Publications by authors named "Daniel E Crocker"

118 Publications

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

Proc Biol Sci 2021 Oct 13;288(1960):20211258. Epub 2021 Oct 13.

Department of Ecology and Evolutionary Biology, University of California Santa Cruz, 130 McAllister Way, Santa Cruz, CA 95060, USA.

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 (). 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.
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http://dx.doi.org/10.1098/rspb.2021.1258DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8511744PMC
October 2021

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

J Exp Biol 2021 09 28;224(18). Epub 2021 Sep 28.

Department of Integrative Biology, University of California, Berkeley, CA 94720-3200, USA.

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-β 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.
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http://dx.doi.org/10.1242/jeb.243198DOI Listing
September 2021

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

Am J Physiol Regul Integr Comp Physiol 2021 10 4;321(4):R537-R546. Epub 2021 Aug 4.

Department of Molecular & Cell Biology, School of Natural Sciences, University of California, Merced, California.

The prolonged, postweaning fast of northern elephant seal () 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 ( = 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) ( < 0.03) in T0 samples, whereas insulin infusion resulted in an inverse change in area-under-the-curve (AUC) levels in these same metabolites ( < 0.05). In addition, 12-12-hydroperoxyeicosatetraenoic acid (HpETE) and 12-HETE decreased with fasting and insulin infusion, respectively ( < 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.
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http://dx.doi.org/10.1152/ajpregu.00016.2021DOI Listing
October 2021

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

Am J Physiol Regul Integr Comp Physiol 2021 09 14;321(3):R413-R428. Epub 2021 Jul 14.

Department of Integrative Biology, University of California, Berkeley, California.

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.
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http://dx.doi.org/10.1152/ajpregu.00052.2021DOI Listing
September 2021

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

Ecol Evol 2021 Jun 3;11(12):7579-7590. Epub 2021 May 3.

Department of Animal Behaviour Bielefeld University Bielefeld Germany.

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 () 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.
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http://dx.doi.org/10.1002/ece3.7590DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8216952PMC
June 2021

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

Gen Comp Endocrinol 2021 Jul 27;308:113760. Epub 2021 Mar 27.

Department of Biology, Sonoma State University, Rohnert Park, CA 94928, United States.

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.
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http://dx.doi.org/10.1016/j.ygcen.2021.113760DOI Listing
July 2021

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

Sci Adv 2021 Mar 17;7(12). Epub 2021 Mar 17.

Department of Ecology and Evolutionary Biology, University of California, Santa Cruz, Santa Cruz, CA, USA.

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 ( = 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.
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http://dx.doi.org/10.1126/sciadv.abd9818DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7968837PMC
March 2021

Exogenous GLP-1 stimulates TCA cycle and suppresses gluconeogenesis and ketogenesis in late-fasted northern elephant seals pups.

Am J Physiol Regul Integr Comp Physiol 2021 04 6;320(4):R393-R403. Epub 2021 Jan 6.

Department of Molecular & Cell Biology, School of Natural Sciences, University of California, Merced, California.

The postweaning fast of northern elephant seal pups is characterized by a lipid-dependent metabolism and associated with a decrease in plasma glucagon-like peptide-1 (GLP-1), insulin, and glucose and increased gluconeogenesis (GNG) and ketogenesis. We have also demonstrated that exogenous GLP-1 infusion increased plasma insulin despite simultaneous increases in cortisol and glucagon, which collectively present contradictory regulatory stimuli of GNG, ketogenesis, and glycolysis. To assess the effects of GLP-1 on metabolism using primary carbon metabolite profiles in late-fasted seal pups, we dose-dependently infused late-fasted seals with low (LDG; 10 pM/kg; = 3) or high (HDG; 100 pM/kg; = 4) GLP-1 immediately following a glucose bolus (0.5 g/kg), using glucose without GLP-1 as control ( = 5). Infusions were performed in similarly aged animals 6-8 wk into their postweaning fast. The plasma metabolome was measured from samples collected at five time points just prior to and during the infusions, and network maps constructed to robustly evaluate the effects of GLP-1 on primary carbon metabolism. HDG increased key tricarboxylic acid (TCA) cycle metabolites, and decreased phosphoenolpyruvate and acetoacetate ( < 0.05) suggesting that elevated levels of GLP-1 promote glycolysis and suppress GNG and ketogenesis, which collectively increase glucose clearance. These GLP-1-mediated effects on cellular metabolism help to explain why plasma GLP-1 concentrations decrease naturally in fasting pups as an evolved mechanism to help conserve glucose during the late-fasting period.
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http://dx.doi.org/10.1152/ajpregu.00211.2020DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8238143PMC
April 2021

Lipolysis and Leptin Production of Elephant Seal Blubber Using Precision-Cut Adipose Tissue Slices.

Front Physiol 2020 10;11:615784. Epub 2020 Dec 10.

Department of Biology, Sonoma State University, Rohnert Park, CA, United States.

Adipose tissue plays key roles in energy homeostasis. Understanding its metabolism and regulation is essential to predict the impact of environmental changes on wildlife health, especially in fasting-adapted species. However, experimental work in wild vertebrates can be challenging. We have developed a novel approach of precision-cut adipose tissue slices from northern elephant seal () as a complementary approach to whole animal models. Blubber biopsies were collected from 14 pups during early and late post-weaning fast (Año Nuevo, CA, United States), precision-cut into 1 mm thick slices and maintained in culture at 37°C for at least 63 h. The slices exhibited an efficient response to ß-adrenergic stimulation, even after 2 days of culture, revealing good tissue function. The response to lipolytic stimulus did not vary between regions of outer and inner blubber, but was higher at early than at late fast for inner blubber slices. At early fast, lipolysis significantly reduced leptin production. At this stage, inner blubber slices were also more efficient at producing leptin than outer blubber slices, especially in the non-lipolytic condition. This model will aid the study of adipose tissue metabolism and its response to environmental stressors in marine mammals.
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http://dx.doi.org/10.3389/fphys.2020.615784DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7758477PMC
December 2020

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

Oecologia 2021 Jan 19;195(1):25-35. Epub 2020 Dec 19.

Department of Animal Behaviour, Bielefeld University, Morgenbreede 45, 33615, Bielefeld, Germany.

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.
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http://dx.doi.org/10.1007/s00442-020-04815-5DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7882553PMC
January 2021

Similar foraging energetics of two sympatric albatrosses despite contrasting life histories and wind-mediated foraging strategies.

J Exp Biol 2020 12 2;223(Pt 23). Epub 2020 Dec 2.

Department of Biological Sciences, San Jose State University, One Washington Square, San Jose, CA 95192, USA.

Understanding the environmental and behavioral factors that influence how organisms maintain energy balance can inform us about their potential resiliency to rapid environmental changes. Flexibility in maintaining energy balance is particularly important to long-lived, central-place foraging seabirds that are constrained when locating food for offspring in a dynamic ocean environment. To understand the role of environmental interactions, behavioral flexibility and morphological constraints on energy balance, we used doubly labeled water to measure the at-sea daily energy expenditure (DEE) of two sympatrically breeding seabirds, Campbell () and grey-headed ( ) albatrosses. We found that species and sexes had similar foraging costs, but DEE varied between years for both species and sexes during early chick rearing in two consecutive seasons. For both species, greater DEE was positively associated with larger proportional mass gain, lower mean wind speeds during water take-offs, greater proportions of strong tailwinds (>12 m s), and younger chick age. Greater proportional mass gains were marginally more costly in male albatrosses that already have higher wing loading. DEE was higher during flights with a greater proportion of strong headwinds for grey-headed albatrosses only. Poleward winds are forecasted to intensify over the next century, which may increase DEE for grey-headed albatrosses that heavily use this region during early chick rearing. Female Campbell albatrosses may be negatively affected by forecasted slackening winds at lower latitudes due to an expected greater reliance on less energy efficient sit-and-wait foraging strategies. Behavioral plasticity associated with environmental variation may influence future population responses to climate change of both species.
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http://dx.doi.org/10.1242/jeb.228585DOI Listing
December 2020

Blood oxygen stores of olive ridley sea turtles, Lepidochelys olivacea are highly variable among individuals during arribada nesting.

J Comp Physiol B 2021 01 16;191(1):185-194. Epub 2020 Oct 16.

Biology Department, Sonoma State University, 1801 East Cotati Ave, Rohnert Park, CA, 94928, USA.

Sea turtles dive with a full lung of air and these O stores are supplemented by O stored in blood and muscle. Olive ridley sea turtles exhibit polymorphic nesting behavior, mass nesting behavior called arribada, where thousands of turtles will nest at once, and solitary nesting behavior. The potential physiological differences between the individuals using these strategies are not well understood. We measured blood volume and associated variables, including blood hemoglobin content and hematocrit, to estimate total blood O stores. There were no significant differences in mean values between nesting strategies, but arribada nesting individuals were more variable than those performing solitary nesting. Mass-specific plasma volume was relatively invariant among individuals but mass specific blood volume and blood oxygen stores varied widely, twofold and threefold, respectively. Blood O stores represented 32% of total body O stores. Under typical mean diving conditions of 26 °C and high levels of activity, blood stores confer ~ 14 min to aerobic dive times and are likely critical for the long duration, deep diving exhibited by the species. Individual differences in blood O stores strongly impact estimated aerobic dive limits and may constrain the ability of individuals to respond to changes on ocean climate.
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http://dx.doi.org/10.1007/s00360-020-01321-1DOI Listing
January 2021

Measurement of free glucocorticoids: quantifying corticosteroid binding capacity and its variation within and among mammal and bird species.

Conserv Physiol 2020 28;8(1):coaa057. Epub 2020 Jul 28.

Centre for the Neurobiology of Stress, Department of Biological Sciences, University of Toronto Scarborough, 1265 Military Trail, Toronto, ON M1C 1A4, Canada.

Plasma glucocorticoid (CORT) levels are one measure of stress in wildlife and give us insight into natural processes relevant to conservation issues. Many studies use total CORT concentrations to draw conclusions about animals' stress state and response to their environment. However, the blood of tetrapods contains corticosteroid-binding globulin (CBG), which strongly binds most circulating CORT. Only free CORT (CORT not bound by CBG) leaves the circulation and exerts biological effects on CORT-sensitive tissues. Measuring free CORT concentrations provides insight to an animal's stress response that cannot be revealed by simply measuring total CORT. To calculate free CORT concentrations in plasma or serum samples, one needs three measurements: the binding affinity of CBG for CORT (which varies by species), the total CORT concentration in the sample and the maximum corticosteroid binding capacity (MCBC) of CBG in the sample. Here, we detail the measurement of CBG binding capacity. We compare and contrast the three main methods to measure MCBC: charcoal, cell harvester and dialysis. Each is defined by the means by which free and bound CORT are separated. We weigh the relative merits and challenges of each. We conclude that sample volume, species and taxon binding specificity, and availability of equipment are the primary considerations in selecting the appropriate separation method. For most mammals, the charcoal method is recommended. For birds, the harvester method has critical advantages over the charcoal method. The dialysis method is widely regarded as the gold standard and has lower equipment costs but is more time-intensive and costly in terms of radioactive isotope needed and is less suited to processing large numbers of samples. The binding capacity of CBG varies tremendously within and among the bird and marine mammal species studied, and we discuss the implication of this variation for understanding the role of stress in wildlife.
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http://dx.doi.org/10.1093/conphys/coaa057DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7476546PMC
July 2020

A blubber gene expression index for evaluating stress in marine mammals.

Conserv Physiol 2020 28;8(1):coaa082. Epub 2020 Aug 28.

Department of Biological Sciences, University of the Pacific, Stockton, CA 95211, USA.

Evaluating the impacts of anthropogenic disturbance on free-ranging marine mammal populations, many of which are in decline, requires robust diagnostic markers of physiological stress and health. However, circulating levels of canonical 'stress hormones' such as glucocorticoids, which are commonly used to evaluate animal health, do not capture the complexity of species-specific responses and cannot be easily measured in large, fully aquatic marine mammals. Alternatively, expression of stress-responsive genes in hormone target tissues such as blubber, the specialized subcutaneous adipose tissue that can be manually or remotely sampled from many marine mammals, may be a more informative and sensitive indicator of recent (within 24 h) exposure to stressors. We previously identified genes that were upregulated in the inner blubber of juvenile northern elephant seals during experimental stimulation of the hypothalamic-pituitary-adrenal axis. In this study, we measured baseline expression levels of a subset of these genes in inner blubber of unmanipulated juvenile elephant seals of varying physiological states and correlated them with other stress markers (body condition index, corticosteroid and thyroid hormone levels). Expression of 10 genes, including those associated with lipid metabolism (, , ), redox homeostasis (), adipokine signaling (), lipid droplet formation (, ) and adipogenesis (, , ), was described by three principal components and was associated with cortisol and thyroid hormone levels. Significantly, baseline gene expression levels were predictive of circulating hormone levels, suggesting that these markers may be potential indicators of exposure to stressors in marine mammal species that are inaccessible for blood sampling. A similar approach may be used to identify species-specific stress markers in other tissues that can be sampled by remote biopsy dart from free-ranging marine mammals, such as outer blubber and skin.
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http://dx.doi.org/10.1093/conphys/coaa082DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7456562PMC
August 2020

Endocrine response to simulated U.S. Navy mid-frequency sonar exposures in the bottlenose dolphin (Tursiops truncatus).

J Acoust Soc Am 2020 03;147(3):1681

United States Navy Marine Mammal Program, San Diego, California 92152, USA.

Little information exists on endocrine responses to noise exposure in marine mammals. In the present study, cortisol, aldosterone, and epinephrine levels were measured in 30 bottlenose dolphins (Tursiops truncatus) before and after exposure to simulated U.S. Navy mid-frequency sonar signals (3250-3450 Hz). Control and exposure sessions, each consisting of ten trials, were performed sequentially with each dolphin. While swimming across the experimental enclosure during exposure trials, each dolphin received a single 1-s exposure with received sound pressure levels (SPLs, dB re 1 μPa) of 115, 130, 145, 160, 175, or 185 dB. Blood samples were collected through behaviorally conditioned, voluntary participation of the dolphins approximately one week prior to, immediately following, and approximately one week after exposure were analyzed for hormones via radioimmunoassay. Aldosterone was below detection limits in all samples. Neither cortisol nor epinephrine showed a consistent relationship with received SPL, even though dolphins abandoned trained behaviors after exposure to the highest SPLs and the severity of behavioral changes scaled with SPL. It remains unclear if dolphins interpret high-level anthropogenic sound as stressful, annoying, or threatening and whether behavioral responses to sound can be equated to a physiological (endocrine) response.
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http://dx.doi.org/10.1121/10.0000924DOI Listing
March 2020

Antioxidant response to cadmium exposure in primary skeletal muscle cells isolated from humans and elephant seals.

Comp Biochem Physiol C Toxicol Pharmacol 2020 Jan 22;227:108641. Epub 2019 Oct 22.

Centro de Investigaciones Biológicas del Noroeste (CIBNOR), S.C., Instituto Politécnico Nacional 195, Col. Playa Palo de Santa Rita Sur, La Paz, Baja California Sur C.P. 23096, Mexico. Electronic address:

Cadmium (Cd) occurs naturally; however, its concentration can increase with anthropogenic activities. Excess Cd increases reactive oxygen species (ROS) production and oxidative damage, which can lead to pathological conditions. Marine mammals accumulate Cd in the liver and the kidney; yet, there are no reports of Cd-associated tissue damage in whales, seals or dolphins. Response to Cd exposure (0-5.0 μM CdCl for 1-12 h) was analyzed and compared in primary skeletal muscle cells isolated from northern elephant seals (Mirounga angustirostris) and humans (Homo sapiens). Antioxidant enzyme activities (glutathione S-transferase, glutathione reductase, glutathione peroxidase), glutathione concentration, and protein carbonyl levels (an indicator of oxidative damage) were quantified. Glutathione levels were higher in northern elephant seal than in human cells. Protein carbonyl content in cells exposed to Cd was lower and had a smaller variability range in elephant seals than in humans. Generalized linear models (GLIM) identified Cd exposure and antioxidant defenses as significant contributors to protein carbonyl variability in human but not in elephant seal cells. These results suggest that the previously observed differences in circulating and tissue glutathione levels between marine and terrestrial mammals are maintained under cell culture conditions and that northern elephant seal and human muscle cells respond differently to Cd exposure. The results also suggest that the observed differences could potentially be associated with the protective mechanisms that allow northern elephant seals to tolerate extreme conditions that result in increased ROS generation (e.g. diving, sleep apnea, fasting) with no oxidative damage.
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http://dx.doi.org/10.1016/j.cbpc.2019.108641DOI Listing
January 2020

Expression of obesity-related adipokine genes during fasting in a naturally obese marine mammal.

Am J Physiol Regul Integr Comp Physiol 2019 10 7;317(4):R521-R529. Epub 2019 Aug 7.

Department of Ecology and Evolutionary Biology, University of California, Santa Cruz, California.

Northern elephant seals () are exceptional among fasting-adapted animals in coupling prolonged fasting with energetically costly activities, relying on oxidation of fat stores accrued during foraging to power metabolic demands of reproduction and molting. We hypothesized that high rates of energy expenditure, insulin resistance, and immune responses to colonial breeding in fasting seals are mediated by adipokines, or signaling molecules secreted by adipose tissue that are associated with obesity and inflammation in humans. We measured mRNA expression of 10 adipokine genes in blubber tissue of adult female elephant seals sampled early and late during their lactation and molting fasts and correlated gene expression with adiposity and circulating levels of corticosteroid and immune markers. Expression of adiponectin () and its receptor , leptin receptor (), resistin (), retinol binding protein 4 (), and visfatin/nicotinamide phosphoribosyltransferase () was increased, whereas that of fat mass and obesity-associated protein () was decreased in late-fasted compared with early-fasted groups. Abundance of adipokine transcripts that increased in late fasting was negatively associated with body mass and positively associated with cortisol, suggesting that they may mediate local metabolic effects of cortisol in blubber during fasting. Expression of several adipokines was correlated with the immune markers IL-6, haptoglobin, IgM, and IgE, suggesting a potential role in modulating immune responses to colonial breeding and molting. Since many of these adipokines have not been measured in other wild animals, this study provides preliminary insights into their local regulation in fat tissue and targeted assays for future studies.
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http://dx.doi.org/10.1152/ajpregu.00182.2019DOI Listing
October 2019

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

Conserv Physiol 2019 15;7(1):coz010. Epub 2019 May 15.

Department of Biology, Sonoma State University, Rohnert Park, CA, USA.

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,  29; male,  38) in central California and adult male CSL ( 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.
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http://dx.doi.org/10.1093/conphys/coz010DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6518924PMC
May 2019

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

Physiol Biochem Zool 2019 May/Jun;92(3):326-338

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.
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http://dx.doi.org/10.1086/702960DOI Listing
May 2019

Blubber transcriptome responses to repeated ACTH administration in a marine mammal.

Sci Rep 2019 02 25;9(1):2718. Epub 2019 Feb 25.

Department of Biological Sciences, University of the Pacific, Stockton, CA, 95211, USA.

Chronic physiological stress impacts animal fitness by catabolizing metabolic stores and suppressing reproduction. This can be especially deleterious for capital breeding carnivores such as marine mammals, with potential for ecosystem-wide effects. However, the impacts and indicators of chronic stress in animals are currently poorly understood. To identify downstream mediators of repeated stress responses in marine mammals, we administered adrenocorticotropic hormone (ACTH) once daily for four days to free-ranging juvenile northern elephant seals (Mirounga angustirostris) to stimulate endogenous corticosteroid release, and compared blubber tissue transcriptome responses to the first and fourth ACTH administrations. Gene expression profiles were distinct between blubber responses to single and repeated ACTH administration, despite similarities in circulating cortisol profiles. We identified 61 and 12 genes that were differentially expressed (DEGs) in response to the first ACTH and fourth administrations, respectively, 24 DEGs between the first and fourth pre-ACTH samples, and 12 DEGs between ACTH response samples from the first and fourth days. Annotated DEGs were associated with functions in redox and lipid homeostasis, suggesting potential negative impacts of repeated stress on capital breeding, diving mammals. DEGs identified in this study are potential markers of repeated stress in marine mammals, which may not be detectable by endocrine profiles alone.
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http://dx.doi.org/10.1038/s41598-019-39089-2DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6390094PMC
February 2019

Variation in Corticosterone Levels in Two Species of Breeding Albatrosses with Divergent Life Histories: Responses to Body Condition and Drivers of Foraging Behavior.

Physiol Biochem Zool 2019 Mar/Apr;92(2):223-238

Corticosterone (CORT) is a glucocorticoid hormone that maintains energy balance and can modulate foraging behaviors in seabirds. However, CORT responses are not always predictable under similar biophysical conditions and do not necessarily influence the same behaviors across breeding stages and species. To enhance our understanding of CORT's role as a proximate determinant of foraging behavior and energy maintenance, we examined the relationships between body condition, CORT, foraging behavior, and foraging success between two sympatric breeding albatross species with differing foraging strategies and life histories, the Campbell albatross (Thalassarache impavida) and the gray-headed albatross (Thalassarache chrysostoma), from Campbell Island, New Zealand. Pre- and postforaging CORT did not differ between species or stage, potentially as a result of behavioral plasticity or different functional roles of CORT across stages. Unexpectedly, body condition did not correlate with preforaging CORT during incubation, although a negative correlation was observed in Campbell albatrosses during the guard stage. Furthermore, CORT mediated foraging success in both species and stages, but CORT mediated foraging behavior only in incubation-stage Campbell albatrosses that had shorter foraging ranges with higher pretrip CORT. Additionally, CORT positively correlated with mass gain and the time elapsed since the last feeding event in guard-stage albatrosses. Our results highlight the complexity of CORT in mediating energy balance in free-ranging animals. Our results also support that if CORT is to be usefully interpreted, breeding stage must be considered because the physiological and behavioral functionality of CORT may differ across stages, with enhanced sensitivity to energy reserves during chick rearing.
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http://dx.doi.org/10.1086/702656DOI Listing
March 2019

A sample preparation workflow for adipose tissue shotgun proteomics and proteogenomics.

Biol Open 2018 Nov 19;7(11). Epub 2018 Nov 19.

Conservation and Biological Research Program, National Marine Mammal Foundation, San Diego, CA, USA.

Animals with large adipose stores, such as marine mammals, may provide insights into the evolution and function of this multifunctional tissue in health and disease. In the absence of sequenced genomes, molecular information can be rapidly obtained by proteomics and transcriptomics, but their application to adipose tissue is hindered by low nucleic acid and protein yields. We sequenced and compared proteomes isolated from the blubber of four elephant seals using phenol and guanidine thiocyanate (Qiazol) or detergent (sodium deoxycholate) buffer. Qiazol recovered more subcellular proteins such as metabolic enzymes, in addition to extracting RNA, facilitating proteogenomic analyses of small lipid-rich tissue biopsies. We also compared proteomics data analysis platforms and found that peptide sequencing improved protein identification sensitivity compared to database search alone. We report sample preparation and data analysis workflows for proteogenomics and a proteome of elephant seal blubber containing 2678 proteins, including many of interest for further functional studies.This article has an associated First Person interview with the first author of the paper.
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http://dx.doi.org/10.1242/bio.036731DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6262853PMC
November 2018

Lactation and resource limitation affect stress responses, thyroid hormones, immune function, and antioxidant capacity of sea otters ().

Ecol Evol 2018 Aug 25;8(16):8433-8447. Epub 2018 Jul 25.

Department of Biology Sonoma State University Rohnert Park California.

Lactation is the most energetically demanding stage of reproduction in female mammals. Increased energetic allocation toward current reproduction may result in fitness costs, although the mechanisms underlying these trade-offs are not well understood. Trade-offs during lactation may include reduced energetic allocation to cellular maintenance, immune response, and survival and may be influenced by resource limitation. As the smallest marine mammal, sea otters () have the highest mass-specific metabolic rate necessitating substantial energetic requirements for survival. To provide the increased energy needed for lactation, female sea otters significantly increase foraging effort, especially during late-lactation. Caloric insufficiency during lactation is reflected in the high numbers of maternal deaths due to End-Lactation Syndrome in the California subpopulation. We investigated the effects of lactation and resource limitation on maternal stress responses, metabolic regulation, immune function, and antioxidant capacity in two subspecies of wild sea otters (northern: and southern: ) within the California, Washington, and Alaska subpopulations. Lactation and resource limitation were associated with reduced glucocorticoid responses to acute capture stress. Corticosterone release was lower in lactating otters. Cortisol release was lower under resource limitation and suppression during lactation was only evident under resource limitation. Lactation and resource limitation were associated with alterations in thyroid hormones. Immune responses and total antioxidant capacity were not reduced by lactation or resource limitation. Southern sea otters exhibited higher concentrations of antioxidants, immunoglobulins, and thyroid hormones than northern sea otters. These data provide evidence for allocation trade-offs during reproduction and in response to nutrient limitation but suggest self-maintenance of immune function and antioxidant defenses despite energetic constraints. Income-breeding strategists may be especially vulnerable to the consequences of stress and modulation of thyroid function when food resources are insufficient to support successful reproduction and may come at a cost to survival, and thereby influence population trends.
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http://dx.doi.org/10.1002/ece3.4280DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6145021PMC
August 2018

Ancient convergent losses of yield potential risks for modern marine mammals.

Science 2018 08;361(6402):591-594

Department of Computational and Systems Biology, University of Pittsburgh, Pittsburgh, PA, USA.

Mammals diversified by colonizing drastically different environments, with each transition yielding numerous molecular changes, including losses of protein function. Though not initially deleterious, these losses could subsequently carry deleterious pleiotropic consequences. We have used phylogenetic methods to identify convergent functional losses across independent marine mammal lineages. In one extreme case, () accrued lesions in all marine lineages, while remaining intact in all terrestrial mammals. These lesions coincide with PON1 enzymatic activity loss in marine species' blood plasma. This convergent loss is likely explained by parallel shifts in marine ancestors' lipid metabolism and/or bloodstream oxidative environment affecting PON1's role in fatty acid oxidation. PON1 loss also eliminates marine mammals' main defense against neurotoxicity from specific man-made organophosphorus compounds, implying potential risks in modern environments.
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http://dx.doi.org/10.1126/science.aap7714DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6317340PMC
August 2018

Repeated adrenocorticotropic hormone administration alters adrenal and thyroid hormones in free-ranging elephant seals.

Conserv Physiol 2018 17;6(1):coy040. Epub 2018 Jul 17.

Department of Biological Sciences, University of the Pacific, Stockton, CA, USA.

Understanding the physiological response of marine mammals to anthropogenic stressors can inform marine ecosystem conservation strategies. Stress stimulates the activation of the hypothalamic-pituitary-adrenal (HPA) axis and synthesis of glucocorticoid (GC) hormones, which increase energy substrate availability while suppressing energy-intensive processes. Exposure to repeated stressors can potentially affect an animal's ability to respond to and recover from subsequent challenges. To mimic repeated activation of the HPA axis by environmental stressors (or challenges), we administered adrenocorticotropic hormone (ACTH) to free-ranging juvenile northern elephant seals (; = 7) once daily for 4 days. ACTH administration induced significant elevation in circulating cortisol and aldosterone levels. The cortisol responses did not vary in magnitude between the first ACTH administration on Day 1 and the last administration on Day 4. In contrast, aldosterone levels remained elevated above baseline for at least 24 h after each ACTH injection, and responses were greater on Day 4 than Day 1. Total triiodothyronine (tT3) levels were decreased on Day 4 relative to Day 1, while reverse triiodothyronine (rT3) concentrations increased relative to baseline on Days 1 and 4 in response to ACTH, indicating a suppression of thyroid hormone production. There was no effect of ACTH on the sex steroid dehydroepiandrosterone. These data suggest that elephant seals are able to mount adrenal responses to multiple ACTH administrations. However, repeated ACTH administration resulted in facilitation of aldosterone secretion and suppression of tT3, which may impact osmoregulation and metabolism, respectively. We propose that aldosterone and tT3 are informative additional indicators of repeated stress in marine mammals.
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http://dx.doi.org/10.1093/conphys/coy040DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6048993PMC
July 2018

Comprehensive endocrine response to acute stress in the bottlenose dolphin from serum, blubber, and feces.

Gen Comp Endocrinol 2018 09 29;266:178-193. Epub 2018 May 29.

National Marine Mammal Foundation, 2240 Shelter Island Dr Suite 200, San Diego, CA 92106, United States.

Several hormones are potential indicators of stress in free-ranging animals and provide information on animal health in managed-care settings. In response to stress, glucocorticoids (GC, e.g. cortisol) first appear in circulation but are later incorporated into other tissues (e.g. adipose) or excreted in feces or urine. These alternative matrices can be sampled remotely, or by less invasive means, than required for blood collection and are especially valuable in highly mobile species, like marine mammals. We characterized the timing and magnitude of several hormones in response to a stressor in bottlenose dolphins (Tursiops truncatus) and the subsequent incorporation of cortisol into blubber, and its metabolites excreted in feces. We evaluated the endocrine response to an acute stressor in bottlenose dolphins under managed care. We used a standardized stress protocol where dolphins voluntarily beached onto a padded platform and remained out of water for two hours; during the stress test blood samples were collected every 15 min and blubber biopsies were collected every hour (0, 60, and 120 min). Each subject was studied over five days: voluntary blood samples were collected on each of two days prior to the stress test; 1 and 2 h after the conclusion of the out-of-water stress test; and on the following two days after the stress test. Fecal samples were collected daily, each afternoon. The acute stressor resulted in increases in circulating ACTH, cortisol, and aldosterone during the stress test, and each returned to baseline levels within 2 h of the dolphin's return to water. Both cortisol and aldosterone concentrations were correlated with ACTH, suggesting both corticosteroids are at least partly regulated by ACTH. Thyroid hormone concentrations were generally unaffected by the acute stressor. Blubber cortisol increased during the stress test, and fecal GC excretion was elevated on the day of the stress test. We found that GCs in bottlenose dolphins can recover within hours of acute stress, and that cortisol release can be detected in alternate matrices within a few hours-within 2 h in blubber, and 3.5-5 h in fecal samples.
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http://dx.doi.org/10.1016/j.ygcen.2018.05.015DOI Listing
September 2018

Adipose transcriptome analysis provides novel insights into molecular regulation of prolonged fasting in northern elephant seal pups.

Physiol Genomics 2018 07 6;50(7):495-503. Epub 2018 Apr 6.

Department of Molecular & Cellular Biology, University of California, Merced, California.

The physiological and cellular adaptations to extreme fasting in northern elephant seals ( Mirounga angustirostris, NES) are remarkable and may help to elucidate endocrine mechanisms that regulate lipid metabolism and energy homeostasis in mammals. Recent studies have highlighted the importance of thyroid hormones in the maintenance of a lipid-based metabolism during prolonged fasting in weaned NES pups. To identify additional molecular regulators of fasting, we used a transcriptomics approach to examine changes in global gene expression profiles before and after 6-8 wk of fasting in weaned NES pups. We produced a de novo assembly and identified 98 unique protein-coding genes that were differentially expressed between early and late fasting. Most of the downregulated genes were associated with lipid, carbohydrate, and protein metabolism. A number of downregulated genes were also associated with maintenance of the extracellular matrix, consistent with tissue remodeling during weight loss and the multifunctional nature of blubber tissue, which plays both metabolic and structural roles in marine mammals. Using this data set, we predict potential mechanisms by which NES pups sustain metabolism and regulate adipose stores throughout the fast, and provide a valuable resource for additional studies of extreme metabolic adaptations in mammals.
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http://dx.doi.org/10.1152/physiolgenomics.00002.2018DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6087879PMC
July 2018

Foraging and fasting can influence contaminant concentrations in animals: an example with mercury contamination in a free-ranging marine mammal.

Proc Biol Sci 2018 02;285(1872)

Department of Ecology and Evolutionary Biology, University of California, Santa Cruz, Santa Cruz, CA, USA.

Large fluctuations in animal body mass in relation to life-history events can influence contaminant concentrations and toxicological risk. We quantified mercury concentrations in adult northern elephant seals () before and after lengthy at sea foraging trips ( = 89) or fasting periods on land ( = 27), and showed that mercury concentrations in blood and muscle changed in response to these events. The highest blood mercury concentrations were observed after the breeding fast, whereas the highest muscle mercury concentrations were observed when seals returned to land to moult. Mean female blood mercury concentrations decreased by 30% across each of the two annual foraging trips, demonstrating a foraging-associated dilution of mercury concentrations as seals gained mass. Blood mercury concentrations increased by 103% and 24% across the breeding and moulting fasts, respectively, demonstrating a fasting-associated concentration of mercury as seals lost mass. In contrast to blood, mercury concentrations in female's muscle increased by 19% during the post-breeding foraging trip and did not change during the post-moulting foraging trip. While fasting, female muscle mercury concentrations increased 26% during breeding, but decreased 14% during moulting. Consequently, regardless of exposure, an animal's contaminant concentration can be markedly influenced by their annual life-history events.
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http://dx.doi.org/10.1098/rspb.2017.2782DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5829211PMC
February 2018

Climate mediates the success of migration strategies in a marine predator.

Ecol Lett 2018 Jan 2;21(1):63-71. Epub 2017 Nov 2.

Department of Ecology and Evolutionary Biology, University of California Santa Cruz, 115 McAllister Way, Santa Cruz, CA, 95060, USA.

Individual behavioural specialisation has far-reaching effects on fitness and population persistence. Theory predicts that unconditional site fidelity, that is fidelity to a site independent of past outcome, provides a fitness advantage in unpredictable environments. However, the benefits of alternative site fidelity strategies driving intraspecific variation remain poorly understood and have not been evaluated in different environmental contexts. We show that contrary to expectation, strong and weak site fidelity strategies in migratory northern elephant seals performed similarly over 10 years, but the success of each strategy varied interannually and was strongly mediated by climate conditions. Strong fidelity facilitated stable energetic rewards and low risk, while weak fidelity facilitated high rewards and high risk. Weak fidelity outperformed strong fidelity in anomalous climate conditions, suggesting that the evolutionary benefits of site fidelity may be upended by increasing environmental variability. We highlight how individual behavioural specialisation may modulate the adaptive capacity of species to climate change.
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http://dx.doi.org/10.1111/ele.12871DOI Listing
January 2018

Characterization of seasonal reproductive and stress steroid hormones in wild Radiated Tortoises, Astrochelys radiata.

Gen Comp Endocrinol 2017 11 6;253:70-78. Epub 2017 Sep 6.

Department of Biology, Sonoma State University, Rohnert Park, CA, USA.

The critically endangered Radiated Tortoise (Astrochelys radiata) is endemic to the southern coastlines of Madagascar. Once common, wild populations of this tortoise have undergone dramatic declines in recent years. Although there have been studies documenting reproductive activities, reproductive physiological parameters are unknown yet may be crucial in the recovery of the species. Over four research seasons in remote field locations native to A. radiata, we surveyed for, radio-tracked, and sampled wild, free ranging tortoises. We sampled and measured stress and reproductive parameters (corticosterone [CORT], testosterone [T], estradiol-17β [E2], and progesterone [P]) in 311 plasma samples from 203 wild A. radiata, capturing their active period. Generally, hormone concentrations were associated with body condition, temperature, and humidity. There was wide variation in CORT that varied monthly and by group. Juvenile tortoises maintained more than twice the mean basal CORT concentrations than either adult sex, with the most dramatic distinctions in the middle of the wet season. For adult sex hormones, the last months of the dry season and into the wet season when ground humidities are low and just begin to rise prior to temperature declines, male T concentrations gradually increased to a peak before returning to near undetectable values into the dry season. We had limited data for T concentrations in females, but found average T concentrations were much lower than in males and positively correlated with larger female home range sizes. For female hormone cycles, E2 also peaked in the early 1/3 of the wet season along with male T, and was followed by an uptick in P which correlates to the putative ovulatory cycle. Females tracked over four years showed variation in patterns of P, indicating that number and frequency of clutches vary. Our results suggest that 1) there is high species plasticity in response to stress; 2) A. radiata reproductive cycling is somewhat dissociated with courtship timing and is instead triggered by environmental cues; and 3) individual female reproductive output is irregular. This study is oone of the first to document and describe multi-year seasonal stress and reproductive hormones in a free-ranging Malagasy chelonian. These data may be used to identify key high-production habitats for conservation, and aide in captive management and reproduction in assurance colonies for species health and survival.
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http://dx.doi.org/10.1016/j.ygcen.2017.09.001DOI Listing
November 2017
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