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Bilateral infant transfer and adoption in olive baboons (Papio cynocephalus)
W. A. Lawrence Department of Anthropoloey, The Ohio State University, Ohio 43210, U.S.A. Received 12 December 1981 and accepted 20 May 1982 Keywords: infant exchange, baboon, adoption.
Bilateral Infant Transfer and Adoption in OHve Baboons (Papio cynocephalas) The objective of this paper is to discuss an occurrence of self-lnitiated exchange of newborns and the infants' subsequent adoption by female baboons (Papio cynocephalusanubis) at the Southwest Foundation for Research and Education in San Antonio, Texas. Observations were collected using focal animal samples on a captive social group composed of 16 adults (15 females and one male) and three infants (one female and two males). Infants were born into the social group during the study period between October and February. The possibIe influences of parity, infant sex, previous rearing experience of the mother and the dominance rank of the mother were assessed. Mother's rank was associated with acceptance of and adoption of the exchanged infants. Parity, infant sex, and previous rearing experience of the mother show no association with mother's rank or with the exchange and adoption of the infants. Both females involved in the transfer were of low rank in the overall hierarchy; however, the more dominant of the two females demonstrated rejection of the infant while the more subordinate female demonstrated complete acceptance of the infant. The infant rejection by the more dominant female included physical abuse to the point where the infant's life was endangered. It is suggested that a lack of individual specific discrimination abilities by the mothers and infants facilitated this exchange and adoption.
1. I n t r o d u c t i o n A m o n g the primates, as well as m a m m a l s i n general, the m o t h e r - i n f a n t b o n d is the earliest a n d the strongest b o n d formed. Besides insuring the initial survival of the infant, the m o t h e r - i n f a n t b o n d is perhaps the prototype for all subsequent bonds (Poirier, 1972). Serving not only as the central feature of the n e o n a t e ' s world, b u t also as the n e o n a t e ' s mode of locomotion, the m o t h e r is the m a i n d e t e r m i n a n t of the infant's world. T h e r e are noticeable differences in the m a n n e r of m a t e r n a l care across the order. I n some p r i m a t e species individuals other t h a n m o t h e r play a m a j o r role i n caring for the i n f a n t (Burton, 1972; Mitchell & Brandt, 1972). A m o n g the Cercopithecinae, a noticeable contrast occurs b e t w e e n the l a n g u r - c o l o b u s type a n d m a c a q u e - b a b o o n type m a t e r n a l behavior ( M c K e n n a , 1979). Bernstein (1968), Blaffer-Hrdy (1976), H o r w i c h & M a n s k i (I 975), J a y (1965), Poirier (1968), a n d S u g i y a m a (1965, 1967) have all discussed infant transfer a n d care b y n o n - m o t h e r s a m o n g l a n g u r s a n d colobus. This transfer behavior is quite c o m m o n d u r i n g the early d e v e l o p m e n t a l stages. T h e m a c a q u e - b a b o o n m a t e r n a l behavior p a t t e r n discussed by A l t m a n n (1979), D e V o t e & H a l l (1965), Rowetl (1963) a n d W a s h b u r n & D e V o t e (1961), is i n contrast to the l a n g u r - c o l o b u s m a t e r n a l pattern. W h i l e the presence of the i n f a n t a n d the infant's n a t a l coat draws a t t e n t i o n to the m o t h e r - i n f a n t dyad a n d troop m e m b e r s a p p r o a c h to touch a n d groom both the m o t h e r a n d the infant, attempts to take the infant from the m o t h e r are usually unsuccessful d u r i n g the early d e v e l o p m e n t a l stages. This is especially p r o n o u n c e d a m o n g b o n n e t m a c a q u e s ( K a u f m a n , 1977; Simonds, 1965; R a h a m a n & Parthasary, 1969; R o s e n b l u m & Alpert, 1977). A l t m a n n (1979) notes that b a b o o n infants begin to. move a r o u n d on their m o t h e r a p p r o x i m a t e l y two weeks after birth a n d m a y initiate movements away from the m o t h e r Journal of Human Evolution (1982) 11, 505-510 0047-2484182/060505 -~-06 $03.00]0
9 1982 Academic Press Inc. (London) Limited
506
w.A. LAVCRENCE
within the first month. Towards tile end of the second month a baboon mother's attention to the infant may begin to decline, at which time she may initiate separation. This paper documents an occurrence of a self-initiated, bilateral transfer of newborns by two adult female baboons (Papio cynocephalus anubis) at the Southwest Foundation for Research and Education in San Antonio, Texas, and discusses the female's subsequent behavior patterns.
2. O b s e r v a t l o n s Observations were conducted by a single observer (W.A.L.) on a captive baboon group containing 16 adults (15 females and one male) and three infants (one female and two males). The adults were members of a stable social group and the infants were born into the group during the observation period t:rom October 1980 to March 1981. The first infant, a male, was born on 20 November t980. The second infant, a female, was born on 1 December 1980 and the third infant, another male, was born ten days later on 11 December 1980. Eighty-five and one-half hours of data were collected during 513 ten-minute liberal tbcal animal samples (Altmann, 1974). Observations were conducted on a diurnal schedule, from 0700 to 1700, developed using a random numbers table. Two restrictions were placed on the randomness of the sampling to eliminate other possible biases: no more than one focal sample was collected on any given animal during a single day and a full diurnal was collected on each animal in the group before the next diurnal schedule was begun. Ad libitum sampling was also conducted, but the data collected during these periods was considered qualitative only and not used for any quantitative analysis. As a regular routine at The Foundation, mothers with newborns are removed from their cages within three days of the infant's birth for a routine health examination: the infants are sexed, weighed, measured and blood tests are conducted. The mothers and infants are returned to their cages within a few hours of their removal. Occasionally an animal may be removed from its cage for the treatment of injuries or for additional examination. On 30 December 1980, such an occasion arose and dam 233, an adult female with a female infant was removed from her group. When the infant accompanying the female was examined and Foundation records were checked, it became obvious that there had been an exchange of infants. Female 233, who had given birth to a female infant four weeks prior to this time, was in possession of a male infant. Female 1154, who had given brith to a male two weeks previously, was removed from the gang cage and was found to be in possession of the female infant. A two-way transfer of infants occurred between these two females. The possibility of a three-way transfer was considered, but examination of all other infants present in the group disproved this possibility. This transfer did not occur during a period of stress associated with human intervention. The mothers were returned to their cage without attempting to transfer the infants back to their biological mothers. Upon re-introduction of the dams and the infants to the gang cage, dam 233 began to physically abuse her adoptive infant. After several hours it became apparent that the female was rejecting the infant. Both the infant and dam 233 were removed from the cage. The infant was removed from the dam and placed in the nursery for hand-rearing. The dam was returned to the cage alone. In contrast to this situation, dam 1154 re-entered the gang cage and all behaviors including passive and active contact, holding and grooming of the infant, suggested that she had corn-
BILATERAL INFANT EXCHANGE AND ADOPTION
507
pletely accepted d a m 233's female infant as her own. At this time the infant male and female involved in the transfer were 18 and 29 days old respectively. There was no attempt on the part of d a m 233 to regain her biological infant from d a m 1154. The first interaction witnessed between the two females after the exchange occurred at the end of J a n u a r y 1981, a full month after the transfer was discovered. This encounter consisted of a brief social approach by d a m 233 to d a m 1154 and was terminated when d a m 233 walked away. The interaction occurred approximately one week after the female infant initiated her first movements away from her adoptive mother, d a m 1154. At this time the infant was 53 days old. D a m 1154 remained either in contact or within 3 m of her adoptive daughter until the beginning of March 1981. T h e infant then began to spend over 69 ~ of her time away from her adoptive mother and was the primary initiator of any contact between the " m o t h e r " and the "daughter". D a m 1154 did, however, intercede in extremely stressful situations, retrieving the infant and retreating to a corner of the cage. No other interactions were observed between the biological mother and the adoptive mother or the biological mother and the infant. 3. D i s c u s s i o n
Factors of parity, infant sex of previous births, previous rearing experience of the dam, and the dominance rank of the d a m were assessed for their potential influence on the transfer, and subsequent adoption of and maternal behaviors directed towards the infants by the dams. Table I
Parity and previous rearing experience of f e m a l e s involved in the exchange of infants
Infant sex Dam
Parity
Male
Female
233 1154
5 3
1 3
4 --
Previous rearing experience of dam All dam reared All nursery reared
Both females were multiparous prior to the births of the infants involved in the transfer. While d a m I 154 had given birth to only males previously, after the exchange she accepted the female infant. D a m 233 on the other hand had given birth to both males and females, although 75 ~o of her previous infants had been females. D a m 233 transferred a female infant and rejected the male infant. D a m 1154 had no previous experience in rearing her offspring. All of her infants were removed within the first three days after birth and handreared in the Foundation's nursery for biomedical research purposes. D a m 233, on the other hand, reared all of her previous infants until they were approximately four months old. They were then weaned from the d a m by Foundation staff and placed in peer groups. Although both females involved in the transfer fell within the lower half of the dominance hierarchy of the group, d a m 233 ranked above d a m 1154. Based on the parity records of the dams and their previous rearing experience, it appears that familiarity with infant sex by parity did not influence acceptance or rejection of exchanged infants. Previous rearing experience seemed to have a reverse effect on whether the dams accepted or rejected the exchanged infants. The d a m with no previous experience rearing her own offspring accepted and reared the exchanged infant, while the female with previous experience in rearing offspring rejected the infant.
508
w . a . LAWRENCE
Altmann (1979) suggests that primiparous and experienced mothers difikr in their responses to their infants. Although dam 1t54 was not primiparous, she had little previous experience with her own infants. It is possible that she may have had previous rearing experience through aunting behavior. Experience through aunting may explain her competence as a mother, while lack of experience rearing her own offspring as well as her low rank among the group t~males may explain her tendency to avoid the rest of the group (Lancaster, 1972 ; Altmann, 1979 ; Rowell et al., 1964). Prior to the infant births, the two females exhibited two distinct types of behavior patterns. D a m 233, the more dominant of the two females, was highly mobile and actively avoided 58 ~ of all social approaches. Her visual attention shifted among other animals in the cage and little time was spent in either active or passive contact with others or within 1 m proximity of others: D a m 1154 was less mobile, spending 95 ~ of her time stationary, occupying a single corner of the cage. Her attention was focused primarily on cages adjacent to her own and similar to dam 233, approximately 4 ~ of her time was spent in either active or passive contact with others. Seventy-five per cent of the interactions between the two females involved in the transfer were initiated by dam 1154, the more submissive female. The 25 ~ of the interactions initiated by dam 233 were directly followed by avoidance behaviors on the part of dam 1154. D a m 233 was in constant contact with "her" infant for the first two weeks between the birth of her infant and 30 December, during the observation periods. For the four weeks t~om inthnt birth until 30 December, dam 1154 was in contact with "her" infant 91 ~o of the time. This difference in mothe>infant contact time may be explained by the differential infant ages and the infant's respective degree of reliance on and independence from the mother rather than due to the mother's attempts at retaining the infant near her. Social approaches were directed towards the two dams at similar rates by other group members. Both t~males received approximately 12 approaches per hour, dam 233 avoided 67 ~ of these approaches, while dam 1154 received 10.5 approaches per hour of which she actively avoided 43 ~ . Although rates of social approaches towards the two females and the avoidance rates by the two females were similar, they continued to maintain two distinct behavior patterns. While dam 1154 avoided most stressful situations by remaining in a singular area of the cage and directing nearly all of her attention to either her infant or adjacent cages, dam 233 moved throughout the cage, performing submissive gestures during interactions with others. During the two week period when both females were in possession of newborns, there were no observed interactions between the two females. The restrictiveness of dam 1154 towards her adoptive infant is a pattern which has been previously discussed as partially attributable to low social rank (Altmann, 1979; Rowetl, 1968). Maternal rank may serve as a good predictor of maternal style (Altmann, 1979). Both the mother's restrictiveness and the infant's delay in initiation of separation from the mother suggest the development of a strong bond between the adoptive mother and the adoptive infant. The successful transfer of attachments between mother and daughter from a biological dyad to an adoptive dyad, with no attempt by either tire mother or the infant to reverse the situation is similar to the results of separation studies conducted on langurs by Dolhinow (1978). This shift in attachments is also consistent with the results of separation studies of bonnet macaques (Kaufman, 1977; Kaufman & Rosenblum, 1967).
BILATERAL INFANT EXGtlANGE AND ADOPTION
509
The shift in attachments is interesting in light of the dual transfer and subsequent behaviors exhibited by the two dams when infant recognition of mother and maternal recognition of infant are considered as important aspects of the separation which occurred prior to "adoption" of" the infant. Differentiation of tile mother from other females by infant among species which characteristically show little separation between mother and infant during the neonatal period and where the mother is the primary caregiver may not be a necessary development for infant survival. Altmann's (1979) studies suggest that infant recognition of mother takes a few weeks among yellow baboons. The close contact relationship among such species may also suggest that rapid differentiation of an infant by its mother may not be necessary for infant survival. Lack of individual-specific discrimination by mothers and inPants would help explain how a bilateral transfer of infants, as discussed above, could occur. The adoptive behavior exhibited by dam 1154 may be maternal responses elicited by stimuli such as postnatal hormonal changes in the mother (McKenna, 1979) and neonatal coat color rather than maternal responses to a specific infant.
4. C o n c l u s i o n
Parity, sex of the infant and previous rearing experience of the mothers are factors which may have influenced the infant transfer reported here, as well as the lack of motherinfant specific discrimination responses. Dominance rank as a predictor of maternal patterns may also help explain the bond formed between dam 1154 and the adoptive infant. Due to the paucity of documentation or corcanentary on this type of behavior among baboons, and because this is a singular occurrence of bilateral transfer and adoption of infants, untit further incidences are reported this type of behavior should be considered individual-specific rather than a species-specific behavior.
I would like to thank the staff of the Southwest Foundation, Dr A. M. Coehlo, Jr, and Dr F. E. Poirier for their assistance and suggestions concerning this research. This work was supported by grant funds provided by The Ohio State Alumni Association, NSF Pre-doctoral improvement fellowship (BNS-8016637) and by resources provided by the Primate Ethology Laboratory (NIH-NHLBI-HL19362, NIH-5-507-RR05519-13, NHLBI-80-26), Southwest Foundation for Research and Education. References
Attmann, J. (1974). Observational study of behavior: sampling methods. Behavior 48, 227-265. Altmann, J. (1979). Baboon Mothers and Infants. Chicago: University of Chicago Press. Bernstein, I. (1968). The lutong of Kuala Selangor. Behavior 32, 1-16. Blaffer-Hrdy, S. (1976). Care and exploitation of nonhuman primate infants by conspecificsother than the mother. In (j. S. Rosenblatt, R. A. Hinde, E. Shaw & C. Beer, Eds.) Advances in the Study of Behavior vol. 6, 101-158. New York: Academic Press. Burton, F. D. (1972). The integration of biology and behavior in the socialization process of Macaca sylvanna of Gilbraltar. In (F. E. Poirier, Ed.) Primate Socialization, pp. 29-62. New York: Random House. DeVote, I. & Hall, K. R. L. (1965). Baboon ecology. In (I. DeVore, Ed.) Primate Behavior:field studies of monkeys and apes, pp. 20-52. New York: Holt, Rinehart & Winston. Dolhinow, P. (1978). Langur monkey mother loss and adoption. Commentary. Behavioral Brain Science 3, 443-444.
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Horwich, R. H. & Manski, D. (1975). Maternal care and infant transfer in two species of Colobus monkeys. Primates 16, 49-73. Jay, P. (1965). The common langur of North India. In (I. DeVore, Ed.) Primate Behavior: field studies of monkeys and apes, pp. 197-249. New York: Holt, Rinehart and Winston. Kaufman, I. C. (1977). Developmental considerations of anxiety and depression: psycho-biological studies in monkeys. I n (T. Shapiro, Ed.) Psychoanalysisand ContemporaryScience, pp. 317-363. New York : International University Press. Kaufman, I. C. & Roseblum (1967). Depression in int'ant monkeys separated from their mothers. Science 155, 1030-1031. Lancaster, J. B. (1972). Play-mothering: the relations between juvenile females and young infants among free-ranging Vervet monkeys. In (F. E. Poirier, Ed.) Primate Socialization, pp. 83-104. New York: R a n d o m House. McKenna, J. J. (1979). Aspects of infant socialization, attachment, and maternal caregiving patterns among primates: a cross disciplinary review. Yearbook of Physical Anthropology 22, 250-286. Mitchell, G. & Brandt, E. M. (t972). Paternal Behavior in Primates. In (F. E. Poirier~ Ed.) Primate Socialization, pp. 173-206. New York: R a n d o m House. Poirier, F. E. (1968). The Niligiri Langur (Presbytisjohnii) mother-infant dyad. Primates 9, 45H68. Poirier, F. E. (1972). Introduction. Primate Socialization. New York: R a n d o m House. R a h a m a n , H. & Parthasary, M. (1969). Studies of social behavior of bonnet monkeys. Primates 10, 149-162. Rosenblum, L. A. & Alpert, S. (1977). Response to mother and stranger: a first step in socialization. In (F. E. Poirier & S. Chevalier-Skolnikoff, Eds) Primate Bio-soeial Development: Biological, Social, and Ecological Determinants, pp. 463-478. New York: Garland Publishing, Inc. Rowell, T. (1963). The social development of some rhesus monkeys. In (G. M. Foss, Ed.) Determinants of Infant Behavior, pp. 35-49. London: Methuen. Rowell, T. (t968). T h e effect of temporary separation from their group on the mother-infant relationship of baboons. Folia Primatologia 9, 114-122. Rowell, T., Hinde, R. A. & Spencer-Booth, Y. (1964). " A u n t " - i n f a n t interaction in captive rhesus monkeys. Animal Behavior 129 219-226. Simonds, P. E. (1965). The bonnet macaque in South India. Ill (1. DeVore, Ed.) Primate Behavior: field studies of monkeys and apes, pp. 175-197. New York: Holt, Rineart & Winston. Sugiyama, Y. (1965). Behavioral development and social structure in two groups of H a n u m a n langurs (Presbytis entellus). Primates 6, 213-247. Sugiyama, Y. (1967). Social organization of H a n u m a n langurs. In (S. A. Altmann, Ed.) Social Communication among Primates, pp. 221-236. Chicago: University of Chicago Press. Washburn, S. L. & DeVore, I. (1961). The social life of baboons. Scientific American 204, 62-71.
Bilateral Infant Transfer and Adoption in OHve Baboons (Papio cynocephalas) The objective of this paper is to discuss an occurrence of self-lnitiated exchange of newborns and the infants' subsequent adoption by female baboons (Papio cynocephalusanubis) at the Southwest Foundation for Research and Education in San Antonio, Texas. Observations were collected using focal animal samples on a captive social group composed of 16 adults (15 females and one male) and three infants (one female and two males). Infants were born into the social group during the study period between October and February. The possibIe influences of parity, infant sex, previous rearing experience of the mother and the dominance rank of the mother were assessed. Mother's rank was associated with acceptance of and adoption of the exchanged infants. Parity, infant sex, and previous rearing experience of the mother show no association with mother's rank or with the exchange and adoption of the infants. Both females involved in the transfer were of low rank in the overall hierarchy; however, the more dominant of the two females demonstrated rejection of the infant while the more subordinate female demonstrated complete acceptance of the infant. The infant rejection by the more dominant female included physical abuse to the point where the infant's life was endangered. It is suggested that a lack of individual specific discrimination abilities by the mothers and infants facilitated this exchange and adoption.
1. I n t r o d u c t i o n A m o n g the primates, as well as m a m m a l s i n general, the m o t h e r - i n f a n t b o n d is the earliest a n d the strongest b o n d formed. Besides insuring the initial survival of the infant, the m o t h e r - i n f a n t b o n d is perhaps the prototype for all subsequent bonds (Poirier, 1972). Serving not only as the central feature of the n e o n a t e ' s world, b u t also as the n e o n a t e ' s mode of locomotion, the m o t h e r is the m a i n d e t e r m i n a n t of the infant's world. T h e r e are noticeable differences in the m a n n e r of m a t e r n a l care across the order. I n some p r i m a t e species individuals other t h a n m o t h e r play a m a j o r role i n caring for the i n f a n t (Burton, 1972; Mitchell & Brandt, 1972). A m o n g the Cercopithecinae, a noticeable contrast occurs b e t w e e n the l a n g u r - c o l o b u s type a n d m a c a q u e - b a b o o n type m a t e r n a l behavior ( M c K e n n a , 1979). Bernstein (1968), Blaffer-Hrdy (1976), H o r w i c h & M a n s k i (I 975), J a y (1965), Poirier (1968), a n d S u g i y a m a (1965, 1967) have all discussed infant transfer a n d care b y n o n - m o t h e r s a m o n g l a n g u r s a n d colobus. This transfer behavior is quite c o m m o n d u r i n g the early d e v e l o p m e n t a l stages. T h e m a c a q u e - b a b o o n m a t e r n a l behavior p a t t e r n discussed by A l t m a n n (1979), D e V o t e & H a l l (1965), Rowetl (1963) a n d W a s h b u r n & D e V o t e (1961), is i n contrast to the l a n g u r - c o l o b u s m a t e r n a l pattern. W h i l e the presence of the i n f a n t a n d the infant's n a t a l coat draws a t t e n t i o n to the m o t h e r - i n f a n t dyad a n d troop m e m b e r s a p p r o a c h to touch a n d groom both the m o t h e r a n d the infant, attempts to take the infant from the m o t h e r are usually unsuccessful d u r i n g the early d e v e l o p m e n t a l stages. This is especially p r o n o u n c e d a m o n g b o n n e t m a c a q u e s ( K a u f m a n , 1977; Simonds, 1965; R a h a m a n & Parthasary, 1969; R o s e n b l u m & Alpert, 1977). A l t m a n n (1979) notes that b a b o o n infants begin to. move a r o u n d on their m o t h e r a p p r o x i m a t e l y two weeks after birth a n d m a y initiate movements away from the m o t h e r Journal of Human Evolution (1982) 11, 505-510 0047-2484182/060505 -~-06 $03.00]0
9 1982 Academic Press Inc. (London) Limited
506
w.A. LAVCRENCE
within the first month. Towards tile end of the second month a baboon mother's attention to the infant may begin to decline, at which time she may initiate separation. This paper documents an occurrence of a self-initiated, bilateral transfer of newborns by two adult female baboons (Papio cynocephalus anubis) at the Southwest Foundation for Research and Education in San Antonio, Texas, and discusses the female's subsequent behavior patterns.
2. O b s e r v a t l o n s Observations were conducted by a single observer (W.A.L.) on a captive baboon group containing 16 adults (15 females and one male) and three infants (one female and two males). The adults were members of a stable social group and the infants were born into the group during the observation period t:rom October 1980 to March 1981. The first infant, a male, was born on 20 November t980. The second infant, a female, was born on 1 December 1980 and the third infant, another male, was born ten days later on 11 December 1980. Eighty-five and one-half hours of data were collected during 513 ten-minute liberal tbcal animal samples (Altmann, 1974). Observations were conducted on a diurnal schedule, from 0700 to 1700, developed using a random numbers table. Two restrictions were placed on the randomness of the sampling to eliminate other possible biases: no more than one focal sample was collected on any given animal during a single day and a full diurnal was collected on each animal in the group before the next diurnal schedule was begun. Ad libitum sampling was also conducted, but the data collected during these periods was considered qualitative only and not used for any quantitative analysis. As a regular routine at The Foundation, mothers with newborns are removed from their cages within three days of the infant's birth for a routine health examination: the infants are sexed, weighed, measured and blood tests are conducted. The mothers and infants are returned to their cages within a few hours of their removal. Occasionally an animal may be removed from its cage for the treatment of injuries or for additional examination. On 30 December 1980, such an occasion arose and dam 233, an adult female with a female infant was removed from her group. When the infant accompanying the female was examined and Foundation records were checked, it became obvious that there had been an exchange of infants. Female 233, who had given birth to a female infant four weeks prior to this time, was in possession of a male infant. Female 1154, who had given brith to a male two weeks previously, was removed from the gang cage and was found to be in possession of the female infant. A two-way transfer of infants occurred between these two females. The possibility of a three-way transfer was considered, but examination of all other infants present in the group disproved this possibility. This transfer did not occur during a period of stress associated with human intervention. The mothers were returned to their cage without attempting to transfer the infants back to their biological mothers. Upon re-introduction of the dams and the infants to the gang cage, dam 233 began to physically abuse her adoptive infant. After several hours it became apparent that the female was rejecting the infant. Both the infant and dam 233 were removed from the cage. The infant was removed from the dam and placed in the nursery for hand-rearing. The dam was returned to the cage alone. In contrast to this situation, dam 1154 re-entered the gang cage and all behaviors including passive and active contact, holding and grooming of the infant, suggested that she had corn-
BILATERAL INFANT EXCHANGE AND ADOPTION
507
pletely accepted d a m 233's female infant as her own. At this time the infant male and female involved in the transfer were 18 and 29 days old respectively. There was no attempt on the part of d a m 233 to regain her biological infant from d a m 1154. The first interaction witnessed between the two females after the exchange occurred at the end of J a n u a r y 1981, a full month after the transfer was discovered. This encounter consisted of a brief social approach by d a m 233 to d a m 1154 and was terminated when d a m 233 walked away. The interaction occurred approximately one week after the female infant initiated her first movements away from her adoptive mother, d a m 1154. At this time the infant was 53 days old. D a m 1154 remained either in contact or within 3 m of her adoptive daughter until the beginning of March 1981. T h e infant then began to spend over 69 ~ of her time away from her adoptive mother and was the primary initiator of any contact between the " m o t h e r " and the "daughter". D a m 1154 did, however, intercede in extremely stressful situations, retrieving the infant and retreating to a corner of the cage. No other interactions were observed between the biological mother and the adoptive mother or the biological mother and the infant. 3. D i s c u s s i o n
Factors of parity, infant sex of previous births, previous rearing experience of the dam, and the dominance rank of the d a m were assessed for their potential influence on the transfer, and subsequent adoption of and maternal behaviors directed towards the infants by the dams. Table I
Parity and previous rearing experience of f e m a l e s involved in the exchange of infants
Infant sex Dam
Parity
Male
Female
233 1154
5 3
1 3
4 --
Previous rearing experience of dam All dam reared All nursery reared
Both females were multiparous prior to the births of the infants involved in the transfer. While d a m I 154 had given birth to only males previously, after the exchange she accepted the female infant. D a m 233 on the other hand had given birth to both males and females, although 75 ~o of her previous infants had been females. D a m 233 transferred a female infant and rejected the male infant. D a m 1154 had no previous experience in rearing her offspring. All of her infants were removed within the first three days after birth and handreared in the Foundation's nursery for biomedical research purposes. D a m 233, on the other hand, reared all of her previous infants until they were approximately four months old. They were then weaned from the d a m by Foundation staff and placed in peer groups. Although both females involved in the transfer fell within the lower half of the dominance hierarchy of the group, d a m 233 ranked above d a m 1154. Based on the parity records of the dams and their previous rearing experience, it appears that familiarity with infant sex by parity did not influence acceptance or rejection of exchanged infants. Previous rearing experience seemed to have a reverse effect on whether the dams accepted or rejected the exchanged infants. The d a m with no previous experience rearing her own offspring accepted and reared the exchanged infant, while the female with previous experience in rearing offspring rejected the infant.
508
w . a . LAWRENCE
Altmann (1979) suggests that primiparous and experienced mothers difikr in their responses to their infants. Although dam 1t54 was not primiparous, she had little previous experience with her own infants. It is possible that she may have had previous rearing experience through aunting behavior. Experience through aunting may explain her competence as a mother, while lack of experience rearing her own offspring as well as her low rank among the group t~males may explain her tendency to avoid the rest of the group (Lancaster, 1972 ; Altmann, 1979 ; Rowell et al., 1964). Prior to the infant births, the two females exhibited two distinct types of behavior patterns. D a m 233, the more dominant of the two females, was highly mobile and actively avoided 58 ~ of all social approaches. Her visual attention shifted among other animals in the cage and little time was spent in either active or passive contact with others or within 1 m proximity of others: D a m 1154 was less mobile, spending 95 ~ of her time stationary, occupying a single corner of the cage. Her attention was focused primarily on cages adjacent to her own and similar to dam 233, approximately 4 ~ of her time was spent in either active or passive contact with others. Seventy-five per cent of the interactions between the two females involved in the transfer were initiated by dam 1154, the more submissive female. The 25 ~ of the interactions initiated by dam 233 were directly followed by avoidance behaviors on the part of dam 1154. D a m 233 was in constant contact with "her" infant for the first two weeks between the birth of her infant and 30 December, during the observation periods. For the four weeks t~om inthnt birth until 30 December, dam 1154 was in contact with "her" infant 91 ~o of the time. This difference in mothe>infant contact time may be explained by the differential infant ages and the infant's respective degree of reliance on and independence from the mother rather than due to the mother's attempts at retaining the infant near her. Social approaches were directed towards the two dams at similar rates by other group members. Both t~males received approximately 12 approaches per hour, dam 233 avoided 67 ~ of these approaches, while dam 1154 received 10.5 approaches per hour of which she actively avoided 43 ~ . Although rates of social approaches towards the two females and the avoidance rates by the two females were similar, they continued to maintain two distinct behavior patterns. While dam 1154 avoided most stressful situations by remaining in a singular area of the cage and directing nearly all of her attention to either her infant or adjacent cages, dam 233 moved throughout the cage, performing submissive gestures during interactions with others. During the two week period when both females were in possession of newborns, there were no observed interactions between the two females. The restrictiveness of dam 1154 towards her adoptive infant is a pattern which has been previously discussed as partially attributable to low social rank (Altmann, 1979; Rowetl, 1968). Maternal rank may serve as a good predictor of maternal style (Altmann, 1979). Both the mother's restrictiveness and the infant's delay in initiation of separation from the mother suggest the development of a strong bond between the adoptive mother and the adoptive infant. The successful transfer of attachments between mother and daughter from a biological dyad to an adoptive dyad, with no attempt by either tire mother or the infant to reverse the situation is similar to the results of separation studies conducted on langurs by Dolhinow (1978). This shift in attachments is also consistent with the results of separation studies of bonnet macaques (Kaufman, 1977; Kaufman & Rosenblum, 1967).
BILATERAL INFANT EXGtlANGE AND ADOPTION
509
The shift in attachments is interesting in light of the dual transfer and subsequent behaviors exhibited by the two dams when infant recognition of mother and maternal recognition of infant are considered as important aspects of the separation which occurred prior to "adoption" of" the infant. Differentiation of tile mother from other females by infant among species which characteristically show little separation between mother and infant during the neonatal period and where the mother is the primary caregiver may not be a necessary development for infant survival. Altmann's (1979) studies suggest that infant recognition of mother takes a few weeks among yellow baboons. The close contact relationship among such species may also suggest that rapid differentiation of an infant by its mother may not be necessary for infant survival. Lack of individual-specific discrimination by mothers and inPants would help explain how a bilateral transfer of infants, as discussed above, could occur. The adoptive behavior exhibited by dam 1154 may be maternal responses elicited by stimuli such as postnatal hormonal changes in the mother (McKenna, 1979) and neonatal coat color rather than maternal responses to a specific infant.
4. C o n c l u s i o n
Parity, sex of the infant and previous rearing experience of the mothers are factors which may have influenced the infant transfer reported here, as well as the lack of motherinfant specific discrimination responses. Dominance rank as a predictor of maternal patterns may also help explain the bond formed between dam 1154 and the adoptive infant. Due to the paucity of documentation or corcanentary on this type of behavior among baboons, and because this is a singular occurrence of bilateral transfer and adoption of infants, untit further incidences are reported this type of behavior should be considered individual-specific rather than a species-specific behavior.
I would like to thank the staff of the Southwest Foundation, Dr A. M. Coehlo, Jr, and Dr F. E. Poirier for their assistance and suggestions concerning this research. This work was supported by grant funds provided by The Ohio State Alumni Association, NSF Pre-doctoral improvement fellowship (BNS-8016637) and by resources provided by the Primate Ethology Laboratory (NIH-NHLBI-HL19362, NIH-5-507-RR05519-13, NHLBI-80-26), Southwest Foundation for Research and Education. References
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