Organization of Group Members at Departure Is Driven by Social Structure in Macaca

Researchers have often explained order of progression of group members during joint movement in terms of the influence of ecological pressures but rarely that of social constraints. We studied the order of joining by group members to a movement in semifree-ranging macaques with contrasting social systems: 1 group of Tonkean macaques (Macaca tonkeana) and 1 group of rhesus macaques (M. mulatta). We used network metrics to understand roles and associations among individuals. The way the macaques joined a movement reflected the social differences between the species in terms of dominance and kinship. Old and dominant male rhesus macaques were more often at the front of the movement, contrary to the Tonkean macaques, which exhibited no specific order. Moreover, rhesus macaques preferred to join high-ranking or related individuals, whereas Tonkean macaques based associations during joining mostly on sexual relationships with a subgroup of peripheral males.     

Social Structure Affects Initiations of Group Movements but Not Recruitment Success in Japanese Macaques (<Emphasis Type="Italic">Macaca fuscata</Emphasis>)

Research on collective movements has often focused on the sociodemographic parameters explaining the success of some individuals as leaders or initiators of collective movements. Several of these studies have shown the influence of social structure, through kinship and affiliative relationships, on the organization of collective movements. However, these studies have been conducted on semi-free-ranging groups of macaques that were not faced with a natural environment and its constraints. In the socially intolerant rhesus macaque (Macaca mulatta) the success of an initiator correlates with its hierarchical rank, the most dominant individuals being the most successful. We investigated the collective movements of another socially intolerant macaque species, Japanese macaques, in the wild, to assess whether the social structure was still a determinant factor under natural conditions. In line with previous studies of macaques, we found that social structure drove the organization of collective movements. More dominant individuals initiated more collective movements. However, dominance did not affect the success of an initiation, i.e., the number of individuals joining. In addition, kinship strongly constrained the associations observed in females during collective movements. These results reflect the social structure of Japanese macaques, in which strong power asymmetry and kinship relationships constrain the majority of interactions between individuals within the group. Moreover, these results are similar to those observed in semi-free-ranging rhesus macaques and support the hypothesis of an effect of social determinants on collective movements of primates even under natural conditions.     

Shared or unshared consensus decision in macaques?

Members of a social group have to make collective decisions in order to synchronise their activities. In a shared consensus decision, all group members can take part in the decision whereas in an unshared consensus decision, one individual, usually a dominant member of the group, takes the decision for the rest of the group. It has been suggested that the type of decision-making of a species could be influenced by its social style. To investigate this further, we studied collective movements in two species with opposed social systems, the Tonkean macaque (Macaca tonkeana) and the rhesus macaque (Macaca mulatta). From our results, it appears that the decision to move is the result of the choices and actions of several individuals in both groups. However, this consensus decision involved nearly all group members in Tonkean macaques whereas dominant and old individuals took a prominent role in rhesus macaques. Thus, we suggest that Tonkean macaques display equally shared consensus decisions to move, whereas in the same context rhesus macaque exhibit partially shared consensus decisions. Such a difference in making a collective decision might be linked to the different social systems of the two studied species.     

三种笼养灵长类活动时间分配的比较研究

采用焦点动物法和连续记录法对3种笼养灵长类活动时间分配进行比较研究。结果表明,川金丝猴Rhi-nopithecus roxellanae和熊猴Macaca assamensis用于休息的时间多于猕猴Macaca mulatta,移动时间则相反;川金丝猴和猕猴用于理毛的时间多于熊猴。不同性别年龄组之间的活动时间分配有差异,主要表现在川金丝猴母亲用于理毛的时间明显多于成年儿子,用于玩耍的时间则相反;猕猴成年雄性的移动时间和理毛时间多于成年雌性,玩耍时间则少于成年雌性;熊猴成年雌性的移动时间多于成年雄性,与成年个体相比,幼体花更多的时间用于玩耍,而相应的减少了其休息时间。     

Coat condition, housing condition and measurement of faecal cortisol metabolites--a non-invasive study about alopecia in captive rhesus macaques (Macaca mulatta)

BACKGROUND: Previous studies have characterized alopecia in captive rhesus macaques (Macaca mulatta) by a mixed partial to complete alopecia in a bilateral symmetric pattern. METHODS: In this study, coat condition assessments were related to exogenous and endogenous factors in captive rhesus macaques under different housing conditions in order to identify disturbances in environmental factors controlling or influencing hair growth. Additionally, the degree of alopecia was investigated in relation to adrenal endocrine function as an indicator of social stress using faecal glucocorticoid measurements. RESULTS: Hair loss was found to vary with season and sex, was most pronounced in adult females during the winter and spring months. Generally, infants were not affected, but alopecia developed during adolescence. However, the housing system, available enclosure space and variations in group size and composition also appeared to influence coat condition. Levels of immunoreactive cortisol metabolites (11-oxoetiocholanolone) in faeces were significantly negatively correlated with alopecia, suggesting a relationship between hypothalamic-pituitary-adrenal (HPA) axis activity and hair loss in captive rhesus macaques. CONCLUSIONS: Although the present study demonstrates the influence of the HPA axis on coat condition, it is not known if hair loss is caused by abnormal behaviour or hormonal imbalances of the HPA axis itself. Our data suggest that alopecia in rhesus macaques is a highly complex multicausal disorder.     

Ranking network of a captive rhesus macaque society: a sophisticated corporative kingdom

We develop a three-step computing approach to explore a hierarchical ranking network for a society of captive rhesus macaques. The computed network is sufficiently informative to address the question: Is the ranking network for a rhesus macaque society more like a kingdom or a corporation? Our computations are based on a three-step approach. These steps are devised to deal with the tremendous challenges stemming from the transitivity of dominance as a necessary constraint on the ranking relations among all individual macaques, and the very high sampling heterogeneity in the behavioral conflict data. The first step simultaneously infers the ranking potentials among all network members, which requires accommodation of heterogeneous measurement error inherent in behavioral data. Our second step estimates the social rank for all individuals by minimizing the network-wide errors in the ranking potentials. The third step provides a way to compute confidence bounds for selected empirical features in the social ranking. We apply this approach to two sets of conflict data pertaining to two captive societies of adult rhesus macaques. The resultant ranking network for each society is found to be a sophisticated mixture of both a kingdom and a corporation. Also, for validation purposes, we reanalyze conflict data from twenty longhorn sheep and demonstrate that our three-step approach is capable of correctly computing a ranking network by eliminating all ranking error.     

中国猕猴生态学研究进展

中国的灵长类学研究始于19世纪中期之后,而兴盛于20世纪80年代至今。猕猴（Macaca mulatta）是世界及中国分布最为广泛的一种非人灵长类动物,在中国境内分布于17个省（市、区）,已被列为国家二级重点保护野生动物。迄今为止,学者们已对猕猴进行了包括地理分布、种群动态、食性、社会生态、保护生态等多方面的研究。本文拟对国内有关猕猴生态学方面的研究工作进行回顾与综述,以期通过对以往工作的汇总,梳理关于猕猴的研究线索与动态,并对今后的研究有所启示。     

Network stability is a balancing act of personality, power, and conflict dynamics in rhesus macaque societies

Stability in biological systems requires evolved mechanisms that promote robustness. Cohesive primate social groups represent one example of a stable biological system, which persist in spite of frequent conflict. Multiple sources of stability likely exist for any biological system and such robustness, or lack thereof, should be reflected and thus detectable in the group's network structure, and likely at multiple levels. Here we show how network structure and group stability are linked to the fundamental characteristics of the individual agents in groups and to the environmental and social contexts in which these individuals interact. Both internal factors (e.g., personality, sex) and external factors (e.g., rank dynamics, sex ratio) were considered from the level of the individual to that of the group to examine the effects of network structure on group stability in a nonhuman primate species. The results yielded three main findings. First, successful third-party intervention behavior is a mechanism of group stability in rhesus macaques in that successful interventions resulted in less wounding in social groups. Second, personality is the primary factor that determines which individuals perform the role of key intervener, via its effect on social power and dominance discrepancy. Finally, individuals with high social power are not only key interveners but also key players in grooming networks and receive reconciliations from a higher diversity of individuals. The results from this study provide sound evidence that individual and group characteristics such as personality and sex ratio influence network structures such as patterns of reconciliation, grooming and conflict intervention that are indicators of network robustness and consequent health and well-being in rhesus macaque societies. Utilizing this network approach has provided greater insight into how behavioral and social processes influence social stability in nonhuman primate groups.     

Stability and Durability of Intra- and Intersex Social Bonds of Captive Rhesus Macaques (Macaca mulatta)

Many social species maintain differentiated relationships with their group members. These social bonds may reflect short-term interactions satisfying immediate needs. Alternatively, individuals of some species may entertain stable and valuable bonds that last much longer than opportunistic interactions would predict. This claim is supported by recent research that revealed clear fitness benefits for long-lasting social bonds. Here, we investigated the stability and equitability of social relationships in captive rhesus macaques, measured using their proximity and grooming patterns over a 3-yr period. We show that, in general, proximity patterns of the whole group were stable over 3 yr. More specifically, each individual’s top two nonkin within and between sex relationships based on proximity were relatively stable and some of these relationships lasted the full 3 yr. Female grooming relationships within and between sex were also stable over 3 yr. Moreover, strong social bonds in females were not based on age similarity and were not sex specific, suggesting that a general underlying mechanism of social bonding in female rhesus macaques. In contrast, patterns of male grooming of other males and of females were relatively unstable and male social bonds were less equitable than those of females. The differences in stability of the relationships between the sexes may reflect the dispersal pattern of rhesus macaques, although we have limited data on non-natal males in our study. With these data we add to a growing body of literature describing the value and durability of relationships among primates and other species.     

Increased produce enrichment reduces trauma in socially‐housed captive rhesus macaques (Macaca mulatta)

Due to primate adaptations for sociality, captive rhesus macaques have optimal welfare and utility as a biomedical model when they can be maintained in outdoor social groups. As a despotic species; however, aggression can result in costly injuries and may result in temporary or permanent removal of specific individuals from social housing. Enrichment items, such as toys, climbing structures, and foraging material, are employed to keep captive animals occupied. We hypothesized that produce enrichment that requires more processing to extract may reduce socially‐derived injuries by keeping animals occupied. We tested the effects of additional weekly produce (corn‐in‐husk, whole melon, or whole squash) on trauma incidence in an outdoor social group of rhesus macaques across two distinct seasons (mating and birthing seasons) at the California National Primate Research Center. Aggression and status behavioral data, food resource use and proximity, and trauma incidence were collected over two 16‐week periods, with eight control and treatment conditions alternating biweekly. Mixed‐effects regression modeling was used to determine the best predictors of trauma risk and severe aggression at the group level and at an individual level. We found that food resource use was an important predictor of trauma risk at both group and individual levels; greater use of food resources reduced trauma risk. Produce enrichment did not; however, reduce severe aggression. We suggest that other captive social groups of rhesus macaques with high levels of trauma may benefit from supplemental produce enrichment that increases animal engagement with food resources.     

Social Interactions through the Eyes of Macaques and Humans

Group-living primates frequently interact with each other to maintain social bonds as well as to compete for valuable resources. Observing such social interactions between group members provides individuals with essential information (e.g. on the fighting ability or altruistic attitude of group companions) to guide their social tactics and choice of social partners. This process requires individuals to selectively attend to the most informative content within a social scene. It is unclear how non-human primates allocate attention to social interactions in different contexts, and whether they share similar patterns of social attention to humans. Here we compared the gaze behaviour of rhesus macaques and humans when free-viewing the same set of naturalistic images. The images contained positive or negative social interactions between two conspecifics of different phylogenetic distance from the observer; i.e. affiliation or aggression exchanged by two humans, rhesus macaques, Barbary macaques, baboons or lions. Monkeys directed a variable amount of gaze at the two conspecific individuals in the images according to their roles in the interaction (i.e. giver or receiver of affiliation/aggression). Their gaze distribution to non-conspecific individuals was systematically varied according to the viewed species and the nature of interactions, suggesting a contribution of both prior experience and innate bias in guiding social attention. Furthermore, the monkeys’ gaze behavior was qualitatively similar to that of humans, especially when viewing negative interactions. Detailed analysis revealed that both species directed more gaze at the face than the body region when inspecting individuals, and attended more to the body region in negative than in positive social interactions. Our study suggests that monkeys and humans share a similar pattern of role-sensitive, species- and context-dependent social attention, implying a homologous cognitive mechanism of social attention between rhesus macaques and humans.     

人工投食行为对非人灵长类社会生态的影响

近年来,国内开展了对几种非人灵长类投食群的研究。借鉴日本猴(Macaca fuscata)、恒河猴(M.mulatta)和黑猩猩(Pan troglodytes)长期积累的研究经验,有利于我们减少人工投食对非人灵长类带来的不利影响,也有利于推动国内非人灵长类社会生态学的深入研究。本文通过比较这三种灵长类野生群和投食群之间的差异,量化地分析了人工投食对灵长类动物社会生态学方面的影响。结果表明在社会行为方面,人工投食会导致灵长类动物的聚集、增加争斗频率、改变个体间等级关系、延缓分群现象、影响活动域和增加新兴行为。在种群数量方面,人工投食会缩短雌性性成熟时间、增加出生率和婴猴存活率、减少成年猴死亡率。而人工投食对雄性性成熟、出生间隔等方面的影响仍需要进一步考证。最后我们讨论了人工投食行为的利弊,并建议应谨慎和妥善地实施人工投食,和对非人灵长类投食群进行合理的监管。     

Cortisol responses to immobilization with Telazol or ketamine in baboons (Papio cynocephalus/anubis) and rhesus macaques (Macaca mulatta)

Little is known about the influence of Telazol on cortisol or of anesthetic agents on immunological measures, and reports of ketamine's effect on cortisol are inconsistent. We measured effects of Telazol, ketamine and blood sampling on cortisol in male rhesus macaques and male savannah baboons. We also obtained leukocyte counts in the macaques. In macaques, Telazol reduced cortisol in the morning but not in the afternoon; ketamine had no effect on cortisol in these animals. In baboons, cortisol changed little post-Telazol but increased post-ketamine. In macaques, lymphocyte numbers decreased following afternoon injection of Telazol, ketamine or saline. The injection and blood sampling process increased cortisol levels in monkeys not trained to extend an arm but exerted no effect on cortisol in trained macaques. Thus, the animals' physiological responses to blood sampling and immobilization are influenced by such variables as anesthetic agent, species, time of day, and familiarity with the blood sampling process.     

Temperament in Rhesus,Long‐Tailed,and Pigtailed Macaques Varies by Species and Sex

Temperament differs among individuals both within and between species. Evidence suggests that differences in temperament of group members may parallel differences in social behavior among groups or between species. Here, we compared temperament between three closely related species of monkey—rhesus (Macaca mulatta), long‐tailed (M. fascicularis), and pigtailed (M. nemestrina) macaques—using cage‐front behavioral observations of individually housed monkeys at a National Primate Research Center. Frequencies of 12 behaviors in 899 subjects were analyzed using a principal components analysis to identify temperament components. The analysis identified four components, which we interpreted as Sociability toward humans, Cautiousness, Aggressiveness, and Fearfulness. Species and sexes differed in their average scores on these components, even after controlling for differences in age and early‐life experiences. Our results suggest that rhesus macaques are especially aggressive and unsociable toward humans, long‐tailed macaques are more cautious and fearful, and pigtailed macaques are more sociable toward humans and less aggressive than the other species. Pigtailed males were notably more sociable than any other group. The differences observed are consistent with reported variation in these species’ social behaviors, as rhesus macaques generally engage in more social aggression and pigtailed macaques engage in more male–male affiliative behaviors. Differences in predation risks are among the socioecological factors that might make these species‐typical behaviors adaptive. Our results suggest that adaptive species‐level social differences may be encoded in individual‐level temperaments, which are manifested even outside of a social context. Am. J. Primatol. 75:303‐313, 2013. © 2012 Wiley Periodicals, Inc.     

Rhesus macaque (Macaca mulatta) group formation and housing: wounding and reproduction in a specific pathogen free (SPF) colony.

In the present report, we examined the effects of group formation strategy and corral design on wounding and reproduction rates in rhesus macaques. Specifically, we examined group formation using a staged strategy, in which small groups of animals were introduced incrementally over a period of weeks, and a rapid formation strategy, in which all animals were introduced in 1 day. We also examined group formation using a divided corral design that facilitated visual and social separation of individuals, and an undivided corral design that did not facilitate visual or social separation. Dependent measures were wounding and reproductive rates over each of the 2 years that followed group formation. Results indicate that incrementally releasing subgroups of animals, and using a corral design that provides for visual and social separation of individuals, are effective strategies for reducing rates of traumatic wounding when forming multimale-multifemale rhesus macaque breeding groups. However, it must be noted that differences in formation strategy and corral design did not lead to higher reproductive rates. We conclude that incrementally releasing animals in hierarchical subgroups, and using a divided vs. undivided housing design, reduced intra-group wounding and associated demands on veterinary and animal management resources following formation of rhesus macaque breeding groups.     

The effects of two novel objects on the behavior of singly caged adult rhesus macaques.

Six female and six male adult rhesus macaques were given sticks and nylon balls as an attempt at simple cage enrichment. A latin square design was used to compare behavior during separate 4-week periods with each object and during a control period with no object. Frequency and duration of 15 different behaviors were recorded. Resting was the most common activity which decreased slightly in duration when the stick or nylon ball was present (P less than 0.02). The mean duration of stick use was longer than that of the nylon ball (P less than 0.01). No other behaviors changed significantly, including the frequency of abnormal behaviors such as self-abuse, stereotypic acts, and bizarre postures. Generally, these objects were used infrequently and led to few changes in the behavior of singly-caged adult rhesus macaques. However, they did appear to stimulate activity for some individuals.     

Impaired reconciliation in rhesus macaques with a history of early weaning and disturbed socialization

An attempt had been made to create five social groups from rhesus macaques with a history of early separation from their mothers, early weaning and hand feeding and, in most cases, previous housing in single cages. We investigated the exchange of affiliative behaviours after an aggressive encounter and selective attraction to the former opponent, a phenomenon previously well described in rhesus monkeys and called reconciliation. Evidence for reconciliation was only found in one of the five groups studied (corrected conciliatory tendency=13%). This group consisted of younger animals that had, at least temporarily, been living together after separation from their mothers. In the other groups studied, containing animals with a varied background, aggressive interactions were not followed by affiliative behaviours or attraction between former opponents. Our results indicate that the use of reconciliatory behaviours in adult monkeys is dependent upon social training. Lack of functional reconciliation might be one of the explanations to the severe and uncontrolled aggression previously found in groups of rhesus macaques created from animals with disturbed early socialization.     

基于团抱行为的太行山猕猴社会联属

社会联属是指一些社会性动物社群内由于不同年龄、性别组的个体的社会角色与等级地位存在明显差异,在个体间形成的复杂的支配-从属关系,而这种支配-从属关系在不同的物种有着各自独特的模式(Clutton-Brock,1974)。了解社群内个体通过亲缘、非亲缘联盟、婚配、竞争而建立的支配-从属关系,是进一步开展社群内个体等级与资源竞争、互惠利益、母系投入策略等诸多研究的前提,     

Changes in social structure and interactions after the introduction of a second group in a free-ranging troop of stumptail macaques (Macaca arctoides): Social relations II

Data on the social changes that occurred after the release of 12 additional stumptails into a free-ranging group are reported here. In spite of the fact that the members of the two groups had known each other for years, that genealogical relatives were re-united and that there were no limitations exerted by spatial conditions and social density, the release produced dramatic increments in aggressive and other social interactions. The resident group's alpha male was killed by two newcomer males, a restructuring of the dominance order took place, and the adult females were found to be important individuals in the re-establishment of stability. Comparisons with group formation and re-introduction experiments conducted in captive rhesus and pigtail macaques were carried out. Research supported by grants from the Behavioral Science Foundation (U. S.), NSF No. GB-42235 and Behavioral Science Foundation.     

Whole-genome sequencing and analysis of the Malaysian cynomolgus macaque (Macaca fascicularis) genome

ABSTRACT: BACKGROUND: The genetic background of the cynomolgus macaque (Macaca fascicularis) is made complex by the high genetic diversity, population structure, and gene introgression from the closely related rhesus macaque (Macaca mulatta). Herein we report the whole-genome sequence of a Malaysian cynomolgus macaque male with more than 40-fold coverage, which was determined using a resequencing method based on the Indian rhesus macaque genome. RESULTS: We identified approximately 9.7 million single nucleotide variants (SNVs) between the Malaysian cynomolgus and the Indian rhesus macaque genomes. Compared with humans, a smaller nonsynonymous/synonymous SNV ratio in the cynomolgus macaque suggests more effective removal of slightly deleterious mutations. Comparison of two cynomolgus (Malaysian and Vietnamese) and two rhesus (Indian and Chinese) macaque genomes, including previously published macaque genomes, suggests that Indochinese cynomolgus macaques have been more affected by gene introgression from rhesus macaques. We further identified 60 nonsynonymous SNVs that completely differentiated the cynomolgus and rhesus macaque genomes, and that could be important candidate variants for determining species-specific responses to drugs and pathogens. The demographic inference using the genome sequence data revealed that Malaysian cynomolgus macaques have experienced at least three population bottlenecks. CONCLUSIONS: This list of whole-genome SNVs will be useful for many future applications, such as an array-based genotyping system for macaque individuals. High-quality whole-genome sequencing of the cynomolgus macaque genome may aid studies on finding genetic differences that are responsible for phenotypic diversity in macaques and may help control genetic backgrounds among individuals.