Seasonal variation in fecal testosterone levels in free-ranging male Japanese macaques

Seasonal variation in fecal testosterone levels in free-ranging male Japanese macaques (Macaca fuscata) was examined with reference to their dominance rank and age class. Six adult (>or=7 years old, three higher-ranking and three lower-ranking) and four adolescent (5-6 years old, two higher-ranking and two lower-ranking) males were selected as target animals. Fecal samples of these males were collected during the first 3-5 days of each month and analyzed by the method developed by Barrett et al. [Primates 43:29-39, 2002 b]. Testosterone levels varied significantly across the 12 months, and were highest in the early and middle parts of the mating season (i.e., October and November). Higher-ranking adult males displayed a peak testosterone level in October, whereas lower-ranking adults had no clear peak in the mating season. Such a difference in testosterone peaks in males could provide higher-ranking males more opportunities to fertilize females at first ovulation in the mating season than lower-ranking males.     

Brief report: Newborn adoption in a confined group of Japanese macaques

In a group of Japanese macaques, a multiparous high-ranking female gave birth to an infant and, two days later, adopted a neonate abandoned right after birth by a primiparous low-ranking female. Both infants were reared successfully. Whereas the “selfish” explanation does not accord with the evidence from the present case, the “altruistic” explanation cannot be discarded definitively. However, the context and the consequences of the adoption suggest reproductive error on the part of the adoptive mother as the most likely explanation.     

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.     

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.     

Long distance mobility of male Japanese macaques evidenced by mitochondrial DNA

A 487-nucleotide sequence in the polymorphic D-loop region of matrilineally inherited mitochondrial DNA was compared in samples from 14 (9 adult males and 5 females or young) Japanese macaques (Macaca fuscata fuscata) of two troops at Gagyusan in Takahashi City, Okayama Prefecture, Japan. The majority (7 out of the sampled 9) of the adult males associated with the troops had nucleotide sequences of six distinct types, all of which were different from that of the Gagyusan troop females, whereas two young solitary males shared the same sequence. The present study exemplified a case in which the majority of adult males immigrated from outside the local population. Notably, two of the males were revealed to share the same sequence determined for a matriline 45 km away. Electronic Publication     

Relationship between sexual interactions and the timing of the fertile phase in captive female Japanese macaques (Macaca fuscata)

Japanese macaques live in multi‐male/multi‐female social groups in which competition between males, female mate choice, and alternative male mating strategies are important determinants of mating and reproductive success. However, the extent to which adult males rely on female behavior to make their mating decisions as well as the effect of social rank on mating success are not clear as results are inconclusive, varying from study to study. In this study, we combined behavioral and endocrine data of 14 female Japanese macaques to examine the relationship between ovarian cycle phase and frequency of sexual behaviors, and to investigate how social rank influences sexual behavior in this species. We found that there was no increase in female proceptive behaviors during the fertile phase of the ovarian cycle, suggesting that female behaviors did not clearly signal the probability of conception. In spite of that, the frequencies of ejaculatory copulations were highest during this phase, indicating that the attractivity of females increased significantly during the period with higher probability of conception. Males, and especially the highest ranking male, were able to discriminate females nearing ovulation and to concentrate their mating effort, implying that the timing of ovulation was not concealed from them. The α male seemed able to monopolize most female matings, which is probably due in part to the low number of females simultaneously ovulating and to the limited number of inconspicuous places that the lower ranking males have to mate with females and avoid α male aggression. All together, these results suggest that different males may have access to different signals of ovulation and/or are differentially restrained as to how they can act on that information. The exact nature of the estrogen‐related cues males use to recognize female reproductive status, and to what extent males use them warrants further investigation. Am. J. Primatol. 71:868–879, 2009. © 2009 Wiley‐Liss, Inc.     

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.     

Habitual hot-spring bathing by a group of Japanese macaques (Macaca fuscata) in their natural habitat

Japanese macaques (Macaca fuscata) in a free-ranging group in Jigokudani valley, Nagano prefecture, are known to bathe in a hot spring. We used scan sampling in a study aimed at elucidating the causal factors and possible social transmission of this behavior. From 1980-2003, 31% of a total 114 females in the group habitually bathed in the hot spring. The habit was more widespread in dominant matrilines than in subordinate matrilines. Infants whose mothers bathed were more likely to bathe than infants of mothers who did not bathe. The number of monkeys bathing was clearly influenced by ambient air temperature. More monkeys bathed in the hot spring in winter than in summer. The results support the thermoregulation hypothesis of hot-spring bathing. Bathing behavior varies among age and sex categories of monkeys, with adult females and juveniles bathing more often than adult males and subadults. We compared hot-spring bathing with other thermoregulatory behaviors in various primate populations.     

Puberty in male Japanese macaques (Macaca fuscata): Social and sexual behavior in a confined troop

The social and sexual behaviors of four groups of males (4, 5, 9, and 10 years old) were compared throughout one complete mating season in a confined troop of Japanese macaques (Macaca fuscata). The aim of this research was to document social behavior changes that occurred during adolescence and to relate them to changes in sexual behavior that occurred at puberty. The 4-year-old males all mounted females and ejaculated but they had significantly fewer ejaculations and female partners than did the older males. The 4-year-old males also showed a pattern of delayed development in tail carriage and courtship, and they played more frequently than the older males. There were no significant differences in the frequency of aggression among the groups, but both 4-year-old and 5-year-old males were displaced by adult males and females more frequently than were the older males. We concluded that the development of adult patterns of social behavior in this genus is not climactic, but occurs slowly one to two years after physiological puberty has been reached.     

Female reproductive parameters and fruit availability: factors determining onset of estrus in Japanese macaques

This study examined the onset of estrus, nutritional conditions during the mating season, and female reproductive parameters in a troop of unprovisioned Japanese macaques (Macaca fuscata fuscata). The mean interbirth interval (IBI) was 25.1 mo, suggesting a 2-yr birth cycle. The mean IBI following the death of an infant before the mating season was only 19.8 mo, whereas the mean IBI was 27.8 mo when the infant survived. Estrus occurred during the time of the greatest food quality, in the autumn (i.e., mating season). A female whose infant did not survive the mating season tended to come into estrus more readily than one with a surviving infant. Only one of the 19 females whose infants survived came into estrus, whereas 43 of the 58 (74.1%) females whose infants did not survive came into estrus. Fruit conditions during the mating season each year were evaluated by the seed crop of the two species (Fagus crenata and Zelkova serrata) that constituted the main food source for the macaques; fruiting levels were classified as "high-fruit" or "low-fruit." Females came into estrus more often during high-fruit mating seasons than during low-fruit mating seasons: 36 (97.3%) of 37 females came into estrus during high-fruit mating seasons, whereas eight (20%) of 40 females came into estrus during low-fruit mating seasons. Although females came into estrus under both high- and low-fruit conditions during the mating season, estrus seldom occurred when females had a surviving infant, and it appears that the absence of a surviving infant is an almost essential variable for the onset of estrus. When females with a surviving infant were excluded from the analysis because they were unlikely to come into estrus, all 35 remaining females (100%) came into estrus during high-fruit mating seasons, whereas only eight (34.8%) of 23 females came into estrus during low-fruit mating seasons. Therefore, the onset of estrus is strongly affected not only by the survival of infants through the mating season, but also by fruiting conditions, especially the availability of high-quality food.     

Energetic costs of bipedal and quadrupedal walking in Japanese macaques

We investigated the energetic costs of quadrupedal and bipedal walking in two Japanese macaques. The subjects were engaged in traditional bipedal performance for years, and are extremely adept bipeds. The experiment was conducted in an airtight chamber with a gas analyzer. The subjects walked quadrupedally and bipedally at fixed velocities (<5 km/hr) on a treadmill in the chamber for 2.5-6 min. We estimated energy consumption from carbon dioxide (CO2) production. While walking bipedally, energetic expenditure increased by 30% relative to quadrupedalism in one subject, and by 20% in another younger subject. Energetic costs increased linearly with velocity in quadrupedalism and bipedalism, with bipedal/quadrupedal ratios remaining almost constant. Our experiments were relatively short in duration, and thus the observed locomotor costs may include presteady-state high values. However, there was no difference in experimental duration between bipedal and quadrupedal trials. Thus, the issue of steady state cannot cancel the difference in energetic costs. Furthermore, we observed that switching of locomotor mode (quadrupedalism to bipedalism) during a session resulted in a significant increase of CO2 production. Taylor and Rowntree ([1973] Science 179:186-187) noted that the energetic costs for bipedal and quadrupedal walking were the same in chimpanzees and capuchin monkeys. Although the reason for this inconsistency is not clear, species-specific differences should be considered regarding bipedal locomotor energetics among nonhuman primates. Extra costs for bipedalism may not be great in these macaques. Indeed, it is known that suspensory locomotion in Ateles consumes 1.3-1.4 times as much energy relative to quadrupedal progression. This excess ratio surpasses the bipedal/quadrupedal energetic ratios in these macaques.     

Patterns of sexual behavior in male macaques

One large social group of each of three species of macaques (Macaca mulatta, M. fascicularis, M. radiata), housed in half-acre field cages at the California Primate Research Center, were observed for a total of 150 h. Data on sexual behavior and dominance interactions were recorded by pairs of experienced observers using a focal animal technique. Single or multiple mount-to-ejaculation sequences, number of thrusts per mount, number of mounts per sequence, duration of mounts per sequence, duration of sequences, social rank and frequency of sexual activity were recorded for each adult male. M. mulatta used a multiple mount-to-ejaculation (MME) pattern in 91% of their copulations. M. radiata used a single mount-to-ejaculation (SME) pattern in 91% of their copulations. M. fascicularis used both patterns—53% MME and 47% SME. A positive correlation was found between rank and sexual activity in fascicularis and mulatta males. A negative correlation between rank and sexual activity was found in radiata males and also a positive correlation between rank and age indicating that the youngest and most subordinate radiata males were the most sexually active males. In reviewing the literature, a relationship between degree of intermale competition, intermale tolerance and type of mounting pattern was revealed. Macaque species that primarily use an SME pattern also show sa high degree of intermale tolerance and little interrnale competition. Macaque species that primarily use an MME pattern typically show a high degree of intermale competition and a low degree of intermale tolerance. Possible events leading to such relationships are discussed.     

Frog- and lizard-eating behaviour of wild Japanese macaques in Yakushima,Japan

Frog- and lizard-eating and related behaviours were observed on eight occasions in two troops of wild Japanese macaques (Macaca fuscata yakui) in Yakushima, between March 1984 and April 1989. In each case, the first animal seen handling the prey was an adult. Juveniles showed interest in the prey, sniffed or mouthed it in three cases, and ate discarded parts of it in another. In the three cases where capture was observed, detection of the prey appeared to be fortuitous. Four monkeys ate leaves after eating meat. Those leaves identified were of species not commonly eaten. Though invertebrate-eating is common and widespread among Japanese macaques, the consumption of vertebrates is rare. The possibility that these behaviours represent a local tradition among the Yakushima macaques is discussed.     

Of stones and monkeys: testing ecological constraints on stone handling, a behavioral tradition in Japanese macaques

Japanese macaques are known to manipulate stones by displaying various seemingly functionless behavioral patterns, including carrying a stone, rubbing two stones together, or gathering several stones into a pile. This form of solitary object play called stone handling (SH) is a behavioral tradition in Japanese macaques, showing striking intertroop differences in frequency and form. Here, we evaluated two ecologically based hypotheses invoked to account for these differences. We hypothesized that the occurrence and form of SH would be affected by stone availability and the degree of terrestriality. We used standardized sampling methods to assess differences in SH and terrestriality among four captive and six free-ranging troops of Japanese macaques, and determine site-specific stone availability. Although we demonstrated that SH is almost exclusively a terrestrial activity, our comparative analyses showed that the number of stones readily available and the relative amount of time spent on the ground by the macaques were not associated with the intertroop differences in the occurrence of SH. Failure to accept the terrestriality and stone availability hypotheses suggests that the performance of SH and the motivation to engage in this activity are both more diverse and more complex than the direct links to time spent on the ground or the number of stones locally available. Other environmental influences and sociodemographic factors should be jointly considered to identify the sources of variation in SH, as a beginning to better understand the constraints on the appearance and subsequent diffusion of stone-use traditions in nonhuman primates. Am J Phys Anthropol, 2008. (c) 2007 Wiley-Liss, Inc.     

Radio tracking of a male Japanese macaque emigrated from its group

A male Japanese macaque's ranging behavior before and after emigration from its group was investigated by using radiotelemetry techniques. The male's locations before leaving the troop were regarded as those of the troop, while those after leaving were regarded as those of a solitary male. Monthly home range sizes of the male with the troop were larger than those of the male moving alone, while the whole home range of the male with the troop for three months was much smaller than that of the male moving alone for five months. Overlaps between the male's home ranges with the troop between months were much greater than those between the ranges of the male moving alone. One neighboring troop's home range overlapped the male's range in August and September, and another neighboring troop's range overlapped the male's in October. The mean travel distance and speed of the male with the troop per day did not differ significantly from those of the male moving alone. The results suggest that emigrated males of Japanese macaques may visit home ranges of some troops and stay for a while without interacting troop monkeys before they decide to visit or join the troops.     

Troop extinction and fusion in wild Japanese macaques of Yakushima Island,Japan

A wild Japanese macaque troop decreased in size because the birth rate dropped and infant mortality increased. In the 1989 mating season, the last male left the troop, and the remaining two females joined a neighboring troop. Thus, the troop ceased to exist as an independent troop. A lower limit to troop size may exist, below which a troop cannot effectively defend its range, forcing the females to join a larger troop. © 1994 Wiley-Liss, Inc.     

Food provisioning and stone handling tradition in Japanese macaques: a comparative study of ten troops

By addressing the influence of food provisioning on stone handling (SH), a behavioral tradition in Japanese macaques, this study contributes to the ongoing debate in cultural primatology by asking whether human intervention influences the emergence or propagation of behavioral traditions. SH is a form of object play consisting of the manipulation of stones by performing various behavioral patterns. We tested the hypothesis that the frequency of food provisioning affects the daily performance, form, and context of occurrence of SH by influencing a troop's feeding-related activity budget. We used a standardized observation procedure to investigate SH in ten troops of Japanese macaques. In troops provisioned several times a day, SH was more frequent, longer, and more prevalent during provisioning than nonprovisioning periods. These effects of provisioning were not significant in troops provisioned less frequently. SH was more frequently integrated with food-related activities in troops supplied with food several times a day than in the other troops. Food provisioning may be a key factor in the innovation and transformation phases of the SH tradition in Japanese macaques.     

Male endocrine responses to females: Effects of social cues in cynomolgus macaques

This study tested the hypothesis that the hormonal responses of male macaques to sexually receptive females are mediated by specific socioenvironmental cues. Twelve, socially living male Macaca fascicularis were exposed to two-ovariectomized, estrogen-primed females under pair test, peer group, and peer group without dominant male conditions. Preexposure to postexposure changes in serum cortisol levels and testosterone levels were examined in relation to male dominance rank, age, and conditions of access to stimulus females. The males displayed significantly lower cortisol increases and greater testosterone increases with females under peer group than pair test conditions. Dominant males displayed greater testosterone increases than subordinate males under peer group conditions. The testosterone levels of subordinate males were greatly enhanced by removing the dominant male from each group. Adult males displayed greater cortisol responsivity to changes in conditions of access to females than did subadult males. Subadult males displayed greater testosterone responsivity to removal of the dominant male from the group than did adult males. It is concluded that specific social cues can greatly influence the endocrine responses of males to receptive females, and further, that there may be optimal socioenvironmental parameters for eliciting testosterone increases in male primates.