Bioacoustic monitoring of aggression in group-housed rhesus macaques

Many captive primate facilities house rhesus macaques in multimale-multifemale social groups in large enclosures that simulate the natural social and environmental features characteristic of the species, enhancing their reproductive performance as well as their psychological well-being, yet one of the most difficult management problems in socially housed macaques is their propensity for exhibiting spontaneous bouts of deleterious aggression. To address this management problem, an automated bioacoustic monitoring system might be developed that is capable of detecting and forecasting problematic patterns of contact aggression. To evaluate the utility of this approach, this study examined the magnitude of aggression and the co-occurrence of certain vocalization types and aggression in 10 groups of rhesus macaques. The data confirmed aggression as a significant problem in rhesus groups and indicated that certain patterns of vocalizations are indicative of the type or level of aggression. The detection and classification of these vocalization types need further research to eventually design and implement an efficacious bioacoustic system for monitoring aggression in rhesus macaques.     

Mother–infant relationships and maternal estrogen metabolites changes in macaques (<Emphasis Type="Italic">Macaca fuscata,M. mulatta</Emphasis>)

This research assessed mother–infant relationships in rhesus and Japanese macaques living in analogous captive social groups, and monitored changes in the levels of excreted estrogen metabolites during the peripartum period. Each mother–infant pair was focally observed 3 h per week during the first 12 weeks of life of newborns. Fecal samples were collected twice a week from each mother, starting 4 weeks before delivery and ending 4 weeks after delivery. Infant-directed behaviors appeared to be consistently less protective/controlling and more rejecting in rhesus macaques than in Japanese macaques. Estrogen metabolite levels during the perinatal period were, on average, 3-fold higher in Japanese macaques and showed a sharp increase during the last weeks of pregnancy only in the Japanese macaque group. Considering the ecological and behavioral similarities between Japanese and rhesus macaques, the divergence between the two species in the onset and maintenance of maternal behavior was unexpected. This was possibly linked to the difference in the overall body size and life history, and to the striking divergence in estrogen metabolite variation during the peripartum period. Group size, social relationships, and average age of individuals in the two captive groups were not clearly involved in the recorded differences in maternal behavior. Electronic Publication     

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.     

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.     

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.     

Joint Modeling of Multiple Social Networks to Elucidate Primate Social Dynamics: I. Maximum Entropy Principle and Network-Based Interactions

In a complex behavioral system, such as an animal society, the dynamics of the system as a whole represent the synergistic interaction among multiple aspects of the society. We constructed multiple single-behavior social networks for the purpose of approximating from multiple aspects a single complex behavioral system of interest: rhesus macaque society. Instead of analyzing these networks individually, we describe a new method for jointly analyzing them in order to gain comprehensive understanding about the system dynamics as a whole. This method of jointly modeling multiple networks becomes valuable analytical tool for studying the complex nature of the interaction among multiple aspects of any system. Here we develop a bottom-up, iterative modeling approach based upon the maximum entropy principle. This principle is applied to a multi-dimensional link-based distributional framework, which is derived by jointly transforming the multiple directed behavioral social network data, for extracting patterns of synergistic inter-behavioral relationships. Using a rhesus macaque group as a model system, we jointly modeled and analyzed four different social behavioral networks at two different time points (one stable and one unstable) from a rhesus macaque group housed at the California National Primate Research Center (CNPRC). We report and discuss the inter-behavioral dynamics uncovered by our joint modeling approach with respect to social stability.     

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.     

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.     

Social Relationships in Free-Ranging Male Macaca arctoides

Macaque social relationships differ greatly between species. Based on captive studies that focus mainly on females, researchers have classified stumptail macaque (Macaca arctoides) social relationships as tolerant, as indicated by a high rate of affiliation, frequent aggression, and symmetrical conflicts. To accumulate more data on male social relationships, which are relatively understudied, and to generate comparative data, we investigated male social relationships in a provisioned group of 68 free-ranging, naturally dispersing stumptail macaques in southern Thailand. We collected continuous focal animal and ad libitum data on 7 adult and 2 subadult males, recording social behavior during 283 contact hours between December 2006 and March 2007. Stumptail macaques of this population were less tolerant than predicted based on previous studies on captive groups: Rates of spatial proximity, affiliation, and aggression were low, most males directed affiliative behavior toward higher-ranking males, and conflicts were generally of low intensity and relatively asymmetrical. Thus, male stumptail macaques of the focal group appear to differ in their social style from a previous study of a captive group that mainly comprised of females. In some traits, they are even more intolerant than rhesus macaques, an intensively studied intolerant macaque species. We also compare our data on stumptail macaque males to those on other male macaques, but available data are too sparse to draw final conclusions.     

Genetic characterization of wild and captive rhesus macaques in China

The genetic structures of wild and captive rhesus macaque populations within China were compared by analyzing the mtDNA sequences of 203 captive-bred Chinese rhesus macaques with 77 GenBank sequences from wild-caught animals trapped throughout China. The genotypes of 22 microsatellites of captive Chinese rhesus macaques were also compared with those of captive Indian animals. The Chinese population is significantly differentiated from the Indian population and is more heterogeneous. Thus, compared with Indian rhesus macaques the phenotypic variance of traits with high heritability will be inflated in Chinese animals. Our data suggest that the western Chinese provinces have more subdivided populations than the eastern and southern Chinese provinces. The southern Chinese populations are the least structured and might have been more recently established. Human-mediated interbreeding among captive Chinese populations has occurred, implying that Chinese breeding strategies can influence the interpretation of biomedical research in the USA.     

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。     

Maternal Anxiety in Rhesus Macaques (Macaca mulatta)

Visual monitoring and scratching were used as behavioral indicators of maternal and social anxiety in small captive groups of rhesus macaques. Young infants were especially at risk from other group members during the first weeks of locomotion away from their mothers. Mothers received aggression from other individuals irrespective of their infants' presence or absence. The rate at which mothers scratched themselves increased significantly when their infants moved away from them and when the infants approached or were approached by individuals who frequently harassed them. The rate of maternal scratching and the rate of glancing at the infant and at other individuals when the infant was away decreased as infants grew older and became less vulnerable to harassment. In contrast, the rate of maternal scratching and visual monitoring of other individuals when the infant was in contact remained stable across the first 12 wk of lactation. The rate of maternal scratching increased when the mother-infant pair was in spatial proximity to the adult male or higher ranking adult females. Although visual monitoring and scratching showed a similar sensitivity to social variables, it is speculated that they might reflect different components of anxiety, namely, anticipation of danger and uncertainty due to motivational conflict. The results of this investigation indicate that a macaque mother's emotional reactivity to a perceived danger for herself and her infant can be measured quite accurately using the rates of visual monitoring and scratching and that the latter represent reliable tools to investigate the emotional correlates of maternal behavior in nonhuman primates.     

Early social experience affects behavioral and physiological responsiveness to stressful conditions in infant rhesus macaques (Macaca mulatta)

Studies on early development have demonstrated the profound effects of early social experience on the behavioral development and physiology of young rhesus macaques. Given these relationships, we hypothesized that rhesus macaques exposed to different nursery-rearing conditions may develop unique biobehavioral profiles. If this is true, the assessment of temperament may allow us to pinpoint successful rearing environments, thus improving the overall health of nonhuman primates that are raised in captive environments. We conducted biobehavioral assessments in order to examine differences in the development of infants raised under four different peer-rearing conditions (continuous pairing (CP), intermittent pairing, CP with partner rotation, and intermittent rotational pairing) and compared these animals with data from a mother-reared control group. Overall, continuous rotationally paired animals were most similar to mother-reared controls on most behavioral and temperament measures, suggesting that more socially complex rearing environments (greater number of social partners) favor a more active behavioral style. Cortisol profiles of mother-reared controls were similar to both CP groups, and these three groups had higher cortisol concentrations than the intermittent rotational-pairing group. In addition, intermittently paired infants displayed a significantly higher frequency of self-stroke behavior during a human intruder challenge, an abnormal behavior also known as floating limb which has been shown to be a precursor of self-biting. Overall, the data are consistent with the idea that social complexity in the nursery, as operationalized in our continuous rotational pairing, leads to a biobehavioral profile that is most similar to that of infants raised by their mothers in large, socially complex, cages.     

Effect of outbreeding on weight and growth rate of captive infant rhesus macaques

The introduction of unrelated conspecifics into captive groups of primate species is desirable to inhibit inbreeding. However, for many species, such groups increasingly represent highly inbred isolate populations that are analogous to regionally isolated populations of the same species among whom the effects of outcrossing on fitness are unknown. A study of potentially adverse effects of cross-breeding between regionally isolated populations of rhesus macaques was conducted to assess the maximum advantage or disadvantage to be expected for cross-breeding such populations of other cercopithecoid primates. For this purpose, the infant weights and rates of growth of hybrid Chinese/Indian rhesus macaques were compared to those of their nonhybrid Indian peers and to those of consanguineously inbred Indian rhesus macaques from several other captive breeding groups. Neither adverse nor advantageous effects of such hybridization were detected, suggesting that outcrossing between isolates of other cercopithecoid primates with a similar social structure and mating pattern should not affect the fitness of resulting offspring. Since levels of inbreeding are roughly inversely proportional to levels of genetic diversity within populations, such outcrossing should be intensified by zoos and other captive breeding centers to ensure the continued survival of captive species, especially those that are endangered or otherwise irreplaceable.     

Emergence of complex social networks from spatial structure and rules of thumb: a modelling approach

Individual-based computer models show that simple heuristic governing individuals’ behavior may suffice to generate complex patterns of social behavior at the group level such as those observed in animal societies. ‘GrooFiWorld’ is an example of such kind of computer models. In this model, self-organization and simple behavioral rules generate complex patterns of social behavior like those described in tolerant and intolerant societies of macaques. Social complexity results from the socio-spatial structure of the group, the nature of which is, in turn, a side-effect of intensity of aggression. The model suggests that a similar mechanism may give rise to complex social structures in macaques. It is, however, unknown if the spatial structure of the model and that of macaques are indeed similar. Here we used social networks analysis as a proxy for spatial structure of the group. Our findings show that the social networks of the model share similar qualitative features with those of macaques. As group size increases, the density and the average individual eigenvector centrality decrease and the modularity and centralization of the network increase. In social networks emerging from simulations resembling intolerant societies the density is lower, the modularity and centralization are higher, and the individuals ranking higher in the dominance hierarchy are more central than in the social networks emerging from simulations resembling egalitarian societies. Given the qualitative similarity between the social networks of the model and that of empirical data, our results suggest that the spatial structure of macaques is similar to that of the model. It seems thus plausible that, as in the model, the spatial structure combined with simple behavioral rules plays a role in the emergence of complex social networks and complex social behavior in macaques.     

CSF 5-HIAA concentration as an early screening tool for predicting significant life history outcomes in female specific-pathogen-free (SPF) rhesus macaques (Macaca mulatta) maintained in captive breeding groups

We examined relationships among cerebrospinal fluid (CSF) concentrations of the major serotonin metabolite (5-HIAA, 5-hydroxyindoleacetic acid) and significant medical and behavioral outcomes for female rhesus macaques. Based on earlier findings with males we predicted that low CSF 5-HIAA concentrations would be associated with a range of negative life history outcomes in our captive specific-pathogen-free (SPF) breeding colony. We found that the mean CSF 5-HIAA concentration among animals that died over the course of the study period was significantly lower than among animals that survived. Further examination indicated an inverse relationship between CSF 5-HIAA concentration and number of treatments for illness, further suggesting a link between serotonergic functioning and overall animal health. Examination of behavioral data indicated that individuals with low CSF 5-HIAA concentrations were more often the targets of aggressive bouts than were individuals with high CSF 5-HIAA concentrations. Finally, we found a positive relationship between CSF 5-HIAA concentration and infant survivorship. These results suggest negative life history consequences of impaired serotonergic functioning in captive female rhesus macaques, and indicate that CSF 5-HIAA concentration sampled early in life may provide a useful tool in facilitating colony management decisions concerning utilization of scarce and increasingly valuable non-human primate resources.     

Activity patterns in a captive group of Celebes black apes (Macaca nigra)

Both time of day and weather significantly influenced the behavioral activity profile of a captive group of Celebes black apes. There were significant differences when their activity profile was compared to those of stumptail macaques, pigtail macaques, sooty mangabeys and geladas observed under similar conditions. There were, nonetheless several remarkable consistencies, especially among taxonomically related forms. Significant sex differences were also noted for grooming, social interaction rates, self-directed activity, agonistic and sexual behavior. Scores were consistent with data on a second group of black apes and previously reported unusual behavioral categories were confirmed.     

Toward developing a genome-wide microsatellite marker set for linkage analysis in the rhesus macaque (Macaca mulatta): identification of 76 polymorphic markers

Linkage analysis can be problematic in humans because of the lack of large, multigenerational pedigrees and the difficulties in obtaining phenotypic data on all family members. In contrast, large, captive colonies of rhesus macaque are a potentially valuable resource for linkage studies because detailed phenotypic and genealogical data are kept, inbreeding is avoided, and DNA samples can usually be obtained. Microsatellite marker sets for genome-wide screening are available in a number of species, but not for the rhesus macaque. We tested primers to 400 human microsatellite markers from a genome-wide mapping set using DNA from nine unrelated female rhesus macaques. We found that 76 (19%) of the primers amplified a polymorphic product using the standard protocols for human DNA. The average heterozygosity of the markers in humans was 0.80, compared to 0.65 in the rhesus macaques. This study provides preliminary data, which could be used toward the development of a linkage mapping set in this species. There would be a need, however, to confirm the Mendelian inheritance of the markers.     

Effects of geographic origin on captive Macaca mulatta mitochondrial DNA variation

Partial sequences from mitochondrial (mt) 12S and 16S rRNA genes were analyzed to characterize diversity among captive rhesus macaques (Macaca mulatta) originating from various geographic regions. Several nested clades, defined by closely related haplotypes, were identified, suggesting considerable genetic subdivision, probably relics from heterogeneous origins, founder effects, and genetic drift, followed by breeding isolation. The rhesus matrilineages from India differed discretely and markedly from Chinese matrilineages; approximately 90% of the genetic heterogeneity among the combined samples of Indian and Chinese rhesus macaques studied here was due to country of origin. In addition, mtDNA sequences from macaques of China were more diverse than those from rhesus macaques of India, an outcome consistent with China's greater subspecies diversity and with nuclear genotype distributions. Otherwise, the distribution of mtDNA variation within rhesus macaques of China, and especially within those of India, exhibited far less structure and did not conform to a simple isolation-by-distance model. As the demand for genetically heterogeneous and well-characterized rhesus macaques for biomedical-based research increases, mtDNA haplotypes can be useful for genetically defining, preserving maximal levels of genetic diversity within, and confirming the geographic origin of captive breeding groups of rhesus macaques.     

Determining overweight and underweight with a new weight‐for‐height index in captive group‐housed macaques

Housing primates in naturalistic groups provides social benefits relative to solitary housing. However, food intake may vary across individuals, possibly resulting in overweight and underweight individuals. Information on relative adiposity (the amount of fat tissue relative to body weight) is needed to monitor overweight and underweight of group‐housed individuals. However, the upper and lower relative adiposity boundaries are currently only known for macaques living solitarily in small cages. We determined the best measure of relative adiposity and explored the boundaries of overweight and underweight to investigate their incidence in group‐housed adult male and female rhesus macaques and long‐tailed macaques living in spacious enclosures at the Biomedical Primate Research Centre (BPRC), the Netherlands. During yearly health checks different relative adiposity measures were obtained. For long‐tailed macaques, comparable data on founder and wild animals were also available. Weight‐for‐height indices (WHI) with height to the power of 3.0 (WHI3.0) for rhesus macaques and 2.7 (WHI2.7) for long‐tailed macaques were optimally independent of height and were highly correlated with other relative adiposity measures. The boundary for overweight was similar in group‐housed and solitary‐housed macaques. A lower boundary for underweight, based on 2% body fat similar to wild primates, gave a better estimate for underweight in group‐housed macaques. We propose that for captive group‐housed rhesus macaques relative adiposity should range between 42 and 67 (WHI3.0) and for long‐tailed macaques between 39 and 62 (WHI2.7). The majority of group‐housed macaques in this facility have a normal relative adiposity, a considerable proportion (17–23%) is overweight, and a few (0–3%) are underweight.