Groups Of Rhesus Macaques Research Articles

Sharing from the Same Bowl: Resource Partitioning between Sympatric Macaque Species in the Western Himalaya, India

Comparative studies of closely related species with similar ecological requirements are essential to understand the behavioral adaptations that allow them to live in sympatry. We investigated the mechanisms that enable the coexistence of two congeneric macaques—the Assamese macaque (Macaca assamensis) and rhesus macaque (M. mulatta)—in the Western Himalaya along the India–Nepal border in the State of Uttarakhand, India. For five months from December 2016, we collected scan samples of the behavior of one Assamese macaque group (N = 9975 samples) and two rhesus macaque groups (N = 14,402). Activity budget comparisons revealed that the former spent more time on feeding and the latter on resting and moving. Although the two species had 29 (37%) of 78 food items in common, only Mallotus philippensis and agricultural crops formed a major part of their shared diet (contributing to >1% of feeding scans). The Assamese macaque fed predominantly on leaves and had a broader niche than did the rhesus macaque, which fed mostly on fruits. We also observed differences in feeding schedules and feeding heights of the two species. The two species showed variation in home range, daily movement patterns, habitat use, and sleeping sites that need further investigation. The two species exhibited a lower dietary and spatial niche overlap in winter, a period of relatively low resource abundance than in spring. The observed differences in diet and space use suggest that the niches of the two macaques are separated in several dimensions, which may have promoted their coexistence in this region. Similar long-term studies across different habitats and seasons can improve our understanding of resource use by primates in sympatry.

CD8+ T cell-based strong selective pressure on multiple simian immunodeficiency virus targets in macaques possessing a protective MHC class I haplotype

In human immunodeficiency virus (HIV) and simian immunodeficiency virus (SIV) infections, host major histocompatibility complex class I (MHC-I) genotypes have a great impact on viral replication and MHC-I-associated viral genome mutations are selected under CD8+ T-cell pressure. Association of MHC-I genotypes with HIV/SIV control has been investigated at MHC-I allele levels but not fully at haplotype levels. We previously established groups of rhesus macaques sharing individual MHC-I haplotypes. In the present study, we compared viral genome diversification after SIV infection in macaques possessing a protective MHC-I haplotype, 90-010-Id, with those possessing a non-protective MHC-I haplotype, 90-010-Ie. These two MHC-I haplotypes are associated with immunodominant CD8+ T-cell responses targeting similar regions of viral Nef antigen. Analyses of viral genome sequences and antigen-specific T-cell responses showed four and two candidates of viral CD8+ T-cell targets associated with 90-010-Id and 90-010-Ie, respectively, in addition to the Nef targets. In these CD8+ T-cell target regions, higher numbers of mutations were detected at the setpoint after SIV infection in macaques possessing 90-010-Id than those possessing 90-010-Ie. These results indicate higher selective pressure on overall CD8+ T-cell targets associated with the protective MHC-I haplotype, suggesting a pattern of HIV/SIV control by multiple target-specific CD8+ T-cell responses.

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.

Interactions with humans impose time constraints on urban-dwelling rhesus macaques (Macaca mulatta)

Abstract Time is a valuable but limited resource, and animals’ survival depends on their ability to carefully manage the amount of time they allocate to each daily activity. While existing research has examined the ecological factors affecting animals’ activity budgets, the impact of anthropogenic factors on urban-dwelling animals’ time budgets remains understudied. Here we collected data through focal animal sampling from three groups of rhesus macaques in Northern India to examine whether interactions with humans decrease macaques’ resting and social time (time constraints hypothesis), or whether, by contrast, foraging on anthropogenic food, that is potentially high in calories, leads macaques to spend more time resting and in social interactions (free time hypothesis). We found that macaques who interacted more frequently with people spent significantly less time resting and grooming, supporting the time constraints hypothesis. We argue that these time constraints are likely caused by the unpredictability of human behaviour.

Rates of human-macaque interactions affect grooming behavior among urban-dwelling rhesus macaques (Macaca mulatta).

The impact of anthropogenic environmental changes may impose strong pressures on the behavioral flexibility of free-ranging animals. Here, we examine whether rates of interactions with humans had both a direct and indirect influence on the duration and distribution of social grooming in commensal rhesus macaques (Macaca mulatta). Data were collected in two locations in the city of Shimla in northern India: an urban setting and a temple area. We divided these two locations in a series of similar-sized physical blocks (N = 48) with varying rates of human-macaque interactions. We conducted focal observations on three free-ranging rhesus macaque groups, one in the urban area and two in the temple area. Our analysis shows that macaques engaged in shorter grooming bouts and were more vigilant while grooming in focal sessions during which they interacted with people more frequently, suggesting that humans directly affected grooming effort and vigilance behavior. Furthermore, we found that in blocks characterized by higher rates of human-macaque interactions grooming bouts were shorter, more frequently interrupted by vigilance behavior, and were less frequently reciprocated. Our work shows that the rates of human-macaque interaction had both a direct and indirect impact on grooming behavior and that macaques flexibly modified their grooming interactions in relation to the rates of human-macaque interaction to which they were exposed. Because grooming has important social and hygienic functions in nonhuman primates, our work suggests that human presence can have important implications for animal health, social relationships and, ultimately, fitness. Our results point to the need of areas away from people even for highly adaptable species where they can engage in social interactions without human disruption.

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.

Effects of group size and rank on mother–infant relationships and reproductive success in rhesus macaques (Macaca mulatta)

In the present study, we compared mother-infant relationships in 57 mother-infant dyads residing in two wild, semi-provisioned (22 mother-infant dyads in 2014, 35 dyads in 2015) groups of rhesus macaques (Macaca mulatta) in the Nanwan Nature Reserve for Rhesus Macaques, Hainan, China. We also compared reproductive success between these two groups. The ecology and provisioning regime for each group was similar. These groups differed however, in size. Group 1 contained ∼35 individuals and Group 2 contained ∼120 individuals. Data were collected over a 2-year period (2014-2015). We found that during the birth season, mother-infant relationships in the larger group were characterized by less time in contact and more time separated than in the smaller group. Mothers in the smaller group initiated more contact and proximity with their infants. During the mating season when infants were approximately 6 months old, mother-infant relationships in the smaller group were more rejecting. We also found that birth rates were significantly higher but infant survivorship (to 1-year-old) was significantly lower in the smaller group. Moreover, higher-ranking mothers in the larger group were characterized by a higher reproductive output than females of lower rank. In the smaller group, female rank did not affect reproductive output. There was, however, no clear relationship between infant survivorship and maternal rank. We hypothesize that differences in reproductive success and changes in mother-infant relationships between the birth and mating seasons reflect differences in the costs and benefits of group size: females in the larger group faced (i) higher intragroup feeding competition leading to a reduction in birth rate but also (ii) lower predation risk, resulting in higher infant survival rate compared to females in the smaller group. The results of this study point to the tradeoffs that primate females face in living in smaller and larger social groups.

Trauma rates and patterns in specific pathogen free (SPF) rhesus macaque (Macaca mulatta) groups.

There are some predictable patterns of trauma in captive rhesus macaque (Macaca mulatta) social groups. Several factors have been documented to contribute to these patterns, including group formation of unrelated animals, and the establishment of dominance ranks. Here, we report on how socially induced trauma in groups of rhesus monkeys is influenced by the breeding season, numbers of matrilines per group and matriline size. We analyzed 3 years of data collected from veterinary admittance logs for four groups in our specific pathogen free (SPF) breeding colony. Since the groups differed in time from formation, both the numbers of matrilines and the composition of those matrilines were different. Across the four groups, trauma rates were significantly higher during the fall breeding season than the spring and summer months when births occur. The group that was formed most recently, comprised of the greatest number of matrilines but fewest related animals, showed significantly higher rates of trauma than the older social groups. Further, the middle and lowest ranking families received signifincantly higher rates of trauma than the highest ranking families, suggesting a rank-related phenomenon. Additionally, there was a significant negative correlation between numbers of adult females in a matriline and rates of trauma observed in each matriline, but the numbers of adult females are significantly higher in the top ranked families compared to all of the other matrilines. These findings suggest that trauma rates increase during the breeding season and may be exacerbated in recently formed breeding groups that have smaller matrilines and reduced opportunities for social support to mitigate rank-related aggression. Management practices should be devised to ensure adequate matrilineal size to decrease rates of trauma in captive rhesus macaque groups.

The Hand That Feeds the Monkey: Mutual Influence of Humans and Rhesus Macaques (Macaca mulatta) in the Context of Provisioning

Historically, humans and other primates (primates henceforth) have coexisted across cultures and contexts, and many primate populations use anthropogenic food sources as their main or supplementary food. While primates may actively forage for such food, they are also directly provisioned by humans in many regions. Ethnoprimatology views humans and primates as cohabitants of integrated socioecological spaces who mutually influence each other’s ecologies and social lives. We contextualized provisioning of primates by humans within an ethnoprimatological framework and examined if the availability of anthropogenic food affected primate diets or the amount of time primates spent in anthropogenic habitats and whether primates influenced the human act of provisioning. To this end, we used scan sampling on a group of rhesus macaques across a year, and conducted interviews with 86 people who paused at a nearby tea shop for refreshments. We found that the macaques’ consumption of natural resources and dietary diversity decreased, and they spent more time in human-modified habitats when provisioned food was available. We also found that particular behaviors of the provisioned macaques stimulated provisioning by humans. Our findings show that provisioning influences macaque feeding ecology and habitat use, and that the behavior of the macaques themselves drives people to provide them with food subsidies, illustrating a complex web of interactions between the sympatric species.

Social hair pulling in captive rhesus macaques (Macaca mulatta).

Alopecia is common among captive populations of nonhuman primates. There are many potential causes of alopecia, including physiological conditions such as hormonal imbalance and infection, features of the captive environment such as housing type, ground substrate, and group density, as well as behavioral abnormalities such as self-plucking. A potential behavioral cause of alopecia in group-housed primates is social hair pulling, where one animal pulls hair from a conspecific. While social hair pulling has been conflated with overgrooming in some of the alopecia literature, other authors have categorized it as a form of aggression rather than a form of excessive grooming. In this study, we examined social hair pulling, grooming, and aggression within seven groups of rhesus macaques (Macaca mulatta) (N = 319). We took weekly 30-min behavioral observations on each group for one year to assess the patterns of hair pulling and grooming, which monkeys were receiving and initiating these behaviors, as well as aggression and other behaviors indicating dominance. We also assessed the amount of alopecia on each individual monthly. While grooming tended to be directed "up" the hierarchy (i.e., monkeys were more likely to groom animals of a higher rank than lower rank), most hair pulling was directed "down" the hierarchy. Further, hair pulling seldom co-occurred with aggressive behaviors, suggesting that it was not a form of aggression. Hair pulling also usually resulted in ingestion of the pulled hair. Hair pulling was correlated with alopecia; monkeys who were frequent recipients of hair pulling scored higher on monthly alopecia ratings than those who were less often observed having hair pulled. Our results suggest that social hair pulling is a behavior distinct from either grooming or aggressive behavior, and that it may contribute to alopecia in socially housed macaques.

Social network dynamics precede a mass eviction in group-living rhesus macaques

Network dynamics can reveal information about the adaptive function of social behaviour and the extent to which social relationships can flexibly respond to extrinsic pressures. Changes in social networks occur following changes to the social and physical environment. By contrast, we have limited understanding of whether changes in social networks precede major group events. Permanent evictions can be important determinants of gene flow and population structure and are a clear example of an event that might be preceded by social network dynamics. Here we examined the social networks of a group of rhesus macaques, Macaca mulatta, in the 2 years leading up to the eviction of 22% of adult females, which are the philopatric sex. We found that females engaged in the same amount of aggression and grooming in the 2 years leading up to the eviction but that there were clear changes in their choice of social partners. Females that would eventually be evicted received more aggression from lower-ranking females as the eviction approached. Evicted females also became more discriminating in their grooming relationships in the year nearer the split, showing a greater preference for one another and becoming more cliquish. Put simply, the females that would later be evicted continued to travel with the rest of the group as the eviction approached but were less likely to interact with other group members in an affiliative manner. These results have potential implications for understanding group cohesion and the balance between cooperation and competition that mediates social groups.

Vaccine-induced immune responses against both Gag and Env improve control of simian immunodeficiency virus replication in rectally challenged rhesus macaques.

The ability to control lentivirus replication may be determined, in part, by the extent to which individual viral proteins are targeted by the immune system. Consequently, defining the antigens that elicit the most protective immune responses may facilitate the design of effective HIV-1 vaccines. Here we vaccinated four groups of rhesus macaques with a heterologous vector prime/boost/boost/boost (PBBB) regimen expressing the following simian immunodeficiency virus (SIV) genes: env, gag, vif, rev, tat, and nef (Group 1); env, vif, rev, tat, and nef (Group 2); gag, vif, rev, tat, and nef (Group 3); or vif, rev, tat, and nef (Group 4). Following repeated intrarectal challenges with a marginal dose of the neutralization-resistant SIVmac239 clone, vaccinees in Groups 1–3 became infected at similar rates compared to control animals. Unexpectedly, vaccinees in Group 4 became infected at a slower pace than the other animals, although this difference was not statistically significant. Group 1 exhibited the best post-acquisition virologic control of SIV infection, with significant reductions in both peak and chronic phase viremia. Indeed, 5/8 Group 1 vaccinees had viral loads of less than 2,000 vRNA copies/mL of plasma in the chronic phase. Vaccine regimens that did not contain gag (Group 2), env (Group 3), or both of these inserts (Group 4) were largely ineffective at decreasing viremia. Thus, vaccine-induced immune responses against both Gag and Env appeared to maximize control of immunodeficiency virus replication. Collectively, these findings are relevant for HIV-1 vaccine design as they provide additional insights into which of the lentiviral proteins might serve as the best vaccine immunogens.

MAIT cells (CD8+CD161++TCR7.2++) are functionally impaired during chronic SHIV infection.

Abstract Mucosa-associated invariant T-cells (MAIT) are abundant in humans and recognize bacterial ligands. Here, we have studied the distribution and function of MAIT cells during chronic SHIV infection using rhesus macaques (RM). Two groups of RM, healthy and SHIV infected were studied. lymphocytes from various tissues were analysed for MAIT (TCR7.2++ CD161++) cells using multicolor flow cytometry and characterized for their distribution, phenotype and function during chronic SHIV infection. Similar to human, we found significant fraction of (~2%) RM CD8 T cells co-express MAIT cell markers TCR7.2, CD161, IL-18R, CCR6 and display central memory (CCR7+CD45RA−) phenotype. The frequency of MAIT cells were decreased during chronic SHIV infection and tissue analysis showed a significant enrichment of MAIT cells in liver (~8%) and BAL (3%) than in blood (1%), spleen(0.5%), lymph node(0.13%) and gut (0.2%). Importantly, during chronic SHIV infection more than 80% of MAIT cells expressed T cell exhaustion marker PD-1 in blood and the level of expression was higher (>95%) in tissue resident CD69+MAIT cells. These cells lack proliferating capacity (Ki-67) and cytokine production (IFN- g and IL-17) in the blood, suggesting their functional impairment. The preserved blood and gut MAIT cells correlate inversely with plasma viral RNA levels and associate directly with gut CD4 T cell levels, suggesting that CD4 help maintains MAIT cell frequencies in the gut. These data demonstrate that MAIT cells are decreased in blood and are functionally exhausted during chronic SHIV infection. Future studies focused on blocking the PD-1 pathway to retrive MAIT cell exhaustion during chronic SHIV/HIV infection may yield therapeutic benefit to HIV/SHIV infection.

Long-term analysis on the variance of extra-group paternities in rhesus macaques

Extra-group paternity (EGP) has been described in various mammalian species; however, little is known about which factors contribute to the variation in EGP, as the majority of studies were restricted in time and the number of groups considered. Using longitudinal demographic and genetic data, we aim to investigate which factors predict rates of EGP in the free-ranging rhesus macaque population of Cayo Santiago, Puerto Rico (USA). Of the 1649 infants considered which were born into six social groups over 9 years, we identified an average of 16% of infants resulting from EGPs. We tested the influence of group size, breeding group sex ratio, female reproductive synchrony, and group instability on the occurrence of EGPs. Our results suggest a tendency for EGPs to increase as the proportion of females increased in larger groups, but no such effect in smaller groups. Furthermore, as group instability and female reproductive synchrony decreased, the number of EGPs tended to increase. Our results support the hypothesis that group structure affects the occurrence of EGPs, which might be mediated by male mating opportunities, male monopolization potential, and/or female choice.Significance statementIn several species, both sexes seek alternative reproductive strategies to enhance their reproductive success. For instance, females may pursue EGPs to potentially increase genetic compatibility with males, or males may seek EGPs to improve their mating opportunities. Our longitudinal analysis, including demographic and genetic data over 9 years of six social groups of rhesus macaques, revealed high variation in the occurrence of EGPs across groups and years, and this variation tended to depend on group characteristics such as breeding group size, sex ratio, female synchrony, and group instability. The data suggest that group structure affects the number of EGPs in this group-living primate. Our results show that EGPs can affect the distribution of paternity within social groups and should be taken into account when assessing reproductive success.

Cabotegravir long acting injection protects macaques against intravenous challenge with SIVmac251.

We evaluated the effectiveness of cabotegravir (CAB; GSK1265744 or GSK744) long acting as preexposure prophylaxis (PrEP) against intravenous simian immunodeficiency virus (SIV) challenge in a model that mimics blood transfusions based on the per-act probability of infection. CAB long acting is an integrase strand transfer inhibitor formulated as a 200 mg/ml injectable nanoparticle suspension that is an effective PrEP agent against rectal and vaginal simian/human immunodeficiency virus transmission in macaques. Three groups of rhesus macaques (n = 8 per group) were injected intramuscularly with CAB long acting and challenged intravenously with 17 animal infectious dose 50% SIVmac251 on week 2. Group 1 was injected with 50 mg/kg on week 0 and 4 to evaluate the protective efficacy of the CAB long-acting dose used in macaque studies mimicking sexual transmission. Group 2 was injected with 50 mg/kg on week 0 to evaluate the necessity of the second injection of CAB long acting for protection against intravenous challenge. Group 3 was injected with 25 mg/kg on week 0 and 50 mg/kg on week 4 to correlate CAB plasma concentrations at the time of challenge with protection. Five additional macaques remained untreated as controls. CAB long acting was highly protective with 21 of the 24 CAB long-acting-treated macaques remaining aviremic, resulting in 88% protection. The plasma CAB concentration at the time of virus challenge appeared to be more important for protection than sustaining therapeutic plasma concentrations with the second CAB long acting injection. These results support the clinical investigation of CAB long acting as PrEP in people who inject drugs.

Grooming interchange for resource tolerance: biological markets principles within a group of free-ranging rhesus macaques

In group-living animals, allogrooming is a common, heterogeneously distributed affiliative behaviour. Among non-human primates, Barrett et al. (1999) predicted ways in which Biological Markets principles interact with competitive regimes to influence grooming reciprocity and interchange. Most tests of these predictions, done at a group level, have produced inconsistent results. Here we take a novel approach by testing these predictions across individuals within a group. This is based on the premise that in groups facing moderate-to-high within-group-competition, individuals vary in their abilities to access resources based on their competitive abilities, causing them to pursue different grooming exchange strategies. We examine evidence for grooming reciprocity and interchange for tolerance at drinking sources among adult females within a group of rhesus macaques (Macaca mulatta) on Cayo Santiago. We test the above premise by assessing hierarchical steepness, and the relationship between individuals’ David’s scores (DS) and access to drinking sources. Finally, we examine the relationship of DS with grooming reciprocity and interchange to see whether they are consistent with the operation of market forces among individuals. Social network comparisons revealed that giving grooming was strongly predicted by both receiving drinking tolerance (interchange) and receiving grooming (reciprocity), despite strong associations with proximity and maternal kinship. The group showed a moderately steep hierarchy, and negative correlations between individuals’ David’s scores and difficulties in accessing drinking stations. Finally, we found partial support for a market-based explanation. Individuals with relatively low David’s scores were more likely to interchange grooming with drinking tolerance. However, grooming reciprocity wasn’t greater among individuals with higher David’s scores. Our findings suggest that multiple explanatory frameworks — reciprocity, market-based interchange, and/or proximity-mediated interchange/social bond investment — may all shape rhesus grooming exchange patterns. Future directions include examining evidence for additional forms of grooming interchange, and the influence of between-group-competition and stress-indicators on grooming reciprocity.

Influence of Fruit Availability on Fruit Consumption in a Generalist Primate, the Rhesus Macaque Macaca mulatta

Fluctuations in resource availability occur in all ecosystems. To survive, species must alter their foraging strategies according to the quantity, quality, and distribution of available food. The rhesus macaque (Macaca mulatta), a commensal primate, is considered a generalist omnivore and very few studies have addressed how its feeding strategies change with respect to resource availability. We examined dietary diversity and frugivory levels in a group of rhesus macaques at the Buxa Tiger Reserve in northern India across one year. Using behavioural observations of diet and phenological monitoring, we found that although rhesus macaques fed on 107 food items including leaves, flowers, fruits, seeds, and insects, fruits made up ca. 74% of their diet. Fruit consumption correlated positively with fruit availability, but fruit preference appeared to play an important role; 16% of all the fruit species they fed on accounted for > 50% of all fruit feeding observations. We suggest that afforestation programs involving preferred fruit species at the agricultural land-forest interface would prevent forest groups of rhesus macaques from gravitating toward human habitations and reduce conflict over anthropogenic resources. We further propose that the movement of certain primates in the direction of human habitations may be contingent on resource availability and food preference rather than an inherent propensity to gravitate to anthropogenic areas.

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.

Altered activity-based sleep measures in rhesus monkeys following cocaine self-administration and abstinence

BackgroundImpairments in sleep and cognitive function have been observed in patients with substance abuse disorders and may be potential factors contributing to drug relapse. In addition, sleep disruption may itself contribute to cognitive deficits. In the present study we examined the impact of prolonged cocaine self-administration and abstinence on actigraphy-based measures of night-time activity in rhesus macaques as an inferential measure of sleep, and determined whether sleep-efficiency correlated with cognitive impairments in the same subjects on drug free days. MethodsActigraphy data was obtained from a group of rhesus macaques intravenously self-administering cocaine (n=6) and a control group (n=5). Periods were evaluated during which the mean cumulative doses of cocaine were 3.0+0.0 and 4.5+0.2mg/kg/day for 4days (Tuesday–Thursday) each week. ResultsActigraphy-based sleep efficiency decreased during days of cocaine self-administration in a dose-dependent manner. Consistent with this observation, sleep became more fragmented. Activity-based sleep efficiency normalized during the weekend without cocaine prior to cognitive assessment on Monday. The magnitude of activity-based sleep disruption during self-administration did not correlate with the level of cognitive impairment on drug free days. With continued self-administration, the impact of cocaine on activity-based sleep efficiency declined indicating the development of tolerance. ConclusionsCocaine self-administration disrupted sleep efficiency in rhesus macaques as measured by actigraphy, but normalized quickly in the absence of cocaine. The cognitive impairment observed on drug free days was unlikely to be related to disruption of the nightly activity patterns on days of cocaine self-administration.