Age-specific functions of stone handling, a solitary-object play behavior, in Japanese macaques (Macaca fuscata)

Stone handling (SH) in Japanese macaques, a form of solitary-object play, is newly acquired only by young individuals, and is the first example of a directly nonadaptive behavior that is maintained as a behavioral tradition within free-ranging provisioned social troops. We report here the first systematic investigation of this behavior in a stable captive social troop, the Takahama troop, which is housed in an outdoor enclosure of the Primate Research Institute (PRI), Kyoto University, Japan. This study was conducted to evaluate relevant competing hypotheses regarding the function of object play (e.g., misdirected foraging behavior and motor training) to explain the proximal causes and ultimate function(s) of SH. The "misdirected foraging behavior" hypothesis can be ruled out because of the lack of a clear temporal relationship between feeding and the occurrence of SH in any age class. Age-related differences in SH performance and behavioral patterns were observed, suggesting possible differences in the immediate cause and ultimate function between young and adults. Young individuals engaged in frequent bouts of short duration, involving locomotion and vigorous body actions throughout the day, which is typical for play by young in general. This pattern of behavior is consistent with the motor training hypothesis, which states that play occurs during the development of motor and perceptual skills and is thus potentially critical for neural and cognitive development. This practice is continued by those who acquire it at an early age, with adults engaging in significantly fewer but longer bouts that involve more stationary, complex manipulative patterns, almost exclusively in the late afternoon. We propose that for adults, at the proximate level SH is psychologically relaxing, but ultimately functions to maintain and regenerate neural pathways, and potentially helps to slow down the deterioration of cognitive function associated with advanced age in long-lived provisioned and captive macaques.     

Environmental and Social Factors Associated with the Occurrence of Stone-Handling Behavior in a Captive Troop of <Emphasis Type="Italic">Macaca fuscata</Emphasis>

Stone-handling, a documented behavioral tradition in Japanese macaques (Macaca fuscata), occurs in both captive and provisioned free-ranging troops. We utilize data systematically collected as part of a broader investigation of stone-handling behavior in a captive troop to elucidate the environmental and social factors responsible for its occurrence. We analyzed contexts of stone-handling over 18 mo to determine under what conditions individuals most often perform it. There is clear seasonal variation in the occurrence of stone-handling. The lowest number and shortest duration of stone-handling bouts were in winter, gradually increasing to a peak in summer, and again decreasing toward autumn. Monkeys stone-handled more on clear sunny days than on cloudy or rainy ones. They displayed the behavior less under stressful conditions caused by human intervention or by aggression among troop members. Such stressful social conditions appeared to decrease individual motivation for stone-handling. In other words, individuals most frequently performed stone-handling under more relaxed environmental and social conditions. The findings are consistent with the hypothesis that stone-handling is a form of solitary object play behavior in macaques.     

Effects of MDMA Injections on the Behavior of Socially-Housed Long-Tailed Macaques (Macaca fascicularis)

3,4-methylenedioxy-N-methyl amphetamine (MDMA) is one of the few known molecules to increase human and rodent prosocial behaviors. However, this effect has never been assessed on the social behavior of non-human primates. In our study, we subcutaneously injected three different doses of MDMA (1.0, 1.5 or 2.0mg/kg) to a group of three, socially housed, young male long-tailed macaques. More than 200 hours of behavioral data were recorded, during 68 behavioral sessions, by an automatic color-based video device that tracked the 3D positions of each animal and of a toy. This data was then categorized into 5 exclusive behaviors (resting, locomotion, foraging, social contact and object play). In addition, received and given social grooming was manually scored. Results show several significant dose-dependent behavioral effects. At 1.5mg/kg only, MDMA induces a significant increase in social grooming behavior, thus confirming the prosocial effect of MDMA in macaques. Additionally, at 1.5 and 2.0 mg/kg MDMA injection substantially decreases foraging behavior, which is consistent with the known anorexigenic effect of this compound. Furthermore, at 2.0 mg/kg MDMA injection induces an increase in locomotor behavior, which is also in accordance with its known stimulant property. Interestingly, MDMA injected at 1.0mg/kg increases the rate of object play, which might be interpreted as a decrease of the inhibition to manipulate a unique object in presence of others, or, as an increase of the intrinsic motivation to manipulate this object. Together, our results support the effectiveness of MDMA to study the complex neurobiology of primates’ social behaviors.     

Stone handling behavior in rhesus macaques (Macaca mulatta), a behavioral propensity for solitary object play shared with Japanese macaques

Stone handling (SH) behavior was systematically studied in a captive troop of rhesus macaques housed at the Primate Research Institute of Kyoto University, and compared with the results of long-term studies of this behavior in Japanese macaques, to evaluate the similarities of SH behavior in these two closely related species. Similar to Japanese macaques, rhesus macaques showed age-related differences in SH. Young animals were more active and displayed more SH patterns and bouts than did adults. Furthermore, the young displayed SH at a higher frequency and their bouts were of a shorter duration, compared to adults. Young adults were more active and displayed more patterns than did older adults. On the other hand, older adults were more conservative and displayed fewer patterns, and engaged in them for longer durations. All individuals displayed SH more frequently in relaxed environmental and social conditions. While lacking an apparent immediate adaptive value, practice of the behavior has been proposed to have long-term functional value for neural and cognitive development in the young and for the maintenance or repair of neuro-pathways in aging macaques that habitually perform the behavior. The results presented here are consistent with what we know about Japanese macaque SH. Given the uniformity of SH behavioral parameters and these two macaque species’ close phylogenetic relatedness, we propose that a similar functional and adaptive value for SH can be inferred for rhesus macaques.     

Do infant Japanese macaques (<Emphasis Type="Italic">Macaca fuscata</Emphasis>) categorize objects without specific training?

In the present study, we examined whether infant Japanese macaques categorize objects without any training, using a similar technique also used with human infants (the paired-preference method). During the familiarization phase, subjects were presented twice with two pairs of different objects from one global-level category. During the test phase, they were presented twice with a pair consisting of a novel familiar-category object and a novel global-level category object. The subjects were tested with three global-level categories (animal, furniture, and vehicle). It was found that they showed significant novelty preferences as a whole, indicating that they processed similarities between familiarization objects and novel familiar-category objects. These results suggest that subjects responded distinctively to objects without training, indicating the possibility that infant macaques possess the capacity for categorization.     

Playing it cool: Characterizing social play,bout termination,and candidate play signals of juvenile and infant Tibetan macaques(Macaca thibetana)

Play behaviors and signals during playful interactions with juvenile conspecifics are important for both the social and cognitive development of young animals.The social organization of a species can also influence juvenile social play. We examined the relationships among play behaviors, candidate play signals, and play bout termination in Tibetan macaques(Macaca thibetana) during juvenile and infant social play to characterize the species play style. As Tibetan macaques are despotic and live in groups with strict linear dominance hierarchies and infrequent reconciliation, we predicted that play would be at risk of misinterpretation by both the individuals engaged in the play bout and by those watching, possibly leading to injury of the players. Animals living in such societies might need to frequently and clearly signal playful intent to play partners and other group members to avoid aggressive outcomes. We gathered video data on 21 individually-identified juvenile and infant macaques(one month to five years of age)from the Valley of the Wild Monkeys, Mt. Huangshan,China. We used all-occurrence sampling to record play behaviors and candidate play signals based on an ethogram. We predicted that play groups would use multiple candidate play signals in a variety of contexts and in association with the number of audience members in proximity to the players and play bout length. In the 283 playful interactions we scored,juvenile and infant macaques used multiple body and facial candidate play signals. Our data showed that juvenile and infant Tibetan macaques use a versatile repertoire of play behaviors and signals to sustain play.     

History and Present Scope of Field Studies on <Emphasis Type="Italic">Macaca fuscata yakui</Emphasis> at Yakushima Island,Japan

Field studies on Japanese macaques on Yakushima Island started in the mid-1970s, >25 yr after the emergence of Japanese primatology, in response to criticism of methods using provisioning and the desire to find the socioecological factors influencing the social life of macaques in natural habitats. We habituated macaques without provisioning mainly in the coastal warm-temperate forest and found that they lived in small troops with a high socionomic sex ratio. Observations of several troop fissions and troop takeovers by nontroop males suggest that Yakushima macaques have a different social organization from that of Japanese macaques in other habitats. For example, youngest ascendancy as the dominance relationhip among sisters, which usually occurs in provisioned troops, was absent in Yakushima macaques. We compared their ecological and social features with those of Japanese macaques at Kinkazan (cool-temperate forests) and found that abundance of high-quality foods may cause stronger intra- and intertroop competition at Yakushima. Female Yakushima macaques may more positively solicit nontroop males to associate with them during the mating season. Such a tendency may promote frequent male movement between troops and frequent troop fissions. Though ecological factors form social features of Japanese macaques, some features such as male association and movements between troops are not accounted for via socioecology. Recent field studies have focused on macaques living at higher altitudes in Yakushima and on individual survival strategies by taking diverse viewpoints and using new technologies. DNA analysis of fecal samples shows low genetic diversity and suggests the macaques’ recent expansion from lowland to highland forests in Yakushima. The population censuses conducted annually indicate that the higher-altitude macaques have a larger home range but a similar group size versus their counterparts at low elevations. The unsolved issues in socioecology will pose a challenge to the younger generation of primatologists. Conservation of macaques and their habitat is one of our major activities at Yakushima. The level of protection has gradually increased in the National Park at Yakushima and, via our various conservation efforts, its most important area was designated a World Heritage Site by UNESCO in 1993. However, large-scale logging in the 1960s and 1970s caused the loss of macaque habitats and led to increased crop damage by them in the 1980s. We have proposed effective methods to protect cultivated fields from macaques as well as several plans for sustainable use of forests, such as ecotourism and a fieldwork course for university students. Local residents and researchers have created several nongovernment organizations (NGOs) to promote conservation and nature study at Yakushima. The role of local NGOs is particularly important to mitigate conflicts between people and wildlife. Though hundreds of macaques are still captured as pests annually in Yakushima, we continue the conservation measures and spread awareness of conservation in cooperation with the local NGOs.     

Manipulation of objects in a captive group of lion-tailed macaques (Macaca silenus)

The purpose of this study was to investigate the manipulative propensities of a captive group of lion-tailed macaques (Macaca silenus). Simple natural objects (browse and bamboo poles) were provided regularly in the home cage. Findings indicate richness in the frequency and form of manipulative activities, with juvenile males manipulating the test objects more frequently and exhibiting more goal-directed manipulative activity than adult females. A variety of goal-directed manipulative activities (use of objects to act as ladders, to apply leverage, and to create perches) occurred spontaneously, with some instances involving joint action or social use. These data are consistent with the hypotheses that macaques possess extensive capacities for object exploration and social facilitation, and that an evolutionary history of omnivorous foraging habits correlates positively with the expression of anomalous sensorimotor skills.     

The Effect of Age and Sex on Object Exploration and Manipulative Behavior in a Neotropical Raptor,the Chimango Caracara,Milvago chimango

We studied object exploration and manipulative behavior in wild‐caught Chimango Caracaras (Milvago chimango), an opportunistic and generalist raptor species, in relation to age and sex differences. Each bird was presented with six objects. We then recorded the latencies to approach and first contact with the objects, the number of objects explored, and the number of exploration events performed on each object. Age influenced the tendency to explore in M. chimango. Compared with adults, juveniles were more likely to explore the objects, approaching and contacting them more quickly. The number of objects explored was also higher in young than adult birds. Both age classes used a variety of manipulative behaviors to explore the objects, some of which have been described as play in others studies. Sex did not affect an individual's likelihood to explore or the number and frequency of manipulative behaviors used during object exploration. The tendency for both young and adult birds to explore and manipulate objects that not resemble prey is likely to be a distinct advantage for a generalist species like M. chimango which must cope with a high diversity of modified environments.     

Mobility of surrogate mothers and persistent neophobia in cynomolgus monkeys (Macaca fascicularis)

In search of the relevant difference between mother rearing and surrogate rearing with respect to the emergence of neophobic behavior in macaques, we tested the hypothesis that mobility of surrogate mothers prevents the development of neophobic behavior in cynomolgus macaques. The experimental group consisted of ten surrogate-reared subjects which during their first year got rides on surrogate mothers moving through the cage. The control group consisted of nine subjects reared with immobile surrogate mothers. Between the age of 7 and 27 months the reactions to two different novel objects were tested. First exposure to one object occurred at 6 months of age and to the other object at 20 months. The kind of object and the age of first exposure made no difference. Contrary to our expectations mobility of surrogates did not affect the incidence of neophobia: most subjects in both groups persistently avoided the objects. This finding seems to support Hofer's hypothesis that the mother acts as a regulator of the infant's behavior and physiology.     

Affiliative relations among male Japanese macaques (Macaca fuscata yakui) within and outside a troop on Yakushima Island

Male Japanese macaques (Macaca fuscata yakui) in a troop on Yakushima Island frequently groom other males. However, previous studies have not compared the social relations of troop males to those of non-troop males. I followed all troop males and non-troop males in and near a troop during a mating season and during the following non-mating season and recorded their neighbors, grooming, and agonistic interactions. Comparisons of the social relations of troop males and non-troop males with other troop members revealed that grooming and agonistic interactions with females during the mating season were similar between troop and non-troop males. However, troop males groomed each other more often and had fewer agonistic interactions among themselves than did non-troop males. Compared to what occurred in the mating season, troop males groomed females less often and exchanged grooming bouts more often with other troop males during the non-mating season. One non-troop male groomed females more frequently than did any troop male in both seasons, and this male groomed troop males more frequently than did any troop male in the non-mating season. This male immigrated into the troop during the following mating season. Regardless of their competition with respect to reproduction, male Japanese macaques on Yakushima Island maintain affiliative relations, probably to cooperatively defend fertile females from non-troop males.     

Object manipulation by wild red colobus monkeys living in the Abuko Nature Reserve,the Gambia

Temminck's red colobus (Procolobus badius temminckii) inhabiting the Abuko Nature Reserve, the Gambia, manipulate objects during solitary play, social play where there is an obvious goal involved, agonistic and intimidation displays, and tug-of-war contests. Some of the object manipulation may be regarded as true tool use and manufacture. Variation in the form and frequency of manipulative activities shows clear sex differences which may relate to sex differences in social behavior. All observed cases of tool manufacture occurred at times of maximum social upheaval for the individual concerned in the act.     

Compete to Play: Trade-Off with Social Contact in Long-Tailed Macaques (Macaca fascicularis)

Many animal species engage in various forms of solitary object play, but this activity seems to be of particular importance in primates. If playing objects constitute a valuable resource, and access to such objects is limited, a competitive context may arise. We inserted a unique toy within a mini-colony of long-tailed macaque (Macaca fascicularis) and compared their behaviors to sessions without playing object. An automatic color-based 3D video device was used to track the positions of each animal and the toy, and this data was categorized into 5 exclusive behaviors (resting, locomotion, foraging, social contact and object play). As expected, the delay to first access to the object reflected the hierarchy of the colony, indicating that a competition took place to own this unique resource of entertainment. In addition, we found that the amount of object play was not correlated with social or foraging behavior, suggesting independent motivational mechanisms. Conversely, object playing time was negatively correlated with idling time, thus indicating its relation to pastime activities. Interestingly, the amount of social contacts in the group was significantly reduced by the heightened competitive context, suggesting that competitors are more likely to be perceived as potential threat requiring caution, as shown in humans. Experimental manipulation of competitive contexts in primates reveals common mental processes involved in social judgment, and shows that access to valuable resources can be a sufficient cause for variations in group cohesion.     

The range of action of the mother and the avoidance of big novel objects in long-tailed macaques

Most surrogate-reared long-tailed macaques persistently avoid a big novel object, whereas most mother-reared subjects approach it. A striking difference between these attachment figures is that the mothers moved about with their infants, whereas the surrogates were fixed to the wall In this experiment, we aimed to find out whether mobility of the attachment figure plays a part in the development of an infant’s responses to big novel objects. We studied the effects of mobility of the attachment figure by restraining mothers in their range of action. We confined mothers of the experimental group in a small part of the home cage. Their infants could leave the cage in which their mothers were restrained. Infants that were growing up with unrestrained mothers made up the control group. At two different ages all infants encountered a big novel object. We used two different objects. We found that the range of action of the mother did not significantly affect the responses of infants to big novel objects. As in the previous studies, most of the mother-reared monkeys approached the objects. The age at which an infant was first exposed to an object did not significantly affect its behavior toward it. Further, the two different objects evoked the same reactions.     

Responses to a snake model in captive crab-eating macaques (Macaca fascicularis) and captive tufted capuchins (Cebus apella)

The responses to a model snake in captive crab-eating macaques (Macaca fascicularis) and captive tufted capuchins (Cebus apella) were investigated. In both species the amount of fear behavior was higher in the presence of the model than during baseline conditions. Unlike the macaques, in the capuchins the frequency of these behaviors decreased across trials. In the two species the amount of explorative and manipulative behaviors and the use of space were also different. Unlike macaques, all capuchins manipulated the objects available in the testing room, and three subjects contacted the apparatus by using objects. Macaques did not show significant preferences for any particular part of the testing room. In both conditions, capuchins used the floor more than macaques did. Further, capuchins increased the use of the floor across experimental trials. Latency to reach the floor was higher in macaques than in capuchins. When on the floor, capuchins spent most of the time close to the snake apparatus. It is proposed that the behavioral differences between capuchins and macaques in the responses to a potential predator indicate that capuchins have a greater propensity to explore and to contact the novel stimulus directly, or by means of objects, than macaques do. These tendencies may lead to the exploitation of novel features in the environment.     

Intergroup affiliative interactions and intergroup transfer of young male Japanese macaques (Macaca fuscata)

The social interactions between young male Japanese macaques (Macaca fuscata) and members of two adjacent groups were studied. Young males usually associated with members of a single group. Although some young males occasionally interacted with members of the neighboring group, the frequency of their intergroup affiliative interactions was much lower than that of their intragroup interactions. The intergroup affiliative interactions were less symmetrical than the intragroup interactions. Three- or four-year-old males who remained in their natal group interacted with males of the neighboring group, whereas males over 5 years old did not. Young males revealed a dramatic change in their association partners from males in one group to those in another during the course of their intergroup transfer. Males who remained in their natal group did not attempt to interact with females of the neighboring group. In contrast, males who had transferred to a non-natal group interacted with females in their natal group. It is suggested that intergroup affiliative interactions and intergroup transfer of young male macaques are influenced by close associations between males. The immediate motivation for transfer of young natal macaques may be some attraction to males outside their group rather than sexual attraction to unfamiliar females.     

Contestable shelters provoke aggression among 0+ perch, <Emphasis Type="BoldItalic">Perca fluviatilis</Emphasis>

Synopsis We examined behavioural interactions and feeding within triads of young-of-the-year (YOY) Eurasian perch, Perca fluviatilis, in aquaria with and without a shelter. For the first time we showed that competition for shelters, but not for food, provokes aggressiveness and triggers establishment of social hierarchy among young perch. No aggressiveness occurred during feeding bouts, when food was a limited resource. We expect the observed interactions to occur in natural heterogeneous habitats providing limited number of refuges and high local density of fish. They may ultimately lead to previously anticipated interference competition among juvenile perch.     

Developmental trends in mother-infant interactions in Java macaques (Macaca fascicularis) during the first ten days of life

In this study on Java macaques themain characteristics of the mother-infant relationship during infants' first 10 days have been elaborated. Early mother and infant behaviour is described and early interactions between mothers and their young have been analyzed. Observations and trend analyses of early behaviours like ventro-ventral contact behaviour, being on nipple, and explorative behaviour, make it clear that Java macaque infants play an important role in the early development of mother-infant interactions. In contrast to the rhesus and the stumptailed infant, the young Java macaque appears to develop a great variety of behaviours in its first 10 days. Whereas the infant's behaviour gains in complexity and social initiative, the mother becomes increasingly more passive and self-oriented. Early mother-infant interaction can be characterized by mutual adjustment.     

A preliminary study of vocal communication in wild long-tailed macaques (Macaca fascicularis). II. Potential of calls to regulate intragroup spacing

This study is a preliminary assessment of the potential of long-tailed macaque (Macaca fascicularis) calls to operate in systems of within-group spacing. Covariation in the rate of occurrence of calls with party spread, size, and activity among wild individuals of one group suggested that four classes of calls may function in intragroup spacing. Two of them are “clear” calls of long duration and pronounced frequency modulation. Calling rate increased with party spread for low- and high-frequency variants of these calls during resting and feeding respectively, suggesting possible utility in maintenance of spatial relations over moderately long distances. A third “harsh” call was negatively correlated with party spread during foraging and may thus function to increase dispersion among foraging individuals. Another harsh call with a tonal onset was unique among all calls in the vocal repertoire in being more frequently performed by lone, isolated individuals than by macaques accompanied by others, suggesting a possible function in reestablishing contact that has been severed. The functional significance of these calls with respect to their acoustic structures is discussed. Macaques that use calls to regulate intragroup spacing can control communication distance and direction by their choice of acoustically different vocalizations. This choice may be affected not only by varying environmental constraints on sound transmission, but also by social and ecological factors such as intragroup competition.