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.

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.

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'.

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.

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.

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.

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.

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.

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.

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.