Masayuki Nakamichi

Birth in Free-ranging Macaca fuscata

The birth process is an integral part of reproductive success in mammals, yet detailed, quantitative descriptions of parturition in nonhuman primates are still rare. Observations of free-ranging births can help to elucidate factors involved in this critical event, to contribute to our understanding of how maternal and infant behaviors during parturition affect infant survival and to explain the evolution of human birth. We provide data on the parturition behavior of 4 multiparous Japanese macaques: 2 daytime live births that we photographed and video recorded at the Awajishima Monkey Center (AMC), Awaji Island, Japan in 2006; a daytime live birth video recorded in 1993 at the AMC; and a nocturnal breech stillbirth of a captive Macaca fuscata, video recorded at the Kyoto Primate Research Institute in 2006. Certain behaviors were similar among the females, such as touching of the vulva followed by licking of fingers, squatting during contractions, and average contraction durations. Parturient females facilitated the birth manually by guiding the emerging infant. There were also dissimilarities in the duration of the labor and birth stages, condition of the infant at birth, and the mother’s behavior immediately postpartum. The mother’s postpartum behavior ranged from almost entirely infant-focused to predominantly related to the consumption of the placenta. The 3 free-ranging females all showed considerable social tolerance during labor and birth. We argue that social proximity at parturition is more common in nonhuman primates than previously emphasized, and has potential adaptive advantages.

Disability, Compensatory Behavior, and Innovation in Free‐Ranging Adult Female Japanese Macaques (Macaca Fuscata)

Little is known about consequences of disability in nonhuman primates, yet individuals with disabilities can reveal much about behavioral flexibility, innovation, and the capabilities of a species. The Macaca fuscata population surrounding the Awajishima Monkey Center has experienced high rates of congenital limb malformation for at least 40 years, creating a unique opportunity to examine consequences of physical impairment in situ, in a relatively large sample of free‐ranging adult monkeys. Here we present behavioral data on 11 disabled adult females and 12 nondisabled controls from 279 hours of randomly ordered 30‐minute focal animal follows collected during May–August in 2005, 2006, and 2007. We quantified numerous statistically significant disability‐related behavioral differences among females. Disabled females spent less time begging for peanuts from tourists, and employed a behavioral variant of such peanut begging; they had a lower frequency of hand use in grooming and compensated with increased direct use of the mouth or a two‐arm pinch technique; and they had a higher frequency of self‐scratching, and more use of feet in self‐scratching. Self‐scratching against substrates was almost exclusively a disability associated behavior. Two females used habitual bipedalism. These differences not withstanding, disabled females behaved similarly to controls in many respects: overall reliance on provisioned and wild foods, time spent feeding, and feeding efficiency did not differ among females, and there was no time difference in behavior performed arboreally or terrestrially. Disabled adult females were able to compensate behaviorally to perform social and life‐sustaining activities, modifying existing behaviors to suit their individual physical situations and, occasionally, inventing new ways of doing things. Am. J. Primatol. 74:788‐803, 2012.

Distribution of dorsal carriage among simians

We surveyed the literature and obtained information from primate researchers and zookeepers to study the distribution of dorsal carriage among 77 simian species including New and Old World monkeys and apes in relation to arboreality and terrestriality, birth (litter) weight relative to maternal weight, and presence or absence of distinct natal coat colors. All New World monkeys are arboreal and commonly carry their infants dorsally. Conversely, arboreal Old World monkeys do not use dorsal carriage, and only some predominantly terrestrial Old World monkeys do so. Whereas lesser apes (which are highly arboreal) do not use dorsal carriage, arboreal as well as more terrestrial great apes commonly carry their infants dorsally. These findings indicate that simple arboreality or terrestriality is inadequate to explain dorsal carriage by monkeys. Infants of small- to medium-sized New World monkeys have relatively high birth weight compared with maternal weight, and are most likely to be carried dorsally than ventrally even on the first postnatal day. In contrast, infants of large-bodied New World monkeys are carried ventrally first and then dorsally up to the end of their second year, albeit increasingly infrequently. Among Old World monkeys, no association was found between mode of infant transport and birth weight relative to maternal weight, but some terrestrial Old World monkeys displaying dorsal carriage tend to do so with older infants, indicating that such behavior enables the mother to transport the infant with lower energy expenditure. Among terrestrial Old World monkeys, infants with distinctive natal coat colors are rarely carried dorsally until the natal coat color changes to adult coloration: infants with distinctive coat colors clinging to the backs of carriers could be highly visible and thus vulnerable to predation. Dorsal carriage by mothers may prolong the affiliative mother–infant relationship.

Social consequences of disability in a nonhuman primate

Debates about the likelihood of conspecific care for disabled individuals in ancestral hominins rely on evidence from extant primates, yet little is known about social treatment (positive, neutral or negative) of physically disabled individuals in nonhuman primates. A group of free-ranging Japanese macaques (Macaca fuscata) at the Awajishima Monkey Center (AMC) in Japan presents a unique opportunity to investigate the relationships between physical impairment and social behavior, in the context of congenital limb malformation in adult nonhuman primates. We collected behavioral data on 23 focal animals, taking 30-minute continuous time samples on disabled and nondisabled adult female Japanese macaques during three consecutive birth seasons (May-August 2005, 2006, and 2007). Disabled females were less social overall compared with nondisabled controls, a pattern that was evident from a variety of measures. Disabled females rested significantly more and socialized significantly less compared with controls, had fewer adult female affiliates, fewer adult female grooming partners, and spent less time engaged in grooming with adult females. Some measures suggested that the social differences were the result of behavioral flexibility on the part of disabled females compensating for their disabilities with lower levels of social involvement and more rest. Disabled females were as successful at groom solicitations as were nondisabled females and the ratio of disabled and nondisabled affiliates was similar among focal animals; there was no strong preference related to the disability status of affiliates. Disabled females were also bitten and chased less frequently. Overall, there was little evidence either for conspecific care or for social selection against disability. In general, there was a socially neutral response to disability, and while neutral social context allows for the possibility of care behaviors, our findings emphasize the self-reliant abilities of these disabled primates and suggest caution when inferring conspecific care for even very disabled ancestral humans.

Function of grunts, girneys and coo calls of Japanese macaques ( Macaca fuscata ) in relation to call usage, age and dominance relationships

We investigated how the context of the production of vocalizations used in social interactions among Japanese macaques (Macaca fuscata) affects their outcome. We focused on a variety of soft vocalizations, including three acoustically distinct call types: grunts, girneys, and coo calls. We predicted that call outcomes would be influenced by call combinations and exchanges, and by the relationship between the caller and the recipient. We observed social interactions among female Japanese macaques, and found that individuals were less likely to initiate agonistic behaviour when they emitted calls. Call exchanges and call combinations increased the occurrence of affiliative interactions. The probability of affiliative interaction following a given type of call differed according to the relationship between the caller and the recipient. These findings suggest that recipients interpret these calls within a social context; they also demonstrate the existence of complex communicative abilities that integrate vocalizations and context in these monkeys.

Influence of social interactions with nonmother females on the development of call usage in Japanese macaques

The goal of this study was to clarify whether social experience affects developmental changes in call usage in Japanese macaques, Macaca fuscata. We focused on vocalizations primarily used as greeting signals, such as grunts, girneys and coo calls. We hypothesized that the degree of interaction with adult females other than mothers would facilitate selective call usage towards less familiar individuals in young monkeys. To test this, we conducted observations on female monkeys from infancy to full adulthood in a free-ranging group, and found that young adult and full adult subjects produced calls more frequently when approaching unrelated, than related, adult females. In contrast, subadults, juveniles and infants did not produce calls selectively towards unrelated adults. Monkeys older than juveniles were more likely to engage in affiliative interactions after approaching unrelated females with than without calls, indicating that calling can be beneficial for signallers. Individuals who had more frequent interactions with unrelated adult females used calls more frequently towards unrelated adult females in subsequent observation years, an effect that was stronger in older animals. These findings suggest that calling towards unrelated adult females is facilitated through tangible interactions with these females. The interactions with related adult females did not influence calling towards relatives or nonrelatives, indicating that interaction with relatives did not facilitate call usage. We conclude that social experience with unrelated adult females modifies vocal greeting behaviours, which, in turn, may mediate social relationships between unrelated individuals.

Japanese macaque (Macaca fuscata) mothers huddle with their young offspring instead of adult females for thermoregulation

It is unclear whom animals select to huddle with for thermoregulation. In this study, we investigated whom Japanese macaque (Macaca fuscata) mothers huddled with-their young offspring or other adult group members-when there is need for thermoregulation. We used a focal-animal sampling method, targeting 17 females at Katsuyama, Okayama Prefecture, Japan. A majority of huddling among adult females was recorded during winter season (December, January, and February). Females who had young (0- or 1-year-old) offspring huddled less frequently with other adult females compared to females who did not have young offspring in winter. However, including young offspring, the frequency of huddling with any other individuals did not differ by whether females had young offspring. Moreover, the females who did not have young offspring huddled with other adult females more often in cloudy than in sunny weather during winter season. In contrast, females who had young offspring increased huddling with their young offspring in cloudy than in sunny weather, but did not do so with other adult females. This study indicates that Japanese macaque mothers huddle with their young offspring instead of other adult females when there is need for thermoregulation.

Twelve‐year proximity relationships in a captive group of western lowland gorillas (Gorilla gorilla gorilla) at the San Diego Wild Animal Park, California, USA

Proximity data were collected in a captive breeding group of gorillas (Gorilla gorilla gorilla) at the San Diego Wild Animal Park (currently called the San Diego Zoo Safari Park) twice a year (spring and fall periods) for over 12 years, by using a convenient method in which individuals less than 5 m from each animal in the group were recorded by scan sampling, approximately once per hour. Immature females from infancy to young adulthood maintained relatively frequent proximity to both their mothers and the silverback male and spent little time alone (no animals within 10 m), with relatively large individual differences. On the other hand, immature males decreased the time spent near their mothers and the silverback male and increased the time spent alone with increasing age. Therefore, sex differences in proximity to mothers and the silverback male became apparent after late juvenility. Some adult females maintained increased frequency of proximity to the silverback male than that by other females over the 12-year period, indicating the presence of long-term, stable proximity relationships between the silverback male and the adult females. Such long-term, stable proximity relationships were also observed among adult females. Some association patterns reported in wild gorillas, such as frequent proximity between adult females with dependent offspring and the silverback male and close relationships between related females, were not observed in the present study. The idiosyncratic or individual factors influencing some association patterns were easily reflected in captive situations.