Measuring stress responses in female Geoffroy's spider monkeys: Validation and the influence of reproductive state

Abstract

Fecal glucocorticoid metabolites are increasingly used to investigate physiological stress. However, it is crucial for researchers to simultaneously investigate the effects of reproductive state because estradiol and placental hormones can affect circulating glucocorticoid concentrations. Reports on the relationships between glucocorticoids and reproductive state are inconsistent among females. Unlike several primate species that have heightened glucocorticoid activity during lactation, humans experience reduced glucocorticoid activity during lactation. Rather than a taxonomic difference, we hypothesize that this is a result of different environmental stressors, particularly the threat of infanticide. Here, we expand the number of wild primate species tested by validating a glucocorticoid assay for female Geoffroy's spider monkeys. We investigate the effects of reproductive state on their glucocorticoid concentrations. Utilizing a routine veterinary exam on a captive population, we determined that fecal glucocorticoid metabolites increase in response to a stressor (anesthesia), and this rise is detected approximately 24 hours later. Additionally, we found that extracted hormone patterns in a wild population reflected basic reproductive biology – estradiol concentrations were higher in cycling than lactating females, and in lactating females with older offspring who were presumably resuming their cycle. However, we found that estradiol and glucocorticoid concentrations were significantly correlated in lactating but not cycling females. Similarly, we found that reproductive state and estradiol concentration, but not stage of lactation, predicted glucocorticoid concentrations. Unlike patterns in several other primate species that face a relatively strong threat of infanticide, lactating spider monkeys experience reduced glucocorticoid activity, possibly due to attenuating effects of oxytocin and lower male-initiated aggression than directed at cycling females. More broadly, we conclude that future studies using fecal glucocorticoid metabolites to index stress should consider that reproductive state might confound glucocorticoid measurements.

Female Spider Monkeys (Ateles geoffroyi) Cope with Anthropogenic Disturbance Through Fission–Fusion Dynamics

“…Two Geoffroy’s spider monkey communities are present at El Zota: one community ranges in the northern primary forest, and the other ranges in the southern secondary forest (Lindshield 2006; Pruetz and LaDuke 2001; Rodrigues 2007, 2014; Rodrigues et al 2015). I studied the well-habituated Pilón community, which ranges in the southern secondary forest adjacent to the field station.…”

“…These 17 females were part of a community containing 39–41 individuals, including the females, 15 immature individuals, and 7–9 adult and subadult males (Rodrigues et al 2015). I determined reproductive condition retrospectively based on births and nursing.…”

“…I determined reproductive condition retrospectively based on births and nursing. My focal subjects were seven females that were cycling, six that were lactating, two that transitioned from late lactation to cycling, and two that were pregnant (Rodrigues et al 2015). I observed one female (JI) during pregnancy and early lactation, and one female (ST) during cycling, pregnancy, and early lactation.…”

“…This assay cross-reacts with multiple glucocorticoids and we validated it for use with captive female Geoffroyi’s spider monkeys (Rodrigues et al 2015). We washed cartridges with 1 mL of a 95:5 water: methanol solution.…”

“…The inter- and intraassay coefficients of variation for the two pools were 15.8/9 and 13.1/6. We previously established that estradiol had a significant effect on fecal glucocorticoid metabolite concentrations, but time of day and days in storage had no effect (Rodrigues et al 2015). …”