Effects of reproductive condition and dominance rank on cortisol responsiveness to stress in free‐ranging female rhesus macaques

Abstract

The hypothalamic-pituitary-adrenal (HPA) axis modulates individuals’ physiological responses to social stress, which is an inevitable aspect of the daily lives of group-living animals. Previous nonhuman primate studies have reported that sex, age, rank and reproductive condition influence cortisol levels under stressful conditions. In this study we investigated cortisol responses to stress among 70 multiparous, free-ranging female rhesus macaques (Macaca mulatta) on the island of Cayo Santiago, PR. Plasma cortisol samples were collected in two consecutive years under similar conditions. Twenty-two females were sampled both years, and most of those females were lactating in only one of the years. Individual differences in cortisol levels were stable across years, even though reproductive condition changed for most individuals. No relationship was found between age or social rank and cortisol levels. Of the females that changed reproductive conditions, cortisol levels were higher when they were lactating than when they were cycling, and the amount of change in cortisol from cycling to lactating was greatest for low-ranking individuals. Heightened reactivity to stress during lactation may be the result of concerns about infant safety, and such concerns may be higher among low-ranking mothers than among higher ranking mothers. Psychosocial stress and hyperactivation of the HPA axis during lactation can suppress immune function and increase vulnerability to infectious diseases, thus explaining why adult females in the free-ranging rhesus macaque population on Cayo Santiago have a higher probability of mortality during the birth season than during the mating season.

Species-specific patterns in fecal glucocorticoid and androgen levels in zoo-living orangutans (Pongo spp.)

“…Lactating females of both species had higher GC levels compared to nonlactating adult and immature females, a result that has also been found in other primate species (e.g. macaques; [27,34]). We also found a very small but significant linear increase in GC levels with increasing age in females, independent of sex and species.…”

“…In gorillas, post-partum maternal behavior was related negatively to urinary cortisol levels in the mother [4]. Higher stress levels and a heightened reactivity to stress during lactation was attributed to concerns about infant safety, especially in lower-ranking females, in a study carried out on rhesus macaques [27]. The higher stress levels of orangutan mothers living in social housing conditions may also be caused by the perception that their infants are at risk from other group members.…”

“…Since it is well known that GC secretion in female primates is influenced by reproductive state (e.g. [27,61]), we also entered this as a factor in the model. Two females were pregnant during the sampling period.…”

Effects of age on cerebrospinal fluid oxytocin levels in free-ranging adult female and infant rhesus macaques.

“…The following morning, blood and CSF samples were collected as described below. It is important to note that plasma cortisol and CSF oxytocin levels measured the morning after capture presumably reflect the cumulative stressful effects of capture and overnight housing (Hoffman et al , in press; Laudenslager et al , 1999; Maestripieri et al , 2008), rather than basal hormone levels in free-ranging monkeys.…”

Social status, glucocorticoids, immune function, and health: Can animal studies help us understand human socioeconomic-status-related health disparities?

“…For blood measures (plasma, serum), we indicate whether basal (undisturbed) or stimulated levels were measured. Estimates of basal levels come from blood samples collected within minutes of animal disturbance whereas most stimulated measures come from blood samples collected 20-60 min after capture (Hoffman et al, 2010 represents an exception to this in that their stimulated blood samples were collected 24 h following capture). Period of CORT sampling: refers to how many days, weeks (wk), months (mo), or years (yr) samples were collected.…”