Yukiko Shimooka

Seasonal variation in association patterns of wild spider monkeys (Ateles belzebuth belzebuth) at La Macarena, Colombia.

Spider monkeys exhibit a fission–fusion type of social organization. I studied party size and party composition in wild long-haired spider monkeys (Ateles belzebuth belzebuth) in three study periods at La Macarena, Colombia and found that overall party size was larger in the fruit-abundant season. Mean party size in which males were observed was relatively stable across seasons. In contrast, the mean party size of females varied. Females were observed in larger parties in the fruit-abundant season than in the fruit-scarce season. Moreover, whereas males associated with each other at an almost equal frequency across seasons, females associated with each other more frequently in the fruit-abundant season. Females with infants or small juveniles were more often in association with other individuals than were cycling females. The intensity of individual relationships varied according to season, such that even mothers and sons were not always strongly associated. In a large party, females with infants may gain from predation avoidance but they are at a disadvantage in terms of scramble competition. The balance between these factors may change with fruit availability and may influence party size in different periods. For males, party formation may facilitate the defense of resources from neighboring groups more than provide predation avoidance.

Sexual Differences in Ranging of Ateles belzebuth belzebuth at La Macarena, Colombia

I examined sex differences in the ranging patterns of 3 female and 3 male wild spider monkeys. Each of the focal males used the home range widely, whereas each of the focal females used a distinct, restricted area of the home range. The males traveled longer distances than the females did. Although males were consistently in larger parties than females were, travel speed was affected by party composition rather than party size. All-male parties traveled faster than other party types did. Foraging manner also differed between sexes. Males spent more time feeding on fruits and less time on flowers and traveled longer distances between feeding trees. Both males and females used salados, where they ate soil and drank water. Salado location is likely to have affected the ranging pattern. Males used boundary areas more frequently than females did, often traveling along the boundary area in alliance with other males. Males also used areas that had been part of neighboring groups’ home ranges and were not used at all by females of the group. Greater travel distance of males is likely to be facilitated by consumption of a higher caloric diet. I compare the social structure of spider monkeys with that of chimpanzees, whose society is characterized by male-philopatry and female dispersion.

Effects of caller activity and habitat visibility on contact call rate of wild Japanese macaques (Macaca fuscata).

A major function of contact calls in nonhuman primates is to maintain spatial cohesion among individuals in a group. The risks of spatial/visual separation from the group are likely to affect auditory contact behavior, in particular by increasing the call rate. We tested whether the risk of separation influences coo call emission by investigating the variation in call rate among behavioral contexts in two wild populations of Japanese macaques (Macaca fuscata). We focused on caller activity and the degree of visibility within the habitat as primary potential factors mediating call rate. We first estimated the habitat visibility of the two research sites at Yakushima Island (YK) and Kinkazan Island (KZ), Japan. The habitat visibility of YK was significantly more restricted than that of KZ. We then compared the call rate of 20 adult and 12 juvenile female macaques between the two wild populations to examine the potential effects of environmental differences. Both populations had a lower call rate during grooming than during feeding and moving, which are behaviors associated to higher interindividual distances. The call rate of YK adult females was significantly greater than that of both juveniles and KZ adult females, independently of activity. The call rate increased as macaques matured in the YK population, but not in the KZ population, suggesting that different developmental processes involved in contact calling of the two populations. Our findings suggest that separation risk influences call rate, and also imply a possibility of social influence that social structure change effects on the call rates. Am. J. Primatol. 70:1055–1063, 2008.

Association Networks and Life History of Female Spider Monkeys

The social system of spider monkeys is characterized by female dispersal and fission–fusion social organization. After emigration from a natal group, a female spider monkey is expected to experience variation in their reproductive status, which may in turn be expected to alter association patterns within the new group. Until now, analyses on association patterns in spider monkeys have most often been studied on an annual basis, but such time-constrained analyses may bury long-term patterns of association and potential variation across multiple reproductive cycles. In this study, I examine the variation of female association in relation with her reproductive status through social network analysis in three relatively short-term periods of 2–3 months each across several years. Network analysis showed clear clusters for each sex, but there was variation among periods. Lactating females were always central, and cycling females were always drawn outside of their core network. Pregnant and possibly cycling females, and a lone immigrant female, were typically peripheral in other females’ cluster. Two metrics – both eigenvector centrality and network strength – were affected by females’ reproductive status, which were highest in lactating females and lowest in cycling females. Although initially peripheral in the network, a young immigrant female subsequently became the center of a female cluster upon giving birth to a baby, one and a half years after immigrating. Short-term network analysis was useful to explain the variation of roles an individual plays in fission–fusion social organization.

Embracing in a Wild Group of Yakushima Macaques (Macaca fuscata yakui) as an Example of Social Customs

Recently, some primatologists have begun studying social customs, which had been neglected in research despite their importance to human culture. We observed embracing behaviors 64 times during 543.8 hours of focal animal sampling, targeting adult females in a wild group of Japanese macaques in Yakushima, Japan, and compared the results with those in macaques in Kinkazan. Embracing occurred immediately after the spontaneous pause of allogrooming, aggressions, and approach between dyads frequently exchanging antagonistic interactions, all of which are considered to be stressful conditions. Embracing in Yakushima may, therefore, serve to reduce stress; this may also be the case in Kinkazan. Despite this functional similarity, the forms of embracing in Yakushima are slightly different from those in Kinkazan. First, not only ventro-ventral embraces, but also ventro-lateral and ventro-dorsal embraces were found in Yakushima. Second, kneading another’s fur by rhythmically opening and closing the palm occurred in Yakushima, instead of a rhythmic, body-rocking movement in Kinkazan. Because we cannot devise genetic or ecological explanations for the subtle local differences in embraces, this type of behavior may be identified as the first evidence for social customs in wild Japanese macaques.

Life History Tactics in Monkeys and Apes: Focus on Female-Dispersal Species

Primates show life history traits similar to those of cetaceans, such as small litter size, long gestation, long lactation, and long lifespan, in spite of striking contrasts in habitats, diet, mobility, and range size between them. Ecological factors (food and predation) may influence their life history traits in various ways, but social factors (social structure and reproductive strategies) may be more important for the life history of primates, in which both sexes live together even outside the breeding season. Group-living primates are classified into female-bonded species and female-dispersal species, based on the patterns of female dispersal after maturity. A comparison of life history parameters shows that female-dispersal species have a slower life history (gestation length, weaning age, age at first reproduction, and interbirth interval) than the female-bonded species, except for neonatal weight and weaning weight, which may be determined in relationship to female body weight. To elucidate factors promoting the slow life history, we focus on Atelinae and Hominidae (female-dispersal species) and examine their interspecific and intraspecific variation in social structure and male reproductive tactics in relationship to life history traits. Most Atelinae species form multimale and multifemale groups, and variation in their life history features may reflect relationships among males and their reproductive tactics. In howler monkeys, both males and females disperse, and infanticide by males may lead to a fast life history. In other Atelines, infanticide rarely occurs, although it has the effect of reducing interbirth interval. Forcible copulation by males occasionally occurs in spider monkeys. Variations in grouping among females reflecting their flexible foraging efforts according to distribution of high-quality foods may have some effects on the fast–slow continuum in the life history features of female Atelinae. Hominidae exhibit larger variations in life history features than Atelinae, probably because of their diverse social structure. Solitary nature and male reproductive tactics may have great influences on the life history of female great apes. Female orangutans, who usually live a solitary life, show the slowest life history. Maturing female orangutans need a longer time to establish their own home range and relationships with reproductive mates than female chimpanzees and gorillas, who transfer into other groups immediately after emigration. Female gorillas show the lowest age at first reproduction and the shortest interbirth interval. Intensive caretaking of the immature by male gorillas may facilitate early weaning, and infanticide by males may promote a prolonged bonding between a protector male and females to shorten the interbirth interval. Similar life history traits have been found in four long-term study sites of chimpanzees. Only females at Bossou show a fast life history, probably the result of high-quality foods and single male group composition under isolated conditions. The more frequent and stable association between females and males and more promiscuous mating in bonobos may facilitate the search for mating partners and lead to a shorter interbirth interval than chimpanzees. Frugivorous orangutans and chimpanzees may suffer more costs of female dispersal through decreased foraging efficiency than folivorous gorillas, and chimpanzees with fission–fusion grouping may suffer more social stress than gorillas in highly cohesive groups. Such differences may generally shape the fast–slow continuum of life history in female-dispersal primate species.