Faecal glucocorticoid metabolite profiles in diademed sifakas increase during seasonal fruit scarcity with interactive effects of age/sex class and habitat degradation

We measured faecal glucocorticoid metabolites (GCs) in Critically Endangered diademed sifaka to understand how food availability, nutritional intake and habitat disturbance impact stress physiology. GCs elevated with food scarcity and correlated negatively with feeding time. Attenuated GCs in fragmented forest groups suggest a downregulated response to a chronically poor environment. Abstract Glucocorticoids are metabolic byproducts of animals' physiological responses to ecological or social challenges and are thought to represent an adaptive response allowing beneficial responses to short-term challenges. Glucocorticoid metabolites (GCs) can be assayed non-invasively through faeces and therefore can be a useful tool to gauge the health of populations experiencing natural and/or anthropogenic stressors. However, the response of GCs to anthropogenic stressors varies, with both higher and lower GC levels reported. Here, we describe variation in GC secretion within eight diademed sifaka (Propithecus diadema) groups across 1 year. These groups span a gradient of anthropogenic habitat disturbance, including groups in continuous forest (CONT') and disturbed fragments (FRAG'), and indicators of health suggest that FRAG groups are negatively impacted by habitat disturbance. We monitored phenology, used focal animal follows to quantify diet and collected faeces (n = 547) from which we quantified GC content using enzyme immunoassay. All groups showed elevated lean-season GCs, but with a single, brief peak. GCs were inversely correlated with feeding time. No overall effect of habitat (CONT vs. FRAG) was found, but the lean-season peak was significantly higher in CONT groups. There was a significant season*age-sex interaction; adult females had an attenuated lean-season response compared with groupmates. The observed lean-season challenge' is consistent with previous lemur studies, as well as mammals in general. Low and largely invariable GC levels in FRAG, within the context of observed health and nutritional declines, suggest that FRAG groups employ a strategy whereby the adrenal response to stressors is downregulated. More research is needed to contextualize our observations of GC variation and health on an individual level, both in terms of corroborating evidence for ecological and social stressors, and longer-term quantification of reproductive success and fitness.National Geographic Society Committee for Research and Exploration; Rowe/Wright Primate Fund; University of Arizona School of Anthropology; Institute for the Environment; Provost's Office; College of Social and Behavioral Sciences; BIO5Open access journalThis item from the UA Faculty Publications collection is made available by the University of Arizona with support from the University of Arizona Libraries. If you have questions, please contact us at [email protected]

The Nutritional Geometry of Resource Scarcity: Effects of Lean Seasons and Habitat Disturbance on Nutrient Intakes and Balancing in Wild Sifakas

<div><p>Animals experience spatial and temporal variation in food and nutrient supply, which may cause deviations from optimal nutrient intakes in both absolute amounts (meeting nutrient requirements) and proportions (nutrient balancing). Recent research has used the geometric framework for nutrition to obtain an improved understanding of how animals respond to these nutritional constraints, among them free-ranging primates including spider monkeys and gorillas. We used this framework to examine macronutrient intakes and nutrient balancing in sifakas (<i>Propithecus diadema</i>) at Tsinjoarivo, Madagascar, in order to quantify how these vary across seasons and across habitats with varying degrees of anthropogenic disturbance. Groups in intact habitat experience lean season decreases in frugivory, amounts of food ingested, and nutrient intakes, yet preserve remarkably constant proportions of dietary macronutrients, with the proportional contribution of protein to the diet being highly consistent. Sifakas in disturbed habitat resemble intact forest groups in the relative contribution of dietary macronutrients, but experience less seasonality: all groups’ diets converge in the lean season, but disturbed forest groups largely fail to experience abundant season improvements in food intake or nutritional outcomes. These results suggest that: (1) lemurs experience seasonality by maintaining nutrient balance at the expense of calories ingested, which contrasts with earlier studies of spider monkeys and gorillas, (2) abundant season foods should be the target of habitat management, even though mortality might be concentrated in the lean season, and (3) primates’ within-group competitive landscapes, which contribute to variation in social organization, may vary in complex ways across habitats and seasons.</p></div

Habitat characteristics, sample size, average daily energy and protein intakes, and ratio of available protein to non-protein energy (fat, carbohydrate and NDF) for five sifaka groups at Tsinjoarivo, Madagascar.

<p>Habitat characteristics, sample size, average daily energy and protein intakes, and ratio of available protein to non-protein energy (fat, carbohydrate and NDF) for five sifaka groups at Tsinjoarivo, Madagascar.</p

Macronutrient balancing in sifaka groups across seasons at Tsinjoarivo, Madagascar.

<p>Right-angle mixture triangle (RMT) plots showing the proportional contribution of protein, fat and carbohydrates to macronutrient-derived energy intakes for five sifaka groups at Tsinjoarivo, Madagascar across five seasons (1, 4 and 5 represent the lean season). Fat and protein are represented on the y- and x-axes, respectively, and carbohydrate is represented by an implicit axis Z. For clarity, each plot has two “isolines” representing 60% and 80% carbohydrates, shown with dotted lines.</p

Schematic depicting different lean season “rules of compromise” when nutritional target (bullseye) cannot be met.

<p>The abundant season target is assumed to be a balanced target achieved using fruits (lower AP:NPE ratio, steeper nutritional rail) and non-fruit foods (higher AP:NPE ratio, shallower nutritional rail), and one of the major constraints of the lean season is modeled as reduced fruit availability (solid component of fruit nutritional rail). Lower fruit availability in the lean season contracts the available nutritional space from all grey areas to the darker grey area. Mountain gorillas (1) overeat protein-rich non-fruit foods to meet NPE target; spider monkeys (2) fall short on non-protein energy target but meet protein target. Sifakas might be constrained by both fruit availability and a need to preserve the abundant season’s AP:NPE ratio (3), or intakes might be further limited by plant secondary metabolites (PSMs), which limit non-fruit intakes and would explain low lean season mass intakes (4). Note that different species are likely to differ in their “starting points” (a common starting point is used for simplicity of representation); for example, mountain gorillas’ abundant season “targets” are relatively higher in protein than either spider monkeys or sifakas.</p

Foraging and intake variables for five sifaka groups across five seasons at Tsinjoarivo, Madagascar.

<p>The lean season is indicated by grey shading, error bars represent standard error.</p

Seasonality in the contribution of protein to the diet in sifaka groups at Tsinjoarivo, Madagascar.

<p>Bivariate plots showing absolute seasonal averages (daily intakes ± SE) of protein (x-axis) and non-protein energy (fat + carbohydrate + NDF; y-axis), both expressed in kJ, for five sifaka groups at Tsinjoarivo, Madagascar. The fit line represents a linear regression forced through the origin as a visual approximation of each group’s nutritional rail (with grey dashed lines indicating rails for groups in the other panel). The shaded area represents nutritional space (i) left of a vertical line representing estimated minimum protein requirement of 2.8 g●BM_kg^-1●day^-1, equivalent to 234 kJ for a 5-kg sifaka, and/or (ii) below an oblique line representing 500 kJ●BM_kg^-0.762●day^-1, equivalent to 1703 kJ for a 5-kg sifaka (see <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0128046#sec012" target="_blank">discussion</a> for details on requirements).</p