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

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.

A meta-analysis of anthropogenic impacts on physiological stress in wild primates.

As humanity continues to alter the environment extensively, comprehending the effect of anthropogenic disturbances on the health, survival, and fitness of wildlife is a crucial question for conservation science. Many primate populations occupy suboptimal habitats prone to diverse anthropogenic disturbances that may be sources of acute and chronic stress. Quantification of glucocorticoid (GC) concentrations has repeatedly been used to explore the impact of disturbances on physiological stress. Although it is still debated, prolonged elevation of GC levels may impair reproduction, growth, and immune system activity of individuals. We quantified the effect of anthropogenic disturbances on physiological stress in primates with a global meta-analysis based on data from 26 articles, covering 24 distinct species in 13 different countries. Anthropogenic disturbances were classified into 6 distinct categories: habitat loss, habitat degradation, ongoing logging, hunting, tourism, and other human activities. We calculated effect sizes (Hedges' g) with the standardized mean difference in GC concentrations between primates affected by human activity and their undisturbed conspecifics. We ran random-effects models and subgroup analyses to estimate the overall effect as well as a cumulative effect size for each disturbance category. Overall, primates inhabiting sites subject to anthropogenic disturbances exhibited significantly higher GC levels (g = 0.60; 95% CI: 0.28-0.93). Habitat loss and hunting were overall associated with increased GC concentrations, whereas the cumulative effects of the other disturbances were not statistically significant. Biologically, high GC levels may increase fitness by enabling individuals to overcome the challenges linked to anthropogenic disturbances. However, primates in disturbed environments may have sustained elevated GC levels. To strengthen future research, it is necessary to control confounding factors systematically (e.g., diet, reproductive status, predatory pressure, and resource availability) and improve understanding of the link between GC levels and the health, fitness, and survival of animals.

Metaanálisis de los Impactos Antropogénicos sobre el Estrés Fisiológico de los Primates Salvajes Resumen Conforme la humanidad continúa alterando extensivamente el ambiente, comprender el efecto de las perturbaciones antropogénicas sobre la salud, supervivencia y la aptitud de la fauna silvestre es una cuestión muy importante para las ciencias de la conservación. Muchas poblaciones de primates ocupan hábitats subóptimos propensos a varias perturbaciones antropogénicas que pueden ser la fuente de estrés agudo y crónico. La cuantificación de las concentraciones de glucocorticoides se ha usado repetidamente para explorar el impacto de las perturbaciones sobre el estrés fisiológico. Aunque todavía es tema de debate, la elevación prolongada de los niveles de glucocorticoides puede afectar a la reproducción, el crecimiento y la actividad del sistema inmune de los individuos. Cuantificamos el efecto de las perturbaciones antropogénicas sobre el estrés fisiológico de los primates mediante un metaanálisis global basado en los datos tomados de 26 artículos, abarcando así a 24 especies distintas en 13 países diferentes. Las perturbaciones antropogénicas fueron clasificadas en seis categorías distintas: pérdida de hábitat, degradación del hábitat, explotación forestal en curso, cacería, turismo y otras actividades humanas. Calculamos los tamaños del efecto (la g de Hedges) con una diferencia media estandarizada en las concentraciones de glucocorticoides entre los primates afectados por la actividad humana y sus coespecíficos sin perturbaciones. Corrimos modelos de efectos al azar y análisis de subgrupos para estimar el efecto generalizado, así como un tamaño acumulativo de efecto para cada categoría de perturbación. En general, los primates que habitan sitios sujetos a alguna perturbación antropogénica exhibieron niveles de glucocorticoides significativamente más altos (g = 0.60, 95% CI 0.28 a 0.93). La pérdida de hábitat y la cacería fueron asociadas casi siempre con las concentraciones elevadas de glucocorticoides, mientras que los efectos acumulativos de las otras perturbaciones no fueron significativos estadísticamente. Biológicamente, los niveles altos de glucocorticoides pueden incrementar la aptitud al permitir que el individuo supere los retos relaciones con las perturbaciones antropogénicas. Sin embargo, los primates en los ambientes perturbados pueden tener niveles elevados sostenidos de glucocorticoides. Para fortalecer a las futuras investigaciones es necesario controlar sistemáticamente los factores desconcertantes (p. ej.: la dieta, el estado reproductivo, la presión por depredadores, la disponibilidad de recursos) y mejorar el entendimiento de la conexión entre los niveles de glucocorticoides y la salud, aptitud y supervivencia de los animales.

Foraging strategies underlying bird egg predation by macaques: A study using artificial nests.

Bird egg predation is widespread in non-human primates. Although nest predation is often described as opportunistic, little is known about foraging strategies and nest detection in primates. Since it is the prevalent cause of nest failure in the tropics, birds select nest sites within specific microhabitats and use different nest types to increase nesting success. Identifying the nests targeted by the northern pigtailed macaques (Macaca leonina), an omnivorous cercopithecine species, and known nest predator, will shine light on nest foraging strategies in primates. The aim of this research was to reveal if nest predation is a selective or opportunistic feeding behavior. We studied, using artificial nests and camera traps, the influence of nest type (open-cup vs. cavity), microhabitat (i.e., understory density, canopy cover, canopy height, ground cover, and presence vs. absence of thorns and lianas), and nest height, on nest predation by a troop of northern pigtailed macaques in the Sakaerat Biosphere Reserve (Thailand), a degraded environment. In our study, macaque predation on artificial nests was high; out of the 200 nests that were set up, 112 were plundered by macaques. Although predation rates decreased with nest height, nest type, and microhabitat had no significant effect on predation by macaques. Nest detectability and accessibility did not affect predation rates. Macaques actively searched for nests in different microhabitats, suggesting that nest predation by this primate might be considered a selective feeding behavior in this degraded habitat. Consequently, nest predation by this primate might have important conservation implications on the population dynamics of forest-dwelling bird species. Behavior observation methods, such as instantaneous scan sampling, may underestimate nest predation by primates, a furtive and cryptic behavior.