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

Abstract

The littoral forest on sandy soil is among the most threatened habitats in Madagascar and, as such, it represents a hot-spot within a conservation hot-spot. Assessing the health of the resident lemur fauna is not only critical for the long-term viability of these populations, but also necessary for the future re-habilitation of this unique habitat. Since the Endangered collared brown lemur, Eulemur collaris, is the largest seed disperser of the Malagasy south-eastern littoral forest its survival in this habitat is crucial. In this study we compared fecal glucocorticoid metabolite (fGCM) levels, a measure of physiological stress and potential early indicator of population health, between groups of collared brown lemurs living in a degraded forest fragment and groups occurring in a more preserved area. For this, we analysed 279 fecal samples collected year-round from 4 groups of collared brown lemurs using a validated 11-oxoetiocholanolone enzyme immunoassay and tested if fGCM levels were influenced by reproductive stages, phenological seasons, sex, and habitat degradation. The lemurs living in the degraded forest had significantly higher fGCM levels than those living in the more preserved area. In particular, the highest fGCM levels were found during the mating season in all animals and in females during gestation in the degraded forest. Since mating and gestation are both occurring during the lean season in the littoral forest, these results likely reflect a combination of ecological and reproductive pressures. Our findings provide a clear indication that habitat degradation has additive effects to the challenges found in the natural habitat. Since increased stress hormone output may have long-term negative effects on population health and reproduction, our data emphasize the need for and may add to the development of effective conservation plans for the species.

When can we measure stress noninvasively? Postdeposition effects on a fecal stress metric confound a multiregional assessment

“…Other studies have reliably correlated GCM concentration with habitat characteristics for a single population or several populations within the same region, where environmental variables are not likely to differ considerably (Balestri et al. ; Navarro‐Castilla et al. ; Davies et al.…”

“…), degradation (Balestri et al. ; Rizo‐Aguilar et al. ), and proximity to urban environments (French et al.…”

Lower levels of glucocorticoids in crop‐raiders: diet quality as a potential ‘pacifier’ against stress in free‐ranging Asian elephants in a human‐production habitat

“…For instance, elevated stress level observed in Asiatic black bears Ursus thibetanus outside a nature reserve has been related to lack of forest cover, human activity and diet of poorer quality (Malcolm et al, 2014), in grizzly bear Ursus arctos with increased anthropogenic disturbances such as logging areas, roads, railway lines and oil/gas well sites (Bourbonnais et al, 2013), in collared brown lemur Eulemur collaris with residence in degraded forest (Balestri et al, 2014), and in female African lesser bushbaby Galago moholi with urbanisation (Scheun et al, 2015). Yet, these studies do not explicitly tease apart the underlying causes but merely document stress levels in animals within and outside "natural" habitat.…”

Non‐invasive physiological markers demonstrate link between habitat quality, adult sex ratio and poor population growth rate in a vulnerable species, the Cape mountain zebra

“…Few studies have assessed physiological measures across more than one subpopulation of a wild animal species. Faecal glucocorticoid concentrations have been linked to food availability across barren‐ground caribou ( Rangifer tarandus ) populations (Joly, Wasser, & Booth, ), and to habitat degradation in collared brown lemur ( Eulemur collaris ; Balestri et al., ). However, no study has assessed the relative impact of both ecological and demographic factors on individual physiology across several subpopulations of a single species.…”

“…We non‐invasively sampled glucocorticoid and androgen hormone metabolites in adult individuals across seven populations, which vary in ecological factors (habitat quality or grass abundance, season, timing of peak rainfall), demography (adult sex ratio and group size) and measures of performance (population growth rate and female fecundity, or foal:mare ratio; see Lea et al., ). We hypothesised that (i) faecal glucocorticoid concentrations would be elevated in populations in low‐quality habitat (Balestri et al., ; du Dot et al., ; Gobush, Booth, & Wasser, ), (ii) faecal glucocorticoids would reflect seasonal variation such that they would be elevated during cold and/or dry conditions (Balestri et al., ; Landys et al., ; Vick et al., ), (iii) faecal androgen concentrations would be elevated in populations with a male‐biased adult sex ratio or high proportion of non‐breeding bachelor stallions (Le Galliard, Fitze, Ferrière, & Clobert, ; Penzhorn, ) and (iv) given the above hypotheses, female fecundity (foal:mare) and population growth rate should be negatively correlated with both hormones as low habitat quality and male‐biased sex ratios are negatively associated with the number of foals per mare in this species (Lea et al., ).…”