Behavioral responses of free-ranging Japanese macaques (Macaca fuscata) to sudden loud noises.

We opportunistically observed 31 cases of responses to sudden loud noises mainly caused by falling rocks and trees in a free-ranging, provisioned group of Japanese macaques, Macaca fuscata, at Katsuyama, Japan, and analyzed 27 cases for which we successfully recorded their responses. In 88% of the 24 cases in which the highest- or second-highest ranking adult male probably heard the noise, one or both of them vocalized aggressively in response. Other males tended to vocalize when they were far away from the two highest-ranking males (in 5 of 7 cases in which they vocalized). Adult females vocalized in only 8% of cases, even when they fled from the noise source. These findings suggest that, unlike tree-shaking and female-directed aggression - both performed often in the mating season and accompanied by vocalizations in both high- and low-ranking males of Japanese macaques - vocalizing in response to sudden loud noises is usually limited to one or two high-ranking males in the vicinity. This vocal response could be a way for the males to advertise their social status; it may also serve to calm group members scared by the noise, preventing them from fleeing in panic and dispersing widely. Our observations also suggest that males may monitor which other males remain nearby, and that whereas females may scream in response to socially induced fear, they are least likely to do so in response to fear arising from non-social contexts.

Daytime spatial relationships in a family group of black rhinoceros Diceros bicornis at the Hiroshima City Asa Zoological Park, Japan.

Although black rhinoceros Diceros bicornis are mostly solitary in the wild, the Hiroshima City Asa Zoological Park (Asa Zoo) has kept a family group together during the daytime, with good reproductive performance over five decades. Management procedures at the zoo include temporary single housing of the mother before and after giving birth, which facilitates maintenance of a compatible family group. We recorded intra-group spatial relationships for 4 years and 4 months, during which time an adult female reared two consecutive calves. During daytime she remained in an enclosure with her new calf, one or two older offspring, and an adult male, the sire of all her offspring. Proximity (within two adult body-lengths) scores between the mother and her two calves were especially high during the first year after birth, and only slightly lower for her older offspring. The adult male had the lowest proximity scores. The spatial relationships were visualized by applying multidimensional scaling (MDS) to the proximity scores. Mother and calves were plotted close to each other, with older offspring slightly farther apart on the two-dimensional MDS representation; the adult male was more distant from the other group members. These findings indicate clear follower-type characteristics in the mother-calf pair and also older immature offspring, albeit to a lesser degree. Although black rhinoceros are generally solitary in the wild, our results duplicate observations of some wild black rhinoceros groups containing an adult female, her calf, and an older immature, with adult males being largely solitary.

Behavioral responses of solicitors after failure to receive grooming in Macaca fuscata.

Grooming is one of the most common cooperative behaviors among several animal species. However, the tactics used to cope with uncooperative partners in grooming interactions remain unclear. Japanese macaques (Macaca fuscata) solicit grooming from partners through postural behaviors, but may not necessarily receive grooming. This study investigated the behavior of female Japanese macaques after they solicited but did not receive grooming. We predicted that unsuccessful solicitors would engage in grooming interactions with uncooperative partners if they were affiliated. If they were not affiliated, the solicitors would not do so and may seek grooming interactions with other grooming partners. We used a focal-animal sampling method, targeting 17 females at Katsuyama, Okayama Prefecture, Japan. We recognized affiliative relationships by measuring close spatial association. After unsuccessful solicitation, females tended to scratch themselves, suggesting that solicitors may experience anxiety or distress when they do not receive grooming. They also tended to be proximate with affiliated partners after solicitation, regardless of whether the solicitors received grooming from their partners. In contrast, when solicitors failed to receive grooming from unaffiliated partners, their subsequent proximity was lower than when they were groomed. Moreover, unsuccessful solicitors were likely to engage in grooming interactions with affiliated partners who were uncooperative (receivers of unsuccessful solicitations). However, they were less likely to engage in grooming interactions with unaffiliated partners and instead engaged in grooming interactions with other nearby partners. These findings indicate that female Japanese macaques decide whether to engage in grooming interactions with uncooperative partners who have not groomed solicitors based on affiliative relationships and the availability of other grooming partners. It is probable that, when the cost of searching for a grooming partner is low, female Japanese macaques are likely to switch partners, potentially leading to an increase in the benefits obtained from grooming interactions.

Factors affecting captive female giraffe stress response: Male presence, small enclosure, and low temperature.

To improve animal welfare based on suitable social housing conditions, it is important to understand the factors that trigger high-stress responses. Wild giraffes live in a fission-fusion society and males and females are rarely in the same herd for a long period. The captive condition of belonging to a herd with the same individuals for months or years is uncommon in nature. To understand the effect of male presence on female stress levels, fecal glucocorticoid metabolite (fGCM) levels and social interactions in two captive female giraffes were investigated. Additionally, the effect of enclosure size and temperature on fGCM level and social interactions were examined. The results showed no significant difference in the fGCM levels of females based on male presence. The frequency of agonistic behavior by the dominant female toward the subordinate female was significantly increased when a male was present. The subordinate female was significantly less likely to approach the dominant female and showed decreased affiliative and agonistic interactions toward the dominant female when a male was present. The frequencies of agonistic interactions between females were higher in the small enclosure regardless of male presence. Low temperature triggered higher fGCM levels and increased agonistic interaction in an aged female. The findings of this study suggest that these multiple factors should be considered individually to promote the welfare of captive giraffes.

Daytime mother-calf relationships in reticulated giraffes (Giraffa cameloparadalis reticulate) at the Kyoto City Zoo.

The present study quantitatively assesses the relationships between a reticulated giraffe mother and her first- and second-born calves during the first 22 months of the older calf's and the first 12 months of the younger calf's life at the Kyoto City Zoo, Japan. The mother permitted her calves to suckle at over 70% of their suckling attempts in the first month after their births, and the calves ceased suckling spontaneously in 65 to 70% of the suckling bouts. From the second month on, she showed a clear tendency to reject the calves' suckling attempts and terminated almost all of their suckling bouts, which resulted in approximately 60 sec or less of suckling duration per bout. The frequency of proximity between the mother and her calves remained at 20 to 30% throughout the first year, with no apparent developmental changes being evident. The mother was mainly responsible for terminating proximity by walking away from her calves throughout their first year after birth, while both calves were mainly responsible for attempting proximity by approaching their mother after reaching 2 months of age. Our study also showed that the giraffe mother became pregnant again while nursing her calves and ceased lactation (i.e., weaned the calves) before the fetus's growth started accelerating.

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.

Twelve-year proximity relationships in a captive group of western lowland gorillas (Gorilla gorilla gorilla) at the San Diego Wild Animal Park, California, USA.

Proximity data were collected in a captive breeding group of gorillas (Gorilla gorilla gorilla) at the San Diego Wild Animal Park (currently called the San Diego Zoo Safari Park) twice a year (spring and fall periods) for over 12 years, by using a convenient method in which individuals less than 5 m from each animal in the group were recorded by scan sampling, approximately once per hour. Immature females from infancy to young adulthood maintained relatively frequent proximity to both their mothers and the silverback male and spent little time alone (no animals within 10 m), with relatively large individual differences. On the other hand, immature males decreased the time spent near their mothers and the silverback male and increased the time spent alone with increasing age. Therefore, sex differences in proximity to mothers and the silverback male became apparent after late juvenility. Some adult females maintained increased frequency of proximity to the silverback male than that by other females over the 12-year period, indicating the presence of long-term, stable proximity relationships between the silverback male and the adult females. Such long-term, stable proximity relationships were also observed among adult females. Some association patterns reported in wild gorillas, such as frequent proximity between adult females with dependent offspring and the silverback male and close relationships between related females, were not observed in the present study. The idiosyncratic or individual factors influencing some association patterns were easily reflected in captive situations.

Disability, compensatory behavior, and innovation in free-ranging adult female Japanese macaques (Macaca fuscata).

Little is known about consequences of disability in nonhuman primates, yet individuals with disabilities can reveal much about behavioral flexibility, innovation, and the capabilities of a species. The Macaca fuscata population surrounding the Awajishima Monkey Center has experienced high rates of congenital limb malformation for at least 40 years, creating a unique opportunity to examine consequences of physical impairment in situ, in a relatively large sample of free-ranging adult monkeys. Here we present behavioral data on 11 disabled adult females and 12 nondisabled controls from 279 hours of randomly ordered 30-minute focal animal follows collected during May-August in 2005, 2006, and 2007. We quantified numerous statistically significant disability-related behavioral differences among females. Disabled females spent less time begging for peanuts from tourists, and employed a behavioral variant of such peanut begging; they had a lower frequency of hand use in grooming and compensated with increased direct use of the mouth or a two-arm pinch technique; and they had a higher frequency of self-scratching, and more use of feet in self-scratching. Self-scratching against substrates was almost exclusively a disability associated behavior. Two females used habitual bipedalism. These differences not withstanding, disabled females behaved similarly to controls in many respects: overall reliance on provisioned and wild foods, time spent feeding, and feeding efficiency did not differ among females, and there was no time difference in behavior performed arboreally or terrestrially. Disabled adult females were able to compensate behaviorally to perform social and life-sustaining activities, modifying existing behaviors to suit their individual physical situations and, occasionally, inventing new ways of doing things.

Professor Masao Kawai, a pioneer and leading scholar in primatology and writer of animal stories for children.

This Editorial is dedicated to Professor Masao Kawai (Fig. 1), who passed away on May 14th, 2021. He served as the sixth Editor-in-Chief of Primates for 15 years (1981-1995). The following is a collection of memories from 20 scholars. Fig. 1 Professor Masao Kawai, a pioneer and leading scholar in primatology (photo taken in January 2020; Courtesy of Ryoko Kawai).

Male care in a free-ranging group of Japanese macaques (Macaca fuscata).

Among the Macaca species, adult male Japanese macaques are the least likely to perform male care (i.e., affiliative interactions between adult males and immatures, including holding, carrying, and grooming); however, they perform male care for infants, albeit infrequently. We examined 17 cases of male care observed for the first time when the immature was younger than 1 year of age. Eleven of the 31 adult males who remained as central males during the 30-year observation period performed male care. Their age and dominance rank did not influence the occurrence of male care. Most cases were first recorded between the last part of the mating season and the first part of the birth season (January-March), whereas male care was rarely observed during the mating season (October-December). In 12 of the 17 cases, male care ceased within 6 months after the first observation, whereas in the remaining cases, it continued for at least 1 year. In 15 of the 17 cases, males tended to perform male care for matrilineally unrelated female infants of low-ranking mothers. In some cases, the male and infant mother showed grooming interactions for 6 months both before and after the start of male care, whereas such grooming interactions were never recorded either before or after the start of male care in other cases. We also examined some hypotheses on male-immature associations and the probable benefits that males and infants might acquire through male care.

Triadic grooming among adult females in a free-ranging group of Japanese macaques.

This study aimed to quantitatively describe triadic grooming bouts in a free-ranging group of Japanese macaques (Macaca fuscata). Two types of triadic grooming bouts occurred less frequently and for a shorter duration than dyadic grooming bouts: straight-line type (SL), where individual A grooms B, who then grooms C; and two-to-one type (TO), where individuals X1 and X2 groom Y. TO-type grooming was recorded more often than SL-type grooming. As in the dyadic grooming bouts, two females who had direct grooming interactions in both SL-type (i.e., between A and B or between B and C) and TO-type groomings (i.e., between X1 and Y and between X2 and Y) and two groomers who did not have direct grooming interactions in TO-type grooming were closely related to each other in more than the half of the pairs recorded. Groomers were more likely to be subordinate to groomees in triadic grooming. Almost all of the observed pairs in SL- and TO-type groomings were also recorded in dyadic grooming bouts. These findings indicate that like dyadic grooming, triadic grooming bouts are largely influenced by blood relatedness through maternal lines and dominance relationships between participants. Based on affiliative relationships maintained through dyadic grooming, triadic grooming could be influenced by such affiliative relationships and then function to strengthen bonds between participants. Possible relationships between triadic grooming and the level of social tolerance among individuals are discussed from the viewpoints of interspecies differences among macaque species and regional differences in Japanese macaques.

Distribution of dorsal carriage among simians.

We surveyed the literature and obtained information from primate researchers and zookeepers to study the distribution of dorsal carriage among 77 simian species including New and Old World monkeys and apes in relation to arboreality and terrestriality, birth (litter) weight relative to maternal weight, and presence or absence of distinct natal coat colors. All New World monkeys are arboreal and commonly carry their infants dorsally. Conversely, arboreal Old World monkeys do not use dorsal carriage, and only some predominantly terrestrial Old World monkeys do so. Whereas lesser apes (which are highly arboreal) do not use dorsal carriage, arboreal as well as more terrestrial great apes commonly carry their infants dorsally. These findings indicate that simple arboreality or terrestriality is inadequate to explain dorsal carriage by monkeys. Infants of small- to medium-sized New World monkeys have relatively high birth weight compared with maternal weight, and are most likely to be carried dorsally than ventrally even on the first postnatal day. In contrast, infants of large-bodied New World monkeys are carried ventrally first and then dorsally up to the end of their second year, albeit increasingly infrequently. Among Old World monkeys, no association was found between mode of infant transport and birth weight relative to maternal weight, but some terrestrial Old World monkeys displaying dorsal carriage tend to do so with older infants, indicating that such behavior enables the mother to transport the infant with lower energy expenditure. Among terrestrial Old World monkeys, infants with distinctive natal coat colors are rarely carried dorsally until the natal coat color changes to adult coloration: infants with distinctive coat colors clinging to the backs of carriers could be highly visible and thus vulnerable to predation. Dorsal carriage by mothers may prolong the affiliative mother-infant relationship.

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.

Temporal adjustment of short calls according to a partner during vocal turn-taking in Japanese macaques.

Turn-taking is a common feature in human speech, and is also seen in the communication of other primate species. However, evidence of turn-taking in vocal exchanges within a short time frame is still scarce in nonhuman primates. This study investigated whether dynamic adjustment during turn-taking in short calls exists in Japanese macaques Macaca fuscata. We observed exchanges of short calls such as grunts, girneys, and short, low coos during social interactions in a free-ranging group of Japanese macaques. We found that the median gap between the turns of two callers was 250 ms. Call intervals varied among individuals, suggesting that call intervals were not fixed among individuals. Solo call intervals were shorter than call intervals interrupted by responses from partners (i.e., exchanges) and longer than those between the partner's reply and the reply to that call, indicating that the monkeys did not just repeat calls at certain intervals irrespective of the social situation. The differences in call intervals during exchanged and solo call sequences were explained by the response interval of the partner, suggesting an adjustment of call timing according to the tempo of the partner's call utterance. These findings suggest that monkeys display dynamic temporal adjustment in a short time window, which is comparable with turn-taking in human speech.

The relationship between female rank and reproductive parameters of the ringtailed lemur: a preliminary analysis.

We used data from a 13-year field study of wild ringtailed lemurs to analyze the relationship between female rank and reproductive parameters. In medium and small groups there were no significant differences in birth rate, infant mortality rate, and the number of surviving infants between the female rank categories. On the other hand, in large sized groups low-ranked females had a smaller number of surviving infants than middle-ranked females. This suggests that in large sized groups, within-group competition lowered the values of reproductive parameters of low-ranked females. On the other hand, high and low-ranked females of small sized groups tended to have a smaller number of surviving infants than high-ranked females of medium sized groups and middle-ranked females of large sized groups. Between-group competition should lower the values of their reproductive parameters. In sum, these results fit the expectation from Wrangham's (1980) inter group feeding competition model.

Monkeys with disabilities: prevalence and severity of congenital limb malformations in Macaca fuscata on Awaji Island.

The Awajishima Monkey Center (AMC) free-ranging, provisioned population of Japanese macaques has included individuals with congenital limb malformations (CLMs) for at least 40 years. Including new data from this study, 16.1% of AMC infants from 1969 to 2007 (185 of 1,150) were born with CLMs. However, relatively little is known about the demographics of CLMs in the population, particularly the relationships among occurrence and severity of CLMs and age-sex demographics after infancy. In 2004, we conducted a census at AMC. Of the 199 monkeys censused, 34 individuals (17.1%) had CLMs. To estimate the severity of CLMs, we created an index that ranks individuals on a scale of 0 to 1 based on affected and absent limbs and digits. The severity of CLMs varied greatly (index range = 0.01-0.79, mean = 0.29), with similar variation in severity in each age-sex class (Student t-test, P > 0.05).