Free-ranging Japanese Macaques Research Articles

Metacognition in wild Japanese macaques: cost and stakes influencing information-seeking behavior

Metacognition allows us to evaluate memories and knowledge, thus enabling us to distinguish between what we know and what we do not. Studies have shown that species other than humans may possess similar abilities. However, the number of species tested was limited. Testing ten free-ranging Japanese macaques (Macaca fuscata) on a task in which they had to find food hidden inside one of the four opaque tubes, we investigated whether these subjects would seek information when needed. The monkeys could look inside the tubes before selecting one. We varied three parameters: the baiting process, the cost that monkeys had to pay to look inside the tubes, and the reward at stake. We assessed whether and how these parameters would affect the monkeys’ tendency to look inside the tube before selecting one. When they were not shown which tube contained the reward, nine monkeys looked significantly more frequently in at least one condition. Half of them tended to reduce their looks when the cost was high, but only when they already knew the location of the reward. When a high-quality reward was at stake, four monkeys tended to look more inside the tubes, even though they already knew the reward’s location. Our results are consistent with those of rhesus macaques, suggesting that metacognitive-like abilities may be shared by Cercopithecidae, and that, at least some monkeys may be aware of their lack of knowledge.

Examining infantile facial features and their influence on caretaking behaviors in free-ranging Japanese macaques (Macaca fuscata).

Facial features of immature individuals play a pivotal role in eliciting caretaking behaviors in humans. It has been posited that non-human animals share particular infantile facial features with humans, which can elicit caregivers' attention and caretaking behaviors. Nevertheless, the empirical examination of this hypothesis is extremely limited. In this study, we investigated infantile facial features in Japanese macaques (Macaca fuscata), their developmental processes, and their correlation with caretaking and infant behaviors, based on 470 facial photographs from one free-ranging group. We measured the size of facial parts and evaluated these features using non-contact procedures with the animals. The results indicated that, although some partial species differences were observed, the infantile facial features in Japanese macaques were broadly consistent with those previously observed in humans and great apes. Furthermore, half of the infant subjects displayed non-linear developmental trajectories of infantile faces, similar to those suggested in humans. However, unlike previous studies in humans, infantile faces were not significantly associated with maternal or non-maternal caretaking behaviors, nor were their developmental changes correlated with infant behavioral development. These findings indicate that while many aspects of infantile facial features are shared among particular primates, humans may have evolved a uniquely elevated preference for selecting such features among the primate lineage.

No food left behind: foraging route choices among free-ranging Japanese macaques (Macaca fuscata) in a multi-destination array at the Awajishima Monkey Center, Japan.

Animals must make route choices every day when moving through their habitat while foraging. Choosing an optimal route can be cognitively costly, and primates and other animals have been shown to use simple heuristics, "rules of thumb", to make foraging route choices. We investigated the potential use of heuristics among foraging free-ranging Japanese monkeys (Macaca fuscata) during solitary foraging trials. We also investigated the potential influence of individual variables (age and sex) and social variables (presence in the central group, presence of potential inter- and intraspecific competitors), on the use of heuristics, route length and trial time. We used a multi-destination foraging experiment with 6 platforms in a (4m×8m) Z-array, completed by 29 Japanese macaques in 155 runs at the Awajishima Monkey Center in Japan. Our results showed that the macaques chose routes consistent with heuristics (e.g. nearest neighbour heuristic 19.4%, convex hull heuristic 4.5%) and selected optimal routes (shortest path in 23.9% of the trials). We also identified a potential new heuristic that was used most frequently, that we termed the "sweep heuristic" (27.1% of trials), which we interpreted as a strategy to deal with competitive foraging trade-offs - choosing routes to prioritize not leaving isolated food pieces behind. Age was significantly related to trial time; juvenile macaques were faster than adults and young adults, using speed to gain access to resources. Solitary trials with conspecifics present took significantly longerroutes. Our results suggest that contextual factors led to variation in Japanese macaque decision-making, and we suggest that the preferential use of a sweep heuristic may have been a response to high intragroup competition.

Mothers of disabled infants had higher cortisol levels in a free-ranging group of Japanese macaques (Macacafuscata).

Glucocorticoids (GCs) are hormones released in response to stressors and can provide insight into an organism's physiological well-being. Experiencing chronic challenges to homeostasis is associated with significant deviations from baseline fecal GCs (fGCs) in many species, providing a noninvasive biomarker for assessing stress. In the group of free-ranging Japanese macaques (Macaca fuscata) at the Awajishima Monkey Center in Japan, ~17% have congenital limb malformations. We collected 646 fecal samples from 27 females over three consecutive birth seasons (May-August)and analyzed them using enzyme immunoassay to extract fGCs. We explored the relationship between fGC levels and individual (physical impairment and reproductive status), social (dominance rank and availability of kin for social support), and ecological variables (exposure to potential predators, rainfall, and wild fruit availability). A disabled infant was associated significantly with higher fGC in the mother; however, physical impairment in adult females was not significantly related to fGC levels. Females with higher dominance rank had significantly lower fGC levels than lower ranking females. Other factors did not relate significantly to fGC. These results suggest that providing care that meets the support needs of disabled infants poses a physiological challenge for mothersand suggests that physically impaired adults are able to effectively compensate for their disabilities with behavioral plasticity. Once an individual with congenital limb malformations survives infancy through their mother's care, physical impairment does not appear to influence fGC values, while social variables like dominance rank significantly influenced cortisol values in free-ranging female Japanese macaques.

Measuring short-term changes in stress-associated salivary analytes in free-ranging Japanese macaques (Macaca fuscata).

Monitoring short-term changes of endocrine responses in non-human primates living in wild populations is a challenge. Saliva contains enzymes, steroids, and various analytes that can be broadly useful for helping us understand physiological responses to social and environmental sources of stress as well as other compromises to an individual's health homeostasis. Salivary alpha-amylase and salivary cortisol are known to respond rapidly to stress, which can allow us to use these analytes to monitor stress on a time scale of minutes. We developed a non-invasive methodology for the collection of saliva and verified its applicability by conducting short-term interval sampling of focal individuals under varying social conditions in a group of semi-provisioned free-ranging Japanese macaques (Macaca fuscata) living endemically on the island of Koshima, Miyazaki prefecture, Japan. Monkeys were habituated to sampling by using ingestive attractants applied to cotton ropes. Their receptivity to chewing on the saliva sampling material provided and chewing time was recorded ad libitum during the initial habituation period of the troop to the sampling procedure. Focal animal behavior observations were conducted in conjunction with saliva sampling. Salivary analytes associated with stress, alpha-amylase and cortisol, were measured via enzyme immunoassay. Short-term changes in salivary alpha-amylase and salivary cortisol were examined in relation to short-term changes in social behavior, in particular aggression or grooming. We tested flow-rate effects in both analytes and found strong correlations between original sample results and their respective flow-rate transformed equivalents. Additionally, temperature effects on samples were tested and both analytes showed nearly the same values when stored at -20, 4, and 30°C conditions for 6h; important information expected to facilitate future sampling in field conditions where freezer storage is uncertain. Our study shows that saliva can be repeatedly sampled non-invasively to investigate short-term changes in stress-associated markers in free-ranging Japanese macaques.

Effects of Vegetation Structure on the Habitat Utilization of Free-Ranging Japanese Macaques (Macaca fuscata) in a Coniferous Plantation Area

Abstract. We studied home range use of crop-raiding Japanese macaques (Macaca fuscata) in Shiga Prefecture, central Japan, to address the effects of vegetation structure, specifically forest edge, on their habitat utilization. We compared the home range use of a troop inhabiting a rural area surrounded by a coniferous plantation with that of a troop inhabiting deciduous/coniferous forest mixed area. We then conducted a vegetation survey to evaluate the forest structure and food availability within their home ranges. Both troops frequently used the coniferous plantations and preferred them. The rural troop also preferred deciduous forest. Both troops preferred bamboo forest and avoided other vegetation types. The vegetation survey found that food availability in deciduous forest was the greatest. Both troops frequently used the forest edges, likely due to higher food availability as well as its role as a refuge. We found higher similarity in composition of food plant species between coniferous plantation and the deciduous forest, which implied that the former can be converted to the latter through thinning. We suggest an idea on the habitat management through thinning of the coniferous plantation to improve the present situation of the human-macaque conflict.

Japanese Macaques\u2019 (Macaca fuscata) sensitivity to human gaze and visual perspective in contexts of threat, cooperation, and competition

Gaze sensitivity allows us to interpret the visual perspective of others, inferring their intentions and attentional states. In order to clarify the evolutionary history of this ability, we assessed the response of free-ranging Japanese macaques (Macaca fuscata) to human gaze in three contexts: threat (Experiment 1), cooperation (Experiment 2), and competition (Experiment 3). Subjects interpreted the direct gaze of an approaching human as a sign of threat, showing a greater flight initiation distance and more threats towards the human in this condition than when the human gazed in another direction. Subjects also adapted their behavior to the attentional cues of a human who gave them food, by for example moving into his visual field. However, the macaques did not seem to take the visual perspective of a human competing with them over food, as they failed to first retrieve the food that was not visible to the human (i.e., located behind an opaque barrier). Our results support the idea that Japanese macaques can respond to a human’s gaze flexibly depending on the context. Moreover, they highlight the importance of studying animal behavior across different species and contexts to better understand the selective pressures that might have led to its evolution.

Social grooming efficiency and techniques are influenced by manual impairment in free-ranging Japanese macaques (Macaca fuscata).

Animals born with physical impairments may particularly require behavioural flexibility and innovation to survive and carry out social activities, such as grooming. Studies on free-ranging Japanese macaques on Awaji Island, Japan, have shown that individuals with congenital limb malformations exhibited compensatory behaviours while grooming, such as increased mouth and elbow use for removing ectoparasites. The aim of this study is to explore disabled and nondisabled grooming techniques to determine whether and to what extent disabled monkeys develop novel grooming techniques, and if there is disability-associated variation in grooming efficiency. We hypothesized that modified grooming techniques used by disabled monkeys fulfilled the social and relaxing functions of grooming, however, that grooming by manually impaired individuals may still carry a hygienic cost to the recipients. Grooming behavioural data were collected by video in 2007 on 27 adult females (11 with CLMs). With a detailed grooming-related ethogram, we transcribed 216 2-minute continuous grooming video samples. We analyzed the data using generalized linear mixed effects models in R. We found that monkeys with manual impairment were less efficient groomers, as measured by removal and movement efficiency during grooming. However, there were no significant differences associated with the number of grooming movements per sample among the focal animals. Additionally, with a behavioural sequential analysis, we isolated 8 distinct grooming techniques and 3 novel disability-specific movements. Our results indicate that innovation and modification of movement types does not entirely compensate for manual disability, and that manual impairment carries a cost to the hygienic function of grooming. However, for the grooming recipient, the experience of being groomed by a disabled or nondisabled groomer is likely similar, and through movement compensation, disabled monkeys are able to engage in the social aspect of grooming without incurring any disability-associated costs.

Social consequences of disability in a nonhuman primate

Debates about the likelihood of conspecific care for disabled individuals in ancestral hominins rely on evidence from extant primates, yet little is known about social treatment (positive, neutral or negative) of physically disabled individuals in nonhuman primates. A group of free-ranging Japanese macaques (Macaca fuscata) at the Awajishima Monkey Center (AMC) in Japan presents a unique opportunity to investigate the relationships between physical impairment and social behavior, in the context of congenital limb malformation in adult nonhuman primates. We collected behavioral data on 23 focal animals, taking 30-minute continuous time samples on disabled and nondisabled adult female Japanese macaques during three consecutive birth seasons (May–August 2005, 2006, and 2007). Disabled females were less social overall compared with nondisabled controls, a pattern that was evident from a variety of measures. Disabled females rested significantly more and socialized significantly less compared with controls, had fewer adult female affiliates, fewer adult female grooming partners, and spent less time engaged in grooming with adult females. Some measures suggested that the social differences were the result of behavioral flexibility on the part of disabled females compensating for their disabilities with lower levels of social involvement and more rest. Disabled females were as successful at groom solicitations as were nondisabled females and the ratio of disabled and nondisabled affiliates was similar among focal animals; there was no strong preference related to the disability status of affiliates. Disabled females were also bitten and chased less frequently. Overall, there was little evidence either for conspecific care or for social selection against disability. In general, there was a socially neutral response to disability, and while neutral social context allows for the possibility of care behaviors, our findings emphasize the self-reliant abilities of these disabled primates and suggest caution when inferring conspecific care for even very disabled ancestral humans.

Redirected aggression reduces the cost for victims in semi-provisioned free-ranging Japanese macaques (Macaca fuscata fuscata)

In many social species, the victim often attacks an uninvolved third individual soon after a conflict. This behaviour is called ‘redirected aggression’ or ‘redirection’, and its role(s) remain(s) controversial. We observed semi-provisioned free-ranging Japanese macaques at Iwatayama Monkey Park in Arashiyama, Kyoto, Japan, to test three hypotheses concerning the function of redirected aggression: Japanese macaques perform redirection to (1) indirectly retaliate against the aggressor, (2) reduce post-conflict stress, or (3) reduce post-conflict uncertainty. When we observed aggressive interactions, we recorded the behaviour of victims during the subsequent 10 min. Redirection occurred more frequently when the rank of the victim of the initial conflict was high, when the victim was an older monkey, and when conflicts occurred among kin. The results largely supported hypothesis 3. Victims received renewed aggression not only from the initial aggressor but also from bystanders more frequently within 1 min after the initial conflict than in the subsequent 9 min. Victims who performed redirection received less aggression from bystanders. Victims might have been able to avoid renewed aggression because they could change their state from victim to aggressor by performing redirection. This effect of redirection did not differ with the victim’s rank. However, the lower the victim’s rank, the higher the risk that they would receive retaliation from the target of the redirected aggression or the latter’s kin. Thus, redirection caused the same magnitude of benefit and a different magnitude of risk according to the victim’s rank. The victim may need to judge his/her own situation when making the decision as to whether to perform redirection.

The effect of solicitations on grooming exchanges among female Japanese macaques at Katsuyama

In group-living primates, individuals often exchange grooming with not only kin but also non-kin. We investigated the effect of soliciting behaviors on grooming exchanges in a free-ranging Japanese macaque (Macaca fuscata) group at Katsuyama. In this study, we used a focal animal sampling method, targeting 14 females. Data were collected for 15.75 ± 2.67 (mean ± SD) hours per focal female. We classified female-female pairs into three pair types: kin pairs, affiliated non-kin pairs, and unaffiliated non-kin pairs. Females received grooming more frequently when they solicited after grooming their partners than when they did not solicit in all pair types. In addition, females received grooming less frequently when they did not groom their unaffiliated non-kin partners before soliciting; prior grooming was not needed to receive grooming from kin or affiliated non-kin partners. The degree of grooming reciprocity did not differ according to the frequency with which females in kin or affiliated non-kin pairs solicited after grooming. On the other hand, grooming reciprocity between unaffiliated non-kin females was more balanced when they solicited frequently after grooming, as compared with when they did not. In conclusion, our study suggests that soliciting behaviors promote grooming exchanges in female Japanese macaques.

Food-snatching behavior of free-ranging Japanese macaques observed on Shodoshima Island: a preliminary report

We investigated the characteristics of a particular food-snatching behavior in which one individual forced another's mouth open and grabbed the food, as performed by free-ranging Japanese macaques (Macaca fuscata) in Choshikei Monkey Park on Shodoshima Island, western Japan. We conducted a survey in late June 2012 and observed one of two monkey troops, comprising 214 monkeys. We recorded the age classes and sexes of the individuals who performed the snatching behavior and were snatched from, and examined the effects of provisioned food distribution and quantity on the frequency of snatching trials and success. During the survey, we recorded 747 snatching trials, of which 609 were successful, all of which were performed by seven individuals: one adult male and six adult females. The snatching behavior occurred only during provisioning. The target animals were primarily juveniles (650 trials, 578 successful), while cases in which food was snatched from adult females (93 trials, 30 successful) and subadult females (4 trials, 1 success) were less frequent. Among the juveniles, small juveniles had food snatched more frequently than large juveniles. The higher frequency of snatching trials against juveniles was likely due to their subordinate nature. Neither the distribution nor quantity of the provisioned foods had significant effects on the number of snatching trials and successes, while the time elapsed after provisioning had significant negative effects, attributed to a decrease in the number of wheat grains left within the mouth pouch of the potential target animals.

Japanese Macaques (Macaca fuscata) as Natural Reservoir of Bartonella quintana.

Bartonella quintana bacteremia was detected in 6 (13.3%) of 45 wild-caught Japanese macaques (Macaca fuscata). Multilocus sequence typing of the isolates revealed that Japanese macaques were infected with a new and specific B. quintana sequence type. Free-ranging Japanese macaques thus represent another natural reservoir of B. quintana.

Maternal investment in sons and daughters in provisioned, free-ranging Japanese macaques (<i>Macaca fuscata</i>)

It has been suggested that the physical condition of a mother may affect her pattern of investment in her sons or daughters. In addition, when competition over local resources becomes intense, severe aggression among the philopatric sex leads to a higher mortality of the sex and a biased birth sex ratio toward the opposite sex in the low rank. Parental sex-biased investment has been studied in many animal species to test these hypotheses, but the results have been highly inconsistent. We examined maternal sex-biased investment in relation to dominance rank using data on infant growth, infant mortality, birth sex ratio, and delay of subsequent reproduction by rearing current offspring from a provisioned, free-ranging Japanese macaque (Macaca fuscata) troop at Takasakiyama, Japan. The results showed that there was no sex difference in infant body mass among offspring of high- and low-ranking females. Use of the logistic regression model to analyze infant mortality with several independent variables failed to show a statistically significant sex bias. Birth sex ratio did not differ significantly between high- and low-ranking females. Among high-ranking females, there was no significant difference in delivery rate in the next year between those that reared a son and those that reared a daughter. For low-ranking females, however, the delivery rate after rearing daughters was markedly lower than that after rearing sons. Thus, there was no evidence of statistically significant maternal male-biased investment. For low-ranking females, we found a delay in subsequent reproduction for mothers after rearing daughters and no sex difference in offspring mortality. These results suggest that the females increased their offspring’s chances of survival, irrespective of sex, by postponing their subsequent delivery.

A photogrammetric method to evaluate nutritional status without capture in habituated free-ranging Japanese macaques (Macaca fuscata): a pilot study

The quantification of nutritional status (e.g., total body fat) of animals is difficult, because the linear dimension (body length) required for the calculation of proxy parameters, such as the physique or body mass indices, cannot be measured without capture. One solution is photogrammetry of body length, provided the following two criteria are met: (1) the camera axes and subject are oriented vertically, and (2) anatomical landmarks are easily identified with low measurement error. By modifying Mori's (Primates 20:371-397, 1979) approach, we devised an accurate photogrammetric method that uses a horizontal bar with an attached ruler for the monkey to traverse, and the anatomical landmarks of the eye and upper border of the ischial callosity to measure body length. We tested the applicability of this method on 11 adult female, habituated, free-ranging Japanese macaques (Macaca fuscata). Somatometric body length (crown-rump length and anterior trunk length) was statistically compared with the body length obtained using photogrammetry. The significant correlation of the photogrammetric body length with each somatometric measurement verified that the former could be employed to calculate various indices that are used to characterize fat mass (nutritional status) in Japanese macaques. The advantages and disadvantages of photogrammetry are also discussed.

Changes in Demographic Parameters of Macaca fuscata at Takasakiyama in Relation to Decrease of Provisioned Foods

Though researchers have studied population dynamics extensively in many free-ranging primate populations, information on the relationship between food abundance and demographic parameters based on long-term data is sparse. We examined changes in demographic parameters in relation to decreased provisioning of foods based on data gathered for >50 yr in a provisioned, free-ranging Japanese macaque (Macaca fuscata) population at Takasakiyama, Oita Prefecture, in the southern region of Japan. At Takasakiyama, population size increased linearly because of heavy provisioning in the 1950s and 1960s. The provisioning of food to macaques decreased from 1965. We examined changes in the physique index of full adult females, primiparous age, birth percentage, infant mortality rate, population density, and annual population growth rate relative to the decrease of provisioned foods between the 1970s and 1990s. As a result of the drastic decrease in the amount of foods provisioned, the physique index of full adult females decreased, primiparous age increased, birth percentage decreased, and infant mortality rate increased, such that annual population growth rate diminished substantially. Ours is the first study to demonstrate quantitatively the relationship between provisioned food abundance and demographic parameters based on long-term data.

Age‐dependent patterns of intensive observation on elders by free‐ranging juvenile Japanese macaques (Macaca fuscata yakui) within foraging context on Yakushima

Early learning about edible food in the environment is a critical survival task for young nonhuman primates. Social learning and social facilitation are often cited to explain how youngsters learn to select and find their food. In this framework, we observed eight mother-youngster pairs of free-ranging Japanese macaques divided into two sets according to the age of the young (infants aged between 7 and 12 months and juveniles aged between 1.5 and 2 years) during three winter months. We systematically investigated the intensive observation directed by the youngsters toward elders by recording the target's identity (e.g. mother, subadult), the items manipulated by the elder and those items closely observed by the youngster, along with the behavior of the youngster preceding and immediately following an intensive observation period. The diet of the mothers and juveniles was estimated from time records of each feeding occurrence for each food item (identified to species level) and from the quantity of fresh matter ingested. The results show that intensive observation by both infants and juveniles were directed toward those elders engaged in plant and invertebrate foraging. Such behavior was age-dependent, being more frequent in infants than in juveniles. The majority of the intensive observations were directed toward the mother. Intensive observations also shaped a change in the behavior of infants by significantly stimulating the investigation of food items and locations otherwise not investigated by juveniles. Moreover, infants showed a particular interest in rare food items and especially invertebrates. Age differences between the two sets of young and their interest in rare foods are discussed with reference to the occurrence of intensive observation within the framework of kin relationships, social organization, and social transmission of information about food type and food location and its survival values.

Courtship behaviour in Japanese macaques during heterosexual and homosexual consortships

Female Japanese macaques (Macaca fuscata) in the Arashiyama population near Kyoto, Japan, are unusual, in that they exhibit what many would consider to be male-typical sexual characteristics. Specifically, they mount other females within the context of temporary, but exclusive, sexual relationships (i.e., homosexual consortships) and they sometimes exhibit a preference for female sexual partners, even when given the choice of a sexually motivated male alternative. In this study, we examined whether female Japanese macaques also exhibited male-typical patterns of courtship behaviour during homosexual consortships. Data were collected on courtship behaviour during heterosexual and homosexual consortships in free-ranging Japanese macaques from the Arashiyama (Japan) population. We analyzed the occurrence of 12 different courtship behaviours during 3374 heterosexual inter-mount intervals and 1412 homosexual inter-mount intervals. Sex differences between heterosexually consorting males and females existed for only two of the 12 courtship behaviours we investigated: inclined-back presentations and sexual vocalizations. Dominant and subordinate homosexually consorting females were sex-typical in their expression of inclined-back presentations and sexual vocalizations. Consequently, facultative same-sex sexual partner preference, mounting and consortships do not co-occur with male-typical patterns of courtship behaviour in female Japanese macaques.

The effect of male tenure and female mate choice on paternity in free‐ranging Japanese macaques

In this study, the paternity of all the infants born in 2002 and 2003 in a free-ranging Japanese macaque (Macaca fuscata) group at Arashiyama in Kyoto, Japan, was analyzed in relation to males' age, dominance rank, and tenure and females' mate choice. The fathers of 20 out of 23 infants were determined by DNA analyses. Central adult (high-ranking) males sired two infants, whereas peripheral adult (low-ranking) males sired 14 infants. Young males sired only one infant. Among adult males, tenure was the most dominant factor that negatively affected male reproductive success. The mating behavior of females who gave birth was also analyzed. The number of male copulations in the peri-fertilization period was positively correlated with the number of infants that they sired. Females copulated with central males with a long tenure only when fertilization was unlikely or impossible. The females probably avoided insemination by males with a long tenure and selected males with a shorter tenure as their mating partners during the ovulation period.

Nulliparous pregnant females tried to suckle yearlings just before their first parturition but non-kin yearlings did not hold the nipples in their mouths among free-ranging Japanese macaques

Nulliparous pregnant females tried to suckle yearlings just before their first parturition but non-kin yearlings did not hold the nipples in their mouths among free-ranging Japanese macaques