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.     

Allocare in a nocturnal primate: data on the spectral tarsier, Tarsius spectrum

Non-maternal infant care in many of the small-bodied New World primate species has been hypothesized by some researchers to be related to the high infant/adult weight ratio found in these species. The spectral tarsier, Tarsius spectrum, an Old World primate, has one of the highest infant/adult weight ratios of any primate, with infants weighing between 20-33% of adult weight at birth. On the basis of the hypothesized relationship between allocare and the infant/adult weight ratio, it is predicted that the spectral tarsier will also exhibit extensive allocaretaking behaviour. The results of this study indicate that although spectral tarsiers show care by male and female subadults as well as adult males, it is extremely limited compared to the extensive allocaretaking behavior observed in New World primate species such as Aotus and Callicebus. Spectral tarsier subadult females provide substantially more allocare to infants than do subadult males or adult males. Female subadults were observed sharing food, transporting, grooming, playing, alarm calling, baby-sitting and maintaining physical contact with infants more than other age/sex classes. Although the amount of allocare exhibited by adult males and subadult males was much less than that exhibited by female subadults, the data suggest that adult and subadult male spectral tarsiers do play a small part in the care and socialization of the infant. Adult males and subadult males were both observed occasionally engaging in allocaretaking behaviors such as grooming and playing, as well as frequently patrolling and defending the territory's boundaries. The results from this study suggest that although a high infant/adult weight ratio may be a prerequisite for selection to favor extensive allocare, it is not a causal factor. Additional research is needed in order to understand better the selective pressures involved and the costs and benefits of providing allocare to subadults and adult male spectral tarsiers.     

Do Adult Male Spider Monkeys (Ateles geoffroyi) Preferentially Handle Male Infants?

Infant tolerance by adult males has been observed in many primate species with multimale–multifemale mating systems, but males do not usually initiate interactions with infants. In male philopatric species, such as spider monkeys, adult males within a community exhibit high levels of cooperation and affiliation, and they might therefore be motivated to create bonds with potential future allies. Based on this hypothesis we predicted that adult male spider monkeys would participate in infant handling more than adult females and they would preferentially direct handling toward male infants. Between January 2008 and July 2010, we collected 884?h of observation on a community of wild spider monkeys at Runaway Creek Nature Reserve in Belize. During this period we observed 120 incidences of affiliative interactions between infants and adults other than their mother. The adult initiated the majority of nonmother adult–infant interactions (78?%). All available infants (5 males, 7 females) were handled during the study. All 9 of the community adult males handled infants but only 7 of 14 adult females did so. Adult males handled infants significantly more often than did adult females and males also handled young infants more often than older infants. Significant infant sex differences in handling appeared in infants >6?mo when adult males handled males significantly more than females. The patterns of infant handling among age–sex class dyads reflect the affiliative social patterns that we see in adult spider monkeys. These results provide support for the hypothesis that adult males preferentially handle male infants as a strategy for fostering social bonds.     

Sex ratio and mortality in a laboratory colony of the common marmoset (Callithrix jacchus).

In a retrospective study sex ratio and mortality were analysed in a captive colony of common marmosets (Callithrix jacchus). Seven hundred and thirty-five infants in 294 litters (20 singletons, 119 twins, 140 triplets, 14 quadruplets) out of 57 breeding females were evaluated. The sex ratio at birth was 0.95 males:1.0 females. The frequency of males and females, as well as the sex composition of twins and triplets confirm the assumption of dizygotic twinning in the common marmoset. According to age at death, 9 categories were differentiated, with perinatal mortality being the highest. Once early infancy had passed the probability of a common marmoset infant of our colony reaching childhood is nearly 95%. Sixty per cent of all liveborn infants survived beyond 18 months. Mortality of infants at birth from primiparous mothers did not differ from that of pluriparous females, nor did the survival rate of infants with the filial generation the respective female had reached (F1 to F6). Females with a high ratio of triplets and quadruplets had a lower reproductive success than females with a majority of singleton or twin deliveries. Differential mortality between males and females was not observed. The frequency of stillbirths was not strongly related to parity, but was to litter-size. Most stillborn babies were seen in sets of quadruplets, most abortions in singletons. A normal socialization in a stable social environment, as well as not pairing the animals before they are fully adult, are considered important factors in good breeding success and infant survival.     

Maternal Investment and Infant Survival in Gray-Cheeked Mangabeys (Lophocebus albigena)

Differences among females in infant survival can contribute substantially to variance in fitness. Infant survival is a product of external risk factors and investment by kin, especially the mother, and is thus closely tied with the evolution of behavior and life history. Here we present a 9-yr study (2004–2012) of infant survival and sex ratio relative to age and dominance ranks of mothers and the presence of immigrant males in a free-ranging population of gray-cheeked mangabeys (Lophocebus albigena) in Kibale National Park, Uganda. We consider immigrant males because they are known to increase infant mortality in several other species. We found that infants of older mothers had higher survival than those of younger mothers but that high rank did not confer a significant benefit on infant survival. Female infants had higher survival than male infants. Young, low-ranking females had more male infants than young, high-ranking females, which had slightly more daughters, but this difference declined as females aged because low-ranking females had more daughters as they aged. With limited data, we found a significant relationship between the presence of male immigrants and infant mortality (falls and unexplained disappearances) to 18 mo. Our results suggest that infant survival in gray-cheeked mangabeys is most precarious when mothers must allocate energy to their own growth as well as to their infants, that sons of young mothers are at greatest risk, and that immigrant males can negatively affect infant survival.     

Sex differences in interest in infants in juvenile rhesus monkeys: relationship to prenatal androgen

Yearling rhesus monkey females interact more with infants than do males. However, the continuity of this sex difference throughout the juvenile period is unknown. Human females display similar sexually differentiated interest in infants, and studies of girls with congenital adrenal hyperplasia suggest that this sex difference may be modulated by prenatal androgen exposure. We investigated infant interest in 1- to 3-year-old juvenile rhesus monkeys. Hormonal influences on this behavior were investigated by treating pregnant females with an androgen-receptor blocker (flutamide), testosterone enanthate, or vehicle, early or late in gestation. Subjects were reared in their well-established natal groups, composed of species-typical matrilineal social structures, including members of all ages. Yearling control females interacted with infants more than did yearling control males. At 2 and 3 years of age, the magnitude of the sex difference in interactions with infants increased markedly, producing effect sizes of more than 2.5 standard deviations. These effects are larger than those reported in humans. Androgen treatment did not affect male or female interactions with infants, but late gestation flutamide masculinized aspects of females' interest in infants. Although early flutamide prevented complete masculinization of male genitalia, this treatment was not accompanied by any alterations in the masculine pattern of infant interest. We found no evidence that the robust juvenile sex difference in frequency of infant interactions results from socialization. However, it was largely unaffected by our hormone manipulations. Whether this reflects characteristics of our specific treatments or is evidence of nonhormonal influences on infant interest remains unanswered.     

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.     

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.     

Rate of growth in length of Bangladeshi infants as a function of attained length.

We examine variation in the rate of growth in length of breast-feeding infants from rural Bangladesh. These data were collected between November 1985 and February 1986 from two rural sites. Eighty-eight infants, ranging from birth to 4 months of age at the start of the study and their mothers were measured monthly for 4 months. Length increased linearly with age over this 4-month period (infants' average bias-adjusted R2 = 0.90). The relationship between infant rate of growth in length and attained length was analyzed by two different methods: Oldham's (1962) method of regressing rate of growth on mean length and Blomqvist's (1977) method of regressing rate of growth on estimated initial length. The methods gave similar results. The rate of growth was negatively associated with mean infant length over the 4-month period (p less than 0.001); that is, shorter infants grew at a faster rate than longer infants. For every centimeter shorter the infant was, the rate of growth was 0.1 cm/mo faster on average; the effect was greater among males than among females. The average rate of growth was greater for males than for females and greater in financially solvent households and varied by site. Infant growth rate was slower among older infants than among younger infants, as expected. However, after adjusting for mean infant length, age was no longer significantly associated with infant growth rate, although mean infant length remained highly significant. Forty-one percent of the variation in infant rate of growth in length was explained by mean infant length, sex, sex by length interaction, household financial solvency, and site.     

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.     

Alloparental behavior in a captive group of spider monkeys (Ateles geoffroyi) at the Auckland zoo

I studied alloparental behavior in a captive group of spider monkeys at the Auckland Zoo using seven infants as focal subjects and assessed the effects of age, sex, and reproductive status of alloparents on patterns of infant-other interaction. Adult males initiated interactions with infants most often, followed by adult females. Immature individuals interacted with infants infrequently. Infants themselves initiated contact with adult males more often than with other members of the group. Alloparental behavior in spider monkeys differs from that in most other species in that the infant is an active rather than a passive participant in alloparental interactions. I discuss the patterns of infant-other interaction in relation to the social structure and dispersal patterns of Ateles.     

Investigation of the role of postnatal testosterone in the expression of sex differences in behavior in infant rhesus macaques (Macaca mulatta)

In several primate species, males have been shown to exhibit a surge in circulating testosterone during the early postnatal period. This surge has been postulated to play a role in the development of sex differences in behavior. In this study, the role of postnatal testosterone in infant behavioral development was investigated in socially living rhesus macaques. Seven male infants were treated with a GnRH agonist, avorelin, from the first week of life onwards. Ten female infants were exposed to testosterone by implantation of capsules containing testosterone. The behavioral development of these and control infants was recorded from birth to 6 months of age. The sexually dimorphic patterns of play and mounting were not affected by manipulation of postnatal testosterone in either male or female infants. Similarly, most mother-infant interactions were not affected by the hormonal manipulation of infants. Mothers of testosterone-treated females were found to take more responsibility for moving into and out of arm's reach of their infants than mothers of some other groups of infants; however, this measure did not normally differ between mothers of male and female infants. Manipulation of the postnatal testosterone surge does significantly affect penile growth and development, but does not affect the expression of infant sex differences in behavior nor greatly affect the development of the mother-infant relationship in rhesus macaques.     

Analysis of infant handling and the effects of female rank among Tana River adult female yellow baboons (Papio cynocephalus cynocephalus) using permutation/randomization tests.

Infant handling has been documented in numerous species. Among cercopithecines, interaction motivations are reported to range from aunting to kidnapping; these interactions are often distressful for both mother and infant. Here we examine handling by adult female yellow baboons (Papio cynocephalus cynocephalus) at the Tana River National Primate Reserve, Kenya, using a relatively new, computer-intensive statistical approach of permutation/randomization tests to deal with repeated measures effects and a skewed sample. We hypothesized 1) a tendency for handlers to handle the infants of females ranked similarly or lower than themselves, and 2) more successful infant handling by higher-ranked females, particularly with very young infants. We collected focal data on 23 females (11 mother-infant pairs) over an 11-mo period, with a total of 303 attempted and/or successful "handles" utilized in the permutation analyses. The general patterns apparent in the data seemed to support our hypotheses. However, the permutation tests showed that while females are somewhat more likely to attempt to handle the infants of females ranked "same or lower" than themselves, lower-ranked females are able to prevent more than three-fourths of the attempted interactions, and there is no statistically significant trend for females to successfully handle these infants. Further refinement of the analyses showed no significant tendencies for females to handle those infants ranked "lower" or "immediately lower" than themselves, casting doubt on the significant finding for "same or lower" attempts. Further, there was no significant effect for higher-ranked females to successfully handle an infant during its first month. Thus, rank does not seem to offer any privileges in terms of handling an infant in this population. We believe the permutation tests are an effective way to analyze repeated measures data and offer a more sensitive analysis tool for determining true significance.     

Maternal aggressive contact vocalizations in captive bottlenose dolphins (Tursiops truncatus): Wide-band,low-frequency signals during mother/aunt-infant interactions

The mother-infant bond in bottlenose dolphins is critical to infant survival and has been reported to last from 3-10 years in both captive and wild populations. Little information on mother-infant communication during early development has been collected. This paper reports on a newly discovered dolphin vocalization, termed thunk, which is predominantly used by mothers toward infants. Four mother-infant pairs and one aunt-infant pair were the subjects for this study. Methods included a focal animal sampling technique using 2.5 min interval and event/continuous sampling regimes on audio- or videotape. Results indicated that thunks are produced by mothers or aunting females during infant departures (distances greater than 5 feet) and are frequently followed by disciplinary activity by the mother or aunt. In addition, thunks appeared to cease at approximately 9-10 months after birth, concurrent with a decrease in infant dependence. Thunks also were analyzed acoustically for frequency and duration parameters. Thunks have a harmonic structure with an energy peak in the 273–350 Hz range and ranged from 129–5,556 Hz in frequency and from 21–171 ms in duration. They appear to function as aggressive contact vocalizations produced by mothers and other adult females toward infants in order to maintain infant proximity. © 1995 Wiley-Liss, Inc.     

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.     

Social behavior of a group of orangutans (Pongo pygmaeus) on an artificial island in Singapore Zoological Gardens

The behavior of 12 orangutans (three adult males, two adult females, two subadult males, three adolescent males, and two infant males) was observed on a 450-m² island at the Singapore Zoological Gardens (SZG). Male orangutans (6–18 years old) showed less social and solitary play as they aged; adults (over 16 years old) were not seen to play. As they grew older males increasingly spent less time making physical contact, but the amount of time they spent in proximity (within arm's length) to others increased. Adult females regularly played with other group members. Contact, allogrooming, and social play showed nonrandom relationships between individuals. Adult females showed the most allogrooming and contact, adolescent and subadult males the most play. There was no obvious dominance hierarchy. One adult male spent about 10% of his time walking around the perimeter of the island. One-year-old infants rarely interacted with other individuals apart from their own and the other infant's mother. While orangutans lead relatively solitary lives in nature, it was concluded that the opportunities for social contact and play provided by the SZG orangutan island were beneficial to this species in captivity. Opportunities for social interaction provided the animals with a means of increasing the stimulus component of their environment, thus compensating for the inevitable restriction of complexity and unpredictability as compared with the wild state.     

Infant-directed behavior of rhesus monkeys during their first pregnancy and parturition

To determine whether pregnancy influences the response of rhesus monkeys towards infants, 11 females were observed during 15-min exposures to a 1- to 15-day-old infant at 1- to 2-week intervals throughout pregnancy. No evidence was found for increasing willingness to contact infants as pregnancy progressed. The parturition of 5 of these females was observed, which included 1 live breech birth. These primiparae all established ventral contact with their infants at birth, though most of them appeared to passively allow the infant to initiate contact while their own attention was directed at licking the birth fluids.     

Development of behavior and sex differences in infants; with reference to the formation of sex role

In order to observe the formation of sex role, an investigation was made on the development of behavior and sex differences in infants aged 1 to 6 at Fukuoka-city. The present study consisted of questionnaire on behavior of daily living and breeding, block construction test and coloring a drawing test. The parents instructed their infants to become masculine for males and feminine for females on the basis of traditional view. No sex differences were observed in construction ability of infants aged 4. Favorite colors were different according to sex.     

Male-infant relationships in semifree-ranging Barbary macaques (Macaca sylvanus) of affenberg salem/FRG: Testing the “male care” hypothesis

The infant-directed behavior of Barbary macaque males was analyzed in order to determine whether it is essential for an infant's survival during the first year and whether males interact selectively with closely related infants. Dyadic male-infant contacts were recorded in a large group of semifree-ranging Barbary macaques. Data collected during the first 12 weeks of life on each infant born in 1983 (n = 36) were analyzed. All adult and almost all subadult males established strong relationships with at least one infant. Almost two-thirds of the infants (22) had frequent contacts with one or several males. Males showed no preference for closely related infants. Sexual associations with an infant's mother during the preceding mating season had no significant effect. Natal males did not prefer infants of their own matrilineage. There was no evidence that contacts with males had a positive influence on infant survival or that other benefits to the infants resulted from these contacts. Instead, excessive carrying by males and females led to starvation of some very young infants and was a major cause of neonatal deaths in this population. Males interacted preferentially with infants that were born early in the birth season, had a high-ranking multiparous mother, and were male. Younger males established strong relationships with male infants only, while mother's rank was more important for older males. It is suggested that certain mothers prevented early contacts between their infants and males so that the observed preferences for certain infants were also a result of easier access to them. All results suggested that males interacted with infants for their own benefit.     

Infanticide risk and infant defence in multi-male free-ranging sooty mangabeys, Cercocebus atys

For years, infanticide by males was thought to be unlikely in multi-male primate species. Recent studies have, however, presented evidence of infanticide in such species and a recent model by Broom and colleagues predicts that males’ age and rank influence the occurrence of infanticide: youngest and highest-ranking immigrant males are more likely to commit infanticide than their older and lower-ranking counterparts if putative fathers fail to protect infants. I collected data on adult free-ranging sooty mangabey females in the Taï National Park, Ivory Coast, over 11 months including a birth and a mating season. Infanticide had been previously reported in captivity for this species, but not in the wild. Several males entered the group prior to and during the mating season. As predicted by the model, only the more dominant immigrant ones attacked mother-infant pairs significantly more often than did other males. Mothers often reacted with counter-attacks. Potential fathers guarded and supported infants and mothers throughout the period of infant vulnerability. Furthermore, as only one of seven infants died despite 136 observed attacks on mother-infant pairs and unattended infants by immigrant males, we conclude that cooperation between putative fathers and mothers represents an effective protection against infanticide.