Archives o f Sexual Behavior, VoL 4, No. 1, 1975
Initial Heterosexual Behavior of Adolescent Rhesus Monkeys (Macaca mulatta) J. Erwin, Ph.D., 1'2 and G. Mitchell, Ph.D. 1'2'3
This report describes the first heterosexual encounters o f twelve 3-year-old rhesus monkeys, six o f each sex. The sub/ects were all laboratory-born, and were reared in wire cages for the first 8 months o f life, accompanied only by their mothers. After these animals were weaned, each was placed in a cage with another animal o f the same age and sex. The pairs formed in this way remained intact until the animals were 2years oM. When heterosexual dyads were formed, some o f the subjects attacked and bit the animal with which they had been paired, while the members o f other pairs established almost immediate rapport as evidenced by mutual grooming and adequate sexual behavior. The initial sexual interactions o f most pairs were uncoordinated, but all eventually demonstrated qualitatively species-typical patterns o f sexual behavior. Despite their immaturity, two o f these pairs succeeded in producing offspring, both o f which were healthy. KEY WORDS: rhesus monkey; heterosexual; adolescent; copulation. INTRODUCTION Relationships between early social experience and later social adequacy, particularly in the realm o f heterosexual activity, have been investigated using nonhuman primates as subjects (cf Harlow et al., 1972; Mitchell et al., 1966; Senko, 1966). Such studies have clearly indicated that nonhuman primates which are reared in social isolation exhibit deficits in sociosexual behavior as This research was supported by USPHS grants MH-22253 to G. Mitchell, HD-04335 to L. Chapman, and RR-00169 to California Primate Research Center. 1California Primate Research Center, Davis, California, and Department of Psychology, University of California, Davis, California. Department of Behavioral Biology, University of California, School of Medicine, Davis, California. 3Reprint requests may be sent to either J. Erwin or G. Mitchell, Department of Psychology, University of California, Davis, California 95616. 97 © 1 9 7 5 P l e n u m Publishing C o r p o r a t i o n , 2 2 7 West 1 7 t h Street, N e w Y o r k , N . Y . 1 0 0 1 1 . N o part o f this p u b l i c a t i o n m a y be r e p r o d u c e d , stored in a retrieval system, or t r a n s m i t t e d , in a n y f o r m or by a n y means, e l e c t r o n i c , mechanical, p h o t o c o p y i n g , m i c r o f i l m i n g , r e c o r d i n g , or otherwise, w i t h o u t w r i t t e n permission o f the publisher.
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adults. Research has also shown that neither social experience only with the mother nor experience only with peers can guarantee completely adequate sociosexual development, although social experience with either the mother or peers is deafly superior to rearing in social isolation (cf Mitchell, 1970). Even combined mother and peer experience does not appear to be sufficient to produce appropriate adult male copulatory behavior if the maternal experience is limited to the first 3 months of life (Anonymous, 1972). In free-ranging groups of rhesus monkeys, the normal pattern of social developmem involves a waning of the infant's tie to his mother during the infant's second half year of life and an increasing preoccupation with peer interactions, particularly with peers of the same sex (Sade, 1966). Peer interactions are especially frequent during the second year of life (Lindburg, 1971), and the importance of peel' interactions during this developmental phase is, consequently, likely to be especially great. While there are overlaps between developmental phases, the sequence always (under normal conditions) progresses, as Harlow and Harlow (1965) have suggested, from the mother-infant affectional system, which develops first, to the peer affectional system, and, eventually, to the mature heterosexual affectional system. Under normal group-living conditions, of course, it is most difficult to distinguish between cross-sexed peer affectional interactions and immature heterosexual interactions, and it is virtually impossible to determine if a specific sexual interaction is the first for an animal. This report describes the initial heterosexual responses of young rhesus monkeys which had received sequential social experience with mothers and likesexed peers in a laboratory setting. We were interested in evaluating the effects of this sequential pattern of rearing experience on heterosexual social behavior, and were particularly interested in the initial sociosexual responses of these animals to other-sexed peers.
Subjects The subjects for this study were 12 young rhesus monkeys (Macaca mulatta), six males and six females. All of the subjects were laboratory-born and had been reared in wire cages accompanied only by their mothers. No peer contact was allowed until after weaning, which took place at about 8 months of age. At an average of 9 months, each subject was paired with another of the same age and sex. When the subjects were a little over 2 years old, the members of each dyad were separated from one another (Erwin et at., 1971). Shortly after their separation from like-sexed peers, eight of these animals were paired with 6-month-old infants (Brandt and Mitchell, 1973) from which they were sepa-
Initial Heterosexual Behavior of Adolescent Rhesus Monkeys
rated after 3 months (Maple et al., 1973). The infants involved in these pairings were divided evenly across sex and rearing experience (mother-only and social isolation). Half the pairings were same-sex and half were other-sex. Thus two male and two female subjects employed in the present study received experience with other-sexed infants. About 3 months after the separation from infants, these animals were selected for the cross-sex pairings reported here. The mean age of the subjects at the time of this study was 3.15 years for the males (range 3.10-3.24 years) and 2.98 years for the females (range 2.94-3.03 years). Procedure Each pairing was accomplished by introducing one male and one female into a 3- by 3- by 3-ft cage identical to the cages in which the subjects had been previously housed. The cages were constructed of wire mesh except for the front wall, which was made of 3/8-inch thick acrylite. The cages were all in the same room. All subjects were in auditory, and to some extent, visual contact. Responses to pairing were recorded by two observers, one observing each subject, for a period of 30 rain. The initial 3 rain of each pairing, as well as some other portions of the observation period, was recorded cinematographically. All pairs were also observed twice each week for 6 weeks, during which each pair experienced a 2-day separation (Erwin et al., 1973a). They were occasionally observed during the following 6-month period as well. This report focuses primarily on the initial 30 min during which these heterosexually naive animals were exposed to one another. RESULTS
While there was much variablity in the subjects' responses to pairing, there were also some consistencies. The initial responses of most of the pairs were awkward and uncoordinated. The behavior of each pair will be described separately in order to facilitate appreciation of the individual differences displayed in the interactions. Pair 1 At the introduction of the first pair, the male immediately attempted to mount the female but the female did not assume the appropriate receptive sexual-present posture. Instead she sat, crouched, or collapsed. The male repeatedly attempted to mount, and thrusted against whatever portion of his partner was proximal. Eventually he bit the female's neck and dragged her about the cage. During the initial observation period, the female presented once, and then
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only briefly. This pair was later observed to copulate normally, but the rate of copulation remained low throughout the entire period during which they were together. Pair 2 By contrast with the female of pair 1, the female of the second dyad presented fully within the first minute of pairing. The male mounted immediately, but ejaculated without achieving intromission. During the rest of the second pair's initial 30 min together, the male ignored the female despite her attempts to attract his attention with full and enduring sexual presents. This pattern of interaction continued to be typical of pair 2. Copulation occurred infrequently, but the female was almost perpetually solicitous. She sometimes hung upside down from the top of the cage shaking her head from side to side. This activity was interrupted only by long gazes in the direction of the male or by sexual presents. She often initiated contact with the male, but the male usually ignored or actively avoided her advances. However, the pattern of copulation in this pair was sufficient for the female to conceive within the first month of pairing. The male was allowed to remain with the female during the entire term of her pregnancy, and he was present during the birth of a healthy female infant. Copulation was observed during the time when the female was pregnant, and attempted mounting was observed immediately prior to, during, and following parturition. Pair 3
In the third dyad, the male mounted the female immediately on introduction, but the female did not present. The male persisted in mounting, but each time he did so the female sat down or collapsed under his weight. After about 8 min of pairing, the female presented adequately and within the next 5 min the male had achieved several intromissions and had ejaculated. This pattern was repeated, and before the initial observation period had expired the sexual behavior of this pair closely resembled the pattern typical of experienced adult consort pairs. The female presented, the male mounted (with species-typical ankle clasp), the female turned her face toward that of the male, both lipsmacked at one another, and the female reached back with one hand to grasp the thigh of the male. This pair exhibited very little social contact or sexual activity during later periods of observation, aside from their reunion after a 2-day separation. The separation took place after they had been paired for 2 weeks. Pair 4
The fourth dyad displayed the most unusual response to pairing. The female immediately presented to the male. The male mounted several times with
Initial Heterosexual Behavior of Adolescent Rhesus Monkeys
adequate posture and apparent intromision, but began to bite the female's neck (normal copulating males sometimes do this). Immediately following these bites, she turned on him and attacked him repeatedly, biting his neck, face, back, and tail. The male crouched, grimaced, and screeched, but the female continued her attacks. When the female finally presented to him, the male did not mount but instead presented. The female responded by mounting the male several times, complete with extended bouts of pelvic thrusting. Toward the end of the initial 30-rain observation period, the male alternately groomed and mounted the female. The female was observed to mount the male at other times, particularly during periods of excitement, but this pair did display adequate heterosexual behavior as well. Pair 5 The animals in the fifth dyad established contact immediately, when they were paired, by embracing ventroventrally. They maintained contact for the first few minutes that they were together, spending most of the time huddled together with the male embracing the female. After nearly 6 rain of contact, the male attempted to mount. First, he clutched the female about the chest with both arms, then he oriented appropriately, and thrusted rapidly against the female's posterior. He failed, however, to clasp her ankles with his feet. She did not present, but sat down. There were no successful copulations by pair 5 during the initial observation period. These animals copulated adequately but not frequently during the remaining 6 months. They did, however, exhibit an unusually high degree of social proximity and contact, including frequent and enduring bouts of grooming. Fellatio was observed only in this pair, and was initiated during extended grooming bouts by the female. The duration of fellatio was generally brief. The male usually swatted the female away shortly before ejaculation, and completed arousal to ejaculation by masturbation. The ejaculate was usually eaten by both members of the dyad. Another idiosyncratic pattern of sexual behavior emerged from extended grooming by the female. The male often stretched out flat on his back as the female groomed his chest and abdomen. Occasionally the female straddled the male as he lay on his back and thrusted rapidly against his ventrum. Pair 6 The sixth pair was the most sexually active. When they were first introduced, the male immediately established contact by mounting, thrusting, and neck biting. The male alternately groomed and mounted. Initially the mounts were unsuccessful, largely as a result of the female's response (she sat down, backed into a comer, or collapsed). After only 236 rain, however, this pair executed a fully coordinated present-mount-intromission sequence which lasted
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for more than 30 sec. Much awkward mounting occurred during the initial observation period. Some of this was the result of poor orientation on the part of the male and some resulted from inappropriate female posturing. Eight complete present-mount sequences (with intromission but without evidence of ejaculation) were observed during the first 30 min. The male bit the female's back and neck repeatedly, pulling out mouthfuls of hair, but she responded with neither avoidance nor grimacing. This pair continued to be sexually active throughout most of the period during which they were paired, even though the female conceived shortly after the two animals were paired. The male was present at the birth of this pair's healthy female offspring. The members of pair 6 also groomed one another frequently, although not as often as did pair 5.
DISCUSSION The results of this study demonstrated that rhesus monkeys which receive maternal care (during the period in which mother-infant interaction is normally most intense), supplemented by experience with one same-sexed peer (during the period when peer interaction is normally highest), are capable of establishing qualitatively species-typical patterns of sociosexual behavior. While most initial attempts at copulation in our subjects were clumsy and uncoordinated, the animals adapted very quickly. All six pairs copulated in species4ypical fashion within the first 3 weeks they were together, and three pairs did so within their first 30 min of social access. Apparently practice was needed by the members of some pairs before coordinated copulation was possible. It should be noted, however, that the males had some prior practice at mounting, since each had been observed to mount the like-sexed animal with which he had been paired for his second year of life. This earlier practice may have also played an important role in the development of adequate sexual posturing. The copulatory ~'acility of the males in this study was particularly remarkable because of their young age (cf Napier and Napier, 1967; Maple et al., 1973). Although they occasionally displayed bizarre behaviors, e.g., self-biting, self-clasping, and eye poking ("salute"), which are commonly associated with restricted early social experience, they did so very seldom, and only under such conditions of intense stimulation as have been observed to elicit similar responses from caged feral-reared animals (Erwin et al., 1973b). While the occurrence of such behaviors may reflect residual effects of early deprivation, the degree of social deprivation which these subjects experienced was not sufficiently severe to suppress sexual competence. While all males attempted to mount their female partners during the first 30 min, not all females were receptive to these attempts. The mean number of mounts by males (including attempted mounts) during the initial 30 min of
Initial Heterosexual Behavior of Adolescent Rhesus Monkeys
pairing was 15.5, while the mean number of presents by females was only 3.8. One factor which may have contributed to the lack of receptivity on the part of some females may have been their stage of sexual cycle. However, rhesus monkeys, unlike many mammals, do not have a well-defined estrus period (Rowell, 1963). They instead have a menstrual cyCle which resembles that of the human, and they display a pattern of receptivity which is remarkably similar to the human pattern (Michael and Zumpe, 1970), i.e., they are receptive throughout the cycle, although in general there is greater receptivity during the follicular phase than during the luteal phase. Individual differences in receptivity are great, however, both for humans and for rhesus monkeys, with some females being almost constantly solicitous o f sexual activity and others being rarely receptive. The sexual cyclicity of our females was not directly monitored, but inspection of the data acquired over the 6-week period following pairing revealed no marked cyclical fluctuations in sexual activity. Thus the stage of female sexual cycles was not responsible for a major proportion of the individual differences observed in the initial responses of these animals to their first heterosexual encounters. Other "personality" factors (such as aggressiveness, submissiveness, irritability, and attractiveness), all of which have complex developmentalpsychobiological bases, probably contributed greatly to the variability observed between pairs. ACKNOWLEDGMENT The authors gratefully acknowledge the value of Edna Brandt's observations. REFERENCES
Anonymous (1972). Male monkeys raised only with peers likely to show sex deficits at maturity, Primate Rec. 3(2): 12-13. Brandt, E. M., and Mitchell, G. (1973). Pairing pre-adolescents with infants (Maeaca mulatta). Develop, Psyehol. 8(1): 222-228. Erwin, J., Mobaldi, J., and Mitchell, G. (1971). Separation of rhesus monkey juveniles of the same sex. J. Abnorm. PsyehoL 78(2): 134-139. Erwin, J., Brandt, E. M., and Mitchell, G. (1973a). Attachment formation and separation in heterosexually naive pre-adult rhesus monkeys. Develop. Psychobiol. 6:531-538 Erwin, J., Mitchell, G., and Maple, T. (1973b). Abnormal behavior in non-isolate-reared rhesus monkeys. PsychoL Rep. 33: 515-523. Harlow, H. F., and Harlow, M. K. (1965). The affectional systems. In Schrier, A. M., Harlow, H. F., and Stollnitz, F. (eds.), Behavior of Nonhuman Primates, Vol. II, Academic Press, New York, pp. 287-334. Harlow, H. F., Harlow, M. K., Hansen, E. W., and Soumi, S. J. (1972). Infantile sexuality in monkeys. Arch. Sex. Behav. 2: 1-7. Lindburg, D. G. (1971). The rhesus monkey in northern India: An ecological and behavioral study. In Rosenblum, L. A. (ed.), Primate Behavior: Developments in Laboratory and Field Research. Vol. II, Academic Press, New York, pp. 1-106.
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Maple, T., Brandt, E. M., and Mitchell, G. (1973). Separation of preadotescents from infants (Macaca mulatta). Paper read at annual meeting of Western Psychological Association, Anaheim, Calif., April 11-t6. Maple, T., Erwin, J., and Mitchell, G. (1973). Age of sexual maturity in laboratory born pairs of rhesus monkeys (Macaca mulatta). Primates 14: 427-428. Michael, R. P., and Zumpe, D. (1970). Rhythmic changes in the copulatory frequency of rhesus monkeys (Macaca mulatta) in relation to the menstrual cycle, and a comparison with the human cycle. J. Reprod. Fertil. 21: 199-201. Mitchell, G. (1970). Abnormal behavior in primates. In Rosenblum, L. A. (ed.), Primate Behavior: Developments in Field and Laboratory Research, Vol. I, Academic Press, New York, pp. 195-249. Mitchell, G., Raymond, E. J., Ruppenthal, G. C., and Harlow, H. F. (1966). Long-term effects of total social isolation upon behavior of rhesus monkeys. PsychoL Rep. t8: 567-580. Napier, J. R., and Napier, P. H. (1967). A Handbook of Living Primates, Academic Press, London. Rowell, T. E. (1963). Behavior and female reproductive cycles of rhesus macaques. Z Reprod. Fertil. 6: 193-203. Sade, D. S. (1966). Ontogeny of social relations in a group of free-ranging rhesus monkeys (Macaca mulatta). Unpublished doctoral dissertation, University of California, Berkeley, Calif. Senko, M. G. (1966). The effects of early, intermediate, and late experience upon adult macaque sexual behavior. M. S. thesis, University of Wisconsin, Madison, Wis.