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.

Limiting opportunities for captive nonhuman primates (NHPs) to express species-specific social behaviors may disrupt the adaptive drive for social companionship and may lead to increases in coping behaviors and inactivity. While captive NHPs show improved welfare when moving to pair-housing from single-housing, the impact of daily separation of pair-mates, as is implemented in intermittent pair-housing, is not fully understood. We compared behavioral indices of welfare exhibited by adult female rhesus macaques (Macaca mulatta) in two conditions: (1) intermittent pair-housing, involving daily overnight separation of pair-mates, and (2) continuous pair-housing, involving little separation of pair-mates. A within-subjects study design tested two groups of females experiencing both pairing conditions in an alternate order, switching either from continuous to intermittent pair-housing, or from intermittent to continuous pair-housing. Behavioral observations, recording activity state, self-directed, abnormal, and social behaviors, were conducted at midday when all females were paired, and in the afternoon when intermittent pairs were separated. Females exhibited higher levels of inactivity and self-directed behavior when separated due to intermittent pair-housing in comparison to continuous pair-housing. In addition, intermittently paired females showed higher levels of grooming and other types of affiliation when paired, than during the same time frame when they were continuously paired. These results suggest that females in the continuous presence of a social partner experience improved levels of activity and do not need to elevate levels of behavioral coping mechanisms (e.g., self-scratching, increased affiliation) as they receive the benefits associated with social companionship consistently throughout the day. Overall, this study provides the first evidence that continuous pair-housing affords better welfare than intermittent pair-housing in adult female rhesus macaques. Pair-housing options, such as continuous pairing, that reduce reliance on behavioral coping mechanisms and promote adaptive social behavior throughout the entirety of the day should be prioritized over husbandry care scheduled for convenience.

Objectives

Cercopithicine 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 methods

To 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.

Results

In 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.

Discussion

These 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.

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.

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.

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.

Macaque species, specifically rhesus (Macaca mulatta), are the most common nonhuman primates (NHPs) used in biomedical research due to their suitability as a model of high priority diseases (e.g., HIV, obesity, cognitive aging), cost effective breeding and housing compared to most other NHPs, and close evolutionary relationship to humans. With this close evolutionary relationship, however, is a shared adaptation for a socially stimulating environment, without which both their welfare and suitability as a research model are compromised. While outdoor social group housing provides the best approximation of a social environment that matches the macaque behavioral biology in the wild, this is not always possible at all facilities, where animals may be housed indoors in small groups, in pairs, or alone. Further, animals may experience many housing changes in their lifetime depending on project needs, changes in social status, management needs, or health concerns. Here, we review the evidence for the physiological and health effects of social housing changes and the potential impacts on research outcomes for studies using macaques, particularly rhesus. We situate our review in the context of increasing regulatory pressure for research facilities to both house NHPs socially and mitigate trauma from social aggression. To meet these regulatory requirements and further refine the macaque model for research, significant advances must be made in our understanding and management of rhesus macaque social housing, particularly pair-housing since it is the most common social housing configuration for macaques while on research projects. Because most NHPs are adapted for sociality, a social context is likely important for improving repeatability, reproducibility, and external validity of primate biomedical research. Am. J. Primatol. 79:e22528, 2017. © 2016 Wiley Periodicals, Inc.

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.

Objectives

Policing 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 methods

For 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).

Results

Networks 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.

Conclusions

Our 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.

Laboratory rhesus macaques are often housed in pairs and may be temporarily or permanently separated for research, health, or management reasons. While both long-term social separations and introductions can stimulate a stress response that impacts inflammation and immune function, the effects of short-term overnight separations and whether qualities of the pair relationship mediate these effects are unknown. In this study, we investigated the effects of overnight separations on the urinary cortisol concentration of 20 differentially paired adult female rhesus macaques (Macaca mulatta) at the California National Primate Research Center. These females were initially kept in either continuous (no overnight separation) or intermittent (with overnight separation) pair-housing and then switched to the alternate pair-housing condition part way through the study. Each study subject was observed for 5 weeks, during which we collected measures of affiliative, aggressive, anxious, abnormal, and activity-state behaviors in both pair-housing conditions. Additionally, up to three urine samples were collected from each subject per week and assayed for urinary free cortisol and creatinine. Lastly, the behavioral observer scored each pair on four relationship quality attributes ("Anxious," "Tense," "Well-meshed," and "Friendly") using a seven-point scale. Data were analyzed using a generalized linear model with gamma distribution and an information theoretic approach to determine the best model set. An interaction between the intermittent pairing condition and tense pair adjective rating was in the top three models of the best model set. Dominance and rates of affiliation were also important for explaining urinary cortisol variation. Our results suggest that to prevent significant changes in HPA-axis activation in rhesus macaque females, which could have unintended effects on research outcomes, pairs with "Tense" relationships and overnight separations preventing tactile contact should be avoided.