Post-Conflict Anxiety in Japanese Macaques (Macaca fuscata): Aggressor's and Victim's Perspectives

The aim of this study was to investigate the short‐term consequences of aggression in socially living Japanese macaques (Macaca fuscata) focusing on the emotional response of both aggressors and victims of aggression. Both individuals involved showed an increase in the rate of scratching (a behavioural indicator of anxiety) in the minutes following the aggressive confrontation. Such increase was larger in victims than in aggressors. Multivariate analyses of the factors modulating post‐conflict scratching showed that for both the aggressor and the victim the main predictor of post‐conflict scratching was its opponent’s post‐conflict scratching. These results suggest both opponents shared the same perception of the consequences of aggression, and responded with similar emotional arousal.     

Urological Screening of a Wild Group of Japanese Macaques (Macaca fuscata yakui): Investigating Trends in Nutrition and Health

Primates are among the most threatened of animal taxa, and it is therefore increasingly important to examine ways to monitor their health in the wild. We here investigate trends in nutrition and health in Japanese macaques (Macaca fuscata yakui) under natural conditions using a common tool from human and veterinary health practices: urinalysis. Between October 2007 and August 2009, we collected 103 urine samples ad libitum from 29 identified individuals of a group of macaques on Yakushima Island. We used multireagent dipstick analysis to examine variation in 10 urine chemistry parameters across subjects in combination with systematic monitoring of clinical signs of disease (via focal sampling). Positive tests tended to be transient and weak, i.e., analytes detected in trace amounts, and were not associated with clinical signs of disease. In addition, most urine samples we collected were highly concentrated (urine specific gravity ≥1.030), which could have increased the likelihood of detecting clinically insignificant amounts of analytes that can occur in urine. However, we found that ketone bodies, which are not normally found in urine, were more prevalent during winter than summer, which may indicate that Japanese macaques inhabiting the richest habitat available to the species nonetheless experience an energy deficit during periods of low food quality and high thermoregulatory costs. We conclude that dipstick urinalysis can be used to examine general trends in nutrition and health, but that results must be interpreted with care because positive tests may not reflect clinically significant urological conditions in many cases.     

Socioecological Context of Parturition in Wild Japanese Macaques (Macaca fuscata) on Yakushima Island

Female primates may adopt special feeding, foraging, and social strategies around the time of giving birth. We observed 8 females during the prepartum period, the day of birth, and the postpartum period in a wild troop of Japanese macaques (Macaca fuscata yakui) on Yakushima Island, Japan. We collected data on their activity budgets, quantitative feeding and foraging behavior, and on female-male interactions. On the day of birth, females spent less time moving and feeding, and more time resting relative to other periods. Overall dietary diversity as well as arthropod foraging also decreased on the day of birth. Females fed mostly on mature leaves, new leaves and shoots during prepartum periods but mostly on fruit during postpartum periods. Decreased feeding on leaves and increased feeding on fruit probably changed as a result of seasonal availability, independently of parturition. Feeding on flowers, fungi and other items remained constant over all periparturitional periods. On the day of birth, new mothers had fewer social interactions with males and spent more time out of proximity with other adults than in other periods. Females rejected grooming presentations from males, groomed less with males, spent less time 3 m of males, and received less aggression from males on the day of birth. In the postpartum period, interactions with males returned to prepartum values. Grooming with females did not differ across the three periods. These results suggest that interactions with males may be costly for females on the day of birth.     

Discrimination of mother by infant among Japanese Macaques (Macaca fuscata)

Experiments on five mother-infant pairs of Japanese monkeys (Macaca fuscata)living together in a captive group were conducted during the first 12 weeks after birth in order to assess the time at which infants begin to discriminate their own mothers from other adult females. After removal from their social group, infants exposed to their mothers and three unfamiliar adult females at a distance of 150 cm failed to orient visually toward their mothers. However, when the infants were allowed to approach the four females, they responded preferentially to their mothers during the third month of life. We concluded that by 8–12 weeks of age, infant Japanese macaques are able to discriminate between their mothers and other adult females.     

Multimodal Advertisement of Pregnancy in Free-Ranging Female Japanese Macaques (Macaca fuscata)

The role of multiple sexual signals in indicating the timing of female ovulation, and discrimination of this timing by males, has been particularly well studied among primates. However the exhibition of pregnancy signals, and how such signals might modulate male post-conception mating decisions, is still poorly understood. Here we aimed to determine if Japanese macaque males use changes in female sexual signals (behavioral, visual and auditory) to discriminate pregnancy and adjust their socio-sexual behaviors. We combined behavioral observations, digital photography and endocrinological (progestogen and estrogen) data, collected systematically during three one-month periods: the pre-conceptive period, the 1^st month of pregnancy and the 2^nd month of pregnancy. We analyzed variation in the probability of detecting male and female socio-sexual behaviors and estrus calls, as well as changes in female face color parameters, in relation to female reproductive state. Based on our focal observations, we found that males did not copulate during the pregnancy period, and that female socio-sexual behaviors generally decreased from the pre-conceptive to post-conceptive periods. Female face luminance decreased from the pre-conceptive month to the pregnancy period whereas face color only varied between the 1^st and 2^nd month of gestation. Our results suggest that Japanese macaque females display sexual cues of pregnancy that males might use to reduce energy wasted on non-reproductive copulations with pregnant females. We hypothesize that females advertize their pregnancy through changes in behavioral, visual and potential auditory signals that males can use to adjust their mating behaviors. We finish by discussing implications for male and female post-conception strategies.     

Consort Intrusion and Female Mate Choice in Japanese Macaques (Macaca fuscata)

Consort intrusion behavior has been proposed to largely function as a means of preventing or suppressing the reproductive activity of subordinate males. In the Japanese macaques of Arashiyama B troop this behavior was found to be ineffective in influencing female mate choice and affecting differential reproduction. Mainly directed towards the female of the pair intrusion resembled sexual solicitation and appeared to be an extension of consort behavior. Although the intruder male was almost always dominant over the other male, intrusion failed to provide priority of access to the estrous female as she most frequently chose to remain with her current partner. Copulations which were intruded upon were as likely to end in ejaculation as those which were undisturbed. Only a small proportion of intruder male-female pairs mated. Pairs that did mate were likely to have been in consort before or during the period in which intrusion occurred. No significant correlation was found between male rank order and number of possible females impregnated. Individual young, middle to lower ranking males were estimated to have been reproductively the most successful.     

Measuring male-female relationships during the mating season in wild Japanese macaques (Macaca fuscata yakui)

Heterosexual relationships during one mating season were examined in a wild troop of Japanese macaques (Macaca fuscata yakui) on Yakushima Island, Japan. Validation tests of putative mate choice behaviors demonstrated that female initiation and maintenance of proximity, female lookback at the male, and sexual presents to the male, were associated with increased mating. Male grooming the female was also associated with increased mating. Ten dyadic social behaviors were subject to principal components analysis to empirically define behavioral dimensions of male-female relationships. The analysis yielded four relationship dimensions: ‘Mutual Choice and Male Coercion,’ ‘Female Choice’ (two types), and ‘Mutual Choice’ Dyads tended to be characterized by more than one dimension. The results suggested that females sought matings with multiple males of various dominance ranks. Female relationships with high ranking males contained elements of male coercion and mate guarding, however, because these males attempted to inhibit females from mating with lower ranking males. The correlation between each relationship dimension and mating success depended, in part, on the dominance rank of males. Relationships involving high ranking males, which were most likely to contain elements of male coercion and mate guarding, were associated with mating success. Relationships involving low ranking males, which usually lacked such coercive elements. were less strongly correlated with mating success. These results, obtained from a wild troop, are compared to those previously obtained in captive and provisioned groups of Japanese macaques.     

The Long-Term Effects of Reconciliation in Japanese Macaques Macaca fuscata

With one exception, all previous studies of reconciliation in non-human primates (friendly reunion between former opponents) have focused on demonstrating the immediate, short-term effects despite the widely held view that reconciliation has a long-term function of repairing social relationships following aggression. To investigate this long-term function I compared mean interaction rates between opponents during the 10 d following reconciled and non-reconciled conflicts to baseline levels of interaction. Aggression rates during the 10 d after non-reconciled conflicts were significantly higher than the baseline rate, whereas after reconciled conflicts aggression was minimal. Similarly, grooming, proximity and approach rates during the 10 d after non-reconciled conflicts were significantly lower than the baseline rate whereas grooming, proximity and approach rates in the 10 d after reconciled conflicts were restored to baseline levels. These results indicate that there are consequences to not reconciling with a former opponent and highlight the fact that these may be costly in terms of increased risk of long-term aggression and reduced affiliation. The data support predictions from the Relationship-Repair Hypothesis suggesting that reconciliation functions as a mechanism for the repair of social relationships damaged by aggression.     

Seasonal Effects on Reconciliation in Macaca fuscata yakui

Dietary composition may have profound effects on the activity budgets, level of food competition, and social behavior of a species. Similarly, in seasonally breeding species, the mating season is a period in which competition for mating partners increases, affecting amicable social interactions among group members. We analyzed the importance of the mating season and of seasonal variations in dietary composition and food competition on reconciliation in wild female Japanese macaques (Macaca fuscata yakui) on Yakushima Island, Japan. Yakushima macaques are appropriate subjects because they are seasonal breeders and their dietary composition significantly changes among the seasons. Though large differences occurred between the summer months and the winter and early spring months in activity budgets and the consumption of the main food sources, i.e., fruits, seeds, and leaves, the level of food competition and conciliatory tendency remained unaffected. Conversely, conciliatory tendency is significantly lower during the mating season than in the nonmating season. Moreover, conciliatory tendency is lower when 1 or both female opponents is in estrous than when they are not. Thus the mating season has profound effects on reconciliation, whereas seasonal changes in activity budgets and dietary composition do not. The detrimental effects of the mating season on female social relationships and reconciliation may be due to the importance of female competition for access to male partners in multimale, multifemale societies.     

Birth-season interactions of adult female Japanese Macaques(Macaca fuscata) without newborn infants

The affiliative interactions of 11 adult female Japanese macaques that did not deliver an infant during the 1981 birth season of the Arashiyama West troop were examined. Consideration was given to the effects of kinship as a structuring element in these birth-season interactions and to the degree of association with various categories of troop members based on age, sex, and (in the case of adult females) whether or not the females were new mothers. Females without infants interacted predominantly with their yearling off-spring, although it was the behavior of the offspring that precipitated the interaction. These females were active in soliciting affiliation with nonkin new mothers, whereas female matrilineal relatives with new infants approached and remained in proximity to them more than did nonrelated new mothers. Females without newborns groomed and approached nonkin infants more than infants within their own matriline, and these infants were predominantly those of females in the highest-ranking matriline of the troop. Adult males were responsible for 40% of all grooming received from nonkin by the females without newborns, and these males approached them significantly more than did other adult females without infants. These patterns demonstrate that the structure of social relationships is influenced by the particular dynamics of troop contexts such as birth seasons, as well as by enduring, broad-based affinities which are less affected by cyclic changes in troop context.     

Cheek-pouch dispersal of seeds by Japanese monkeys (Macaca fuscata yakui) on Yakushima Island, Japan

Seed dispersal by Japanese monkeys (Macaca fuscata yakui) via cheek-pouch was studied in a warm temperate evergreen forest on Yakushima Island. Plant list was compiled based on a study during 1986–1995, of which troops of monkeys have been habituated without artificial feeding. We followed the well-habituated monkeys in 1993 and 1994 to observe the feeding behavior and their treatments of fruits and seeds, and collected seeds dispersed by monkeys to record the distance carried from the mother trees. We checked the difference of germination ratio between seeds dispersed via cheek-pouch and seeds taken from mother trees by sowing experiments. Seeds and acorns of 22 species were observed to be dispersed via cheek-pouch of monkeys. Among them, three species with acorns were never dispersed via feces, and 15 species with drupes were seldom dispersed via feces. Plant species of which seeds are dispersed only via cheek-pouch had larger seeds than those of dispersed both via cheek-pouch and via feces, and typically had only one or two seeds in a fruit. As for one of cheek-pouch dispersal species,Persea thunbergii, the mean distance when seeds were carried from the mother trees via cheek-pouch was 19.7 m, and the maximum distance was as long as 105 m although more than 80% of seeds were dispersed within 30 m from mother trees. And 82% of seeds dispersed via cheek-pouch germinated. The easy separation of seeds from other parts of the fruit seems to facilitate cheek-pouch dispersal more than dispersal via feces. Cheek-pouch dispersal by monkeys has possibly enhanced the natural selection for larger seeds which bring forth larger seedlings with high shade-tolerance. In conclusion, cheek-pouch dispersal by monkeys is quite an important mode for trees in the mature stand in a warm temperate evergreen forest on Yakushima Island.     

Voiceprint identification and its application to sociological studies of wild Japanese monkeys (Macaca fuscata yakui)

Japanese monkeys often exchange the particular vocal sound, “coo,” especially when they feed or move as a group. It was considered that the “coo” sound had no positive social meaning, perhaps because the “coo” sound network and its function were hidden behind other behavioral observations. For identification of the vocalizer only from hearing the “coo” sound, three phonetic values, i.e., the “fundamental,” “duration,” and “formants,” plus other characteristics were used as indices of voiceprints. The results indicated that these were effective for identifying the vocalizer in two-thirds of the adults in the study troop which was composed of 12 adults and 16 immature members. The “coo” sound exchange network among the troop members (adults) was drawn on the basis of the voiceprint identification. The network showed three characteristics as follows: (1) matriarchs of the kin-groups frequently exchanged “coo” sounds with each other; (2) the other females exchanged “coo” sounds mostly within their own kin-groups; and (3) males seldom participated in the “coo” sound exchange. This suggests that “coo” sound exchange plays a central role for the matriarch of kin-groups in binding each kin-group and, ultimately, in binding all members together into an organized troop.     

Mirror guided behavior in Japanese monkeys (Macaca fuscata fuscata)

Two male Japanese monkeys were trained to use a mirror to reach an object that could not be seen directly. Training to use a mirror in this way proceeded, step-by-step, from reaching a piece of apple to key-tracking. In Experiment 1 the monkeys were trained to use the mirror to locate a desired object, a piece of apple in a box facing the mirror, which could be seen only by looking into the mirror. The apple, once located, however, could be grasped without further reference to the mirror. This behavior is referred to as mirror mediated object discrimination. In subsequent experiments the monkeys could not reach the goal object except by observing it and his hand movement in the mirror. In Experiment 2 the target was a piece of apple visible in the mirror, in Experiment 3 an illuminated key and in Experiment 4 a series of keys which were illuminated sequentially. Mirror guided behavior such as shown in Experiment 2, 3, and 4 has not previously been demonstrated in monkeys.     

Sex, Rank and Age Differences in the Japanese Macaque (Macaca fuscata yakui) Participation in Inter-Group Encounters

In many species interactions among group are often characterized by agonistic behaviour. Although animals may participate in inter‐group encounters in different ways, depending on their energetic requirements, reproductive tactics, and/or developmental stage, the proximate causes affecting an animal's participation in inter‐group encounters are still poorly understood. Indeed, many studies have analysed the behaviour of males and females during inter‐group encounters without considering the importance of additional factors (e.g. rank). This study focuses on wild non‐provisioned Japanese macaques (Macaca fuscata yakui) living on Yakushima Island, Japan. It aims to determine how monkeys of different sex, age, and rank behave during inter‐group encounters and it discusses the implications and consequences of their behaviour on group composition and male dispersal. Males participated significantly more than females in inter‐group encounters, by displaying more aggressive or affiliative behaviour. High‐ranking and/or adult males were more aggressive than low‐ranking and/or subadult males during encounters occurring in the mating season and they also showed more herding behaviour. This trend was not found in inter‐group encounters occurring during the non‐mating season. Finally, males which then emigrated to new groups were low‐ranking and/or subadult individuals. Those males displayed more affiliative behaviour towards foreign males than males which did emigrate. These data indicate that in non‐territorial species with male dominance over female and high competition for mating partners males play an active, and often aggressive, role during inter‐group encounter while female participation is scarce. Factors such as age, rank and period of the year (in seasonally breeding species) have to be taken into considerations when analysing interactions between groups and their effects on group composition and social behaviour.     

Activity patterns of a troop of Japanese monkeys (Macaca fuscata yakui) on Yakushima Island,Japan

Activity patterns of Japanese monkeys (Macaca fuscata) were observed for 240 hr from August to December 1976 on the western slope of Mt. Kuniwari, Yakushima Island, Japan. Activity patterns and the time budget of a habituated wild troop which consisted of 47 animals in August 1976, were studied quantitatively by using the scan-sampling method at 15-min intervals. Six thousand seven hundred and six animals were recorded in 959 scans during the study period and the mean number of animals seen per scan was 7.0. The time budget established for different categories of activity was as follows: inactive—20.9%; moving—22.8%; feeding—23.5%; social grooming—27.9%; self-grooming—1.2%; and other activities—3.7%. Adult males spent less time in feeding and more time in resting or being inactive than females or juveniles. The daily activity patterns were highly variable with respect to time. Intraspecific variations were examined between troops in several regions of Japan and it was noted that the percentages of time devoted to feeding were similar in all areas. Inter-species variations in the activity budgets of several species of primates were also examined. The percentage of time spent in social grooming by Japanese monkeys is exceptionally high compared to that recorded in other species.     

Post-conflict Behaviour in Long-tailed Macaques (Macaca fascicularis)

After being the victim of an agonistic conflict, long-tailed macaques increased the rate of tension-related activities such as scratching, body-shake and selfgrooming. This increase indicates that they experienced physiological changes preparing them to cope with the uncertainty of the post-conflict situation. Indeed, victims of agonistic conflict experienced a higher risk of renewed attacks. However, victims were also involved in social interactions characteristic of post-conflict situations, namely reconciliation and redirection. These two post-conflict social events reduced the rate of scratching, body-shake and selfgrooming. This suggests a faster termination of the stress response. Indeed, the two social events also decreased the likelihood of renewed attacks, one of the causes of the state of uncertainty. Reconciliation is more effective than redirection in this process probably because the restoration of the relationship with the former aggressor allows the victim to resume control of the situation.     

Socio-sexual factors of troop fission in wild Japanese monkeys (Macaca fuscata yakui) on Yakushima Island,Japan

The troop fissions which occurred in a wild population of Japanese monkeys (Macaca fuscata yakui) were observed from 1977 to 1979 on Yakushima Island. The fissions were initiated in the breeding season by non-troop males who established a consort relation with estrous females. In order to analyze the socio-sexual factors which accelerated the fissions, the male emigrations and immigrations before and after two successive fissions, and the copulation frequencies, competition among males and preferences of mating partners in both sexes in the 1977–78 breeding season after the first fission were examined. The results indicated that three factors (a large number of non-troop males, a shortage of troop males and the females' choice of mating partners) effectively influenced on the establishment of consort relationships between non-troop males and estrous females. It is suggested that these factors may exert different effects on the troop disorganization in relation to troop size. In small-sized troops, a large number of non-troop males and a shortage of troop males may lead to stronger competition between them, and the females' choice affected by prolonged intimate relations with the dominant TMs may reduce their priority of access to estrous females. This situation possibly stimulates fission or male emigration in small-sized troops under the natural conditions on Yakushima Island. In contrast, in large-sized troops under isolated conditions, a surplus rather than a shortage of troop males may contribute to troop disorganization, as most former studies have suggested. A higher socionomic sex ratio may decrease the mating activities of subordinate troop males and increase the competition among them. This situation possibly accelerates the fission of large-sized troops through prolonged interactions between females and subordinate or peripheral troop males. A lower ratio and the females' choice, however, raise the mating chances of subordinate troop males and may not promote the fission of large-sized troops under isolated conditions. This study was financed in part by a Grant-in-Aid for Special Project Research on Biological Aspects of Optimal Strategy and Social Structure from the Japan Ministry of Education, Science and Culture, and by the Cooperative Research Fund of the Primate Research Institute, Kyoto University.