Play face in Japanese macaques reflects the sender's play motivation.

Animals often initiate social interactions by exchanging signals. Especially when initiating amicable interactions, signaling one's friendly stance toward others in advance may be important to avoid being misunderstood as having hostile intentions. We used data on dyadic play fighting in a group of Japanese macaques, Macaca fuscata, to examine the function of "play face" at the opening of a play session. We found no support for the previously proposed hypothesis that play face expression is likelier before entering risky situations (e.g., before gaining an undue advantage over the partner) to avoid being misunderstood. The results showed that play face expression was likelier in male juveniles before initiating play with other males than in females before initiating play with males or other females and that juveniles were likelier to express play face before initiating play with others closer in age. As male Japanese macaques play more frequently than females, and juveniles prefer to play with individuals closer in age, play face expression before play initiation may reflect the individual's motivation for subsequent play interactions. This interpretation is supported by our observation that play bouts lasted longer when initiated with bidirectional play face by both participants than when initiated without play face. We also argued that since there was no tendency that play face was likelier to be expressed toward individuals with low play propensity (e.g., females) or infrequent partners to play with (e.g., individuals more distant in age), Japanese macaques may not tactically deploy this signal to recruit reluctant partners.

Male-male social bonds predict tolerance but not coalition formation in wild Japanese macaques.

Social bonds have been construed as differentiated and enduring affiliative relationships. Strong bonds will improve fitness through interchanging with coalition formation or tolerance over resources. Social bonds have been found in a variety of taxa and predict the formation of coalitions even amongst males. However, in species exhibiting steeply linear dominance hierarchies, coalitions are hypothesized to be suppressed due to severe competition amongst males, and thus strong bonds may manifest in other forms of behavior, notably social tolerance. The aim of this study was to examine the effects of male-male social bonds and dominance on agonistic supports and aggressive interaction in one of the most despotic primate species, Japanese macaques. I conducted focal samples on male individuals, recording their grooming, proximity to other members, agonistic supports and membership, and aggressive interactions over a 2-year observation period. Male macaques formed differentiated affiliative relationships across dyads and those relationships showed positive relations between the non-mating and the mating seasons. Steep dominance hierarchies were found amongst males. The occurrence of agonistic supports was not explained by the strength of social bonds but by the dominance of the participants, whereas strong bonds predicted less frequent aggressive interaction. These results are in line with the hypothesis that dominance is a major mechanism underlying coalition formation amongst males. Unlike more egalitarian species, strong bonds do not predict coalition formation but rather tolerance in despotic species. These results suggest male-male social bonds will bring alternative consequences according to dominance structures.

Fake twins? Two cases of intensive allomaternal care by female Japanese macaques before and after their own partum.

Allomaternal care is widely observed among primate species. Although diverse allomothering behavioral repertoire and types of caretakers have been reported, it remains unclear what social or physiological conditions may trigger such care in each individual. For a better understanding of mechanisms that give rise to allomaternal care in primates, more observational reports are needed with information on social or physiological conditions of caretakers. Here I report two cases of intensive allomaternal care in two different populations of Japanese macaques (Macaca fuscata). The two adult females provided intensive allomaternal care including carrying, grooming, and nursing towards others' infants. Their allomaternal care began 20 or 29 days prior to their own partum and lasted for 84 days at the most. This study firstly showed that nursing forms part of the allomothering behavioral repertoire, and allomaternal caretakers can be individuals that are prior to the time of their own partum in Japanese macaques. Their intensive allomaternal care may stem from their good nutritional conditions, increased concentrations of several hormones, or disappearance of the newborn infants' biological mothers.

Food Cleaning by Japanese Macaques: Innate, Innovative or Cultural?

Japanese macaques (Macaca fuscata) display a number of cultural behaviours including food washing, stone handling and certain grooming techniques. These are deemed cultural behaviours because it is presumed that they are socially learned and, importantly, that social learning is essential for their emergence. Recently, however, research has revealed that culturally naïve primates can re-innovate presumed cultural behaviours. These behaviours are said to fall within that species' "zone of latent solutions" (ZLS). A notable cultural behaviour of Japanese macaques is food washing, first reported by Japanese researchers studying wild Japanese macaques in the 1950s. To test whether culturally naïve Japanese macaques would spontaneously wash food and also, therefore, whether food-washing behaviour is within their ZLS, we presented 12 zoo-housed macaques with sweet potato covered in sand near a pool in their exhibit. Over 11 days we recorded the macaques' behaviour. While 11 of the 12 macaques ate the potato pieces, none washed them. However, 4 macaques cleaned their food, brushing off the sand using their hand or rubbing the potato against their body or another food item, using three distinct techniques. We found no change over time in the rate at which monkeys cleaned or consumed potato, but there was a significant positive correlation between the number of potato pieces a monkey ate and the number of cleaning behaviours performed. We conclude that, minimally, food-cleaning behaviour is within macaques' ZLS.

Spatial position-associated mating strategies employed by male Japanese macaques (Macaca fuscata yakui) in Yakushima.

In bisexual groups, dominant males occupy the central part of the group, which is advantageous because it is reproductively beneficial. However, high-ranking males do not necessarily monopolize reproductive success, which indicates that low-ranking males increase their reproductive success through alternative mating strategies. To reveal the effectiveness and cost of these strategies employed by group males, it is necessary to clarify the spatial configuration of males and their group, and show how males combine strategies in different situations. This study demonstrates the spatial configuration of male Japanese macaques (Macaca fuscata yakui) and their group when males adopt three mating strategies: mate guarding, sneak mating, and cross-boundary mating (mating with females of another group). High-ranking males tended to perform mate guarding, but they also mated with females in other groups when there were few sexually active females in their group. Low-ranking males performed sneak mating; they remained in the central part of the group to monitor sexually active females and moved toward the periphery for copulation but never completely left the group. In addition, males individually ventured outside the group's ranging area and succeeded in mating with females of other groups. The cross-boundary mating strategy has the advantage of increasing the number of potential mating partners, which is not present in the other two strategies. However, because of considerable costs and low contribution to mating frequency, this strategy is complementary and is employed when the expectation of mating success in their group is low.

Changes in social behavior and fecal glucocorticoids in a Japanese macaque (Macaca fuscata) carrying her dead infant.

Maternal care towards dead infants has been observed in many wild and captive mammals, but the consequences of this behavior for social interactions and the physiological status of the mother remain elusive. Here, we report changes in rates of aggression and grooming time, and fecal glucocorticoid (fGC) levels in a free-ranging female Japanese macaque (Macaca fuscata) that carried her dead infant for 20 days. Our observations revealed that when carrying the dead infant, the mother showed increased rates of grimace, avoidance, and human-directed behaviors, along with reduced allogrooming time and fleeing from other individuals. Postpartum fGC levels were comparable to those of non-pregnant and non-lactating females, suggesting that the energetic costs and stress of carrying a dead infant are low. Our findings indicate that carrying a dead neonate can have three profound consequences on the mother: increased fearful behavior, decreased allogrooming, and a rapid return to baseline fGC levels. We hypothesize that dead infant-carrying may have evolved as a strategy to mitigate stress from infant loss. These findings have implications for our understanding of grief in nonhuman primates and can impact management protocols surrounding deaths in captive social groups.

Face-to-face opening phase in Japanese macaques' social play enhances and sustains participants' engagement in subsequent play interaction.

A face-to-face "opening phase" in human interaction serves as a platform for the interactants to initiate and manage their interaction collaboratively. This study investigated whether, as is the case in humans, a face-to-face opening phase in animal interaction serves to manage a subsequent interaction and establish interactants' engagement. We compared the dyadic play fighting of Japanese macaques (Macaca fuscata) initiated with and without a face-to-face opening phase. Our observations showed that play sessions with a face-to-face opening phase lasted longer than did sessions without one. Furthermore, our results indicate that facing toward playmates was a sign of interactants' engagement. In sessions with a face-to-face opening phase, both players were likely to gain an advantage over their playmates, whereas in sessions without such an opening phase, only an individual who unidirectionally faced toward another individual who looked away when play began was likely to maintain an advantage over a long period. Our findings demonstrate that a face-to-face opening phase has a socio-cognitive function to establish and sustain interactants' social engagement during subsequent interaction not only in humans but also in Japanese macaques.

High but not low tolerance populations of Japanese macaques solve a novel cooperative task.

Currently, it has been revealed that high levels of tolerance facilitate the occurrence of cooperative behavior in animals. This predicts that Japanese macaques (Macaca fuscata) would fail to solve cooperative food-retrieval tasks because of their low level of social tolerance. However, Japanese macaques exhibit regional differences in their levels of tolerance. In this study, we showed how inter-group difference in social tolerance could affect cooperation, by presenting a well-established cooperative rope-pulling task with two free-ranging groups of Japanese macaques that exhibit different levels of social tolerance. We used the task that required two macaques to pull both ends of a single rope simultaneously to obtain food rewards. We found that some macaques from the more tolerant group successfully solved the task, and one of them learned to wait for a partner when a partner was absent. In contrast, however, those of the less tolerant group almost never succeeded in the task. These results indicate that Japanese macaques possess the abilities to cooperate with conspecifics, but such abilities may be constrained in their typically despotic society.