Patterns in forage fish mercury concentrations across Northeast US estuaries.

Biogeochemical conditions and landscape can have strong influences on mercury bioaccumulation in fish, but these effects across regional scales and between sites with and without point sources of contamination are not well understood. Normal means clustering, a type of unsupervised machine learning, was used to analyze relationships between forage fish (Fundulus heteroclitus and Menidia menidia) mercury (Hg) concentrations and sediment and water column Hg and methylmercury (MeHg) concentrations, ancillary variables, and land classifications within the sub-watershed. The analysis utilized data from 38 sites in 8 estuarine systems in the Northeast US, collected over five years. A large range of mercury concentrations and land use proportions were observed across sites. The cluster correlations indicated that for Fundulus, benthic and pelagic Hg and MeHg concentrations were most related to tissue concentrations, while Menidia Hg was most related to water column MeHg, reflecting differing feeding modes between the species. For both species, dissolved MeHg was most related to tissue concentrations, with sediment Hg concentrations influential at contaminated sites. The models considering only uncontaminated sites showed reduced influence of bulk sediment MeHg for both species, but Fundulus retained sediment drivers at some sites, with dissolved MeHg still highly correlated for both. Dissolved organic carbon (DOC), chlorophyll, land use, and other ancillary variables were of lesser importance in driving bioaccumulation, though DOC was strongly related within some clusters, likely in relation to dissolved Hg. Land use, though not of primary importance, showed relationships opposite to those observed in freshwater, with development positively correlated and forests and agriculture negatively correlated with tissue concentrations across clusters and species. Clusters were composed of sites from geographically distinct systems, indicating the greater importance of small scale drivers of MeHg formation and uptake into the food web over system or region-wide influences.

Bioaccumulation of methylmercury in wood frogs and spotted salamanders in Vermont vernal pools.

Mercury (Hg) has accumulated in forested landscapes in the Northeastern U.S., and hotspots with enhanced deposition have been identified throughout the region. Due to a variety of favorable landscape characteristics, including relatively high dissolved organic carbon (DOC), fluctuating water levels, and low pH and dissolved oxygen, vernal pools provide ideal conditions for the conversion of Hg to its more toxic and bioavailable form, methylmercury (MeHg). Yet little is known about the concentrations, speciation, and bioavailability of Hg in vernal pools, or its bioaccumulation in vernal pool fauna and potential export into terrestrial systems. We investigated the role of forest cover type on the bioaccumulation of MeHg in wood frog (Lithobates sylvatica) and spotted salamander (Ambystoma maculatum) eggs, larvae, and adults, and investigated relationships among MeHg and water chemistry (pH, DOC). Water samples from pools located in coniferous stands had greater concentrations of THg and MeHg compared to deciduous pool water, and showed significant positive correlation to DOC (r = 0.683, P < 0.001) and correlated negatively with pH (r = -0.613, P < 0.001). Methylmercury levels in amphibian embryos were similar between the two species (L. sylvatica mean = 5.4 ng/g dw; A. maculatum mean = 3.5 ng/g dw). Concentrations of MeHg increased substantially in larvae, and were significantly greater in A. maculatum (mean = 237.6 ng/g ± 18.5 SE) than L. sylvatica larvae (62.5 ng/g ± 5.7 SE). Forest cover type did not explain variation in MeHg concentration among amphibian embryos or larvae. Methylmercury levels in adult tissue samples were significantly greater in A. maculatum (mean = 79.9 ng/g ± 8.9 SE) compared to L. sylvatica (mean = 47.7 ng/g ± 9.7 SE). This research demonstrates that vernal pools are important hotspots where amphibians bioaccumulate MeHg, which may then be transferred to terrestrial ecosystems. The abundance of amphibian larvae suggests they could be important bioindicators for monitoring MeHg loading and bioavailability.

Spatial and taxonomic variation of mercury concentration in low trophic level fauna from the Mediterranean Sea.

Studies of mercury (Hg) in the Mediterranean Sea have focused on pollution sources, air-sea mercury exchange, abiotic mercury cycling, and seafood. Much less is known about methylmercury (MeHg) concentrations in the lower food web. Zooplankton and small fish were sampled from the neuston layer at both coastal and open sea stations in the Mediterranean Sea during three cruise campaigns undertaken in the fall of 2011 and the summers of 2012 and 2013. Zooplankton and small fish were sorted by morphospecies, and the most abundant taxa (e.g. euphausiids, isopods, hyperiid amphipods) analyzed for methylmercury (MeHg) concentration. Unfiltered water samples were taken during the 2011 and 2012 cruises and analyzed for MeHg concentration. Multiple taxa suggested elevated MeHg concentrations in the Tyrrhenian and Balearic Seas in comparison with more eastern and western stations in the Mediterranean Sea. Spatial variation in zooplankton MeHg concentration is positively correlated with single time point whole water MeHg concentration for euphausiids and mysids and negatively correlated with maximum chlorophyll a concentration for euphausiids, mysids, and "smelt" fish. Taxonomic variation in MeHg concentration appears driven by taxonomic grouping and feeding mode. Euphausiids, due to their abundance, relative larger size, importance as a food source for other fauna, and observed relationship with surface water MeHg are a good candidate biotic group to evaluate for use in monitoring the bioavailability of MeHg for trophic transfer in the Mediterranean and potentially globally.

Influence of sample preparation on estuarine macrofauna stable isotope signatures in the context of contaminant bioaccumulation studies.

The ratios of stable isotopes of carbon and nitrogen provide important information on food sources of aquatic organisms and trophic structure of aquatic food webs. For many studies, trophic position and food source are linked to bioaccumulation and trophic transfer of contaminants from prey to predators. In these cases, it is useful to use measurements on whole organisms to make direct comparisons of contaminant bioaccumulation and food web attributes. There is a great deal of variation in methods used for stable isotope analysis, particularly in the selection of tissue type and sample preparation prior to stable isotope analysis. While there have been aquatic studies that examined methodological differences, few have focused on estuarine organisms. In this study, the effects of depuration and tissue dissection on the stable isotope enrichment of common estuarine invertebrates and fish were examined. Homogenized tissues of non-depurated whole organisms were compared to dissected muscle tissue or depurated whole organisms. A 24 h depuration did not change the mean δ15N and δ13C values for most species examined. Additionally, as expected, significant differences in carbon and nitrogen signatures were found when muscle tissues were compared to whole organisms. However, differences were small enough that food source as inferred by δ13C or trophic level as inferred from δ15N would not be inaccurately represented (differences of <1.9‰ for δ13C and <1.2‰ for δ15N). The results of this study suggest that for these common estuarine fish and macroinvertebrates, stable isotopes ratios of samples can be analyzed without depuration in the same way as samples for contaminant analysis, but differences in tissue types must be taken into account when combining data from different sources.

Spatial variability of metal bioaccumulation in estuarine killifish (Fundulus heteroclitus) at the Callahan mine superfund site, Brooksville, ME.

The former Callahan Mine Site in Brooksville, ME, is an open-pit, hardrock mine site in an intertidal system, thus providing a unique opportunity to evaluate how metal-enriched sediments and overlying water impact estuarine food webs. Copper, zinc, cadmium, and lead concentrations in sediment, whole water, and Atlantic killifish (Fundulus heteroclitus) were evaluated at sites in Goose Pond (GP; Callahan Mine Site) and at reference sites. The metal concentrations of sediment, water, and fish were spatially distinct and significantly greater at the mine site than in the reference estuary. Sediment concentrations were particularly elevated and were above probable effects levels for all four metals adjacent to the tailings pile. Even in this well-mixed system, water metal concentrations were significantly elevated adjacent to the tailings pile, and concentrations of Cu and Zn were above ambient water-quality criteria for chronic marine exposure. Neither organic matter in the sediment nor salinity or pH of the water explained the metal concentrations. Adjacent to the tailings pile, killifish metal body burdens were elevated and were significantly related to both sediment and aqueous concentrations. In conclusion, (1) the contaminated sediment and seepage from the tailings impoundment and waste rock pile no. 3 create a continual flux of metals into the water column, (2) the metals are bioavailable and bioconcentrating as evident in the killifish tissue concentrations, and (3) Callahan Mine is directly affecting metal bioaccumulation in fauna residing in the GP estuary and, potentially, in Penobscot Bay by the way of "trophic nekton relay."

An examination of the factors influencing the bioaccumulation of methylmercury at the base of the estuarine food web.

Estuarine systems have received ongoing mercury (Hg) inputs from both point sources and regional contamination and have high legacy Hg in sediments. This is an environmental concern given that coastal seafood is an important vector for human exposure to methylmercury (MeHg). The base of the food chain represents the most important trophic steps for MeHg bioaccumulation. The magnitude of the uptake by phytoplankton, and their consumers, is influenced by many factors, in addition to sediment and water MeHg concentrations, that impact MeHg assimilation into phytoplankton and the trophic transfer to higher trophic levels, both benthic and pelagic. For forage fish, such as mummichogs (Fundulus heteroclitus), abiotic and biotic (bioenergetic) factors can influence their MeHg content, and diet is also important as they feed both on benthic and pelagic prey. Given that the importance of sediment MeHg versus pelagic MeHg sources has been debated, we updated a phytoplankton bioaccumulation model, and coupled this with a bioaccumulation model for MeHg concentration in mummichog tissue to examine the controlling factors for sites, from Maine to Maryland, USA, ranging widely in their Hg concentrations and other variables. The study highlighted the importance of DOC in modulating uptake into the pelagic food web, but also demonstrated the importance of diet in controlling mummichog MeHg. Finally, the relative importance of MeHg source - sediment or water column - was correlated with the level of Hg contamination. Sediment-derived MeHg was a more important source for highly Hg contaminated systems. As water column and sediment MeHg are not strongly correlated for the studied ecosystems, their importance as a source of MeHg to mummichogs varies with location. The study highlights the differences across ecosystems in MeHg bioaccumulation pathways, and that uptake into phytoplankton is an important variable controlling forage fish concentration.

Nutrient supply and mercury dynamics in marine ecosystems: a conceptual model.

There is increasing interest and concern over the impacts of mercury (Hg) inputs to marine ecosystems. One of the challenges in assessing these effects is that the cycling and trophic transfer of Hg are strongly linked to other contaminants and disturbances. In addition to Hg, a major problem facing coastal waters is the impacts of elevated nutrient, particularly nitrogen (N), inputs. Increases in nutrient loading alter coastal ecosystems in ways that should change the transport, transformations and fate of Hg, including increases in fixation of organic carbon and deposition to sediments, decreases in the redox status of sediments and changes in fish habitat. In this paper we present a conceptual model which suggests that increases in loading of reactive N to marine ecosystems might alter Hg dynamics, decreasing bioavailabilty and trophic transfer. This conceptual model is most applicable to coastal waters, but may also be relevant to the pelagic ocean. We present information from case studies that both support and challenge this conceptual model, including marine observations across a nutrient gradient; results of a nutrient-trophic transfer Hg model for pelagic and coastal ecosystems; observations of Hg species, and nutrients from coastal sediments in the northeastern U.S.; and an analysis of fish Hg concentrations in estuaries under different nutrient loadings. These case studies suggest that changes in nutrient loading can impact Hg dynamics in coastal and open ocean ecosystems. Unfortunately none of the case studies is comprehensive; each only addresses a portion of the conceptual model and has limitations. Nevertheless, our conceptual model has important management implications. Many estuaries near developed areas are impaired due to elevated nutrient inputs. Widespread efforts are underway to control N loading and restore coastal ecosystem function. An unintended consequence of nutrient control measures could be to exacerbate problems associated with Hg contamination. Additional focused research and monitoring are needed to critically examine the link between nutrient supply and Hg contamination of marine waters.

Historic contamination alters mercury sources and cycling in temperate estuaries relative to uncontaminated sites.

Mercury (Hg) is a global and persistent pollutant which can be methylated to more toxic forms (methylmercury; MeHg) in natural systems. Both forms pose a health risk to humans and wildlife, and exposure often begins in aquatic environments. Therefore, quantifying aquatic concentrations and identifying source pathways is important for understanding biotic exposure. In this study, data from estuaries in the Northeast United States were combined to evaluate how point source contamination impacts the concentration and source dynamics of water column total and MeHg with an emphasis on sediment versus non-sediment sources. Partial least squares regression models were implemented to identify a set of variables most related to water column MeHg and total Hg (HgT) across the estuaries. The main findings suggest that contaminated sites have strong internal recycling of HgT that dominates over external inputs, and this leads to elevated concentrations of HgT and MeHg in the local water columns. However, HgT sources in uncontaminated estuarine systems have a strong connection to the local watershed with dissolved HgT linked to dissolved organic carbon, and particulate HgT linked to watershed land use and estuarine mixing. There was little correlative evidence that water column MeHg concentrations were linked to sediment in such systems, but unlike HgT, the concentrations were also not clearly linked to the watershed. Instead, in situ methylation of dissolved water column HgT appeared to dominate the MeHg source pathway. The results suggest that Hg point-source contaminated sites should be considered independently from non-contaminated sites in terms of management, and that land use plays an important indirect role in coastal MeHg dynamics.

The influence of nutrient loading on methylmercury availability in Long Island estuaries.

Estuaries provide critical habitat for food webs supporting fish and shellfish consumed by humans, but estuarine ecosystem health has been threatened by increases in nitrogen loading as well as inputs of the neurotoxin, mercury (Hg), which biomagnifies in food webs and poses risk to humans and wildlife. In this study, the effects of nutrient loading on the fate of Hg in shallow coastal estuaries were examined to evaluate if their interaction enhances or reduces Hg bioavailability in sediments, the water column, and concentrations in lower trophic level fish (Fundulus heteroclitus and Menidia menidia). Multiple sites were sampled within two human impacted coastal lagoons, Great South Bay (GSB) and Jamaica Bay (JB), on the southern coast of Long Island, NY, United States of America (U.S.A.). Carbon (C), nitrogen (N), sulfur (S), Hg, and methylmercury (MeHg) were measured in surface sediments and the water column, and total Hg (THg) was measured in two species of forage fish. Minimal differences were found in dissolved and particulate Hg, dissolved organic carbon (DOC), and salinity between the two bays. Across lagoons, concentrations of chlorophyll-a were correlated with total suspended solids (TSS), and water column THg and MeHg was largely associated with the particulate fraction. Methylmercury concentrations in particulates decreased with increasing TSS and chlorophyll-a, evidence of biomass dilution of MeHg with increasing productivity at the base of the food chain. Water column Hg was associated with THg concentrations in Atlantic silversides, while mummichog THg concentrations were related to sediment concentrations, reflecting their different feeding strategies. Finally, higher nutrient loading (lower C:N in sediments) while related to lower particulate concentrations coincided with higher bioaccumulation factors (BAF) for Hg in both fish species. Thus, in shallow coastal lagoons, increased nutrient loading resulted in decreased Hg concentrations at the base of the food web but resulted in greater bioaccumulation of Hg to fish relative to its availability in algal food.

Preliminary investigation of polymer-based in situ passive samplers for mercury and methylmercury.

Development of an in situ passive sampler for mercury (Hg), and its toxic form, methylmercury (MeHg), using simple polymer films, was explored for the potential to make an efficient and environmentally relevant monitoring tool for this widespread aquatic pollutant. The sulfur-containing polymers polysulfone (PS), and polyphenylene sulfide (PPS), were found to accumulate both MeHg and inorganic Hg (iHg), whereas polyethylene (PE) sorbed iHg but not MeHg, and polyoxymethylene (POM) and polyethersulfone (PES) films had low affinity for both Hg species. Uptake rates of Hg species into polymers were linear over two weeks, and dissolved organic matter at natural levels had no effect on partitioning of MeHg or iHg to the polymers. Sorption of MeHg to PS and PPS from three estuarine sediments correlated with uptake into diffusive gel-type samplers over time, and in PPS, with accumulation by the estuarine amphipod, Leptocheirus plumulosus. These polymers had lower MeHg adsorption rates, but are simpler to assemble, than diffusive gel-type samplers. Higher contaminant concentrations in polymer and gel-type samplers corresponded with porewater concentrations across sediments, suggesting they sample the dissolved MeHg pool, whereas MeHg levels in amphipods were more elevated with higher bulk sediment MeHg, which may reflect feeding strategy. While polymers with higher affinity for MeHg and iHg are needed for some environmental applications, this work suggests a simple sampling approach has potential for time-integrated, environmentally-meaningful MeHg monitoring in contaminated sediments.

Effects of temperature, salinity, and sediment organic carbon on methylmercury bioaccumulation in an estuarine amphipod.

Mercury (Hg) is a global contaminant that poses a human health risk in its organic form, methylmercury (MeHg), through consumption of fish and fishery products. Bioaccumulation of Hg in the aquatic environment is controlled by a number of factors expected to be altered by climate change. We examined the individual and combined effects of temperature, sediment organic carbon, and salinity on the bioaccumulation of MeHg in an estuarine amphipod, Leptocheirus plumulosus, when exposed to sediment from two locations in the Gulf of Maine (Kittery and Bass Harbor) that contained different levels of MeHg and organic carbon. Higher temperatures and lower organic carbon levels individually increased uptake of MeHg by L. plumulosus as measured by the biota-sediment accumulation factor (BSAF), while the effect of salinity on BSAF differed by sediment source. Multi-factor statistical modeling using all data revealed a significant interaction between temperature and organic carbon for both sediments, in which increased temperature had a negative effect on BSAF at the lowest carbon levels and a positive effect at higher levels. Our results suggest that increased temperature and carbon loading, of a magnitude expected as a result from climate change, could be associated with a net decrease in amphipod BSAF of 50 to 71%, depending on sediment characteristics. While these are only first-order projections, our results indicate that the future fate of MeHg in marine food webs is likely to depend on a number of factors beyond Hg loading.

Mercury bioaccumulation increases with latitude in a coastal marine fish (Atlantic silverside, Menidia menidia).

Human exposure to the neurotoxic methylmercury (MeHg) occurs primarily via the consumption of marine fish, but the processes underlying large-scale spatial variations in fish MeHg concentrations [MeHg], which influence human exposure, are not sufficiently understood. We used the Atlantic silverside (Menidia menidia), an extensively studied model species and important forage fish, to examine latitudinal patterns in total Hg [Hg] and [MeHg]. Both [Hg] and [MeHg] significantly increased with latitude (0.014 and 0.048 µg MeHg g-1 dw per degree of latitude in juveniles and adults, respectively). Four known latitudinal trends in silverside traits help explain these patterns: latitudinal increase in MeHg assimilation efficiency, latitudinal decrease in MeHg efflux, latitudinal increase in weight loss due to longer and more severe winters, and latitudinal increase in food consumption as an adaptation to decreasing length of the growing season. Given the absence of a latitudinal pattern in particulate MeHg, a diet proxy for zooplanktivorous fish, we conclude that large-scale spatial variation in growth is the primary control of Hg bioaccumulation in this and potentially other fish species.

Influence of a chlor-alkali superfund site on mercury bioaccumulation in periphyton and low-trophic level fauna.

In Berlin, New Hampshire, USA, the Androscoggin River flows adjacent to a former chlor-alkali facility that is a US Environmental Protection Agency Superfund site and source of mercury (Hg) to the river. The present study was conducted to determine the fate and bioaccumulation of methylmercury (MeHg) to lower trophic-level taxa in the river. Surface sediment directly adjacent to the source showed significantly elevated MeHg (10-40× increase, mean ± standard deviation [SD]: 20.1 ± 24.8 ng g(-1) dry wt) and total mercury (THg; 10-30× increase, mean ± SD: 2045 ± 2669 ng g(-1) dry wt) compared with all other reaches, with sediment THg and MeHg from downstream reaches elevated (3-7× on average) relative to the reference (THg mean ± SD: 33.5 ± 9.33 ng g(-1) dry wt; MeHg mean ± SD: 0.52 ± 0.21 ng g(-1) dry wt). Water column THg concentrations adjacent to the point source for both particulate (0.23 ng L(-1)) and dissolved (0.76 ng L(-1)) fractions were 5-fold higher than at the reference sites, and 2-fold to 5-fold higher than downstream. Methylmercury production potential of periphyton material was highest (2-9 ng g(-1) d(-1) dry wt) adjacent to the Superfund site; other reaches were close to or below reporting limits (0. 1 ng g(-1) d(-1) dry wt). Total Hg and MeHg bioaccumulation in fauna was variable across sites and taxa, with no clear spatial patterns downstream of the contamination source. Crayfish, mayflies, and shiners showed a weak positive relationship with porewater MeHg concentration.

Experimental and natural warming elevates mercury concentrations in estuarine fish.

Marine food webs are the most important link between the global contaminant, methylmercury (MeHg), and human exposure through consumption of seafood. Warming temperatures may increase human exposure to MeHg, a potent neurotoxin, by increasing MeHg production as well as bioaccumulation and trophic transfer through marine food webs. Studies of the effects of temperature on MeHg bioaccumulation are rare and no study has specifically related temperature to MeHg fate by linking laboratory experiments with natural field manipulations in coastal ecosystems. We performed laboratory and field experiments on MeHg accumulation under varying temperature regimes using the killifish, Fundulus heteroclitus. Temperature treatments were established in salt pools on a coastal salt marsh using a natural temperature gradient where killifish fed on natural food sources. Temperatures were manipulated across a wider range in laboratory experiments with killifish exposed to MeHg enriched food. In both laboratory microcosms and field mesocosms, MeHg concentrations in killifish significantly increased at elevated temperatures. Moreover, in field experiments, other ancillary variables (salinity, MeHg in sediment, etc.) did not relate to MeHg bioaccumulation. Modeling of laboratory experimental results suggested increases in metabolic rate as a driving factor. The elevated temperatures we tested are consistent with predicted trends in climate warming, and indicate that in the absence of confounding factors, warmer sea surface temperatures could result in greater in bioaccumulation of MeHg in fish, and consequently, increased human exposure.