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.     

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.     

Age-related differences in the performance, diffusion, and maintenance of stone handling, a behavioral tradition in Japanese macaques

Identifying the sources of behavioral diversity in non-human primates is vital to understanding the evolution of human behavior. Stone handling (SH, hereafter) is a form of object play consisting of the manipulation of stones by performing various behavioral patterns. This behavior is socially transmitted from generation to generation in Japanese macaques (Macaca fuscata), as a behavioral tradition. SH behavior in particular may reflect on the origin and evolution of stone-tool material culture. The objective of this study was to assess how group size, age structure, and age- and sex-related differences may account for the substantial intra- and inter-troop variations in SH reported in ten troops of Japanese macaques. Our results supported the hypothesis that patterns of variation in SH across troops reflected variability in group size and composition in age classes. We found that troop size was correlated with the proportion of troop members exhibiting SH simultaneously. The effect of troop size on the synchronized performance of SH may reveal the contagious nature of play. Our results suggest that the age structure of the group may affect the diffusion of SH. As predicted by the surplus energy hypothesis, a major functional hypothesis about play, intra-group variation in SH reflected more age- than sex-related differences. SH mainly occurred and was more frequent in younger than in older individuals, whereas no significant sex differences were found. SH episodes were shorter, more vigorous, and SH patterns were more diverse and less complex in immature than in mature individuals. The present findings reveal that age-related factors and group size may constrain the performance, diffusion, and maintenance of SH within a troop. Contrary to most other socially transmitted stone-tool using behaviors in non-human primates and early hominids, there is no optimal SH pattern. Provided some form of social learning, the non-adaptive nature of SH may allow particular SH pattern preferences to emerge at the group level. Our findings urge the use of an inter-populational comparative approach based on multivariate analyses when addressing the question of the evolution of behavioral traditions in primate and human populations.     

Comparison of stone handling behavior in two macaque species: implications for the role of phylogeny and environment in primate cultural variation

This study describes the stone handling (SH) behavior of captive rhesus macaques and compares it with that of a captive troop of Japanese macaques with reference to the relative contributions of phylogeny-driven behavioral propensities, environmental differences and socially facilitated learning to the formation of culture. These systematically collected data demonstrate for the first time that two closely related macaque species might share a common cultural behavior, SH. The rhesus troop displayed SH behavioral patterns that was already described in Japanese macaque troops. The one exception was a new pattern not yet seen in any Japanese macaque troop. Differences in the physical environment of the two study enclosures may be responsible for some of the variation in observed SH behavioral patterns in these two troops. These data support the idea that environmental factors can be important for the formation of cultural variation, when the key materials needed to perform the behavior are present in both habitats (stones). Our results are consistent with the prediction made by Huffman and Hirata [The biology of tradition: Models and evidence. Cambridge: Cambridge University Press. p 267-296] that an interactive triad of phylogenetic, environmental and social factors can be responsible for the formation of cultural variation in primates.     

Social object play among young Japanese macaques (Macaca fuscata) in Arashiyama, Japan

Social object play (SOP), i.e., social play using portable object(s), among young Japanese macaques (Macaca fuscata; 0-4 years old) in the Arashiyama E troop was studied using a modified sequence sampling method from July to October 2000. SOP was a relatively common activity for most of the young macaques and often continued for long periods. Participants used many kinds of object, including edible natural objects and artificial objects, such as plastic bottles, but they never used provisioned food or wild fruit in SOP bouts. An analysis of long bouts (>/=0.5 min) revealed the following interactive SOP features: (1) at any given time, participants used only one object, and only one participant held the object; (2) during SOP play-chasing, the object holder was likely to be chased by others; (3) during long bouts, the object changed hands frequently; and (4) agonistic competition for an object among young macaques was rare. Combinations of sexes, ages, relative ranks, or matrilines of the object holder and non-holder did not affect the tendency that the holder was chased by non-holder(s) during play-chasing. Even when there was a change in object holders, the repetitiveness of this interactive pattern, i.e., that the holder would be chased during SOP bouts, distinguished the SOP structure from that of other types of social play without object(s). General proximate social play mechanisms, such as self-handicapping or role taking, were associated with SOP. Other mechanisms that affected SOP included the following: (1) young macaques treated an object as a target in play competition, and (2) 'being the holder of a target object' was associated with the 'role of the chasee.'     

The foraging behavior of Japanese macaques Macaca fuscata in a forested enclosure:Effects of nutrient composition,energy and its seasonal variation on the consumption of natural plant foods

In the wild, primate foraging behaviors are related to the diversity and nutritional properties of food, which are affected by seasonal variation. The goal of environmental enrichment is to stimulate captive animals to exhibit similar foraging behavior of their wild counterparts, e.g. To extend foraging time. We conducted a 12-month study on the foraging behavior of Japanese macaques in a semi-naturally forested enclosure to understand how they use both provisioned foods and naturally available plant foods and what are the nutritional criteria of their consumption of natural plants. We recorded time spent feeding on provisioned and natural plant foods and collected the plant parts ingested of their major plant food species monthly, when available.We conducted nutritional analysis (crude protein, crude lipid, neutral detergent fiber-'NDF', ash) and calculated total non-slructural carbohydrate - 'TNC' and total energy of those food items. Monkeys spent 47% of their feeding time foraging on natural plant species. The consumption of plant parts varied significantly across seasons. We found that leaf items were consumed in months when crude protein, crude protein-to-NDF ratio, TNC and total energy were significantly higher and NDF was significantly lower, fruit/nut items in months when crude protein and TNC were significantly higher and crude lipid content was significantly lower, and bark items in months when TNC and total energy were higher and crude lipid content was lower. This preliminary investigation showed that the forested enclosure allowed troop members to more fully express their species typical flexible behavior by challenging them to adjust their foraging behavior to seasonal changes of plant item diversity and nutritional content, also providing the possibility for individuals to nutritionally enhance their diet.     

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 troop's 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.     

Age class differences in the feeding behavior of captive Japanese macaques (Macaca fuscataia) in the forested and nonvegetated enclosure groups

Age class differences in feeding behavior of primates are affected by many factors, including feeding competition, foraging skills, habitat type, food abundance and distribution, body mass, and food types. Two captive groups of Japanese macaques (Macaca fuscata), one housed in a forested enclosure and the other in a nonvegetated enclosure, were studied to examine the effect of environmental enrichment on age class differences in feeding behavior. Although there was no significant age class difference in time spent feeding on provisioned foods in either enclosure, the feeding rate (intake of unit food/minute) of adults consuming provisioned monkey chow was significantly higher than that of immatures in both enclosures, and was faster for both age groups in the nonvegetated than in the forested enclosure. Overall, feeding time was greatly extended for individuals of both age classes in the forested enclosure compared with their counterparts in the nonvegetated enclosure. Immatures in the forested enclosure utilized a significantly greater number of plant species and food items, exploiting many food items available among the terminal branches, and spent significantly more time feeding than adults. Perhaps constrained by larger body size, adults fed more often on the ground or middle height of the trees, likely reducing competition over plant food resources between adults and immatures. The natural vegetation played an important role in extending feeding time and segregating substrate use during feeding by adults and immatures. This study revealed the benefits concerning environmental enrichment of a naturally forested enclosure, which provides captive primates the opportunity to exhibit age class and species-typical feeding behaviors of importance for their dietary maintenance and general health.     

The Development of Social Behavior Through Play in the Steller Sea Lion

Steller sea lion pups were observed from birth through the eighthweek of life. Data were collected on dyadic interactions among19 marked animals. The results showed that among these precociousanimals adult-like behavioral patterns are clearly evident by2 weeks of age. In play bouts motor components of many adultmotivational states occur in mixed sequence. Most of the motorcomponents in play bouts resembled male agonistic behavior.By analyzing for the ratio of one behavioral pattern to another,play bouts were divisible into types, e.g., fighting bouts wereclearly separable from boundary defense bouts. Age, sex, terrain,and the specific play partner were all determinants of the motorcomponents used in an encounter. Sexual dimorphism was obviousand measurable, but no clear sign of a dominance hierarchy wasfound. The results are discussed in terms of the possible rolethat play behavior holds in establishing the relative stabilityor flexibility of behavior among adults.     

Plasma cholesterol levels in free-ranging macaques compared with captive macaques and humans

Plasma total cholesterol in free-ranging Japanese macaques (Macaca fuscata) on Koshima islet and in free-ranging long-tailed macaques (Macaca fascicularis) at Pangandaran in Indonesia was found to occur at very low levels compared with captive macaques and humans. Although total cholesterol levels in captive macaques were lower than humans, differences in HDL cholesterol levels were only small. In both sexes of wild and captive Japanese macaques, total cholesterol levels decreased from birth through to young adulthood but then increased in adult females of the captive group. In contrast, the value for adult females of the wild troop remained at a low level. Low TCH levels in adult females of the wild Japanese macaque troop may be due to a low energy intake and may have caused a delay in the onset of sexual maturation. Plasma TCH levels increased with the addition of 0.1% dietary cholesterol over six weeks in captive long-tailed macaques. That the cholesterol value after six weeks was dependent on cholesterol levels prior to supplementation indicates that captive macaques are slightly saturated with cholesterol.     

Status of urban populations of the long-tailed macaque (<Emphasis Type="Italic">Macaca fascicularis</Emphasis>) in West Sumatra,Indonesia

We studied long-tailed macaque (Macaca fascicularis) populations in Padang, West Sumatra, Indonesia, focusing on the effect of human provisioning on their demography and dietary composition. We conducted a field survey at three sites in the city: Gunung Meru, Gunung Padang, and Gunung Panggilun. Mean troop size (range 28–68) and infant ratio (range 0.38–1.00) were greater in Gunung Meru, where the macaques have been highly provisioned, than at the other two study sites (troop size 10–15; infant ratio 0.00–0.33). The macaques at all sites consumed both natural and human foods, but dependence on the latter differed among sites: three-quarters of the diet of macaques in Gunung Meru consisted of human foods, while human foods comprised less than 5% of the macaque diet at the other sites. The ability of macaques to modify the proportion of human food is a behavioral flexibility that facilitates the survival of the long-tailed macaque in urban habitats. Without restrictions on provisioning, the degree of dependence of macaques on human foods and population size could increase, especially in Gunung Meru, and human–macaque conflict could escalate. In order to create an effective management policy for urbanized monkeys, long-term quantitative data on macaque behavior and monitoring of population parameters are required.     

Stone handling by Japanese macaques (Macaca fuscata): Implications for tool use of stone

Stone-play, a newly innovated cultural behavior, has been observed among the free-ranging Arashiyama B troop Japanese macaques near Kyoto, Japan since 1979. Conditions in which the non-purposeful handling of stones might possibly give rise to tool behavior are discussed. The progression of this behavior is traced through three phases: transmission, tradition, and transformation. During the first two phases, through social learning, the behavior was established within the group as a regular item of their behavioral repertoire and was most frequently observed after eating provisioned grain. In the third phase, observations suggest a “faddish” shift in the practice of certain behavioral sub-types between 1984 and 1985. During this period young individuals increasingly began to carry stones away from the feeding station, mixing stone manipulation with forage-feeding activities in the forest. Observations suggest under such conditions, stone handling is likely to lead to the occasional use of stone as a tool. This conclusion probably can be applied to species other thanMacaca fuscata. Consideration of the eco-setting and social learning correlates of stone handling suggests how the instrumental use of stone might emerge from a tradition of non-instrumental manipulation.     

猕猴觅食策略的地域性差异

本文通过1年连续野外观察（2015年12月至2016月11月）,对比研究了广东省内伶仃—福田国家级自然保护区野生群和台山上川岛猕猴省级自然保护区内半野生投食群的猕猴觅食策略异同,分析了食物数量和食物营养对猕猴觅食行为的影响,探讨了猕猴对生境变化的应对策略及其适应机制。研究结果表明,野生群和半野生群猕猴均偏好取食低灰分果实。另外,比起取食较少的果实,半野生群猕猴主要取食的果实具有低含水量和低蛋白等特点。全年来看,野生群猕猴偏好取食分布数量多的果实;半野生群猕猴食果频率月间波动受环境果实量影响,符合能量最大化理论。野生群和半野生群猕猴采食乔木树叶的行为均不受乔木数量的影响;而且两者采食所有生活型植被的叶的行为不受叶营养的影响。本研究表明猕猴会根据环境的食物资源数量和质量调整其觅食策略,具有对不同生活环境灵活适应的能力。     

Of stones and monkeys: testing ecological constraints on stone handling, a behavioral tradition in Japanese macaques

Japanese macaques are known to manipulate stones by displaying various seemingly functionless behavioral patterns, including carrying a stone, rubbing two stones together, or gathering several stones into a pile. This form of solitary object play called stone handling (SH) is a behavioral tradition in Japanese macaques, showing striking intertroop differences in frequency and form. Here, we evaluated two ecologically based hypotheses invoked to account for these differences. We hypothesized that the occurrence and form of SH would be affected by stone availability and the degree of terrestriality. We used standardized sampling methods to assess differences in SH and terrestriality among four captive and six free-ranging troops of Japanese macaques, and determine site-specific stone availability. Although we demonstrated that SH is almost exclusively a terrestrial activity, our comparative analyses showed that the number of stones readily available and the relative amount of time spent on the ground by the macaques were not associated with the intertroop differences in the occurrence of SH. Failure to accept the terrestriality and stone availability hypotheses suggests that the performance of SH and the motivation to engage in this activity are both more diverse and more complex than the direct links to time spent on the ground or the number of stones locally available. Other environmental influences and sociodemographic factors should be jointly considered to identify the sources of variation in SH, as a beginning to better understand the constraints on the appearance and subsequent diffusion of stone-use traditions in nonhuman primates. Am J Phys Anthropol, 2008. (c) 2007 Wiley-Liss, Inc.     

Playmate relationships among individuals of the Japanese monkey troop in arashiyama

Observations of play behavior were made on a troop of Japanese monkeys for five months. The troop consisted of 125 animals during the study period. Only 104 animals were observed playing with the troop members while the other 21 animals were never observed playing with other individuals. Two-member play was the most frequent. On the average, a monkey played with 20.7 individuals. A total of 6,068 play bouts were observed. The frequency of play appeared to be affected by age, sex, and degree of relatedness. One-year-old infant males played most with other members and the frequency of play decreased with age. Between monkeys whose disparity of age was less than two years, 5,763 bouts (95.0% of the total) were observed. Moreover, among sameaged monkeys who comprised 10.6% of the possible pair combinations, 2,739 play bouts (45.1%) were observed. Juvenile males played with same-sexed peers more than with opposite-sexed peers, whereas older juvenile females appeared to play with infants of both sexes. Individuals who were related and similarly-ranked tended to play together. There was no apparent preference for animals to play with the offspring of the highest-ranking female. Dominance rank of infnats and juveniles was primarily affected by rank of their mothers and to a lesser extent by play partners. Dominance rank of older juvenile males is more likely to be affected by play partners than females. It may be a critical time for males when they leave their natal troop and join a new troop. The timing of troop shifting by males seemed to be affected by the presence or absence of play-mates. For male Japanese monkeys, play is very important in developing social bonds. Play may act to perpetuate social bonds, enhance the chance of survival, and may contribute to their future reproductive success.     

Measuring male-female relationships during the mating season in wild Japanese macaques (Macaca fuscata yakui)

Heterosexual relationships during one mating season were examined in a wild troop of Japanese macaques (Macaca fuscata yakui) on Yakushima Island, Japan. Validation tests of putative mate choice behaviors demonstrated that female initiation and maintenance of proximity, female lookback at the male, and sexual presents to the male, were associated with increased mating. Male grooming the female was also associated with increased mating. Ten dyadic social behaviors were subject to principal components analysis to empirically define behavioral dimensions of male-female relationships. The analysis yielded four relationship dimensions: ‘Mutual Choice and Male Coercion,’ ‘Female Choice’ (two types), and ‘Mutual Choice’ Dyads tended to be characterized by more than one dimension. The results suggested that females sought matings with multiple males of various dominance ranks. Female relationships with high ranking males contained elements of male coercion and mate guarding, however, because these males attempted to inhibit females from mating with lower ranking males. The correlation between each relationship dimension and mating success depended, in part, on the dominance rank of males. Relationships involving high ranking males, which were most likely to contain elements of male coercion and mate guarding, were associated with mating success. Relationships involving low ranking males, which usually lacked such coercive elements. were less strongly correlated with mating success. These results, obtained from a wild troop, are compared to those previously obtained in captive and provisioned groups of Japanese 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.     

Leptin, body composition, adrenal and gonadal hormones among captive male baboons

Morphometric and hormonal measures were collected from 21 captive savanna baboons (Papio cynocephalus) maintained at the Tulane National Primate Research Center in order to determine age-related patterns in leptin levels over the life course as well as their relationships to body composition and adrenal and gonadal steroids. Comparison of leptin levels between peri-pubertal, adolescent, young adult, and fully mature males show lower levels among adolescent as compared with young adult males (P = 0.05 by Kruskal-Wallis ANOVA). In addition, abdominal fat varied among age groups (P = 0.003 by Kruskal-Wallis ANOVA) with the peri-pubertal animals lower than the adolescents, young adults, and prime adults. However leptin was not related to any measure of body composition, including abdominal fat, or to adrenal hormones (dehydroepiandrosterone, dehydroepiandrosterone-sulfate, and cortisol) or gonadal hormones (testosterone and estradiol). Age-related changes in leptin appear similar to those reported for captive rhesus macaques, while the failure to find an association between leptin and abdominal fat is interestingly different. These results confirm elevated levels of leptin in captive baboons compared with their wild counterparts and suggest that they result from changes in fetal development.