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Daniel P. Costa

Publications and source records attributed to Daniel P. Costa.

15 recordsLinked to original sources

Cumulative effects of multiple stressors on marine mammals: Elephant seals as a model system

Noise exposure is a potential stressor for free-ranging marine mammals and is often studied in the absence of other environmental factors. Here, a multi-investigator, interdisciplinary effort was undertaken to examine the response of elephant seals to multiple stressors. An integrated physiological and ecological approach was taken, including immunology, stress physiology, toxicology, animal behavior, population biology, and life history theory, to examine the cumulative effects of exposure to multiple stressors in elephant seals. While we measured the response of individual animals, a population response can be predicted by incorporating these results into the long-term data on elephant seal demographics.

Book chapter

Foraging behavior and age affect maternal transfer of mercury to northern elephant seal pups

Deep ocean foraging northern elephant seals ( Mirounga angustirostris ) consume fish and squid in remote depths of the North Pacific Ocean. Contaminants bioaccumulated from prey are subsequently transferred by adult females to pups during gestation and lactation, linking pups to mercury contamination in mesopelagic food webs (200–1000 m depths). Maternal transfer of mercury to developing seal pups was related to maternal mercury contamination and was strongly correlated with maternal foraging behavior (biotelemetry and isotopes). Mercury concentrations in lanugo (hair grown in utero) were among the highest observed worldwide for young pinnipeds (geometric mean 23.01 μg/g dw, range 8.03–63.09 μg/g dw; n = 373); thus, some pups may be at an elevated risk of sub-lethal adverse health effects. Fetal mercury exposure was affected by maternal foraging geographic location and depth; mercury concentrations were highest in pups of the deepest diving, pelagic females. Moreover, pup lanugo mercury concentrations were strongly repeatable among successive pups of individual females, demonstrating relative consistency in pup mercury exposure based on maternal foraging strategies. Northern elephant seals are biosentinels of a remote deep-sea ecosystem. Our results suggest that mercury within North Pacific mesopelagic food webs may also pose an elevated risk to other mesopelagic-foraging predators and their offspring.

Scientific Reports

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.

Environmental Science & Technology

Mismatches in scale between highly mobile marine megafauna and marine protected areas

Marine protected areas (MPAs), particularly large MPAs, are increasing in number and size around the globe in part to facilitate the conservation of marine megafauna under the assumption that large-scale MPAs better align with vagile life histories; however, this alignment is not well established. Using a global tracking dataset from 36 species across five taxa, chosen to reflect the span of home range size in highly mobile marine megafauna, we show most MPAs are too small to encompass complete home ranges of most species. Based on size alone, 40% of existing MPAs could encompass the home ranges of the smallest ranged species, while only < 1% of existing MPAs could encompass those of the largest ranged species. Further, where home ranges and MPAs overlapped in real geographic space, MPAs encompassed < 5% of core areas used by all species. Despite most home ranges of mobile marine megafauna being much larger than existing MPAs, we demonstrate how benefits from MPAs are still likely to accrue by targeting seasonal aggregations and critical life history stages and through other management techniques.

Frontiers in Marine Science

Site fidelity as a maladaptive behavior in the Anthropocene

Site fidelity, or the behavior of returning to previously visited locations, has been observed across taxa and ecosystems. By developing familiarity with a particular location, site fidelity provides a range of benefits and is advantageous in stable or predictable environments. However, the Anthropocene is characterized by rates of environmental change that outpace the evolutionary history of extant taxa, which can result in site fidelity becoming maladaptive. Here we outline the theoretical underpinnings for maladaptive site fidelity and synthesize empirical research supporting its occurrence, and examine it in the context of a related concept, ecological traps, whereby organisms exhibit maladaptive behavior in habitat selection. We then discuss adaptive mechanisms that may enable species with site fidelity to continue to persist in the Anthropocene. With ongoing environmental change, researchers and practitioners should expect fidelity-induced ecological traps to become more common, and initiate projects to identify and understand their origins. Such knowledge will help conserve the widespread and ecologically important behavior of site fidelity.

Frontiers in Ecology and the Environment

Overhauling ocean spatial planning to improve marine megafauna conservation

Tracking data have led to evidence-based conservation of marine megafauna, but a disconnect remains between the many thousands of individual animals that have been tracked and the use of these data in conservation and management actions. Furthermore, the focus of most conservation efforts is within Exclusive Economic Zones despite the ability of these species to move thousands of kilometres across multiple national jurisdictions. To assist the goal of the United Nations General Assembly’s recent effort to negotiate a global treaty to conserve biodiversity on the high seas, we propose the development of a new frontier in dynamic marine spatial management. We argue that a global approach combining tracked movements of marine megafauna and human activities at-sea, and using existing and emerging technologies (e.g., through new tracking devices and big data approaches) can be applied to deliver near real-time diagnostics on existing risks and threats to mitigate global risks for marine megafauna. With technology developments over the next decade expected to catalyse the potential to survey marine animals and human activities in ever more detail and at global scales, the development of dynamic predictive tools based on near real-time tracking and environmental data will become crucial to address increasing risks. Such global tools for dynamic spatial and temporal management will, however, require extensive synoptic data updates and will be dependent on a shift to a culture of data sharing and open access. We propose a global mechanism to store and make such data available in near real-time, enabling a holistic view of space use by marine megafauna and humans that would significantly accelerate efforts to mitigate impacts and improve conservation and management of marine megafauna.

Frontiers in Marine Science

Energy-rich mesopelagic fishes revealed as a critical prey resource for a deep-diving predator using quantitative fatty acid signature analysis

Understanding the diet of deep-diving predators can provide essential insight to the trophic structure of the mesopelagic ecosystem. Comprehensive population-level diet estimates are exceptionally difficult to obtain for elusive marine predators due to the logistical challenges involved in observing their feeding behavior and collecting samples for traditional stomach content or fecal analyses. We used quantitative fatty acid signature analysis (QFASA) to estimate the diet composition of a wide-ranging mesopelagic predator, the northern elephant seal ( Mirounga angustirostris ), across five years. To implement QFASA, we first compiled a library of prey fatty acid (FA) profiles from the mesopelagic eastern North Pacific. Given the scarcity of a priori diet data for northern elephant seals, our prey library was necessarily large to encompass the range of potential prey in their foraging habitat. However, statistical constraints limit the number of prey species that can be included in the prey library to the number of dietary FAs in the analysis. Exceeding that limit could produce non-unique diet estimates (i.e., multiple diet estimates fit the data equally well). Consequently, we developed a novel ad-hoc method to identify which prey were unlikely to contribute to diet and could, therefore, be excluded from the final QFASA model. The model results suggest that seals predominantly consumed small mesopelagic fishes, including myctophids (lanternfishes) and bathylagids (deep sea smelts), while non-migrating mesopelagic squids comprised a third of their diet, substantially less than suggested by previous studies. Our results revealed that mesopelagic fishes, particularly energy-rich myctophids, were a critical prey resource, refuting the long-held view that elephant seals are squid specialists.

Frontiers in Marine Science

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

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 (Mirounga angustirostris) before and after lengthy at sea foraging trips (n = 89) or fasting periods on land (n = 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.

Proceedings of the Royal Society B

High-energy, high-fat lifestyle challenges an Arctic apex predator, the polar bear

Regional declines in polar bear ( Ursus maritimus ) populations have been attributed to changing sea ice conditions, but with limited information on the causative mechanisms. By simultaneously measuring field metabolic rates, daily activity patterns, body condition, and foraging success of polar bears moving on the spring sea ice, we found that high metabolic rates (1.6 times greater than previously assumed) coupled with low intake of fat-rich marine mammal prey resulted in an energy deficit for more than half of the bears examined. Activity and movement on the sea ice strongly influenced metabolic demands. Consequently, increases in mobility resulting from ongoing and forecasted declines in and fragmentation of sea ice are likely to increase energy demands and may be an important factor explaining observed declines in body condition and survival.

Science

Toward a national animal telemetry network for aquatic observations in the United States

Animal telemetry is the science of elucidating the movements and behavior of animals in relation to their environment or habitat. Here, we focus on telemetry of aquatic species (marine mammals, sharks, fish, sea birds and turtles) and so are concerned with animal movements and behavior as they move through and above the world&rsquo;s oceans, coastal rivers, estuaries and great lakes. Animal telemetry devices (&ldquo;tags&rdquo;) yield detailed data regarding animal responses to the coupled ocean&ndash;atmosphere and physical environment through which they are moving. Animal telemetry has matured and we describe a developing US Animal Telemetry Network (ATN) observing system that monitors aquatic life on a range of temporal and spatial scales that will yield both short- and long-term benefits, fill oceanographic observing and knowledge gaps and advance many of the U.S. National Ocean Policy Priority Objectives. ATN has the potential to create a huge impact for the ocean observing activities undertaken by the U.S. Integrated Ocean Observing System (IOOS) and become a model for establishing additional national-level telemetry networks worldwide.

Animal Biotelemetry

Mercury correlations among blood, muscle, and hair of northern elephant seals during the breeding and molting fasts

Mercury (Hg) biomonitoring and toxicological risk assessments for marine mammals commonly sample different tissues, making comparisons to toxicity benchmarks and among species and regions difficult. Few studies have examined how life history events, such as fasting, influence the relationship between total Hg (THg) concentrations in different tissues. We evaluated the relationships between THg concentrations in blood, muscle, and hair of female and male northern elephant seals ( Mirounga angustirostris ) at the start and end of the breeding and molting fasts. The relationships between tissues varied among tissue pairs and differed by sampling period and sex. Blood and muscle were generally related at all time periods; however, hair, an inert tissue, did not strongly represent the metabolically active tissues (blood and muscle) at all times of year. The strongest relationships between THg concentrations in hair and those in blood or muscle were observed during periods of active hair growth (end of the molting period) or during time periods when internal body conditions were similar to those when the hair was grown (end of the breeding fast). Our results indicate that THg concentrations in blood or muscle can be translated to the other tissue type using the equations we developed, but that THg concentrations in hair were generally a poor index of internal THg concentrations except during the end of fasting periods.

California

Effects of age, colony, and sex on mercury concentrations in California sea lions

We measured total mercury (THg) concentrations in California sea lions ( Zalophus californianus ) and examined how concentrations varied with age class, colony, and sex. Because Hg exposure is primarily via diet, we used nitrogen ( &delta; 15 N) and carbon ( &delta; 13 C) stable isotopes to determine if intraspecific differences in THg concentrations could be explained by feeding ecology. Blood and hair were collected from 21 adult females and 57 juveniles from three colonies in central and southern California (San Nicolas, San Miguel, and A&ntilde;o Nuevo Islands). Total Hg concentrations ranged from 0.01 to 0.31 &mu;g g &minus;1 wet weight (ww) in blood and 0.74 to 21.00 &mu;g g &minus;1 dry weight (dw) in hair. Adult females had greater mean THg concentrations than juveniles in blood (0.15 vs. 0.03 &mu;g &minus;1 ww) and hair (10.10 vs. 3.25 &mu;g &minus;1 dw). Age class differences in THg concentrations did not appear to be driven by trophic level or habitat type because there were no differences in &delta; 15 N or &delta; 13 C values between adults and juveniles. Total Hg concentrations in adult females were 54 % (blood) and 24 % (hair) greater in females from San Miguel than females from San Nicolas Island, which may have been because sea lions from the two islands foraged in different areas. For juveniles, we detected some differences in THg concentrations with colony and sex, although these were likely due to sampling effects and not ecological differences. Overall, THg concentrations in California sea lions were within the range documented for other marine mammals and were generally below toxicity benchmarks for fish-eating wildlife.

Archives of Environmental Contamination and Toxico

Evaluating hair as a predictor of blood mercury: the influence of ontogenetic phase and life history in pinnipeds

Mercury (Hg) biomonitoring of pinnipeds increasingly utilizes nonlethally collected tissues such as hair and blood. The relationship between total Hg concentrations ([THg]) in these tissues is not well understood for marine mammals, but it can be important for interpretation of tissue concentrations with respect to ecotoxicology and biomonitoring. We examined [THg] in blood and hair in multiple age classes of four pinniped species. For each species, we used paired blood and hair samples to quantify the ability of [THg] in hair to predict [THg] in blood at the time of sampling and examined the influence of varying ontogenetic phases and life history of the sampled animals. Overall, we found that the relationship between [THg] in hair and blood was affected by factors including age class, weaning status, growth, and the time difference between hair growth and sample collection. Hair [THg] was moderately to strongly predictive of current blood [THg] for adult female Steller sea lions (Eumetopias jubatus), adult female California sea lions (Zalophus californianus), and adult harbor seals (Phoca vitulina), whereas hair [THg] was poorly predictive or not predictive (different times of year) of blood [THg] for adult northern elephant seals (Mirounga angustirostris). Within species, except for very young pups, hair [THg] was a weaker predictor of blood [THg] for prereproductive animals than for adults likely due to growth, variability in foraging behavior, and transitions between ontogenetic phases. Our results indicate that the relationship between hair [THg] and blood [THg] in pinnipeds is variable and that ontogenetic phase and life history should be considered when interpreting [THg] in these tissues.

Archives of Environmental Contamination and Toxico

Marine foraging ecology influences mercury bioaccumulation in deep-diving northern elephant seals

Mercury contamination of oceans is prevalent worldwide and methylmercury concentrations in the mesopelagic zone (200&ndash;1000 m) are increasing more rapidly than in surface waters. Yet mercury bioaccumulation in mesopelagic predators has been understudied. Northern elephant seals (Mirounga angustirostris) biannually travel thousands of kilometres to forage within coastal and open-ocean regions of the northeast Pacific Ocean. We coupled satellite telemetry, diving behaviour and stable isotopes (carbon and nitrogen) from 77 adult females, and showed that variability among individuals in foraging location, diving depth and &delta; 13 C values were correlated with mercury concentrations in blood and muscle. We identified three clusters of foraging strategies, and these resulted in substantially different mercury concentrations: (i) deeper-diving and offshore-foraging seals had the greatest mercury concentrations, (ii) shallower-diving and offshore-foraging seals had intermediate levels, and (iii) coastal and more northerly foraging seals had the lowest mercury concentrations. Additionally, mercury concentrations were lower at the end of the seven-month-long foraging trip (n = 31) than after the two-month- long post-breeding trip (n = 46). Our results indicate that foraging behaviour influences mercury exposure and mesopelagic predators foraging in the northeast Pacific Ocean may be at high risk for mercury bioaccumulation.

California

Detection of sea otters in boat-based surveys of Prince William Sound, Alaska

Boat-based surveys have been commonly used to monitor sea otter populations, but there has been little quantitative work to evaluate detection biases that may affect these surveys. We used ground-based observers to investigate sea otter detection probabilities in a boat-based survey of Prince William Sound, Alaska. We estimated that 30% of the otters present on surveyed transects were not detected by boat crews. Approximately half (53%) of the undetected otters were missed because the otters left the transects, apparently in response to the approaching boat. Unbiased estimates of detection probabilities will be required for obtaining unbiased population estimates from boat-based surveys of sea otters. Therefore, boat-based surveys should include methods to estimate sea otter detection probabilities under the conditions specific to each survey. Unbiased estimation of detection probabilities with ground-based observers requires either that the ground crews detect all of the otters in observed subunits, or that there are no errors in determining which crews saw each detected otter. Ground-based observer methods may be appropriate in areas where nearly all of the sea otter habitat is potentially visible from ground-based vantage points.

Alaska