Rearing infant monkeys (Macaca nemestrina) in pairs produces deficient social development compared with rearing in single cages

Many scientists and colony managers assume that social housing is a beneficial living condition for all captive primates. Several older studies of primate development question the generality of this assumption. We recently tested this assumption by comparing the social development of pigtailed macaque infants raised in pairs and those that were raised in individual cages. All animals received 30 min of daily socialization in a playroom. Infants paired from postnatal week 3 through month 4 developed a playroom behavioral repertoire consisting largely of mutual clinging, fear, and social withdrawal. This was especially true of females. Unlike the singly caged infants, pair-reared monkeys did not successfully adapt to living in a large social group at 8–10 months of age. In this situation, pair-reared infants were subordinate and spent almost all of their time huddling on the pen floor. It was concluded that rearing macaque infants in pairs produces a behavioral repertoire that is maladaptive with respect to social development.     

Infant Mortality Risk and Paternity Certainty Are Associated with Postnatal Maternal Behavior toward Adult Male Mountain Gorillas (Gorilla beringei beringei)

Sexually selected infanticide is an important source of infant mortality in many mammalian species. In species with long-term male-female associations, females may benefit from male protection against infanticidal outsiders. We tested whether mountain gorilla (Gorilla beringei beringei) mothers in single and multi-male groups monitored by the Dian Fossey Gorilla Fund’s Karisoke Research Center actively facilitated interactions between their infants and a potentially protective male. We also evaluated the criteria mothers in multi-male groups used to choose a preferred male social partner. In single male groups, where infanticide risk and paternity certainty are high, females with infants <1 year old spent more time near and affiliated more with males than females without young infants. In multi-male groups, where infanticide rates and paternity certainty are lower, mothers with new infants exhibited few behavioral changes toward males. The sole notable change was that females with young infants proportionally increased their time near males they previously spent little time near when compared to males they had previously preferred, perhaps to encourage paternity uncertainty and deter aggression. Rank was a much better predictor of females’ social partner choice than paternity. Older infants (2–3 years) in multi-male groups mirrored their mothers’ preferences for individual male social partners; 89% spent the most time in close proximity to the male their mother had spent the most time near when they were <1 year old. Observed discrepancies between female behavior in single and multi-male groups likely reflect different levels of postpartum intersexual conflict; in groups where paternity certainty and infanticide risk are both high, male-female interests align and females behave accordingly. This highlights the importance of considering individual and group-level variation when evaluating intersexual conflict across the reproductive cycle.     

Adoption by captive parturient rhesus macaques: Biological vs. adopted infants and the cost of being a “twin” and rearing “twins”

Four rhesus macaque (Macaca mulatta) mothers each spontaneously adopted and reared an abandoned, unrelated neonate in addition to their own neonate. Data on relative time spent in maternal contact and who maintained proximity were collected for the biological and adopted “twins” and singleton control infants using focal animal sampling. Infant weight gain and the subsequent conception history for each mother were obtained for the following year. Biological infants spent more time in maternal contact than their adopted “twin” siblings. When in contact with their mothers, biological “twins” spent more time in the ventro-ventral position and more ventral time alone than adoptees. Mothers initiated more contacts with their biological infants than their adopted infants, suggesting these differences may be due to differential maternal behavior. “Twins” gained weight at a slower rate than singletons, and mothers rearing “twins” produced significantly fewer offspring the following season. Am. J. Primatol. 43:259–264, 1997. © 1997 Wiley-Liss, Inc.     

Early predictors of self-biting in socially-housed rhesus macaques (Macaca mulatta)

The development of self-biting behavior in captive monkeys is little understood and poses a serious risk to their well-being. Although early rearing conditions may influence the expression of this behavior, not all animals reared under similar conditions self-bite. The purpose of this study was to examine the effects of three rearing conditions on biting behavior and to determine whether early infant behavior can predict later self-biting. The subjects were 370 rhesus macaques born at the National Institutes of Health (NIH) Animal Center between 1994 and 2004. They were reared under three conditions: mother-reared in social groups (n=183), peer-reared in groups of four (n=84), and surrogate-peer-reared (n=103). Significantly more surrogate-peer-reared animals self-bit compared to peer-only or mother-reared animals. There was no sex difference in self-biting, but this result may have been affected by a sex bias in the number of observations. The durations of behaviors exhibited by the surrogate-peer-reared subjects were recorded in 5-min sessions twice a week from 2 to 6 months of age while the animals were in their home cages and play groups. In the play-group situation, surrogate-peer-reared subjects who later self-bit were found to be less social and exhibited less social clinging than those that did not self-bite. Home-cage behavior did not predict later self-biting, but it did change with increasing age: surrogate clinging and self-mouthing decreased, while environmental exploration increased. Our findings suggest that surrogate rearing in combination with lower levels of social contact during play may be risk factors for the later development of self-biting behavior.     

Social development of stumptail macaques (Macaca arctoides): Momentary touching and other interactions with adult males during the infants’ first 60 days of life

Fourteen categories of male-infant social behavior were recorded during the early infancy of seven stumptail macaques living with four adult males in two colony groups. Momentary touching of infants by males occurred earlier and more often than behaviors such as clinging and grooming, which are usually associated with maternal attachment. Differences among infants in the amount of paternal attention received, and among males in the amount given, were explained in terms of the affiliation patterns of adult group members.     

Are demographic correlates of white-faced capuchin monkey (Cebus capucinus) “Gargle and Twargle” vocalization rates consistent with the infanticide risk assessment hypothesis?

Zahavi's “Bond Testing Hypothesis” states that irritating stimuli are used to elicit honest information from social partners regarding their attitudes towards the relationship. Two elements of the Cebus capucinus vocal repertoire, the “gargle” and “twargle,” have been hypothesized to serve such a bond-testing function. The greatest threat to C. capucinus infant survival, and to adult female reproductive success, is infanticide perpetrated by alpha males. Thus, we predicted that infants (<8 months), pregnant females and females with infants would gargle/twargle at higher rates than the rest of the population, directing these vocalizations primarily to the alpha male. Over 16 years, researchers collected data via focal follows in 11 habituated groups of wild capuchins in Lomas Barbudal, Costa Rica. We found some support for our hypothesis. Infants and females with infants (<8 months) vocalized at higher rates than the rest of the population. Pregnant females did not vocalize at relatively high rates. Infants (age 8–23 months) were the only target group that vocalized more when the alpha male was not their father. Monkeys gargled and twargled most frequently towards the alpha male, who is both the perpetrator of infanticide and the most effective protector against potentially infanticidal males.     

Social development in nursery-reared pigtailed macaques (Macaca nemestrina)

The social development of 240 nursery-reared pigtailed macaques (Macaca nemestrina) was studied from postnatal weeks 4 to 32. The objectives of the study were to document developmental trends and evaluate social behavior in laboratory-reared M. nemestrina raised at the University of Washington Infant Primate Laboratory, and to identify husbandry factors that might affect early social development. Only infants who had not undergone invasive postnatal experimental manipulation and had no chronic illness or injuries were included in the study. Infants were separated from their mothers and housed singly, but had access to peers for 30 min a day, 5 days a week, in a large playroom. Play and social behaviors emerged early in development, increased during the developmental period studied and occupied a large portion of the infants' time budgets. Although disturbance behaviors occurred with some frequency and duration early in development, they occupied a very small portion of the infants' time budget at 8 months of age. Weaning from infant formula at 16–19 weeks retarded development of play behavior. Permanent removal of a cloth comforter (diaper) during weeks 20–24 had no long-term behavioral effects. It was concluded that at 8 months of age these infants showed relatively normal species-typical behavioral repertoires. Am J Primatol 41:23–35, 1997. © 1997 Wiley-Liss, Inc.     

Birth rate and mortality rate of infants with congenital malformations of the limbs in the Awajishima free-ranging group of Japanese monkeys (Macaca fuscata)

The birth rate and mortality rate of infants with congenital malformations of the limbs were examined in the Awajishima free-ranging group of Japanese macaques (Macaca fuscata). Of the 606 infants born between 1978 and 1995, 86 (14.2%) were malformed. The male-female ratio did not differ between malformed and normal infants. Most kin-groups included females who gave birth to malformed infants at least once. The mortality rate within the first year after birth for malformed infants (28.2%) was significantly higher than that for normal infants (10.0%). However, this indicates that more than 70% of malformed infants were able to survive for the first year of life, even though they were unable to cling to their mothers ventrum due to their limb deformities. This finding indicates that maternal care-taking is sufficient to enable malformed infants to survive during the early stages of development and that clinging by the infant is not necessary for the display of maternal care. Am. J. Primatol. 42:225–234, 1997. © 1997 Wiley-Liss, Inc.     

Rearing condition and plasma cortisol in rhesus monkey infants

Previous studies comparing plasma cortisol levels in mother-reared and nursery-reared rhesus monkey infants under baseline and stress conditions have reported conflicting findings. Differences in subject age, procedures, and specific rearing history may account for many of the discrepant findings. In the present study, mother-reared infants from large social groups, peer-only reared animals, and infants reared with surrogates and limited peer contact were studied in different test conditions across the first 6 months of life. Infants were sampled under three conditions: following a neonatal assessment at Days 14 and 30, immediately upon capture on Day 60, and after 30-min isolation periods on Days 90, 120, and 150. Mother-reared infants exhibited higher cortisol levels on Days 14 and 30 than did both types of nursery-reared infants. In addition, Day 60 basal values of mother-reared infants were higher than those of both peer-reared and surrogate/peer-reared infants. However, on Days 90, 120, and 150, both mother-reared and peer-reared infants exhibited higher cortisol levels in response to separation and 30-min isolation than did the surrogate/peer-reared infants. These differences may reflect group-specific variations in physical environment, capture time, feeding regimen, or diurnal HPA axis rhythms. Am. J. Primatol. 46:311–321, 1998. © 1998 Wiley-Liss, Inc.     

Kastom and Anticolonialism on Malaita: “Culture” as Political Symbol

Most Melanesians invoking ideologies of kastom have, in becoming Christianized and partly Westernized, hearkened back to ways now lost or abandoned. But the Kwaio of Malaita are preoccupied with kastom, while traditional religion, social organization and exchange still prevail. Why and how? The Kwaio are compared with Kwara'ae and other Malaita peoples concerned with kastom - many Christianized, others clinging to old ways.     

Integration of a hand-reared chimpanzee (Pan troglodytes) infant into a social group of conspecifics

Rejections of infants among non-human primates occasionally occur in the wild as well as in captive settings. Controlled adoptions of orphans and introductions of individuals into new groups are therefore sometimes necessary in captivity. Consequently, behavioral research on integration procedures and on the acceptance of infants by adoptive mothers is much needed. In this study, the introduction and subsequent adoption were examined in an 18-month-old hand-reared chimpanzee (Pan troglodytes). The infant was introduced into an age/sex-diversified social group of conspecifics at Furuvik Zoo, Gävle, Sweden, and continuous focal data was collected during the final stage of integration, including infant care exhibited by the group members and the infant’s secure base behavior. The infant was successfully integrated into the group and engaged in positive social interactions with all group members. An adult primiparous female chimpanzee formed a bond resembling a mother–infant relationship with the infant, which continues to be maintained at publication. However, the female initially showed very limited interest in the infant. It was, in fact, two other younger female group members that exhibited most infant care. The infant’s secure base behavior patterns indicate that she adapted well to the new circumstances in the chimpanzee group as the integration progressed. This provides evidence that a final adopter does not necessarily initially show maternal interest and that there can be flexibility in maternal behavior in adult chimpanzee females. Moreover, the methods applied employing gradual familiarization with all the group members and the use of an integration enclosure, may have contributed to a successful result. These findings extend our knowledge of introduction procedures in captivity as well as provide information on foster mother–infant attachment in chimpanzees.     

Early social experience affects behavioral and physiological responsiveness to stressful conditions in infant rhesus macaques (Macaca mulatta)

Studies on early development have demonstrated the profound effects of early social experience on the behavioral development and physiology of young rhesus macaques. Given these relationships, we hypothesized that rhesus macaques exposed to different nursery-rearing conditions may develop unique biobehavioral profiles. If this is true, the assessment of temperament may allow us to pinpoint successful rearing environments, thus improving the overall health of nonhuman primates that are raised in captive environments. We conducted biobehavioral assessments in order to examine differences in the development of infants raised under four different peer-rearing conditions (continuous pairing (CP), intermittent pairing, CP with partner rotation, and intermittent rotational pairing) and compared these animals with data from a mother-reared control group. Overall, continuous rotationally paired animals were most similar to mother-reared controls on most behavioral and temperament measures, suggesting that more socially complex rearing environments (greater number of social partners) favor a more active behavioral style. Cortisol profiles of mother-reared controls were similar to both CP groups, and these three groups had higher cortisol concentrations than the intermittent rotational-pairing group. In addition, intermittently paired infants displayed a significantly higher frequency of self-stroke behavior during a human intruder challenge, an abnormal behavior also known as floating limb which has been shown to be a precursor of self-biting. Overall, the data are consistent with the idea that social complexity in the nursery, as operationalized in our continuous rotational pairing, leads to a biobehavioral profile that is most similar to that of infants raised by their mothers in large, socially complex, cages.     

Special relationships instead of female dominance for redfronted lemurs,Eulemur fulvus rufus

Most lemurs yet studied in detail exhibit some mode of adult female social dominance over males. The known exception, a brown lemur subspecies known as rufous or redfronted lemurs (Eulemur fulvus rufus), forms multimale–multifemale social groups within which unambiguous dominance relations are not observed among adults. Resting groups of redfronted lemurs consistently include huddling adult male–female pairs whose males selectively scentmark and rub their heads in the scentmarks of their female huddling partners. Quantitative observations confirmed that some of these male–female pairs maintain special relationships satisfying all criteria originally developed in research on cercopithecine monkeys. Observations before, during, and after mating season, intergroup encounters, male transfers, and changes in male–female affiliations illuminated developmental and functional aspects of male–female partnerships. Each adult female in two semi-free-ranging study groups shared high rates of association, grooming, and agonistic support and low rates of agonistic interaction with one unrelated or distantly related adult male partner. Such affinity characterized small proportions of adult male–female relationships. Several males directed not only support but also aggression toward adult females with whom they sought to affiliate. All bonded males sought to copulate with their partners, and some appeared to ignore estrus in nonpartners. All females accepted copulation attempts from partners and some seemed to prefer their partners as mates. Partial synchronization of brief estrus periods together with concealed ovulation appeared to minimize chances for polygynous mating. Results support the view that the male–female pair is the fundamental social unit of E. fulvus and suggest that female partnership with individual males obviates dominance behavior, including female dominance, in this lemurid primate. Am. J. Primatol. 43:239–258, 1997. © 1997 Wiley-Liss, Inc.     

Parity-related differences in suckling behavior and nipple preference among free-ranging Japanese macaques

Suckling behavior of primiparae in free-ranging Japanese macaques (Macaca fuscata) was compared with that of multiparae at Jigokudani Monkey Park, the Shiga Heights, Nagano Prefecture, Japan, from April 1984 to June 1994. The estimated rates of milk secretion in a single preferred nipple among primiparae were lower than those among multiparae from birth to 5 months of age. Milk secretion capabilities of primiparous mothers, hence, appear to be inferior to those of multiparous mothers. In nutritive sucking, although Japanese macaque infants preferred one single nipple, nipple preferences in primiparae were weaker than those in multiparae. With supplementary two-nipple use during sucking, however, the infants of primiparae appear to overcome a suckling flaw of their primiparous mothers. After infants were 5 months of age and after a drop (from approximately 10% to approximately 5%) in the rates of milk secretion, however, milk secretion rates in a single preferred nipple among primiparae were similar to those in multiparae and the supplementary two-nipple use in primiparous mother-infant dyads disappeared. Am. J. Primatol. 42:331–339, 1997. © 1997 Wiley-Liss, Inc.     

Social context affects phee call production by nonreproductive common marmosets (Callithrix jacchus)

Common marmosets produce two variants of their long call (phee call) in different situations. Intergroup calls are produced in territorial situations, and intragroup separation calls are produced by marmosets isolated from group members. Marmoset groups frequently include postpubertal, nonreproductive members; their roles in the spontaneous production of territorial vocalizations is unclear. This study analyzed the production of home cage phee calls by nonreproductive, postpubertal marmosets while they were housed in their natal groups and after pairing with an opposite-sex conspecific. Additionally, the production of the separation phee call variant was assessed in both social conditions. The results indicated that the marmosets rarely produced home cage, or territorial, phee calls while they were natally housed. In contrast, both males and females produced the territorial phee call at a much higher rate as early as 4 days after pairing. Age-matched females remaining in their natal groups throughout the study produced home cage phee calls infrequently. Most marmosets produced separation phee calls at a high rate after separation from either their natal group or a partner, suggesting that the makeup of a social group has little effect on an animal's motivation to reunite with conspecifics. These results suggest that the social environment has an important influence on the production of territorial phee calls. Am. J. Primatol. 43:135–146, 1997. © 1997 Wiley-Liss, Inc.     

Pattern of play behavior in infant (age 1 to 12 months) white‐headed langurs in limestone forests,southwest China

Play behavior is a significant trait of immature nonhuman primates (hereafter primates) that plays an important role in sensory, locomotor, socio‐cognitive, and developmental processes. It has been suggested that the function of play is to practice and improve motor skills related to foraging, avoiding predators, attracting mates, raising offspring, and strengthening the skills needed for the formation and maintenance of social bonds. From September 2009 to August 2010, we investigated the play behavior of 1–12 month‐old infant white‐headed langurs (Trachypithecus leucocephalus) a Critically Endangered primate species endemic to China. We carried out this study in the Guangxi Chongzuo White‐headed Langur National Nature Reserve, and recorded 4421 play bouts and 1302 min of play engaged in by seven infants. We found that infants of different ages exhibited different patterns of play behavior. Specifically, nonsocial play behaviors appeared at one month of age, social play behaviors at two months, and an expanded repertoire of social and non‐social play behaviors at three months of age. The frequency and duration of nonsocial play peaked at five months of age and then decreased, while social play gradually increased with age. Nonsocial play did not differ between the sexes, whereas social play showed sex specificity, with a higher frequency and longer duration of social play in male infants compared to female infants. In addition, male and female white‐headed langur infants appeared to prefer individuals of same sex as social playmates, but no obvious choice preference for a specific individual. In conclusion, we provide the first report of play behavior in a population of wild Critically Endangered white‐headed langurs. We suggest that age‐ and sex‐specific differences in play behavior of infants form the bases for age and sex‐based differences in the social interactions of adult langurs.     

Effects of Pair-Bond and Social Context on Male–Female Interactions in Captive Titi Monkeys (Callicebus moloch, Primates: Cebidae)

In monogamous species, an abiding relationship between a specific adult male and a specific adult female is a defining feature of the social system. The interactions between these individuals are influenced by many factors, including not only the history of their relationship (for example, development of a mutual bond), but also the immediate effects of the prevailing social context (for example, presence and sex of extra‐pair conspecifics). In this study we examined the effects of an existing bond and of social context on interactions between adult heterosexual pairs of the monogamous titi monkeys (Callicebus moloch). Twelve adult males and 12 adult females were tested with their cagemates and with an unfamiliar partner of the opposite sex in five social contexts: (1) mated male–female pair; (2) unfamiliar pair; (3) single female; (4) single male; and (5) empty stimulus cage. Results show that mated pairs were more affiliative than unfamiliar pairs and differentiated social contexts more sharply. Males were more responsive to context than females. Distance between mates was less and physical contact was more frequent in the presence of male–female pairs or a single male, than in the presence of a single female or an empty cage. These findings suggest that the presence and sex of strangers have a stronger influence on male–female interactions when the pair has an existing relationship.     

Improved behavioral indices of welfare in continuous compared to intermittent pair-housing in adult female rhesus macaques (Macaca mulatta)

Limiting opportunities for captive nonhuman primates (NHPs) to express species-specific social behaviors may disrupt the adaptive drive for social companionship and may lead to increases in coping behaviors and inactivity. While captive NHPs show improved welfare when moving to pair-housing from single-housing, the impact of daily separation of pair-mates, as is implemented in intermittent pair-housing, is not fully understood. We compared behavioral indices of welfare exhibited by adult female rhesus macaques (Macaca mulatta) in two conditions: (1) intermittent pair-housing, involving daily overnight separation of pair-mates, and (2) continuous pair-housing, involving little separation of pair-mates. A within-subjects study design tested two groups of females experiencing both pairing conditions in an alternate order, switching either from continuous to intermittent pair-housing, or from intermittent to continuous pair-housing. Behavioral observations, recording activity state, self-directed, abnormal, and social behaviors, were conducted at midday when all females were paired, and in the afternoon when intermittent pairs were separated. Females exhibited higher levels of inactivity and self-directed behavior when separated due to intermittent pair-housing in comparison to continuous pair-housing. In addition, intermittently paired females showed higher levels of grooming and other types of affiliation when paired, than during the same time frame when they were continuously paired. These results suggest that females in the continuous presence of a social partner experience improved levels of activity and do not need to elevate levels of behavioral coping mechanisms (e.g., self-scratching, increased affiliation) as they receive the benefits associated with social companionship consistently throughout the day. Overall, this study provides the first evidence that continuous pair-housing affords better welfare than intermittent pair-housing in adult female rhesus macaques. Pair-housing options, such as continuous pairing, that reduce reliance on behavioral coping mechanisms and promote adaptive social behavior throughout the entirety of the day should be prioritized over husbandry care scheduled for convenience.     

Social development of stumptail macaques (Macaca arctoides): Momentary touching,play, and other interactions with aunts and immatures during the infants' first 60 days of life

Interactions of seven infant stumptail macaques with aunts and immatures were observed during the infants' first 60 days of life in colony groups. Data were collected using 14 interaction categories, including typical maternal behaviors, play, and five categories of momentary touching. Aunts and immatures rarely engaged in maternal behaviors such as clinging, carrying, or retrieving. Both aunts and immatures were recorded momentarily touching the infants; aunts groomed them and immatures began playing with them during the second month. Such play was primarily between age-mates and rarely between infants and yearlings. Adult males engaged in more maternal behavior than aunts during the infants' first two months of life.     

Maternal Behavior and Infant Congenital Limb Malformation in a Free-Ranging Group of <Emphasis Type="Italic">Macaca fuscata</Emphasis> on Awaji Island,Japan

We studied the relationship between maternal behavior and infant disability in 12 mother-infant dyads for the first 5 weeks of infant life in the free-ranging Japanese macaque (Macaca fuscata) group on Awaji Island, Japan, from May to September 2001. Congenital limb malformations are prevalent in this population, and as such carry implications for behavior and conservation. We did not detect any differences in maternal activity budgets, mother-infant physical contact, infant holding, and overall nursing and infant transport time between mothers of non-disabled infants, disabled infants that were able to cling to their mothers, and disabled infants whose limb structure prevented clinging. Mothers of infants with limb malformations severe enough to prevent normal clinging behavior manually supported their infants during nursing and locomotion significantly more than other mothers did theirs. Increased support-carrying and support-nursing, and higher frequencies of holding the infant to one's ventrum, suggest that mothers of extensively malformed infants may be investing more to facilitate the survival of their offspring and that infant disability appears to be influencing maternal behaviors in this population.