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.

Growth in marine mammals: a review of growth patterns, composition and energy investment.

Growth of structural mass and energy reserves influences individual survival, reproductive success, population and species life history. Metrics of structural growth and energy storage of individuals are often used to assess population health and reproductive potential, which can inform conservation. However, the energetic costs of tissue deposition for structural growth and energy stores and their prioritization within bioenergetic budgets are poorly documented. This is particularly true across marine mammal species as resources are accumulated at sea, limiting the ability to measure energy allocation and prioritization. We reviewed the literature on marine mammal growth to summarize growth patterns, explore their tissue compositions, assess the energetic costs of depositing these tissues and explore the tradeoffs associated with growth. Generally, marine mammals exhibit logarithmic growth. This means that the energetic costs related to growth and tissue deposition are high for early postnatal animals, but small compared to the total energy budget as animals get older. Growth patterns can also change in response to resource availability, habitat and other energy demands, such that they can serve as an indicator of individual and population health. Composition of tissues remained consistent with respect to protein and water content across species; however, there was a high degree of variability in the lipid content of both muscle (0.1-74.3%) and blubber (0.4-97.9%) due to the use of lipids as energy storage. We found that relatively few well-studied species dominate the literature, leaving data gaps for entire taxa, such as beaked whales. The purpose of this review was to identify such gaps, to inform future research priorities and to improve our understanding of how marine mammals grow and the associated energetic costs.

Deep dives and high tissue density increase mean dive costs in California sea lions (Zalophus californianus).

Diving is central to the foraging strategies of many marine mammals and seabirds. Still, the effect of dive depth on foraging cost remains elusive because energy expenditure is difficult to measure at fine temporal scales in wild animals. We used depth and acceleration data from eight lactating California sea lions (Zalophus californianus) to model body density and investigate the effect of dive depth and tissue density on rates of energy expenditure. We calculated body density in 5 s intervals from the rate of gliding descent. We modeled body density across depth in each dive, revealing high tissue densities and diving lung volumes (DLVs). DLV increased with dive depth in four individuals. We used the buoyancy calculated from dive-specific body-density models and drag calculated from swim speed to estimate metabolic power and cost of transport in 5 s intervals during descents and ascents. Deeper dives required greater mean power for round-trip vertical transit, especially in individuals with higher tissue density. These trends likely follow from increased mean swim speed and buoyant hinderance that increasingly outweighs buoyant aid in deeper dives. This suggests that deep diving is either a 'high-cost, high-reward' strategy or an energetically expensive option to access prey when prey in shallow waters are limited, and that poor body condition may increase the energetic costs of deep diving. These results add to our mechanistic understanding of how foraging strategy and body condition affect energy expenditure in wild breath-hold divers.

Estimating energetic intake for marine mammal bioenergetic models.

Bioenergetics is the study of how animals achieve energetic balance. Energetic balance results from the energetic expenditure of an individual and the energy they extract from their environment. Ingested energy depends on several extrinsic (e.g prey species, nutritional value and composition, prey density and availability) and intrinsic factors (e.g. foraging effort, success at catching prey, digestive processes and associated energy losses, and digestive capacity). While the focus in bioenergetic modelling is often on the energetic costs an animal incurs, the robust estimation of an individual's energy intake is equally critical for producing meaningful predictions. Here, we review the components and processes that affect energy intake from ingested gross energy to biologically useful net energy (NE). The current state of knowledge of each parameter is reviewed, shedding light on research gaps to advance this field. The review highlighted that the foraging behaviour of many marine mammals is relatively well studied via biologging tags, with estimates of success rate typically assumed for most species. However, actual prey capture success rates are often only assumed, although we note studies that provide approaches for its estimation using current techniques. A comprehensive collation of the nutritional content of marine mammal prey species revealed a robust foundation from which prey quality (comprising prey species, size and energy density) can be assessed, though data remain unavailable for many prey species. Empirical information on various energy losses following ingestion of prey was unbalanced among marine mammal species, with considerably more literature available for pinnipeds. An increased understanding and accurate estimate of each of the components that comprise a species NE intake are an integral part of bioenergetics. Such models provide a key tool to investigate the effects of disturbance on marine mammals at an individual and population level and to support effective conservation and management.

An anchovy ecosystem indicator of marine predator foraging and reproduction.

Forage fishes are key energy conduits that transfer primary and secondary productivity to higher trophic levels. As novel environmental conditions caused by climate change alter ecosystems and predator-prey dynamics, there is a critical need to understand how forage fish control bottom-up forcing of food web dynamics. In the northeast Pacific, northern anchovy (Engraulis mordax) is an important forage species with high interannual variability in population size that subsequently impacts the foraging and reproductive ecology of marine predators. Anchovy habitat suitability from a species distribution model (SDM) was assessed as an indicator of the diet, distribution and reproduction of four predator species. Across 22 years (1998-2019), this anchovy ecosystem indicator (AEI) was significantly positively correlated with diet composition of all species and the distribution of common murres (Uria aalge), Brandt's cormorants (Phalacrocorax penicillatus) and California sea lions (Zalophus californianus), but not rhinoceros auklets (Cerorhinca monocerata). The capacity for the AEI to explain variability in predator reproduction varied by species but was strongest with cormorants and sea lions. The AEI demonstrates the utility of forage SDMs in creating ecosystem indicators to guide ecosystem-based management.

Estimating reproductive costs in marine mammal bioenergetic models: a review of current knowledge and data availability.

Reproductive costs represent a significant proportion of a mammalian female's energy budget. Estimates of reproductive costs are needed for understanding how alterations to energy budgets, such as those from environmental variation or human activities, impact maternal body condition, vital rates and population dynamics. Such questions are increasingly important for marine mammals, as many populations are faced with rapidly changing and increasingly disturbed environments. Here we review the different energetic costs that marine mammals incur during gestation and lactation and how those costs are typically estimated in bioenergetic models. We compiled data availability on key model parameters for each species across all six marine mammal taxonomic groups (mysticetes, odontocetes, pinnipeds, sirenians, mustelids and ursids). Pinnipeds were the best-represented group regarding data availability, including estimates of milk intake, milk composition, lactation duration, birth mass, body composition at birth and growth. There were still considerable data gaps, particularly for polar species, and good data were only available across all parameters in 45% of pinniped species. Cetaceans and sirenians were comparatively data-poor, with some species having little or no data for any parameters, particularly beaked whales. Even for species with moderate data coverage, many parameter estimates were tentative or based on indirect approaches, necessitating reevaluation of these estimates. We discuss mechanisms and factors that affect maternal energy investment or prey requirements during reproduction, such as prey supplementation by offspring, metabolic compensation, environmental conditions and maternal characteristics. Filling the existing data gaps highlighted in this review, particularly for parameters that are influential on bioenergetic model outputs, will help refine reproductive costs estimated from bioenergetic models and better address how and when energy imbalances are likely to affect marine mammal populations.

The influence of prey availability on behavioral decisions and reproductive success of a central-place forager during lactation.

Marine central-place foragers are increasingly faced with altered prey landscapes, necessitating predictions of the impact of such changes on behavior, reproductive success, and population dynamics. We used state-dependent behavioral life history theory implemented via Stochastic Dynamic Programming (SDP) to explore the influence of changes in prey distribution and energy gain from foraging on the behavior and reproductive success of a central place forager during lactation. Our work is motivated by northern fur seals (Callorhinus ursinus) because of the ongoing population decline of the Eastern Pacific stock and projected declines in biomass of walleye pollock (Gadus chalcogrammus), a key fur seal prey species in the eastern Bering Sea. We also explored how changes in female and pup metabolic rates, body size, and lactation duration affected model output to provide insight into traits that might experience selective pressure in response to reductions in prey availability. Simulated females adopted a central-place foraging strategy after an initial extended period spent on land (4.7-8.3 days). Trip durations increased as the high energy prey patch moved farther from land or when the energy gain from foraging decreased. Increases in trip duration adversely affected pup growth rates and wean mass despite attempts to compensate by increasing land durations. Metabolic rate changes had the largest impacts on pup wean mass, with reductions in a pup's metabolic rate allowing females to successfully forage at distances of 600+ km from land for up to 15+ days. Our results indicate that without physiological adaptations, a rookery is unlikely to be viable if the primary foraging grounds are 400 km or farther from the rookery. To achieve pup growth rates characteristic of a population experiencing rapid growth, model results indicate the primary foraging grounds need to be <150 km from the rookery.

Key questions in marine mammal bioenergetics.

Bioenergetic approaches are increasingly used to understand how marine mammal populations could be affected by a changing and disturbed aquatic environment. There remain considerable gaps in our knowledge of marine mammal bioenergetics, which hinder the application of bioenergetic studies to inform policy decisions. We conducted a priority-setting exercise to identify high-priority unanswered questions in marine mammal bioenergetics, with an emphasis on questions relevant to conservation and management. Electronic communication and a virtual workshop were used to solicit and collate potential research questions from the marine mammal bioenergetic community. From a final list of 39 questions, 11 were identified as 'key' questions because they received votes from at least 50% of survey participants. Key questions included those related to energy intake (prey landscapes, exposure to human activities) and expenditure (field metabolic rate, exposure to human activities, lactation, time-activity budgets), energy allocation priorities, metrics of body condition and relationships with survival and reproductive success and extrapolation of data from one species to another. Existing tools to address key questions include labelled water, animal-borne sensors, mark-resight data from long-term research programs, environmental DNA and unmanned vehicles. Further validation of existing approaches and development of new methodologies are needed to comprehensively address some key questions, particularly for cetaceans. The identification of these key questions can provide a guiding framework to set research priorities, which ultimately may yield more accurate information to inform policies and better conserve marine mammal populations.

Fetal mercury concentrations in central California Pacific harbor seals: Associated drivers and outcomes.

Mercury (Hg) is a well-known toxicant in wildlife and humans. High total Hg concentrations ([THg]) have been reported in central California harbor seals Phoca vitulina richardii. We evaluated the effects of presence/absence of early natal coat (lanugo), year (2012 to 2017), sex, stranding location, and trophic ecology (ẟ13C and ẟ15N values) on hair [THg] along coastal central California. Also examined were [THg] effects on growth rates of pups in rehabilitation and probability of release (e.g., successful rehabilitation). The [THg] ranged from 0.46-81.98 mg kg-1 dw, and ẟ15N and ẟ13C ranged from 13.6-21.5‰, and -17.2 to -13.0‰, respectively. Stranding location, year, and presence of lanugo coat were important factors explaining variation in [THg]. Seals from Sonoma and San Mateo County had higher [THg] than other locations. Seals with full or partial lanugo coat had lower [THg]. Seals from 2016 and 2017 had higher [THg] than those from 2015. Hair [THg] exceeded lower and upper toxicological thresholds (>20 mg kg-1 by year (5.88% to 23.53%); >30 mg kg-1 (0% to 12.31%)) with a pronounced increase from 2015 to 2016. Pups in 2017 had significantly higher odds ratio of [THg] above 20 mg kg-1 than pups of 2015, and pups in 2016 had significantly higher odds ratio than those from 2013 and 2015 (similar when using 30 mg kg-1). Pups in Sonoma County had the highest odds ratio for [THg] in lanugo above 20 mg kg-1. ẟ15N values were higher in 2015-2017, particularly relative to 2014, probably associated with the El Niño event. The [THg] was not a good predictor for probability of release and mass-specific growth rates in captivity. Further investigation of temporal trends of [THg] in harbor seals is warranted given the relatively high percentage of samples exceeding threshold values, particularly in the most recent sampling years.

Predicting the population consequences of acoustic disturbance, with application to an endangered gray whale population.

Acoustic disturbance is a growing conservation concern for wildlife populations because it can elicit physiological and behavioral responses that can have cascading impacts on population dynamics. State-dependent behavioral and life history models implemented via Stochastic Dynamic Programming (SDP) provide a natural framework for quantifying biologically meaningful population changes resulting from disturbance by linking environment, physiology, and metrics of fitness. We developed an SDP model using the endangered western gray whale (Eschrichtius robustus) as a case study because they experience acoustic disturbance on their summer foraging grounds. We modeled the behavior and physiological dynamics of pregnant females as they arrived on the feeding grounds and predicted the probability of female and offspring survival, with and without acoustic disturbance and in the presence/absence of high prey availability. Upon arrival in mid-May, pregnant females initially exhibited relatively random behavior before they transitioned to intensive feeding that resulted in continual fat mass gain until departure. This shift in behavior co-occurred with a change in spatial distribution; early in the season, whales were more equally distributed among foraging areas with moderate to high energy availability, whereas by mid-July whales transitioned to predominate use of the location that had the highest energy availability. Exclusion from energy-rich offshore areas led to reproductive failure and in extreme cases, mortality of adult females that had lasting impacts on population dynamics. Simulated disturbances in nearshore foraging areas had little to no impact on female survival or reproductive success at the population level. At the individual level, the impact of disturbance was unequally distributed across females of different lengths, both with respect to the number of times an individual was disturbed and the impact of disturbance on vital rates. Our results highlight the susceptibility of large capital breeders to reductions in prey availability, and indicate that who, where, and when individuals are disturbed are likely to be important considerations when assessing the impacts of acoustic activities. This model provides a framework to inform planned acoustic disturbances and assess the effectiveness of mitigation strategies for large capital breeders.

HAIR, WHOLE BLOOD, AND BLOOD-SOAKED CELLULOSE PAPER-BASED RISK ASSESSMENT OF MERCURY CONCENTRATIONS IN STRANDED CALIFORNIA PINNIPEDS.

Mercury (Hg) poses a health risk to wildlife populations and has been documented at relatively high concentrations in many marine mammals, including wild-caught pinnipeds along the central California, US coast. We measured total Hg concentrations ([THg]) in hair and blood of live-stranded harbor seals (HS; Phoca vitulina), California sea lions (CSL; Zalophus californianus), and northern elephant seals (NES; Mirounga angustirostris) in California to quantify species, temporal, and spatial variability in [THg] and assess the relationships between [THg] measured by different methods (blood vs. filter paper) and in different matrices (blood vs. hair). We compared [THg] with toxicologic thresholds of concern to aid in identification of at-risk individuals or groups and better understand how the use of different methods and matrices affects assumed toxicologic risk. There was a wide range of [THg] in blood (<0.01-1.13 µg/g) and hair (0.45-81.98 µg/g), and NES had higher [THg] compared with HS and CSL. All three species had individuals with [THg] that exceeded the lower threshold for one or both matrices, but only HS pups had [THg] exceeding upper thresholds. Spatial differences in [THg] were detected, with higher concentrations in HS pups from areas surrounding San Francisco Bay, but differences were dependent on sampling year and matrix. The relationship between [THg] in blood and filter paper (r2=0.98) was strong, and differences had little influence on comparisons with toxicologic thresholds. Blood and hair [THg] were generally in agreement (r2=0.72), but large mismatches for a few seals underscore the importance of combined sampling in adverse effects studies where accurate assessment of Hg exposure is crucial. The wide range of [THg] in stranded HS pups that exceeded published thresholds of concern makes them a promising candidate for adverse effects studies, particularly because different matrices represent Hg exposure across key developmental stages.

What's in a whisker? Disentangling ecological and physiological isotopic signals.

RATIONALE: Stable isotope analysis of keratinized tissues is an informative tool for quantifying foraging ecology that can address questions related to niche specialization and temporal variation in behavior. Application of this approach relies on an understanding of tissue growth and how isotope ratios relate to physiological and ecological processes, data that are lacking for many species. METHODS: We collected paired whisker length measurements from northern elephant seals to estimate growth and shedding patterns (n = 16). A subset of seals (n = 5) carried a satellite tag and time-depth recorder across the 7+ month foraging trip following the annual pelage molt. Stable isotopes of carbon and nitrogen were measured in whisker segments grown across the 6+ week fasting on land and the subsequent foraging trip; profiles were combined with growth parameters to timestamp each segment and investigate relationships with foraging behavior. RESULTS: Whisker loss and initial regrowth primarily occurred during the annual pelage molt, but newly grown whiskers exhibited active, nonlinear growth across the foraging trip. The δ13 C and δ15 N values were higher in segments grown on land than at sea and exhibited a characteristic decline upon departure from the rookery. There was a relationship between latitude and longitude and δ15 N values, and individual whisker segments grown at sea could be classified to the correct ecoregion with 81% accuracy. CONCLUSIONS: Fasting affected both δ13 C and δ15 N values and the ability to exclude these values from ecological investigations is crucial given the temporal overlap with tissue growth. The rapid decline in isotope ratios upon departure can be used to isolate portions of the whisker with a strong physiological signal, even for whiskers with unknown growth histories. The active growth across the foraging trip combined with the ability to identify differences in foraging behavior validates the utility of this approach for addressing ecological questions.

Factors affecting energy expenditure in a declining fur seal population.

Quantifying metabolic rates and the factors that influence them is key to wildlife conservation efforts because anthropogenic activities and habitat alteration can disrupt energy balance, which is critical for reproduction and survival. We investigated the effect of diving behaviour, diet and season on field metabolic rates (FMR) and foraging success of lactating northern fur seals (Callorhinus ursinus) from the Pribilof Islands during a period of population decline. Variation in at-sea FMR was in part explained by season and trip duration, with values that ranged from 5.18 to 9.68 W kg-1 (n = 48). Fur seals experienced a 7.2% increase in at-sea FMR from summer to fall and a 1.9% decrease in at-sea FMR for each additional day spent at sea. There was no effect of foraging effort, dive depth or diet on at-sea FMR. Mass gains increased with trip duration and were greater in the fall compared with summer, but were unrelated to at-sea FMR, diving behaviour and diet. Seasonal increases in at-sea FMR may have been due to costs associated with the annual molt but did not appear to adversely impact the ability of females to gain mass on foraging trips. The overall high metabolic rates in conjunction with the lack of any diet-related effects on at-sea FMR suggests that northern fur seals may have reached a metabolic ceiling early in the population decline. This provides indirect evidence that food limitation may be contributing to the low pup growth rates observed in the Pribilof Islands, as a high metabolic overhead likely results in less available energy for lactation. The limited ability of female fur seals to cope with changes in prey availability through physiological mechanisms is particularly concerning given the recent and unprecedented environmental changes in the Bering Sea that are predicted to have ecosystem-level impacts.

The energetic consequences of behavioral variation in a marine carnivore.

Intraspecific variability in foraging behavior has been documented across a range of taxonomic groups, yet the energetic consequences of this variation are not well understood for many species. Understanding the effect of behavioral variation on energy expenditure and acquisition is particularly crucial for mammalian carnivores because they have high energy requirements that place considerable pressure on prey populations. To determine the influence of behavior on energy expenditure and balance, we combined simultaneous measurements of at-sea field metabolic rate (FMR) and foraging behavior in a marine carnivore that exhibits intraspecific behavioral variation, the California sea lion (Zalophus californianus). Sea lions exhibited variability in at-sea FMR, with some individuals expending energy at a maximum of twice the rate of others. This variation was in part attributable to differences in diving behavior that may have been reflective of diet; however, this was only true for sea lions using a foraging strategy consisting of epipelagic (<200 m within the water column) and benthic dives. In contrast, sea lions that used a deep-diving foraging strategy all had similar values of at-sea FMR that were unrelated to diving behavior. Energy intake did not differ between foraging strategies and was unrelated to energy expenditure. Our findings suggest that energy expenditure in California sea lions may be influenced by interactions between diet and oxygen conservation strategies. There were no apparent energetic trade-offs between foraging strategies, although there was preliminary evidence that foraging strategies may differ in their variability in energy balance. The energetic consequences of behavioral variation may influence the reproductive success of female sea lions and result in differential impacts of individuals on prey populations. These findings highlight the importance of quantifying the relationships between energy expenditure and foraging behavior in other carnivores for studies addressing fundamental and applied physiological and ecological questions.

Characterizing habitat suitability for a central-place forager in a dynamic marine environment.

Characterizing habitat suitability for a marine predator requires an understanding of the environmental heterogeneity and variability over the range in which a population moves during a particular life cycle. Female California sea lions (Zalophus californianus) are central-place foragers and are particularly constrained while provisioning their young. During this time, habitat selection is a function of prey availability and proximity to the rookery, which has important implications for reproductive and population success. We explore how lactating females may select habitat and respond to environmental variability over broad spatial and temporal scales within the California Current System. We combine near-real-time remotely sensed satellite oceanography, animal tracking data (n = 72) from November to February over multiple years (2003-2009) and Generalized Additive Mixed Models (GAMMs) to determine the probability of sea lion occurrence based on environmental covariates. Results indicate that sea lion presence is associated with cool (<14°C), productive waters, shallow depths, increased eddy activity, and positive sea-level anomalies. Predictive habitat maps generated from these biophysical associations suggest winter foraging areas are spatially consistent in the nearshore and offshore environments, except during the 2004-2005 winter, which coincided with an El Niño event. Here, we show how a species distribution model can provide broadscale information on the distribution of female California sea lions during an important life history stage and its implications for population dynamics and spatial management.

A Dynamic State Model of Migratory Behavior and Physiology to Assess the Consequences of Environmental Variation and Anthropogenic Disturbance on Marine Vertebrates.

Integrating behavior and physiology is critical to formulating new hypotheses on the evolution of animal life-history strategies. Migratory capital breeders acquire most of the energy they need to sustain migration, gestation, and lactation before parturition. Therefore, when predicting the impact of environmental variation on such species, a mechanistic understanding of the physiology of their migratory behavior is required. Using baleen whales as a model system, we developed a dynamic state variable model that captures the interplay among behavioral decisions, energy, reproductive needs, and the environment. We applied the framework to blue whales (Balaenoptera musculus) in the eastern North Pacific Ocean and explored the effects of environmental and anthropogenic perturbations on female reproductive success. We demonstrate the emergence of migration to track prey resources, enabling us to quantify the trade-offs among capital breeding, body condition, and metabolic expenses. We predict that periodic climatic oscillations affect reproductive success less than unprecedented environmental changes do. The effect of localized, acute anthropogenic impacts depended on whales' behavioral response to the disturbance; chronic, but weaker, disturbances had little effect on reproductive success. Because we link behavior and vital rates by modeling individuals' energetic budgets, we provide a general framework to investigate the ecology of migration and assess the population consequences of disturbance, while identifying critical knowledge gaps.

Seals and sea lions are what they eat, plus what? Determination of trophic discrimination factors for seven pinniped species.

RATIONALE: Mixing models are a common method for quantifying the contribution of prey sources to the diet of an individual using stable isotope analysis; however, these models rely upon a known trophic discrimination factor (hereafter, TDF) that results from fractionation between prey and animal tissues. Quantifying TDFs in captive animals is ideal, because diet is controlled and the proportional contributions and isotopic values of all prey items are known. METHODS: To calculate TDFs for the Hawaiian monk seal, northern elephant seal, bearded seal, ringed seal, spotted seal, harbor seal, and California sea lion, we obtained whiskers, serum, plasma, red blood cells, and prey items from nine captive individuals. We obtained δ(13) C and δ(15) N values using continuous-flow isotope-ratio mass spectrometry. The average δ(13) C and δ(15) N values from bulk and lipid-corrected prey from the diet were subtracted from the δ(13) C and δ(15) N values of each blood and whisker sample to calculate tissue-specific TDFs for each individual (∆(13) C or ∆(15) N). RESULTS: The ∆(13) C values ranged from +1.7 to +3.2‰ (bulk prey) and from +0.8 to +1.9‰ (lipid-corrected prey) for the various blood components, and from +3.9 to +4.6‰ (bulk prey) or +2.6 to +3.9‰ (lipid-corrected prey) for whiskers. The ∆(15) N values ranged from +2.2 to +4.3‰ for blood components and from +2.6 to +4.0‰ for whiskers. The TDFs tended to group by tissue, with whiskers having greater ∆(13) C values than blood components. In contrast, the ∆(15) N values were greater in serum and plasma than in red blood cells and whiskers. CONCLUSIONS: By providing the first TDF values for five seal species (family Phocidae) and one otariid species (family Otariidae), our study facilitates more accurate mixing models for these species. These values are particularly important for critically endangered Hawaiian monk seals and the three Arctic seal species (bearded, ringed, and spotted) that are faced with a rapidly changing environment.

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 (δ (15)N) and carbon (δ (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 Año Nuevo Islands). Total Hg concentrations ranged from 0.01 to 0.31 µg g(-1) wet weight (ww) in blood and 0.74 to 21.00 µg g(-1) dry weight (dw) in hair. Adult females had greater mean THg concentrations than juveniles in blood (0.15 vs. 0.03 µg(-1) ww) and hair (10.10 vs. 3.25 µg(-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 δ (15)N or δ (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.

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.

Selenium and mercury concentrations in harbor seals (Phoca vitulina) from central California: health implications in an urbanized estuary.

We measured total selenium and total mercury concentrations ([TSe] and [THg]) in hair (n=138) and blood (n=73) of harbor seals (Phoca vitulina) from California to assess variation by geography and sex, and inferred feeding relationships based on carbon, nitrogen, and sulfur stable isotopes. Harbor seals from Hg-contaminated sites had significantly greater [THg], and lesser [TSe] and TSe:THg molar ratios than seals from a relatively uncontaminated site. Males had significantly greater [THg] than females at all locations. Sulfur stable isotope values explained approximately 25% of the variability in [THg], indicating increased Hg exposure for seals with a greater use of estuarine prey species. Decreased [TSe] in harbor seals from Hg-contaminated regions may indicate a relative Se deficiency to mitigate the toxic effects of Hg. Further investigation into the Se status and the potential negative impact of Hg on harbor seals from Hg-contaminated sites is warranted.