Interspecific Variations in the Internal Mercury Isotope Dynamics of Antarctic Penguins: Implications for Biomonitoring.

Mercury (Hg) biomonitoring requires a precise understanding of the internal processes contributing to disparities between the Hg sources in the environment and the Hg measured in the biota. In this study, we investigated the use of Hg stable isotopes to trace Hg accumulation in Adélie and emperor penguin chicks from four breeding colonies in Antarctica. Interspecific variation of Δ199Hg in penguin chicks reflects the distinct foraging habitats and Hg exposures in adults. Chicks at breeding sites where adult penguins predominantly consumed mesopelagic prey showed relatively lower Δ199Hg values than chicks that were primarily fed epipelagic krill. Substantial δ202Hg variations in chick tissues were observed in both species (Adélie: -0.11 to 1.13‰, emperor: -0.27 to 1.15‰), whereas only emperor penguins exhibited the lowest δ202Hg in the liver and the highest in the feathers. Our results indicate that tissue-specific δ202Hg variations and their positive correlations with % MeHg resulted from MeHg demethylation in the liver and kidneys of emperor penguin chicks, whereas Adélie penguin chicks showed different internal responses depending on their exposure to dietary MeHg. This study highlights the importance of considering intra- and interspecific variations in adult foraging ecology and MeHg demethylation when selecting penguin chicks for Hg biomonitoring.

Internal Dynamics and Metabolism of Mercury in Biota: A Review of Insights from Mercury Stable Isotopes.

Monitoring mercury (Hg) levels in biota is considered an important objective for the effectiveness evaluation of the Minamata Convention. While many studies have characterized Hg levels in organisms at multiple spatiotemporal scales, concentration analyses alone often cannot provide sufficient information on the Hg exposure sources and internal processes occurring within biota. Here, we review the decadal scientific progress of using Hg isotopes to understand internal processes that modify the speciation, transport, and fate of Hg within biota. Mercury stable isotopes have emerged as a powerful tool for assessing Hg sources and biogeochemical processes in natural environments. A better understanding of the tissue location and internal mechanisms leading to Hg isotope change is key to assessing its use for biomonitoring. We synthesize the current understanding and uncertainties of internal processes leading to Hg isotope fractionation in a variety of biota, in a sequence of better to less studied organisms (i.e., birds, marine mammals, humans, fish, plankton, and invertebrates). This review discusses the opportunities and challenges of using certain forms of biota for Hg source monitoring and the need to further elucidate the physiological mechanisms that control the accumulation, distribution, and toxicity of Hg in biota by coupling new techniques with Hg stable isotopes.

Mercury Stable Isotopes Reveal Influence of Foraging Depth on Mercury Concentrations and Growth in Pacific Bluefin Tuna.

Pelagic ecosystems are changing due to environmental and anthropogenic forces, with uncertain consequences for the ocean's top predators. Epipelagic and mesopelagic prey resources differ in quality and quantity, but their relative contribution to predator diets has been difficult to track. We measured mercury (Hg) stable isotopes in young (<2 years old) Pacific bluefin tuna (PBFT) and their prey species to explore the influence of foraging depth on growth and methylmercury (MeHg) exposure. PBFT total Hg (THg) in muscle ranged from 0.61 to 1.93 µg g-1 dw (1.31 µg g-1 dw ±0.37 SD; 99% ± 6% MeHg) and prey ranged from 0.01 to 1.76 µg g-1 dw (0.13 µg g-1 dw ±0.19 SD; 85% ± 18% MeHg). A systematic decrease in prey δ202Hg and Δ199Hg with increasing depth of occurrence and discrete isotopic signatures of epipelagic prey (δ202Hg: 0.74 to 1.49‰; Δ199Hg: 1.76-2.96‰) and mesopelagic prey (δ202Hg: 0.09 to 0.90‰; Δ199Hg: 0.62-1.95‰) allowed the use of Hg isotopes to track PBFT foraging depth. An isotopic mixing model was used to estimate the dietary proportion of mesopelagic prey in PBFT, which ranged from 17% to 55%. Increased mesopelagic foraging was significantly correlated with slower growth and higher MeHg concentrations in PBFT. The slower observed growth rates suggest that prey availability and quality could reduce the production of PBFT biomass.

Results of a national survey of high-frequency fish consumers in the United States.

Exposure to contaminants in fish may be associated with adverse health outcomes even as fish consumption is generally considered beneficial. Risk assessments conducted to support regulatory analyses rely on quantitative fish consumption estimates. Here we report the results of a national survey of high-frequency fish consumers (n = 2099) based on a survey population statistically representative of ~17.6 million U.S. individuals consuming three or more fish meals per week. The survey was conducted during 2013 using an on-line survey instrument. Total fish consumption averaged 111g/day from market, restaurant and self-caught sources. Depending on the season, the incidence of individuals reporting consumption of self-caught species ranged between 10-12% of our high-frequency fish consuming demographic, averaging approximately 30g/day and comprising 23% of total fish consumption from all sources of fish. Recreational or self-caught consumption rates vary regionally and are poorly understood, particularly for high-frequency consumers, making it difficult to support national-scale assessments. A divergence between sport-fishing and harvesting of fish as a food-staple is apparent in survey results given differences in consumption patterns with income and education. Highest consumption rates were reported for low income respondents more likely to harvest fish as a food staple. By contrast, the incidence of self-caught fish consumption was higher with income and education although overall consumption rates were lower. Regional differences were evident, with respondents from the East-South Central and New England regions reporting lowest consumption rates from self-caught fish on the order of 12-16g/day and those from Mountain, Pacific and Mid-Atlantic regions reporting highest rates ranging from 44 to 59g/day. Respondent-specific consumption rates together with national-level data on fish tissue concentrations of PCBs, MeHg, and PFOS suggest that 10-58% of respondents reporting self-caught fish consumption are exposed to concentrations of these contaminants that exceed threshold levels for health effects based on a target hazard index of one, representing 2.3M to 19M individuals. The results of this nationwide survey of high-frequency fish consumers highlights regional and demographic differences in self-caught and total fish consumption useful for policy analysis with implications for distributional differences in potential health impacts in the context of both contaminant exposures as well as protective effects.

Future Impacts of Hydroelectric Power Development on Methylmercury Exposures of Canadian Indigenous Communities.

Developing Canadian hydroelectric resources is a key component of North American plans for meeting future energy demands. Microbial production of the bioaccumulative neurotoxin methylmercury (MeHg) is stimulated in newly flooded soils by degradation of labile organic carbon and associated changes in geochemical conditions. We find all 22 Canadian hydroelectric facilities being considered for near-term development are located within 100 km of indigenous communities. For a facility in Labrador, Canada (Muskrat Falls) with planned completion in 2017, we probabilistically modeled peak MeHg enrichment relative to measured baseline conditions in the river to be impounded, downstream estuary, locally harvested fish, birds and seals, and three Inuit communities. Results show a projected 10-fold increase in riverine MeHg levels and a 2.6-fold increase in estuarine surface waters. MeHg concentrations in locally caught species increase 1.3 to 10-fold depending on time spent foraging in different environments. Mean Inuit MeHg exposure is forecasted to double following flooding and over half of the women of childbearing age and young children in the most northern community are projected to exceed the U.S. EPA's reference dose. Equal or greater aqueous MeHg concentrations relative to Muskrat Falls are forecasted for 11 sites across Canada, suggesting the need for mitigation measures prior to flooding.

Environmental Origins of Methylmercury Accumulated in Subarctic Estuarine Fish Indicated by Mercury Stable Isotopes.

Methylmercury (MeHg) exposure can cause adverse reproductive and neurodevelopmental health effects. Estuarine fish may be exposed to MeHg produced in rivers and their watersheds, benthic sediment, and the marine water column, but the relative importance of each source is poorly understood. We measured stable isotopes of mercury (δ202Hg, Δ199Hg, and Δ201Hg), carbon (δ13C), and nitrogen (δ15N) in fish with contrasting habitats from a large subarctic coastal ecosystem to better understand MeHg exposure sources. We identify two distinct food chains exposed to predominantly freshwater and marine MeHg sources but do not find evidence for a benthic marine MeHg signature. This is consistent with our previous research showing benthic sediment is a net sink for MeHg in the estuary. Marine fish display lower and less variable Δ199Hg values (0.78‰ to 1.77‰) than freshwater fish (0.72‰ to 3.14‰) and higher δ202Hg values (marine: 0.1‰ to 0.57‰; freshwater: -0.76‰ to 0.15‰). We observe a shift in the Hg isotopic composition of juvenile and adult rainbow smelt (Osmerus mordax) when they transition between the freshwater and marine environment as their dominant foraging territory. The Hg isotopic composition of Atlantic salmon (Salmo salar) indicates they receive most of their MeHg from the marine environment despite a similar or longer duration spent in freshwater regions. We conclude that stable Hg isotopes effectively track fish MeHg exposure sources across different ontogenic stages.

Assessing sources of human methylmercury exposure using stable mercury isotopes.

Seafood consumption is the primary route of methylmercury (MeHg) exposure for most populations. Inherent uncertainties in dietary survey data point to the need for an empirical tool to confirm exposure sources. We therefore explore the utility of Hg stable isotope ratios in human hair as a new method for discerning MeHg exposure sources. We characterized Hg isotope fractionation between humans and their diets using hair samples from Faroese whalers exposed to MeHg predominantly from pilot whales. We observed an increase of 1.75‰ in δ(202)Hg values between pilot whale muscle tissue and Faroese whalers' hair but no mass-independent fractionation. We found a similar offset in δ(202)Hg between consumed seafood and hair samples from Gulf of Mexico recreational anglers who are exposed to lower levels of MeHg from a variety of seafood sources. An isotope mixing model was used to estimate individual MeHg exposure sources and confirmed that both Δ(199)Hg and δ(202)Hg values in human hair can help identify dietary MeHg sources. Variability in isotopic signatures among coastal fish consumers in the Gulf of Mexico likely reflects both differences in environmental sources of MeHg to coastal fish and uncertainty in dietary recall data. Additional data are needed to fully refine this approach for individuals with complex seafood consumption patterns.

Interactive effects of phosphorus and copper on Hyalella azteca via periphyton in aquatic ecosystems.

This research examined the interaction between dissolved copper and phosphorus, with respect to their effects on the freshwater amphipod Hyalella azteca feeding on periphyton. Field-collected periphyton communities were exposed to different nutrient and metal conditions in indoor recirculating streams. H. azteca were then exposed to water and periphyton from these streams. There was rapid Cu accumulation by periphyton but the total Cu concentration of periphyton was not directly related to dissolved P. In terms of H. azteca growth, an interactive effect was found between Cu and P as growth was reduced more than expected in the low Cu-high P treatment. Our data suggest that eutrophic conditions result in greater Cu toxicity to benthic macroinvertebrates at lower metal concentrations, likely due to higher assimilation efficiency of dietary Cu from periphyton incubated under eutrophic conditions. These results imply that non-additive interactions between multiple stressors may cause ecosystem effects as detected in standard laboratory bioassays conducted under controlled conditions.

Elucidating sources of mercury in the west coast of Korea and the Chinese marginal seas using mercury stable isotopes.

Nearshore systems play an important role as mercury (Hg) sources to the open ocean and to human health via fish consumption. The nearshore system along East Asia is of particular concern given the rapid industrialization, which contributes to significant anthropogenic Hg emissions and releases. We used Hg stable isotopes to characterize Hg sources in the sediment and fish along the west coast of Korea, located at the northeast of the East China Sea. The Hg isotope ratios of the west coast sediments (δ202Hg; -0.89 to -0.27‰, Δ199Hg; -0.04 to 0.14‰) were statistically similar with other nearshore sediments (δ202Hg; -0.99 to -0.30‰, Δ199Hg; -0.04 to 0.19‰) and overlapped with the industrial Hg source end-member (δ202Hg; -0.5‰, Δ199Hg; 0.01‰) estimated from the Chinese marginal seas. Using a ternary mixing model, we estimated that industrial Hg sources contribute 83-97% in the west coast of Korea, and riverine and atmospheric Hg sources play minor roles in the Korean west coast and the Chinese marginal seas. The comparison between Hg isotope ratios of the sediment and nearshore fish revealed that the fish in the most west coast sites are exposed to MeHg produced in the sediment. At a few southwest coast sites, external MeHg produced in rivers and the open ocean water column appears to be more important as a source in fish. This is supported by much higher δ202Hg (0.74‰; similar to oceanic fish) and lower δ202Hg (-0.71‰; similar to riverine sources) compared to fish collected from other west coast sites influenced by sedimentary MeHg. The substantial Hg contributions from industrial activities suggest the national policies regulating anthropogenic Hg releases can directly mitigate human Hg exposure originating via local fish consumption. This study contributes to the growing regional and global inventories of Hg fluxes and sources exported into coastal oceans.

The beneficial and hazardous effects of selenium on the health of the soil-plant-human system: An overview.

Selenium (Se), which can be both hazardous and beneficial to plants, animals and humans, plays a pivotal role in regulating soil-plant-human ecosystem functions. The biogeochemical behavior of Se and its environmental impact on the soil-plant-human system has received broad attention in the last decades. This review provides a comprehensive understanding of Se biogeochemistry in the soil-plant-human system. The speciation, transformation, bioavailability as well as the beneficial and hazardous effects of Se in the soil-plant-human system are summarized. Several important aspects in Se in the soil-plant-human system are detailed mentioned, including (1) strategies for biofortification in Se-deficient areas and phytoremediation of soil Se in seleniferous areas; (2) factors affecting Se uptake and transport by plants; (3) metabolic pathways of Se in the human body; (4) the interactions between Se and other trace elements in plant and animals, in particular, the detoxification of heavy metals by Se. Important research hotspots of Se biogeochemistry are outlined, including (1) the coupling of soil microbial activity and the Se biogeochemical cycle; (2) the molecular mechanism of Se metabolic in plants and animals; and (3) the application of Se isotopes as a biogeochemical tracer in research. This review provides up-to-date knowledge and guidelines on Se biogeochemistry research.

Investigating the dynamics of methylmercury bioaccumulation in the Beaufort Sea shelf food web: a modeling perspective.

High levels of methylmercury (MeHg) have been reported in Arctic marine biota, posing health risks to wildlife and human beings. Although MeHg concentrations of some Arctic species have been monitored for decades, the key environmental and ecological factors driving temporal trends of MeHg are largely unclear. We develop an ecosystem-based MeHg bioaccumulation model for the Beaufort Sea shelf (BSS) using the Ecotracer module of Ecopath with Ecosim, and apply the model to explore how MeHg toxicokinetics and food web trophodynamics affect bioaccumulation in the BSS food web. We show that a food web model with complex trophodynamics and relatively simple MeHg model parametrization can capture the observed biomagnification pattern of the BSS. While both benthic and pelagic production are important for transferring MeHg to fish and marine mammals, simulations suggest that benthic organisms are primarily responsible for driving the high trophic magnification factor in the BSS. We illustrate ways of combining empirical observations and modelling experiments to generate hypotheses about factors affecting food web bioaccumulation, including the MeHg elimination rate, trophodynamics, and species migration behavior. The results indicate that population dynamics rather than MeHg elimination may determine population-wide concentrations for fish and lower trophic level organisms, and cause large differences in concentrations between species at similar trophic levels. This research presents a new tool and lays the groundwork for future research to assess the pathways of global environmental changes in MeHg bioaccumulation in Arctic ecosystems in the past and the future.

Internal dynamics of inorganic and methylmercury in a marine fish: Insights from mercury stable isotopes.

Mercury isotope ratios in fish tissues have been used to infer sources and biogeochemical processes of mercury in aquatic ecosystems. More experimental studies are however needed to understand the internal dynamics of mercury isotopes and to further assess the feasibility of using fish mercury isotope ratios as a monitoring tool. We exposed Olive flounder (Paralichthys olivaceus) to food pellets spiked with varying concentrations (400, 1600 ng/g) of methylmercury (MeHg) and inorganic mercury (IHg) for 10 weeks. Total mercury (THg), MeHg concentrations, and mercury isotope ratios (δ202Hg, Δ199Hg, Δ200Hg) were measured in the muscle, liver, kidney, and intestine of fish. Fish fed mercury unamended food pellets and MeHg amended food pellets showed absence of internal δ202Hg and Δ199Hg fractionation in all tissue type. For fish fed IHg food pellets, the δ202Hg and Δ199Hg values of intestine equilibrated to those of the IHg food pellets. Kidney, muscle, and liver exhibited varying degrees of isotopic mixing toward the IHg food pellets, consistent with the degree of IHg bioaccumulation. Liver showed additional positive δ202Hg shifts (∼0.63‰) from the binary mixing line between the unamended food pellets and IHg food pellets, which we attribute to redistribution or biliary excretion of liver IHg with a lower δ202Hg to other tissues. Significant δ202Hg fractionation in the liver and incomplete isotopic equilibration in the muscle indicate that these tissues may not be suitable for source monitoring at sites heavily polluted by IHg. Instead, fish intestine appears to be a more suitable proxy for identifying IHg sources. The results from our study are essential for determining the appropriate fish tissues for monitoring environmental sources of IHg and MeHg.

Selenium and stable mercury isotopes provide new insights into mercury toxicokinetics in pilot whales.

High exposures of mammalian species to inorganic mercury (HgII) and methylmercury (MeHg) have been associated with adverse effects on behavior and reproduction. Different mammalian species exhibit varying responses to similar external exposure levels, reflecting potential differences in Hg toxicokinetics. Here, we use Hg stable isotopes, total Hg, MeHg and selenium (Se) concentrations measured in multiple tissues of North Atlantic pilot whales (Globicephala melas) to investigate processes affecting the distribution and accumulation of HgII and MeHg. We find that simple mixing of two distinct isotopic end-members: MeHg (1.4‰) and HgII (-1.6‰) can explain the observed variability of δ202Hg in brain tissue. A similar isotopic composition for the MeHg end-member in the brain, muscle, heart, and kidney suggests efficient exchange of MeHg in blood throughout the body. By contrast, the Hg isotopic composition of the liver of adult whales is different from younger whales and other tissues that follow the two-end member mixing model. Measured Se:Hg ratios are lowest in adult whales with the highest levels of MeHg exposure. In these individuals, Se availability is likely reduced by complexation with demethylated HgII. We speculate that this results in a higher fraction of labile HgII eliminated from the liver of adult whales compared to young whales and subsequent redistribution to other tissues, potentially affecting toxicity.

Primary amino acids affect the distribution of methylmercury rather than inorganic mercury among tissues of two farmed-raised fish species.

The distributions of primary amino acids, MeHg and IHg in body tissues of two commonly farm-raised fish species (common carp: Cyprinus carpio; grass carp: Ctenopharyngodon idellus) in Guizhou Province, SW China, were investigated to understand the effects of primary amino acids on MeHg and IHg metabolism in farm-raised fish. The primary amino acids were classified into four groups: (1) essential and polar amino acids; (2) essential and non-polar amino acids; (3) non-essential and polar amino acids; and (4) non-essential and non-polar amino acids. For both fish species, groups (1, 2 and 3) were enriched in muscle and kidney, whereas group (4) was enriched in scale. The two fish species showed low MeHg concentrations (grass carp: 0.5-3.9 ng/g; common carp:1.0-7.4 ng/g) and low MeHg proportions (grass carp: 2-45%; common carp: 6-37%) in their tissues, which are mainly due to the simple food web structures and the fast growth of the farm-raised fish. Positive correlations (r = 0.342 to 0.472; p < 0.01; n = 78) were observed between MeHg and several primary amino acids (cysteine, threonine, phenylalanine, leucine, valine, glutamate serine and tyrosine) in fish tissues, which may be driven by the formation of MeHg-Cys complexes within fish body. However, no significant correlations were observed between IHg and any primary amino acids, indicating the metabolic processes of IHg and MeHg are different. This study advances our understanding that cysteine and its related/derived amino acids may be an important driving force for MeHg distribution and translocation in fish.

Organ-specific differences in mercury speciation and accumulation across ringed seal (Phoca hispida) life stages.

Methylmercury (MeHg) is a central nervous system toxicant and exposures can adversely affect the health of marine mammals. Mercuric selenide (HgSe) in marine mammal tissues is hypothesized to result from a protective detoxification mechanism, but toxicokinetic processes contributing to its formation are poorly understood. Here, new data is reported on speciated Hg concentrations in multiple organs of n = 56 ringed seals (Phoca hispida) from Labrador, Canada, and compare concentrations to previously published data from Greenland seals. A higher proportion of Hg is found to accumulate in the kidney of young-of-the-year (YOY) ringed seals compared to adults. A toxicokinetic model for Hg species is developed and evaluated to better understand factors affecting variability in Hg concentrations among organs and across life stages. Prior work postulated that HgSe formation only occurs in the liver of mature seals, but model results suggest HgSe formation occurs across all life stages. Higher proportions of HgSe in mature seal livers compared to YOY seals likely results from the slow accumulation and elimination of HgSe (total body half-life = 500 days) compared to other Hg species. HgSe formation in the liver reduces modeled blood concentrations of MeHg by only 6%. Thus, HgSe formation may not substantially reduce MeHg transport across the blood-brain barrier of ringed seals, leaving them susceptible to the neurotoxic effects of MeHg exposure.

Phospholipid Levels Predict the Tissue Distribution of Poly- and Perfluoroalkyl Substances in a Marine Mammal.

Exposure to poly- and perfluoroalkyl substances (PFASs) has been linked to many negative health impacts in humans and wildlife. Unlike neutral hydrophobic organic pollutants, many PFASs are ionic and have been hypothesized to accumulate in both phospholipids and protein-rich tissues. Here we investigate the role of phospholipids for PFAS accumulation by analyzing associations among concurrent measurements of phospholipid, total protein, total lipid and 24 PFASs in the heart, muscle, brain, kidney, liver, blubber, placenta and spleen of North Atlantic pilot whales (Globicephala melas). The sum of 24 PFASs ( ∑ 24 PFAS ) was highest in the liver (median 260 ng g-1; interquartile range (IQR) 216-295 ng g-1) and brain (86.0; IQR 54.5-91.3 ng g-1), while phospholipid levels were highest in brain. The relative abundance of PFASs in the brain greatly increases with carbon chain lengths of 10 or greater, suggesting shorter-chained compounds may cross the blood-brain barrier less efficiently. Phospholipids were significant predictors of the tissue distribution of the longest-chained PFASs: perfluorodecanesulfonate (PFDS), perfluorododecanoate (PFDoA), perfluorotridecanoate (PFTrA), and perfluorotetradecanoic acid (PFTA) (rs = 0.5-0.6). In all tissues except the brain, each 1 mg g-1 increase in phospholipids led to a 12%-25% increase in the concentration of each PFAS. We conclude that partitioning to phospholipids is an important mechanism of bioaccumulation for long-chained PFASs in marine mammals.

Erratum: "Decadal Changes in the Edible Supply of Seafood and Methylmercury Exposure in the United States".

[This corrects the article DOI: https://doi.org/10.1289/EHP2644.].

Decadal Changes in the Edible Supply of Seafood and Methylmercury Exposure in the United States.

BACKGROUND: Methylmercury (MeHg) exposure is associated with adverse effects on neurodevelopment and cardiovascular health. Previous work indicates most MeHg is from marine fish sold in the commercial market, but does not fully resolve supply regions globally. This information is critical for linking changes in environmental MeHg levels to human exposure in the U.S. population. OBJECTIVES: We used available data to estimate the geographic origins of seafood consumed in the United States (major ocean basins, coastal fisheries, aquaculture, freshwater) and how shifts in edible supply affected MeHg exposures between 2000-2002 and 2010-2012. METHODS: Source regions for edible seafood and MeHg exposure in the United States were characterized from national and international landing, export and import data from the Food and Agricultural Organization of the United Nations and the U.S. National Marine Fisheries Service. RESULTS: Our analysis suggests 37% of U.S. population-wide MeHg exposure is from mainly domestic coastal systems and 45% from open ocean ecosystems. We estimate that the Pacific Ocean alone supplies more than half of total MeHg exposure. Aquaculture and freshwater fisheries together account for an estimated 18% of total MeHg intake. Shifts in seafood types and supply regions between 2000-2002 and 2010-2012 reflect changes in consumer preferences (e.g., away from canned light meat tuna), global ecosystem shifts (e.g., northern migration of cod stocks), and increasing supply from aquaculture (e.g., shrimp and salmon). CONCLUSION: Our findings indicate global actions that reduce anthropogenic Hg emissions will be beneficial for U.S. seafood consumers because open ocean ecosystems supply a large fraction of their MeHg exposure. However, our estimates suggest that domestic actions can provide the greatest benefit for coastal seafood consumers. https://doi.org/10.1289/EHP2644.