Density feedbacks mediate effects of environmental change on population dynamics of a semidesert rodent.

Population dynamics are the result of an interplay between extrinsic and intrinsic environmental drivers. Predicting the effects of environmental change on wildlife populations therefore requires a thorough understanding of the mechanisms through which different environmental drivers interact to generate changes in population size and structure. In this study, we disentangled the roles of temperature, food availability and population density in shaping short- and long-term population dynamics of the African striped mouse, a small rodent inhabiting a semidesert with high intra- and interannual variation in environmental conditions. We parameterized a female-only stage-structured matrix population model with vital rates depending on temperature, food availability and population density, using monthly mark-recapture data from 1609 mice trapped over 9 years (2005-2014). We then applied perturbation analyses to determine relative strengths and demographic pathways of these drivers in affecting population dynamics. Furthermore, we used stochastic population projections to gain insights into how three different climate change scenarios might affect size, structure and persistence of this population. We identified food availability, acting through reproduction, as the main driver of changes in both short- and long-term population dynamics. This mechanism was mediated by strong density feedbacks, which stabilized the population after high peaks and allowed it to recover from detrimental crashes. Density dependence thus buffered the population against environmental change, and even adverse climate change scenarios were predicted to have little effect on population persistence (extinction risk over 100 years <5%) despite leading to overall lower abundances. Explicitly linking environment-demography relationships to population dynamics allowed us to accurately capture past population dynamics. It further enabled establishing the roles and relative importances of extrinsic and intrinsic environmental drivers, and we conclude that doing this is essential when investigating impacts of climate change on wildlife populations.

Differential plasticity of size and mass to environmental change in a hibernating mammal.

Morphological changes following changes in species' distribution and phenology have been suggested to be the third universal response to global environmental change. Although structural size and body mass result from different genetic, physiological, and ecological mechanisms, they are used interchangeably in studies evaluating population responses to environmental change. Using a 22-year (1991-2013) dataset including 1768 individuals, we investigated the coupled dynamics of size and mass in a hibernating mammal, the Alpine marmot (Marmota marmota), in response to local environmental conditions. We (i) quantified temporal trends in both traits, (ii) determined the environmental drivers of trait dynamics, and (iii) identified the life-history processes underlying the observed changes. Both phenotypic traits were followed through life: we focused on the initial trait value (juvenile size and mass) and later-life development (annual change in size [Δsize] and mass [Δmass]). First, we demonstrated contrasting dynamics between size and mass over the study period. Juvenile size and subsequent Δsize showed significant declines, whereas juvenile mass and subsequent Δmass remained constant. As a consequence of smaller size associated with a similar mass, individuals were in better condition in recent years. Second, size and mass showed different sensitivities to environmental variables. Both traits benefited from early access to resources in spring, whereas Δmass, particularly in early life, also responded to summer and winter conditions. Third, the interannual variation in both traits was caused by changes in early life development. Our study supports the importance of considering the differences between size and mass responses to the environment when evaluating the mechanisms underlying population dynamics. The current practice of focusing on only one trait in population modeling can lead to misleading conclusions when evaluating species' resilience to contemporary climate change.

Convenience polyandry or convenience polygyny? Costly sex under female control in a promiscuous primate.

Classic sex roles depict females as choosy, but polyandry is widespread. Empirical attempts to understand the evolution of polyandry have often focused on its adaptive value to females, whereas 'convenience polyandry' might simply decrease the costs of sexual harassment. We tested whether constraint-free female strategies favour promiscuity over mating selectivity through an original experimental design. We investigated variation in mating behaviour in response to a reversible alteration of sexual dimorphism in body mass in the grey mouse lemur, a small primate where female brief sexual receptivity allows quantifying polyandry. We manipulated body condition in captive females, predicting that convenience polyandry would increase when females are weaker than males, thus less likely to resist their solicitations. Our results rather support the alternative hypothesis of 'adaptive polyandry': females in better condition are more polyandrous. Furthermore, we reveal that multiple mating incurs significant energetic costs, which are strikingly symmetrical between the sexes. Our study shows that mouse lemur females exert tight control over mating and actively seek multiple mates. The benefits of remating are nevertheless not offset by its costs in low-condition females, suggesting that polyandry is a flexible strategy yielding moderate fitness benefits in this small mammal.

Torpor use during gestation and lactation in a primate.

Torpor is an energy-saving mechanism that allows endotherms to overcome energetic challenges. Torpor should be avoided during reproduction because of potential incompatibility with offspring growth. To test if torpor can be used during gestation and lactation to compensate for food shortage, we exposed reproductive female grey mouse lemurs (Microcebus murinus), a heterothermic primate, to different levels of food availability. Torpor use was characterised by daily skin temperature profiles, and its energetic outcome was assessed from changes in body mass. Food shortage triggered torpor during the end of the gestation period (n = 1), ranging from shallow in response to 40% food restriction to deep daily torpor in response to 80% restriction. During the early period of lactation, females fed ad libitum (n = 2) or exposed to a 40% restriction (n = 4) remained normothermic; but 80% food restricted females (n = 5) gave priority to energy saving, increasing the frequency and depth of torpor bouts. The use of torpor was insufficient to compensate for 80% energetic shortage during lactation resulting in loss of mass from the mother and delayed growth in the pups. This study provides the first evidence that a heterothermic primate can use torpor to compensate for food shortages even during reproduction. This physiological flexibility likely evolved as a response to climate-driven fluctuations in food availability in Madagascar.

Physiological flexibility and acclimation to food shortage in a heterothermic primate.

As ecosystems undergo changes worldwide, physiological flexibility is likely to be an important adaptive response to increased climate instability. Extreme weather fluctuations impose energetical constraints such as unpredictable food shortage. We tested how grey mouse lemurs (Microcebus murinus) could adjust their daily heterothermy and locomotor activity to these 'energetic accidents' with a food restriction experiment. The experimental design consisted of acute calorie restriction (2 weeks, 80% restriction) in the middle of winter, after a fattening season with low (11 weeks, 40% restriction) versus high (ad libitum) food availability. This design aimed at simulating the combined effects of the quality of the fattening season (acclimation effect) and a sudden, severe food shortage during the lean season. Hour of start and duration of torpor were the most flexible components of energy savings, increasing in response to the acute food shortage with facilitation by chronic restriction (acclimation effect). Modulations of locomotor activity did not support the hypothesis of energy savings, as total locomotor activity was not reduced. Nonetheless, acutely restricted individuals modified their temporal pattern of locomotor activity according to former food availability. We provide the first experimental evidence of different temporal levels of flexibility of energy-saving mechanisms in a heterotherm exposed to food shortage. The acclimation effect of past food scarcity suggests that heterothermic organisms are better able to respond to unpredicted food scarcity during the lean season. The flexible control of energy expenditure conferred by heterothermy may facilitate the plastic response of heterothermic species to more frequent climatic hazards.

High Yolk Testosterone Transfer Is Associated with an Increased Female Metabolic Rate.

Yolk androgens of maternal origin are important mediators of prenatal maternal effects. Although in many species short-term benefits of exposure to high yolk androgen concentrations for the offspring have been observed, females differ substantially in the amount of androgens they transfer to their eggs. It suggests that costs for the offspring or the mother constrain the evolution of maternal hormone transfer. However, to date, the nature of these costs remains poorly understood. Unlike most previous work that focused on potential costs for the offspring, we here investigated whether high yolk testosterone transfer is associated with metabolic costs (i.e., a higher metabolic rate) for the mother. We show that Japanese quail (Coturnix japonica) females that deposit higher testosterone concentrations into their eggs have a higher resting metabolic rate. Because a higher metabolic rate is often associated with a shorter life span, this relationship may explain the negative association between yolk testosterone transfer and female longevity observed in the wild. Our results suggest that metabolic costs for the mother can balance the short-term benefits of yolk testosterone exposure for the offspring, thereby contributing to the maintenance of variation in maternal yolk hormone transfer in natural populations.

Reproductive resilience to food shortage in a small heterothermic primate.

The massive energetic costs entailed by reproduction in most mammalian females may increase the vulnerability of reproductive success to food shortage. Unexpected events of unfavorable climatic conditions are expected to rise in frequency and intensity as climate changes. The extent to which physiological flexibility allows organisms to maintain reproductive output constant despite energetic bottlenecks has been poorly investigated. In mammals, reproductive resilience is predicted to be maximal during early stages of reproduction, due to the moderate energetic costs of ovulation and gestation relative to lactation. We experimentally tested the consequences of chronic-moderate and short-acute food shortages on the reproductive output of a small seasonally breeding primate, the grey mouse lemur (Microcebus murinus) under thermo-neutral conditions. These two food treatments were respectively designed to simulate the energetic constraints imposed by a lean year (40% caloric restriction over eight months) or by a sudden, severe climatic event occurring shortly before reproduction (80% caloric restriction over a month). Grey mouse lemurs evolved under the harsh, unpredictable climate of the dry forest of Madagascar and should thus display great potential for physiological adjustments to energetic bottlenecks. We assessed the resilience of the early stages of reproduction (mating success, fertility, and gestation) to these contrasted food treatments, and on the later stages (lactation and offspring growth) in response to the chronic food shortage only. Food deprived mouse lemurs managed to maintain constant most reproductive parameters, including oestrus timing, estrogenization level at oestrus, mating success, litter size, and litter mass as well as their overall number of surviving offspring at weaning. However, offspring growth was delayed in food restricted mothers. These results suggest that heterothermic, fattening-prone mammals display important reproductive resilience to energetic bottlenecks. More generally, species living in variable and unpredictable habitats may have evolved a flexible reproductive physiology that helps buffer environmental fluctuations.