Linking glucocorticoid variations to monthly and daily behavior in a wild endangered neotropical primate

Abstract

Identifying the factors swaying physiological stress levels in wild animals can help depict how they cope with environmental and social stressors, shedding light on their feeding ecology, behavioral plasticity, and adaptability. Here, we used noninvasive methods to explore the link between glucocorticoid levels and behavior in an endangered neotropical primate facing habitat fragmentation pressure, the black lion tamarin (Leontopithecus chrysopygus). We investigated monthly and day‐to‐day glucocorticoid variations independently to attempt to disentangle the complex nature of the adrenocortical activity. Between May 2019 to March 2020, we followed two groups of black lion tamarins in two different areas, a continuous forest and a small fragment, and gathered behavioral data (over 95 days in total; 8.6 ± 3.9 days/month) and fecal samples (Nsamples = 468; 4.93 ± 3.5 samples/day) simultaneously. Preliminary analyses enabled us to identify circadian variations linked to the biological rhythm, which were taken into account in subsequent models. Monthly analyses revealed that black lion tamarin fecal glucocorticoid metabolite levels vary according to changes in activity budget associated with the fruit consumption, movement, and resting time of the groups. At a day‐to‐day level, while intergroup encounters led to increases in fecal glucocorticoid metabolite concentrations, we found that changes in food intake or activity level did not trigger physiological stress responses. These findings suggest that diet and ranging patterns, driven by food availability and distribution, influence physiological stress at a seasonal scale, while acute stressors such as interspecific competition trigger short‐term stress responses. Exploring fecal glucocorticoid metabolite variations over different timescales can help uncover the predictive and reactive facets of physiological stress in wild species. Moreover, having a comprehensive understanding of the physiological state of species is a valuable conservation tool for evaluating how they cope in changing environments.

Analytical and biological validation of a noninvasive measurement of glucocorticoid metabolites in feces of Geoffroy's spider monkeys (Ateles geoffroyi)

“…The method is thus likely suitable for research questions focusing on factors that influence wild Geoffroy's spider monkeys' HPA activation in a similar magnitude as the physiological phenomena demonstrated here. However, it remains to be explored whether the methodology also allows to capture more subtle or more acute changes in HPA activation in an uncontrolled wild setting, such as those linked to involvement in affiliative or aggressive interactions (e.g., intergroup aggression: Kaisin et al, 2023; Schoof & Jack, 2013, affiliative interactions: Crockford et al, 2008).…”

“…The hypothalamus receives signals to initiate the cascade either from the central nervous system when fast signaling is required (e.g., a threat perceived by the senses) or by hormonal integration when reacting to slower changes in energetic demands within the body (Boonstra, 2013; Stanley et al, 2019). Hence, GCs allow individuals to cope with a wide variety of predictable (e.g., social interaction: Kaisin et al, 2023; seasonal food/water scarcity: Carnegie et al, 2011; Rimbach et al, 2014; seasonal changes in temperature: Beehner & McCann, 2008; reproduction: Strier et al, 2003) and unpredictable challenges (e.g., predation: Wasserman et al, 2013; dominance instability: Carnegie et al, 2011; logging/hunting/fragmentation: Rimbach et al, 2013).…”

“…These procedures also interfere with the animal's natural behavior and induce HPA activation (Suleman et al, 2004; Wasserman et al, 2013). To investigate the effects of naturally displayed behavior on GC concentrations in highly arboreal species, noninvasive collection of feces has proven to be effective, as feces usually reach the ground where they can be collected (Hodges & Heistermann, 2011; e.g., Carnegie et al, 2011; Kaisin et al, 2023; Rimbach et al, 2013). Fecal samples provide integrative information on HPA activity, as they reflect the GC concentrations of several hours up to several days, depending on the gut‐transit time of the study species (Hodges & Heistermann, 2011; Touma & Palme, 2005).…”

“…Such circadian rhythm is usually described for serum or salivary GC concentrations, but it might not be readily found in fGCM due to the integrative nature of fecal samples (Heistermann, 2010). Hence, significant effects of time of fecal sample collection have been found in some primate species (e.g., Ateles hybridus : Rimbach et al, 2013; Leontopithecus chrysopygus : Kaisin et al, 2023; Pan troglodytes : Murray et al, 2013) but not in others (e.g., Ateles geoffroyi : Ordóñez‐Gómez et al, 2016; Rodrigues et al, 2015; Procolobus gordonorum : Barelli et al, 2015; Gorilla gorilla : Shutt et al, 2012).…”