What you have, not who you know: food-enhanced social capital and changes in social behavioural relationships in a non-human primate.

Social network position in non-human primates has far-reaching fitness consequences. Critically, social networks are both heterogeneous and dynamic, meaning an individual's current network position is likely to change due to both intrinsic and extrinsic factors. However, our understanding of the drivers of changes in social network position is largely confined to opportunistic studies. Experimental research on the consequences of in situ, controlled network perturbations is limited. Here we conducted a food-based experiment in rhesus macaques to assess whether allowing an individual the ability to provide high-quality food to her group changed her social behavioural relationships. We considered both her social network position across five behavioural networks, as well as her dominance and kin interactions. We found that gaining control over a preferential food resource had far-reaching social consequences. There was an increase in both submission and aggression centrality and changes in the socio-demographic characteristics of her agonistic interaction partners. Further, we found that her grooming balance shifted in her favour as she received more grooming than she gave. Together, these results provide a novel, preliminary insight into how in situ, experimental manipulations can modify social network position and point to broader network-level shifts in both social capital and social power.

Social stability via management of natal males in captive rhesus macaques (Macaca mulatta).

Keystone individuals are expected to disproportionately contribute to group stability. For instance, rhesus macaques (Macaca mulatta) who police conflict contribute towards stability. Not all individuals' motivations align with mechanisms of group stability. In wild systems, males typically disperse at maturity and attempt to ascend via contest competition. In a captive system, dispersal is not naturally enabled - individuals attempt to ascend in their natal groups, which can be enabled by matrilineal kin potentially destabilizing group dynamics. We relocated select high-ranking natal males from five groups and assessed group stability before and after. We quantified hierarchical metrics at the individual and group level. After removal, we found significantly higher aggression against the established hierarchy (reversals), indicative of opportunistic attempts to change the hierarchy. Mixed-sex social signaling became more hierarchical, but the strength of this effect varied. Stable structure was not uniformly reached across the groups and alpha males did not all benefit. Indiscriminate natal male removal is an unreliable solution to group instability. Careful assessment of how natal males are embedded within their group is necessary to balance individual and group welfare.

Effect of behavioural sampling methods on local and global social network metrics: a case-study of three macaque species.

Social network analysis (SNA) is a powerful, quantitative tool to measure animals' direct and indirect social connectedness in the context of social groups. However, the extent to which behavioural sampling methods influence SNA metrics remains unclear. To fill this gap, here we compare network indices of grooming, huddling, and aggression calculated from data collected from three macaque species through two sampling methods: focal animal sampling (FAS) and all-occurrences behaviour sampling (ABS). We found that measures of direct connectedness (degree centrality, and network density) were correlated between FAS and ABS for all social behaviours. Eigenvector and betweenness centralities were correlated for grooming and aggression networks across all species. By contrast, for huddling, we found a correlation only for betweenness centrality while eigenvector centralities were correlated only for the tolerant bonnet macaque but not so for the despotic rhesus macaque. Grooming and huddling network modularity and centralization were correlated between FAS and ABS for all but three of the eight groups. By contrast, for aggression network, we found a correlation for network centralization but not modularity between the sampling methodologies. We discuss how our findings provide researchers with new guidelines regarding choosing the appropriate sampling method to estimate social network metrics.

Pedigree Data from Six Rhesus Macaque (Macaca mulatta) Matrilines at the California National Primate Research Center Indicate Inbreeding and Loss of Genetic Variation.

Relatedness and kinship structure in matrilines are a potential source of social stability. The current study aimed to analyze the extant pedigrees of 6 living matrilines in different field cages to assess rates of cross-generational inbreeding and loss of genetic variation over time. All 6 matrilines showed increasing levels of inbreeding over generation time, although the rates of increase were different. The female-to-male-adult sex ratio was correlated with average matriline inbreeding levels, while the number of adult males was positively correlated with average matriline genetic diversity. Over five times more paternal half-sibs than maternal half-sibs were present because paternity had been restricted to a few males yearly. Therefore, the relatedness through the paternal lines was over five times greater than that of the maternal lines. Overall, each matriline lost low to moderate levels of genetic variation with time. The current rates of gene flow between field cages by cross-fostered infants have not stopped inbreeding within these matrilines or loss of diversity due to genetic drift. This situation probably developed because translocated animals, especially males, may not breed successfully. Only 4 of the 22 translocated individuals, all females, eventually reproduced, resulting in 13 offspring and generating an overall breeding success of 0.59 across all 6 study matrilines. However, even this low rate of reproduction by the translocated animals reduced inbreeding and kinship among matrilines and increased genetic heterogeneity in the matrilines. Based on this study, we propose several colony management strategies, including equalizing adult sex ratios to increase the effective population size in the field cages, increasing the number of cross-fostered infants, and relying more on multigenerational pedigree data to aid the alignment of genetic and behavioral management techniques.

The impact of housing on birth outcomes in breeding macaque groups across multiple research centers.

Demand for nonhuman primates in research has increased over the past several years, while nonhuman primate supply remains a challenge in the United States. Global nonhuman primate supply issues make it increasingly important to maximize domestic colony production. To explore how housing conditions across primate breeding colonies impact infant survival and animal production more broadly, we collected medical records from 7959 rhesus macaques (Macaca mulatta) and 492 pigtail macaques (Macaca nemestrina) across seven breeding facilities and used generalized mixed-effect modeling to determine prenatal and infant survival odds by housing type and group size. Infant survival odds for each housing type and group size varied for prenatal, neonatal, early infant, and late infant age groups. Odds of prenatal survival were lowest in paired indoor housing and small and medium outdoor groups. No housing type performed better than large outdoor groups for neonatal survival. Odds of early infant survival was greatest in indoor and mixed indoor/outdoor housing compared to large outdoor enclosures. Large outdoor housing was associated with higher survival odds for late infant survival compared to small and medium outdoor housing. These results may influence housing choices at macaque breeding facilities hoping to maximize infant success, although there are relative care costs, the promotion of species-typical behaviors, and infrastructure factors to also consider. Our study used an interinstitutional collaboration that allowed for the analysis of more infant macaque medical records than ever before and used the broad variations across the seven national primate research centers to make the results applicable to many other facilities housing macaques.

Impact of joint interactions with humans and social interactions with conspecifics on the risk of zooanthroponotic outbreaks among wildlife populations.

Pandemics caused by pathogens that originate in wildlife highlight the importance of understanding the behavioral ecology of disease outbreaks at human-wildlife interfaces. Specifically, the relative effects of human-wildlife and wildlife-wildlife interactions on disease outbreaks among wildlife populations in urban and peri-urban environments remain unclear. We used social network analysis and epidemiological Susceptible-Infected-Recovered models to simulate zooanthroponotic outbreaks, through wild animals' joint propensities to co-interact with humans, and their social grooming of conspecifics. On 10 groups of macaques (Macaca spp.) in peri-urban environments in Asia, we collected behavioral data using event sampling of human-macaque interactions within the same time and space, and focal sampling of macaques' social interactions with conspecifics and overall anthropogenic exposure. Model-predicted outbreak sizes were related to structural features of macaques' networks. For all three species, and for both anthropogenic (co-interactions) and social (grooming) contexts, outbreak sizes were positively correlated to the network centrality of first-infected macaques. Across host species and contexts, the above effects were stronger through macaques' human co-interaction networks than through their grooming networks, particularly for rhesus and bonnet macaques. Long-tailed macaques appeared to show intraspecific variation in these effects. Our findings suggest that among wildlife in anthropogenically-impacted environments, the structure of their aggregations around anthropogenic factors makes them more vulnerable to zooanthroponotic outbreaks than their social structure. The global features of these networks that influence disease outbreaks, and their underlying socio-ecological covariates, need further investigation. Animals that consistently interact with both humans and their conspecifics are important targets for disease control.

Measuring dominance certainty and assessing its impact on individual and societal health in a nonhuman primate model: a network approach.

The notion of dominance is ubiquitous across the animal kingdom, wherein some species/groups such relationships are strictly hierarchical and others are not. Modern approaches for measuring dominance have emerged in recent years taking advantage of increased computational power. One such technique, named Percolation and Conductance (Perc), uses both direct and indirect information about the flow of dominance relationships to generate hierarchical rank order that makes no assumptions about the linearity of these relationships. It also provides a new metric, known as 'dominance certainty', which is a complimentary measure to dominance rank that assesses the degree of ambiguity of rank relationships at the individual, dyadic and group levels. In this focused review, we will (i) describe how Perc measures dominance rank while accounting for both nonlinear hierarchical structure as well as sparsity in data-here we also provide a metric of dominance certainty estimated by Perc, which can be used to compliment the information dominance rank supplies; (ii) summarize a series of studies by our research team reflecting the importance of 'dominance certainty' on individual and societal health in large captive rhesus macaque breeding groups; and (iii) provide some concluding remarks and suggestions for future directions for dominance hierarchy research. This article is part of the theme issue 'The centennial of the pecking order: current state and future prospects for the study of dominance hierarchies'.

Sex Differences in Hierarchical Stability in a Formation of a Mixed-sex Group of Rhesus Macaques.

Forming groups of captive rhesus macaques (Macaca mulatta) is a common management practice. New formations of unfamiliar macaques can be costly, with high levels of trauma, particularly as intense aggression is used to establish a dominance hierarchy. Combining previous subgroups into one new group may be beneficial, as some individuals already have established dominance relationships. We tested this hypothesis by forming a new mixed-sex group of rhesus macaques that combined an established group of females with an established group of males. Prior to the mixed-sex group formation, both the female and male hierarchies had been stable for 3 y; after mixed-sex group formation these hierarchies were maintained by the females and were initially maintained by the males for 3 wks. However, the temporary hospitalization (due to a laceration caused by aggression) of the alpha male destabilized the male hierarchy. Age and weight then predicted male rank. Temporary hospitalizations resulted in rank changes for the males, evidenced by reversals in subordination signals. This study indicates that using established groups of familiar individuals may maintain female hierarchical stability in a mixedsex group formation, but further research is needed to understand how to maintain and predict male hierarchical stability to reduce trauma. Improved knowledge of hierarchical stability would be invaluable to managers of large rhesus macaque groups and would help improve the welfare of captive rhesus macaques.

Implementing social network analysis to understand the socioecology of wildlife co-occurrence and joint interactions with humans in anthropogenic environments.

Human population expansion into wildlife habitats has increased interest in the behavioural ecology of human-wildlife interactions. To date, however, the socioecological factors that determine whether, when or where wild animals take risks by interacting with humans and anthropogenic factors still remains unclear. We adopt a comparative approach to address this gap, using social network analysis (SNA). SNA, increasingly implemented to determine human impact on wildlife ecology, can be a powerful tool to understand how animal socioecology influences the spatiotemporal distribution of human-wildlife interactions. For 10 groups of rhesus, long-tailed and bonnet macaques (Macaca spp.) living in anthropogenically impacted environments in Asia, we collected data on human-macaque interactions, animal demographics, and macaque-macaque agonistic and affiliative social interactions. We constructed 'human co-interaction networks' based on associations between macaques that interacted with humans within the same time and spatial locations, and social networks based on macaque-macaque allogrooming behaviour, affiliative behaviours of short duration (agonistic support, lip-smacking, silent bare-teeth displays and non-sexual mounting) and proximity. Pre-network permutation tests revealed that, within all macaque groups, specific individuals jointly took risks by repeatedly, consistently co-interacting with humans within and across time and space. GLMMs revealed that macaques' tendencies to co-interact with humans was positively predicted by their tendencies to engage in short-duration affiliative interactions and tolerance of conspecifics, although the latter varied across species (bonnets>rhesus>long-tailed). Male macaques were more likely to co-interact with humans than females. Neither macaques' grooming relationships nor their dominance ranks predicted their tendencies to co-interact with humans. Our findings suggest that, in challenging anthropogenic environments, less (compared to more) time-consuming forms of affiliation, and additionally greater social tolerance in less ecologically flexible species with a shorter history of exposure to humans, may be key to animals' joint propensities to take risks to gain access to resources. For males, greater exploratory tendencies and less energetically demanding long-term life-history strategies (compared to females) may also influence such joint risk-taking. From conservation and public health perspectives, wildlife connectedness within such co-interaction networks may inform interventions to mitigate zoonosis, and move human-wildlife interactions from conflict towards coexistence.

Factors influencing the success of male introductions into groups of female rhesus macaques: Introduction technique, male characteristics and female behavior.

In captive populations of rhesus macaques, novel adult males are commonly introduced to female groups every few years to prevent inbreeding, which mimics male dispersal in wild macaque populations. However, introducing adult males is challenging because macaques are aggressive to newcomers, which can result in serious injuries. Efforts to reduce trauma risk during the introduction process and increase the probability of success are needed. Here we investigate the impact of multiple factors, including male attributes (e.g., age, weight, rank, and experience), introduction method (punctuated vs. continual exposure to females), and female behavior, on males' trauma risk and integration success. We studied eight introductions of multimale cohorts (3-7 males each; N = 36 total) into existing female groups of rhesus macaques at the Yerkes National Primate Research Center. Four cohorts were introduced using the punctuated exposure method where adult males were moved each morning from run housing to the females' indoor enclosure and returned to run housing in the afternoon, and four cohorts were introduced using the continual exposure method where adult males were moved to an introduction enclosure attached to the females' outdoor compound, allowing males to live in protected contact next to the female group continuously. Generalized linear mixed models fitted to trauma risk (e.g., latency to first trauma; total trauma count) and success or failure to integrate (i.e., continual residence within the female group for greater than 53% of days within a 28-day window after first overnight stay) showed that continual exposure to females in the introduction enclosure reduced male trauma risk and increased the likelihood of successful integration compared to punctuated exposure. Males received less trauma when they received a higher rate of grooming from females. Male attributes had no effect. These findings highlight the importance of introduction technique and female behavior in the process of males' social integration into female groups.

Monkey's Social Roles Predict Their Affective Reactivity.

Accumulating evidence demonstrates that the number of social connections an individual has predicts health and wellbeing outcomes in people and nonhuman animals. In this report, we investigate the relationship between features of an individuals' role within his social network and affective reactivity to ostensibly threatening stimuli, using a highly translatable animal model - rhesus monkeys. Features of the social network were quantified via observations of one large (0.5 acre) cage that included 83 adult monkeys. The affective reactivity profiles of twenty adult male monkeys were subsequently evaluated in two classic laboratory-based tasks of negative affective reactivity (human intruder and object responsiveness). Rhesus monkeys who had greater social status, characterized by age, higher rank, more close social partners, and who themselves have more close social partners, and who played a more central social role in their affiliative network were less reactive on both tasks. While links between social roles and social status and psychological processes have been demonstrated, these data provide new insights about the link between social status and affective processes in a tractable animal model of human health and disease.

Female social structure influences, and is influenced by, male introduction and integration success among captive rhesus macaques (Macaca mulatta).

Animal social structure is influenced by multiple socioecological factors. Of these, the links between changes to group demography through the arrival of new individuals and residents' social structure remain unclear. Across seven groups of captive rhesus macaques (Macaca mulatta), we examine how male introductions may be influenced by, and in-turn influence, aspects of female social structure. GLMMs revealed that males integrated more successfully into groups in which females showed more 'despotic' social structures, i.e., higher aggression rates, steeper dominance hierarchies, and greater rank-skew in allogrooming network connectedness. Yet during periods that followed males' social integration, females increased their social tolerance (decreased aggression and shallower hierarchies) and group cohesivity (less clustered allogrooming networks), but retained their tendencies to groom dominants. Our findings, independent of group size and matrilineal relatedness, help better understand how dispersal/immigration may influence social structure, and how assessing changes to social structure may inform macaque welfare and management.

Impact of individual demographic and social factors on human-wildlife interactions: a comparative study of three macaque species.

Despite increasing conflict at human-wildlife interfaces, there exists little research on how the attributes and behavior of individual wild animals may influence human-wildlife interactions. Adopting a comparative approach, we examined the impact of animals' life-history and social attributes on interactions between humans and (peri)urban macaques in Asia. For 10 groups of rhesus, long-tailed, and bonnet macaques, we collected social behavior, spatial data, and human-interaction data for 11-20 months on pre-identified individuals. Mixed-model analysis revealed that, across all species, males and spatially peripheral individuals interacted with humans the most, and that high-ranking individuals initiated more interactions with humans than low-rankers. Among bonnet macaques, but not rhesus or long-tailed macaques, individuals who were more well-connected in their grooming network interacted more frequently with humans than less well-connected individuals. From an evolutionary perspective, our results suggest that individuals incurring lower costs related to their life-history (males) and resource-access (high rank; strong social connections within a socially tolerant macaque species), but also higher costs on account of compromising the advantages of being in the core of their group (spatial periphery), are the most likely to take risks by interacting with humans in anthropogenic environments. From a conservation perspective, evaluating individual behavior will better inform efforts to minimize conflict-related costs and zoonotic-risk.

A multiplex centrality metric for complex social networks: sex, social status, and family structure predict multiplex centrality in rhesus macaques.

Members of a society interact using a variety of social behaviors, giving rise to a multi-faceted and complex social life. For the study of animal behavior, quantifying this complexity is critical for understanding the impact of social life on animals' health and fitness. Multilayer network approaches, where each interaction type represents a different layer of the social network, have the potential to better capture this complexity than single layer approaches. Calculating individuals' centrality within a multilayer social network can reveal keystone individuals and more fully characterize social roles. However, existing measures of multilayer centrality do not account for differences in the dynamics and functionality across interaction layers. Here we validate a new method for quantifying multiplex centrality called consensus ranking by applying this method to multiple social groups of a well-studied nonhuman primate, the rhesus macaque. Consensus ranking can suitably handle the complexities of animal social life, such as networks with different properties (sparse vs. dense) and biological meanings (competitive vs. affiliative interactions). We examined whether individuals' attributes or socio-demographic factors (sex, age, dominance rank and certainty, matriline size, rearing history) were associated with multiplex centrality. Social networks were constructed for five interaction layers (i.e., aggression, status signaling, conflict policing, grooming and huddling) for seven social groups. Consensus ranks were calculated across these five layers and analyzed with respect to individual attributes and socio-demographic factors. Generalized linear mixed models showed that consensus ranking detected known social patterns in rhesus macaques, showing that multiplex centrality was greater in high-ranking males with high certainty of rank and females from the largest families. In addition, consensus ranks also showed that females from very small families and mother-reared (compared to nursery-reared) individuals were more central, showing that consideration of multiple social domains revealed individuals whose social centrality and importance might otherwise have been missed.

Impact of anthropogenic factors on affiliative behaviors among bonnet macaques.

OBJECTIVES: In primates, allogrooming and other affiliative behaviors confer many benefits and may be influenced by many socioecological factors. Of these, the impact of anthropogenic factors remain relatively understudied. Here we ask whether interactions with humans decreased macaques' affiliative behaviors by imposing time-constraints, or increased these behaviors on account of more free-/available-time due to macaques' consumption of high-energy human foods. MATERIALS AND METHODS: In Southern India, we collected data on human-macaque and macaque-macaque interactions using focal-animal sampling on two groups of semi-urban bonnet macaques for 11 months. For each macaque within each climatic season, we calculated frequencies of human-macaque interactions, rates of monitoring human activity and foraging on anthropogenic food, dominance ranks, grooming duration, number of unique grooming partners, and frequencies of other affiliative interactions. RESULTS: We found strong evidence for time-constraints on grooming. Macaques that monitored humans more groomed for shorter durations and groomed fewer partners, independent of their group membership, sex, dominance rank, and season. However, monitoring humans had no impact on other affiliative interactions. We found no evidence for the free-time hypothesis: foraging on anthropogenic food was unrelated to grooming and other affiliation. DISCUSSION: Our results are consistent with recent findings on other urban-dwelling species/populations. Macaques in such environments may be especially reliant on other forms of affiliation that are of short duration (e.g., coalitionary support, lip-smacking) and unaffected by time-constraints. We stress on the importance of evaluating human impact on inter-individual differences in primate/wildlife behavior for conservation efforts.

Individuals in urban dwelling primate species face unequal benefits associated with living in an anthropogenic environment.

In primates, living in an anthropogenic environment can significantly improve an individual's fitness, which is likely attributed to access to anthropogenic food resources. However, in non-professionally provisioned groups, few studies have examined whether individual attributes, such as dominance rank and sex, affect primates' ability to access anthropogenic food. Here, we investigated whether rank and sex explain individual differences in the proportion of anthropogenic food consumed by macaques. We observed 319 individuals living in nine urban groups across three macaque species. We used proportion of anthropogenic food in the diet as a proxy of access to those food resources. Males and high-ranking individuals in both sexes had significantly higher proportions of anthropogenic food in their diets than other individuals. We speculate that unequal access to anthropogenic food resources further increases within-group competition, and may limit fitness benefits in an anthropogenic environment to certain individuals.

Sex differences in the impact of social status on hair cortisol concentrations in rhesus monkeys (Macaca mulatta).

Social status impacts stress in primates, but the direction of the effect differs depending on species, social style, and group stability. This complicates our ability to identify broadly applicable principles for understanding how social status impacts health and fitness. One reason for this is the fact that social status is often measured as linear dominance rank, yet social status is more complex than simply high or low rank. Additionally, most research on social status and health ignores the effects of sex and sex-specific relationships, despite known differences in disease risk, coping strategies, and opposite-sex dominance interactions between males and females in many species. We examine the influence of social status, sex, and opposite-sex interactions on hair cortisol concentrations (HCC) in a well-studied species, rhesus macaques, where the literature predicts low ranking individuals would experience more chronic stress. Animals in three captive, seminaturalistic social groups (N = 252; 71 male) were observed for 6 weeks to obtain metrics of social status (rank and dominance certainty [DC]). DC is a measure of one's fit within the hierarchy. Hair samples were collected from each subject and analyzed for HCC. Generalized linear mixed models were used to examine (a) whether rank, DC, or sex predicted HCC; (b) whether same- or opposite-sex dominance relationships differentially impacted HCC; and (c) whether aggressive interactions initiated or received could explain any observed relationships. Results indicated that DC, not rank, predicted HCC in a sex-specific manner. For males, high HCC were predicted by receiving aggression from or having high DC with other males as well as having low DC with females. For females, only high DC with males predicted high HCC. These results likely relate to sex-specific life history pattern differences in inherited versus earned rank that are tied to female philopatry and male immigration.

High rates of aggression do not predict rates of trauma in captive groups of macaques.

Socially inflicted traumas are a major concern for the management of captive groups of rhesus macaques. Rhesus macaques are the most commonly used nonhuman primate in biomedical research, and social housing is optimal for promoting psychological well-being. However, trauma is frequent due to a strong reliance on aggression to establish and maintain hierarchical relationships. We studied six captive groups of rhesus macaques (Macaca mulatta) that underwent a variety of social perturbations and explored whether rates of aggression mapped onto rates of trauma using a fine-grained analysis that divided both aggression and trauma variables into specific, behaviorally-relevant categories (e.g., severe aggression by adult males relative to lacerations). Results did not show the expected positive relationship between aggression variables and trauma variables. Instead, rates of trauma (i.e., lacerations, moderate-severe trauma, total trauma) were negatively associated with the rate of impartial interventions (i.e., an intervention directed at both targets during an ongoing conflict) during baseline periods. Additionally, rates of trauma (i.e., lacerations, punctures, moderate-severe trauma, total trauma) were negatively associated with rates of total aggression following temporary knockouts of the individuals who commonly intervene impartially (i.e., conflict policers), and punctures and moderate-severe trauma were negatively associated with rates of severe aggression by adult males following permanent knockout of a high-ranked natal male. These results suggest that under homeostatic conditions, impartial interventions serve as a mechanism to reduce socially inflicted trauma but, following social manipulations of high-ranking males, an imbalance emerges. Our results underscore the importance of developing management strategies for rhesus macaque groups that promote internal social mechanisms of social stability such as maintaining conflict policing individuals (i.e., adult males) in social groups.

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.

Affiliation and disease risk: social networks mediate gut microbial transmission among rhesus macaques.

In social animals, affiliative behaviours bring many benefits, but also costs such as disease risk. The ways in which affiliation may affect the risk of infectious agent transmission remain unclear. Moreover, studies linking variation in affiliative interactions to infectious agent incidence/diversity have speculated that disease transmission may have occurred, rather than revealing that transmission did occur. We address these gaps using the phylogenetics of commensal gut Escherichia coli to determine whether affiliative grooming and huddling social networks mediated microbial transmission among rhesus macaques. We collected behavioural and microbial data from adult macaques across a 12-week period that was split into two 6-week phases to better detect dyadic transmission. We reconstructed undirected social networks from affiliative interactions and reconstructed microbial transmission networks from the pairwise phylogenetic similarity of E. coli pulsotypes from macaques within and across adjacent sampling events. Macaque E. coli pulsotypes were more phylogenetically similar to each other than to environmental isolates, which established a premise for socially mediated transmission. Dyadic grooming and huddling frequencies strongly influenced the likelihood of E. coli transmission during the second data collection phase, but not the first. Macaques that were more central/well connected in both their grooming and huddling networks were also more central in the E. coli transmission networks. Our results confirmed that affiliative grooming and huddling behaviours mediate the transmission of gut microbes among rhesus macaques, particularly among females and high-ranking individuals. The detectability of socially mediated E. coli transmission maybe partially masked by environmental acquisition in males, or by high frequencies of interactions in captivity. Predicting the potential transmission pathways of gastrointestinal parasites and pathogens, our findings add to current knowledge of the coevolutionary relationships between affiliative behaviour and health and may be used to identify 'superspreader' individuals as potential targets for disease control strategies.