Intracellular negative feedback mechanisms in blubber and muscle moderate acute stress responses in fasting seals.

Animals may limit the cost of stress responses during key life history stages such as breeding and molting by reducing tissue sensitivity to energy-mobilizing stress hormones (e.g. cortisol). We measured expression of genes encoding glucocorticoid receptor (GR, NR3C1), GR inhibitor (FKBP5) and cortisol-inactivating enzyme (HSD11B2) in blubber and muscle of northern elephant seals before and after stress axis stimulation by adrenocorticotropic hormone (ACTH) early and late in a fasting period associated with molting. ACTH elevated cortisol levels for >24 h and increased FKBP5 and HSD11B2 expression while downregulating NR3C1 expression in blubber and muscle, suggesting robust intracellular negative feedback in peripheral tissues. This feedback was maintained over prolonged fasting, despite differences in baseline cortisol and gene expression levels between early and late molt, suggesting that fasting-adapted animals use multiple tissue-specific, intracellular negative feedback mechanisms to modulate downstream impacts of acute stress responses during key life history stages.

Adrenal response to ACTH challenge alters thyroid and immune function and varies with body reserves in molting adult female northern elephant seals.

Intrinsic stressors associated with life-history stages may alter the responsiveness of the hypothalamic-pituitary-adrenal axis and responses to extrinsic stressors. We administered adrenocorticotropic hormone (ACTH) to 24 free-ranging adult female northern elephant seals (NESs) at two life-history stages: early and late in their molting period and measured a suite of endocrine, immune, and metabolite responses. Our objective was to evaluate the impact of extended, high-energy fasting on adrenal responsiveness. Animals were blood sampled every 30 min for 120 min post-ACTH injection, then blood was sampled 24 h later. In response to ACTH injection, cortisol levels increased 8- to 10-fold and remained highly elevated compared with baseline at 24 h. Aldosterone levels increased 6- to 9-fold before returning to baseline at 24 h. The magnitude of cortisol and aldosterone release were strongly associated, and both were greater after extended fasting. We observed an inverse relationship between fat mass and the magnitude of cortisol and aldosterone responses, suggesting that body reserves influenced adrenal responsiveness. Sustained elevation in cortisol was associated with alterations in thyroid hormones; both tT3 and tT4 concentrations were suppressed at 24 h, while rT3 increased. Immune cytokine IL-1ß was also suppressed after 24 h of cortisol elevation, and numerous acute and sustained impacts on substrate metabolism were evident. Our data suggest that female NESs are more sensitive to stress after the molt fast and that acute stress events can have important impacts on metabolism and immune function. These findings highlight the importance of considering life-history context when assessing the impacts of anthropogenic stressors on wildlife.

Effects of disease on foraging behaviour and success in an individual free-ranging northern elephant seal.

Evaluating consequences of stressors on vital rates in marine mammals is of considerable interest to scientific and regulatory bodies. Many of these species face numerous anthropogenic and environmental disturbances. Despite its importance as a critical form of mortality, little is known about disease progression in air-breathing marine megafauna at sea. We examined the movement, diving, foraging behaviour and physiological state of an adult female northern elephant seal (Mirounga angustirostris) who suffered from an infection while at sea. Comparing her to healthy individuals, we identified abnormal behavioural patterns from high-resolution biologging instruments that are likely indicators of diseased and deteriorating condition. We observed continuous extended (3-30 minutes) surface intervals coinciding with almost no foraging attempts (jaw motion) during 2 weeks of acute illness early in her post-breeding foraging trip. Elephant seals typically spend ~ 2 minutes at the surface. There were less frequent but highly extended (30-200 minutes) surface periods across the remainder of the trip. Dive duration declined throughout the trip rather than increasing. This seal returned in the poorest body condition recorded for an adult female elephant seal (18.3% adipose tissue; post-breeding trip average is 30.4%). She was immunocompromised at the end of her foraging trip and has not been seen since that moulting season. The timing and severity of the illness, which began during the end of the energy-intensive lactation fast, forced this animal over a tipping point from which she could not recover. Additional physiological constraints to foraging, including thermoregulation and oxygen consumption, likely exacerbated her already poor condition. These findings improve our understanding of illness in free-ranging air-breathing marine megafauna, demonstrate the vulnerability of individuals at critical points in their life history, highlight the importance of considering individual health when interpreting biologging data and could help differentiate between malnutrition and other causes of at-sea mortality from transmitted data.

Reduction of Paraoxonase Expression Followed by Inactivation across Independent Semiaquatic Mammals Suggests Stepwise Path to Pseudogenization.

Convergent adaptation to the same environment by multiple lineages frequently involves rapid evolutionary change at the same genes, implicating these genes as important for environmental adaptation. Such adaptive molecular changes may yield either change or loss of protein function; loss of function can eliminate newly deleterious proteins or reduce energy necessary for protein production. We previously found a striking case of recurrent pseudogenization of the Paraoxonase 1 (Pon1) gene among aquatic mammal lineages-Pon1 became a pseudogene with genetic lesions, such as stop codons and frameshifts, at least four times independently in aquatic and semiaquatic mammals. Here, we assess the landscape and pace of pseudogenization by studying Pon1 sequences, expression levels, and enzymatic activity across four aquatic and semiaquatic mammal lineages: pinnipeds, cetaceans, otters, and beavers. We observe in beavers and pinnipeds an unexpected reduction in expression of Pon3, a paralog with similar expression patterns but different substrate preferences. Ultimately, in all lineages with aquatic/semiaquatic members, we find that preceding any coding-level pseudogenization events in Pon1, there is a drastic decrease in expression, followed by relaxed selection, thus allowing accumulation of disrupting mutations. The recurrent loss of Pon1 function in aquatic/semiaquatic lineages is consistent with a benefit to Pon1 functional loss in aquatic environments. Accordingly, we examine diving and dietary traits across pinniped species as potential driving forces of Pon1 functional loss. We find that loss is best associated with diving activity and likely results from changes in selective pressures associated with hypoxia and hypoxia-induced inflammation.

Brain activity of diving seals reveals short sleep cycles at depth.

Sleep is a crucial part of the daily activity patterns of mammals. However, in marine species that spend months or entire lifetimes at sea, the location, timing, and duration of sleep may be constrained. To understand how marine mammals satisfy their daily sleep requirements while at sea, we monitored electroencephalographic activity in wild northern elephant seals (Mirounga angustirostris) diving in Monterey Bay, California. Brain-wave patterns showed that seals took short (less than 20 minutes) naps while diving (maximum depth 377 meters; 104 sleeping dives). Linking these patterns to accelerometry and the time-depth profiles of 334 free-ranging seals (514,406 sleeping dives) revealed a North Pacific sleepscape in which seals averaged only 2 hours of sleep per day for 7 months, rivaling the record for the least sleep among all mammals, which is currently held by the African elephant (about 2 hours per day).

Physiological tipping points in the relationship between foraging success and lifetime fitness of a long-lived mammal.

Although anthropogenic change is often gradual, the impacts on animal populations may be precipitous if physiological processes create tipping points between energy gain, reproduction or survival. We use 25 years of behavioural, diet and demographic data from elephant seals to characterise their relationships with lifetime fitness. Survival and reproduction increased with mass gain during long foraging trips preceding the pupping seasons, and there was a threshold where individuals that gained an additional 4.8% of their body mass (26 kg, from 206 to 232 kg) increased lifetime reproductive success three-fold (from 1.8 to 4.9 pups). This was due to a two-fold increase in pupping probability (30% to 76%) and a 7% increase in reproductive lifespan (6.0 to 6.4 years). The sharp threshold between mass gain and reproduction may explain reproductive failure observed in many species and demonstrates how small, gradual reductions in prey from anthropogenic disturbance could have profound implications for animal populations.

Mercury Bioaccumulation and Cortisol Interact to Influence Endocrine and Immune Biomarkers in a Free-Ranging Marine Mammal.

Mercury bioaccumulation from deep-ocean prey and the extreme life history strategies of adult female northern elephant seals (Mirounga angustirostris) provide a unique system to assess the interactive effects of mercury and stress on animal health by quantifying blood biomarkers in relation to mercury (skeletal muscle and blood mercury) and cortisol concentrations. The thyroid hormone thyroxine (tT4) and the antibody immunoglobulin E (IgE) were associated with mercury and cortisol concentrations interactively, where the magnitude and direction of the association of each biomarker with mercury or cortisol changed depending on the concentration of the other factor. For example, when cortisol concentrations were lowest, tT4 was positively related to muscle mercury, whereas tT4 had a negative relationship with muscle mercury in seals that had the highest cortisol concentrations. Additionally, we observed that two thyroid hormones, triiodothyronine (tT3) and reverse triiodothyronine (rT3), were negatively (tT3) and positively (rT3) associated with mercury concentrations and cortisol in an additive manner. As an example, tT3 concentrations in late breeding seals at the median cortisol concentration decreased by 14% across the range of observed muscle mercury concentrations. We also observed that immunoglobulin M (IgM), the pro-inflammatory cytokine IL-6 (IL-6), and a reproductive hormone, estradiol, were negatively related to muscle mercury concentrations but were not related to cortisol. Specifically, estradiol concentrations in late molting seals decreased by 50% across the range of muscle mercury concentrations. These results indicate important physiological effects of mercury on free-ranging apex marine predators and interactions between mercury bioaccumulation and extrinsic stressors. Deleterious effects on animals' abilities to maintain homeostasis (thyroid hormones), fight off pathogens and disease (innate and adaptive immune system), and successfully reproduce (endocrine system) can have significant individual- and population-level consequences.

Whiskers provide time-series of toxic and essential trace elements, Se:Hg molar ratios, and stable isotope values of an apex Antarctic predator, the leopard seal.

In an era of rapid environmental change and increasing human presence, researchers need efficient tools for tracking contaminants to monitor the health of Antarctic flora and fauna. Here, we examined the utility of leopard seal whiskers as a biomonitoring tool that reconstructs time-series of significant ecological and physiological biomarkers. Leopard seals (Hydrurga leptonyx) are a sentinel species in the Western Antarctic Peninsula due to their apex predator status and top-down effects on several Antarctic species. However, there are few data on their contaminant loads. We analyzed leopard seal whiskers (n = 18 individuals, n = 981 segments) collected during 2018-2019 field seasons to acquire longitudinal profiles of non-essential (Hg, Pb, and Cd) and essential (Se, Cu, and Zn) trace elements, stable isotope (ẟ15N and ẟ13C) values and to assess Hg risk with Se:Hg molar ratios. Whiskers provided between 46 and 286 cumulative days of growth with a mean ~ 125 days per whisker (n = 18). Adult whiskers showed variability in non-essential trace elements over time that could partly be explained by changes in diet. Whisker Hg levels were insufficient (<20 ppm) to consider most seals being at "high" risk for Hg toxicity. Nevertheless, maximum Hg concentrations observed in this study were greater than that of leopard seal hair measured two decades ago. However, variation in the Se:Hg molar ratios over time suggest that Se may detoxify Hg burden in leopard seals. Overall, we provide evidence that the analysis of leopard seal whiskers allows for the reconstruction of time-series ecological and physiological data and can be valuable for opportunistically monitoring the health of the leopard seal population and their Antarctic ecosystem during climate change.

Oxidative Stress Is a Potential Cost of Synchronous Nesting in Olive Ridley Sea Turtles.

Olive ridley sea turtles, Lepidochelys olivacea, exhibit a polymorphic reproductive behavior, nesting solitarily or in mass aggregations termed "arribadas", where thousands of individuals nest synchronously. Arribada nesting provides fitness benefits including mate finding during nearshore aggregations and predator satiation at the time of hatching, but it is unknown if such benefits come with a physiological cost. We used plasma metabolite profiling, stable isotope analysis, biochemical and endocrine assays to test whether metabolic parameters differ between nesting modes, and if arribada nesting is associated with increased levels of oxidative damage compared to solitary nesting. Arribada nesters were bigger and had higher circulating thyroid hormone levels than solitary nesters. Similarly, pathways related to phospholipid and amino acid metabolism, catabolic processes, and antioxidant defense were enriched in individuals nesting in arribada. Stable isotope signatures in skin samples showed differences in feeding zones with arribada nesters likely feeding on benthic and potentially more productive grounds. Arribada nesters had increased levels of plasma lipid peroxidation and protein oxidation products compared to solitary nesters. These results suggest that metabolic profiles differ between nesting modes and that oxidative stress is a trade-off for the fitness benefits associated with arribada nesting.

Elephant seals time their long-distance migrations using a map sense.

Many marine animals migrate between foraging areas and reproductive sites, often timing the return migration with extreme precision. In theory, the decision to return should reflect energy acquisition at foraging areas, energetic costs associated with transit, and timing arrival for successful reproduction. For long-distance migrations to be successful, animals must integrate 'map' information to assess where they are relative to their reproductive site as well as 'calendar' information to know when to initiate the return migration given their distance from home1. Elephant seals, Mirounga angustirostris, migrate thousands of kilometers from reproductive sites to open ocean foraging areas (Figure 1A), yet return within a narrow window of time to specific beaches2. Each year, pregnant female elephant seals undertake a ∼240-day, 10,000 km foraging migration across the Northeast Pacific Ocean before returning to their breeding beaches, where they give birth 5 days after arriving2. We found that the seals' abilities to adjust the timing of their return migration is based on the perception of space and time, which further elucidates the mechanisms behind their astonishing navigational feats3.

Changes in apolipoprotein abundance dominate proteome responses to prolonged fasting in elephant seals.

Unlike many animals that reduce activity during fasting, northern elephant seals (NES) undergo prolonged fasting during energy-intensive life-history stages such as reproduction and molting, fueling fasting energy needs by mobilizing fat stores accrued during foraging. NES display several unique metabolic features such as high fasting metabolic rates, elevated blood lipid and high-density lipoprotein (HDL) cholesterol levels, efficient protein sparing and resistance to oxidative stress during fasting. However, the cellular mechanisms that regulate these adaptations are still not fully understood. To examine how metabolic coordination is achieved during prolonged fasting, we profiled changes in blubber, skeletal muscle and plasma proteomes of adult female NES over a 5 week fast associated with molting. We found that while blubber and muscle proteomes were remarkably stable over fasting, over 50 proteins changed in abundance in plasma, including those associated with lipid storage, mobilization, oxidation and transport. Apolipoproteins dominated the blubber, plasma and muscle proteome responses to fasting. APOA4, APOE and APOC3, which are associated with lipogenesis and triglyceride accumulation, decreased, while APOA1, APOA2 and APOM, which are associated with lipid mobilization and HDL function, increased over fasting. Our findings suggest that changes in apolipoprotein composition may underlie the maintenance of high HDL levels and, together with adipokines and hepatokines that facilitate lipid catabolism, may mediate the metabolic transitions between feeding and fasting in NES. Many of these proteins have not been previously studied in this species and provide intriguing hypotheses about metabolic regulation during prolonged fasting in mammals.

Trade-offs between foraging reward and mortality risk drive sex-specific foraging strategies in sexually dimorphic northern elephant seals.

Sex-specific phenotypic differences are widespread throughout the animal kingdom. Reproductive advantages provided by trait differences come at a cost. Here, we link sex-specific foraging strategies to trade-offs between foraging reward and mortality risk in sexually dimorphic northern elephant seals (Mirounga angustirostris). We analyse a decadal dataset on movement patterns, dive behaviour, foraging success and mortality rates. Females are deep-diving predators in open ocean habitats. Males are shallow-diving benthic predators in continental shelf habitats. Males gain six times more mass and acquire energy 4.1 times faster than females. High foraging success comes with a high mortality rate. Males are six times more likely to die than females. These foraging strategies and trade-offs are related to different energy demands and life-history strategies. Males use a foraging strategy with a high mortality risk to attain large body sizes necessary to compete for females, as only a fraction of the largest males ever mate. Females use a foraging strategy with a lower mortality risk, maximizing reproductive success by pupping annually over a long lifespan. Our results highlight how sex-specific traits can drive disparity in mortality rates and expand species' niche space. Further, trade-offs between foraging rewards and mortality risk can differentially affect each sex's ability to maximize fitness.

Ontogeny of Carbon Monoxide-Related Gene Expression in a Deep-Diving Marine Mammal.

Marine mammals such as northern elephant seals (NES) routinely experience hypoxemia and ischemia-reperfusion events to many tissues during deep dives with no apparent adverse effects. Adaptations to diving include increased antioxidants and elevated oxygen storage capacity associated with high hemoprotein content in blood and muscle. The natural turnover of heme by heme oxygenase enzymes (encoded by HMOX1 and HMOX2) produces endogenous carbon monoxide (CO), which is present at high levels in NES blood and has been shown to have cytoprotective effects in laboratory systems exposed to hypoxia. To understand how pathways associated with endogenous CO production and signaling change across ontogeny in diving mammals, we measured muscle CO and baseline expression of 17 CO-related genes in skeletal muscle and whole blood of three age classes of NES. Muscle CO levels approached those of animals exposed to high exogenous CO, increased with age, and were significantly correlated with gene expression levels. Muscle expression of genes associated with CO production and antioxidant defenses (HMOX1, BVR, GPX3, PRDX1) increased with age and was highest in adult females, while that of genes associated with protection from lipid peroxidation (GPX4, PRDX6, PRDX1, SIRT1) was highest in adult males. In contrast, muscle expression of mitochondrial biogenesis regulators (PGC1A, ESRRA, ESRRG) was highest in pups, while genes associated with inflammation (HMOX2, NRF2, IL1B) did not vary with age or sex. Blood expression of genes involved in regulation of inflammation (IL1B, NRF2, BVR, IL10) was highest in pups, while HMOX1, HMOX2 and pro-inflammatory markers (TLR4, CCL4, PRDX1, TNFA) did not vary with age. We propose that ontogenetic upregulation of baseline HMOX1 expression in skeletal muscle of NES may, in part, underlie increases in CO levels and expression of genes encoding antioxidant enzymes. HMOX2, in turn, may play a role in regulating inflammation related to ischemia and reperfusion in muscle and circulating immune cells. Our data suggest putative ontogenetic mechanisms that may enable phocid pups to transition to a deep-diving lifestyle, including high baseline expression of genes associated with mitochondrial biogenesis and immune system activation during postnatal development and increased expression of genes associated with protection from lipid peroxidation in adulthood.

Density-dependent effects on reproductive output in a capital breeding carnivore, the northern elephant seal (Mirounga angustirostris).

All organisms face resource limitations that will ultimately restrict population growth, but the controlling mechanisms vary across ecosystems, taxa, and reproductive strategies. Using four decades of data, we examine how variation in the environment and population density affect reproductive outcomes in a capital-breeding carnivore, the northern elephant seal (Mirounga angustirostris). This species provides a unique opportunity to examine the relative importance of resource acquisition and density-dependence on breeding success. Capital breeders accrue resources over large temporal and spatial scales for use during an abbreviated reproductive period. This strategy may have evolved, in part, to confer resilience to short-term environmental variability. We observed density-dependent effects on weaning mass, and maternal age (experience) was more important than oceanographic conditions or maternal mass in determining offspring weaning mass. Together these findings show that the mechanisms controlling reproductive output are conserved across terrestrial and marine systems and vary with population dynamics, an important consideration when assessing the effect of extrinsic changes, such as climate change, on a population.

Repeated stimulation of the HPA axis alters white blood cell count without increasing oxidative stress or inflammatory cytokines in fasting elephant seal pups.

The hypothalamic-pituitary-adrenal (HPA) axis controls the release of glucocorticoids, which regulate immune and inflammatory function by modulating cytokines, white blood cells and oxidative stress via glucocorticoid receptor (GR) signaling. Although the response to HPA activation is well characterized in many species, little is known about the impacts of HPA activation during extreme physiological conditions. Hence, we challenged 18 simultaneously fasting and developing elephant seal pups with daily intramuscular injections of adrenocorticotropin (ACTH), a GR antagonist (RU486), or a combination of the two (ACTH+RU486) for 4 days. We collected blood at baseline, 2 h and 4 days after the beginning of treatment. ACTH and ACTH+RU486 elevated serum aldosterone and cortisol at 2 h, with effects diminishing at 4 days. RU486 alone induced a compensatory increase in aldosterone, but not cortisol, at 4 days. ACTH decreased neutrophils at 2 h, while decreasing lymphocytes and increasing the neutrophil:lymphocyte ratio at 4 days. These effects were abolished by RU486. Despite alterations in white blood cells, there was no effect of ACTH or RU486 on transforming growth factor-ß or interleukin-6 levels; however, both cytokines decreased with the 4 day fasting progression. Similarly, ACTH did not impact protein oxidation, lipid peroxidation or antioxidant enzymes, but plasma isoprostanes and catalase activity decreased while glutathione peroxidase increased with fasting progression. These data demonstrate differential acute (2 h) and chronic (4 days) modulatory effects of HPA activation on white blood cells and that the chronic effect is mediated, at least in part, by GR. These results also underscore elephant seals' extraordinary resistance to oxidative stress derived from repeated HPA activation.

Oxylipin responses to fasting and insulin infusion in a large mammalian model of fasting-induced insulin resistance, the northern elephant seal.

The prolonged, postweaning fast of northern elephant seal (Mirounga angustirostris) pups is characterized by a reliance on lipid metabolism and reversible, fasting-induced insulin resistance, providing a unique model to examine the effects of insulin on lipid metabolism. We have previously shown that acute insulin infusion induced a shift in fatty acid metabolism dependent on fasting duration. This study complements the previous study by examining the effects of fasting duration and insulin infusion on circulating levels of oxylipins, bioactive metabolites derived from the oxygenation of polyunsaturated fatty acids. Northern elephant seal pups were studied at two postweaning periods (n = 5/period): early fasting (1-2 wk postweaning; 127 ± 1 kg) and late fasting (6-7 wk postweaning; 93 ± 4 kg). Different cohorts of pups were weighed, sedated, and infused with 65 mU/kg of insulin. Plasma was collected prior to infusion (T0) and at 10, 30, 60, and 120 min postinfusion. A profile of ∼80 oxylipins was analyzed by UPLC-ESI-MS/MS. Nine oxylipins changed between early and late fasting and eight were altered in response to insulin infusion. Fasting decreased prostaglandin F2α (PGF2α) and increased 14,15-dihydroxyicosatrienoic acid (14,15-DiHETrE), 20-hydroxyeicosatetraenoic acid (20-HETE), and 4-hydroxy-docosahexaenoic acid (4-HDoHE) (P < 0.03) in T0 samples, whereas insulin infusion resulted in an inverse change in area-under-the-curve (AUC) levels in these same metabolites (P < 0.05). In addition, 12-12-hydroperoxyeicosatetraenoic acid (HpETE) and 12-HETE decreased with fasting and insulin infusion, respectively (P < 0.04). The oxylipins altered during fasting and in response to insulin infusion may contribute to the manifestation of insulin resistance and participate in the metabolic regulation of associated cellular processes.

Elephant seal muscle cells adapt to sustained glucocorticoid exposure by shifting their metabolic phenotype.

Elephant seals experience natural periods of prolonged food deprivation while breeding, molting, and undergoing postnatal development. Prolonged food deprivation in elephant seals increases circulating glucocorticoids without inducing muscle atrophy, but the cellular mechanisms that allow elephant seals to cope with such conditions remain elusive. We generated a cellular model and conducted transcriptomic, metabolic, and morphological analyses to study how seal cells adapt to sustained glucocorticoid exposure. Seal muscle progenitor cells differentiate into contractile myotubes with a distinctive morphology, gene expression profile, and metabolic phenotype. Exposure to dexamethasone at three ascending concentrations for 48 h modulated the expression of six clusters of genes related to structural constituents of muscle and pathways associated with energy metabolism and cell survival. Knockdown of the glucocorticoid receptor (GR) and downstream expression analyses corroborated that GR mediates the observed effects. Dexamethasone also decreased cellular respiration, shifted the metabolic phenotype toward glycolysis, and induced mitochondrial fission and dissociation of mitochondria-endoplasmic reticulum (ER) interactions without decreasing cell viability. Knockdown of DNA damage-inducible transcript 4 (DDIT4), a GR target involved in the dissociation of mitochondria-ER membranes, recovered respiration and modulated antioxidant gene expression in myotubes treated with dexamethasone. These results show that adaptation to sustained glucocorticoid exposure in elephant seal myotubes involves a metabolic shift toward glycolysis, which is supported by alterations in mitochondrial morphology and a reduction in mitochondria-ER interactions, resulting in decreased respiration without compromising cell survival.

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.

Changes in serum adipokines during natural extended fasts in female northern elephant seals.

Adipose tissue is essential to endotherms for thermoregulation and energy storage as well as functioning as an endocrine organ. Adipose derived hormones, or adipokines, regulate metabolism, energy expenditure, reproduction, and immune function in model systems but are less well studied in wildlife. Female northern elephant seals (NES) achieve high adiposity during foraging and then undergo natural fasts up to five weeks long during haul-outs associated with reproduction and molting, resulting in large changes in adipose reserves. We measured circulating levels of four adipokines: leptin, resistin, adiponectin, and kisspeptin-54, in 196 serum samples from female NES at the beginning and end of their breeding and molting fasts. We examined the relationships between these adipokines and life-history stage, adiposity, mass, cortisol, and an immune cytokine involved in the innate immune response interleukin 6 (IL-6). All four adipokines varied with life-history stage. Leptin concentrations were highest at the beginning of the breeding haul-out. Resistin concentrations were higher throughout the breeding haul-out compared to the molt haul-out. Adiponectin concentrations were highest at the beginning of both haul-outs. Kisspeptin-54 concentrations were highest at the end of the breeding haul-out. Leptin, resistin, and adiponectin were associated with measures of body condition, either adiposity, mass, or both. Resistin, adiponectin, and kisspeptin-54 were associated with circulating cortisol concentrations. Resistin was strongly associated with circulating IL-6, a multifunctional cytokine. Adiponectin was associated with glucose concentrations, suggesting a potential role in tissue-specific insulin sensitivity during life-history stages categorized by high adiposity. Increased cortisol concentrations late in lactation were associated with increased kisspeptin-54, suggesting a link to ovulation initiation in NES. This study suggests dramatic changes in circulating adipokines with life-history and body condition that may exert important regulatory roles in NES. The positive relationship between adiponectin and adiposity as well as the lack of a relationship between leptin and kisspeptin-54 differed from model systems. These differences from biomedical model systems suggest the potential for modifications of expression and function of adipose-derived hormones in species that undergo natural changes in adiposity as part of their life-history.

Lightscapes of fear: How mesopredators balance starvation and predation in the open ocean.

Like landscapes of fear, animals are hypothesized to strategically use lightscapes based on intrinsic motivations. However, longitudinal evidence of state-dependent risk aversion has been difficult to obtain in wild animals. Using high-resolution biologgers, we continuously measured body condition, time partitioning, three-dimensional movement, and risk exposure of 71 elephant seals throughout their 7-month foraging migrations (N = 16,000 seal days). As body condition improved from 21 to 32% fat and daylength declined from 16 to 10 hours, seals rested progressively earlier with respect to sunrise, sacrificing valuable nocturnal foraging hours to rest in the safety of darkness. Seals in superior body condition prioritized safety over energy conservation by resting >100 meters deeper where it was 300× darker. Together, these results provide empirical evidence that marine mammals actively use the three-dimensional lightscape to optimize risk-reward trade-offs based on ecological and physiological factors.