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In animal social groups, the extent to which individuals consistently win agonistic interactions and their ability to monopolize resources represent 2 core aspects of their competitive regime. However, whether these two aspects are closely correlated within groups has rarely been studied. Here, we tested the hypothesis that hierarchy steepness, which is generally used to represent power differentials between group members, predicts the variation in the distribution of fitness-related benefits (i.e. fecundity, infant survival, mating success, and feeding success) in relation to individual dominance ranks. We tested this hypothesis in primate groups using comparative phylogenetic meta-analytical techniques. Specifically, we reviewed published and unpublished studies to extract data on individual dominance ranks, their access to fitness-related benefits, and hierarchy steepness. We collected and included in our analysis a total of 153 data points, representing 27 species (including 2 chimpanzee sub-species). From these, we used 4 common methods to measure individual dominance ranks and hierarchy steepness, i.e. D ij -based normalized Davids scores, randomized Elo-ratings, and Davids scores and Elo-ratings estimated in Bayesian frameworks. We found that hierarchy steepness had no effect on the strength of the relationship between dominance rank and access to fitness-related benefits. Our results suggest that hierarchy steepness does not reflect between-group variation in the extent to which individual dominance affects the acquisition of fitness-related benefits in primates. Although the ability to win agonistic encounters is essential, we speculate that other behavioral strategies adopted by individuals may play crucial roles in resource acquisition in animal competitive regimes.

Comparative studies reliant on single personality surveys to rate wild primates are scarce yet remain critical for developing a holistic comparative understanding of personality. Differences in survey design, item exclusion, and factor selection impede cross-study comparisons. To address these challenges, we used consistently collected data to assess personality trait structures in wild rhesus (Macaca mulatta), bonnet (M. radiata), and long-tailed (M. fascicularis) macaques that varied in their degree of phylogenetic closeness, species-typical social styles, and anthropogenic exposure in urban or urban-rural environments. We administered 51-item personality surveys to familiar raters, and, after reliability and structure screenings, isolated 4-5 factor solutions among the species. Four consistent factors emerged: Confident, Sociable, Active, and Irritable/Equable. This latter factor had differential expression across species. Item composition of the Irritable/Equable factor was consistent with their anticipated differences in social styles, but confounded by cross-site anthropogenic variation. We also administered a 43-item survey confined to human-primate situations which paralleled our findings of social style variation, while also exhibiting variation that aligned with population differences in human density. Our findings indicate that macaque personality trait structures may be emergent outcomes of evolutionary and/or socioecological processes, but further research is needed to parse these processes relative contributions.

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 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.

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.

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'.

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.

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.

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.

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.

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.

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.

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.

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.

Humans and their associated anthropogenic factors may strongly affect the demographics, activity and fragmentation of wild animal populations. Yet, the degree and nature of such impact on indicators of animals’ social relationships remain largely under-investigated, despite the well-documented importance of strong social ties for an individual's health and fitness. Here, we examined whether interactions with humans may affect core aspects of social life in a primate species, by constraining the time available for individuals to engage in social interactions. Specifically, we predicted that individuals who spend more time monitoring or interacting with humans would reduce their time socializing with conspecifics (i.e. the time constraints hypothesis). Alternatively, human presence may result in increased levels of stress, leading to an increase in social behaviours that serve as a coping mechanism (i.e. the social stress hypothesis). We collected data between September 2016 and September 2017 on four groups of longtailed macaques, Macaca fascicularis, in Malaysia at two sites with differing levels of human impact. In support of the time constraints hypothesis, we found that at the site with moderate human impact, monkeys who monitored human activity more frequently engaged less often in grooming. In contrast, at the site with high human impact, we found evidence supporting the social stress hypothesis, as indicators of stress were positively associated with social interactions, although we could not link them to the presence of humans. Our results suggest that the nature of human impact on macaques’ social behaviour is dependent upon the intensity of human activity and interaction with the macaques. These findings therefore provide insights into how humans may influence individual fitness and group social structure in animals living in an anthropogenic environment. More broadly, our results may lead to a better understanding of animal behaviour in anthropogenic environments, implementing conservation and population management strategies and mitigating human–wildlife conflict.

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.

Biomedical facilities across the nation and worldwide aim to develop cost-effective methods for the reproductive management of macaque breeding groups, typically by housing macaques in large, multi-male multi-female social groups that provide monkey subjects for research as well as appropriate socialization for their psychological well-being. One of the most difficult problems in managing socially housed macaques is their propensity for deleterious aggression. From a management perspective, deleterious aggression (as opposed to less intense aggression that serves to regulate social relationships) is undoubtedly the most problematic behavior observed in group-housed macaques, which can readily escalate to the degree that it causes social instability, increases serious physical trauma leading to group dissolution, and reduces psychological well-being. Thus for both welfare and other management reasons, aggression among rhesus macaques at primate centers and facilities needs to be addressed with a more proactive approach.Management strategies need to be instituted that maximize social housing while also reducing problematic social aggression due to instability using efficacious methods for detection and prevention in the most cost effective manner. Herein we review a new proactive approach using social network analysis to assess and predict deleterious aggression in macaque groups. We discovered three major pathways leading to instability, such as unusually high rates and severity of trauma and social relocations.These pathways are linked either directly or indirectly to network structure in rhesus macaque societies. We define these pathways according to the key intrinsic and extrinsic variables (e.g., demographic, genetic or social factors) that influence network and behavioral measures of stability (see Fig. 1). They are: (1) presence of natal males, (2) matrilineal genetic fragmentation, and (3) the power structure and conflict policing behavior supported by this power structure. We discuss how these three major pathways leading to greater understanding and predictability of deleterious aggression in macaque social groups.

In group-living animals, heterogeneity in individuals' social connections may mediate the sharing of microbial infectious agents. In this regard, the genetic relatedness of individuals' commensal gut bacterium Escherichia coli may be ideal to assess the potential for pathogen transmission through animal social networks. Here we use microbial phylogenetics and population genetics approaches, as well as host social network reconstruction, to assess evidence for the contact-mediated sharing of E. coli among three groups of captively housed rhesus macaques (Macaca mulatta), at multiple organizational scales. For each group, behavioral data on grooming, huddling, and aggressive interactions collected for a six-week period were used to reconstruct social network communities via the Data Cloud Geometry (DCG) clustering algorithm. Further, an E. coli isolate was biochemically confirmed and genotypically fingerprinted from fecal swabs collected from each macaque. Population genetics approaches revealed that Group Membership, in comparison to intrinsic attributes like age, sex, and/or matriline membership of individuals, accounted for the highest proportion of variance in E. coli genotypic similarity. Social network approaches revealed that such sharing was evident at the community-level rather than the dyadic level. Specifically, although we found no links between dyadic E. coli similarity and social contact frequencies, similarity was significantly greater among macaques within the same social network communities compared to those across different communities. Moreover, tests for one of our study-groups confirmed that E. coli isolated from macaque rectal swabs were more genotypically similar to each other than they were to isolates from environmentally deposited feces. In summary, our results suggest that among frequently interacting, spatially constrained macaques with complex social relationships, microbial sharing via fecal-oral, social contact-mediated routes may depend on both individuals' direct connections and on secondary network pathways that define community structure. They lend support to the hypothesis that social network communities may act as bottlenecks to contain the spread of infectious agents, thereby encouraging disease control strategies to focus on multiple organizational scales. Future directions includeincreasing microbial sampling effort per individual to better-detect dyadic transmission events, and assessments of the co-evolutionary links between sociality, infectious agent risk, and host immune function.

ObjectivesCercopithicine primates tend to have nepotistic hierarchies characterized by predictable, kinship-based dominance. Although aggression is typically directed down the hierarchy, insubordinate aggression does occur. Insubordination is important to understand because it can precipitate social upheaval and undermine group stability; however, the factors underlying it are not well understood. We test whether key social and demographic variables predict insubordination among captive female rhesus macaques.Materials and methodsTo identify factors influencing insubordination, multivariate analyses of 10,821 dyadic conflicts among rhesus macaque females were conducted, using data from six captive groups. A segmented regression analysis was used to identify dyads with insubordination. Negative binomial regression analyses and an information theoretic approach were used to assess predictors of insubordination among dyads.ResultsIn the best models, weight difference (w = 1.0; IRR = 0.930), age (dominant: w = 1.0, IRR = 0.681; subordinate: w = 1.0, IRR = 1.069), the subordinate's total number of allies (w = 0.727, IRR = 1.060) or non-kin allies (w = 0.273, IRR = 1.165), the interaction of the dominant's kin allies and weight difference (w = 0.938, IRR = 1.046), violation of youngest ascendancy (w = 1.0; IRR = 2.727), and the subordinate's maternal support (w = 1.0; IRR = 2.928), are important predictors of insubordination.DiscussionThese results show that both intrinsic and social factors influence insubordinate behavior. This adds to evidence of the importance of intrinsic factors and flexibility in a social structure thought to be rigid and predetermined by external factors. Further, because insubordination can precipitate social overthrow, determining predictors of insubordination will shed light on mechanisms underlying stability in nepotistic societies.

Conspecific aggression in outdoor-housed rhesus macaques (Macaca mulatta) at primate research facilities is a leading source of trauma and can potentially influence animal wellbeing and research quality. Although aggression between macaques is a normal part of daily social interactions, human presence might affect the frequency of various behaviors and instigate increases in conspecific aggression. We sought to determine how and which human management events affect conspecific aggression both immediately after an event and throughout the course of a day. From June 2008 through December 2009, we recorded agonistic encounters among macaques living in 7 social groups in large outdoor field cages. Behavioral data were then synchronized with specific management events (for example, feeding, enclosure cleaning, animal catching) that occurred within or near the enclosure. By using an Information Theoretical approach, 2 generalized linear mixed models were developed to estimate the effects of human management events on 1) aggression after individual management events and 2) daily levels of aggression. Univariate analysis revealed an increase in the rate of aggression after a management event occurred. The best predictor of aggression in a cage was the type of management event that occurred. Various factors including the number of daily management events, the total time of management events, the technicians involved, reproductive season, and their interactions also showed significant associations with daily aggression levels. Our findings demonstrate that human management events are associated with an increase in conspecific aggression between rhesus macaques and thus have implications regarding how humans manage primates in research facilities.

There has been a recent surge in research on primate infectious disease ecology. Two major areas remain relatively unaddressed to date-the prevalence of enteric bacterial parasites and the role of anthropogenic environmental factors in parasite acquisition in commensally living primate populations. In this preliminary assessment, we address both these gaps by assessing the prevalence, and the role of anthropogenic factors in shaping this prevalence, of three enteric bacterial parasites-E . coli O157:H7, Salmonella sp., Shigella sp.-across populations of rhesus macaques (M. mulatta) that live commensally with humans in Dehradun, northern India. Across 10-week study period, we collected data on (1) human-macaque behavioral interactions, (2) macaque and human demographic and activity scans, and (3) macaque fecal samples from the environment at four different locations in Dehradun. Biochemical tests and morphology-based confirmations clearly established the presence of all three enteric bacterial parasites in rhesus macaques. Overall prevalence ranged from 2 to 5 %, with Shigella sp. being the most prevalent. Regression analyses linking anthropogenic factors to bacterial prevalence showed a positive association between rates of macaques eating human garbage and E. coli O157:H7 (β = 0.23, p = 0.083), but a negative association with Salmonella sp. (β = -0.17, p = 0.026). Rather, the prevalence of Salmonella sp. was positively linked to rates of macaque eating provisioned food (β = 0.0012, p = 0.058). Finally, we found no relationship between anthropogenic factors and the prevalence of Shigella sp. Our findings establish the prevalence of enteric bacterial parasites in commensal populations of primates and suggest that although anthropogenic factors are linked to bacterial prevalence, the nature of the relationships may depend on the socioecological/foraging strategies of macaques and the food sources that facilitate the environmental survival of particular types of enteric bacteria over others.

ObjectivesPolicing is a conflict-limiting mechanism observed in many primate species. It is thought to require a skewed distribution of social power for some individuals to have sufficiently high social power to stop others' fights, yet social power has not been examined in most species with policing behavior. We examined networks of subordination signals as a source of social power that permits policing behavior in rhesus macaques.Materials and methodsFor each of seven captive groups of rhesus macaques, we (a) examined the structure of subordination signal networks and used GLMs to examine the relationship between (b) pairwise dominance certainty and subordination network pathways and (c) policing frequency and social power (group-level convergence in subordination signaling pathways).ResultsNetworks of subordination signals had perfect linear transitivity, and pairs connected by both direct and indirect pathways of signals had more certain dominance relationships than pairs with no such network connection. Social power calculated using both direct and indirect network pathways showed a heavy-tailed distribution and positively predicted conflict policing.ConclusionsOur results empirically substantiate that subordination signaling is associated with greater dominance relationship certainty and further show that pairs who signal rarely (or not at all) may use information from others' signaling interactions to infer or reaffirm the relative certainty of their own relationships. We argue that the network of formal dominance relationships is central to societal stability because it is important for relationship stability and also supports the additional stabilizing mechanism of policing.

Humans live in societies full of rich and complex relationships that influence health. The ability to improve human health requires a detailed understanding of the complex interplay of biological systems that contribute to disease processes, including the mechanisms underlying the influence of social contexts on these biological systems. A longitudinal computational systems science approach provides methods uniquely suited to elucidate the mechanisms by which social systems influence health and well-being by investigating how they modulate the interplay among biological systems across the lifespan. In the present report, we argue that nonhuman primate social systems are sufficiently complex to serve as model systems allowing for the development and refinement of both analytical and theoretical frameworks linking social life to health. Ultimately, developing systems science frameworks in nonhuman primate models will speed discovery of the mechanisms that subserve the relationship between social life and human health.

In social animals, group living may impact the risk of infectious disease acquisition in two ways. On the one hand, social connectedness puts individuals at greater risk or susceptibility for acquiring enteric pathogens via contact-mediated transmission. Yet conversely, in strongly bonded societies like humans and some nonhuman primates, having close connections and strong social ties of support can also socially buffer individuals against susceptibility or transmissibility of infectious agents. Using social network analyses, we assessed the potentially competing roles of contact-mediated transmission and social buffering on the risk of infection from an enteric bacterial pathogen (Shigella flexneri) among captive groups of rhesus macaques (Macaca mulatta). Our results indicate that, within two macaque groups, individuals possessing more direct and especially indirect connections in their grooming and huddling social networks were less susceptible to infection. These results are in sharp contrast to several previous studies that indicate that increased (direct) contact-mediated transmission facilitates infectious disease transmission, including our own findings in a third macaque group in which individuals central in their huddling network and/or which initiated more fights were more likely to be infected. In summary, our findings reveal that an individual's social connections may increase or decrease its chances of acquiring infectious agents. They extend the applicability of the social buffering hypothesis, beyond just stress and immune-function-related health benefits, to the additional health outcome of infectious disease resistance. Finally, we speculate that the circumstances under which social buffering versus contact-mediated transmission may occur could depend on multiple factors, such as living condition, pathogen-specific transmission routes, and/or an overall social context such as a group's social stability.

BackgroundAlthough a wealth of literature points to the importance of social factors on health, a detailed understanding of the complex interplay between social and biological systems is lacking. Social status is one aspect of social life that is made up of multiple structural (humans: income, education; animals: mating system, dominance rank) and relational components (perceived social status, dominance interactions). In a nonhuman primate model we use novel network techniques to decouple two components of social status, dominance rank (a commonly used measure of social status in animal models) and dominance certainty (the relative certainty vs. ambiguity of an individual's status), allowing for a more complex examination of how social status impacts health.MethodsBehavioral observations were conducted on three outdoor captive groups of rhesus macaques (N = 252 subjects). Subjects' general physical health (diarrhea) was assessed twice weekly, and blood was drawn once to assess biomarkers of inflammation (interleukin-6 (IL-6), tumor necrosis factor-alpha (TNF-α), and C-reactive protein (CRP)).ResultsDominance rank alone did not fully account for the complex way that social status exerted its effect on health. Instead, dominance certainty modified the impact of rank on biomarkers of inflammation. Specifically, high-ranked animals with more ambiguous status relationships had higher levels of inflammation than low-ranked animals, whereas little effect of rank was seen for animals with more certain status relationships. The impact of status on physical health was more straightforward: individuals with more ambiguous status relationships had more frequent diarrhea; there was marginal evidence that high-ranked animals had less frequent diarrhea.DiscussionSocial status has a complex and multi-faceted impact on individual health. Our work suggests an important role of uncertainty in one's social status in status-health research. This work also suggests that in order to fully explore the mechanisms for how social life influences health, more complex metrics of social systems and their dynamics are needed.

Macaques live in close contact with humans across South and Southeast Asia, and direct interaction is frequent. Aggressive contact is a concern in many locations, particularly among populations of rhesus and longtail macaques that co-inhabit urbanized cities and towns with humans. We investigated the proximate factors influencing the occurrence of macaque aggression toward humans as well as human aggression toward macaques to determine the extent to which human behavior elicits macaque aggression and vice versa. We conducted a 3-month study of four free-ranging populations of rhesus macaques in Dehradun, India from October-December 2012, using event sampling to record all instances of human-macaque interaction (N = 3120). Our results show that while human aggression was predicted by the potential for economic losses or damage, macaque aggression was influenced by aggressive or intimidating behavior by humans as well as recent rates of conspecific aggression. Further, adult female macaques participated in aggression more frequently than expected, whereas adult and subadult males participated as frequently as expected. Our analyses demonstrate that neither human nor macaque aggression is unprovoked. Rather, both humans and macaques are responding to one another's behavior. Mitigation of human-primate conflict, and indeed other types of human-wildlife conflict in such coupled systems, will require a holistic investigation of the ways in which each participant is responding to, and consequently altering, the behavior of the other.

Social stability in group-living animals is an emergent property which arises from the interaction amongst multiple behavioral networks. However, pinpointing when a social group is at risk of collapse is difficult. We used a joint network modeling approach to examine the interdependencies between two behavioral networks, aggression and status signaling, from four stable and three unstable groups of rhesus macaques in order to identify characteristic patterns of network interdependence in stable groups that are readily distinguishable from unstable groups. Our results showed that the most prominent source of aggression-status network interdependence in stable social groups came from more frequent dyads than expected with opposite direction status-aggression (i.e. A threatens B and B signals acceptance of subordinate status). In contrast, unstable groups showed a decrease in opposite direction aggression-status dyads (but remained higher than expected) as well as more frequent than expected dyads with bidirectional aggression. These results demonstrate that not only was the stable joint relationship between aggression and status networks readily distinguishable from unstable time points, social instability manifested in at least two different ways. In sum, our joint modeling approach may prove useful in quantifying and monitoring the complex social dynamics of any wild or captive social system, as all social systems are composed of multiple interconnected networks.

What do the behavior of monkeys in captivity and the financial system have in common? The nodes in such social systems relate to each other through multiple and keystone networks, not just one network. Each network in the system has its own topology, and the interactions among the system's networks change over time. In such systems, the lead into a crisis appears to be characterized by a decoupling of the networks from the keystone network. This decoupling can also be seen in the crumbling of the keystone's power structure toward a more horizontal hierarchy. This paper develops nonparametric methods for describing the joint model of the latent architecture of interconnected networks in order to describe this process of decoupling, and hence provide an early warning system of an impending crisis.

The signaling context has been found to change the meaning of the silent bared-teeth display (SBT) in pigtail macaques (Macaca nemestrina) such that the SBT in apparently peaceful contexts communicates subordination, a long-term pattern of behavior, whereas in conflict contexts it communicates immediate submission (PNAS, 104: 1581-1586). However, the context dependent nature of the SBT has not yet been explored in other species. We investigated SBT usage with respect to grooming, severe aggression, and signaler-receiver sex, rank difference, and body size in seven captive groups of rhesus macaques. Peaceful SBTs were given most often to male receivers by male and female signalers whereas conflict SBTs were given to both male and female receivers primarily by female signalers. Male signalers rarely gave SBTs (peaceful or conflict) to female receivers. Unlike pigtail macaques, peaceful SBTs in rhesus were often accompanied by withdrawal behavior (referred to as peaceful SBT-leave), which influenced grooming, but not aggression, at the dyadic level. Severe aggression was less frequent among dyads using peaceful SBTs (regardless of withdrawal behavior) than those using conflict SBTs. In contrast, grooming was more frequent among dyads using peaceful SBT-stay signals than those using peaceful SBT-leave signals or conflict SBTs. In total, our results indicate that peaceful SBTs are a functionally different signal from conflict SBTs in rhesus macaques.

In any scientific field there are thematic changes over time as new technologies and methods of investigation are developed and accumulated knowledge drives new research directions.  The current study examines how themes in the investigation of social behavior and health have changed over the last 20 years.  Literature searches were performed to identify articles published between 1993-2012 that investigate the intersection between social behavior and health in mammals.  Results identify the top journals that publish articles in this field and describe trends in how sub-divisions in social behavior (e.g. aggression or dominance) and health (e.g. immunity or brain chemicals) have changed over the last 20 years.  Our results suggest a dramatic increase in publications on the intersection between social behavior and health over this time span.  Major categories of study include relationships between general social behavior or social stress and health outcomes relating to stress responses, endocrinology, and the brain.

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. [ABSTRACT FROM AUTHOR]

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.

Studies of prosocial policing in nonhuman societies traditionally focus on impartial interventions because of an underlying assumption that partial support implies a direct benefit to the intervener, thereby negating the potential for being prosocial in maintaining social stability for the benefit of the group. However, certain types of partial interventions have significant potential to be prosocial in controlling conflict, e.g. support of non-kin subordinates. Here, we propose a policing support hypothesis that some types of agonistic support serve a prosocial policing function that maintains group stability. Using seven large captive groups of rhesus macaques, we investigated the relationship between intervention type and group-level costs and benefits (rates of trauma, severe aggression, social relocation) and individual level costs and benefits (preferential sex-dyad targeting, dominance ambiguity reduction, access to mates, and return aggression). Our results show that impartial interventions and support of subordinate non-kin represent prosocial policing as both (1) were negatively associated with group-level rates of trauma and severe aggression, respectively, (2) showed no potential to confer individual dominance benefits, (3) when performed outside the mating season, they did not increase chances of mating with the beneficiary, and (4) were low-cost for the highest-ranking interveners. We recommend expanding the definition of 'policing' in nonhumans to include these 'policing support interventions'.

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.

The persistence of biological systems requires evolved mechanisms which promote stability. Cohesive primate social groups are one example of stable biological systems, which persist in spite of regular conflict. We suggest that genetic relatedness and its associated kinship structure are a potential source of stability in primate social groups as kinship structure is an important organizing principle in many animal societies. We investigated the effect of average genetic relatedness per matrilineal family on the stability of matrilineal grooming and agonistic interactions in 48 matrilines from seven captive groups of rhesus macaques. Matrilines with low average genetic relatedness show increased family-level instability such as: more sub-grouping in their matrilineal groom network, more frequent fighting with kin, and higher rates of wounding. Family-level instability in multiple matrilines within a group is further associated with group-level instability such as increased wounding. Stability appears to arise from the presence of clear matrilineal structure in the rhesus macaque group hierarchy, which is derived from cohesion among kin in their affiliative and agonistic interactions with each other. We conclude that genetic relatedness and kinship structure are an important source of group stability in animal societies, particularly when dominance and/or affilative interactions are typically governed by kinship.

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. © 2011 McCowan et al.