This article was downloaded by: [Memorial University of Newfoundland] On: 10 March 2015, At: 15:59 Publisher: Routledge Informa Ltd Registered in England and Wales Registered Number: 1072954 Registered office: Mortimer House, 37-41 Mortimer Street, London W1T 3JH, UK
The Journal of General Psychology Publication details, including instructions for authors and subscription information: http://www.tandfonline.com/loi/vgen20
A Phylogenetic Perspective for Social Behavior in Primates a
Bill Seay & Nathan W. Gottfried
a
a
Louisiana State University , USA Published online: 06 Jul 2010.
To cite this article: Bill Seay & Nathan W. Gottfried (1975) A Phylogenetic Perspective for Social Behavior in Primates, The Journal of General Psychology, 92:1, 5-17, DOI: 10.1080/00221309.1975.9711323 To link to this article: http://dx.doi.org/10.1080/00221309.1975.9711323
PLEASE SCROLL DOWN FOR ARTICLE Taylor & Francis makes every effort to ensure the accuracy of all the information (the “Content”) contained in the publications on our platform. However, Taylor & Francis, our agents, and our licensors make no representations or warranties whatsoever as to the accuracy, completeness, or suitability for any purpose of the Content. Any opinions and views expressed in this publication are the opinions and views of the authors, and are not the views of or endorsed by Taylor & Francis. The accuracy of the Content should not be relied upon and should be independently verified with primary sources of information. Taylor and Francis shall not be liable for any losses, actions, claims, proceedings, demands, costs, expenses, damages, and other liabilities whatsoever or howsoever caused arising directly or indirectly in connection with, in relation to or arising out of the use of the Content.
Downloaded by [Memorial University of Newfoundland] at 15:59 10 March 2015
This article may be used for research, teaching, and private study purposes. Any substantial or systematic reproduction, redistribution, reselling, loan, sub-licensing, systematic supply, or distribution in any form to anyone is expressly forbidden. Terms & Conditions of access and use can be found at http://www.tandfonline.com/page/terms-and-conditions
The Journal of General Psychology, 1975, 92, 5-17.
A PHYLOGENETIC PERSPECTIVE FOR SOCIAL BEHAVIOR IN PRTMATES*
Downloaded by [Memorial University of Newfoundland] at 15:59 10 March 2015
Louisiana State University
BILL SEAY
AND
w.GOTTFRIED
NATHAN SUMMARY
Three selected groups of studies of primate social behavior and development are discussed. In the first group of studies the social development of rhesus monkeys reared in different environments is considered. Rhesus show remarkable similarity in behavior in diverse environments, demonstrating a phylogenetic set to develop species-typical behavioral repertoires. The second set of studies reports on three species (Macaca mulatta, Macaca fasicularis, and Erythrocebus patas) reared in similar settings. Species differences observed in these settings were a result of phylogenetic set. Finally, mother-infant separation studies conducted with several monkey species are reviewed. The results of these studies were interpreted to be the product of interactions of the species-typical behavior and social organization of each species, the specific setting or apparatus used, and the independent variable manipulation employed. Caution is recommended in cross-species generalization within primates. A.
INTRODUCTION
This paper presents a perspective from which to view the findings of the many recent research reports concerning primate social behavior and development. No attempt will be made to provide a comprehensive review of this vast literature. Instead, three selected sets of studies will be considered, and a conceptual framework abstracted from these data. The concept, phylogenetic set, provides a descriptive term for some phenomena evident in primate social behavior. Phylogenetic set is the tendency to develop species-typical behaviors. Every organism shares with other members of his species genetic characteristics which influence his
* Recommended by John Horrocks of the Editorial Board, and received in the Editorial Office, Provincetown, Massachusetts, on January 29, 1974. Copyright, 1975, by The Journal Press. 5
Downloaded by [Memorial University of Newfoundland] at 15:59 10 March 2015
6
JOURNAL OF GENERAL PSYCHOLOGY
behavior. These characteristics do not determine behavior, but certain behavioral traits are probable consequences of normal development in any given species. The expression of phylogenetic set requires interaction with some environment. The influence of phylogenetic set is indicated when species-typical behavior developes in organisms subjected to different environments during development. Failure to develop species-typical behavior in some particular environment does not necessarily indicate that phylogenetic set is not involved in the normal development of that behavior. It is presumed that the expression of phylogenetic set may be blocked or modified in individual organisms. This would occur when the organism encounters environments in which salient features differ markedly from environments typically encountered by members of the species. In the first group of studies, the development of social behavior of a single species, the rhesus monkey, is examined in a number of different early environments. As will be seen, this species exhibits unexpectedly low variability in development across environments, demonstrating a phylogenetic set to develop similar social behavior repertoires in a wide variety of environments. The second group of studies deals with three species reared in identical environments. These species show species-specific developmental trends, thus demonstrating phylogenetic set when environmental factors are held constant. The third selection of studies includes a number of mother-infant separation studies. In these separation studies apparatus and procedure interact with the experimental treatment in different ways for different species, demonstrating the influence of phylogenetic set on the effects of an apparently simple experimental manipulation. Before considering the behavioral data, it may be well to consider the subject species most frequently used in studies of monkey social behavior and development. A recent bibliography concerning social behavior in macaques, baboons, and patas monkeys provides an example of the popularity of the rhesus monkey. In this list, which was prepared by the Primate Information Center of the University of Washington Primate Research Center at the authors’ request, 168 titles refer clearly to rhesus monkeys. The pigtailed macaque, Macaca nemistrina, was the next most frequently studied macaque with 36 titles. All baboon species combined were indicated in only 40 titles. The rhesus monkey, Macaca mulatta, is native to northern and central India, and lives in a wide variety of habitats across this range. In one
Downloaded by [Memorial University of Newfoundland] at 15:59 10 March 2015
BILL SEAY AND NATHAN W. GOTTFRIED
7
sense, Macaca mulatta can be said to have no single natural environment. It lives in forests, small towns, and large.cities, adapting successfully to these complex and demanding environments. Rhesus monkeys are social animals, living in troops with fairly clear dominance hierarchies among adults, forming moderately stable social organization within the troop. One goal of research in the social behavior and development of rhesus monkeys has been a search for principles sufficiently general to enhance our understanding of human social development. Therefore, some comparisons between rhesus monkeys and human beings may be in order. One striking difference between these species is the relative physical maturity of the rhesus infant at birth. At the age of two or three days an infant rhesus monkey can locomote; by two or three weeks of age his motor development appears to be free of reflexive control under most conditions. A second difference between infant humans and infant rhesus monkeys is the amount of physical contact between mother and neonate. The rhesus monkey infant remains closely attached to the mother’s ventral surface almost constantly for several weeks. It sleeps in close ventral contact with the mother for nearly a year. Infant-mother contact in our society contrasts sharply with this pattern. Even in societies where the infant is carried by the mother for a large part of the day, a cloth sling, cradle board, or a similar device serves to reduce intimate physical contact with the mother. Other differences between human and rhesus infants could be mentioned, but these two characteristics are sufficient to suggest the need for considerable caution in generalizing from one to the other. As will be seen below, even among monkey species one cannot necessarily make reliable predictions from one species to another.
B. RHESUS SOCIALDEVELOPMENT The first group of investigations to be considered here deals with the most familiar example of research in primate social behavior. At the University of Wisconsin Primate Laboratory rhesus monkeys have been reared in a variety of early environments (10). Observation of socially restricted monkeys throughout their life span has been a primary source of information concerning primate social development. These studies will be viewed as an example of the evaluation of the effects of environmental manipulation in a single species. When rhesus infants are separated from their mothers at birth and subsequently housed alone, their social behavior is markedly affected. The
Downloaded by [Memorial University of Newfoundland] at 15:59 10 March 2015
8
JOURNAL OF GENERAL PSYCHOLOGY
duration and extent of disruption of species-typical social behavior depends on the duration and extent of restriction. In the first reports of socially restricted animals, Mason (13, 14) studied a group of juvenile rhesus monkeys which had been allowed to see and smell, but not touch and manipulate conspecifics in the same condition. Their behavior was compared to that of wild-born animals of about the same age. Mason’s restricted group was hyperaggressive, exhibited disoriented and infrequent sexual behavior, engaged in little play, and rarely groomed other animals. As adults, animals reared in similar situations continued to exhibit aberrant behavior to the extent that no males, and only about half of the females reproduced (10). Socially restricted females impregnated by wildborn males are unlikely to care for their first infant (3, 21). More severe restrictions of social stimulation have proved to have even more debilitating results (9). If infant rhesus monkeys are prevented from seeing or touching other members of their own (or any other) species for a year after birth, they are almost totally socially incompetent. They are not only incapable of social interaction, but are incapable of defending themselves, or even effectively retreating from hyperaggressive peers. One would predict that these animals, like the less severely restricted monkeys discussed above, would be unlikely to achieve adult reproductive and maternal competence. These dramatic disruptions of social behavior are the most striking results of the series of early experience manipulations conducted in the Wisconsin Research program. This paper will focus on some less dramatic, but intriguing results of those investigations. Infant monkeys have been reared in a number of other situations in the Wisconsin Lab. One group of infants was singly housed, but permitted to play with identically housed conspecifics for 15-30 minutes a day (16). Another group was housed in home cages of a four-unit playpen apparatus and confined to a home cage and adjacent play cage for 22 hours each day (7). This group of infants was permitted to interact with conspecific age mates for two hours each day. A number of rhesus infants have been reared in a so-called “togethertogether” situation in which two to four infant monkeys are housed together from birth (2). Still other infants were permitted to stay with their mothers, at least for the first six months of life (7, 19). Some mother-reared animals were permitted to play with other infants from birth, (7, 19), while others interacted exclusively with their mothers (1). These mothers were, in some cases, maternally adequate wild-born females (7, 19) and, in others, brutal or indifferent “motherless mothers” (3, 21). These diverse social and
BILL SEAY AND NATHAN W. GOTTFRIED
9
Downloaded by [Memorial University of Newfoundland] at 15:59 10 March 2015
physical environments result in the development of strikingly similar behavioral repertoires in rhesus monkeys.
C. COMPARATIVE STUDIES Formal comparisons of two or more groups of these variously reared animals have revealed few differences in social behavior and development. For example, when the infants of brutal or indifferent mothers were compared with those of adequate mothers, few differences were evident (21). Abused infants were somewhat slower in developing contact or rough-and-tumble play, but by six months of age no differences were seen. Chasing play was somewhat less frequent during the first six months of development for the abused infants. Despite this difference in frequency, the behavior pattern was identical to that seen in adequately mothered infants. Infants reared by their mothers, but deprived of peer experience for four or eight months were compared to those who had both peer experience and maternal care (1). The peer-deprived infants were somewhat more aggressive than the peer-experienced monkeys. However, both groups showed similar patterns of play and sexual behavior. Furthermore, species typical group structure developed in both groups. In another investigation (19) two groups of peer-experienced, motherreared infants were compared with a group of surrogate-reared, peerexperienced infants. Differences between the two mother-reared groups were more extreme than between either mother-reared group and the surrogate-reared animals. If an experienced primatologist were to classify the animals on the basis of the data, he would select as normal one mother-reared group and the surrogate group. The remaining motherreared group would be classified as unusual. However, all three groups of animals exhibited competent, species-typical behavior with few consistent differences among the groups. A final study illustrates the persistence of species typical development in a variety of social environments (2). Four groups of infants were compared: one group was reared with surrogate mothers, but denied contact with other monkeys for the first six months of life; in the second group, animals were reared together in one cage for six months; monkeys in the third group were reared with inadequate mothers but given peer experience; animals comprising the last group were reared by adequate mothers and had access to age-mates. Only the s o c i d y restricted animals showed consistent differences from any other group. The peer-deprived,
Downloaded by [Memorial University of Newfoundland] at 15:59 10 March 2015
10
JOURNAL OF GENERAL PSYCHOLOGY
surrogate-reared monkeys were clumsy, avoided prolonged physical contact with other monkeys, and showed inadequate sexual behavior. However, after prolonged social experience, they achieved comparable levels of play and developed typical group structure. Recent research at the University of Wisconsin indicates that animals reared in total isolation for six months retained the capacity for speciestypical social behavior if provided with younger normal peer “therapists” at the end of the period (8). By age one year, after six months of treatment, the isolates showed nearly normal levels of exploratory, locomotor, and play behavior. It is evident that a number of early environments may serve as an adequate experiential basis for species-typical social development in the rhesus macaque. In fact, only bizarre and restrictive environments disrupt the development of appropriate patterns of group structure, play, and sexual behavior. With few exceptions, the development of social behavior involving particular play patterns, specific sexual behavior patterns, and a degree of social organization is a highly probable result of maturation in the rhesus. Relative environmental independence is also shown in the data just reviewed. These data suggest that macaque social development resists all but the most extreme environmental pressures. The evidence does not support the interpretation that animals with different histories do not differ in the frequencies with which various social behavior patterns are displayed. Nor can it be said that animals with species-typical social behavior repertoires will be free of abnormal or atypical behaviors (6). These results present characteristics for which an adequate label is not available. The term phylogenetic set has been coined to provide such a label. A phylogenetic set is a probabilistic tendency for an organism to develop species-typical behavior. By virtue of its membership in a species, an organism is possessed of a gestalt of reflexes, neuromuscular structures, perceptual capacities, and learning dispositions, which determine the probability of specific aspects of behavioral development. Across many environments, almost identical behavioral repertoires develop in conspecific animals; only in extremely unfavorable environments will the behavioral repertoire of the species fail to appear. Furthermore, even the organism maturing in an environment inadequate to support species-typical behavior will not develop unique techniques for coping with that environment. Rather, his behavioral repertoire will consist of fragments of the behavior patterns which ensure individual and species survival for most of his species-mates.
Downloaded by [Memorial University of Newfoundland] at 15:59 10 March 2015
BILL SEAY AND NATHAN W. GOTTFRIED
11
D. SPECIESCOMPARISONS In the previous sections, we have discussed the influence of diverse environments on members of a single species. The second set of observations to be considered involves three species reared in similar settings. Infant monkeys were reared by their own mothers in the home cage of a playpen apparatus. The infants, but not the mothers, had access to an adjacent play area via a small opening in the cage wall. For a short time each day, infants were permitted to interact with other infants similarly housed. Mother reared rhesus infants in this environment have been studied by a number of investigators (e.g., 1, 7, 19). The earliest appearing play pattern for the species is rough-and-tumble or contact play which may be described as play fighting. Developing somewhat later, a second pattern of chasing or approach-avoidance play is frequently seen. During the first six months of life in the playpen situation, rhesus monkeys show behavioral sex differences characterized by male infants, more than females, engaging in social approaches, threats, rough-and-tumble play, and pelvic thrusting. Females more frequently withdraw and exhibit passivity or rigidity to social or physical stimulation. Aware of the tendency to generalize research results based on rhesus macaques to all primates, investigators at Louisiana State University (LSU) have studied the normative development of two other species in the playpen apparatus. The common or crab-eating macaque or cynomologous monkey, Macaca fascicularis, was selected to provide comparable data from a related macaque species. This macaque, which will be called the cynomologous monkey throughout this paper, is a somewhat smaller animal than the rhesus, and is found across a wide range in coastal areas of Southeast Asia. The behavior of cynomologous monkeys observed in the playpen apparatus is essentially identical to rhesus monkeys reared in similar conditions (23, 24). Indices of the mother-infant relationship, such as nursing or ventral contact, dropped sharply with increasing infant age. Physical contact with age-mates appeared early and persisted across the six-month period of study. Play fighting appeared early and seemed to be an important play pattern for cynomologous monkeys. Sex differences in social behavior, similar to those reported for rhesus macaques, appeared during the first six months of development. It would be reasonable, then, to generalize from laboratory studies of the rhesus monkey to laboratory studies of the cynomologous monkey. The similarity of maternal, filial, and peer-directed social behavior patterns
Downloaded by [Memorial University of Newfoundland] at 15:59 10 March 2015
12
JOURNAL O F GENERAL PSYCHOLOGY
between these two species is evident. Manipulations of the early environments of cynomologous monkeys would be expected to produce effects at least grossly similar to those reported for the rhesus macaque. Bear in mind that the two species are closely related members of the same genus. Indeed, some authorities consider cynomologous and rhesus monkeys to be subspecies of a single species. The other species observed at LSU was Erythrocebus patus, the hussar or African red monkey. The patas monkey is closely related to the circopithecus genus and is sometimes classified Circopithecus patas. Its typical behavior differs from that of most circopithecus monkeys in that most of its waking hours are spent on the ground; it is a rather clumsy tree climber. This savannah dweller lives in single male groups, with a clear female dominance hierarchy. Groups of pat& monkeys are widely separated from one another in the wild. Individuals usually maintain greater distances from other group members than do most macaques. One unique characteristic of the species is that it is probably the fastest moving primate, reported to attain speeds of 35-40 mph over short distances. The development of patas social behavior in the playpen setting presents contrasts to that of the macaque (23). The most pervasive differences have to do with infant physical contact. When a four-month-old macaque infant ventures out of his home cage into an open play area, another infant joins him despite the protests and interference of his mother. In contrast, a four-month-old patas infant in an open play area is seldom joined by another infant. When a second infant enters the play area, the first infant returns to his mother’s cage. Physical contact between patas infants was relatively infrequent throughout the first six months of life. The most frequent form of infant play observed in young patas monkeys was noncontact and chasing play; contact play or play fighting was infrequently seen. The mother-infant relationship in patas monkeys is complementarily different from that of macaques (24). Rhesus and cynomologous mothers are somewhat intolerant of manipulation of their body by their infants, often reacting to unpleasant exploratory or play fighting responses by hitting or biting their infants. At the same time, they frequently permit long as these infants other than their own to come into their cage-as infants are not overactive or overaggressive. Patas mothers, on the other hand, are tolerant of personal insult by their own infants, either not reacting at all or reciprocating elements of play fighting. However, patas monkey mothers will not tolerate another patas infant in the home cage. Patas infants in the playpen situation go into the wrong home cage only
Downloaded by [Memorial University of Newfoundland] at 15:59 10 March 2015
BILL SEAY AND NATHAN W. GOTTFRIED
13
once. Physical contact between patas mother-infant pairs is also somewhat different from the macaque pattern. Even while nursing, the patas infant is less likely than a macaque infant to have a major part of his body surface directly touching the mother. This is, no doubt, a partial consequence of the long-limbed, rangy, physical structure of the patas. These data suggest that the rhesus monkey is not a representative primate. It is intriguing to consider to what extent our current ideas about primate social development have been determined by the selection of Macaca mulatta and other macaques as experimental subjects. One would be hesitant, indeed, to predict that the effects of peer and maternal deprivation would be identical for patas and rhesus monkeys. The possibility of early experience research with various monkey species is an exciting one. What is evident from these comparisons of three species in comparable environments is that the species of an organism is a partial determinant of his reactions to an environment. Phylogenetic set accounts for species differences in behavior when environments are consistent across species.
E. MATERNAL SEPARATION STUDIES A final group of studies illustrates an experimental manipulation evaluated across species and environments. In these studies infant monkeys are separated from their mothers. The behavior of the infants is observed before and during separation and after reunion with the mother. Of particular interest is the similarity of reactions of macaque and human infants and juveniles to mother-infant separation. The first studies of rhesus monkey mother-infant separation were conducted in the playpen apparatus (20, 22). Two separation techniques have been employed. In one study infants were trapped in the play cage where they could see and hear their mother throughout the three-week separation. In an alternative, somewhat cleaner, procedure the mother-infant pair were removed from the apparatus, separated, and the infant only was returned to the home cage. In both procedures, the infant’s initial reaction was similar. After separation from the mother, infants scampered about the cage, screamed, and defecated. This violent emotional reaction exhibited by the rhesus was similar to the protest stage of a human child’s reaction to maternal separation, as described by Bowlby (4, 5). After a day or two, the infants settled down, but their peer-directed social behavior was influenced by the mother’s absence. Play, typical in six-month-old macaques, almost disappeared. Activity levels were reduced. In short, the macaque infants exhibited a pattern of behavior similar to the despair
Downloaded by [Memorial University of Newfoundland] at 15:59 10 March 2015
14
JOURNAL OF GENERAL PSYCHOLOGY
reaction in human maternal separation. Upon return of the mother, the monkey infants spent a day or two clinging to her, and then resumed social interactions with other infants at preseparation levels. Recovery of social behavior is not universal; other studies of rhesus separation report a more pervasive effect. Spencer-Boothe and Hinde (25) conducted a study of rhesus monkey separation in a large enclosure occupied by juveniles, infants, and adult monkeys of both sexes. The mother was removed from the enclosure, and the infant left to fend for itself. The abandoned infant was clearly disturbed, at first wildly scampering about the cage, and then showing the low activity, despair-like behavior typical of playpen-separated rhesus. Return of the mother in this situation was not as effective in eliminating the effects of separation as in the playpen studies. Even after several weeks, infants who had been separated played less and spent more time on the mother than control subjects who had not been abandoned. Macaque monkey infants living in complex social groupings described by Spencer-Boothe and Hinde are dependent on their mothers in many ways. In many primate groups, infants are differentially treated by other adult monkeys, depending on the dominance and status of their mothers (11). Removal of the mother from the infant in this setting probably modifies the behavior of other adults toward the infant, as well as the behavior of the infant toward adults. For rhesus monkey infants, removal of the mother in the presence of other adults and older juvenile monkeys is probably more stress-producing than maternal separation in the playpen setting. Rosenblum and Kaufman (1 2, 17) conducted mother-infant separation studies in group housing with two other macaque species. Pig-tailed monkey infants, Macaca nemestrina, responded even more profoundly to maternal separation than did rhesus infants. They sat hunched in a ball, isolat3d from their surroundings for nearly a week before moving about in the apparatus. After reunion with the mother, intensification of the mother-infant relationship was evident for at least three months. The same procedure of removing the mother and leaving the infant in a mixed age and sex social group was employed with the use of bonnet macaque infants (Macaca radiata). In this species, the effects of maternal separation were short-lived and slight. The infants showed initial disturbance, but quickly attached themselves to substitute mothers. They did not appear to develop the depression reported for rhesus and pig-tailed macaques. The speciestypical social organization of bonnet and pig-tailed monkeys interacts with
Downloaded by [Memorial University of Newfoundland] at 15:59 10 March 2015
BILL SEAY AND NATHAN W. GOTTFRIED
15
the experimenter’s manipulation to produce different effects of motherinfant separation in these two species. If playpen separation studies were to be conducted on pig-tailed and bonnet macaques, the results would, in all probability, conform to the results of rhesus playpen separations. Playpen separation, in which the infant is left alone except for short interaction sessions with another separated infant, would be less stressful and debilitating for a pig-tailed infant than desertion in the social group. In contrast, the bonnet monkey infant would be more severely affected by playpen separation than by desertion in the group, since the group setting the behavior of the remaining adult female monkeys serves to ameliorate the effects of separation. Playpen separation studies have been conducted at Louisiana State University with cynomologous (18) and patas (15) monkey subjects. As in the studies of normative social development, results for cynomologous monkeys were similar to those obtained for rhesus monkey subjects. Initially, the infants were violently disturbed, settled down into a low-activity little-play routine, reattached to the mother upon reunion, and then resumed preseparation levels of infant social interaction. Persisting elevation of contact with the mother indicated the effects of playpen separation were more long lasting in cynomologous infants than in rhesus. In general, however, playpen separation produced the same results in cynomologous and rhesus monkeys. The effects of playpen separation on patas infants were rather different from macaques, as might be expected from developmental differences previously discussed. Patas infants showed disturbance on removal of their mothers and some reduction in activity. Chasing play declined but not significantly, although it looked less playful to the observers. After reunion with the mothers, recovery of social behavior to preseparation levels was extremely rapid. Furthermore, the separation experiences seemed to initiate contact play behavior in some patas infants. As can be seen from these data, the effects of manipulating an apparently simple and direct independent variable, mother-infant separation, are a joint function of the species studied and the apparatus or situation employed in the study. Removal of the mother disturbs the infant in every case, but the severity and pervasiveness of the effect varies considerably. For rhesus macaques, abandonment in a group appears to be more stressful than being left in an empty cage. Pig-tailed macaques react even more violently than rhesus to abandonment in a group, while bonnet monkey
Downloaded by [Memorial University of Newfoundland] at 15:59 10 March 2015
16
JOURNAL OF GENERAL PSYCHOLOGY
infants rapidly recover as a result of attention from foster mothers. Playpen separation appears to be equally stressful for cynomologous and rhesus infants, but the patas monkey shows less disturbance and more rapid recovery from the effects of separation. Mother-infant separation must be evaluated in terms of the behavioral repertoire and social organization of the subject species being studied. Further, the characteristics of the species interact with the experimental situation or apparatus to modify the effects of the experimenter’s manipulation of the infant and mother. Species differences in the effects of independent variables are not limited to mother-infant separation, or to social behavior in monkeys. The scientist necessarily works with a particular species in a particular setting. The peculiar species-setting combination he employs necessarily modifies the effect of any experimental manipulation.
F. CONCLUSIONS The three groups of studies considered here are related by the degree to which the results are in part determined by the species of the subjects studied-by phylogenetic set. Across a wide variety of environments rhesus macaques develop species-typical social behavior repertoires, and only under the most bizarre conditions are these patterns of behavior disrupted. Social development in similar environments is essentially species-specific -the organism brings with it a probabilistic tendency to develop in a particular way. Closely related species, such as rhesus and cynomologous monkeys, show similar patterns of development, while other organisms, such as the patas monkey, exhibit contrasting courses of development. Finally, it is evident that the effect of an experimental manipulation on behavior is a joint function of the species studied and the situation in which the manipulation is accomplished. REFERENCES 1. 2.
3. 4. 5.
ALEXANDER,B. K. The effects of early peer-deprivation on juvenile behavior of rhesus monkeys. Unpublished Doctoral dissertation, University of Wisconsin, Madison, 1966. ALEXANDER,B. K., & HARLOW,H. F. Social behavior of juvenile rhesus monkeys subjected to different rearing conditions during the first six months of life. 2001.Jahrb. Abt. A&. Zool. Physiol. Tiere, 1965, 71, 489-508. ARLINC,G. L., & HARLOW,H. F. Effects of social deprivation on maternal behavior of rhesus monkeys. J . Comp. 6. Physiol. Psychol., 1967, 64, 371-377. BOWLBY,J . Grief and mourning in infancy and early childhood. Psychoanal. Study Child, 1960, 75, 9-52. . The nature of the child’s tie to the mother. Internat. J . Psychoanal., 1958, 39,
~
1-24.
BILL SEAY AND NATHAN W. COTTFRIED 6.
7.
Downloaded by [Memorial University of Newfoundland] at 15:59 10 March 2015
8.
9. 10. 11. 12. 13. 14. 15. 16. 17. 18. 19.
20. 21.
22. 23. 24.
25.
17
ERWIN, J., MITCHELL,G., & MAPLE,T. Abnormal behavior in non-isolate-reared rhesus monkeys. Psychol. Rep., 1973, 33, 515-523. HANSEN, E. W. The development of maternal and infant behavior in the rhesus monkey. Behavior, 1966, 27, 107-149. HARLOW, H. F., & SOUMI,J. Social recovery by isolation reared monkeys. Proc. Nat. Acad. Sci. U.S.A., 1971, 68, 1534-1538. HARLOW,H. F., DODSWORTH, R. O., & HARLOW, M. K. Total social isolation in monkeys. Proc. Nat. Acad. Sci. U.S.A., 1965, 54, 90-97. HARLOW, H. F., HARLOW,M. K., & SOUMI,S. J. From thought to therapy: Lessons from a primate laboratory. Amer. Sci., 1971, 59, 538-549. JAY, P. Field Studies. In Schrier, A. M. Harlow, H. F. Stollnitz, F. (Eds.), Behavim of Nonhuman Primates (Vol. II). New York Academic Press, 1965. 4. 525-591. KAUFMAN,I. C., & ROSENBLUM,L. A. Depression in infant monkeys separated from their mothers. Science, 1967, 155, 1030-1031. MASON,W. A. The effects of social restriction on the behavior of rhesus monkeys I Free social behavior. J. Comp. 6.Physiol. Psychol., 1960, 53, 582-589. . The effects of social restriction on the behavior of rhesus monkeys 11: Tests of Gregariousness. J. Comp. 6. Physiol. Psychol., 1961, 54, 287-290. PRESTON,D. G., BAKER,R. F., & SEAY, B. Mother-infant separation in the patas monkey. Devel. Psychol., 1970, 3, 298-306. ROSENBLUM, L. A. The development of social behavior in the rhesus monkey. Unpublished Doctoral dissertation, Univenity of Wisconsin, Madison, 1961. ROSENBLUM, L. A., & KAUFMAN,I. C. Variations in infant development and response to maternal loss in monkeys. Amer. J. Orthopsychiatry, 1968, 38, 418-426. SCHLOTTMANN,R. S., & SEAY, B. Mother-infant separation in the Java monkey (Macaca irus). J. Comp. 6.Physiol. Psychol. 1972, 79, 334-340. SEAY, B. Maternal behavior in primiparous and multiparous rhesus monkeys. Folia Ptimatol., 1966, 4, 146-168. SEAY, B., & HARLOW, H. F. Maternal separation in the rhesus monkey. J. N e w . 6. Ment. Dis., 1964, 140, 434-441. SEAY, B., ALEXANDER,B. K., & HARLOW, H. F. Maternal behavior of socially deprived rhesus monkeys. J. Abn. 6.SOC. Psychol., 1964, 69, 34.5-354. SEAY,B., HANSEN,E. W., & HARLOW,H. F. Mother-infant separation in monkeys. J. Child Psychol. 6 Psychiat., 1962, 3, 123-132. SEAY, B., SCHLOTTMANN, R. S., & GANDOLFO,R. Early social interaction in two monkey species. J. Cen. Psychol., 1972, 87, 37-43. SEAY,B., SCHLQTTMANN,R. S., & THORNE,B. M. Maternal and filial behavior in monkeys. Devel. Psychol., 1970, 3, 66-72. SPENCER-BOOTHE, Y., & HINDE,R. A. The effects of separating rhesus monkey infants from their mothers for six days. J. Child Psychol. 6. Psychiat., 1967, 7 , 179-197.
Department of Psychology Louisiana State UHiversity Baton Rouge, Louisiana 70803
The Journal of General Psychology Publication details, including instructions for authors and subscription information: http://www.tandfonline.com/loi/vgen20
A Phylogenetic Perspective for Social Behavior in Primates a
Bill Seay & Nathan W. Gottfried
a
a
Louisiana State University , USA Published online: 06 Jul 2010.
To cite this article: Bill Seay & Nathan W. Gottfried (1975) A Phylogenetic Perspective for Social Behavior in Primates, The Journal of General Psychology, 92:1, 5-17, DOI: 10.1080/00221309.1975.9711323 To link to this article: http://dx.doi.org/10.1080/00221309.1975.9711323
PLEASE SCROLL DOWN FOR ARTICLE Taylor & Francis makes every effort to ensure the accuracy of all the information (the “Content”) contained in the publications on our platform. However, Taylor & Francis, our agents, and our licensors make no representations or warranties whatsoever as to the accuracy, completeness, or suitability for any purpose of the Content. Any opinions and views expressed in this publication are the opinions and views of the authors, and are not the views of or endorsed by Taylor & Francis. The accuracy of the Content should not be relied upon and should be independently verified with primary sources of information. Taylor and Francis shall not be liable for any losses, actions, claims, proceedings, demands, costs, expenses, damages, and other liabilities whatsoever or howsoever caused arising directly or indirectly in connection with, in relation to or arising out of the use of the Content.
Downloaded by [Memorial University of Newfoundland] at 15:59 10 March 2015
This article may be used for research, teaching, and private study purposes. Any substantial or systematic reproduction, redistribution, reselling, loan, sub-licensing, systematic supply, or distribution in any form to anyone is expressly forbidden. Terms & Conditions of access and use can be found at http://www.tandfonline.com/page/terms-and-conditions
The Journal of General Psychology, 1975, 92, 5-17.
A PHYLOGENETIC PERSPECTIVE FOR SOCIAL BEHAVIOR IN PRTMATES*
Downloaded by [Memorial University of Newfoundland] at 15:59 10 March 2015
Louisiana State University
BILL SEAY
AND
w.GOTTFRIED
NATHAN SUMMARY
Three selected groups of studies of primate social behavior and development are discussed. In the first group of studies the social development of rhesus monkeys reared in different environments is considered. Rhesus show remarkable similarity in behavior in diverse environments, demonstrating a phylogenetic set to develop species-typical behavioral repertoires. The second set of studies reports on three species (Macaca mulatta, Macaca fasicularis, and Erythrocebus patas) reared in similar settings. Species differences observed in these settings were a result of phylogenetic set. Finally, mother-infant separation studies conducted with several monkey species are reviewed. The results of these studies were interpreted to be the product of interactions of the species-typical behavior and social organization of each species, the specific setting or apparatus used, and the independent variable manipulation employed. Caution is recommended in cross-species generalization within primates. A.
INTRODUCTION
This paper presents a perspective from which to view the findings of the many recent research reports concerning primate social behavior and development. No attempt will be made to provide a comprehensive review of this vast literature. Instead, three selected sets of studies will be considered, and a conceptual framework abstracted from these data. The concept, phylogenetic set, provides a descriptive term for some phenomena evident in primate social behavior. Phylogenetic set is the tendency to develop species-typical behaviors. Every organism shares with other members of his species genetic characteristics which influence his
* Recommended by John Horrocks of the Editorial Board, and received in the Editorial Office, Provincetown, Massachusetts, on January 29, 1974. Copyright, 1975, by The Journal Press. 5
Downloaded by [Memorial University of Newfoundland] at 15:59 10 March 2015
6
JOURNAL OF GENERAL PSYCHOLOGY
behavior. These characteristics do not determine behavior, but certain behavioral traits are probable consequences of normal development in any given species. The expression of phylogenetic set requires interaction with some environment. The influence of phylogenetic set is indicated when species-typical behavior developes in organisms subjected to different environments during development. Failure to develop species-typical behavior in some particular environment does not necessarily indicate that phylogenetic set is not involved in the normal development of that behavior. It is presumed that the expression of phylogenetic set may be blocked or modified in individual organisms. This would occur when the organism encounters environments in which salient features differ markedly from environments typically encountered by members of the species. In the first group of studies, the development of social behavior of a single species, the rhesus monkey, is examined in a number of different early environments. As will be seen, this species exhibits unexpectedly low variability in development across environments, demonstrating a phylogenetic set to develop similar social behavior repertoires in a wide variety of environments. The second group of studies deals with three species reared in identical environments. These species show species-specific developmental trends, thus demonstrating phylogenetic set when environmental factors are held constant. The third selection of studies includes a number of mother-infant separation studies. In these separation studies apparatus and procedure interact with the experimental treatment in different ways for different species, demonstrating the influence of phylogenetic set on the effects of an apparently simple experimental manipulation. Before considering the behavioral data, it may be well to consider the subject species most frequently used in studies of monkey social behavior and development. A recent bibliography concerning social behavior in macaques, baboons, and patas monkeys provides an example of the popularity of the rhesus monkey. In this list, which was prepared by the Primate Information Center of the University of Washington Primate Research Center at the authors’ request, 168 titles refer clearly to rhesus monkeys. The pigtailed macaque, Macaca nemistrina, was the next most frequently studied macaque with 36 titles. All baboon species combined were indicated in only 40 titles. The rhesus monkey, Macaca mulatta, is native to northern and central India, and lives in a wide variety of habitats across this range. In one
Downloaded by [Memorial University of Newfoundland] at 15:59 10 March 2015
BILL SEAY AND NATHAN W. GOTTFRIED
7
sense, Macaca mulatta can be said to have no single natural environment. It lives in forests, small towns, and large.cities, adapting successfully to these complex and demanding environments. Rhesus monkeys are social animals, living in troops with fairly clear dominance hierarchies among adults, forming moderately stable social organization within the troop. One goal of research in the social behavior and development of rhesus monkeys has been a search for principles sufficiently general to enhance our understanding of human social development. Therefore, some comparisons between rhesus monkeys and human beings may be in order. One striking difference between these species is the relative physical maturity of the rhesus infant at birth. At the age of two or three days an infant rhesus monkey can locomote; by two or three weeks of age his motor development appears to be free of reflexive control under most conditions. A second difference between infant humans and infant rhesus monkeys is the amount of physical contact between mother and neonate. The rhesus monkey infant remains closely attached to the mother’s ventral surface almost constantly for several weeks. It sleeps in close ventral contact with the mother for nearly a year. Infant-mother contact in our society contrasts sharply with this pattern. Even in societies where the infant is carried by the mother for a large part of the day, a cloth sling, cradle board, or a similar device serves to reduce intimate physical contact with the mother. Other differences between human and rhesus infants could be mentioned, but these two characteristics are sufficient to suggest the need for considerable caution in generalizing from one to the other. As will be seen below, even among monkey species one cannot necessarily make reliable predictions from one species to another.
B. RHESUS SOCIALDEVELOPMENT The first group of investigations to be considered here deals with the most familiar example of research in primate social behavior. At the University of Wisconsin Primate Laboratory rhesus monkeys have been reared in a variety of early environments (10). Observation of socially restricted monkeys throughout their life span has been a primary source of information concerning primate social development. These studies will be viewed as an example of the evaluation of the effects of environmental manipulation in a single species. When rhesus infants are separated from their mothers at birth and subsequently housed alone, their social behavior is markedly affected. The
Downloaded by [Memorial University of Newfoundland] at 15:59 10 March 2015
8
JOURNAL OF GENERAL PSYCHOLOGY
duration and extent of disruption of species-typical social behavior depends on the duration and extent of restriction. In the first reports of socially restricted animals, Mason (13, 14) studied a group of juvenile rhesus monkeys which had been allowed to see and smell, but not touch and manipulate conspecifics in the same condition. Their behavior was compared to that of wild-born animals of about the same age. Mason’s restricted group was hyperaggressive, exhibited disoriented and infrequent sexual behavior, engaged in little play, and rarely groomed other animals. As adults, animals reared in similar situations continued to exhibit aberrant behavior to the extent that no males, and only about half of the females reproduced (10). Socially restricted females impregnated by wildborn males are unlikely to care for their first infant (3, 21). More severe restrictions of social stimulation have proved to have even more debilitating results (9). If infant rhesus monkeys are prevented from seeing or touching other members of their own (or any other) species for a year after birth, they are almost totally socially incompetent. They are not only incapable of social interaction, but are incapable of defending themselves, or even effectively retreating from hyperaggressive peers. One would predict that these animals, like the less severely restricted monkeys discussed above, would be unlikely to achieve adult reproductive and maternal competence. These dramatic disruptions of social behavior are the most striking results of the series of early experience manipulations conducted in the Wisconsin Research program. This paper will focus on some less dramatic, but intriguing results of those investigations. Infant monkeys have been reared in a number of other situations in the Wisconsin Lab. One group of infants was singly housed, but permitted to play with identically housed conspecifics for 15-30 minutes a day (16). Another group was housed in home cages of a four-unit playpen apparatus and confined to a home cage and adjacent play cage for 22 hours each day (7). This group of infants was permitted to interact with conspecific age mates for two hours each day. A number of rhesus infants have been reared in a so-called “togethertogether” situation in which two to four infant monkeys are housed together from birth (2). Still other infants were permitted to stay with their mothers, at least for the first six months of life (7, 19). Some mother-reared animals were permitted to play with other infants from birth, (7, 19), while others interacted exclusively with their mothers (1). These mothers were, in some cases, maternally adequate wild-born females (7, 19) and, in others, brutal or indifferent “motherless mothers” (3, 21). These diverse social and
BILL SEAY AND NATHAN W. GOTTFRIED
9
Downloaded by [Memorial University of Newfoundland] at 15:59 10 March 2015
physical environments result in the development of strikingly similar behavioral repertoires in rhesus monkeys.
C. COMPARATIVE STUDIES Formal comparisons of two or more groups of these variously reared animals have revealed few differences in social behavior and development. For example, when the infants of brutal or indifferent mothers were compared with those of adequate mothers, few differences were evident (21). Abused infants were somewhat slower in developing contact or rough-and-tumble play, but by six months of age no differences were seen. Chasing play was somewhat less frequent during the first six months of development for the abused infants. Despite this difference in frequency, the behavior pattern was identical to that seen in adequately mothered infants. Infants reared by their mothers, but deprived of peer experience for four or eight months were compared to those who had both peer experience and maternal care (1). The peer-deprived infants were somewhat more aggressive than the peer-experienced monkeys. However, both groups showed similar patterns of play and sexual behavior. Furthermore, species typical group structure developed in both groups. In another investigation (19) two groups of peer-experienced, motherreared infants were compared with a group of surrogate-reared, peerexperienced infants. Differences between the two mother-reared groups were more extreme than between either mother-reared group and the surrogate-reared animals. If an experienced primatologist were to classify the animals on the basis of the data, he would select as normal one mother-reared group and the surrogate group. The remaining motherreared group would be classified as unusual. However, all three groups of animals exhibited competent, species-typical behavior with few consistent differences among the groups. A final study illustrates the persistence of species typical development in a variety of social environments (2). Four groups of infants were compared: one group was reared with surrogate mothers, but denied contact with other monkeys for the first six months of life; in the second group, animals were reared together in one cage for six months; monkeys in the third group were reared with inadequate mothers but given peer experience; animals comprising the last group were reared by adequate mothers and had access to age-mates. Only the s o c i d y restricted animals showed consistent differences from any other group. The peer-deprived,
Downloaded by [Memorial University of Newfoundland] at 15:59 10 March 2015
10
JOURNAL OF GENERAL PSYCHOLOGY
surrogate-reared monkeys were clumsy, avoided prolonged physical contact with other monkeys, and showed inadequate sexual behavior. However, after prolonged social experience, they achieved comparable levels of play and developed typical group structure. Recent research at the University of Wisconsin indicates that animals reared in total isolation for six months retained the capacity for speciestypical social behavior if provided with younger normal peer “therapists” at the end of the period (8). By age one year, after six months of treatment, the isolates showed nearly normal levels of exploratory, locomotor, and play behavior. It is evident that a number of early environments may serve as an adequate experiential basis for species-typical social development in the rhesus macaque. In fact, only bizarre and restrictive environments disrupt the development of appropriate patterns of group structure, play, and sexual behavior. With few exceptions, the development of social behavior involving particular play patterns, specific sexual behavior patterns, and a degree of social organization is a highly probable result of maturation in the rhesus. Relative environmental independence is also shown in the data just reviewed. These data suggest that macaque social development resists all but the most extreme environmental pressures. The evidence does not support the interpretation that animals with different histories do not differ in the frequencies with which various social behavior patterns are displayed. Nor can it be said that animals with species-typical social behavior repertoires will be free of abnormal or atypical behaviors (6). These results present characteristics for which an adequate label is not available. The term phylogenetic set has been coined to provide such a label. A phylogenetic set is a probabilistic tendency for an organism to develop species-typical behavior. By virtue of its membership in a species, an organism is possessed of a gestalt of reflexes, neuromuscular structures, perceptual capacities, and learning dispositions, which determine the probability of specific aspects of behavioral development. Across many environments, almost identical behavioral repertoires develop in conspecific animals; only in extremely unfavorable environments will the behavioral repertoire of the species fail to appear. Furthermore, even the organism maturing in an environment inadequate to support species-typical behavior will not develop unique techniques for coping with that environment. Rather, his behavioral repertoire will consist of fragments of the behavior patterns which ensure individual and species survival for most of his species-mates.
Downloaded by [Memorial University of Newfoundland] at 15:59 10 March 2015
BILL SEAY AND NATHAN W. GOTTFRIED
11
D. SPECIESCOMPARISONS In the previous sections, we have discussed the influence of diverse environments on members of a single species. The second set of observations to be considered involves three species reared in similar settings. Infant monkeys were reared by their own mothers in the home cage of a playpen apparatus. The infants, but not the mothers, had access to an adjacent play area via a small opening in the cage wall. For a short time each day, infants were permitted to interact with other infants similarly housed. Mother reared rhesus infants in this environment have been studied by a number of investigators (e.g., 1, 7, 19). The earliest appearing play pattern for the species is rough-and-tumble or contact play which may be described as play fighting. Developing somewhat later, a second pattern of chasing or approach-avoidance play is frequently seen. During the first six months of life in the playpen situation, rhesus monkeys show behavioral sex differences characterized by male infants, more than females, engaging in social approaches, threats, rough-and-tumble play, and pelvic thrusting. Females more frequently withdraw and exhibit passivity or rigidity to social or physical stimulation. Aware of the tendency to generalize research results based on rhesus macaques to all primates, investigators at Louisiana State University (LSU) have studied the normative development of two other species in the playpen apparatus. The common or crab-eating macaque or cynomologous monkey, Macaca fascicularis, was selected to provide comparable data from a related macaque species. This macaque, which will be called the cynomologous monkey throughout this paper, is a somewhat smaller animal than the rhesus, and is found across a wide range in coastal areas of Southeast Asia. The behavior of cynomologous monkeys observed in the playpen apparatus is essentially identical to rhesus monkeys reared in similar conditions (23, 24). Indices of the mother-infant relationship, such as nursing or ventral contact, dropped sharply with increasing infant age. Physical contact with age-mates appeared early and persisted across the six-month period of study. Play fighting appeared early and seemed to be an important play pattern for cynomologous monkeys. Sex differences in social behavior, similar to those reported for rhesus macaques, appeared during the first six months of development. It would be reasonable, then, to generalize from laboratory studies of the rhesus monkey to laboratory studies of the cynomologous monkey. The similarity of maternal, filial, and peer-directed social behavior patterns
Downloaded by [Memorial University of Newfoundland] at 15:59 10 March 2015
12
JOURNAL O F GENERAL PSYCHOLOGY
between these two species is evident. Manipulations of the early environments of cynomologous monkeys would be expected to produce effects at least grossly similar to those reported for the rhesus macaque. Bear in mind that the two species are closely related members of the same genus. Indeed, some authorities consider cynomologous and rhesus monkeys to be subspecies of a single species. The other species observed at LSU was Erythrocebus patus, the hussar or African red monkey. The patas monkey is closely related to the circopithecus genus and is sometimes classified Circopithecus patas. Its typical behavior differs from that of most circopithecus monkeys in that most of its waking hours are spent on the ground; it is a rather clumsy tree climber. This savannah dweller lives in single male groups, with a clear female dominance hierarchy. Groups of pat& monkeys are widely separated from one another in the wild. Individuals usually maintain greater distances from other group members than do most macaques. One unique characteristic of the species is that it is probably the fastest moving primate, reported to attain speeds of 35-40 mph over short distances. The development of patas social behavior in the playpen setting presents contrasts to that of the macaque (23). The most pervasive differences have to do with infant physical contact. When a four-month-old macaque infant ventures out of his home cage into an open play area, another infant joins him despite the protests and interference of his mother. In contrast, a four-month-old patas infant in an open play area is seldom joined by another infant. When a second infant enters the play area, the first infant returns to his mother’s cage. Physical contact between patas infants was relatively infrequent throughout the first six months of life. The most frequent form of infant play observed in young patas monkeys was noncontact and chasing play; contact play or play fighting was infrequently seen. The mother-infant relationship in patas monkeys is complementarily different from that of macaques (24). Rhesus and cynomologous mothers are somewhat intolerant of manipulation of their body by their infants, often reacting to unpleasant exploratory or play fighting responses by hitting or biting their infants. At the same time, they frequently permit long as these infants other than their own to come into their cage-as infants are not overactive or overaggressive. Patas mothers, on the other hand, are tolerant of personal insult by their own infants, either not reacting at all or reciprocating elements of play fighting. However, patas monkey mothers will not tolerate another patas infant in the home cage. Patas infants in the playpen situation go into the wrong home cage only
Downloaded by [Memorial University of Newfoundland] at 15:59 10 March 2015
BILL SEAY AND NATHAN W. GOTTFRIED
13
once. Physical contact between patas mother-infant pairs is also somewhat different from the macaque pattern. Even while nursing, the patas infant is less likely than a macaque infant to have a major part of his body surface directly touching the mother. This is, no doubt, a partial consequence of the long-limbed, rangy, physical structure of the patas. These data suggest that the rhesus monkey is not a representative primate. It is intriguing to consider to what extent our current ideas about primate social development have been determined by the selection of Macaca mulatta and other macaques as experimental subjects. One would be hesitant, indeed, to predict that the effects of peer and maternal deprivation would be identical for patas and rhesus monkeys. The possibility of early experience research with various monkey species is an exciting one. What is evident from these comparisons of three species in comparable environments is that the species of an organism is a partial determinant of his reactions to an environment. Phylogenetic set accounts for species differences in behavior when environments are consistent across species.
E. MATERNAL SEPARATION STUDIES A final group of studies illustrates an experimental manipulation evaluated across species and environments. In these studies infant monkeys are separated from their mothers. The behavior of the infants is observed before and during separation and after reunion with the mother. Of particular interest is the similarity of reactions of macaque and human infants and juveniles to mother-infant separation. The first studies of rhesus monkey mother-infant separation were conducted in the playpen apparatus (20, 22). Two separation techniques have been employed. In one study infants were trapped in the play cage where they could see and hear their mother throughout the three-week separation. In an alternative, somewhat cleaner, procedure the mother-infant pair were removed from the apparatus, separated, and the infant only was returned to the home cage. In both procedures, the infant’s initial reaction was similar. After separation from the mother, infants scampered about the cage, screamed, and defecated. This violent emotional reaction exhibited by the rhesus was similar to the protest stage of a human child’s reaction to maternal separation, as described by Bowlby (4, 5). After a day or two, the infants settled down, but their peer-directed social behavior was influenced by the mother’s absence. Play, typical in six-month-old macaques, almost disappeared. Activity levels were reduced. In short, the macaque infants exhibited a pattern of behavior similar to the despair
Downloaded by [Memorial University of Newfoundland] at 15:59 10 March 2015
14
JOURNAL OF GENERAL PSYCHOLOGY
reaction in human maternal separation. Upon return of the mother, the monkey infants spent a day or two clinging to her, and then resumed social interactions with other infants at preseparation levels. Recovery of social behavior is not universal; other studies of rhesus separation report a more pervasive effect. Spencer-Boothe and Hinde (25) conducted a study of rhesus monkey separation in a large enclosure occupied by juveniles, infants, and adult monkeys of both sexes. The mother was removed from the enclosure, and the infant left to fend for itself. The abandoned infant was clearly disturbed, at first wildly scampering about the cage, and then showing the low activity, despair-like behavior typical of playpen-separated rhesus. Return of the mother in this situation was not as effective in eliminating the effects of separation as in the playpen studies. Even after several weeks, infants who had been separated played less and spent more time on the mother than control subjects who had not been abandoned. Macaque monkey infants living in complex social groupings described by Spencer-Boothe and Hinde are dependent on their mothers in many ways. In many primate groups, infants are differentially treated by other adult monkeys, depending on the dominance and status of their mothers (11). Removal of the mother from the infant in this setting probably modifies the behavior of other adults toward the infant, as well as the behavior of the infant toward adults. For rhesus monkey infants, removal of the mother in the presence of other adults and older juvenile monkeys is probably more stress-producing than maternal separation in the playpen setting. Rosenblum and Kaufman (1 2, 17) conducted mother-infant separation studies in group housing with two other macaque species. Pig-tailed monkey infants, Macaca nemestrina, responded even more profoundly to maternal separation than did rhesus infants. They sat hunched in a ball, isolat3d from their surroundings for nearly a week before moving about in the apparatus. After reunion with the mother, intensification of the mother-infant relationship was evident for at least three months. The same procedure of removing the mother and leaving the infant in a mixed age and sex social group was employed with the use of bonnet macaque infants (Macaca radiata). In this species, the effects of maternal separation were short-lived and slight. The infants showed initial disturbance, but quickly attached themselves to substitute mothers. They did not appear to develop the depression reported for rhesus and pig-tailed macaques. The speciestypical social organization of bonnet and pig-tailed monkeys interacts with
Downloaded by [Memorial University of Newfoundland] at 15:59 10 March 2015
BILL SEAY AND NATHAN W. GOTTFRIED
15
the experimenter’s manipulation to produce different effects of motherinfant separation in these two species. If playpen separation studies were to be conducted on pig-tailed and bonnet macaques, the results would, in all probability, conform to the results of rhesus playpen separations. Playpen separation, in which the infant is left alone except for short interaction sessions with another separated infant, would be less stressful and debilitating for a pig-tailed infant than desertion in the social group. In contrast, the bonnet monkey infant would be more severely affected by playpen separation than by desertion in the group, since the group setting the behavior of the remaining adult female monkeys serves to ameliorate the effects of separation. Playpen separation studies have been conducted at Louisiana State University with cynomologous (18) and patas (15) monkey subjects. As in the studies of normative social development, results for cynomologous monkeys were similar to those obtained for rhesus monkey subjects. Initially, the infants were violently disturbed, settled down into a low-activity little-play routine, reattached to the mother upon reunion, and then resumed preseparation levels of infant social interaction. Persisting elevation of contact with the mother indicated the effects of playpen separation were more long lasting in cynomologous infants than in rhesus. In general, however, playpen separation produced the same results in cynomologous and rhesus monkeys. The effects of playpen separation on patas infants were rather different from macaques, as might be expected from developmental differences previously discussed. Patas infants showed disturbance on removal of their mothers and some reduction in activity. Chasing play declined but not significantly, although it looked less playful to the observers. After reunion with the mothers, recovery of social behavior to preseparation levels was extremely rapid. Furthermore, the separation experiences seemed to initiate contact play behavior in some patas infants. As can be seen from these data, the effects of manipulating an apparently simple and direct independent variable, mother-infant separation, are a joint function of the species studied and the apparatus or situation employed in the study. Removal of the mother disturbs the infant in every case, but the severity and pervasiveness of the effect varies considerably. For rhesus macaques, abandonment in a group appears to be more stressful than being left in an empty cage. Pig-tailed macaques react even more violently than rhesus to abandonment in a group, while bonnet monkey
Downloaded by [Memorial University of Newfoundland] at 15:59 10 March 2015
16
JOURNAL OF GENERAL PSYCHOLOGY
infants rapidly recover as a result of attention from foster mothers. Playpen separation appears to be equally stressful for cynomologous and rhesus infants, but the patas monkey shows less disturbance and more rapid recovery from the effects of separation. Mother-infant separation must be evaluated in terms of the behavioral repertoire and social organization of the subject species being studied. Further, the characteristics of the species interact with the experimental situation or apparatus to modify the effects of the experimenter’s manipulation of the infant and mother. Species differences in the effects of independent variables are not limited to mother-infant separation, or to social behavior in monkeys. The scientist necessarily works with a particular species in a particular setting. The peculiar species-setting combination he employs necessarily modifies the effect of any experimental manipulation.
F. CONCLUSIONS The three groups of studies considered here are related by the degree to which the results are in part determined by the species of the subjects studied-by phylogenetic set. Across a wide variety of environments rhesus macaques develop species-typical social behavior repertoires, and only under the most bizarre conditions are these patterns of behavior disrupted. Social development in similar environments is essentially species-specific -the organism brings with it a probabilistic tendency to develop in a particular way. Closely related species, such as rhesus and cynomologous monkeys, show similar patterns of development, while other organisms, such as the patas monkey, exhibit contrasting courses of development. Finally, it is evident that the effect of an experimental manipulation on behavior is a joint function of the species studied and the situation in which the manipulation is accomplished. REFERENCES 1. 2.
3. 4. 5.
ALEXANDER,B. K. The effects of early peer-deprivation on juvenile behavior of rhesus monkeys. Unpublished Doctoral dissertation, University of Wisconsin, Madison, 1966. ALEXANDER,B. K., & HARLOW,H. F. Social behavior of juvenile rhesus monkeys subjected to different rearing conditions during the first six months of life. 2001.Jahrb. Abt. A&. Zool. Physiol. Tiere, 1965, 71, 489-508. ARLINC,G. L., & HARLOW,H. F. Effects of social deprivation on maternal behavior of rhesus monkeys. J . Comp. 6. Physiol. Psychol., 1967, 64, 371-377. BOWLBY,J . Grief and mourning in infancy and early childhood. Psychoanal. Study Child, 1960, 75, 9-52. . The nature of the child’s tie to the mother. Internat. J . Psychoanal., 1958, 39,
~
1-24.
BILL SEAY AND NATHAN W. COTTFRIED 6.
7.
Downloaded by [Memorial University of Newfoundland] at 15:59 10 March 2015
8.
9. 10. 11. 12. 13. 14. 15. 16. 17. 18. 19.
20. 21.
22. 23. 24.
25.
17
ERWIN, J., MITCHELL,G., & MAPLE,T. Abnormal behavior in non-isolate-reared rhesus monkeys. Psychol. Rep., 1973, 33, 515-523. HANSEN, E. W. The development of maternal and infant behavior in the rhesus monkey. Behavior, 1966, 27, 107-149. HARLOW, H. F., & SOUMI,J. Social recovery by isolation reared monkeys. Proc. Nat. Acad. Sci. U.S.A., 1971, 68, 1534-1538. HARLOW,H. F., DODSWORTH, R. O., & HARLOW, M. K. Total social isolation in monkeys. Proc. Nat. Acad. Sci. U.S.A., 1965, 54, 90-97. HARLOW, H. F., HARLOW,M. K., & SOUMI,S. J. From thought to therapy: Lessons from a primate laboratory. Amer. Sci., 1971, 59, 538-549. JAY, P. Field Studies. In Schrier, A. M. Harlow, H. F. Stollnitz, F. (Eds.), Behavim of Nonhuman Primates (Vol. II). New York Academic Press, 1965. 4. 525-591. KAUFMAN,I. C., & ROSENBLUM,L. A. Depression in infant monkeys separated from their mothers. Science, 1967, 155, 1030-1031. MASON,W. A. The effects of social restriction on the behavior of rhesus monkeys I Free social behavior. J. Comp. 6.Physiol. Psychol., 1960, 53, 582-589. . The effects of social restriction on the behavior of rhesus monkeys 11: Tests of Gregariousness. J. Comp. 6. Physiol. Psychol., 1961, 54, 287-290. PRESTON,D. G., BAKER,R. F., & SEAY, B. Mother-infant separation in the patas monkey. Devel. Psychol., 1970, 3, 298-306. ROSENBLUM, L. A. The development of social behavior in the rhesus monkey. Unpublished Doctoral dissertation, Univenity of Wisconsin, Madison, 1961. ROSENBLUM, L. A., & KAUFMAN,I. C. Variations in infant development and response to maternal loss in monkeys. Amer. J. Orthopsychiatry, 1968, 38, 418-426. SCHLOTTMANN,R. S., & SEAY, B. Mother-infant separation in the Java monkey (Macaca irus). J. Comp. 6.Physiol. Psychol. 1972, 79, 334-340. SEAY, B. Maternal behavior in primiparous and multiparous rhesus monkeys. Folia Ptimatol., 1966, 4, 146-168. SEAY, B., & HARLOW, H. F. Maternal separation in the rhesus monkey. J. N e w . 6. Ment. Dis., 1964, 140, 434-441. SEAY, B., ALEXANDER,B. K., & HARLOW, H. F. Maternal behavior of socially deprived rhesus monkeys. J. Abn. 6.SOC. Psychol., 1964, 69, 34.5-354. SEAY,B., HANSEN,E. W., & HARLOW,H. F. Mother-infant separation in monkeys. J. Child Psychol. 6 Psychiat., 1962, 3, 123-132. SEAY, B., SCHLOTTMANN, R. S., & GANDOLFO,R. Early social interaction in two monkey species. J. Cen. Psychol., 1972, 87, 37-43. SEAY,B., SCHLQTTMANN,R. S., & THORNE,B. M. Maternal and filial behavior in monkeys. Devel. Psychol., 1970, 3, 66-72. SPENCER-BOOTHE, Y., & HINDE,R. A. The effects of separating rhesus monkey infants from their mothers for six days. J. Child Psychol. 6. Psychiat., 1967, 7 , 179-197.
Department of Psychology Louisiana State UHiversity Baton Rouge, Louisiana 70803
