Patterns of infant handling and relatedness in Barbary macaques (<Emphasis Type="Italic">Macaca sylvanus</Emphasis>) on Gibraltar

Among papionin primates, the Barbary macaque (Macaca sylvanus) shows the most extensive interactions between infants and group members other than the mother. Two different types of interactions occur: (1) long-lasting dyadic interactions between a handler and an infant, and (2) brief triadic interactions between two handlers involving an infant. Previous investigations showed that infant handling by males is best explained as use of infants to manage relationships with other males. In contrast, no adaptive explanation for infant handling by females emerged. Here, we compared the infant-handling pattern between subadult/adult males and subadult/adult females in a free-ranging group of 46 Barbary macaques on Gibraltar to test whether the relationship management hypothesis also applies to female handlers. We further investigated the infant-handling pattern of juveniles and used microsatellite markers to estimate relatedness between infant handlers and the infant’s mother. We found that males, females and juveniles all participated extensively in triadic interactions using infants of above-average related females. In contrast, only males and juveniles were highly involved in dyadic interactions with infants of related females, while females rarely handled infants other than their own. The pattern of infant handling was entirely compatible with the predictions of the relationship management hypothesis for males and mostly so for females. Moreover, our genetic analysis revealed that males and females differ in their partner choice: while females preferred to interact with related females, males had no significant preference to interact with related males. We further discuss the observed above-average relatedness values between infant handlers and the infant’s mother in the light of kin-selection theory.     

Effects of six-day maternal separation on tonkean macaque infants

Maternal separation may induce a depressive state in infant macaques. However, this does not occur in all macaque species. From present hypotheses, it may be predicted that infants belonging to a species characterized by open and tolerant social relationships should not develop severe depressive symptoms. Tonkean macaques (Macaca tonkeana) stand as such a species. The goal of the study was to verify that the infant’s reaction to mother loss is related to the social environment. The mothers of eight 5- to 9-month-old infants were removed during 6-day experimental periods. Infants’ behavior was characterized by a mild initial protest stage, followed by a slight decrease in activity during later maternal separation, and quick recovery after the mother’s return. No despair stage occurred. During separation, group members compensated for mother’s absence by cradling the infants. That social networks determine the intensity of the infant’s response to separation has far-reaching implications with regard to the meaning of depression occurrence within social networks.     

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.     

The range of action of the mother and the avoidance of big novel objects in long-tailed macaques

Most surrogate-reared long-tailed macaques persistently avoid a big novel object, whereas most mother-reared subjects approach it. A striking difference between these attachment figures is that the mothers moved about with their infants, whereas the surrogates were fixed to the wall In this experiment, we aimed to find out whether mobility of the attachment figure plays a part in the development of an infant’s responses to big novel objects. We studied the effects of mobility of the attachment figure by restraining mothers in their range of action. We confined mothers of the experimental group in a small part of the home cage. Their infants could leave the cage in which their mothers were restrained. Infants that were growing up with unrestrained mothers made up the control group. At two different ages all infants encountered a big novel object. We used two different objects. We found that the range of action of the mother did not significantly affect the responses of infants to big novel objects. As in the previous studies, most of the mother-reared monkeys approached the objects. The age at which an infant was first exposed to an object did not significantly affect its behavior toward it. Further, the two different objects evoked the same reactions.     

Infanticide following male takeover event in Verreaux’s sifaka (<Emphasis Type="Italic">Propithecus verreauxi verreauxi</Emphasis>)

Two infanticides occurred after a male takeover in a population of Verreaux’s sifaka (Propithecus verreauxi verreauxi) at Beza Mahafaly Special Reserve, Madagascar. The first infant was found dying from wounds received to the chest and groin after three adult males had immigrated into the group. The second infanticide was directly observed 2 weeks later when one of the immigrant males targeted and attacked the infant after it was separated from its mother. The directed nature of the attack suggests that the infant’s death was not a result of generalized aggression during a period of increased group instability. Although the sexual selection argument does not fully explain infanticidal events in seasonally breeding lemurs, such as Verreaux’s sifaka, it is clear that transferring males present a measurable threat to infant survival and female reproductive success in this species.     

Sexually dimorphic transitions revealed in the relationships of yearling rhesus monkeys following the birth of siblings

We report here that in a large captive group of monkeys, Macaca mulatta,sudden sex-related changes occur in social interactions in one short phase of an infant’s development. Social interactions of 1-year-old animals (males, N =12; females, N =8) 6 weeks before the birth of siblings were compared with interactions occurring 6 weeks after the birth. On the day of the siblings’ birth, depression-like postures were seen in two yearling males (YMs); 10 YMs showed hyperactivity. In the postbirth period, YMs refocused their attentions away from their mother and toward other, often unrelated members of the group. Although YMs initiated disengagement of interactions with their mothers, there was evidence that mothers attempted to lessen this disengagement. The YMs had close relationships with specific (“preferred”) male individuals. These relationships (particularly those with adult males) became more pronounced following the birth of the sibling. The adult-male group also took an active role in maintaining interactions with YMs. The preferred partners in the YM-other male relationship before the birth of the sibling were, however, not always the same as those in the period after the birth. Dominance relationships and probably genetic factors determined patterns of interaction between YMs and their preferred male partners. Among yearling females (YFs), no dramatic changes in interactions with their mothers or with other group members were detected after their mothers gave birth. Relationships in YF-mother and YF-other-individual pairs (especially when the other individual was kin) seemed to be consolidated during the postbirth interval. There was little evidence of jealousy between the YFs and their younger siblings. Thus, sibling birth acted as a stimulus for the occurrence of sexually dimorphic interactions in yearlings. We suggest that in natural environments, social interactions in YFs promote relationships that will serve to integrate them into the matrilineal social structure, whereas comparable behavior in YMs encourages relationships with males that they may emigrate with into, or meet again in, nonnatal troops.     

Mother-infant relationships in Vervet Monkeys: Response to new adult males

The reaction of mothers to replacement of breeding adult males was studied in two captive groups of vervet monkeys. Mother-infant behavior for 15 infants born in the season following the introduction of new males was compared to mother-infant behavior for 35 infants born with adult males that had been resident in the group for more than a year. The mothers responded to the presence of new males by being more protective toward their infants in the first 3 months. Increased protectiveness disappeared in the second 3 months, and in the infant’s sixth month of life mothers with new males in the group became more rejecting than mothers with long-term resident males. The combination of increased protectiveness and increased rejection was unusual among the mothers with long-term resident males but was the most common mothering style used in the presence of new males. The rate of rejection was inversely correlated with the interbirth interval, and mothers with new males in the group conceived sooner and had significantly shorter inter-birth intervals compared to mothers with long-term resident males.     

Targeted helping by a wild adolescent male chimpanzee (Pan troglodytes verus): evidence for empathy?

In a unique case where a chimpanzee infant captured by human poachers was returned by researchers to her natal group, an adolescent male helped the injured mother carry her infant on each of 2 days following the return. I explore various hypotheses to explain this behavior and suggest that the apparent recognition of both the infant’s and mother’s needs by the male supports the consideration of empathy in this case. As data accumulate, questions regarding empathy in non-humans should focus on more intricate levels as suggested by DeWaal (Annu Rev Psych 59: 279–300, 2008), rather than adhering to the assertion that empathy is uniquely human.     

What Role Do Mothers Play in the Gestural Acquisition of Bonobos (Pan paniscus) and Chimpanzees (Pan troglodytes)?

Contemporary research hypothesizes that biological inheritance and ontogenetic factors shape the development of gestural communication in nonhuman great apes. However, little is known about the specific role that mothers play in the acquisition of their infants’ gestures. We observed 6 bonobo (Pan paniscus) and 4 chimpanzee (Pan troglodytes) mother–infant dyads and recorded their gesture types and frequency. We analyzed all behavioral contexts in which gestures occurred as well as the play context alone. Infants of both species were unlikely to share gestures with their mother or unrelated adult females. However, gestural sharing was prevalent within age groups. Within and across species, infant–infant and mother–mother groups were homogeneous regarding the types of gestures they shared, although there was individual variation in the frequency of gesture use. Our findings provide limited evidence that infants learned their gestures by imitating their mothers. Phylogenetic influences seem to be vital in gestural acquisition but, we suggest, repertoire development cannot be disentangled from individual social encounters during life.     

Paternal Care in <Emphasis Type="Italic">Propithecus verreauxi coquereli</Emphasis>

Alloparental behavior is documented for several anthropoid primates, but few researchers have investigated the extent or variability of such behavior in prosimians. We report results from a study of male-infant interactions in 2 groups of Coquerel’s sifaka (Propithecus verreauxi coquereli) at the Duke University Primate Center (DUPC). Both groups contained 1 adult pair, 2 juveniles, and a newborn. The adult males exhibited paternal behavior toward their offspring in the form of grooming and holding the infant, though males differed in the amount of time they spent engaged in these activities. Group differences in the proximity maintained between the infants’ parents suggest that the relationship between adult males and females may help account for the variation. The presence of juveniles appeared to diminish paternal behavior in the group exhibiting a higher overall rate of male-infant interaction.     

Social relations in a free-ranging troop of stumptail macaques (Macaca arctoides): Male-care behaviour I

The occurrence of male-care behaviour directed from juvenile and adult males to infants was studied in a free-ranging troop of Stumptail macaques. The study period lasted two months comprising about 140 hours of recorded observations. Infants were a focal subgroup and their interactions with older males were recorded. The following variables were examined in relationship to the sending and receiving of male-care: the infant (its age, sex, and dominance rank), older males (their age and dominance rank), and genetic ties. Infants I received more male-care than infants II and differences in the type of male-care received by infants I and II were found. Male infants received more male-care than female infants and sex differences in the type of care received were evident. No relationship was found between the infant’s dominance rank and the amount of male-care received. A substantial amount of male-care behaviour was sent to genetic kin. Two-three year olds displayed more male care than yearlings. Juveniles as a class displayed more male-care than adults. A positive association was found between the juveniles’ dominance rank and the sending of male-care. However, among the adults, the subordinate male displayed more care behaviour than the alpha male. The presence or absence of the mother was found to influence the older males’ interest in the infant. The results are discussed and compared with data available on other primate species. Supported by grants from the Behavioral Science Foundation (U.S.) and by the Mexican Institute of Anthropology.     

Vervet monkey grandmothers: Interactions with infant grandoffspring

Social relationships of 30 infants with their maternal grandmothers were studied in a captive colony of vervet monkeys (Cercopithecus aethiops sabaeus).Grandmothers and grandinfants formed affiliative relationships with one another that could be distinguished from the infant’s relationships with nonkin adult females and with other adult female kin. The intensity of the grandmother—grandinfant relationship varied according to several factors which were related to the infant’s vulnerability to mortality and to the grandmother’s ability to provide effective social support. High-ranking grandmothers spent more time near their grandinfants, and initiated more grooming and caretaking of their grandinfants, than did lower-ranking grandmothers. Grandmothers spent more time near their daughter’s first surviving infant than near later-born infants, and when grandmothers had more than one adult daughter, they spent more time near the infant of the younger daughter. These results, combined with the fact that the presence of a maternal grandmother has been associated with a reduction in the rate of infant mortality in this colony (Fairbanks and McGuire, 1986), suggest that grandmothers are actively contributing to the reproductive success of their adult daughters and to the survival of their infant grandoffspring.     

Bridging behavior and other affiliative interactions among male tibetan macaques (Macaca thibetana)

I describe bridging behavior and social relationships between adult males and infants in a free- ranging group of Tibetan macaques (Macaca thibetana)at Mt. Huangshan, China. The subjects performed bridging in which two adult males simultaneously lifted up an infant, sucked or touched its genitalia, and then groomed each other in nonagonistic contexts. Males also expressed social behaviors with other males, such as mounting, penis-sucking, and embracing while touching each other’s penes. Males also employ bridging while exploiting an infant as a social tool, not only to reduce the probability of an aggressive response from dominant males (agonistic buffering), but also to develop and to maintain affiliative social relationships with other males. Use of male infants in bridging contributed to frequent male-infant interactions such as holding,grooming, and penis-sucking. Although these interactions might not have a positive influence on infant survival, they may facilitate the maintenance of affiliative relationships with adult males until they reach maturity. The development of bridging might have a close relation to the high socionomic sex ratio (adult male/adult female) and frequent affiliative interactions between males, especially among the adolescents and adults.     

Observation of a birth among wild toque macaques (Macaca sinica)

Most toque macaques give birth to their infants during the night when resting arboreally. Here we report on a birth that occurred in daytime (at 0916 hr) and on the ground. The mother was 7.6 years old; the birth was her second. Prepartum behaviors included lordosis, arching of the back, stretching, squatting, rolling on the ground, and anogenital self-examination. During the birth the female was isolated about 100 m from the rest of her group. The mother stood bipedally during parturition and assisted delivery with her hands. The infant was born within 2 min after first appearing at the vulva. It immediately clung to the mother’s leg and vocalized. The mother licked the infant and oriented it toward her ventrum. She resumed foraging behavior within 20 min after parturition. The infant nursed for the first time 2.25 hr after being born. The mother ate part of the placenta, but the alpha female of the group usurped and also ate a portion of it. Curious group members sniffed and looked at the infant but did not touch it.     

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).     

Food transfer between mother and infant chimpanzees of the Mahale Mountains National Park,Tanzania

We studied food transfer between chimpanzee mothers and infants in the Mahale Mountains National Park, Tanzania. The rate of infant solicitation for food dramatically increased in the second year of life, then gradually decreased and, in the seventh year, virtually disappeared. The pattern of the ontogeny of food sharing precisely followed that of solicitation because mothers shared food only when requested to do so by their infants. The success rate of solicitation, however, did not display extreme changes across ages. Food that was difficult to process was shared more frequently because it was more likely to be demanded by infants. We defined food retrieval as an infant’s recovery of leftovers discarded by its mother. Food types retrieved were often those that are difficult to process and were also likely to be shared by mothers. However, infants tended to solicit small, difficult food types for sharing while they often retrieved the remains of large, difficult food types. The function of food sharing and food retrieval lies in an infant’s learning food types that it cannot easily obtain or process by itself. The level of competition for food between mothers and infants remained low throughout infancy. We noted no particular characteristic about foods from which infants were displaced by mothers. As infants grew older, they increased the distance between themselves and mothers that became more aggressive.     

Male Tibetan macaques' (Macaca thibetana) choice of infant bridging partners

Adult male Tibetan(Macaca thibetana), Barbary(M. sylvanus), and stump-tailed macaques(M. arctoides) engage in bridging, a ritualized infant-handling behavior. Previous researchers found a bias toward the use of male infants for this behavior, but its function is debated. Explanations include three hypotheses: paternal care, mating effort, and agonistic buffering. We studied a group of habituated, provisioned Tibetan macaques to test whether adult males' affiliative relationships with females predicted their use of an infant for bridging. We also examined biases for sex, age, and individual in males' choice of bridging infant. We collected data via all occurrences, focal animal, and scan methods, from August to September 2011 at the Valley of the Wild Monkeys, China. We found that male infants were significantly preferred over females for bridging, but of three male infants in the group, only one was used by all males, while one male infant was used less often than expected. Adult males had females they were significantly more likely to be proximate to and/or to groom, but these corresponded to the mother of the bridging infant for only one male. Our results are most consistent with the agonistic buffering hypothesis: lower-ranked males used the alpha male's preferred bridging infant in an attempt to regulate their interactions with the alpha.     

The brief survival of free-ranging baboon infants (Papio cynocephalus) after separation from their mothers

The importance of mother — infant attachment in free-ranging primates is illustrated by events culminating in the deaths of two baboon infants a few days after losing their mothers. These two cases are contrasted with those of a severely injured infant, not separated from its mother, which lived, and an animal which lost and refound its troop. Protective behavior of adult males is described. In captivity, separation sometimes produces infant depression; in nature, such depression may be fatal.     

Adult male-infant interactions in wild muriquis (Brachyteles arachnoides hypoxanthus)

We examined adult male-infant interactions in wild muriquis (Brachyteles arachnoides hypoxanthus), a species in which close relatedness among philopatric males and high paternity uncertainty should minimize both aggressive and affiliative behavior by males toward infants. As expected, male-infant interactions were extremely rare during this 10-month field study. None were observed in over 236 hr of observation on a cohort of six infants (0 – 13 months old). The 29 interactions observed ad lib involved 5 of the 6 infants and 9 of the 16 adult males in the group. All of the male-infant interactions were affiliative, but extremely brief. The median duration of interactions was only 0.33 min, and none lasted longer than 1.52 min. Infants always initiated, and nearly always terminated, their interactions with adult males. The indifference that appears to characterize muriqui male-infant interactions differs from the ways in which other male primates interact with infants when protection of genetic interests or investment in mating effort are involved.     

Responses of foster-mothers and troop members to adopted newborns in a captive group of rhesus monkeys

Two rhesus monkey males and two females, born to females caged singly, were exchanged with same-sex infants born to females in a large troop which was held in an enclosure in a different building. The ages of the infants were between 24 and 120 hr. The selected foster mothers (FMs) immediately accepted the foreign infants, allowed them to suckle and treated them as their own offspring. Compared with interactions with previous offspring, the FMs initially tended to be more possessive and restrictive of their foster infants: generally they took longer before they allowed the infants to sit at a distance from them and more readily retrieved them. The foster infants tended to be more active (‘fidgety’) than natural (control) offspring born to the troop. Non-related members of the troop, differentiated between foster and control groups. These troop animals more frequently approached and sat in proximity, often in fur-contact with, touched, groomed, and lipsmacked to, foster infants than control infants. The attractiveness of the fostered infants seemed to be slightly associated with the FMs' dominance rank. The foster infants were therefore viewed by others as having assumed the role afforded by the FMs' rank. Thus both FMs and other troop members recognized the unfamiliarity and novelty of the foster infant but the infants were still accepted into the group. We suggest that the different treatment of the foster infants by the troop may have consequences on the infants' future social development.