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.

Hormone-mediated foraging strategies in an uncertain environment: Insights into the at-sea behavior of a marine predator.

Hormones are extensively known to be physiological mediators of energy mobilization and allow animals to adjust behavioral performance in response to their environment, especially within a foraging context.Few studies, however, have narrowed focus toward the consistency of hormonal patterns and their impact on individual foraging behavior. Describing these relationships can further our understanding of how individuals cope with heterogeneous environments and exploit different ecological niches.To address this, we measured between- and within-individual variation of basal cortisol (CORT), thyroid hormone T3, and testosterone (TEST) levels in wild adult female Galápagos sea lions (Zalophus wollebaeki) and analyzed how these hormones may be associated with foraging strategies. In this marine predator, females exhibit one of three spatially and temporally distinct foraging patterns (i.e., "benthic," "pelagic," and "night" divers) within diverse habitat types.Night divers differentiated from other strategies by having lower T3 levels. Considering metabolic costs, night divers may represent an energetically conservative strategy with shorter dive durations, depths, and descent rates to exploit prey which migrate up the water column based on vertical diel patterns.Intriguingly, CORT and TEST levels were highest in benthic divers, a strategy characterized by congregating around limited, shallow seafloors to specialize on confined yet reliable prey. This pattern may reflect hormone-mediated behavioral responses to specific risks in these habitats, such as high competition with conspecifics, prey predictability, or greater risks of predation.Overall, our study highlights the collective effects of hormonal and ecological variation on marine foraging. In doing so, we provide insights into how mechanistic constraints and environmental pressures may facilitate individual specialization in adaptive behavior in wild populations.

Occurrence of Mycoplasmas in Galapagos Sea Lions (Zalophus wollebaeki) and their Association with Other Respiratory Pathogens.

During the 2018 breeding season, an outbreak of respiratory disease occurred among Galapagos sea lions (Zalophus wollebaeki) that inhabit rookeries near urban areas with introduced fauna such as dogs and cats. Several sea lions had nasal discharge and respiratory distress and were in poor body condition. Eighteen sea lions were captured for a general health assessment including collection of blood for serology and nasal discharge for culture and PCR. Samples were analyzed for 15 respiratory pathogens known to infect cats, dogs, and marine mammals. There was no evidence for interspecies pathogen transmission between Galapagos sea lions and domestic animals. Several bacterial pathogens associated with respiratory tract infection in the California sea lion (Zalophus californianus) were isolated. Mycoplasma spp. were identified by PCR in nasal discharge samples but were not the species commonly found in cats and dogs.

Individuality counts: A new comprehensive approach to foraging strategies of a tropical marine predator.

Foraging strategies are of great ecological interest, as they have a strong impact on the fitness of an individual and can affect its ability to cope with a changing environment. Recent studies on foraging strategies show a higher complexity than previously thought due to intraspecific variability. To reliably identify foraging strategies and describe the different foraging niches they allow individual animals to realize, high-resolution multivariate approaches which consider individual variation are required. Here we dive into the foraging strategies of Galápagos sea lions (Zalophus wollebaeki), a tropical predator confronted with substantial annual variation in sea surface temperature. This affects prey abundance, and El Niño events, expected to become more frequent and severe with climate change, are known to have dramatic effects on sea lions. This study used high-resolution measures of depth, GPS position and acceleration collected from 39 lactating sea lion females to analyze their foraging strategies at an unprecedented level of detail using a novel combination of automated broken stick algorithm, hierarchical cluster analysis and individually fitted multivariate hidden Markov models. We found three distinct foraging strategies (pelagic, benthic, and night divers), which differed in their horizontal, vertical and temporal distribution, most likely corresponding to different prey species, and allowed us to formulate hypotheses with regard to adaptive values under different environmental scenarios. We demonstrate the advantages of our multivariate approach and inclusion of individual variation to reliably gain a deeper understanding of the adaptive value and ecological relevance of foraging strategies of marine predators in dynamic environments.

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.

Climate variability and life history impact stress, thyroid, and immune markers in California sea lions (Zalophus californianus) during El Niño conditions.

Wildlife is exposed to a diverse set of extrinsic and intrinsic stressors, such as climatic variation or life history constraints, which may impact individual health and fitness. El Niño and climatic anomalies between 2013 and 2016 had major ecological impacts on the California Current ecosystem. As top marine predators, California sea lions (CSL) experienced decreased prey availability and foraging success, impacting their nutritional state. We hypothesize that chronic stress to juvenile CSL increased during the 2015-2016 El Niño and that breeding represents a period of chronic stress for adults, which impact a variety of physiological processes. We opportunistically captured and sampled juvenile CSL (female, n = 29; male, n = 38) in central California and adult male CSL (n = 76) in Astoria, Oregon and quantified a suite of analytes in serum as indicators of acute stress markers, metabolism and thyroid function, and adaptive immune response. We found that stress hormones and glucose were decreased in juvenile CSL during 2016 relative to 2015 and in adult male CSL after the breeding season, which may indicate chronic stress downregulating HPA (hypothalamic-pituitary-adrenal) axis sensitivity with associated metabolic impacts. Conversely, thyroid hormones for both juvenile and adult male CSL were increased, suggesting greater energetic requirements resulting from increased foraging activity during suboptimal conditions in juveniles and breeding tenure in adult males. Immunoglobulin IgG was elevated in juveniles in 2016 but reduced in adult males post-breeding. This suggests that juveniles may face immunostimulatory pressure during anomalously warm ocean environments; however, for adult males, breeding is a significant energetic cost resulting in reductions to immune function. Our results indicate that environmental conditions and life history stage may influence physiological responses in an important marine predator and a sentinel species of changing ocean ecosystems.

Parasitism Elicits a Stress Response That Allocates Resources for Immune Function in South American Fur Seals (Arctocephalus australis).

Parasites can cause chronic stress in some animal species, and this type of stress response has been associated with adverse consequences for the host. In order to know whether parasitism elicited a stress response associated with decreased host fitness, hookworm (Uncinaria sp.) infection was studied in a colony of South American fur seals (Arctocephalus australis) in which hookworms infect nearly all pups born in a reproductive season. A parasite-free group was generated by treating a subset of pups with an antiparasitic drug before they developed patent hookworm infection. Stress and metabolic hormones, energy balance, and humoral and cellular immune parameters were measured in this group and hookworm-infected pups. Hookworms elicited a marked increase in plasma cortisol levels in fur seal pups. These hookworm-infected pups were able to maintain constant glucose levels, despite losing body mass over the course of infection potentially because of increased protein catabolism. Infected pups were able to mount an effective immune response against the parasite and eliminated hookworms from the intestine, recovering partial body mass lost as a result of hookworm infection at the end of the study period. As shown in previous studies, adequate glucose levels are critical for proper T lymphocyte reactivity, and it is possible that, through activation of a stress response, energy can be readily available for immune response against the parasite contributing to early recovery from infection. Although there are potential fitness costs to mounting a sustained stress response, these could also be adaptive and promote survival during critical life-history stages.