Responses to social and environmental stress are attenuated by strong male bonds in wild macaques

Abstract

In humans and obligatory social animals, individuals with weak social ties experience negative health and fitness consequences. The social buffering hypothesis conceptualises one possible mediating mechanism: during stressful situations the presence of close social partners buffers against the adverse effects of increased physiological stress levels. We tested this hypothesis using data on social (rate of aggression received) and environmental (low temperatures) stressors in wild male Barbary macaques (Macaca sylvanus) in Morocco. These males form strong, enduring, and equitable affiliative relationships similar to human friendships. We tested the effect of the strength of a male’s top three social bonds on his faecal glucocorticoid metabolite (fGCM) levels as a function of the stressors’ intensity. The attenuating effect of stronger social bonds on physiological stress increased both with increasing rates of aggression received and with decreasing minimum daily temperature. Ruling out thermoregulatory and immediate effects of social interactions on fGCM levels, our results indicate that male Barbary macaques employ a tend-and-befriend coping strategy in the face of increased environmental as well as social day-to-day stressors. This evidence of a stress-ameliorating effect of social bonding among males under natural conditions and beyond the mother-offspring, kin or pair bond broadens the generality of the social buffering hypothesis

Social bufferingandcontact transmission: network connections have beneficial and detrimental effects onShigellainfection risk among captive rhesus macaques

“…These were computed using the Statnet and Sna (Handcock et al, 2006) packages in R. Given its estimation of an individual’s direct connections, degree centrality has been extensively used in epidemiological studies to date that have focused on contact-mediated pathogen transmission (Drewe, 2010; Drewe & Perkins, 2015; Rimbach et al, 2015). On the other hand, in- and out-degree and strength in grooming may also be indicative of reduced infection risk via social buffering, given that grooming interactions have well-documented benefits of lowering the physiological stress levels among both givers and receivers (Henzi & Barrett, 1999; Smutt et al, 2007; Young et al, 2014). Although betweenness centrality has been less commonly used in epidemiological studies, it has been proposed as being a key metric in predicting the potential for the flow of infectious agents through the generally more densely connected social networks (Drewe & Perkins, 2015; Farine & Whitehead, 2015; Newman, 2005; VanderWaal et al, 2014).…”

“…On the one hand, increased connections may lead to greater chances of infection from pathogens via contact-mediated transmission (Drewe & Perkins, 2015), making infectious disease acquisition a major cost of social living (Alexander, 1974; Freeland, 1976; Loehle, 1995; MacIntosh et al, 2012). Yet social connections may also mitigate the impact of stressors or immunosuppressive effects of stress, thereby socially buffering an individual to decrease their susceptibility to infection (Hennessy, Kaiser & Sachser, 2009; Kikusui, Winslow & Mori, 2006; McCowan et al, 2016; Sapolsky, 2005; Sapolsky, Romero & Munck, 2000; Segerstrom & Miller, 2004; Young et al, 2014). To better understand the impact of social life on disease risk, it is necessary to characterize the potentially competing impacts of both greater contact-mediated transmission and social buffering on susceptibility to, and transmission of pathogens.…”

“…Even less explored is the possibility that having more direct or indirect connections in a network may, via social buffering , protect individuals from social and environmental stressors (Kaplan et al, 1991; Young et al, 2014), and decrease rather than increase their susceptibilities to infection. In societies where individuals maintain strong social bonds (e.g., humans, some nonhuman primates like baboons ( Papio sp. )…”

“…and macaques ( Macaca sp. )), social buffering is well-documented—having more social ties can mitigate stress to generate positive health outcomes (Cobb, 1976; Young et al, 2014) and indeed, enhance longevity and survival (Archie et al, 2014; Silk et al, 2010). In humans for example, having more connections who provide social support during times of conflict alleviates stress-levels (Janowski et al, 2012) and decreases susceptibility to non-communicable diseases such as cancer and cardiovascular disease (Uchino, 2004; Uchino, 2009).…”

“…In humans for example, having more connections who provide social support during times of conflict alleviates stress-levels (Janowski et al, 2012) and decreases susceptibility to non-communicable diseases such as cancer and cardiovascular disease (Uchino, 2004; Uchino, 2009). In nonhuman primates, grooming (an affiliative social interaction) may be exchanged among group members for access to social support (Seyfarth, 1977), and is also known to lower circulating levels of glucocorticoids by reducing activation of the hypothalamic-pituitary-adrenal (HPA) axis (Young et al, 2014). Socio-positive interactions appear to be key in alleviating stress, which both enhances immune function (Sapolsky, Romero & Munck, 2000) and decreases susceptibility to infectious agents (Cohen, Janicki-Deverts & Miller, 2007; Segerstrom & Miller, 2004).…”