Play behavior in immature moor macaques (Macaca maura) and Japanese macaques (Macaca fuscata)

Play is widespread across mammalian taxa, but species strongly vary in the ways they play. In less despotic primate species (i.e., with less steep dominance hierarchies, less severe conflicts, and more reconciliation), play has been described as being more frequent, cooperative, and freely expressed. To study the link between social play and dominance style, we compared play behavior in free-ranging infants, juveniles and subadults of more despotic Japanese macaques (Macaca fuscata, N = 24) and less despotic moor macaques (Macaca maura, N = 17). We found interspecific differences in play behavior that corresponded with the contrasting dominance styles of the study species, largely confirming our predictions. In particular, moor macaques spent a larger proportion of time in solitary and social play than Japanese macaques, while Japanese macaques spent a larger proportion of time in grooming interactions. In moor macaques, play sessions included more players, a larger variety of play behaviors, greater play face rates, a greater proportion of time in contact play, and a higher rate of reciprocal play-biting than in Japanese macaques. Aggressive escalations were not common, but more frequent in Japanese macaques. Finally, a higher frequency of play faces during play sessions predicted the occurrence of more reciprocal play-bites, but not the proportion of time spent in contact play behaviors. Additional studies on other groups and species will allow a better understanding of the link between dominance style and social play.     

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 behavior and hormonal correlates during the perinatal period in Japanese macaques

This work assessed the changes in both social interactions and estrogen metabolite excreted in feces in eight group-living Japanese macaques (Macaca fuscata). We tested the hypothesis that the social behavior of pregnant females shows significant changes during the late prepartum and early postpartum period. We also tested the hypothesis that the marked fluctuation in estrogen levels during the perinatal period is associated with the changes in social behavior. We found that pregnant females withdrew from the social life of their group in preparation for parturition and only slowly regained their normal social activity after delivery. These changes were correlated with the fluctuation in estrogen conjugate excreted in feces, giving further evidence that hormones can enhance responsiveness to the infant and may predict maternal competence in macaques. We also found that the high frequency of self-grooming by pregnant females during the perinatal period may be a functional way to improve the quality of care toward an infant by a simple shifting from the care for oneself to the care for the infant after parturition.     

Development of intervention behavior in Japanese macaques: Testing the targeting hypothesis

Matrilineal dominance systems, which characterize several species of cercopithecines, are determined largely by the patterning of third-party aggressive interventions in conflicts. Although the role of interventions in structuring rank relations has received much attention, very few studies have dealt specifically with the development of intervention behavior. In other words,most studies have focused on the interventions received and their effect on the recipients rather than on the interventions performed and the goals of the interveners. We analyzed the intervention behavior of 10 juvenile females in a colony of 40 Japanese macaques (Macaca fuscata)housed at the University of Montreal Laboratory of Behavioral Primatology. The analysis of 749 interventions performed by the juveniles over their first 4 years and 2425 interventions received over the same period reveals that (1) juvenile females intervened selectively against females ranking below their mother, (2) they began to intervene at about the same time that they began to challenge the latter females in dyadic contests, (3) they sided with females as well as with males against these females, (4) juvenile interveners incurred little risks in terms of aggressive retaliation from their targets, (5) they derived immediate benefits in terms of conflicts won over stronger targets, (6) interventions often did not take place when the possible recipients needed support, and (7) interveners did not conform to a pattern of mutually preferential support. These results support the view that interventions by juveniles are selfish (vs altruistic) and constitute a low-cost and effective means to target and to outrank prospectively subordinate females.     

Agonistic behavior in a transplanted troop of Japanese macaques: Arashiyama west

Arashiyama A troop was transplanted from Japan to Texas, U.S.A. in February 1972 and released into a large outdoor enclosure (42 ha) in a semi-free ranging condition. Agonistic behavior was quantified during the first six months after the release. Agonistic interactions occurred at about one incident per 100 monkeys every 2 to 9 minutes. In general, peaks in frequency of agonistic interactions coincided with peaks in feeding activity. 97.5% of all incidents were of a “mild” type, and 85.7% were simple one-to-one, unidirectional interactions. “Severe” forms of agonistic behavior occurred only during the first month and then only rarely. Adult females and juveniles were initiators in about 93% of all cases. In general, the more severe the form of attack, the more pronounced was the form of submission.     

Female-male mounting in Japanese macaques: the proximate role of sexual reward

Female Japanese macaques (Macaca fuscata), in certain populations, routinely engage in female-male mounting. In this study, we documented patterns of vulvar, perineal and anal (VPA) stimulation during female-male mounting in Japanese macaques. During approximately 45% of the female-male mounts analyzed, two thirds of female mounters engaged in VPA stimulation. Given the VPA region's primary role in mediating sexual response, the results of this research provide direct evidence bearing on the sexual nature of a substantial proportion of female-male mounts in Japanese macaques.     

Neonatal abandonment in Japanese macaques

This study analyzed long-term demographic data relative to a captive colony of Japanese macaques (Macaca fuscata) in order to evaluate factors predicting increased probability of infant neonatal abandonment. Overall, 7.7% of liveborn infants were abandoned at birth. Probability of abandonment was significantly increased in primiparous and, to a lesser extent, low-ranking mothers. Primiparous mothers abandoned about 40% of their infants at birth. Mother age and infant sex had no independent effects on the probability of neonatal abandonment. Primiparous mothers that did not abandon their infants suffered increased infant mortality and showed longer interbirth intervals compared to same-age multiparous mothers. These results are partially consistent with adaptive hypotheses predicting maternal divestment under unfavorable conditions, and with proximate explanations linking abandonment to inexperience and stress.     

Maze behavior in macaques

Specialization of the right cerebral hemisphere in man for analysis of spatial relations suggests that a similar specialization may exist in macaques. This possibility is being examined in animals first trained to negotiate a maze and then subjected to transection of optic chiasm and forebrain commissures. In the one successful experiment to date, clear evidence of such specialization was obtained for the left hemisphere in a monkey consistently using its left hand for retrieval of food. Provisional evidence for the existence of unilateral engrams in such circumstances was also obtained by limiting input during training to one eye and hemisphere and testing the other before and after completion of transection of the forebrain commissures. Finally, it was found that in the split brain macaque, a lesion in the parietal-occipital area of one hemisphere initially disrupted maze performance using either hemisphere.     

Infant kidnapping and co-mothering in Japanese macaques

The fatal kidnapping of a Japanese macaque infant is described. Kidnapping was followed by a long period (10 weeks) of co-mothering. Quantitative recording showed that both the biological mother (a 8-year-old, low-ranking, multiparous female) and the kidnapper (a 4-year-old, high-ranking female with no maternal experience) displayed an affectionate style of mothering and never responded negatively to the infant's demands for contact. Given the large maternal investment on the part of the kidnapper, we suggest that the fatal outcome for the infant was not the result of reproductive competition. © 1993 Wiley-Liss, Inc.     

Grooming and aggression in captive Japanese macaques

This study investigated the relations between allogrooming and aggression in a captive group of Japanese macaques (Macaca fuscata). Our aim was to test whether evidence of an interchange between allogrooming and a reduction in aggression could be identified at a group level. Female Japanese macaques did not direct less aggression to those group mates that groomed them most. Although generally they did not direct more grooming to those group mates that attacked them most, they did show increased grooming towards those nonkin group mates that showed the most aggression. These results are interpreted in light of the conflicting processes that are likely to underlie macaque social choices.     

Dominance style of Japanese macaques compared with rhesus and stumptail macaques

In the present study, we seek to relate dominance style with group cohesion in a captive group of Japanese macaques (Macaca fuscata). Social data were gathered on approach rate, result, and direction, aggression rate and intensity, grooming rate and direction, and conciliatory tendency. Data were collected using focal animal sampling and instantaneous scan sampling. Reconciliation data were collected using ad libitum observations of aggression with ten-minute post-conflict and matched-control focal observations. Data were compared to prior studies on rhesus (M. mulatta) and stumptail macaques (M. arctoides) living in similar environments. Each species demonstrated the presence of a formalized dominance hierarchy based on the teeth-baring display. The Japanese macaque group showed a lower rate of approach with a higher proportion of negative outcomes than either of the other species. Rates of aggression and reconciliation were also lower in the study troop, suggesting a strict hierarchy while maintaining an optimal nearest-neighbor distance. Overall, this group of Japanese macaques was less sociable than other groups of the same species, perhaps due to a history of individual removals. © 1995 Wiley-Liss, Inc.     

Japanese macaques (Macaca fuscata) social development: Sex differences in Juvenile behavior

We have quantitatively documented the development of sex differences in the behavior of juvenile Japanese macaques (1 to 2 years of age). Mothers treated their offspring differently by sex, i.e., mothers of males broke contact with them more frequently than did mothers of females. Juvenile males played more, and mounted other macaques more frequently; juvenile females groomed their mothers more and were also punished by other group members more frequently than were males. Males showed a pattern of decreasing interactions with their mothers, but females increased the frequency of their maternal interactions. These patterns appear to presage the life histories of the sexes. However, comparisons with other species of nonhuman primates indicate that although sex differences in behavior are common, the variability among species severely limits cross-specific generalizations.     

Vertebral age changes in Japanese macaques

This study deals with maturation and aging of the vertebrae in Japanese macaques (Macaca fuscata fuscata) of known chronological age. The samples used were 103 skeletons of captive raised Japanese macaques varying in age from 6-23 years. Epiphyseal union between the vertebral body and the epiphyseal disk (epiphyseal ring, annular epiphysis) and degenerative changes of the vertebrae were macroscopically examined. It was revealed that vertebral epiphyseal union develops comparatively rapidly in the sacral and cervical vertebrae, moderately in the lumbar vertebrae, and slowly in the thoracic vertebrae. It was found that, as a central tendency, the vertebral epiphyseal union begins at about 6 years of age, progresses lineally in proportion to age, and completes at about 23 years of age. However, considerable variation in developmental states of union was observed among individuals of the same age. Concerning vertebral degenerative changes, few were observed among the present samples. Compared with the other primates with regard to the timing of vertebral maturation, shortening of duration of maturation was found among humans. Human vertebrae may have become an early-maturing organ in order to sustain the increased loading that is accompanied by the adoption of habitual erect posture and bipedal locomotion.     

Relationship between ovarian cycle phase and sexual behavior in female Japanese macaques (Macaca fuscata)

We conducted behavioral observations simultaneously with fecal sample collection on eight nonlactating females 2-3 times per week, October 1997-March 1998, to examine the relationship between ovarian hormones and the sexual behavior of female Japanese macaques (Macaca fuscata) during the mating season. We analyzed samples by enzyme immunoassay for fecal hormone levels. Hormone profiles of estrone-glucuronide (E1) and pregnanediol-glucuronide (PdG) were used to separate ovarian cycles into three phases (follicular, periovulatory, and luteal). Hormonal profiles indicate average cycle lengths of 27.6 +/- 4.2 days (+/- SD; n = 26). Average lengths of the luteal and follicular phases were 12.3 +/- 3.8 days (+/- SD) and 8.3 +/- 3.4 days (+/- SD), respectively. We observed female Japanese macaques engaging in sexual activity throughout the ovarian cycle, with the highest rates occurring during the follicular and periovulatory phases as compared to the luteal phase. The attractivity of female Japanese macaques increased significantly during the follicular and periovulatory phases of the ovarian cycle, when E1 levels are peaking and PdG levels drop to baseline. In addition, females displayed a significant increase in proceptive behavior during the follicular and periovulatory phases. Grooming bouts, as well as proximity between female and male macaques, also increased significantly during the follicular and periovulatory phases. We conclude that fluctuating levels of ovarian hormones in different phases of the cycle are significantly associated with variable rates of copulatory and pericopulatory behaviors in these Japanese macaque females.