What defines successful integration into a social group for hand-reared chimpanzee infants?

Hand-rearing of captive great ape infants is sometimes necessary but can have negative behavioral consequences. Modern hand-rearing protocols, including early integration into a diverse group of conspecifics, appear to reduce the negative consequences of hand-rearing, but the process of integration is not well studied. We investigated six potential metrics of success during the introduction of two hand-reared chimpanzee infants into a troop of nine other chimpanzees at the Maryland Zoo in Baltimore. Little aggression was observed and the infants continue to be maintained in the troop at publication. As we predicted, during the introduction the hand-reared infants showed consistent levels of stress-related behaviors, participated in affiliative interactions with all available partners, and acted, received, and mutually engaged in these interactions. Solitary behaviors by these infants were similar to a mother-reared infant in the same group. Each infant also formed a relationship with a specific female that involved nest-sharing, carrying, retrieval, and intervening to reduce risk to the infant; these relationships could be classified as allomothering because they involved maternal behavior but occupied significantly less of the infants’ time than a maternal relationship. Contrary to our prediction, the hand-reared infants therefore spent significantly less time in social behavior than a mother-reared infant of the same age. In addition, the hand-reared infants continued to show strong social preferences for each other as introductions progressed and to direct a low but consistent number of nonfeeding social behaviors to humans. The successful introduction of hand-reared infants appeared to involve adding conspecific social relationships to the infants’ social repertoire, but not eliminating social interactions directed at humans.     

Behavioral response of a chimpanzee mother toward her dead infant

The mother-offspring bond is one of the strongest and most essential social bonds. Following is a detailed behavioral report of a female chimpanzee 2 days after her 16-month-old infant died, on the first day that the mother is observed to create distance between her and the corpse. A series of repeated approaches and retreats to and from the body are documented, along with detailed accounts of behaviors directed toward the dead infant by the mother and other group members. The behavior of the mother toward her dead infant not only highlights the maternal contribution to the mother-infant relationship but also elucidates the opportunities chimpanzees have to learn about the sensory cues associated with death, and the implications of death for the social environment.     

Behavioral changes during weaning in captive chimpanzees

Behavioral changes during weaning of chimpanzee infants in captive social groups were compared with those of infants in the natural habitat. Results of the weaning process were the same for the mother-infant pairs in captivity and the natural habitat, i.e., an infant independent of suckling, regular maternal transport and sleeping with the mother. The captive infants, however, did not respond to weaning with depression or regression to infantile behaviors as did infants in the natural habitat. Quite probably the social and physical environmental differences between the two habitats faciliated a less stressful weaning period for the captive mother-infant pairs.     

Sex differences in infant integration in a semifree-ranging group of Barbary macaques (Macaca sylvanus,L. 1758) at Salem,Germany

Sixteen multiparous Barbary macaque females with newborns were studied over a 16 month period within the context of their naturally formed group. Analysis of their social behavior revealed 1) triadic interactions involving focal females, their newborns, and other group members occurred mainly with other females; and 2) mothers with female newborns interacted mainly with females of their own matriline, while mothers with male newborns interacted mainly with nonmatriline females. Observed in two successive birth seasons, this pattern indicates that partners of maternal interactions chose each other according to the sex of the newborn. Measures of distance from the mother also reflected differences between infants of different sex. At about five months of age, female infants were observed close to their mothers significantly more often than males. This finding follows the pattern of a sex-specific infant socialization process which integrates female infants into the network of their matrilines and male infants into the broader group. This sex-specific integration pattern is interpreted as supporting female philopatry and male dispersal. © 1995 Wiley-Liss, Inc.     

神农架川金丝猴投食群的母婴关系

灵长类动物母亲的育婴行为不仅对后代的存活起着关键作用,而且对婴猴的发育和成年后的社会交往有着重大影响,因此母-婴关系一直是灵长类学研究的热点之一。为了解川金丝猴的母-婴关系,探讨川金丝猴母-婴关系个体差异的影响因素,我们于2013年3月至2014年10月,以母-婴间相对距离表示照料强度,对神农架川金丝猴的母-婴照料关系以及母亲照料强度个体差异的影响因素进行了定量研究。结果表明：母亲照料行为强度、母亲对阿姨行为的容忍与婴猴年龄相关,限制行为与婴猴年龄不相关。身体接触与婴猴年龄不相关;腹部接触以及母-婴相对距离小于1 m与婴猴年龄呈负相关;相对距离1 m至5 m、相对距离5 m至10 m和相对距离大于10 m与婴猴年龄呈正相关;母亲对阿姨行为的拒绝与婴猴年龄呈负相关;母亲对婴猴的限制行为与年龄不相关。总的来说,即随着婴猴成长,母婴间距离越来越远,母亲也逐渐减少对婴猴的保护。母亲的生育经验、婴猴性别、婴猴出生先后和社会单元大小对神农架川金丝猴母婴关系没有显著影响,补食群丰富的食物资源和群内雌性友好的关系可能是导致本结果的原因。     

Behavioral responses of an infant gorilla to maternal separation in a captive social group of lowland gorillas (Gorilla gorilla gorilla)

The present report describes behavioral reactions of a 33-month-old female infant gorilla to maternal separation in a captive social group whose composition is similar to that of wild groups. The infant gorilla responded differently to two types of maternal separation. When she remained alone for a few hours, she cried repeatedly and moved restlessly, indicating protest. Upon reunion and also for a few days thereafter, an intensification of the mother-infant relationship occurred. On the other hand, when she was separated from her mother but remained with the other group members for nine days, she did not display any behaviors that could be characterized as protest, but rather showed clear behavioral depression. During the 9-day separation period, she hardly played with other group members but she developed affiliative relationships with the leading male. After the reunion from the 9-day separation, she spent as much time near her mother as before separation and played with other infants at a level similar to that before separation, while she sometimes displayed behavioral patterns demanding the maintenance of physical contact with her mother. The present findings are compared with other reports in great apes and human children.     

Transport of dead infant mountain gorillas by mothers and unrelated females

This report describes prolonged carriage of the corpses of two mountain gorilla infants by both related and unrelated adult females. Two hypotheses regarding this transport are considered: 1) that maternal behavior toward unrelated infants may be a by‐product of the hormonal condition of pregnancy, and 2) that the animals may be “learning to mother,” as nulliparous females could benefit from the experience of handling an infant that is no longer alive. Some factors pertinent to the event of infant deaths in captivity are considered. Zoo Biol 23:375–378, 2004. © 2004 Wiley‐Liss, Inc.     

Attachment and social preferences in cooperatively-reared cotton-top tamarins

In many primate species a close attachment between mother and infant provides a secure base for the infant when the infant is frightened or under stress. In cooperatively breeding primates infant carrying is divided among several individuals in the group, with the mother often doing little more than nursing. In these species it is not clear which individual would best serve as a secure base for the infant. We studied eight infant cotton-top tamarins from birth through 20 weeks of age, noting who carried the infant during the first 100 days, who transferred food with the infants, and, as infants became independent, with whom they associated during social play and affiliative behavior. From week 9 to week 20, when infants were independent of carriers most of the time, we presented families with six trials (once every 2 weeks) with a threatening stimulus (a human dressed in a lab coat and wearing an animal mask). Infants played primarily with their twin or youngest sibling and had affiliative interactions with many family members. However, in fearful situations, infants ran to those who had carried them and transferred food with them the most-their father or oldest brother (never to the mother). Although adults increased rates of mobbing calls in response to the threat, infants significantly reduced their vocalization rate. For these cooperatively breeding monkeys, the attachment object for infants is the family member that invested the most effort in carrying the infant and transferring food with the infant. These results parallel and extend results from bi-parental infant care species in which the father serves as the primary attachment figure.     

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.     

Adoption of an additional infant by a Western lowland gorilla (Gorilla gorilla gorilla).

A 10-year-old Western lowland gorilla, already caring for her own 14-month-old son, adopted a female neonate. The infant's mother (aged 7 years, 4 months) showed no interest in the infant, and it is unclear whether she abandoned the infant or whether it was seized by the dominant foster-mother. The foster-mother gave more maternal attention to the adoptee than to her own son but gave both infants the same protection. She adjusted her forms of transport to the age of each infant. The subadult mother of the neonate did not seek contact with her offspring during the first 4 weeks and in fact showed more interest in the 14-month-old male infant. Interactions between the two mothers were rare. The foster-mother's own male infant died 2 months after she had adopted the female infant. She looked after the adopted infant for 1 year, but then lost interest so that the adoptee had to be separated.     

Birth Timing and Behavioral Responsiveness Predict Individual Differences in the Mother–Infant Relationship and Infant Behavior During Weaning and Maternal Breeding

There is a great deal of variability in mother–infant interactions and infant behavior across the first year of life in rhesus monkeys. The current article has two specific aims: (1) to determine if birth timing predicts variability in the mother–infant relationship and infant behavior during weaning and maternal breeding, and (2) to identify predictors of infant behavior during a period of acute challenge, maternal breeding. Forty‐one mother–infant pairs were observed during weaning when infants were 4.5 months old, and 33 were followed through maternal breeding. Subjective ratings of 16 adjectives reflecting qualities of maternal attitude, mother–infant interactions, and infant attitude were factor analyzed to construct factors relating to the mother–infant relationship (Relaxed and Aggressive) and infant behavior (Positive Engagement and Distress). During weaning, late born infants were more Positively Engaged than peak born infants (ANOVA, P < 0.05); however, birth timing did not affect the mother–infant relationship factors Relaxed and Aggressive or the infant attitude factor Distress. During maternal breeding, early born infants had less Relaxed relationships with their mothers than peak or late born infants, higher Positive Engagement scores than peak or late born infants, and tended to have higher Distress scores than peak born infants (repeated‐measures ANOVA, P < 0.05). In addition, Distress scores were higher during maternal breeding than during the pre‐ and postbreeding phases. Finally, multiple regression (P < 0.05) indicated that while infant behavioral responsiveness predicted infant Positive Engagement during the acute challenge of maternal breeding, qualities of the mother–infant relationship predicted infant Distress. These data suggest that birth timing influences the patterns of mother–infant interactions during weaning and maternal breeding. Additionally, infant behavioral responsiveness and mother–infant relationship quality impact infant social engagement and affect expression, respectively. Am. J. Primatol. 74:734‐746, 2012. © 2012 Wiley Periodicals, Inc.     

Infanticide in chimpanzees: Review of cases and a new within-group observation from the Kanyawara study group in Kibale National Park

A prolonged attack on a mother and 2-year-old infant that resulted in the death of the infant was observed in the Kanyawara study group in Kibale National Park. The mother was a border-area resident who was first observed associating with unit-group males six years previously. The attackers were an adult male and an adult female with a 6-week-old infant clinging ventrally to her. The attack was unusual in several respects: it is the first time a male and a female chimpanzee have been observed cooperating closely in an infanticidal attack; the adult female initially attempted to intervene in the victim's behalf, but later joined in the attack after receiving aggression from the male; and the episode was longer in duration than other reported cases. In the year following the incident, the mother did not increase her association with community males, but was seen with the male who killed her infant. The relevance of these observations to sexual selection-based explanations for infanticide in chimpanzees is discussed.     

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.     

The birth of a lowland gorilla in captivity

A 7 year-old captive-born mother-reared gorilla gave birth to a healthy infant after being in labor for 27 min. The young female was a wholly competent mother although she had never observed gorilla mothers or interacted with gorilla infants. This reinforces previous evidence, still often ignored by zoo officials, that gorillas do not have to learn maternal behavior.     

Tactics of care for young infants by forest-living ruffed lemurs (Varecia variegata variegata): Ground nests,parking, and biparental guarding

Over a 4 month period, systematic and ad libitum observations were conducted on two adult female black-and-white ruffed lemurs (Varecia variegata variegata) and their infants in a 3.5 ha forest enclosure. The females were mother and daughter, members of a family group that had been semifree-ranging for 2 years and 3 months at the time of the births. One to two weeks before parturition, the females independently constructed nests, in which they kept their infants during the first few weeks following parturition. The older mother, cage-reared herself, prepared at least one nest. Her daughter, who has lived in the forest since late juvenescence, prepared at least four. Two to three weeks after parturition, the mothers moved their infants high into trees. During periods of maternal absence, the infants were often alone, and they rarely or never moved, vocalized, or groomed themselves. The mothers often kept their infants together after nests were no longer used. Each infant nursed freely from both lactating females. The infants were carried orally only by their mothers and were never transported by clinging to the pelage of any group members. Previously, researchers suggested that ruffed lemurs build nests for care of infants high up in trees. The present observations, however, suggest that two major modes of neonate care in Varecia exist: serial use of multiple ground nests and “parking” of infants high in trees. Advance preparation of several nest sites, relative lack of large predators, alternate maternal and paternal guarding of infants, infant immobility during absence of mother, and rapid infant development make this tactic of care for neonates plausible.     

The social development of free-ranging infantLemur catta at Berenty reserve,Madagascar

The social development of 11 free-ranging infantLemur catta was examined over the first 16 weeks of the infants' lives. By 16 weeks, infants still occasionally suckled and were carried dorsally, but on the whole, they were independent of their mothers. Sex or mother's rank was not found to affect frequency or type of play behavior. Mother's rank had no effect on frequency of maternal rejections, from the nipple or from riding, but female infants were rejected slightly more frequently than males were. Mothers tended to reject infants more severely and more frequently from dorsal riding than from the nipple. Sex and rank differences were not found with respect to behaviors determined as measures of independence; however, lower-ranking infants engaged in significantly more dependent behaviors than higher-ranking young did. It may be necessary for the infant of a low-ranking mother to maintain closer proximity to its mother for a longer period of time during infancy because such infants may be subject to abuse by higher-ranking group members and, furthermore, may not be as readily rescued in a stressful or dangerous situation as a higher-ranking infant. Sex was not found to be a factor in terms of measures of dependence. The lack of sex differences in developmental behaviors in this species may be related to female dominance, as well as to the fact that, as adults, both sexes engage in aggressive territorial behavirs.     

Mother-infant relationship in the slender loris (Loris tardigradus lydekkerianus)

Close observations under caged conditions were made on the behaviour of four mother lorises towards their own and alien infants. There appears to be no mutual recognition between the mother and her infant, and the relationship appears to be less specific. The infants are accepted by and get settled with any lactating female. In the first few weeks after birth, there is an intense attachment exhibited by the mother towards her baby. When the baby is separated, it exhibits a series of “fixed action patterns.” As the infant grows older, maternal interest declines and is lost after about 15–20 weeks post partum. Vocalization of the separated juveniles evokes greater maternal response than the visual cue.     

Changes in nearest‐neighbor associations in a captive group of western lowland gorillas after the introduction of five hand‐reared infants

The successful management of a captive gorilla population often necessitates the hand‐rearing of infants and their subsequent re‐integration into social groups of conspecifics. In the present study we quantified the changes in nearest‐neighbor associations in a group consisting of a silverback male, three adult females, and two sub‐adult females after the introduction of five hand‐reared infants. Additionally, we examined the associations among kin and non‐kin group members to determine whether genetic relatedness was a factor influencing the integration of the infants into the group and the subsequent patterns of association among infants and adults. Results showed that after the introduction, the silverback male spent >60% of his time in close proximity to an infant and 10% of his time within a “cluster” of infants. There was a significant change in a female's nearest‐neighbor associations; however, the change did not include an infant. The most significant finding among infants was a strong bias by each to associate with another infant. When the infants associated with an adult, three of the five associated most with the silverback male (P < 0.001), whereas the other two infants distributed their time among all the adults. The most significant change in behavior patterns was exhibited by one of the sub‐adult females who displayed parental behaviors 18% of the time compared to <1% for all other females. Adults and one sub‐adult female associated significantly more often with related infants compared to unrelated infants (P < 0.025), and the infants showed a bias to associate with another related infant (P < 0.0001). Results of an infant's association with an adult showed that three of the five infants preferred to associate with a related adult (P < 0.0001). An individual's age, sex, and behavioral profile may have also influenced association patterns among group members. These findings lend strong support to the importance of peer groups and the presence of a silverback male for facilitating the integration of hand‐reared infants into established adult groups. Zoo Biol 18:261–278, 1999. © 1999 Wiley‐Liss, Inc.     

A case of the adoption of an infant chimpanzee by a suckling foster chimpanzee

Chimpanzees in captivity have grown up in a rather unnatural social environment and there frequently are problems when they have to nurse their own offspring. It is most remarkable that a chimpanzee mother in a captive colony, who had lost her child almost immediately after birth, adopted without problems a five-week-old infant, which had been reared by humans from the day of its birth. Successful adoption has not been reported for feral chimpanzees; similar cases in captivity are not known.     

Periparturitional behavior of a primiparous lowland gorilla

The behavioral interactions of a primiparous lowland gorilla and her newborn female infant were observed and recorded during the birth of the infant and the subsequent 27 hours. The mother's behavior, initially unresponsive to the infant, progressed rapidly through a series of interactions that are described as preliminary to, and perhaps essential for the ultimate development of appropriate maternal behavior. The relationship between different critical activities, such as: (1) the ingestion of birth fluids by the mother and the establishment of initial contact with the infant, (2) the progression from impersonal contact to ventral-ventral contact, and (3) the coordination between the mother's and infant's vocalizations and activity preceding nursing are described, analyzed, and interpreted.