Energetics in wild female Assamese macaques (Macaca assamensis): a behavioral and physiological approach

Abstract

Energy is a key requirement of life. It is involved in life history traits such as body maintenance, growth and reproduction. Energy is a limiting resource and therefore has to be strategically allocated. When facing an energetic challenge (e.g. low food availability), an individual energy balance, i.e. the difference between energy intake and expenditure, is likely to decrease, leading to shifts in energy-allocation strategies. Such challenging situations can bear drastic fitness consequences and two important adaptations have emerged in order to offset these energetic costs. First, individuals can modify their behavior to maximize energy intake and/or decrease energy expenditure. By adapting their feeding behavior and activity budget, individuals can therefore compensate the costs induced by energetic challenges. Second, physiological adaptations also participate in overcoming such costs. Major hormones such as insulin, thyroid hormones and glucocorticoids are involved in energy metabolism since they regulate energy assimilation, energy expenditure (through metabolic rate) and energy store mobilization. Their concentrations are typically modulated in times of energy deficit or heightened energy demands. A considerable advantage of these hormones is that they can be assessed non-invasively from urine samples. Behavioral and physiological shifts contribute to offsetting energetic costs. However, to date few studies have used an integrative approach investigating how such adaptations can act in concert when facing an energetic challenge. Such investigations are needed to determine complementary adaptations that have emerged concomitantly and to assess on a fine-scale energetic conditions induced by different challenges among mammals. In addition, this integrative approach will allow a better evaluation of the magnitude of the energetic costs of various challenges which will lend valuable insight into the way such energetic constraints might have driven life history traits in different species. In this thesis, I aim at investigating the behavioral and physiological responses to potential energetic challenges faced by female Assamese macaques (Macaca assamensis) in their seasonal natural habitat. I specifically examined the effects of cold ambient temperature, physical activity, low energy intake and female reproduction on female behavior and hormone levels. I collected behavioral and nutritional data and assessed urinary C-peptide (uCP, a marker of insulin production), triiodothyronine (T3, a thyroid hormone) and cortisol (one of the main glucocorticoids in vertebrates) levels. The results showed that the four energetic challenges triggered a specific combination of physiological and behavioral responses. First, low ambient temperatures induced a rise in cortisol but no rise in T3. This likely illustrates the fact that ambient temperatures did not decrease low enough or for long enough to trigger thermogenesis through an increase in T3 levels. A rise in cortisol alone might therefore be enough for female to cope with cold temperatures. Second, travel distance was not associated with a cortisol or a T3 response, suggesting that walking distances are not very energetically demanding in females. Third, a rise in cortisol was paired with a decline in T3 when energy intake is low. Energy intake can therefore be limited enough for females to mobilize their fat stores and reduce their metabolic rate in order to support their energetic needs and save energy, respectively. Fourth, a rise in cortisol was combined with a rise in T3 during late gestation, illustrating elevated energy requirements at this stage of the reproductive cycle. In addition, uCP levels were also high in late gestation which is likely induced by insulin resistance and maternal metabolic shifts in order to spare readily available energy to the fetus needs. The interpretation of similar levels of cortisol, T3 and uCP between lactating and non-gestating – non-lactating females were promoted by the integration of behavioral responses. Contrary to the other reproducing females, early lactating females follow a behavioral energy-conserving strategy (they rest more and feed efficiently), which might offset the energetic costs of lactation. This dissertation contributes to the growing body of literature in the use of non-invasive markers of energy. Integrating my findings with the other reported ones, I also highlight some uncertainty and inconsistencies and suggest some directions for future investigations. Lastly, my dissertation provides a powerful integrative approach when investigating energetic costs. I shed light on the importance of tackling research questions on energetics through a multifaceted prism by considering both physiological and behavioral responses, since one promotes the interpretation of the other.