinson, 1979; Soini, 1982). In contrast to sympatric gibbons, members of a family group of siamangs usually spend the night in a single tree (Chivers, 1972, 1974; Gittins and Raemaekers, 1980). These cases indicate that the hypothesis should be modified to take account of the strong nighttime cohesion shown by these monogamous primates. It seems likely that nighttime dispersal of members of primate groups is at least partly a response to danger from predators. Increased cohesion and large sleeping congregations might facilitate detection of predators and group defense. An alternative solution, exemplified in the extreme by patas monkeys, is to take up solitary sleeping positions and remain inconspicuous. At night, members of a patas group may be dispersed over an area of 250,000 m2 (Hall, 1966, 1967). Struhsaker (1967b) also considered subgrouping at night as an antipredator pattern in vervets. The contrasting night-dispersal tendencies Df sympatric gibbons and siamangs might thus reflect different approaches to the same problem (Ellefson, 1974). B.

SUBGROUPING

Although the degree of nighttime cohesion of an entire group is a variable aspect of primate social organization, at a finer level of analysis increased cohesion at night can be seen in almost all cases, as sleeping subgroups form within the group. Subgrouping in east African vervets occurred on 51 of 52 nights (Struhsaker. 1967b). Even in the relatively widely spread gibbon or patas group, for example, mothers will sleep huddled with their infants (Chivers, 1972; Hall, 1967). Other types of subgroups form too, based to varying extents on intrasex-

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ual affiliations (examples: Anderson and McGrew, 1983; DuMond, 1968; Koyama, 1973), sexual relations, dominance, and kinship (Struhsaker, 1967b; see below). The development of an individual’s social sleeping arrangements generally corresponds with its social development within the group. With increasing independence, youngsters spend increasing amounts of waking time away from the mother but still return to sleep with her at night (Altmann et al., 1981; Chivers, 1971a; Gautier-Hion, 1970; Mohnot, 1978). “Senior groups” of immature gelada baboons formed during the day, but the members descended the sleeping cliff to join their respective natal one-male units in the evening (Mori, 1979). With increased maturity, a primate’s independence from the mother extends to staying away from her at night to sleep alone or with other juveniles and subadults (see Anderson and McGrew, 1983; Chivers, 1971a; Gautier-Hion, 1970; Struhsaker, 1967b). This seems to be particularly true for males. Kummer (1968a) observed groups of second-year juvenile and subadult male Hamadryas baboons to form sleeping groups on ledges apart from those occupied by onemale units. Juvenile male siamangs tend to sleep nearer the adult male than the adult female (Chivers, 1972). Among great apes, offspring may share the mother’s nest until up to 5 years of age, even if the mother has a young infant (Fossey, 1979; Goodall, 1979; Schaller, 1963; Horr, 1977). However, the tendency of a juvenile to sleep apart from the mother rises quite sharply with the birth of a younger sibling (Horvat and Kraemer, 1982), and there may be tantrums from the juvenile when its attempts to sleep with the mother are rebuffed (Horr, 1972). Young orangutans and chimpanzees have been observed to abandon their own nests and construct new ones nearer to their mothers (Horr, 1977; van Lawick-Goodall, 1968). One chimpanzee mother whose young infant died permitted her older son to sleep with her for 4 years after he was weaned (Clark, 1977). Some early reports on gorillas suggested that during the process of establishing separate nests, mothers and offspring constructed “amoeba”-shaped nests, with the juvenile’s nest eventually becoming fully detached (Bolwig, 1959; Kawai and Mizuhara, 1959). However, this has not been confirmed in subsequent studies (see Dixson, 1981). With the approach of adulthood, males often move to the periphery of the group during the day and continue to sleep at the edge of the group, or apart from it, at night (e.g., Chivers, 1972; Kawai et al., 1968; Neville, 1968b; Vessey, 1973). In Kloss gibbons, peripheral sleeping positions were taken up by mature offspring of both sexes (Tenaza, 1976). Eventually, emigration from the natal group occurs in most males, and resulting singletons or “bachelor groups” range and sleep away from main groups (e.g., Altmann and Altmann, 1970; Bourliere et al., 1970; DuMond, 1968; Hamilton and Tilson, 1982; Mori, 1979), sometimes in less favorable sites (Slatkin and Hausfater, 1976; Sugiyama et al., 1965). Adolescent and mature male chimpanzees (Kuroda, 1979; van Lawick-

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Goodall, 1968) and blackback male gorillas (Schaller, 1963) may also nest at the pcriphery of the group. Group fission. in which a subgroup containing both males and females breaks away from the original group, is also characterized by the gradual establishment of separate slccping sites by the two factions (Bourliere et d.,1970; Eiscnberg et ol., 1972; McGuire et d., 1974; Ransom, 1981). Indeed, Struhsaker ( 1967b) proposed that a basic tendency to form sleeping subgroups could facilitate the establishment of permanent separate groups in vervet monkeys. Examination of sleeping subgroups can thus reveal information about social dynamics (Fady. 1977: Southwick and Siddiqi. 1967; Vessey, 1973). Preferences for particular sleeping partners reflect affiliative relationships which are less obvious when the animals go about their waking business (Altmann, 1980; Ransom, 1981). The widely observed nightly return of young juveniles to their mothers and infant siblings clarifies the significance of matrilines in the organization of many primate groups (see Anderson and McGrew, 1983; Gautier-Hion, 1970. 1973: Green. 1978; Jay, 1965b; Vessey. 19731, while the cohesive sleeping huddles of callitrichids illustrate the strong nuclear familial pattern upon which these species’ social organization is based. The proximity of adult males to distinct subgroups of adult females illustrates the harem structures of gelada and Hamadryas baboons. Dunbar and Nathan (1972) found that the most frequent sleeping huddles in a group of Guinea baboons consisted of one adult male and one to two adult females with associated young. This was taken as support for the view that Guinea baboons show a harem-like reproductive system, but in a detailed study Anderson and McGrew ( 1983) did not replicate the finding and observed shifts by estrous females from one adult male to another. The reproductive organization of this species in the wild is not yet settled. Altmann (1980) found that preferred mating partners in a group of yellow baboons slept in the same sleeping subgrove. Consorting orangutans (Horr, 1972) and chimpanzees (van Lawick-Goodall. 1968, 1971) may nest close together, but do not share a nest (but see Kuroda, 1980, for a possible instance in pygmy chimpanzees). In a captive group of adolescent chimpanzees, some sleeping associations reflected consort relationships (Riss and Goodall. 1976). Given the evidence for sexual relations influencing social aspects of sleeping, it may be expected that the compositions of sleeping subgroups vary with the stage of the annual breeding cycle. Male-female consort pairs of rhesus were most likely to continue through the night in the breeding season (Vessey, 1973). During the birth season in a troop of squirrel monkeys, females with infants and attendant females slept in one area apart from the males (DuMond, 1968). Anderson and McGrew ( 1983) found seasonal differences in the frequencies of different types of huddling subgroups in Guinea baboons, but relationships with reproductive activity remain to be determined. Since in general data on sleeping

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habits are so scant, seasonal variation in patterns of subgrouping at night, and their significance, are hardly known. C. EFFECTSOF DOMINANCE

As discussed earlier, dominance relations can operate in the allocation of sleeping places to members of a group or between groups, which in turn may affect variables such as body temperature (Gaulin and Gaulin, 1982; Tollman, 1982). Dominance probably influences other aspects of sleep too. For example, Brain (1965) reported that the three dominant vervets in a group of seven regularly formed into one huddle at night while the four subordinate members formed another huddle, suggesting that the formation of sleeping subgroups might be partly based on rank. Infants of subordinate adult females in a captive group of pigtailed macaques tended to take longer to fall asleep than infants of dominant females (Reite et al., I976), possibly because subordinate mothers less readily achieve suitable social sleeping arrangements. Postures may also be affected: Kummer (1957, cited in Hediger, 1961) observed the dominant monkey to rest its chin across the nape of the huddling partner, whereas the subordinate placed its head on the chest of the partner, like an immature individual. Kummer also reported an inverse relationship between dominance rank and frequency of stirring during the night in four captive adult female Hamadryas baboons; the correlation persisted when the hierarchy changed. Such effects of dominance on sleep patterns have scarcely received any attention in the literature and deserve further study. It is not known, for example, whether total sleep time varies with dominance. Behavioral observations of artificially formed groups of juvenile stump-tailed macaques suggested that it does not (Chamove, 1982). A final effect of dominance to be considered here concerns selection of the sleeping site. It appears that the dominant silverback male of a gorilla group decides where and when the group should nest (Schaller, 1963, 1965), and one report suggests that he sites his nest toward the direction of a neighboring group (Elliot, 1976). A group of stump-tailed macaques on an island always slept in one particular tree (Estrada and Estrada, 1978). The death of the alpha male resulted in a shift of sleeping site, suggesting that this individual had been responsible for the previous choice of location. The question of who decides where to sleep, influencing the rest of the group, has not often been asked. In cases where the choice of sites is very restricted, the question loses importance, but where there are several sites, who chooses where to sleep might reflect a significant social role. There do not appear to be reports of shifts of sleeping sites by harem groups with new resident males (e.g., langurs). Conceivably, in many societies where the adult females constitute the stable core of a group and there is a marked turnover of males, it is the females who choose where the group will

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sleep (but see Jay, 1965b). In thc following section, the question of who initiates departure from the sleeping site in the morning as well as retiring in the evening will be considered further. One conclusion to emerge from the review of spacing patterns at night is that species. social organization, and environmental conditions are all influencing variables. In most groups of anthropoid monkeys, the pattern will typically be one of small huddles of animals interspersed with some solitary individuals, and in some cases certain aspects of the spacing are quite predictable. It is clear that "cohesion" at night can be considered at two levels: the group as a whole and subgroups within the group. Although many monkeys may be together in one sleeping tree (e.g., up to 65 in Pupiopnpio, Anderson and McGrew, 1983; up to 42 in M n c ~ ~fnsciculrrris, ca Wheatley, 1980), their subdivision into often distinct subgroups renders thc term "sleeping together" adequate only at a gross level of analysis (Haddow, 1952). D.

HUDDLESAND HEAT

To close the discussion of sleeping subgroups, huddles will be considered in terms other than purely social ones. Between 50 and 70% of a sleeping party of Guinea baboons slept in huddles, usually in groups of 2-3 (Anderson and McGrew, 1983; see also Dunbar and Nathan, 1972). Although there may be small species differences in mean size of huddles, this measure does not appear t o vary very widely across species: 2 (maximum 8) in bonnet macaques (Koyama, 1973), 2-3 in rhesus (Vessey, 1973), 1-5 in long-tailed macaques (Kurland. 1973), 2.7 (maximum 7) in talapoins (Gautier-Hion, 1970, 1973), 3-4 in niangabeys (Chalmers, 1968; Lumsden. 1951), 2-4 in chacma baboons (Hall, 1962; Stolz and Saayman, 1970). 2-3 (maximum 1 1 ) in spider monkeys (Klein and Klein. 1975). Of course, all the members of a family group of Callitrichids or Ctrllicehus monkeys commonly sleep in one bunch. Bertrand (1969). who gave a huddle size of 6-7 for stump-tailed macaques, suggested that the number of animals in a huddle could reflect the aggressiveness of a species; comparative studies remain to be done. It is also possible that the size of' huddles in groups reflects the number of members of various matrilines in the group. Although a family group of cotton-top tamarins usually slept in one huddle, there were two occasions on which the members split into two subgroups, possibly as a response to limited space (Neyman, 1978). It is reasonable to expect that size of huddles in other species might similarly be constrained-the end of a branch may only be able to support a given number of monkeys or apes. Hall ( 1962), studying chacma baboons, also considered that sleeping subgroups might be shaped by the physical characteristics of the sleeping site. Other ecological factors probably affect huddling. For example, the following

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authors have all suggested that monkeys huddle together to increase warmth or to conserve body heat: Altmann (1980, yellow baboons), Bertrand (1969, stumptailed macaques), Bishop (1979, common langurs), Chernyshev (1971, captive rhesus macaques), Dawson (1979, Geoffroy's tamarins), Erffmeyer (1982, captive rhesus), Gartlan and Brain (1968, vervet monkeys), Hall (1962, chacma baboons), Hamson (1983b, green monkeys), Schultz (1961, 1969), Suzuki (1965, Japanese macaques). Some illustrative examples follow: In mild weather a captive group of rhesus slept in two subgroups, one to each compartment of an outdoor box, but when the temperature dropped, the monkeys formed into one large huddle in a single compartment (Day et al., 1968). Wild rhesus monkeys typically slept in huddles of 2-6 in summer, but in huddles of 10-15 in winter (Southwick et al., 1965). Members of various groups of primates in outdoor enclosures were most often in proximity or contact with each other during rain or cold weather (e.g., Bernstein, 1972). The juvenile of a family group of siamang would be about 1 m away from the adult male when the observer left at dusk, but would always be found huddling with the male at dawn, which was the coolest time of the day (Chivers, 1974). Kummer et al. (1981) described huddling by Hamadryas baboons in response to an early morning temperature of 1O"C, and Gaulin and Gaulin (1982) described sleeping clusters as an adaptation to overnight temperatures of around 10°C in howler monkeys. Harrison (1962) observed a semiwild juvenile orangutan abandon its nest to huddle with another juvenile during a rainy night. The above reports suggest that primates use each other for warmth. Tollman (1982) used biotelemetry with captive vervet monkeys and found that body temperature fluctuated more in singly housed individuals than in group members. However, two studies that considered sleeping huddles in relation to temperature have found no effects. Vessey (1973) reported no difference in sizes of huddles of rhesus monkeys between winter and summer, despite a drop in minimum temperature of 5°C in winter. Anderson and McGrew (1983) found no effect of the lower night temperatures of the dry season on either the mean size of huddles or the proportion of the group huddling in Guinea baboons. In fact, there were indications of contrary trends, i.e., increased huddling in the wet season. Rahaman and Parthasarathy (1969) and Struhsaker (1967b) reported that bonnet macaques and vervet monkeys respectively huddled together during rain. Anderson and McGrew analyzed wet season huddling records for the occurrence of wet versus dry nights or early mornings, but huddling was not affected by this variable. Possibly in the studies by Vessey and Anderson and McGrew, the fluctuations in temperature were not extreme enough to affect huddling. Furthermore, in Guinea baboons troop size and sleeping party size are both larger in the wet season than the dry season (Anderson and McGrew, 1983; Sharman, 1981); this by itself may lead to more huddling activity in the wet season. One effect that did emerge, however, was that huddles tended to be slightly larger during

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strong winds, indicating a possible role of huddling in increasing stability in the sleeping tree. Roonwal and Mohnot (1977) pointed out that an infant monkey sandwiched betwccn its mother and another monkey was thus protected against the possibility of falling out of the sleeping tree. and Elliot (1913, cited in Haddow , 1952) appears to have suggested that monkeys hold onto each other in trees at night. but in general the possibility of huddling as a tactic to mutually increase stability during sleep has been neglected. To conclude, primates probably conserve heat at night by increasing physical contact with others. The mother as a source of heat and shelter for a sleeping infant is recognized (e.g., Altmann and Altmann, 1970; Baldwin and Baldwin, 1973; Harrisson, 1962), although changes in light levels alone may affect the degree of infant contact (Ainsworth and Baker, 1982). Adults are certain to know that they can obtain warmth from each other. However, most reports that consider huddles and heat at night lack good data, and adaptative aspects of social sleeping arrangements are not well studied. As a final example, Mukherjee and Saha ( 1974) reported that adult langurs (Presbytis peei) did not form sleeping huddles at night. It is not clear whether this reflects limited sampling, high intragroup tension, an antipredator tactic, or mild weather.

IX.

AWAKENING AND LEAVING THE SLEEPING SITE

In general, primates in the wild do not sleep late into the morning; as a rough guide it can be said that daily activity starts around dawn. Variations are discussed below. On awakening, many primates yawn, stretch, rub their eyes, scratch, and adjust postures. If they are wet, they may rub or shake the water off their coats (references to movement and activity upon awakening: Anderson and McGrew. 1983; Baldwin and Baldwin, 1972; Bertrand, 1969; Chivers et al.. 1975; Dawson, 1979; Defler, 1979; Estrada and Estrada, 1976; Rahaman and Parthasarathy, 1969; Roonwal and Mohnot, 1977; Rowell, 1972a; Simonds, 1974: Southwick et nl., 1965). Great apes may also stir (chimpanzees, Goodall, 1965; gorillas. Schaller, 1963), or even feed (orangutans, Harrisson, 1962; MacKinnon, 1974), and then lie down again in the nest. Some social behavior may occur in situ, but many groups of primates leave the initial bout of morning socializing until they have left their sleeping places. A.

EARLY CALLING

In several species, early morning calls are given from the sleeping tree. For example, dawn choruses by mantled howler monkeys were heard every morning, usually between dawn and sunrise (Baldwin and Baldwin, 1976). Sekulic (1982) gives reasons why howlers should engage in loud calling shortly after awaken-

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ing, including favorable sound transmission, fewer temperature constraints, and preventing neighboring groups moving in the direction of the caller(s). These factors probably also apply to the tendency of adult male gibbons and siamangs to give most morning choruses while they are still in the sleeping tree (e.g., Chivers, 1972; Gittins, 1982; Tenaza, 1976). Adult males of the monogamous langur Presybtis pofenziuni on Siberut Island do likewise (Tilson and Tenaza, 1982). Whitten (1982b) notes that predawn songs of male Kloss gibbons do not have to compete for audibility with the dawn choruses of birds and cicadas. In most of the above cases, singing is largely over by sunrise. During a full moon, “dawn” choruses may start up well before dawn (Baldwin and Baldwin, 1976; Sekulic, 1982), and departures may occur early (e.g., Anderson and McGrew, 1983; Stolz and Saayman, 1970). On the other hand, morning calling may be considerably delayed on cloudy or wet mornings (e.g., Carpenter, 1940; Chivers, 1969; Whitten, 1982b): On some cloudy mornings, siamangs fed before calling (Chivers, 1974). This inhibitory effect of bad weather on calling may be due to the primates being preoccupied with keeping warm, but it may also be related to the noise of wind and rain substantially reducing audibility of calls in the forest. As will be discussed below, weather conditions also affect more general activity of primates that have just woken up. To conclude discussion of early morning “spacing” calls, it should be noted that this behavior may extend to species not normally considered territorial. Rowel1 (1972a) suggested that barking by groups of forest-living baboons as they left their sleeping sites could serve to regulate the day’s travel path so that groups would avoid each other. Other examples are awaited. B.

ELIMINATION

A widespread habit among primates is to defecate and urinate shortly after they have woken up (e.g., Anderson and McGrew, 1983; Braza et al., 1981; Chivers, 1974; Dawson, 1979; Defler, 1979; Robinson, 1979; Roonwal and Mohnot, 1977). There appears to be slight variation in that some primates eliminate before leaving the sleeping place whereas others do it while moving off. However, elimination generally seems not to occur during the night, as Ellefson (1974) noted from the quantity and appearance of waste excreted by gibbons around dawn. Possibly, elimination is less likely at night because of the relatively low general arousal level then. When several members of a troop of langurs were disturbed during the night, urination and defecation occurred (Jay, 1965b). There may be more functional explanations. Normal primates as a rule do not like coming into contact with feces and will avoid it (Freeland, 1976). By not eliminating during the night, primates sleeping in tree holes or in dense tangles of vegetation thus avoid soiling the sleeping place, and members of a group sleeping at different heights in the canopy are unlikely to soil each other.

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Also, there is less disturbance for the individual concerned as well as for other group members. One other possibility is that continence at night reduces the chances of attracting predators. The ground below the sleeping place of a group of primates often accumulates a substantial quantity of feces and urine (e.g., Braza ez nl., 1981; Davidge, 1978a; Hall, 1962; Hausfater and Meade, 1982; Shaman, 1981), which can emit a strong odor (Davidge, 1978b; Poirier, 1972; personal observations). It is conceivable that the sound and odor of falling excreta could attract nocturnal predators to the presence of an otherwise inconspicuous party of sleeping primates. By waiting until morning, the primates deprive potential attackers of this source of information. While this may be true for some primates, it clearly does not apply to many others, as a group may continue to use very few sites over a long period despite the accumulation of excreta. Furthermore, a group of langurs was not discouraged from a regular sleeping site by the stench from rotting carcasses of cattle (Mohnot, 1971). Chimpanzees (Goodall, 1962, 1965; Nissen, 1931) and orangutans (Davenport, 1967; MacKinnon, 1974) eliminate shortly after awakening, either over the edge of the nest or shortly after leaving the nest. Davenport wrote that orangutans urinated through the nest, but this does not seem to be mentioned by other investigators. Only a sick chimpanzee may soil the nest (e.g., van LawickGoodall, 197 1). In contrast, in some groups of gorillas it is the norm to defecate inside the nest. The quantity and appearance of dung left in nests constitute evidence of the age and sex categories of the various members of a gorilla group and their sleeping arrangements. Gorilla feces are much more firm and fibrous than those of the more frugivorous chimpanzees (Dixson, 1981; Goodall, 1979). The latter author has considered the regional variations in the tendency to defecate in the nest and suggests that gorilla groups in colder regions may benefit from the insulating effect of lining the nest with feces.

C . W ~ A T H E RWARMING , UP,

AND

DEPARTURE

Shortly after awakening, many primates separate from their sleeping partners and move into positions for basking in the morning sun. Hamadryas baboons in Ethiopia would sit above their sleeping ledges first facing the early sun, then with their backs to it (Kummer, 1968a). Geladas in Ethiopia and Hamadryas in Saudi Arabia also sunned themselves before starting out on the day’s travel (Crook and Aldrich-Blake, 1968; Kummer er al., 1981). Several investigators have specifically characterized sunning as a method of warming up and drying out on cold and/or damp mornings [Hanuman langurs, Blaffer-Hrdy, 1977; green monkeys, Dunbar, 1974; orangutans, Harrisson, 1962; rhesus macaques, Lindburg, 1971; St. Kitts vervets, Poirier, 1972; rhesus, Schulz, 1969; Southwick ez a / . , 1965: chacma baboons, Stolz and Saayman, 1970; hoolock gibbons (Hylobates hool o c k ) , Tilson, 19791. Water vapor could sometimes be seen rising from the coats

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of sunning Kloss gibbons (Whitten, 1982a). McGuire et al. (1974) noted that St. Kitts vervets only sunned themselves on sunny mornings, which suggested that their taking up exposed positions did indeed reflect sunbathing rather than “sentinel” behavior. The one spot in an outdoor cage to catch the early morning sun was monopolized by the dominant male of a group of vervets (Tollman, 1982), and on Barro Colorado Island, Panama, sunning sites were a source of conflict between howler monkeys and turkey vultures (Cathartes aura) (Young, 1982). Some primates appear to select sleeping sites which facilitate basking in the early morning sun, e.g., northern langurs (Bishop, 1979; Boggess, 1980) and Japanese macaques (Furuichi et al., 1982). Baldwin et al. (1981) noted that by constructing nests open to the sky in the wet season, chimpanzees in Senegal could improve their exposure to the early sun. In contrast, Casimir (1979) analyzed nesting sites of gorillas at Mt. Kahuzi, Zaire, but found no evidence that nests were sited so as to be particularly exposed to the morning sun (see also Goodall, 1979). In many groups of primates, sunning may be combined with social activities including grooming, playing, and sex. In several of the above reports, prolonged “warming up” periods on cold or wet mornings resulted in the group’s departure from the sleeping site being delayed. While several authors have reported an overall correlation between time of astronomical sunrise and the start of a group’s activity (Anderson and McGrew, 1983; Chivers, 1974; Gibbons and Menzel, 1980; Gittins, 1982; Kummer, 1968a; Sigg and Stolba, 1981; Simonds, 1974; Vessey, 1973), initial movement from the sleeping area can be markedly delayed by rain or heavy cloud cover around dawn (some of the above references and Badrian et al., 1981; Braza et al., 1981; Carpenter, 1940; Hall, 1962, 1963; Klein and Klein, 1977; MacKinnon, 1974; Moynihan, 1976; Rowell, 1972a; Schaller, 1963; Soini, 1982). Van Lawick-Goodall (1971) has pointed out that primates might still be tired in the morning if they have lost sleep during a cold, wet night. This might also contribute to the start of the day’s activity being delayed. Moderate to heavy rain later in the day also generally suppresses activity (e.g., Altmann and Altmann, 1970; MacKinnon, 1974; Mittermeier, 1973; Nishida, 1980; Poirier, 1972; Starin, 1978; Whitten, 1982b). Delaying the start of the day’s travel means that the vegetation may have had time to dry out (Curtin, 1980; Dunbar, 1974), thereby reducing the degree to which the primates will get wet as they travel. However, the more general inhibitory effect of rain is not well explained in this way, and a soaking is also likely to result from staying put in a downpour. Some primates will make use of available shelter in such conditions, whereas others simply rely on postural adaptations to minimize discomfort. One reason for the common immobility of primates in a downpour is that there may be increased risks involved in traveling then. Arboreal routes may become slippery, and sounds become muffled. Interestingly, Poirier (1972; Poirier and Smith, 1974) suggested that strong wind reduced movement in the trees by St.

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Kitts vervets for similar reasons, and as noted earlier, winds may require primates to increase their efforts in maintaining stability in their sleeping places. It would be of interest to know whether strong wind per se delays early morning departure from the sleeping area in arboreal primates.

D. Ac-rrviTY BCDGETS Minimum temperature varies with season, as does the availability of food in many regions. Hall ( 1962) recognized the possible confounding effect of these factors in interpreting seasonal differences in time of departure from the sleeping site (olive baboons, see Aldrich-Blake et NI., 1971; Guinea baboons, Anderson and McGrew. 1983; siamangs, Chivers rt al., 1975; chacnia baboons, Davidge, 197%; rhesus macaques, Lindburg, 1971, and Makwana, 1978; Hamadryas baboons. Sigg and Stolba, 1981; chacmas, Stolz and Saayman, 1970; chimpanzees. van Lawick-Goodall, 1968). Harrison (1983b) found that green monkeys in eastern Senegal started feeding early in the late dry season when food was quite scarce, but interpreted this in terms of the monkeys avoiding having to forage in the middle of the day when the heat became intense. Other lines of evidence suggest that variation in foraging requirements influences the time at which primates leave the sleeping site. If there is plenty of food in the vicinity of the sleeping site, then feeding can start almost in situ without any traveling (e.g., squirrel monkeys, Baldwin and Baldwin, 1972; pigtailed macaques, Bernstein, 1968; orangutans, Davenport. 1967: chimpanzees, Goodall, 1965; orangutans, MacKinnon, 1974; black colobus. McKey and Watemian, 1982; and orangutans, Rodman. 1979). Rowell’s (1966)forest-living olive baboons also did this, which might have contributed to their being characterized as late risers. Dawson (1979) detected a direct effect of the previous day’s activity on unusually early or late starts in Geoffroy’s tamarins. Thus if foraging had ended very early the previous afternoon, the monkeys might start very early the following morning. In eastern Senegal, food for Guinea baboons became relatively scarce in the dry season. These baboons tended to leave their sleeping tree slightly earlier before sunrise in the dry season (Anderson and McGrew. 1983). Travel began earlier after a period of socializing, and foraging lasted longer in the dry season than in the wet season ( S h a m a n . 1981). Rasmussen ( 1979) found that yellow baboons left sleeping groves earliest during periods when they used large areas of their home range. but Sigg and Stolba (1981) observed no relationship between time of departure from the sleeping cliff and length of day range in Hamadryas baboons. Thus, while there seems likely to be an influence of foraging requirements on time of departure from the sleeping site (see Altmann and Altmann, 19701, corroborative evidence is still patchy, probably due to a lack of appropriate analyses rather than absence of a relationship. Cross-species comparisons in areas of sympatry are also of help in clarifying

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the relationship between time of starting the day’s activity and feeding requirements. Tilson and Tenaza (1982) reported that langurs (Presbytispotenziani) on Siberut Island left their sleeping trees on average 13 min before gibbons (Hylobates klossi). The earlier start by the langurs and their tendency to feed immediately meant that they achieved a substantial food intake before eventually being supplanted from the food trees by the dominant gibbons. This type of competition might be the reason for similar differences reported between leaf monkeys and siamangs on the Malay peninsula (see Chivers, 1973). Interestingly, gibbons are reportedly active about 30 min before siamangs (MacKinnon, 1977), but the difference does not appear to have been explained. Species differences in exit times are reported elsewhere, e.g., by Richard (1970, Alouatta villosa versus Ateles geofroyyi) and Lumsden (195 1, several species in Uganda), but consideration of such differences in terms of the species’ activity budgeting is lacking in general. A final example of differences in onset of activity in relation to interspecies competition concerns rhesus macaques and humans. Neville (1968a) noted that urban rhesus’ early morning activity peak took place before the streets became busy with people. As indicated earlier, the duration of the early morning “social” period characteristic of many groups, rather than time of becoming active, may be affected by ecological conditions (see Rowell, 1972a). Also, Chivers (1974) found a strong correlation between time of sunrise and time of first movement in siamangs, but not between the former and time of exit from the sleeping tree. These facts suggest that several measures might usefully be taken at sleeping sites in the morning, including the first sign of waking activity, first (and last) exit from the site, duration of socializing, and the time to reach some criterion of departure from the sleeping area. Analysis of the various measures would refine the search for relationships between ecological factors and the onset of early activities. In addition, it seems clear that time relative to sunrise is a better measure than absolute time, since time of sunrise varies through the year. The more meaningful measure has been used in several of the reports reviewed above, but not all. Of course, multiple criteria can also be used in regard to a group’s arrival at a site (e.g., Hall, 1962), and retiring for the night can be considered in relation to time of sunset. Thus, Kummer (1968a) found that while the onset of travel was systematically related to time of sunrise, retiring was not obviously related to time of sunset; the duration of the Hamadryas baboons’ daily march tended to be fairly constant. A final perspective on differences among primates in when they leave their sleeping sites comes from Simonds (1974). He suggests that in areas where crepuscular predators are a threat, primates may delay departure until the light is good (see also Hall, 1962) and that this might be the reason for the generally earlier onset of activity in arboreal, forest-living primates with less pressure from predators. The correctness of the assertion that forest primates are active earlier

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than open-country primates remains to be confirmed, but the hypothesis seems reasonable and could be tested by monitoring the degree of predator activity at study sites.

E.

SOCIAL ASPECTSOF LEAVING

The way in which a group of primates leaves a sleeping site can reveal something of roles in the group. For example, the first Guinea baboon to leave a sleeping tree was usually an adult male (Anderson and McGrew, 1983), which could be an antipredator arrangement in an area with many predators. Adult males were reported to be the first to move from their sleeping places in other studies of baboons (Buskirk et al., 1974; Davidge, 1978a,b) or the first to become active (Stolz and Saayman, 1970). In Davidge’s study area (Cape Point), there were no large carnivores, which suggests that the tendency of adult males to initiate movement away from the sleeping site could reflect a more general “leadership” role. Adult male olive baboons appeared to “suggest” possible directions of travel for the group, but the whole group moved only after an old female got up and followed one of the males (Rowell, 1972a). The silverback male of a gorilla group leads the progression away from the nesting site in the morning (Schaller, 1963). The first individual to become active in the morning is not necessarily the first to exit from the sleeping site, which indicates that the separate information should be recorded where possible. For example, Rowell (1972a) noted that juvenile baboons at Ishasha, Uganda, were the first to wake up, but definite moves away from the sleeping site were initiated by adults. Chivers (1974, 1976) reported that the adult male was usually the first to stir in a group of siamangs, but the adult female usually led the exit from the sleeping tree, and she was usually first to take up a nighttime sleeping position too. In some other studies of family groups of primates, it was the adult female who appeared to lead in either moving into sleeping position or moving away in the morning (Hylobates agilis, Gittins, 1982; Suguinus jitscicollis, Gibbons and Menzel, 1980; Cullicebus torquutus, Kinzey e l a l . , 1977; Kinzey and Wright, 1982). Our knowledge of the pattern and significance of such “leader” roles across primate species remains poor. The development of mother-offspring relations can clearly be seen in some cases when the group leaves the sleeping site. Before leaping out of the sleeping tree, adult female Guinea baboons always took small black infants ventrally, even if they had been riding dorsally beforehand (Anderson and McGrew, 1983); larger brown infants could stay on the mother’s back as she leaped, and some made the jump independently. Aduk female yellow baboons leave their 7- to 8month-old infants to descend from the sleeping tree alone (Altmann et al., 1981). This often elicits protest in the infant, and the two may compromise as the

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mother climbs back part of the way and waits (Altmann, 1980). By 9 months of age, infants are easily able to leave the tree by themselves, with only occasional falls. Individual circumstances such as injury (Shopland, 1982) or temperament (Goodall, 1962) and sickness (Goodall, 1983) also influence early morning behavior. Goodall reported that one adult female chimpanzee was consistently the last in a sleeping party to leave the nest and that with increasing age her infant left her increasingly early in the morning. Individual differences are clearly seen in many aspects of sleep in higher mammals (Webb and Cartwright, 1978). Analysis of behavior around sleeping sites combining both rigorous quantification and a less formal, more “individualistic” approach can therefore contribute more information then either method alone.

X. CONCLUDING COMMENTS From the review of the literature, it is clear that a number of basic questions can be asked about sleeping habits to advance the study of primate behavior. A few of them will be summarized here. In the field, besides plotting the location of sleeping sites, investigators might attempt to monitor the frequency and pattern of their use. Daily meteorological recordings are desirable, and use of the sites should also be considered in terms of the physical environment, e.g., distance from subsistence resources, the extent to which safety from predators, comfort, hygiene, vantage points, or simple “preference” appears important. Adaptation to short-term ecological fluctuations, e.g., in individual circumstances, weather, or foraging requirements, may also be manifested in terms of the subjects’ sleep patterns. Social roles and dynamics, both within and among groups, can also be illuminated by examining behavior around sleeping sites. In captivity, studies of sleep have been largely restricted to physiological investigations, especially electrophysiology. The results of such research are of limited value until they can be better related to the subjects’ lifestyle. An experimental ethological approach to certain aspects of sleep in primates could greatly improve the current state of knowledge about this important part of behavior. Hypotheses from the field could fruitfully be tested in captivity and vice versa. For example, characteristics thought to be influential in determining primates’ choice of sleeping sites in the wild, e.g., height, cover, visibility, accessibility, and temperature, could be systematically tested using captive subjects. Some work of this type has recently been reported by Clauss et al. (198I), who by manipulating the number, position, novelty, and material of potential sleeping boxes, showed that spatial position dominated familiarity with a particular box in the choice of sleeping places in a group of prosimian primates (Perodicticus potto). This approach could be extended, with an aim being to discover what

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aspects of the environment are psychologically relevant to the primates. Such research could have practical implications for the design of captive environments, a point made by Harrisson (1962) on the basis of tame orangutans’ responses to nesting materials and suggested by Bernstein’s ( 1962) observation that captive chimpanzees were never observed to sleep outside of nests which they had made. Also. in captivity schedules of food availability are controllable, permitting analysis of this variable on activity profiles including retiring and awakening times. Finally. social interaction is usually more easy to monitor in captive primates than in free-ranging ones. The question of who sleeps with whom is of considerable social significance in humans. Apart from mother-offspring relationships, this dimension of the social life of nonhuman primates remains poorly known. Acknowledgments I wish to acknowledge the encouragement and assistance of Dr W. C. McGrew, and the accommodation provided by Dr. A. S. Chamove

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Index

A

Cooperation and mating, 28-29 Copulation, see also Mating COSt of, 21-23 neuroendocrine functions of, 7-8 olfactory preferences and, 34-36 sensory regulation of, 34-37 sequence of, 3-6 temporal pattern of, 7-8

Adaptive radiation and development, 63-74 Aggression, 17.5- 176 Anechura bipunctatu, 59, 61, 73 Apes, 185, 189-192, see also Primates Army ants, 81-126 raiding intensity of, 106, 122 subfamilies of, 84-85 Attention, 136-142 Attractivity, 13

D

B Baby talk, 141, 148 Behavioral state, 130- 136 and conditioning, 134, 145-147 and gestures, 136 parental intervention and, 13.5 vectors of, 132-133 Brood-stimulation theory, 82, 85-88, 99- 120 tests of, 99-120

C Callow excitation, 87, 99-102 Causality, 143- 157 Cheliduru pyrenuica, 60 Chemical communication, 88-99 Climate, 60-61, 68-71 Cognitive integration attention and, 136- 142 behavioral state and, 130- 136 causality and, 143-157 perceptual organization and, 136- 142 self-awareness and, 143-157 Color vision, 137 Competition and mating, 21-26 Coolidge effect, 37-38

Dart-hop gait, 15, 18-19 Dermaptera, 51-80 Dialogue distance, 138 Dominance, 2, 21-26, 205-206 Dyadic interventions, 157-158

E Earwigs, 51-80 Eciton, 82-83, 84, 86-88, 89, 93 Eggs, presence of, 56-58 Ejaculation cost of, 11-13, 23 multiple, 31-33 optimal pace for, 7-8, 10-13 Ejaculatory latency, I 1 Ejaculatory series, 8-10 Emigrations of army ants direction of, 107-1 14 and food location, 107-114 frequency of, 114-120, 122 Equivalence classification, 137, 140 Eye contact, 138, 148, 151 Eye-to-eye distances, 138

F Facial expressions, 34, 38, 148, 151 Fasting, 53, 56-58 23 1

232

INDEX

Fetal bcha\ior. 143 50-kHz call. sre Ultrasonic calls Font Romcu. 60-65. 71-73 Food abundance. 114-120. 122 Food location. 107-1 I4 F'rwifit.idu airricirliiria. 5 2 . 55. 58-74

G Greeting rcspon\e. 148

H H e d turning. 134. 145-147 Heat. 196-197, 206-308 Hormones. 55-58 Huddles. 197. 206 -208

competition for, 21-26 in complex environment. 15-17, 32 cooperation and. 28-29 social structure of, 20-3 I Microanalysis of social interaction, 130 Monkeys. 188-189, see ulso Primates

N

Naturalistic observation. 127- 129, I37 Neitamwne.r nigresc'ens. 83, 84, 88. 93. 94 Nesting habits of great apes. 185, 189-192 Nocturnal activity, 198-201 Nomadic behavior in army ants, 82, 85-88 onset of, 99-102 Nomadic-phase length, 102- 103 Nonverbal communication. 139- I40

1

imitation.

.we Parental imitation

Infant looking, 130 Infants. human. 127-163 Intorination processing. 158 Instrumental learning. 146 Interception by female rats. 19, 25-26 Introniishion\ nlultlple. 6. 31-33 optimum intervals for. 7. 10- I 1 pacing of, 7. I!. 21-23

L L d d u r t r riptrria. 5 3 , 54, 55. 57-59. 73

Larval stimulation. 102-103 Learning and cognition. 127- 163 Lordosis roponse. 13. 15. 19

M hlass recruitment. 88-99 chemical basis of, 93 ecological aspects of. 94-98 multiple use of. 98 hlattng. 1-49 choice of mate, 26-28

Observational distance. 138 Ontogeny, 51-52

P Pace. 60-63, 64-73 Panogamy, 5 . 38-41 Parental behavior. 5 1-80 adaptive radiation of. 58-63 development of. 52-58 ethological approach to. 52-55 control of, 56-58 hormones and, 55-58 physiological correlations of, 55 Parental imitation, 15 1 Pattern perception. I37 Perceptual organization, 136- 142 functions of, 137 pattern perception studies, 137 Plahticity. 5 1-80 Postejaculatory quiescience in femaie rats. 18, 19-20, 24, 27 in male rats. 6. 24, 33-34 Predation. 71. 94, 168. 176, 177-182. 193. 195. 200. 202, 210. 213 Primates. 165-229 communication among, 186-187, I89 group cohesion among, 201-202

233

INDEX

subgrouping of, 202-205 vocalizations of, 186-187, 199, 200-201, 208-209 Proceptivity, 13, 18-19 Progestational state, 7-8, 18, 32 Prosody, 140- 141, 148 Prototypicality. 137, 140, 153

R Radiation, 52 Raiding, 106, 122 Rats domestic, 1-49 gait of, 13-15 ultrasonic calls of, 4, 18, 33, 36-37 wild Norway, 15, 39-41 Receptivity, 13 Recruitment overrun, 93, 97-98

S Security, 188-194 Self-awareness, 143-157 Sexual selection at group level, 2, 29-31 intersexual, 26-28 intrasexual, 21-26 Sleep, 165-229 moonlight and, 195, 199-200 postures, 196-198 social aspects of, 201-208 Sleeping sites arrival at, 194-196 awakening at, 208-215 availability of, 168 avoidance of, 193 characteristics of, 177-187 comfort of, 182- 186 competition for, 174-177 concealment of, 179 departure from, 208-21 5 destruction of, 175 distribution of, 170-172 early calling from, 208-209 elimination at, 185, 209-210 familiar, 192- 194 food and, 169-170 of great apes, 185

group size and, 170-172 height of, 178-179 inaccessibility of, 177-182 as information centers, 186- I87 as a limiting resource, 170-174 location of, 166- I70 of monkeys, 188-189 number of, 167-170 odor and, 185 and predators, 168, 176, 177-182, 193, 195, 200, 202, 210, 213 preferred, 167 and ranging patterns, 167- 168, 172- 174 and security, 188 sharing of, 174-177 traditional, 188- 194 water sources and, 170 weather and, 182-184, 210-212 Solicitation by female rats, 6. 13-!9, 25-26, 37 components of, 13- I7 function of, 17-18 Somatosensory perception, 143 Sperm transport, 10, 18, 24, 27, 32-33

T Trail following, 88-93 22-kHz call, see Ultrasonic calls Twins. 158

U Ultrasonic calls, 4, 18, 33, 36-37 Urination, in rats, 4, 33, 35-36

V Vitellogenesis, 53, 55 Visual behavior of infants, 139-140 Vocal matching, 151

W Waking activity, 133 Waking states, 133, 135

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Contents of Previous Volumes Volume 1

Volume 3

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

Behavioral Aspects of Homeostasis D. J. McFARLAND 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 The Study of Visual Depth and Distance Perception in Animals RICHARD D. WALK Physiological and Psychological Aspects of Selective Perception GABRIEL HORN Current Problems in Bird Orientation KLAUS SCHMIDT-KOENIG

Ontogenetic and Phylogenetic Functions of the Parent-Offspring Relationship in Mammals LAWRENCE V. HARPER The Relationships between Mammalian Young and Conspecifics Other Than Mothers and Peers: A Review Y. SPENCER-BOOTH Tool-Using in Primates and Other Vertebrates JANE VAN LAWICK-GOODALL Author Index-Subject Index

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

Volume 4

Author Index-Subject Index

Volume 2

Constraints on Learning SARA J. SHETTLEWORIH

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 Index-Subject Index

Author Index-Subject Index

235

236

CONTENTS OF PREVIOUS VOLUMES

Volume 5

Volume 7

Some Neuronal Mechanisms of Simple Behavior KENNETH D. ROEDER

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

The Orientational and Navigational Basis of Homing in Birds WILLIAM T. KEETON

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

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

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 Life History of Male Japanese Monkeys YUKIMARU SUGIYAMA

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

Feeding Behavior of the Pigeon H. PHILIP ZEIGLER

Author Index-Subject Index

Subject Index

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

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

Volume 9 Attachment as Related to Mother-Infant Interaction MARY D. SALTER AINSWORTH Feeding: An Ecological Approach F. REED HAINSWORTH and LARRY L. WOLF Progress and Prospects in Ring Dove Research: A Personal View MEI-FANG CHENG Sexual Selection and Its Component Parts, Somatic and Genital Selection, as Illustrated 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

Subject Index

Volume 10 Learning, Change, and Evolution: An Enquiry into the Teleonomy of Learning H. C. PLOTKIN and F. J. ODLING-SMEE Social Behavior, Group Structure, and the Control of Sex Reversal in Hermaphroditic Fish DOUGLAS Y,SHAPIRO Mammalian Social Odors: A Critical Review RICHARD E. BROWN

237

JAY S. ROSENBLATT, HAROLD I. SIEGEL, and ANNE D. MAYER Subject Index

Volume 11 Interrelationships among Ecological, Behavioral, and Neuroendocrine Processes in the Reproductive Cycle of Anolis carolinensis and Other Reptiles DAVID CREWS Endocrine and Sensory Regulation of Maternal Behavior in the Ewe PASCAL POINDRON and PIERRE LE NEINDRE The Sociobiology of Pinnipeds PIERRE JOUVENTIN AND ANDRE CORNET Repertoires and Geographical Variation in Bird Song JOHN R. KREBS and DONALD E. KROODSMA Development of Sound Communication in Mammals GUNTER EHRET Ontogeny and Phylogeny of Paradoxical Reward Effects ABRAM AMSEL and MARK STANTON Ingestional Aversion Learning: Unique and General Processes MICHAEL DOMJAN The Functional Organization of Phases of Memory Consolidation R. J. ANDREW

Index

Volume 12

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

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

Progress in the Study of Maternal Behavior in the Rat: Hormonal, Nonhormonal, Sensory, and Developmental Aspects

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

238

CONTENTS OF PREVIOUS VOLUMES

Visceral-Somatic Integration in Behavior, Cognition, and “Psychosomatic” Disease BARRY R. KOMlSARUK Lariguagc in the Great Apes: A Critical Review CAROLYN A. RISTAU and DONALD ROBBINS In&

I

Volume 13 Cooperation-A Biologist’s Dilemma JERRAM L. BROWN Determinants of lnfant Perception GERALD TERKEWITZ. DAVID I LEWKOWICZ. and JL‘DITH M. GARDNER

Observations on the Evolution and Behavioral Significance of “Sexual Skin” in Female Primates A . F. DIXSON Techniques for the Analysis of Social Structure in Animal Societies MARY CORLISS PEARL and STEVEN ROBERT SCHULMAN Thermal Constraints and Influences on Communication DELBERT D. THIESSEN Genes and Behavior: An Evolutionary Perspective ALBERT0 OLIVER10 Suckling Isn’t Feeding, or Is It? A Search for Developmental Continuities W. G. HALL and CHRISTINA L. WILLIAMS in&r