The ontogeny of social relationships with group companions among free-ranging infant rhesus monkeys I. Social networks and differentiation

Social networks of infant rhesus monkeys (Macaca mulatta) in a free-ranging, lineage-based group on Cayo Santiago are described by assessing the extent to which four measures of positive interaction between infants and finely-divided categories of companions are associated with (1) degree of relatedness through maternal lines; (2) sex of the companion; (3) age of the companion; and (4) dominance rank of the infant's lineage. The results suggest that the infant's social network mirrors that of its mother both in the first weeks of life and as late as 30 weeks of age. Infants have more positive social interaction with close kin than with distant kin or with unrelated individuals, and thus function as members of their lineage from the beginning. They associate more with female companions than with male companions, and more with younger immatures than with older immatures. Finally, infants in the top-ranking lineage spend more time with their own relatives than do infants in other lineages. The fact that these patterns change little as the infant gains independence from the mother supports suggestions that early maternal influence serves to pass on aspects of the mother's social network. It is suggested that the ontogeny of early social relationships resembles a process of differentiation.     

Early agonistic experience and rank acquisition among free-ranging infant rhesus monkeys

Several aspects of agonistic experience are described for freeranging infant rhesus monkeys (Macaca mulatta)on Cayo Santiago. Even before infants are fully integrated with peers in rank dominance based on maternal ranks,infants of highranking mothers tend to be threatened less frequently by other members of the group and are less likely to be threatened by unfamiliar individuals than are infants of lowranking mothers. There is no evidence that fearful interactions between pairs of infants are related to their mother’s ranks before 22 weeks of age. However, an imperfect hierarchy can be constructed for infants between 27 and 30 weeks of age. At this age,infants of higherranking mothers are also more likely to receive protection when threatened than are infants of lowerranking mothers. When protected, their protectors are less likely to emit fearful gestures to the infants’ threatener. Close female relatives appear to play a large role in the protection of infants and may be more directly responsible for the differences described above than the mother, other relatives, or other highranking members of the group. It is suggested that more than one mechanism, including intervention by the mother and by close female relatives,may be important in rank acquisition among peers.     

Group and matriline differences in the behaviour of rhesus monkey infants

A ‘Monte Carlo’ method was developed for characterizing matrilines of rhesus monkey infants (Macaca mulatta) born to their mothers within six similar captive social groups, according to behavioural measures, and for characterizing social groups according to their matrilines' median scores. Eight- and 16-week-old infants differed according to their groups, but not according to their matrilines, in measures of their activity in the vicinity of their mothers, and the frequencies with which social companions other than the mother initiated social contacts with them while they were out of contact with their mothers. Sixteen-week-olds differed according to their groups in the frequencies with which their mothers rejected them, and 8-week-olds in the frequencies of the social contacts they initiated with companions other than mother while off their mothers. When tested with their mothers, in a mildly disturbing situation away from other social companions, 52-week-olds differed according to their group of origin in time spent out of contact with their mothers. Different groups were seen as producing infants differing in ‘enterprise’ from their eighth week, in the sense of being ready to initiate social contacts with others while off their mothers at 8 weeks, and of being off their mothers in the test at 52 weeks. Cases where the 8-week measures did not reflect infant enterprise could be explained in terms of other aspects of the relationships involving the infants and their mothers in the social group. In particular, matrilines differed consistently in dominance status, and some mothers also received high levels of aggression from other adults. Mothers receiving high levels of aggression were more responsible for maintaining proximity with their 8-week-old infants, and their 8-week-olds were less often involved in social contacts with others.     

Social behavior of infant and mother Japanese Macaques (Macaca fuscata): Effects of kinship,partner sex,and infant sex

The behavioral interactions of 22 infant and mother Japanese macaques with other group members were studied. Focal-animal observations were made from the time of each infant’s birth until 1 year of age. Infants and mothers both displayed exceedingly strong preferences for associating with matrilineal kin and, specifically, for female kin. The degree of genetic relatedness was positively correlated with levels of spatial proximity, contact, grooming, aggression, and play. Overall frequencies of interactions with nonkin were very low, and partner sex was not an important factor in interactions with nonkin. There were no significant differences between male and female infants in interactions with kin versus nonkin. There was only one significant difference between male and female infants in interactions with males versus females: female infants showed stronger preferences for initiating proximity with females over males than did male infants. Because mothers provide the focal point for infant interactions during the first year of life, we compared the behavior of infants and mothers. Mothers were the recipients of more social interactions than were infants, mothers engaged in more grooming than did infants, and infants engaged in more social play than did mothers. These findings are only partially consistent with kin-selection theory, and the inadequacies of studying matrilineal kin discrimination to test kin selection are reviewed. The near-absence of infant sex differences in associations with social partners suggests that although maternal kin other than the mother are important to infant socialization, they probably do not contribute to the development of behavioral sex differences until after the first year of life.     

Changes in the rhesus mother-infant relationship through the first four months of life

Measurements of the course of interactions between rhesus monkey infants (Macaca mulatta) and their mothers during the infant's first 16 weeks showed changes in the tendencies of both partners to be together and apart. Referring only to the partner who was primarily responsible for an age-related change, by using a single index of responsibility for contact or proximity, was found to be an oversimplification. Maternal rejecting behaviour may have been primarily responsible for changes in the time spent apart only during the first 6 weeks. After the infants' sixth week, both partners' tendencies to be apart increased together. Infants then began to spend longer away partly to interact with social companions other than their mother. Mothers restricted and followed their infants more up to week 4, but after week 8 decreases in these measures allowed infants to spend longer away. Similarities between the time courses of the time spent apart from their mothers by rhesus infants in this study and in field studies are pointed out. The similarities seem striking partly because differences between studies that do not use confidence intervals (or standard errors) cannot be shown easily. Conflict between parent and infant occurred, but how it appears, and how significant it is in each species at each infant age, remains to be discovered.     

Prior experience of risk and individual differences in enterprise shown by rhesus monkey infants in the second half of their first year

A review of the literature suggested that animals exposed to more risk in their social groups should be more enterprising. Rhesus monkey infants of 37 to 44 weeks were attracted to bait in places out of their mothers' reach. The tests were run in the home pen, in the absence of social companions apart from a sibling in its second year of life, if present. In each test the bait was a sawdust and grain mixture, with two or three raisins, and enterprise was measured in terms of the number of raisins taken. Before the test period, the infants had lived in small stable captive social groups. Infants of non-top-ranking mothers took more raisins than infants of top-ranking mothers, if infants subject to high levels of aggression from their own mothers or from the adult males in their groups, were excluded. Observations of the group in a competitive foraging situation confirmed that non-to-ranking infants should be at greater risk than top-ranking ones. The infants receiving notably high levels of aggression from their mothers or the adult males in their groups took more raisins than the remainder. These results are consistent with the view that experience of risk in a social group can promote enterprise in rhesus monkey infants of less than a year old. The problems of assessing “risk” faced by socially living animals, and the mechanisms whereby experience of risk could enhance enterprise, ere discussed.     

The ontogeny of social play in a feral troop of vervet monkeys (Cercopithecus aethiops sabaeus): The function of early play

We describe the ontogeny of social play over the first 30 weeks of age in a troop of feral vervet monkeys (Cercopithecus aethiops sabaeus) in Barbados. Play time increased rapidly for the first 10 weeks but remained relatively constant thereafter. The form of play changed with infant age; bouts became more frequent but of shorter duration. Play time, bout frequency, and bout duration at a given age differed between infants; younger infants altered their play patterns to complement those of older infants. All infants played more within their own year class than with older juveniles; play time increased with decreasing age difference between the infant and the play partner. Infants terminated a higher proportion of their play bouts the greater the age difference between themselves and their play partners. Preferred play partners are therefore individuals of similar age that will be similar in size and have matched motivation to play and form of play. Neither play time nor proportion of bouts initiated or terminated was correlated with the social rank of the play partner, which suggests that play is not directed toward individuals that may be high-value alliance partners. Maternal intervention in play occurred primarily when infants were<10 weeks old. It was not correlated with the age or social rank of the mother or with the age or social rank of her infant's play partner. Infants played more and terminated a lower proportion of their play bouts in the absence of their mothers than in their presence. Our results are consistent with the hypothesis that the primary function of early play is to enhance physical fitness and to develop coordination and other fighting skills, with minimal risk of injury.     

Calf development and mother-calf spatial relationships in Southern right whales

Changes in spatial relationships between mother and calf right whales (Eubalaena australis) from birth to the separation of yearling calves from their mothers were observed. During the first few weeks of a calf's life, mother and calf were within close proximity over 90% of the time, and mothers were responsible for maintenance of contact with their infants. Later calves strayed farther and initiated many more leaves and approaches than their quiescent mothers. The mothers still maintained contact with their infants. Just before migration away from the area, pair members resumed close proximity and leaves and approaches by both diminished. Yearling calves, returning to the area with their mothers after six months, stayed close to their mothers and few leaves and approaches by either pair member were recorded. The yearling calves were responsible for maintaining contact as the mothers left them more than approached them. This behaviour on the part of mothers probably contributed to weaning of yearlings and separation after a few weeks in the area.     

How rhesus monkey mothers and infants keep in touch when infants are at risk from social companions

Ten-to 17-week-old rhesus monkey infants that received hits from companions other than their mother at high rates (relative to their rates of involvement in playful social encounters with those companions) tended to be members of mother-infant dyads that were vigilant. Criteria of vigilance were frequent contacts between mother and infant during the first 5 sec of the infants’ social encounters and/or a bias of mother-infant contacts toward that time. Infants that received few hits per encounter came from both vigilant and nonvigilant dyads. When analyzed alone, mothers’ rates showed the same trends. High levels of vigilance tended to reduce infants’rates of making social contacts. Maternal social rank and other measures of the infants’ social involvement were not correlated with vigilance. There is no evidence that mothers and infants were in conflict with each other about interrupting the infants’ encounters. Understanding vigilance becomes important whenever vigilant activity conflicts with other activities. Special problems arise because decisions about vigilance levels require judgments of risk based on the kinds of events that occur only rarely if vigilance is effective. A model providing a framework for studies of vigilance against the risks of infants’ social activities was developed. It recognizes that (1) risk-reducing vigilant behavior can conflict with acquiring information about risk; (2) in social situations where reliable estimates of risk are impossible, individuals might follow rules of thumb (e.g., be restrictive) rather than modify behavior moment by moment according to the current situation;and (3) at the dyad’s optimum balance between vigilance for the current infant and investment in subsequent off-spring, the infant will not be totally protected, so that while dyads at higher risks are more vigilant, the risks are also realized to a greater extent (e.g., itin terms of the number of hits received per encounter).     

Grooming and Infant Handling Interchange in <Emphasis Type="Italic">Macaca fascicularis</Emphasis>: The Relationship Between Infant Supply and Grooming Payment

Female long-tailed macaques are attracted to infants and frequently groom mothers bearing them. Such grooming often involves the groomer contacting the infant and may be a trade of grooming for infant handling. To identify if grooming and infant handling are directly traded, I collected samples on times after female-to-mother grooming and on interactions in which a female groomed a mother and contacted her infant. I determined that grooming tended to promote an exchange with infant handling and that the supply of available infants was related to how long a female groomed a mother. Grooming interactions were longer when infants were scarce in the surrounding social environment than when they were abundant, indicating a possible supply-and-demand effect. This supports that grooming may be payment for infant handling. Grooming-infant handling interchanges tended to be unidirectional as mothers usually did not reciprocate grooming. Instead, infant contact occurred. A larger proportion of grooming-infant handling interchanges involved younger infants, but infant age did not seem to influence grooming durations. The length of female-to-mother grooming had no observable effect on handling time. Lower-ranked females groomed higher-ranked mothers and their infants longer than vice versa. Moreover, it was possible to predict up-rank grooming via supply and demand better than down-rank grooming. There was no observable influence of kinship on grooming-infant handling interchange. These results support the conclusion that grooming and infant handling may be traded. Grooming promoted infant handling, while supply and rank predicted the grooming payment a female would offer to access an infant.     

Emergence of individual recognition in young macaques

Few studies have addressed the development of nonhuman primate infants' responses to conspecific vocalizations. Previous studies showed that the appropriate response to alarm, intergroup and long-distance contact calls emerged at about 6 months of age. It remained unclear whether this age constitutes a watershed in terms of infants' sociocognitive development or whether it was due to the types of stimuli used in the experiments. I therefore examined the development of infant Barbary macaque, Macaca sylvanus, responses to maternal calls, under the assumption that recognition of the mother is one of the tasks that infants should master as early as possible. I presented infants of different age categories with short bouts of screams recorded from their mothers or another female of the same social group. Experiments on yearlings confirmed the suitability of the experimental approach: yearlings responded significantly more strongly to maternal calls than to calls from unrelated females. Infants were tested at 4, 10 and 16 weeks of age. In the youngest age group, they failed to respond to the playbacks, whereas from 10 weeks of age on they responded significantly more strongly to maternal calls, suggesting that by this age they recognized their mothers by voice. These results suggest that the developmental trajectories in the domain of comprehension learning may be flexible, in the sense that infant responses may depend on the salience of, and the exposure to, the call type under study. The experiments also show that screams may transmit individual-specific characteristics that are perceptually salient to the listeners.     

Mother-offspring conflict and interference at mother's mating inMacaca fascicularis

Theory suggests that it is in the interest of an infant to garner more care than its mother is selected to provide and that a rival sibling would curtail care from the mother. Thus delayed conception in the mother would be of advantage to the infant. One method of achieving this result would be to interfere with the mother's potential matings. To test this theory, the conflict between mothers and their infants in relation to maximizing inclusive fitness has been studied inMacaca fascicularis and infant interference has been observed. Focal animal samples were taken on 8 mothers and their 13 infants. Interactions analyzed were those between the mother and (1) an adult male, (2) her infant, (3) an adult female, (4) her infant and an adult male, (5) her infant and an adult female. Only explicit behaviours were analyzed. The infant's interference was found to be significantly related to its mother's mating, and this produced a deterring effect on the male. Infants did not interfere with any female's matings other than those of their mother. The interference was related to the number of mother-male contacts. In mothers that did subsequently conceive, infant interference at mating increased up to the mother's conception date and decreased thereafter. By contrast to the infants direct method, mothers approached the conflict indirectly. There were significantly more contacts and mounts with males in their infant's absence, they reacted negatively to their infant only when it had interfered, they were more lenient in the presence of an adult female than with an adult male, and they avoided their infant's presence at mother-male contacts. No significant sex bias in interference or the number of contacts with mother-male pairs has been found. There are indications of a sibship pattern of interference.     

Sex differences in the termination of social play in cats

Sixteen measures of social play between kittens were found to decrease significantly between 12 and 16 weeks of age. Behaviour was little influenced by the presence of the mother during this time. Although males' rates of behaviour did not differ from females' rates when the sexes were compared regardless of group composition, males from all-male groups played at higher rates than females from all-female groups. Females' rates of behaviour declined as the number of male companions decreased. Males' behaviour was little influenced by the number of females in the group. Females with male companions behaved more like males than did females with no male companions, but this was not because they directed behaviour to brothers at higher rates than to sisters.     

A case of infant swapping by wild northern muriquis (<Emphasis Type="Italic">Brachyteles hypoxanthus</Emphasis>)

Allo-parenting has been observed in a variety of female primates, and typically infants are reunited with their biological mothers assuming that their mothers are alive. We observed an exception to this pattern when two wild northern muriquis (Brachyteles hypoxanthus) exchanged infants of different sexes and then reared their adopted infants through weaning. The process of this exchange began when the infants were 4 and 8 days old, respectively. The mother of a 4-day old female carried and nursed her own daughter and the 8-day old son of a second female. The exchange ended when the second mother was first observed carrying the wrong infant 1.5 days later. This observation raises questions about the age and mechanisms of mother–infant recognition in this species, and about assumptions of mother–infant relatedness based on behavioral observations alone.     

Development of activity patterns,social interactions,and exploratory behavior in infant tufted capuchins (Cebus apella)

Early organization of activity states was studied in 17 tufted capuchin (Cebus apella) infants from birth to 11 weeks of age. Development of exploration and interactions with mothers and other group members were studied in 14 of these infants up to the age of 1 year. Activity profiles changed from 3 to 8 weeks as infants began to move off mothers and explore their environments. From 2 to 6 months time with mothers decreased; time alone increased correspondingly. Time spent with other group members did not vary significantly over the first year. By 7–9 months capuchin infants spent more time alone or with other group members than with mothers, although weaning was still not completed by the end of the first year. Simple environmental exploration began in the 2nd month and reached stable levels by 4 months. Complex manipulation of food and objects first began at 3–4 months and increased to stable levels in the second half of the first year. Some preliminary differences were evident between infants living in indoor cages and those living in indoor/ outdoor runs. Infants in cages spent less time in dorsal contact with mothers, and less time in social play and proximity to other animals than those in runs. Instead, infants in cages spent more time alone and engaged in more manipulation of food. Some measures of social and exploratory behavior showed a high degree of variability which may be useful in exploring individual differences in infant temperament or reactivity. © 1995 Wiley-Liss, Inc.     

Mating season effects on mother-infant conflict in Japanese macaques,Macaca fuscata

The impact of seasonal mating on the mother-infant relationship during the first year of the infant's life was documented in a confined troop of Japanese macaques. During the weeks in which the mothers were being mounted, negative behaviour directed towards the infants increased. As maternal rejections and punishments escalated, the infants displayed regressive behaviour (showing signs of distress more frequently). Infants also groomed their mothers at an increased rate at this time. Behaviour that indicated increased independence did not show increases during this time. Moreover, behaviour negatively associated with independence, such as ventral contact and proximity to the mother, remained stable throughout this time period. The mother-infant relationship undergoes a period of conflict during the mating season not because the mother is weaning her infant, but because it is to her reproductive advantage to regulate the times in which the infant is allowed to suckle.     

Mother-infant interactions in captive slow lorises (Nycticebus coucang)

Information is presented about mother-infant interactions and infant development in a rarely studied prosimian primate, the slow loris (Nycticebus coucang). Four dyads were observed, by means of closed circuit TV, in a semi-natural environment for 1 hour per day three times a week. Infants were inactive for the first 6–8 weeks. Although mothers carried infants, they also left them alone for substantial periods of time after the 1st week. Over the 20-week study period, there was a significant decline in ventral contact but not in sitting within 12 inches or engaging in active social interactions. By the end of the study, infants were not yet fully independent. Three of the 4 were primarily responsible for maintaining physical closeness to the mother; they made most of the approaches and mothers made most of the departures. However, only 2 of the 4 infants had assumed responsibility for the initiation and maintenance of social interactions with the mother. By comparison with other nocturnal prosimians of similar size, the rate of development is relatively slow. Unlike many anthropoids, mothers were not strongly protective or rejecting. They did not bring infants back to a fixed location or try to prevent infants from leaving them; and the decline in ventral contact was not accompanied by fights between the pair. The 3 group-living mothers were more protective than the single individually housed mother, and it would seem advisable to isolate mother-infant pairs in laboratory breeding colonies.     

Natal Attraction in Adult Female Baboons (Papio cynocephalus ursinus) in the Moremi Reserve, Botswana

Mammalian females are strongly attracted to infants and interact regularly with them. Female baboons make persistent attempts to touch, nuzzle, smell and inspect other females’ infants, but do not hold them for long periods, carry them, or provide other kinds of care for them. Mothers generally tolerate these interactions, but never initiate them. The function of these brief alloparental interactions is not well understood. Infant handling might be a form of reproductive competition if females’ interest in infants causes distress to mothers or harm to their infants. Alternatively, infant handling might be the product of selection for appropriate maternal care if females who are highly responsive to infants are the most successful mothers. We test several predictions derived from these hypotheses with data collected in a free‐ranging group of baboons (Papio cynocephalus ursinus) in the Moremi Reserve of Botswana. Infants were most attractive when they were very young. Mothers of young infants were approached by other adult females on average once every 6 min, and other females attempted to handle their infants approximately once every 9 min. By the time infants were a year old, their mothers were being approached only once every 30 min and infants were being handled only once every 5 h. Females were more strongly attracted to other females’ infants when they had young infants of their own, and their interest in other females’ infants declined as their own infants matured. Females seemed to be equally attracted to all infants, but had greater access to offspring of their relatives and subordinate females. Females nearly always grunted as they handled infants. As in other contexts grunts are a reliable predictive signal that non‐aggressive behavior will follow, the use of grunts before handling suggests that these interactions were not a form of deliberate harassment.     

Early infant development and maternal care in free-ranging vervet monkeys

The interactions of infant vervet monkeys (Cercopithecus aethiops) with their mothers were examined during the first 12 weeks of life. During this period there was a gradual rise in behaviour associated with increasing independence from the mother: female infants were slightly advanced over males on measures of decreasing contact with mothers and increasing rejections from the nipple. There were differences between the mothers in the ways they interacted with their infants such that no consistent maternal styles could be defined. Dominance rank of the mother did however influence her behaviour towards her infant, and high ranking mothers tended to be less rejecting towards sons, but more rejecting towards daughters, than were low ranking mothers. It is suggested that since vervet mothers have access to allomothers they may not be limited to dichotomous mothering styles.     

Fatal attraction: interest in infants and infant abuse in rhesus macaques.

This study investigated whether infant abuse by female rhesus macaques (Macaca mulatta) is a phenomenon specific to their own offspring or reflects a general tendency to interact negatively with infants. Several aspects of the relationship between maternal behavior, infant handling, and infant harassment were also investigated. Study subjects were 20 group-living rhesus mothers with their infants observed during the first 12 weeks of lactation. The results of this study indicate that abusive mothers are highly attracted to infants in general but that infant abuse is a phenomenon specific to their own offspring. Infant harassment is not an accidental by-product of infant handling or the result of maternal inexperience but it is likely related to reproductive competition among lactating females. Maternal behavior and infant handling may be regulated by similar proximate mechanisms, but probably have different adaptive functions and evolutionary history across the Primate order. Am J Phys Anthropol 110:17-25.