Captive Groups Of Rhesus Macaques Research Articles

Factors determining male introduction success and long-term stability in captive rhesus macaques.

The entrance of new males into non-human primate groups bears high social risk, yet migration is necessary to prevent inbreeding. Males are not always accepted in their new group. In the wild, males may increase the likelihood of successful group entry by choosing a new group based on their own and the group’s characteristics. Understanding whether these characteristics also determine a male’s ability to enter captive groups is crucial to improve introduction management. This study aims to identify which factors determine male introduction success (i.e. male stays in the group for at least 4 weeks) and long-term stability (i.e. the male does not cause considerable behavioural problems after success) after male introductions in captive groups of rhesus macaques (Macaca mulatta), creating one-male groups. We studied 64 male introductions at the breeding colony of the Biomedical Primate Research Centre in Rijswijk, The Netherlands. 49 (77%) introductions were successful, with the male obtaining a long-term stable social position in the group in 38 (59%) introductions. Introductions of males that reached at least prime age, into groups with more adult females, but without pregnant females were most successful. Moreover, long-term stability was highest when males were heavier, were at least 3.5 years old when they were first removed from their natal group, and groups had few matrilines and no pregnant females were present. Males should be introduced at the time they would naturally immigrate, when they are strongest. Moreover, groups should consist of few large matrilines, as observed in the wild, with philoatric females and males that are removed at natural age. Our study highlights the importance of composing naturalistic groups and mimicking natural migration patterns to maintain long-term stable breeding groups in captivity.

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

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

Female social behaviour during three male introductions in captive groups of rhesus macaques

Introductions of new males into captive primate groups are often necessary to prevent inbreeding, but also bear high social risks. To minimize these risks, it is crucial to understand the social behaviour accompanying male introductions. While the behaviour of new males is generally understood, information on resident female behaviour during introductions is lacking. We studied female behaviour towards the new male during introductions of three adult male rhesus macaques (Macaca mulatta)—each into a different captive group. All three males were successfully introduced; respectively 100%, 92%, and 83% of the females tolerated the male as a group-member at the end of the introductions. Older females started tolerating the male significantly faster than younger females, while no additional effect of female dominance rank, fertility, or the number of female coalitionary partners on timing of tolerance was found. During the course of the integration, female aggression and submission towards the male, and male mating access decreased, while female affiliation towards the male increased. The increase of female tolerance and the changes in social behaviour were similar between the introductions, indicating a general pattern in female behaviour, although some variation in effect size and significance level was observed. Based on these results, we suggest that low female submission levels towards an introduced male may constitute a criterion to assess the risk of leaving the male in the group full-time. Moreover, low female aggression levels at the end of the introduction may signal long-term group stability. Overall, we conclude that female behaviour can provide valuable information about the male introduction process and should not be overlooked.

Social buffering and contact transmission: network connections have beneficial and detrimental effects on Shigella infection risk among captive rhesus macaques.

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.

Decoupling social status and status certainty effects on health in macaques: a network approach.

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.

Social power, conflict policing, and the role of subordination signals in rhesus macaque society.

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. 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). 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. 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.

Policing in nonhuman primates: partial interventions serve a prosocial conflict management function in rhesus macaques.

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’.

Signaling context modulates social function of silent bared-teeth displays in rhesus macaques (Macaca mulatta).

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.

Factors affecting aggression among females in captive groups of rhesus macaques (Macaca mulatta)

Captive groups of primates often exhibit higher rates of aggression than wild, free-ranging groups. It is important to determine which factors influence aggression in captivity because aggression, particularly intense aggression, can be harmful to animal health and well-being. In this study, we investigated the effect of ground substrate as well as season, rank, age, and group size on rates of agonistic interactions per female in seven captive groups of rhesus macaques (n = 70 females, 1,723 focal samples) at the California National Primate Research Center. Agonistic interactions were divided into three categories: displacements, mild aggression, and intense aggression. Females living in enclosures with gravel substrate were 1.7 times more likely to be involved in intense aggression (e.g. chases and physical contact) than females living in enclosures with grass (Poisson regression model: P < 0.001). High-ranking females were at least 1.3 times more likely to be involved in mild (e.g. threats and lunges) aggression than lower-ranking females (low rank: P = 0.03; mid rank: P = 0.001). Females of all ranks were 1.5-1.9 times more likely to be involved in both intense and mild aggression during the breeding season than other seasons. Age and group size did not affect rates of mild or intense aggression. These findings indicate that although some aggression appears to be natural and unavoidable, i.e. aggression during the breeding season, the well-being of captive macaques can be improved by developing grass substrate in outdoor enclosures.

Detecting instability in animal social networks: genetic fragmentation is associated with social instability in rhesus macaques.

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.

Ground substrate affects activity budgets and hair loss in outdoor captive groups of rhesus macaques (Macaca mulatta)

How the captive environment influences the behavior of animals is relevant to the well-being of captive animals. Captivity diverges from the natural environment in many ways, and one goal of enrichment practices is to encourage species-typical behavior in these unnatural environments. This study investigated the influence of grass vs. gravel substrate on activity budgets and degree of hair loss in seven groups of captive rhesus macaques housed in outdoor enclosures at the California National Primate Research Center. Groups having grass substrate spent a greater proportion of their time foraging and a smaller proportion of time grooming compared with groups having gravel substrate. Increased time spent grooming in gravel enclosures may have contributed to significantly greater hair loss in those enclosures. A causal relationship between ground substrate on foraging and grooming, and therefore hair loss, is strengthened by similar changes in activity budgets and hair loss in a single group that was moved from gravel to grass substrate halfway through the study. These results add to growing evidence that substrate type in captivity is important to consider because it affects animal well-being. In particular, these results reveal that grass substrate is more effective than gravel in stimulating foraging and reducing allo-grooming to levels that are comparable to wild populations, and enable animals to maintain healthier coats.

Utility of social network analysis for primate behavioral management and well-being

New management strategies for detecting social instabilities and promoting social cohesion are needed to reduce aggression-based morbidity and mortality among captive groups of rhesus macaques. This study was conducted to determine the utility of social network analysis for deciphering patterns of aggression and wounding in rhesus macaques. Over 37,000 observations of affiliative, submissive and aggressive activities were collected over a 3-year period on ∼1300 rhesus macaques housed in 13.2ha enclosures. Data also were analyzed on management factors such as age/sex composition and matriline configuration that might promote or reduce aggression in rhesus macaques. Results suggest that social network measures such as subordination degree (social power), displacement fragmentation and groom reciprocity within social groups were not only significantly associated with rates of contact aggression and wounding but with the occurrence of severe aggressive outbreaks, known as cage wars. In addition, groups with a lower proportion of adult females and a more uniform distribution in the number of individuals across matrilines exhibited higher social power and lower fragmentation. These data indicate that by manipulating group composition and matriline configuration of social groups to promote social cohesion and stability, behavioral managers may be able to reduce the level of aggression and aggression-based morbidity and mortality. These data also show that social network measures are valuable predictors of deleterious aggression and even cage wars indicating that such measures could be used to longitudinally track changes in social dynamics to detect significant instabilities, allowing managers to prevent severe outbreaks before they occur in populations of rhesus macaques and perhaps other non-human primate species.

Avoidance of close consanguineous inbreeding in captive groups of rhesus macaques.

In three captive groups of rhesus macaques (Macaca mulatto) the intensity of inbreeding avoidance was directly correlated with the closeness of kinship. The incidence of inbreeding between matrilineal relatives was lower than expected were mating to occur randomly with regard to matrilineal affiliation. The avoidance of mating between sons and their mothers and between matrilineal sibs contributed about squally to this outcome. The incidence of mating between more remote matrilineal relatives was lower than, but could not be shown to differ significantly from, that expected at the 0.05 level of probability. Familiarity fostered by interactions among matriline members probably provides a focus for avoidance of matrilineal inbreeding, and might influence male dispersal. Results of this study are consistent with reports of female rhesus macaques' avoidance of sexual activity with matrilineal male relatives as predicted by parental investment theory The observed incidence of inbreeding between patrilineal relatives was not different from that expected, but significantly fewer of the patrilineally inbred matings involved father/daughter matings than expected were mating random. Recognition of phenotypic similarities might provide a focus for avoidance of inbreeding between fathers and their daughters, but is loss reliable than strategies for avoiding matrilineal inbreeding. Adaptations for avoiding matrilineal inbreeding that are more effective than those for avoiding patrilineal inbreeding might have evolved because the risk of patrilineal inbreeding, and hence the resulting loss in fitness, is marginal compared to that for matrilineal inbreeding in free-ranging groups. © 1995 Wiley-Liss, Inc.

Maternal Anxiety in Rhesus Macaques (Macaca mulatta)

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

Maternal Anxiety in Rhesus Macaques (Macaca mulatta)

AbstractThis study assessed the extent to which emotional reactivity to the social environment influences maternal behaviour in macaques. Visual monitoring and scratching were used as behavioral indicators of maternal and social anxiety in small captive groups of rhesus macaques. Maternal visual monitoring of the infant and of other individuals proved better predictors of individual differences in maternal protectiveness than did characteristics of the mother‐infant dyad such as maternal age, experience and dominance rank, number of immature offspring present in the group, or sex of the infant. Unlike visual monitoring, maternal scratching was not linearly related to protectiveness. Mothers displaying low or high rates of scratching ranked low on protectiveness, and the most protective mothers were those who displayed intermediate levels of scratching. Although individual differences in maternal and social anxiety seem to be mediated by maternal age and experience, they might also be influenced by genetics and early experience.

Heterosis associated with regional crossbreeding between captive groups of rhesus macaques.

The lengths and weights of male and female Chinese-Indian hybrid rhesus macaques were compared with those of age- and sex-matched non-hybrid (Indian) controls to assess the occurrence of heterosis (hybrid vigor). Hybrid males and females had higher average, age-adjusted values of weight than nonhybrids. Hybrid males, but not females, also had a higher average, age-adjusted length than nonhybrids. These results are consistent with the hypothesis that regional crossbreeding of rhesus monkeys fosters heterosis.

Parental rank and reproductive success of natal rhesus males

In primates, the relationship between the ranks of parents and those of their sons has not been studied systematically, yet it has important implications for sociobiological theories. The influence of parents' ranks upon the ranks and reproductive success of their sons who remain and breed within their natal group was tested in two captive groups of rhesus macaques, Macaca mulatta. Paternity exclusion analyses revealed that both the rank and reproductive success of natal males were strongly associated with their mothers', but not their fathers', ranks. The ranks of natal males were also significantly correlated with their own reproductive success. However, this correlation was not nearly as strong as the correlation between the ranks and reproductive success of the fathers of these natal males. This difference was associated with a decline in reproductive success, but not in rank, of some founding males after natal males reached sexual maturity, and might result from an age bias in mating and/or the increase in the ratio of adult males to females. Although the reproductive advantage enjoyed by sons of high-ranking mothers prior to dispersal from their natal groups might be of evolutionary significance, it is important to determine whether or not this advantage persists after dispersal.

Mate choice by lineage in three captive groups of rhesus macaques (Macaca mulatta).

The hypothesis that the matrilineal affiliation of 410 infants born in three captive groups of rhesus macaques is independent of the patrilineal affiliation of these infants was tested. Preferential mating with particular patrilines was observed for matrilineal members. We conclude that lineage affiliation does influence mate choice of rhesus macaques, at least when a large number of matrilines and relatively few patrilines which include natal males are represented in the group. Such nonrandom mating might explain high levels of genetic heterogeneity reported among matrilines within rhesus groups, despite high rates of male emigration, and is consistent with the maintenance of high levels of within-matriline kinship which might promote cooperative behavior among matriline members.

Potential for cumulative inbreeding and its effects upon survival in captive groups of non-human primates

The effect of population structure of six captive groups of rhesus macaques (Macaca mulatta) upon level of inbreeding and resulting survival of offspring is estimated and found to be substantial. Breeding colony management policies designed to minimize inbreeding and its deleterious effects are discussed and compared for their efficiency. It is concluded that the most efficient policy involves the rotation of groups of adult males among several breeding groups every few years.