Jean-Baptiste Leca

Japanese macaque cultures: Inter- and intra-troop behavioural variability of stone handling patterns across 10 troops

Summary Stone handling (SH), a form of solitary object play, consists of an individual manipulating stones by performing various behavioural patterns. Previous findings from the Arashiyama population of Japanese macaques suggested that SH is socially transmitted across generations as a behavioural tradition. To further test the hypothesis that SH is a traditional behaviour in this species, we present the most systematic inter-troop comparison of this behaviour from an investigation of nine troops of Macaca fuscata fuscata and one troop of M. f. yakui living at six sites in Japan. We analyzed a total 1280 video-recorded SH bouts and charted the relative frequency of occurrence of 45 SH behavioural patterns across age classes. Many SH patterns showed geographically patchy distributions and were referred to as local variants or SH traditions. In terms of behavioural complexity, we found three levels of SH culture, each level being defined by troop-dependent clusters of SH traditions. We found a positive correlation between geographic proximity and cultural similarity in SH between troops. To explain similarities in the SH repertoires between the free-ranging troops living at the same site, we discussed the phenomenon of cultural zones. We interpreted intra-group variability in the performance of SH patterns from the viewpoint of developmental factors. We found no major difference between the two subspecies in the occurrence and form of SH.

Indirect social influence in the maintenance of the stone-handling tradition in Japanese macaques, Macaca fuscata

Comparative and longitudinal studies have shown that stone-handling (SH) behaviour, defined as the noninstrumental manipulation of stones by performing various behavioural patterns, is socially transmitted across generations as a cultural behaviour in Japanese macaques. We investigated experimentally how stimulus/local enhancement, a form of indirect social influence through the physical traces typically left in the environment by previous stone handlers, might trigger SH behaviour at the individual level, and thus could contribute to the maintenance of the SH tradition at the group level. Through the semicontrolled conditions of field experiments, conducted in the free-ranging provisioned Arashiyama E troop, in which the SH tradition has been well established for nearly three decades, our results supported the stimulus/local enhancement hypothesis. Most group members preferentially directed their SH behaviour towards typical physical traces of SH activity (piles of stones) over randomly scattered stones. Encountering SH artefacts enhanced the use of these particular stones for performing SH in that particular part of the environment. The common occurrence of such ‘play stations’ may favour the frequent reuse of the same stones over time and explain the transport of stones between and around SH artefacts. We provided evidence for the role of indirect social inputs on the long-term persistence of the SH tradition in Japanese macaques, through SH by-products, the stimulating effect of which can be delayed in time and separate in space from others. We discuss our findings from the perspective of socially mediated behaviours, conformity-enforcing responses and niche construction.

Social Aspects of Fur-rubbing in Cebus capucinus and C. apella

Capuchins rub particular plant materials into their pelage, a behavior for which most authors have proposed a medicinal function (Baker in American Journal of Primatology 38:263–270, 1996, Baker, M. (1998). Fur Rubbing as Evidence for Medicinal Plant Use by Capuchin Monkeys (Cebus capucinus): Ecological, Social, and Cognitive Aspects of the Behavior. Dissertation thesis. University of California Riverside; DeJoseph et al. in Journal of the American Academy of Dermatology 46:924–925, 2002). Individuals fur-rub solitarily or in groups, but researchers have not conducted studies to understand the differences. We investigated the link between the form of fur-rubbing and other social variables in 2 capuchin species. We supplied 2 captive groups —white-faced capuchins and tufted capuchins— with citrus fruit and onions and explored the behavioral processes and social aspects underlying the activity. We documented the occurrence, number of participants, and effect of recruitment behaviors in fur-rubbing subgroups. We investigated the role of kinship, affiliation, and dominance relationships in accounting for fur-rubbing groups. There is a significant difference in the form of fur-rubbing between white-faced and tufted capuchins. White-faced capuchins fur-rubbed mainly in subgroups and performed a particular behavior to recruit prospective participants, whereas tufted capuchins fur-rubbed mainly alone, and showed no particular motivation to be joined by other group members. White-faced capuchins could fur-rub together frequently, whatever their degree of kinship, affiliation, or dominance interval. In tufted capuchins, fur-rubbing appeared to be significantly affected by kinship and dominance.

Cultured Monkeys Social Learning Cast in Stones

Sixty years ago, the notion that animals could have culture was unthinkable to most behavioral scientists. Today, evidence for innovation, transmission, acquisition, long-term maintenance, and intergroup variation of behavior exists throughout the animal kingdom. What can the longitudinal and comparative study of monkeys handling stones tell us about how culture evolved in humans? Now in its 30th year, the systematic study of stone-handling behavior in multiple troops of Japanese macaques has shown that socially mediated learning is essential to explain the spread, persistence, and transformation of individual behavioral innovations among group members. The integrative research paradigm presented here can be applied to the study of various candidate behavioral traditions in other species.

Food provisioning and stone handling tradition in Japanese macaques: a comparative study of ten troops

By addressing the influence of food provisioning on stone handling (SH), a behavioral tradition in Japanese macaques, this study contributes to the ongoing debate in cultural primatology by asking whether human intervention influences the emergence or propagation of behavioral traditions. SH is a form of object play consisting of the manipulation of stones by performing various behavioral patterns. We tested the hypothesis that the frequency of food provisioning affects the daily performance, form, and context of occurrence of SH by influencing a troops feeding‐related activity budget. We used a standardized observation procedure to investigate SH in ten troops of Japanese macaques. In troops provisioned several times a day, SH was more frequent, longer, and more prevalent during provisioning than nonprovisioning periods. These effects of provisioning were not significant in troops provisioned less frequently. SH was more frequently integrated with food‐related activities in troops supplied with food several times a day than in the other troops. Food provisioning may be a key factor in the innovation and transformation phases of the SH tradition in Japanese macaques. Am. J. Primatol. 70:803–813, 2008.

Male Homosexual Behavior in a Free-Ranging All-Male Group of Japanese Macaques at Minoo, Japan

We documented nine male homosexual consortships within three different male–male dyads in a free-ranging all-male group of Japanese macaques (Macaca fuscata), at Minoo, Japan. A total of 63 male–male mounts were observed during these consortships. Male homosexual interactions shared most of the behavioral components that have been reported to characterize heterosexual and female homosexual consortships in this species. Convergent behavioral data, including analysis of male–male solicitations, mounting postures, body orientations, inter-mount activities, and third-party male intrusions supported the conclusion that male–male consortships are a sexual phenomenon. We discussed a series of proximate and ultimate hypotheses that purport to account for the occurrence of male homosexual behavior in all-male groups of primates, including humans. This first report of male homosexual interactions in an all-male group of Japanese macaques contributes to the growing database used to provide insights into the developmental processes, causal mechanisms, adaptive significance, and phylogenetic pathways of same-sex sexual behavior.

Development of sexual and socio-sexual behaviours in free-ranging juvenile male Japanese macaques, Macaca fuscata

The emergence of conceptive and non-conceptive sexual behaviours in mature individuals can be traced back to immature socio-sexual behavioural patterns. We tested the ‘needing-to-learn hypothesis’ in the development of sexual behaviours in the immature male Japanese macaques of Arashiyama, Japan. This hypothesis holds that juvenility serves to provide young individuals with a period in which to practice adult male-like sexual and socio-sexual behaviours and partner choice. Our cross-sectional focal data on mounting behaviour and partner choice in juvenile males (1–3 years) supported most of our predictions: (1) as they became older and learnt more effective patterns of sexual solicitations, juvenile males performed more demonstrative solicitations and less non-demonstrative solicitations, (2) the frequency of mounts performed by juvenile males increased with age and converged on a frequency of mounts typical of adult males, (3) the frequency of mounts reflecting underachievement (i.e., improperly oriented mounts and single/no foot-clasp mounts) decreased as juvenile males became older, (4) the double foot-clasp mounting posture became gradually more common in juvenile males over time, while other mounting postures became less common and (5) from two to three years old, the frequency of males’ sexual mounts directed to adult females increased. Such timelines of gradual increase in the frequency of effective adult-like behavioural patterns and gradual decrease in the frequency of less effective immature behavioural patterns are consistent with the ‘needing-to-learn hypothesis’ emphasizing the role of age and practice in the progressive acquisition of adult-like sexual behaviour, mounting skills, and partner age choice during male juvenility.

Principles and levels of laterality in unimanual and bimanual stone handling patterns by Japanese macaques

The preferential use of one hand over the other is considered the primary behavioral expression of structural and functional asymmetry in cerebral structures, which is a decisive factor in human evolution. We present the first analysis of manual laterality in a form of object play-stone handling (SH) behavior-in a free-ranging group of Japanese macaques. Defined as a stone-directed manipulative activity, and comprised of multiple one-handed SH patterns (e.g., grabbing a stone in one hand and cradling it against its chest), as well as coordinated two-handed SH patterns with manual role differentiation (e.g., holding a stone with one hand and rubbing it with the other), SH behavior is a good candidate for the study of hand lateralization. We systematically followed the methodological framework developed by McGrew and Marchant (1997) to measure and analyze the presence, strength, and direction of manual preference in the performance of SH behavior and in various SH patterns, both at the individual and group level. Some individuals showed a significant manual lateral bias on a single SH pattern (hand preference), whereas others showed consistency in laterality across all or most of the SH patterns they performed (hand specialization). At the group level, we found that, although their collective distribution of left versus right remained random, most subjects were either significantly but incompletely lateralized, or completely lateralized within particular SH patterns (pattern specialization), but not across all SH patterns (no handedness for SH behavior as a whole). As predicted by the task-complexity model, hand specialization and handedness were stronger in the coordinated bimanual SH patterns than in the unimanual patterns. We discuss the implications of our findings for the evolution of manual preferences in noninstrumental object manipulation versus stone tool use in nonhuman primates and hominins.

Complexity in object manipulation by Japanese macaques (Macaca fuscata): a cross-sectional analysis of manual coordination in stone handling patterns.

Defined as a spontaneous stone-directed noninstrumental manipulative behavior, and comprised of multiple one-handed and (a)symmetrical/(un)coordinated two-handed patterns, stone handling (SH) is a good candidate for the study of complexity in object manipulation. We present a cross-sectional developmental analysis of SH complexity in Japanese macaques (Macaca fuscata), through the combined investigation of bimanuality, coordination, and symmetry in hand use. Bimanual SH patterns were more frequent than unimanual patterns. Among bimanual patterns, coordinated actions were more frequent than uncoordinated ones. We recorded five asymmetrical coordinated SH patterns with manual role differentiation, a form of hand use reminiscent of complex actions involving the use of tools in monkeys and apes. Bimanuality in SH was affected by body posture. Aging individuals performed less bimanual and less coordinated SH patterns than younger individuals. Our result on senescent males performing less bimanual patterns than senescent females was consistent with sex differences found in the late deterioration of complex manual movements in other species. Although some SH patterns represent a high degree of behavioral complexity, our results suggest that SH behavior is not as complex as tool-use or tool-manufacture in other nonhuman primates and hominids.

Stone-throwing by Japanese macaques: form and functional aspects of a group-specific behavioral tradition

Throwing is a major behavioral component of hominid evolution. Comparison of this behavior across a broad range of non-human primate species is needed to elucidate the phylogenetic constraints on throwing behavior. In this study of stone-throwing in Japanese macaques, we present a systematic multi-group comparison of the frequency and prevalence of this behavior as well as detailed descriptions and quantitative data on the form, context, and possible social transmission of stone-throwing. Stone-throws were mainly underarm, performed from a tripedal posture, and often accompanied by repeated vertical leaps. We found marked individual hand preferences for throwing, but no consistent group-level handedness. Our results support the hypotheses relating body posture, throwing style, and handedness in throwing by primates. Based on the analysis of the contexts that may elicit the behavior, we postulate that unaimed stone-throwing in Japanese macaques may serve to augment the effect of agonistic displays, and accordingly, can be regarded as spontaneous tool-use. Our findings are consistent with the comparative data using modern non-human primate species to model the structural processes and functional aspects of throwing evolution in early hominids. This study supports the view that tool-use evolves from initially non-functional behaviors, such as stone handling, which is a form of object play. Stone-throwing by Japanese macaques meets several criteria of a behavioral tradition, including group-specificity. This first report of a stone-tool-use tradition in Japanese macaques is of direct relevance to the question of the evolution of stone technology in hominids.