Relationships between affiliative social behavior and hair cortisol concentrations in semi-free ranging rhesus monkeys

Abstract

Sociality is a fundamental aspect of human behavior and health. One benefit of affiliative social relationships is reduced short-term levels of glucocorticoids (GCs), which are indicative of physiological stress. Less is known, however, about chronic GC production in relation to affiliative social behavior. To address this issue, we studied a semi-free ranging troop of rhesus macaques (Macaca mulatta) and collected hair samples to measure hair cortisol concentrations (HCCs), as a measure of chronic GC production, during routine biannual exams. We collected social behavior (both aggressive and affiliative) and hair samples for 32 adult female rhesus macaques over one year (Experiment 1). Our results indicated that adult females who initiated higher levels of social affiliation had significantly lower levels of HCCs. Neither the initiation nor the receipt of aggression were significantly related to HCCs in this study. In a second experiment we studied 28 mother-infant dyads for the first 90 days postpartum to examine mother-infant facial interactions (i.e. mutual gazing). We analyzed HCCs during weaning approximately one year later, which is a major transitional period. We found that infants that engaged in higher levels of mutual gazing in the first 90 days postpartum had significantly lower levels of HCCs during weaning. Finally, we studied 17 infant rhesus macaques (13 males) to examine whether social behavior (such as play) in the first five months of life correlated with infant HCCs over those months (Experiment 3). We found that infant males that engaged in more social play had significantly lower levels of HCCs. By relying on an animal model, our study shows that affiliative social traits are associated with lower long-term GC production. Future research should address the complex interactions between social behavior, chronic GC production, and mental and physical health.

Aggression and social support predict long‐term cortisol levels in captive tufted capuchin monkeys (Cebus [Sapajus] apella)

“…These levels are consistent with previous measures of hair cortisol in capuchin monkeys using the same methods (Phillips et al, ). Consistent with previous findings that cortisol levels in New World primates are up to 10 times higher than those of Old World primates (Coe, Savage, & Bromley, ), the same hair sample extraction and assay method in rhesus monkeys revealed cortisol levels ranging from 40 to 70 pg/mg (Dettmer et al, ; Wooddell et al, ) compared to our 425–1,787 pg/mg. Consistent with previous findings in wild capuchin monkeys (Jack et al, ; Lynch et al, ; Moreira, dos Santos, de Sousa, & Izar, ), cortisol levels did not vary between the sexes (males: 757.48 ± 91.56 pg/mg; females: 767.72 ± 111.40 pg/mg; paired samples t test: t = 0.07, p = .900).…”

“…Affiliative behavior in primates is often measured through dyadic interactions such as grooming, contact, and proximity. Increases in the amount of grooming given (Shutt, MacLarnon, Heistermann, & Semple, ; Wooddell et al, ), higher equitability in grooming relationships (Yamanashi et al, ), concentration of grooming relationships (Sonnweber et al, ), and increased initiation of affiliative behaviors such as contact and play (Wooddell et al, ) have all been associated with low cortisol levels in various primate species. These affiliative interactions often involve physical contact (Dunbar, ).…”

Prenatal stress disrupts social behavior, cortical neurobiology and commensal microbes in adult male offspring

“…Confirming the hypothesis that prenatal stress may increase stress-induced activity of the HPA-axis, which has been associated with reduced social interactions [33,34], we found a significant increase in corticosterone following exposure to the social behavior paradigm in males exposed to PNS. We found a concomitant reduction in CRH in the cortex as well, pointing to sustained HPA axis dysregulation in adulthood in males exposed to PNS.…”

Early-life manipulation of cortisol and its receptor alters stress axis programming and social competence

“…For example, in bonobos (Pan paniscus), aggressive conflicts increase HPA axis activity and promote affiliative behaviours between victims of the conflict and conspecifics [84]. Furthermore, in rhesus macaques (Macaca mulatta), playful behaviours in young males correlate with lower cortisol levels [85]. The interactive effect on affiliative behaviour was the only effect of treatment on behaviour during the experience phase, whereas all other behavioural effects became apparent only during the late juvenile period.…”