A stable foraging polymorphism buffers Galápagos sea lions against environmental change.

Understanding the ability of animals to cope with a changing environment is critical in a world affected by anthropogenic disturbance.1 Individual foraging strategies may influence the coping ability of entire populations, as these strategies can be adapted to contrasting conditions, allowing populations with foraging polymorphisms to be more resilient toward environmental change.2,3 However, environmentally dependent fitness consequences of individual foraging strategies and their effects on population dynamics have not been conclusively documented.4,5 Here, we use biologging data from endangered Galápagos sea lion females (Zalophus wollebaeki) to show that benthically foraging individuals dig after sand-dwelling prey species while pelagic foragers hunt in more open waters. These specialized foraging behaviors result in distinct and temporally stable patterns of vibrissae abrasion. Using vibrissae length as a visual marker for the benthic versus pelagic foraging strategies, we furthermore uncovered an environment-dependent fitness trade-off between benthic and pelagic foragers, suggesting that the foraging polymorphism could help to buffer the population against the negative effects of climate change. However, demographic projections suggest that this buffering effect is unlikely to be sufficient to reverse the ongoing population decline of the past four decades.6 Our study shows how crucial a deeper understanding of behavioral polymorphisms can be for predicting how populations cope within a rapidly changing world. VIDEO ABSTRACT.

Developmental conditions promote individual differentiation of endocrine axes and behavior in a tropical pinniped.

Between-individual variation in behavior can emerge through complex interactions between state-related mechanisms, which include internal physiological constraints or feedback derived from the external environment. State-related conditions can be especially influential during early life, when parental effort and exposure to social stress may canalize consistent differences in offspring hormonal profiles and foster specific behavioral strategies. Here, we unravel how relevant state variables, including sex, somatic condition, local population density, and maternal traits, contribute to within-cohort differences in stress, sex, and thyroid hormone axes in dependent Galapagos sea lions with the primary goal of understanding downstream effects on boldness, docility, habitat use, and activity. Pups within denser natal sites had higher levels of cortisol and thyroid T4, a prohormone and proxy for metabolic reserves, likely as an adaptive physiological response after exposure to increased numbers of conspecific interactions. Furthermore, considering maternal effects, mothers in better body condition produced pups with higher testosterone yet downregulated basal cortisol and thyroid T4. This hormonal profile was correlated with increased boldness toward novel objects and attenuated stress responsiveness during capture. Intriguingly, pups with increased thyroid T3, the biologically active form, maintained faster somatic growth and were observed to have increased activity and extensively explored surrounding habitats. Collectively, these findings provide comprehensive evidence for several links to hormone-mediated behavioral strategies, highlighted by variation in socio-environmental and maternally derived input during a foundational life stage.