Experimental evidence for recovery of mercury-contaminated fish populations.

Anthropogenic releases of mercury (Hg)1-3 are a human health issue4 because the potent toxicant methylmercury (MeHg), formed primarily by microbial methylation of inorganic Hg in aquatic ecosystems, bioaccumulates to high concentrations in fish consumed by humans5,6. Predicting the efficacy of Hg pollution controls on fish MeHg concentrations is complex because many factors influence the production and bioaccumulation of MeHg7-9. Here we conducted a 15-year whole-ecosystem, single-factor experiment to determine the magnitude and timing of reductions in fish MeHg concentrations following reductions in Hg additions to a boreal lake and its watershed. During the seven-year addition phase, we applied enriched Hg isotopes to increase local Hg wet deposition rates fivefold. The Hg isotopes became increasingly incorporated into the food web as MeHg, predominantly from additions to the lake because most of those in the watershed remained there. Thereafter, isotopic additions were stopped, resulting in an approximately 100% reduction in Hg loading to the lake. The concentration of labelled MeHg quickly decreased by up to 91% in lower trophic level organisms, initiating rapid decreases of 38-76% of MeHg concentration in large-bodied fish populations in eight years. Although Hg loading from watersheds may not decline in step with lowering deposition rates, this experiment clearly demonstrates that any reduction in Hg loadings to lakes, whether from direct deposition or runoff, will have immediate benefits to fish consumers.

Low-level experimental selenite additions decrease mercury in aquatic food chains and fish muscle but increase selenium in fish gonads.

We investigated whether low-level addition of selenium (Se) could decrease mercury (Hg) in freshwater fish without imposing Se toxicity. Using a regression design, selenite was added to large mesocosms in a lake to achieve target concentrations ≤1.6 µg/L. (198)Hg (spike Hg) was added to mesocosms to determine changes in Hg bioaccumulation. Adding Se decreased spike total Hg (THg) in fish muscle, ambient THg in fish liver, and bioaccumulation of spike THg in muscle and spike methylmercury (MeHg) in zooplankton and Chironomid larvae relative to controls. Se decreased Hg in the food web but not in water, indicating that the dominant effect of Se on Hg cycling occurs in the food web. Concentrations of Se in gonads of fish were positively correlated with Se concentrations in water but did not exceed reproductive toxicity thresholds after 8 weeks. We conclude that low-level addition of Se decreases MeHg bioaccumulation and increases Se in gonads of fish; however, additions of Se to freshwater systems to decrease Hg in fish should be treated with caution because Se in fish gonads were likely to exceed toxic concentrations if exposed to increased Se for a longer period of time.

Ecological risk of methylmercury to piscivorous fish of the Great Lakes region.

Contamination of fish populations with methylmercury is common in the region of the Laurentian Great Lakes as a result of atmospheric deposition and methylation of inorganic mercury. Using fish mercury monitoring data from natural resource agencies and information on tissue concentrations injurious to fish, we conducted a screening-level risk assessment of mercury to sexually mature female walleye (Sander vitreus), northern pike (Esox lucius), smallmouth bass (Micropterus dolomieu), and largemouth bass (Micropterus salmoides) in the Great Lakes and in interior lakes, impoundments, and rivers of the Great Lakes region. The assessment included more than 43,000 measurements of mercury in fish from more than 2000 locations. Sexually mature female fish that exceeded threshold-effect tissue concentrations of 0.20 µg g(-1) wet weight in the whole body occurred at 8% (largemouth bass) to 43% (walleye) of sites. Fish at 3% to 18% of sites were at risk of injury and exceeded 0.30 µg g(-1) where an alteration in reproduction or survival is predicted to occur. Most fish at increased risk were from interior lakes and impoundments. In the Great Lakes, no sites had sexually mature fish that exceeded threshold-effect concentrations. Results of this screening-level assessment indicate that fish at a substantive number of locations within the Great Lakes region are potentially at risk from methylmercury contamination and would benefit from reduction in mercury concentrations.

Mercury in the Great Lakes region: bioaccumulation, spatiotemporal patterns, ecological risks, and policy.

This special issue examines bioaccumulation and risks of methylmercury in food webs, fish and wildlife in the Laurentian Great Lakes region of North America, and explores mercury policy in the region and elsewhere in the United States and Canada. A total of 35 papers emanated from a bi-national synthesis of multi-media data from monitoring programs and research investigations on mercury in aquatic and terrestrial biota, a 3-year effort involving more than 170 scientists and decision-makers from 55 different universities, non-governmental organizations, and governmental agencies. Over 290,000 fish mercury data points were compiled from monitoring programs and research investigations. The findings from this scientific synthesis indicate that (1) mercury remains a pollutant of major concern in the Great Lakes region, (2) that the scope and intensity of the problem is greater than previously recognized and (3) that after decades of declining mercury levels in fish and wildlife concentrations are now increasing in some species and areas. While the reasons behind these shifting trends require further study, they also underscore the need to identify information gaps and expand monitoring efforts to better track progress. This will be particularly important as new pollution prevention measures are implemented, as global sources increase, and as the region faces changing environmental conditions.

Spatial and temporal trends of mercury in the aquatic food web of the lower Penobscot River, Maine, USA, affected by a chlor-alkali plant.

Mercury (Hg) concentrations in aquatic biota, including fish and shellfish, were measured over the period 2006-2012 in the lower Penobscot River and upper estuary (Maine, USA). The Penobscot is a system contaminated with Hg by a chlor-alkali plant that operated from 1967 to 2000, discharging 6-12 tons of mercury into the river. Mercury levels in aquatic biota were highest at sites downstream of the chlor-alkali plant and spatial trends were similar to those of sediments. Mean total Hg concentrations in fish muscle (adjusted for size or age) in the most affected areas were 521 (480, 566; 95% CI) ng/g ww in American eels, 321 (261,395) in mummichog, 121 (104, 140) in rainbow smelt, 155 (142,169) in tomcod, 55.2 (42.7,71.4) in winter flounder, and 328 (259,413) in American lobster tail and 522 (488,557) ng/g dw in blue mussel. Levels exceeded the 50 ng/g ww considered protective for piscivorous predators and were of concern for human health, with American eels and American lobster exceeding Maine's mercury action level of 200 ng/g ww. Calculations of trophic position (using nitrogen isotopes) suggested that the spatial patterns observed in total Hg concentrations were not due to changes in feeding habits of the species. Fish feeding in benthic food webs, as defined by stomach content and stable carbon isotope analyses, showed no change in Hg concentrations over time. In contrast, declining trends in Hg were found in two species dependent on pelagic food webs. The absence of declines in Hg concentrations in the benthically-based food webs, despite the fact that most Hg was discharged into the system >40 years ago, is consistent with the long recovery predicted from dated sediment cores and from similar studies elsewhere.

Temporal changes in the distribution, methylation, and bioaccumulation of newly deposited mercury in an aquatic ecosystem.

Our objective was to examine how the behavior of atmospheric mercury (Hg) deposited to boreal lake mesocosms changed over time. We added inorganic Hg enriched in a different stable isotope in each of two years, which allowed us to differentiate between Hg added in the first and second year. Although inorganic Hg and methylmercury (MeHg) continued to accumulate in sediments throughout the experiment, the availability of MeHg to the food web declined within one year. This decrease was detected in periphyton, zooplankton, and water mites, but not in gomphid larvae, amphipods, or fish. We suggest that reductions in atmospheric Hg deposition should lead to decreases in MeHg concentrations in biota, but that changes will be more easily detected in short-lived pelagic species than long-lived species associated with benthic food webs.

Tidal fluxes of mercury and methylmercury for Mendall Marsh, Penobscot River estuary, Maine.

Tidal marshes are both important sites of in situ methylmercury production and can be landscape sources of methylmercury to adjacent estuarine systems. As part of a regional investigation of the Hg-contaminated Penobscot River and Bay system, the tidal fluxes of total suspended solids, total mercury and methylmercury into and out of a regionally important mesohaline fluvial marsh complex, Mendall Marsh, were intensively measured over several tidal cycles and at two spatial scales to assess the source-sink function of the marsh with respect to the Penobscot River. Over four tidal cycles on the South Marsh River, the main channel through which water enters and exits Mendall Marsh, the marsh was a consistent sink over typical 12-h tidal cycles for total suspended solids (8.2 to 41 g m-2), total Hg (9.2 to 47 µg m-2), total filter-passing Hg (0.4 to 1.1 µg m-2), and total methylmercury (0.2 to 1.4 µg m-2). The marsh's source-sink function was variable for filter-passing methylmercury, acting as a net source during a large spring tide that inundated much of the marsh area and that is likely to occur during approximately 17% of tidal cycles. Additional measurements on a small tidal channel draining approximately 1% of the larger marsh area supported findings at the larger scale, but differences in the flux magnitude of filter-passing fractions suggest a highly non-conservative transport of these fractions through the tidal channels. Overall the results of this investigation demonstrate that Mendall Marsh is not a significant source of mercury or methylmercury to the receiving aquatic systems (Penobscot River and Bay). While there is evidence of a small net export of filter-passing (<0.4 µm pore size) methylmercury under some tidal conditions, the mass involved represents <3% of the mass of filter-passing methylmercury carried by the Penobscot River.

Elevated mercury in blood and feathers of breeding marsh birds along the contaminated lower Penobscot River, Maine, USA.

Mercury (Hg) concentrations in the blood and feathers of five species of migratory marsh birds, Nelson's sparrow (Ammodramus nelson subvirgatus), song sparrow (Melospiiza melodia), swamp sparrow (Melospiza geogiana), red-winged blackbird (Agelaius phoeniceus), and Virginia rail (Rallus limicola), breeding in marshes along the lower Penobscot River, Maine, far exceeded reference concentrations, exceeded concentrations associated with reproductive health, and are the highest Hg concentrations reported to date for several species. Blood Hg concentrations in adult Nelson's sparrows were greatest in 2007, at 6.6µg/gww (geometric mean) and in 2012, at 6.5µg/gww and greatest in red-winged blackbirds in 2012, 8.0µg/gww. Mercury in blood increased with residence time on the contaminated marshes at an estimated rate of 0.04 to 0.07µg/gww per day. Feather mercury concentrations in specific primary, secondary and tail feathers (P1, S2, R6) were strongly associated with exposure location at the time of feather formation. Geometric mean Hg concentrations in primary feathers (P1) reached 39.6µg/gfw in 2010 in Nelson's sparrows. The paper documents the dynamic nature of Hg concentrations in avian blood and feathers, an important consideration in contaminant study design, and the increased risk to marsh birds posed by Hg deposition from upstream sources.

Fifty years after its discharge, methylation of legacy mercury trapped in the Penobscot Estuary sustains high mercury in biota.

Fifty years ago, the Penobscot Estuary was contaminated by mercury discharged from the chlor-alkali plant located in Orrington, Maine, USA. Almost all of the mercury was discharged from the plant during the late 1960s and early 1970s. Despite the much lower mercury discharges in recent decades, present-day concentrations in surface sediment remain high (averaging 350-1100 ng/g dw) and are still high in blood of marsh birds (up to 10.5 µg/g), black duck muscle (0.8 µg/g), and lobster muscle (0.4 µg/g). Methyl mercury (MeHg) concentrations in marsh birds exceed levels that impair reproduction. There are health advisories for duck hunters and closures of shellfish fisheries. These continuing high mercury concentrations are caused by the trapping of legacy mercury in a mobile pool of sediment that is retained in the upper estuary above a tidally forced salinity front, which travels up and down the estuary each tidal cycle - slowing the transport of particulate mercury to Penobscot Bay. The trapped legacy mercury continues to be available for methylation 50 years after it first entered the estuary. This is demonstrated by the fact that rates of MeHg production are positively related to the inorganic mercury concentration in parts of the estuary with elevated concentrations of legacy mercury. Thus, remediation measures that would lower the THg concentration in surface sediment would lower the MeHg in birds, fish and shellfish. All of this new information leads us to recommend two remediation options. Addition of mercury binding agents may lower mercury concentrations in birds in some wetland areas. System-wide, we also recommend Enhanced Natural Recovery (ENR), a novel approach that involves the partial removal of the contaminated mobile sediment pool followed by replacement with clean-clay particulates to dilute inorganic mercury concentrations, which would lower methylation rates and mercury concentrations in biota.

Distribution and biogeochemical controls on net methylmercury production in Penobscot River marshes and sediment.

The distribution of mercury and methylmercury (MeHg) in sediment, mudflats, and marsh soils of the Hg-contaminated tidal Penobscot River was investigated, along with biogeochemical controls on production. Average total Hg in surface samples (0-3 cm) ranged from 100 to 1200 ng/g; average MeHg ranged from 5 to 50 ng/g. MeHg was usually highest at or near the surface except in highly mobile mudflats. Although total Hg concentrations in the Penobscot are elevated, it is the accumulation of MeHg that stands out in comparison to other ecosystems. Surface soils in the large Mendall Marsh, about 17 km downstream from the contamination source, contained particularly high %MeHg (averaging 8%). In Mendall marsh soil porewaters, MeHg often accounted for more than half of total Hg. Salt marshes are areas of particular concern in the Penobscot River, for they are depositional environments for a Hg-contaminated mobile pool of river sediment, hot spots for net MeHg production, and sources of risk to marsh animals. We hypothesized that exceptionally low mercury partitioning between the solid and aqueous phases (with log Kd averaging ~4.5) drives high MeHg in Penobscot marshes. The co-occurrence of iron and sulfide in filtered soil porewaters, sometimes both above 100 µM, suggests the presence of nanoparticulate and/or colloidal metal sulfides. These colloids may be stabilized by high concentrations of aromatic and potentially sulfurized dissolved organic matter (DOM) in marsh soils. Thus, Hg in Penobscot marsh soils appears to be in a highly available for microbial methylation through the formation of DOM-associated HgS complexes. Additionally, low partitioning of MeHg to marsh soils suggests high MeHg bioavailability to animals. Overall, drivers of high MeHg in Penobscot marshes include elevated Hg in soils, low partitioning of Hg to solids, high Hg bioavailability for methylation, rapidly shifting redox conditions in surface marsh soils, and high rates of microbial activity.

Mercury concentrations in bald eagles across an impacted watershed in Maine, USA.

Mercury (Hg) exposure was evaluated in bald eagles (Haliaeetus leucocephalus) in the lower Penobscot River watershed (PRW) in Maine to assess whether Hg discharges from a chlor-alkali plant (HoltraChem) influenced Hg concentrations in nestling tissues. Mean Hg concentrations in nestling blood and breast feathers sampled in marine and estuarine areas potentially contaminated with Hg from HoltraChem (the potential Hg impact zone) were significantly greater than those from reference sites spanning the Maine coast. To place Hg exposure in the potential Hg impact zone into a broader context, Hg exposure in bald eagle nestlings from four habitat types in the PRW was assessed. Mercury concentrations varied significantly across habitat types within the PRW, generally following the pattern: marine=estuarine

Recovery of mercury-contaminated fisheries.

In this paper, we synthesize available information on the links between changes in ecosystem loading of inorganic mercury (Hg) and levels of methylmercury (MeHg) in fish. Although it is widely hypothesized that increased Hg load to aquatic ecosystems leads to increases in MeHg in fish, there is limited quantitative data to test this hypothesis. Here we examine the available evidence from a range of sources: studies of ecosystems contaminated by industrial discharges, observations of fish MeHg responses to changes in atmospheric load, studies over space and environmental gradients, and experimental manipulations. A summary of the current understanding of the main processes involved in the transport and transformation from Hg load to MeHg in fish is provided. The role of Hg loading is discussed in context with other factors affecting Hg cycling and bioaccumulation in relation to timing and magnitude of response in fish MeHg. The main conclusion drawn is that changes in Hg loading (increase or decrease) will yield a response in fish MeHg but that the timing and magnitude of the response will vary depending of ecosystem-specific variables and the form of the Hg loaded.

The burning question: does burning before flooding lower methyl mercury production and bioaccumulation?

Production of methyl mercury (MeHg) is elevated in new hydroelectric reservoirs because organic carbon stimulates methylation of inorganic mercury (Hg) stored in the terrestrial system. This can cause adverse health in fish and in organisms that eat fish. We expected that burning vegetation before flooding would decrease the amount of Hg and organic carbon and thereby lower MeHg production. We conducted a replicated field experiment to investigate the effects of burning vegetation and soil before flooding on MeHg production and bioaccumulation. Vegetation and soil were added to mesocosms in the following combinations: unburned vegetation and unburned soil (Fresh treatments), burned vegetation and unburned soil (Partial Burn treatments), and burned vegetation and burned soil (Complete Burn treatments). Controls had no added vegetation or soil. During combustion with propane torches, a large percentage of the total Hg (THg) and MeHg was lost from vegetation and soil. THg and MeHg concentrations were highest in the surface water of Fresh treatments, lower in Partial Burn treatments and lowest in Complete Burn treatments and controls. Differences in concentrations of MeHg in biota were consistent among treatments, but did not follow aqueous concentrations. On the final sample date, MeHg concentrations in biota of Controls and Partial Burn treatments were greater than in Complete Burn and Fresh treatments. The lack of relationship between MeHg in biota and MeHg in water may have been due to modification of the bioavailability of MeHg by dissolved organic matter as the ratios of MeHg in biota to water were inversely correlated with concentrations of dissolved organic carbon. Although burning before flooding decreased MeHg concentrations in the water, it did not lower MeHg accumulation in the lower food web.

Strategies to lower methyl mercury concentrations in hydroelectric reservoirs and lakes: A review.

Mercury (Hg) concentrations in fish in lakes are elevated due to increased global cycling of Hg. A special case of elevated Hg concentrations in fish occurs in new hydroelectric reservoirs because of increased rates of converting Hg in the environment into methyl mercury (MeHg). People and wildlife that eat fish from hydroelectric reservoirs have an elevated risk of accumulating too much MeHg. Demand for electrical energy is leading to the creation of new reservoirs. In 2005, Canada derived 60% of its electricity from hydroelectric reservoirs. As a result, hydroelectric companies and governing agencies are exploring strategies to lower MeHg contamination. Strategies may involve lowering the source of Hg before flooding, the rate of Hg methylation, or MeHg bioaccumulation and biomagnification. Possible strategies reviewed in this article include selecting a site to minimize impacts, intensive fishing, adding selenium, adding lime to acidic systems, burning before flooding, removing standing trees, adding phosphorus, demethylating MeHg by ultraviolet light, capping and dredging bottom sediment, aerating anoxic bottom sediment and waters, and water level management. A preventative strategy is to limit the flooded area, especially wetland areas. Flooded upland areas that contain less carbon produce MeHg for a shorter time than wetland areas. Run-of-the-river reservoirs contain lower MeHg concentrations than reservoirs that flood vast areas, at the cost of exporting MeHg downstream. Managing water levels to flush systems during times of peak MeHg production may have benefits for the reservoir, but also transports MeHg downstream. Intensive fishing can lower MeHg in food webs by increasing fish growth rate. Additions of selenium can lower MeHg bioaccumulation, but the mechanisms are not well established and excess selenium causes toxicity. Liming can lower fish Hg concentrations in lakes acidified with sulphuric and nitric acid. Burning before flooding can lower the production of MeHg, but MeHg bioaccumulation may increase. The most promising strategy will be one that is agreeable to all affected people.

Total mercury, methyl mercury, and carbon in fresh and burned plants and soil in Northwestern Ontario.

Terrestrial plants and soil contain substantial amounts of organic carbon (C) and mercury. Flooding terrestrial areas stimulates microbial methyl mercury (MeHg) production and fish obtain elevated MeHg concentrations. Our purpose was to determine the loss of C, total mercury (THg), and MeHg from boreal plants and soil after burning to assess the potential of burning before flooding to lower MeHg. Fresh plants contained 4 to 52 ng g(-1) dry weight (dw) of THg and 0.1 to 1.3 ng g(-1) dw of MeHg. Upland soils contained 162+/-132 ng g(-1) dw of THg and 0.6+/-0.6 ng g(-1) dw of MeHg. Complete burning caused plants to lose 96, 98, 97, and 94% of the mass, C, THg, and MeHg, respectively. Upland soil lost 27, 95, 79, and 82% of the mass, C, THg, and MeHg, respectively. Our results demonstrated that a substantial loss of C, THg, and MeHg was caused by burning.

Mercury transfer from fish carcasses to scavengers in boreal lakes: the use of stable isotopes of mercury.

Scavengers play an important role in the flow of energy, matter and pollutants through food webs. For methylmercury (MeHg), which biomagnifies along food chains, the movement of this metal from fish carcasses to aquatic scavengers has never been demonstrated. We measured the transfer of MeHg from fish carcasses to scavenging leeches in two lakes and in the laboratory. The results of a field experiment indicated that leeches were attracted to fish carcasses and that their Hg concentrations increased by as much as a factor of 5 during the time that Hg-rich fish were available for consumption. Under controlled conditions, we exposed leeches to (202)Hg-labelled fish that had been marked in situ following a whole lake (202)Hg addition. Leeches rapidly accumulated Hg from carcasses, and within two weeks assumed the isotopic signature of the carcasses. Necrophagous invertebrates could therefore return Hg from fish carcasses to other trophic levels in lakes.

Intra- and interpopulation variability in maternal transfer of mercury to eggs of walleye (Stizostedion vitreum).

Mercury concentrations were determined for unfertilized eggs from seven walleye populations and for muscle and liver tissue from three of these seven populations in Canada and the United States. Female walleye transferred very little of their body methylmercury burden to their eggs. Methylmercury concentrations in eggs were 1.1-12% of those in muscle, and methylmercury burdens in eggs represented only 0.2-2.1% of the total body burden. Egg methylmercury as a percentage of total mercury increased with maternal length across populations. Percent methylmercury also increased with egg total mercury concentration but the slope of this relationship varied among populations. Egg methylmercury concentration increased with female age, and both muscle and liver methylmercury concentrations. Egg methylmercury concentration was also affected by female length at age but the effect of this relationship varied among populations. Mean predicted egg methylmercury concentrations (ng g(-1) dry) of 8-year-old, 550-mm females for the seven populations were as follows: Clay Lake, 796; Lake Superior, 24.3; Lake Winnipeg, 16.3; Lake Erie, 11.8; Primrose Lake, 8.76; Lake Manitoba, 7.32; Waconda Lake, 6.69.

Effects of environmental and maternally derived methylmercury on the embryonic and larval stages of walleye (Stizostedion vitreum).

The effects of environmental and maternally derived methylmercury (MeHg) on the embryonic and larval stages of walleye (Stizostedion vitreum) were investigated using eggs collected during two successive spawning seasons. Eggs were collected from fish in a mercury (Hg)-polluted environment (Clay Lake, Ontario, Canada), and from fish in two relatively pristine lakes (Lakes Manitoba and Winnipeg, in the province of Manitoba). Both bioaccumulation of Hg into muscle and its mobilization into eggs was significantly higher in Clay Lake females. Maternal muscle MeHg concentration was positively correlated with female length and egg MeHg was positively correlated with muscle MeHg concentration in all three populations. Hatching success of eggs from all three stocks declined significantly with increasing waterborne MeHg (0.1-7.8 ng l-1). Hatching success was not significantly affected by egg MeHg concentration. Embryonic heart rate declined with increasing waterborne MeHg concentration, but larval growth was not affected. Occurrence of larval deformities was negatively correlated with size of female, but was not significantly correlated with MeHg in either eggs or water. Larval MeHg was positively correlated with the concentrations of MeHg in eggs demonstrating transmission of MeHg from females. Uptake of ambient MeHg was higher in larvae exposed to higher waterborne MeHg concentrations.