Response of Bonnet Macaque Dyads to an Acute Foraqinq Task under Different Motivational Conditions c
c
MICHAEL W. ANDREWS LEONARD A. ROSENBLUM Department of Psychiatry State University of New York Brooklyn, New York
To explore behavioral patterns in bonnet macaque mother-infant dyads under environmental challenge, the motivation of infants to contact their mothers during a 1-hr foraging period was manipulated in two ways. First, sessions were given in which the infants were separated from their mothers for 3 hr prior to the foraging period. Second, sessions were given in which the infants were allowed access to food prior to the foraging period, thereby presumably reducing their motivation to separate from mother to seek food for themselves during the foraging period. Neither manipulation resulted in heightened conflict within the dyads. Separation of the infants prior to the foraging period did result, in general, in mothers forfeiting foraging task engagement to attend to their infants. The extent to which a mother exhibited this pattern correlated with her level of foraging effectiveness. 0 1993 John Wiley & Sons, Inc.
Introduction Our previous laboratory studies of the effects of various foraging demands on bonnet macaque mother-infant relations have demonstrated the ability of dyads to adjust to experimental situations which place a demand on the time and energy of the mother. When a mother is confronted with a physically and psychologically demanding circumstance, there can be long-term consequences for the future social and emotional behavior of the infant (Andrews & Rosenblum, 1988, 1991a; Rosenblum & Paully, 1984; Rosenblum & Sunderland, 1982). Despite these longReprint requests should be sent to Dr. Michael W. Andrews, Department of Psychiatry-Box 120, SUNY Health Science Center at Brooklyn, 450 Clarkson Avenue, Brooklyn, NY 11203, U.S.A. Received for publication 3 December 1991 Revised for publication 22 July 1992 Accepted at Wiley 28 July 1992
Developmental Psychobiology 25(8):557-566 (1992) 0 1993 by John Wiley & Sons, Inc.
CCC 0012- 1630/93/080557-10
558
ANDREWS AND ROSENBLUM
term consequences, if the foraging demand is relatively consistent and predictable during the developmental period, there may be little evidence of sustained, overt conflict within the dyad, rejection of the infant by the mother, or consistent signs of infant distress. Even when the time available for accomplishing the foraging task is rigidly circumscribed by the experimenter, dyads appear to make a relatively smooth adjustment to the situation (Andrews & Rosenblum, in press). Less predictable foraging requirements may result in greater infant emotional disturbance during the developmental period and more enduring affective changes in infants, although still without dramatic increases in overt maternal rejection or punishment (Rosenblum & Paully, 1984; Andrews & Rosenblum, 1991b). Although these findings are consistent with earlier data on the effect of feeding on dyadic cohesiveness in bonnet macaques (Rosenblum, Clark, & Kaufman, 1964), they are somewhat at odds with empirical findings on parent-offspring conflict (cf. Trivers, 1974) obtained with several other primate species. Increased demands on mothers deriving from mating activities have often been shown to increase dyadic conflict (e.g., Collinge, 1987; Fairbanks & McGuire, 1987; Hauser & Fairbanks, 1988; Worlein, Eaton, Johnson, & Glick, 1988). More directly pertinent to the present study, demands on mothers arising from feeding and foraging activities have also been found to alter dyadic interactions. Rosenblum, Clark, and Kaufman (1964) found that pigtail macaque mothers initiated more separations from their infants when confronting a feeding situation. Similarly, Johnson (1986) found maternal rejection in rhesus macaques to increase during feeding bouts. Despite the potential for increased dyadic conflict when mothers are feeding or foraging, baboon dyads, like bonnet macaque dyads, tend to avoid conflict during feeding bouts (Altmann, 1980). Altmann found, however, that changing conditions (e.g., infant weight gain by the 4th to 6th month resulting in preference by mothers for contact while resting) resulted in conflict prior to the restructuring of dyadic contact time. Consistent with the view that altered motivation for contact by mother and/or infant is likely to precipitate dyadic conflict, van de Rijt-Plooij and Plooij (1988) found that developmental reorganization of the young chimpanzee, characterized by increased seeking of maternal proximity, served as a trigger for subsequent dyadic conflict. Our goal in the current study was to further our understanding of the coping strategies and dynamic changes in the behavior of primate mother-infant dyads under conditions of altered motivation for infants to maintain contact with their mothers. Following the emphasis of our previous work, the dyads were studied while mothers were confronted with a foraging task made urgent by a limited time for acquisition of the day’s food ration. The putative motivation of infants to maintain contact with their mothers during the maternal foraging period was manipulated in two ways. In Phase I , infants were separated from the mother for several hours prior to the mother’s imposed foraging task; infant separation from mother has generally been reported to increase infant contact and reduce relatively distant separation for some time after reunion (Hinde & Spencer-Booth, 1971;Rosenblum & Kaufman, 1968; Seay & Harlow, 1965). In Phase 2 these partially self-feeding infants were allowed access to food in the preforaging period; inasmuch as the infants had previously been observed to obtain food items almost exclusively while out of dyadic contact, due largely to seeking food items dropped to the floor by
MACAQUE RESPONSE TO FORAGING TASK
559
adults, it was reasoned that prior feeding would diminish the infant’s own motivation to separate from mother to seek food during the foraging period.
Methods Subjects The subjects used in this study were 4 bonnet macaque (Macaca radiata) mother-infant dyads with previous experience in the experimental foraging task (Andrews & Rosenblum, in press). Two of the infants were male and 2 were female. At the beginning of Phase 1 the infants ranged in age from 6.5-7.5 months; at the beginning of Phase 2 the infants ranged in age from 8-9 months.
Study Environment The group of four dyads was housed in an indoor tile pen (2 m x 4 m x 2.1 m high); 2 one-way glass windows at the front of the pen permitted observation of the group. Perches were located at two levels within the pen. Water was provided ad libitum by animal-activated spigots. The pen lights remained on between 7 a.m. and 7 p.m. A special infant playpen (74 cm x 122 cm x 71 cm high) was located against the back wall of the living area and was constructed of 2.5 cm x 2.5 cm wire mesh. Two pass-through doors (8 cm x 15 cm), one at each end of the playpen, permitted access only by the infants. In addition to the infant playpen, a feeding structure (2.6 m long x 0.5 m wide x 0.7 m high) was located on the floor at the center of the pen. The structure was completely enclosed with the exception of 16 holes (5 cm x 5 cm) on each side, which provided access to 16 food pans (15 cm deep) during periods when food was available. The food in each pan was buried under 12 cm of clean woodchip bedding (See Andrews, Sunderland, & Rosenblum, in press, for further details of the feeding structure).
Procedures General. Monday through Friday of each experimental week the feeder was provisioned at 1 1 a.m.; an amount of food approximately 20% in excess of daily consumption was evenly distributed among the 16 food pans. The monkeys were given access to the feeder for 1 hr after which time all food pans were removed. From Friday afternoon to Monday morning the group was given free access to abundant food. These feeding procedures were quite adequate for maintaining the health of mothers and infants as revealed by daily health checks and weekly weighings. The manipulations of Phases 1 and 2 were carried out Tuesday through Friday of the experimental weeks. Phase 1. Four separations and four sham separations (separation controls) were performed over a 2-week period. The order of treatments was counterbalanced between weeks. On each of the 4 separation days all mothers and infants
560
ANDREWS AND ROSENBLUM
were separated at 8 a.m. The infants were removed to individual cages in another room; the mothers were returned to the home pen. At 11 a.m. the feeding structure was provisioned and observations began with the release of the infants into the home pen. On separation-control days, the mothers and infants were separated at 8 a.m. and immediately reunited in the home pen to control for handling effects. At 11 a.m. the feeding structure was provisioned and observations began. During the foraging hour each mother was the focal subject for a 200-s sample in each quarter hr. During a focal sample the following behaviors were continuously recorded: infant depart from dyadic contact, mother depart from dyadic contact, infant approach to dyadic contact, mother approach to dyadic contact, mother reject infant, mother deter infant in punitive manner, explore object, act dominant towards, act subordinate towards, forage, and obtain food item. In addition, at 2 0 5 intervals during focal observations the following behaviors were scored: spatial-social relationship of mother and infant (grooming, contact without grooming, out of contact but less than 0.3 m apart, or 0.3 m or more apart), eating, agitation, and grooming or passive contact with nondyadic partner. Of the following behaviors, those which were occurring at the time of conclusion of each focal observation were recorded for each infant: contact with mother, social play, affiliative contact with individual other than mother, exercise play, eating, and agitation or depression. See Andrews and Rosenblum (1991b) for further details on behavioral observations. Phase 2. Over a 2-week period, there were 4 days on which the infants received a food supplement prior to the foraging hr (prefeeding days) and 4 days on which the infants did not receive the supplement (prefeeding-control days). The order of treatments was counterbalanced between the 2 experimental weeks. On prefeeding days food was placed in the special infant enclosure at 9 a.m.; at 11 a.m. any food remaining in the infant enclosure was removed and the adult feeding structure was provisioned. Observations began as soon as the feeding structure had been provisioned. On prefeeding-control days no food was placed in the infant enclosure. The group feeding structure was provisioned at 11 a.m. and observations began immediately. Prior to the Phase 2 experimental weeks, it was established that all infants would eat food made available inside the infant enclosure. During the foraging hr each infant was the focal subject for a 200-s sample in each quarter hr; the behaviors scored for the infants in this phase were the same as those scored for mothers in Phase 1, with the exceptions that dominancesubordinance behaviors were dropped from the behaviors previously scored for mothers, and play and depressed behaviors were added to these previously scored behaviors. Following every 200-s focal observation, the occurrence of any of the following was recorded for each mother: hand in feeder while in contact with infant, hand in feeder while not in contact with infant, affiliative contact with individual other than own infant, agonistic interaction, exploration of inanimate object, and eating. Analysis. An estimation of dyadic separation bout length was based on the number of 20-s intervals of separation scored, on average, for each break in dyadic contact. Analysis of behavioral differences between conditions and across time were based upon a repeated-measures analysis of variance.
MACAQUE RESPONSE TO FORAGING TASK
561
Table 1 Percent of samples in which behaviors were scored, Phase 1 Condition Behavior
Separation
Control
df
F
P ~~~
Dyadic Contact Dyadic Grooming Infant Social Play Infant Exercise Play
61 11 0
7.5
33 4 7.5 15
1,3 1,3 1,3 1,3
27.6 6.5 25.0 49.0
~
< 0.05 ns
< 0.05 < 0.01
Results Phase 1 Dyadic Behaviors. In comparison to separation-control sessions, separations were clearly effective in increasing the amount of dyadic contact during the 1-hr foraging sessions. Dyadic contact following separations was nearly double that of control sessions (Table 1). The condition effect for dyadic contact was most pronounced in the first two replications, with little difference between the two conditions by the fourth replication (Fig. 1); this Condition x Replication effect was significant, F ( 3 , 9 ) = 11.45, p < 0.01. Changes in dyadic contact across the 1hr foraging period also differed between the two conditions. Following separations, dyadic contact started much higher and reached a peak earlier in the session than it did in control sessions (Fig. 2); this Condition x quarter-Session interaction effect was significant, F(3, 9) = 4.47, p < 0.05. Neither mothers nor infants exhibited a significant difference between conditions in the frequency with which they made or broke dyadic contact. Grooming was an important component of the dyadic contact following separations; although the overall difference between control and separation sessions was not significant, all four dyads exhibited more grooming following separations (Table 1). Moreover, as is evident in Figure 3, grooming rose more rapidly and to a higher peak following separations than it did in control sessions; this Condition x Quarter-Session interaction effect was highly significant, F(3, 9) = 18.84, p < 0.001. L=] SEPARATION CONTROL SEPARATION
REPLICATION
Fig. 1. Percentage of instantaneous samples in which dyadic contact was scored during the foraging hr by replication of the separation-control and separation conditions.
562
ANDREWS AND ROSENBLUM
QUARTER HOUR
Fig. 2 . Percentage of instantaneous samples in which dyadic contact was scored by quarter of the foraging hr for separation-corrtrol and separution conditions.
Consistent with the finding of greater dyadic contact during separation compared to control, and pointing to some degree of infant disturbance engendered by separations, both social and exercise play were significantly reduced following separations. Social play was completely absent following separations (Table 1). Exercise play following separations was only about half that of control sessions (Table 1). Feeding and Foraging. Based on daily food weighings before and after the foraging hr, there was no difference between control sessions and separation sessions in the mean amount of food obtained each day (454 g vs. 453 g). The mean number of observed foraging bouts by each subject dropped from 12.5 during control sessions to 11.0 in separation sessions, but this small decrease was not significant. Individual differences. tn addition to the general trends identified above, there were important individual differences in the responses of the mothers to the conflicting demands of their infants and the foraging task following the imposed separations. These differences were most pronounced in the 1st quarter of the foraging hr following separations when the motivation to feed was highest and the somewhat distressed infants had just been returned to the home cage. The mothers clearly differed from one another in food acquisition in the 1st quarter of the foraging hr in control sessions, a period in which 66% of all observed
3[
40
[ 0 a ,
SEPARATION CONTROL SEPARATION
T
QUARTER HOUR
Fig. 3 . Percentage of instantaneous samples in which dyadic grooming was scored by quarter of the foraging hr for separation-control and separation conditions.
MACAQUE RESPONSE TO FORAGING TASK
563
Table 2 Percent of samples in which behaviors were scored, Phase 2 Condition Prefed Quarter Hour Behavior
1st
2nd
3rd
Control Quarter Hour 4th
1st
2nd
3rd
4th ~~
Dyadic Contact Mothers Foraging Mothers Eating
6 28 85
9 I5 88
54 5
58
51 0 15
5 20 88
9 5 90
52 5 45
76 0 5
food acquisitions were made. These data were used to characterize the foraging effectiveness of the mothers in the current study. The percentages of total observed food discoveries in the 1st quarter hr made by each individual were 40.8%, 37.4%, 18.4%, and 3.4%. These foraging effectiveness scores in control sessions were highly correlated with dyadic contact scores in the first quarter of separation sessions, Pearson R = 0.96, p < 0.05; from most effective to least effective forager, the percentages of samples in dyadic contact in separation sessions were 75, 58, 17, and 8. Another measure following separation correlated with foraging effectiveness, but exhibited an inverse relationship; there was a strong negative correlation between control-trial foraging effectiveness scores and the changes in effectiveness following separations, Pearson R = -0.96, p < 0.05; from most effective to least effective forager, the changes, from 1st quarter of control sessions to 1st quarter of separation sessions, in mean number of food items found were -3.8, -1.8, -0.5, and +2.0.
Phase 2 Prefeeding Treatment. On prefeeding days, the 4 infants consumed a mean total of 112 g of food prior to the foraging hr. This resulted in a significant reduction in observed infant eating behavior during the foraging hr on these days compared to control days (13.5 bouts vs. 17 bouts), F(1, 3) = 61.74, p < 0.01. Dyadic Behaviors. Prefeeding the infants did not significantly influence the overall level of dyadic contact, frequency of initiation or termination of contact by mother or infant, or frequency of infant rejections. The length of dyadic separation bouts, however, was affected by prefeeding the infants. Separation bout length was significantly greater following prefeeding than it was in prefeeding-control sessions (94.6 s vs. 68.2 s), F(1, 3) = 154.09, p < 0.001. Although the infant prefeeding treatment did not influence the overall level of dyadic contact, contact was influenced by two factors. First, there was a significant increase in dyadic contact across quarter sessions under both control and prefeeding conditions, Table 2, F(3,9) = 32.50, p < 0.001. Second, there was a significant decrease in dyadic contact across replications for the prefeeding and control conditions, mean percent of 20-s intervals, M = 49,31,27, and 23 for each of four replications; F(3, 9) = 8.95, p < 0.01. Feeding and Foraging. Daily weighings of the provisioned food revealed no significant difference in the total amount of food that was dug from the bedding in
564
ANDREWS AND ROSENBLUM
the control and prefeeding conditions (516 g vs. 504 gj. There was, however, a significantly greater amount of foraging behavior by the mothers in the prefeeding condition, F( 1, 3) = 33.00, p < 0.05; the difference occurred in only the I st and 2nd quarters of the l-hr session (Table 2). The mothers also engaged in more eating behavior in the prefeeding condition than in the control condition, with feeding being elevated in the 3rd and 4th quarters of the prefeeding sessions, Table 2; F( 1, 3) = 1 9 . 1 1 , ~< 0.05.
Discussion The findings of this study support the view that the dyadic relationship in the bonnet macaque is highly resistant to overt parent-offspring conflict. For the 7month-old infants, increasing the motivation for attachment behaviors during the foraging hr by an immediately preceding separation between mothers and infants did not increase agitation or depression in the infants, rejection or punishment of infants by mothers, or frequency with which mothers terminated dyadic contact relative to control sessions, despite the continued need for mothers to engage in an urgent foraging task. Similarly, reducing the potential need of the 8.5-monthold infants to separate from their mothers to obtain some of the provisioned food by feeding the infants prior to the foraging hr did not result in heightened infant distress, rejection of infants, or punitive deterrence of infants in foraging hr following prefeeding compared to control hr; in fact, separation bouts were longer when the infants had been fed prior to the foraging hr than when they had not been prefed. Clearly, the dyads were generally able to meet the acute challenges to the dyadic relationship presented in this study with some degree of success. Although infant macaques in the 2nd half-year of life spend increasing periods apart from their mothers during various portions of the daylight period. they still spend long periods in sustained contact and periodic nursing and rapidly move to and maintain contact with the mother when disturbed (e.g., Hinde & SpencerBooth, 1967; Kaufman & Rosenblum, 1969). As might be anticipated, therefore, the dyadic separations that preceded the 1-hr foraging period in Phase 1 presented a greater challenge to the dyads and resulted in greater behavioral changes than did the subsequent prefeeding of these infants. For example, infant play was dramatically reduced following separations, but was unaffected by prefeeding. Similarly pointing to disruption of ongoing patterns of behavior by the 3-hr separations, dyadic contact during the foraging hr was significantly increased following separations; in general following separations, high levels of dyadic contact were maintained during the initial portion of the foraging hr, waning toward control levels by the end of the hr. Overall, although individual variations were apparent, there was a pattern of adjustment in which the mothers initially forfeited foraging activity to spend more time with their infants. The responses of the mothers to the foraging task upon the return of their infants appeared to be related to the foraging effectiveness of each mother during control sessions. Those mothers which most readily obtained food items in control sessions were also the most likely to accommodate their somewhat distressed infants in the separation sessions by restructuring contact time at the cost of some initial foraging success. Accommodation, within the constraints of the present
MACAQUE RESPONSE TO FORAGING TASK
565
design, was rapid. There was little evidence of dyadic conflict regardless of the extent of accommodation. In conclusion, the ability of the four dyads to adapt to the perturbations presented in this study was quite evident in the failure of these manipulations to induce overt or sustained conflict within the dyads. The data suggest, however, that the contingent responsivity of a mother to her infant may be influenced by the control which she has over the accomplishment of other critical tasks in her life. In the present study, the more readily a mother was able to obtain food items, the more responsive she was to her returning infant at the expense of initial foraging effort. Such a difference in contingent responsivity during early rearing may have important consequences for the security of infant-mother attachment (e.g., Ainsworth, Bell, & Stayton, 1971; Andrews & Rosenblurn, 1991b) and the long-term development of social competency in the infants (e.g., Andrews & Rosenblum, 1991a; Bakeman & Brown, 1980; Sroufe, 1979). Experimental manipulations of both mothers’ and infants’ motivations for attachment-related responses at various stages of infant development (particularly with respect to independent feeding and locomotion) and in diverse social settings should provide useful data in broadening our understanding of the dynamic processes which underlie the maintenance and ultimate diminution of the dyadic bond.
Notes The research reported in this article was supported by USPHS Grant MH15965 and funds from the State University of New York.
References Ainsworth, M. D. S., Bell, S. M. V., &Stayton, D. J . (1971). Individualdifferences instrange-situation behaviour of one-year-olds. In H. R. SchalTer (Ed.), The origins of human social relations (pp. 17-57). New York: Academic Press. Altmann, J. (1980). Baboon mothers and infants. Cambridge: Harvard University Press. Andrews, M. W., & Rosenblum, L. A. (1988). Relationship between foraging and affiliative social referencing in primates. In J. E. Fa & C. H. Southwick (Eds.), Ecology and behavior offoodenhanced primate groups (pp. 247-268). New York: Alan R. Liss, Inc. Andrews, M. W . , & Rosenblum, L. A. (1991a). Dominance and social competence in differentially reared bonnet macaques. In A. Ehara, T. Kimura, 0. Takenaka, & M. Iwamoto (Eds.), Primatology today (pp. 347-350). Amsterdam: Elsevier Science Publishers B. V. Andrews, M. W., & Rosenblum, L. A. (1991b). Security of attachment in infants raised in variable- or low-demand environments. Child Development, 62, 686-693. Andrews, M. W., & Rosenblum, L. A. (in press). Dyadic bond maintenance in bonnet macaques under acute challenges. International Journal of Methods in Psychiatric Research. Andrews, M. W., Sunderland, G., & Rosenblum, L. A. (in press). Impact of foraging demand on conflict within mother-infant dyads. In W. A. Mason & S. P. Mendoza (Eds.), Primate socid conflict. Albany: SUNY Press. Bakeman, R., & Brown, J. V. (1980). Early interaction: Consequences for social and mental development at three years. Child Development, 51, 437-447. Collinge, N. E. (1987). Weaning variability in semi-free-ranging Japanese macaques (Macacafuscata). Folia Primatologica, 48, 137-150. Fairbanks, L. A., & McGuire, M. T. (1987). Mother-infant relationships in vervet monkeys: Response to new adult males. International Journal of Primatology, 8, 351-365. Hauser, M. D., & Fairbanks, L. A. (1988). Mother-offspring conflict in vervet monkeys: Variation in reponse to ecological conditions. Animal Behauiour, 36, 802-8 13.
566
ANDREWS AND ROSENBLUM
Hinde, R. A., & Spencer-Booth, Y. (1967). The behaviour of socially living rhesus monkeys in their first two and a half years. Animal Behaviour, 15, 169-196. Hinde, R. A . , & Spencer-Booth, Y. (1971). Effects of brief separation from mother on rhesus monkeys: Temporary absence of the mother affects behavioral development in rhesus monkeys (Macaca mulatta). Science, 173, 111-118. Johnson, R. L. (1986). Mother-infant contact and maternal maintenance activities among free-ranging rhesus monkeys. Primates, 27, 191-203. Kaufman, I. C., & Rosenblum, L. A. (1969). The waning of the mother-infant bond in two species of macaque. In B. M.Foss (Ed.), Determinantsofinfant behauiourZV(pp. 41-59). London: Methuen & Co. Ltd. Rosenblum, L. A., Clark, R. W., & Kaufman, I. C. (1964). Diurnal variations in mother-infant separation and sleep in two species of macaque. Journal of Comparative and Physiological Psychology, 58, 330-332. Rosenblum, L. A., & Kaufman, I. C. (1968). Variations in infant development and response to maternal loss in monkeys. American Journal of Orthopsychiatty, 38, 418-426. Rosenblum, L. A . , & Paully, G . S. (1984). The effects of varying environmental demands on maternal and infant behavior. Child Development, 55, 305-314. Rosenblum, L. A., & Sunderland, G . (1982). Feeding ecology and mother-infant relations. In L. W. Hoff, R. Gandelman, & H. R. Schiffman (Eds.), Parenting: Its causes and consequences (pp. 75-1 10). Hillsdale, NJ: Erlbaum. Seay, B., & Harlow, H. F. (1965). Maternal separation in the rhesus monkey. TheJournal of Nervous and Mental Disease, 140, 434-441. Sroufe, L. A. (1979). The coherence of individual development: Early care, attachment, and subsequent developmental issues. American Psychologist, 34, 834-841. Trivers, R. (1974). Parent-offspring conflict. American Zoologist, 14, 249-264. van de Rijt-Plooij, H. H. C., & Plooij, F. X. (1988). Mother-infant relations, conflict, stress and illness among free-ranging chimpanzees. Developmental Medicine and Child Neurology, 30, 306-3 15. Worlein, J. M., Eaton, G . G . , Johnson, D. F., & Glick, B. B. (1988). Mating season effects on motherinfant conflict in Japanese macaques, Macaca fuscata. Animal Behaviour, 36, 1472-1481.
c
MICHAEL W. ANDREWS LEONARD A. ROSENBLUM Department of Psychiatry State University of New York Brooklyn, New York
To explore behavioral patterns in bonnet macaque mother-infant dyads under environmental challenge, the motivation of infants to contact their mothers during a 1-hr foraging period was manipulated in two ways. First, sessions were given in which the infants were separated from their mothers for 3 hr prior to the foraging period. Second, sessions were given in which the infants were allowed access to food prior to the foraging period, thereby presumably reducing their motivation to separate from mother to seek food for themselves during the foraging period. Neither manipulation resulted in heightened conflict within the dyads. Separation of the infants prior to the foraging period did result, in general, in mothers forfeiting foraging task engagement to attend to their infants. The extent to which a mother exhibited this pattern correlated with her level of foraging effectiveness. 0 1993 John Wiley & Sons, Inc.
Introduction Our previous laboratory studies of the effects of various foraging demands on bonnet macaque mother-infant relations have demonstrated the ability of dyads to adjust to experimental situations which place a demand on the time and energy of the mother. When a mother is confronted with a physically and psychologically demanding circumstance, there can be long-term consequences for the future social and emotional behavior of the infant (Andrews & Rosenblum, 1988, 1991a; Rosenblum & Paully, 1984; Rosenblum & Sunderland, 1982). Despite these longReprint requests should be sent to Dr. Michael W. Andrews, Department of Psychiatry-Box 120, SUNY Health Science Center at Brooklyn, 450 Clarkson Avenue, Brooklyn, NY 11203, U.S.A. Received for publication 3 December 1991 Revised for publication 22 July 1992 Accepted at Wiley 28 July 1992
Developmental Psychobiology 25(8):557-566 (1992) 0 1993 by John Wiley & Sons, Inc.
CCC 0012- 1630/93/080557-10
558
ANDREWS AND ROSENBLUM
term consequences, if the foraging demand is relatively consistent and predictable during the developmental period, there may be little evidence of sustained, overt conflict within the dyad, rejection of the infant by the mother, or consistent signs of infant distress. Even when the time available for accomplishing the foraging task is rigidly circumscribed by the experimenter, dyads appear to make a relatively smooth adjustment to the situation (Andrews & Rosenblum, in press). Less predictable foraging requirements may result in greater infant emotional disturbance during the developmental period and more enduring affective changes in infants, although still without dramatic increases in overt maternal rejection or punishment (Rosenblum & Paully, 1984; Andrews & Rosenblum, 1991b). Although these findings are consistent with earlier data on the effect of feeding on dyadic cohesiveness in bonnet macaques (Rosenblum, Clark, & Kaufman, 1964), they are somewhat at odds with empirical findings on parent-offspring conflict (cf. Trivers, 1974) obtained with several other primate species. Increased demands on mothers deriving from mating activities have often been shown to increase dyadic conflict (e.g., Collinge, 1987; Fairbanks & McGuire, 1987; Hauser & Fairbanks, 1988; Worlein, Eaton, Johnson, & Glick, 1988). More directly pertinent to the present study, demands on mothers arising from feeding and foraging activities have also been found to alter dyadic interactions. Rosenblum, Clark, and Kaufman (1964) found that pigtail macaque mothers initiated more separations from their infants when confronting a feeding situation. Similarly, Johnson (1986) found maternal rejection in rhesus macaques to increase during feeding bouts. Despite the potential for increased dyadic conflict when mothers are feeding or foraging, baboon dyads, like bonnet macaque dyads, tend to avoid conflict during feeding bouts (Altmann, 1980). Altmann found, however, that changing conditions (e.g., infant weight gain by the 4th to 6th month resulting in preference by mothers for contact while resting) resulted in conflict prior to the restructuring of dyadic contact time. Consistent with the view that altered motivation for contact by mother and/or infant is likely to precipitate dyadic conflict, van de Rijt-Plooij and Plooij (1988) found that developmental reorganization of the young chimpanzee, characterized by increased seeking of maternal proximity, served as a trigger for subsequent dyadic conflict. Our goal in the current study was to further our understanding of the coping strategies and dynamic changes in the behavior of primate mother-infant dyads under conditions of altered motivation for infants to maintain contact with their mothers. Following the emphasis of our previous work, the dyads were studied while mothers were confronted with a foraging task made urgent by a limited time for acquisition of the day’s food ration. The putative motivation of infants to maintain contact with their mothers during the maternal foraging period was manipulated in two ways. In Phase I , infants were separated from the mother for several hours prior to the mother’s imposed foraging task; infant separation from mother has generally been reported to increase infant contact and reduce relatively distant separation for some time after reunion (Hinde & Spencer-Booth, 1971;Rosenblum & Kaufman, 1968; Seay & Harlow, 1965). In Phase 2 these partially self-feeding infants were allowed access to food in the preforaging period; inasmuch as the infants had previously been observed to obtain food items almost exclusively while out of dyadic contact, due largely to seeking food items dropped to the floor by
MACAQUE RESPONSE TO FORAGING TASK
559
adults, it was reasoned that prior feeding would diminish the infant’s own motivation to separate from mother to seek food during the foraging period.
Methods Subjects The subjects used in this study were 4 bonnet macaque (Macaca radiata) mother-infant dyads with previous experience in the experimental foraging task (Andrews & Rosenblum, in press). Two of the infants were male and 2 were female. At the beginning of Phase 1 the infants ranged in age from 6.5-7.5 months; at the beginning of Phase 2 the infants ranged in age from 8-9 months.
Study Environment The group of four dyads was housed in an indoor tile pen (2 m x 4 m x 2.1 m high); 2 one-way glass windows at the front of the pen permitted observation of the group. Perches were located at two levels within the pen. Water was provided ad libitum by animal-activated spigots. The pen lights remained on between 7 a.m. and 7 p.m. A special infant playpen (74 cm x 122 cm x 71 cm high) was located against the back wall of the living area and was constructed of 2.5 cm x 2.5 cm wire mesh. Two pass-through doors (8 cm x 15 cm), one at each end of the playpen, permitted access only by the infants. In addition to the infant playpen, a feeding structure (2.6 m long x 0.5 m wide x 0.7 m high) was located on the floor at the center of the pen. The structure was completely enclosed with the exception of 16 holes (5 cm x 5 cm) on each side, which provided access to 16 food pans (15 cm deep) during periods when food was available. The food in each pan was buried under 12 cm of clean woodchip bedding (See Andrews, Sunderland, & Rosenblum, in press, for further details of the feeding structure).
Procedures General. Monday through Friday of each experimental week the feeder was provisioned at 1 1 a.m.; an amount of food approximately 20% in excess of daily consumption was evenly distributed among the 16 food pans. The monkeys were given access to the feeder for 1 hr after which time all food pans were removed. From Friday afternoon to Monday morning the group was given free access to abundant food. These feeding procedures were quite adequate for maintaining the health of mothers and infants as revealed by daily health checks and weekly weighings. The manipulations of Phases 1 and 2 were carried out Tuesday through Friday of the experimental weeks. Phase 1. Four separations and four sham separations (separation controls) were performed over a 2-week period. The order of treatments was counterbalanced between weeks. On each of the 4 separation days all mothers and infants
560
ANDREWS AND ROSENBLUM
were separated at 8 a.m. The infants were removed to individual cages in another room; the mothers were returned to the home pen. At 11 a.m. the feeding structure was provisioned and observations began with the release of the infants into the home pen. On separation-control days, the mothers and infants were separated at 8 a.m. and immediately reunited in the home pen to control for handling effects. At 11 a.m. the feeding structure was provisioned and observations began. During the foraging hour each mother was the focal subject for a 200-s sample in each quarter hr. During a focal sample the following behaviors were continuously recorded: infant depart from dyadic contact, mother depart from dyadic contact, infant approach to dyadic contact, mother approach to dyadic contact, mother reject infant, mother deter infant in punitive manner, explore object, act dominant towards, act subordinate towards, forage, and obtain food item. In addition, at 2 0 5 intervals during focal observations the following behaviors were scored: spatial-social relationship of mother and infant (grooming, contact without grooming, out of contact but less than 0.3 m apart, or 0.3 m or more apart), eating, agitation, and grooming or passive contact with nondyadic partner. Of the following behaviors, those which were occurring at the time of conclusion of each focal observation were recorded for each infant: contact with mother, social play, affiliative contact with individual other than mother, exercise play, eating, and agitation or depression. See Andrews and Rosenblum (1991b) for further details on behavioral observations. Phase 2. Over a 2-week period, there were 4 days on which the infants received a food supplement prior to the foraging hr (prefeeding days) and 4 days on which the infants did not receive the supplement (prefeeding-control days). The order of treatments was counterbalanced between the 2 experimental weeks. On prefeeding days food was placed in the special infant enclosure at 9 a.m.; at 11 a.m. any food remaining in the infant enclosure was removed and the adult feeding structure was provisioned. Observations began as soon as the feeding structure had been provisioned. On prefeeding-control days no food was placed in the infant enclosure. The group feeding structure was provisioned at 11 a.m. and observations began immediately. Prior to the Phase 2 experimental weeks, it was established that all infants would eat food made available inside the infant enclosure. During the foraging hr each infant was the focal subject for a 200-s sample in each quarter hr; the behaviors scored for the infants in this phase were the same as those scored for mothers in Phase 1, with the exceptions that dominancesubordinance behaviors were dropped from the behaviors previously scored for mothers, and play and depressed behaviors were added to these previously scored behaviors. Following every 200-s focal observation, the occurrence of any of the following was recorded for each mother: hand in feeder while in contact with infant, hand in feeder while not in contact with infant, affiliative contact with individual other than own infant, agonistic interaction, exploration of inanimate object, and eating. Analysis. An estimation of dyadic separation bout length was based on the number of 20-s intervals of separation scored, on average, for each break in dyadic contact. Analysis of behavioral differences between conditions and across time were based upon a repeated-measures analysis of variance.
MACAQUE RESPONSE TO FORAGING TASK
561
Table 1 Percent of samples in which behaviors were scored, Phase 1 Condition Behavior
Separation
Control
df
F
P ~~~
Dyadic Contact Dyadic Grooming Infant Social Play Infant Exercise Play
61 11 0
7.5
33 4 7.5 15
1,3 1,3 1,3 1,3
27.6 6.5 25.0 49.0
~
< 0.05 ns
< 0.05 < 0.01
Results Phase 1 Dyadic Behaviors. In comparison to separation-control sessions, separations were clearly effective in increasing the amount of dyadic contact during the 1-hr foraging sessions. Dyadic contact following separations was nearly double that of control sessions (Table 1). The condition effect for dyadic contact was most pronounced in the first two replications, with little difference between the two conditions by the fourth replication (Fig. 1); this Condition x Replication effect was significant, F ( 3 , 9 ) = 11.45, p < 0.01. Changes in dyadic contact across the 1hr foraging period also differed between the two conditions. Following separations, dyadic contact started much higher and reached a peak earlier in the session than it did in control sessions (Fig. 2); this Condition x quarter-Session interaction effect was significant, F(3, 9) = 4.47, p < 0.05. Neither mothers nor infants exhibited a significant difference between conditions in the frequency with which they made or broke dyadic contact. Grooming was an important component of the dyadic contact following separations; although the overall difference between control and separation sessions was not significant, all four dyads exhibited more grooming following separations (Table 1). Moreover, as is evident in Figure 3, grooming rose more rapidly and to a higher peak following separations than it did in control sessions; this Condition x Quarter-Session interaction effect was highly significant, F(3, 9) = 18.84, p < 0.001. L=] SEPARATION CONTROL SEPARATION
REPLICATION
Fig. 1. Percentage of instantaneous samples in which dyadic contact was scored during the foraging hr by replication of the separation-control and separation conditions.
562
ANDREWS AND ROSENBLUM
QUARTER HOUR
Fig. 2 . Percentage of instantaneous samples in which dyadic contact was scored by quarter of the foraging hr for separation-corrtrol and separution conditions.
Consistent with the finding of greater dyadic contact during separation compared to control, and pointing to some degree of infant disturbance engendered by separations, both social and exercise play were significantly reduced following separations. Social play was completely absent following separations (Table 1). Exercise play following separations was only about half that of control sessions (Table 1). Feeding and Foraging. Based on daily food weighings before and after the foraging hr, there was no difference between control sessions and separation sessions in the mean amount of food obtained each day (454 g vs. 453 g). The mean number of observed foraging bouts by each subject dropped from 12.5 during control sessions to 11.0 in separation sessions, but this small decrease was not significant. Individual differences. tn addition to the general trends identified above, there were important individual differences in the responses of the mothers to the conflicting demands of their infants and the foraging task following the imposed separations. These differences were most pronounced in the 1st quarter of the foraging hr following separations when the motivation to feed was highest and the somewhat distressed infants had just been returned to the home cage. The mothers clearly differed from one another in food acquisition in the 1st quarter of the foraging hr in control sessions, a period in which 66% of all observed
3[
40
[ 0 a ,
SEPARATION CONTROL SEPARATION
T
QUARTER HOUR
Fig. 3 . Percentage of instantaneous samples in which dyadic grooming was scored by quarter of the foraging hr for separation-control and separation conditions.
MACAQUE RESPONSE TO FORAGING TASK
563
Table 2 Percent of samples in which behaviors were scored, Phase 2 Condition Prefed Quarter Hour Behavior
1st
2nd
3rd
Control Quarter Hour 4th
1st
2nd
3rd
4th ~~
Dyadic Contact Mothers Foraging Mothers Eating
6 28 85
9 I5 88
54 5
58
51 0 15
5 20 88
9 5 90
52 5 45
76 0 5
food acquisitions were made. These data were used to characterize the foraging effectiveness of the mothers in the current study. The percentages of total observed food discoveries in the 1st quarter hr made by each individual were 40.8%, 37.4%, 18.4%, and 3.4%. These foraging effectiveness scores in control sessions were highly correlated with dyadic contact scores in the first quarter of separation sessions, Pearson R = 0.96, p < 0.05; from most effective to least effective forager, the percentages of samples in dyadic contact in separation sessions were 75, 58, 17, and 8. Another measure following separation correlated with foraging effectiveness, but exhibited an inverse relationship; there was a strong negative correlation between control-trial foraging effectiveness scores and the changes in effectiveness following separations, Pearson R = -0.96, p < 0.05; from most effective to least effective forager, the changes, from 1st quarter of control sessions to 1st quarter of separation sessions, in mean number of food items found were -3.8, -1.8, -0.5, and +2.0.
Phase 2 Prefeeding Treatment. On prefeeding days, the 4 infants consumed a mean total of 112 g of food prior to the foraging hr. This resulted in a significant reduction in observed infant eating behavior during the foraging hr on these days compared to control days (13.5 bouts vs. 17 bouts), F(1, 3) = 61.74, p < 0.01. Dyadic Behaviors. Prefeeding the infants did not significantly influence the overall level of dyadic contact, frequency of initiation or termination of contact by mother or infant, or frequency of infant rejections. The length of dyadic separation bouts, however, was affected by prefeeding the infants. Separation bout length was significantly greater following prefeeding than it was in prefeeding-control sessions (94.6 s vs. 68.2 s), F(1, 3) = 154.09, p < 0.001. Although the infant prefeeding treatment did not influence the overall level of dyadic contact, contact was influenced by two factors. First, there was a significant increase in dyadic contact across quarter sessions under both control and prefeeding conditions, Table 2, F(3,9) = 32.50, p < 0.001. Second, there was a significant decrease in dyadic contact across replications for the prefeeding and control conditions, mean percent of 20-s intervals, M = 49,31,27, and 23 for each of four replications; F(3, 9) = 8.95, p < 0.01. Feeding and Foraging. Daily weighings of the provisioned food revealed no significant difference in the total amount of food that was dug from the bedding in
564
ANDREWS AND ROSENBLUM
the control and prefeeding conditions (516 g vs. 504 gj. There was, however, a significantly greater amount of foraging behavior by the mothers in the prefeeding condition, F( 1, 3) = 33.00, p < 0.05; the difference occurred in only the I st and 2nd quarters of the l-hr session (Table 2). The mothers also engaged in more eating behavior in the prefeeding condition than in the control condition, with feeding being elevated in the 3rd and 4th quarters of the prefeeding sessions, Table 2; F( 1, 3) = 1 9 . 1 1 , ~< 0.05.
Discussion The findings of this study support the view that the dyadic relationship in the bonnet macaque is highly resistant to overt parent-offspring conflict. For the 7month-old infants, increasing the motivation for attachment behaviors during the foraging hr by an immediately preceding separation between mothers and infants did not increase agitation or depression in the infants, rejection or punishment of infants by mothers, or frequency with which mothers terminated dyadic contact relative to control sessions, despite the continued need for mothers to engage in an urgent foraging task. Similarly, reducing the potential need of the 8.5-monthold infants to separate from their mothers to obtain some of the provisioned food by feeding the infants prior to the foraging hr did not result in heightened infant distress, rejection of infants, or punitive deterrence of infants in foraging hr following prefeeding compared to control hr; in fact, separation bouts were longer when the infants had been fed prior to the foraging hr than when they had not been prefed. Clearly, the dyads were generally able to meet the acute challenges to the dyadic relationship presented in this study with some degree of success. Although infant macaques in the 2nd half-year of life spend increasing periods apart from their mothers during various portions of the daylight period. they still spend long periods in sustained contact and periodic nursing and rapidly move to and maintain contact with the mother when disturbed (e.g., Hinde & SpencerBooth, 1967; Kaufman & Rosenblum, 1969). As might be anticipated, therefore, the dyadic separations that preceded the 1-hr foraging period in Phase 1 presented a greater challenge to the dyads and resulted in greater behavioral changes than did the subsequent prefeeding of these infants. For example, infant play was dramatically reduced following separations, but was unaffected by prefeeding. Similarly pointing to disruption of ongoing patterns of behavior by the 3-hr separations, dyadic contact during the foraging hr was significantly increased following separations; in general following separations, high levels of dyadic contact were maintained during the initial portion of the foraging hr, waning toward control levels by the end of the hr. Overall, although individual variations were apparent, there was a pattern of adjustment in which the mothers initially forfeited foraging activity to spend more time with their infants. The responses of the mothers to the foraging task upon the return of their infants appeared to be related to the foraging effectiveness of each mother during control sessions. Those mothers which most readily obtained food items in control sessions were also the most likely to accommodate their somewhat distressed infants in the separation sessions by restructuring contact time at the cost of some initial foraging success. Accommodation, within the constraints of the present
MACAQUE RESPONSE TO FORAGING TASK
565
design, was rapid. There was little evidence of dyadic conflict regardless of the extent of accommodation. In conclusion, the ability of the four dyads to adapt to the perturbations presented in this study was quite evident in the failure of these manipulations to induce overt or sustained conflict within the dyads. The data suggest, however, that the contingent responsivity of a mother to her infant may be influenced by the control which she has over the accomplishment of other critical tasks in her life. In the present study, the more readily a mother was able to obtain food items, the more responsive she was to her returning infant at the expense of initial foraging effort. Such a difference in contingent responsivity during early rearing may have important consequences for the security of infant-mother attachment (e.g., Ainsworth, Bell, & Stayton, 1971; Andrews & Rosenblurn, 1991b) and the long-term development of social competency in the infants (e.g., Andrews & Rosenblum, 1991a; Bakeman & Brown, 1980; Sroufe, 1979). Experimental manipulations of both mothers’ and infants’ motivations for attachment-related responses at various stages of infant development (particularly with respect to independent feeding and locomotion) and in diverse social settings should provide useful data in broadening our understanding of the dynamic processes which underlie the maintenance and ultimate diminution of the dyadic bond.
Notes The research reported in this article was supported by USPHS Grant MH15965 and funds from the State University of New York.
References Ainsworth, M. D. S., Bell, S. M. V., &Stayton, D. J . (1971). Individualdifferences instrange-situation behaviour of one-year-olds. In H. R. SchalTer (Ed.), The origins of human social relations (pp. 17-57). New York: Academic Press. Altmann, J. (1980). Baboon mothers and infants. Cambridge: Harvard University Press. Andrews, M. W., & Rosenblum, L. A. (1988). Relationship between foraging and affiliative social referencing in primates. In J. E. Fa & C. H. Southwick (Eds.), Ecology and behavior offoodenhanced primate groups (pp. 247-268). New York: Alan R. Liss, Inc. Andrews, M. W . , & Rosenblum, L. A. (1991a). Dominance and social competence in differentially reared bonnet macaques. In A. Ehara, T. Kimura, 0. Takenaka, & M. Iwamoto (Eds.), Primatology today (pp. 347-350). Amsterdam: Elsevier Science Publishers B. V. Andrews, M. W., & Rosenblum, L. A. (1991b). Security of attachment in infants raised in variable- or low-demand environments. Child Development, 62, 686-693. Andrews, M. W., & Rosenblum, L. A. (in press). Dyadic bond maintenance in bonnet macaques under acute challenges. International Journal of Methods in Psychiatric Research. Andrews, M. W., Sunderland, G., & Rosenblum, L. A. (in press). Impact of foraging demand on conflict within mother-infant dyads. In W. A. Mason & S. P. Mendoza (Eds.), Primate socid conflict. Albany: SUNY Press. Bakeman, R., & Brown, J. V. (1980). Early interaction: Consequences for social and mental development at three years. Child Development, 51, 437-447. Collinge, N. E. (1987). Weaning variability in semi-free-ranging Japanese macaques (Macacafuscata). Folia Primatologica, 48, 137-150. Fairbanks, L. A., & McGuire, M. T. (1987). Mother-infant relationships in vervet monkeys: Response to new adult males. International Journal of Primatology, 8, 351-365. Hauser, M. D., & Fairbanks, L. A. (1988). Mother-offspring conflict in vervet monkeys: Variation in reponse to ecological conditions. Animal Behauiour, 36, 802-8 13.
566
ANDREWS AND ROSENBLUM
Hinde, R. A., & Spencer-Booth, Y. (1967). The behaviour of socially living rhesus monkeys in their first two and a half years. Animal Behaviour, 15, 169-196. Hinde, R. A . , & Spencer-Booth, Y. (1971). Effects of brief separation from mother on rhesus monkeys: Temporary absence of the mother affects behavioral development in rhesus monkeys (Macaca mulatta). Science, 173, 111-118. Johnson, R. L. (1986). Mother-infant contact and maternal maintenance activities among free-ranging rhesus monkeys. Primates, 27, 191-203. Kaufman, I. C., & Rosenblum, L. A. (1969). The waning of the mother-infant bond in two species of macaque. In B. M.Foss (Ed.), Determinantsofinfant behauiourZV(pp. 41-59). London: Methuen & Co. Ltd. Rosenblum, L. A., Clark, R. W., & Kaufman, I. C. (1964). Diurnal variations in mother-infant separation and sleep in two species of macaque. Journal of Comparative and Physiological Psychology, 58, 330-332. Rosenblum, L. A., & Kaufman, I. C. (1968). Variations in infant development and response to maternal loss in monkeys. American Journal of Orthopsychiatty, 38, 418-426. Rosenblum, L. A . , & Paully, G . S. (1984). The effects of varying environmental demands on maternal and infant behavior. Child Development, 55, 305-314. Rosenblum, L. A., & Sunderland, G . (1982). Feeding ecology and mother-infant relations. In L. W. Hoff, R. Gandelman, & H. R. Schiffman (Eds.), Parenting: Its causes and consequences (pp. 75-1 10). Hillsdale, NJ: Erlbaum. Seay, B., & Harlow, H. F. (1965). Maternal separation in the rhesus monkey. TheJournal of Nervous and Mental Disease, 140, 434-441. Sroufe, L. A. (1979). The coherence of individual development: Early care, attachment, and subsequent developmental issues. American Psychologist, 34, 834-841. Trivers, R. (1974). Parent-offspring conflict. American Zoologist, 14, 249-264. van de Rijt-Plooij, H. H. C., & Plooij, F. X. (1988). Mother-infant relations, conflict, stress and illness among free-ranging chimpanzees. Developmental Medicine and Child Neurology, 30, 306-3 15. Worlein, J. M., Eaton, G . G . , Johnson, D. F., & Glick, B. B. (1988). Mating season effects on motherinfant conflict in Japanese macaques, Macaca fuscata. Animal Behaviour, 36, 1472-1481.
