Validation of an enzyme immunoassay for assessing adrenocortical activity and evaluation of factors that affect levels of fecal glucocorticoid metabolites in two New World primates

Abstract

Non-invasive methods to assess stress hormone output via fecal glucocorticoid metabolites (FGCMs) have become a powerful tool in behavioral studies and conservation biology because they allow exploring the link between behavior, an animal's socio-ecological environment and its adrenocortical activity. However, FGCM levels are influenced by numerous other factors which often confound their interpretation. Thus, before applying these methods, knowledge on the impact of these factors is important. In this study we investigated the effect of (1) time of day, (2) age, (3) sex and (4) female reproductive state on FGCM levels in brown spider monkeys (Ateles hybridus) and red howler monkeys (Alouatta seniculus). Initially, we validated a 11β-hydroxyetiocholanolone enzyme immunoassay for monitoring the physiological stress response via fecal analysis in both species. We determined FGCM levels in fecal samples collected from two and six groups of wild spider monkeys (n=461 samples) and howler monkeys (n=166 samples), respectively. Our analyses revealed a strong effect of time of day on FGCM levels in spider monkeys, but no effect in howler monkeys. Adults of both species had significantly higher FGCM levels than subadults. In neither of the two species we found a sex-effect on FGCM output. Reproductive condition strongly affected FGCM levels in female spider monkeys which showed increasing concentrations with progressing gestation. This was not investigated in female howler monkeys due to an insufficient sample size. Our data indicate that the influence of the tested factors on fecal glucocorticoid metabolite output is species-specific, and that these variables need to be considered when interpreting FGCM levels in the species.

Sex, social status and physiological stress in primates: the importance of social and glucocorticoid dynamics

“…For example, GC metabolism differs between sexes in mice, rats and other rodents, with males typically excreting higher concentrations than females, with exceptions [123,124,127,128], and the specific FGCMs excreted are sexand species-specific [123][124][125]. Quantification of circadian rhythm is difficult: FGCMs can show a diurnal rhythm mirroring that of circulating GCs, but this rhythm can only be documented in animals that defecate multiple times per day [124,126,127]. Intestinal transit time, which regulates FGCM excretion rate, is influenced by physical activity; rodents excrete GCs more rapidly during the active versus passive phases [123].…”

The Effect of Fission–Fusion Zoo Housing on Hormonal and Behavioral Indicators of Stress in Bornean Orangutans (Pongo pygmaeus)

“…We also found no age effect on fGCM concentrations. In contrast, glucocorticoid concentrations have been reported to be higher in older individuals in humans, chimpanzees, brown spider monkeys (Ateles hybridus), and red howlers (Alouatta seniculus) (Rimbach et al 2013;Seraphin et al 2008;Van Cauter et al 1996). An earlier study on orangutans found a small significant increase in fGCM concentrations with increasing age in females but not in male orangutans (Weingrill et al 2011).…”

Habitat Degradation and Seasonality Affect Physiological Stress Levels of Eulemur collaris in Littoral Forest Fragments

“…In the case of primates, physiological stress levels have been shown to increase in males during mating seasons as a consequence of high reproductive competition [28]–[34], but not in species where mate competition is low [22], [35], [36]. Females, on the other hand, have higher energetic demands during gestation and lactation and this may also lead to higher physiological stress [34], [37]–[41]. This seems to hold true despite the fact that, in primates, females have been shown to have lower energetic costs during reproductive stages than other mammals of similar size [42]–[44].…”