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.

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.

Transport of mercury on the finest particles results in high sediment concentrations in the absence of significant ongoing sources.

The mercury contaminated upper Penobscot Estuary in Maine provided a unique opportunity to rigorously examine the effect of sediment type and particle size on mercury concentrations in sediments, and to explain why sediments at different locations in the estuary had different mercury concentrations. This is because the Penobscot Estuary contains a large, well-mixed pool of mobile sediments of many different types (muds, sand, gravel, wood chips), which are the source of material for the permanently deposited surface sediments. Despite this mixing, average surface sediment mercury concentrations were very different in different locations, ranging from 238 ng/gdw to 1032 ng/gdw in the 11 subareas studied. Average total mercury concentrations were highly related to the type of sediment (wood chips > muds > sands) regardless of location in the estuary. The characteristics in both mobile and surface sediments that were positively related to total mercury concentrations were % organic matter (measured as loss on ignition) and %fines (measured usually as <62.5 µ). Also, in a subset of samples it was shown that mercury was positively associated only with the very finest (<44 µ) particles. Thus, side embayments of the estuary such as the Orland River and Mendall Marsh, which experience lower velocity currents and so accumulate more fine particles, tended to be much higher in mercury concentrations. This knowledge will be important in managing remediation of this system, as fine particles can be the most difficult to trap or to retain if dredging is employed. Methyl mercury was well correlated with total mercury and so its distribution would also be affected by transport characteristics. This was the case even in the mobile sediments, which were more oxic and not expected to provide a good habitat for methylation.

Investigation of uptake and retention of atmospheric Hg(II) by boreal forest plants using stable Hg isotopes.

Although there is now a general consensus among mercury (Hg) biogeochemists that increased atmospheric inputs of inorganic Hg(II) to lakes and watersheds can result in increased methylmercury (MeHg) concentrations in fish, researchers still lack kinetic data describing the movement of Hg from the atmosphere, through watershed and lake ecosystems, and into fish. The use of isotopically enriched Hg species in environmental studies now allows experimentally applied new Hg to be distinguished from ambient Hg naturally present in the system. Four different enriched stable Hg(II) isotope "spikes" were applied sequentially over four years to the ground vegetation of a microcatchment at the Experimental Lakes Area (ELA) in the remote boreal forest of Canada to examine retention of Hg(II) following deposition. Areal masses of the spikes and ambient THg (all forms of Hg in a sample) were monitored for eight years, and the pattern of spike retention was used to estimate retention of newly deposited ambient Hg within the ground vegetation pool. Fifty to eighty percent of applied spike Hg was initially retained by ground vegetation. The areal mass of spike Hg declined exponentially over time and was best described by a first-order process with constants(k) ranging between 9.7 x 10(-40 day(-1) and 11.6 x 10(-4) day(-1). Average halflife (t1/2) of spike Hg within the ground vegetation pool (+/-S.D.) was 704 +/- 52 days. This retention of new atmospheric Hg(II) by vegetation delays movement of new Hg(II) into soil, runoff, and finally into adjacent lakes. Ground-applied Hg(II) spikes were not detected in tree foliage and litterfall, indicating that stomatal and/or root uptake of previously deposited Hg (i.e., "recycled" from ground vegetation or soil Hg pools) were likely not large sources of foliar Hg under these experimental conditions.

Long-term wet and dry deposition of total and methyl mercury in the remote boreal ecoregion of Canada.

Although a positive relationship between atmospheric loadings of inorganic mercury (Hg(II)) to watersheds and concentrations of methyl mercury (MeHg) in fish has now been established, net wet and dry deposition of Hg(II) and MeHg to watersheds remains challenging to quantify. In this study, concentrations and loadings of total mercury (THg; all forms of Hg in a sample) and MeHg in open area wet deposition, throughfall, and litterfall were quantified atthe remote Experimental Lakes Area in the boreal ecoregion, NW Ontario, Canada. Between 1992 and 2006, mean annual THg and MeHg loadings in the open were 36 +/- 17 and 0.5 +/- 0.2 mg ha(-1), respectively. Throughfall THg and MeHg loadings were generally 2-4 times and 0.8-2 times higher, respectively, than loadings in the open. Loadings of both THg and MeHg were highest under an old growth spruce/fir canopy and lowest under a deciduous maple canopy, whereas loadings under young jack pine and wetland spruce/pine/alder canopies were intermediate. Litterfall generally represented the largest input of THg (86-105 mg ha(-1)) and MeHg (0.7-0.8 mg ha(-1)) to the landscape on an annual basis. Using the "direct" method of estimating dry deposition (thoughfall + litterfall - open loadings), we calculated that annual dry deposition of THg and MeHg under forest canopies ranged from 105 to 201 mg ha(-1), whereas dry deposition of MeHg ranged from 0.7 to 1.2 mg ha(-1). Photoreduction and emission of wet-deposited Hg(ll) from canopy foliage were accounted for, resulting in 3-5% (5-6 mg ha(-1)) higher annual estimates of dry deposition than via the direct method alone. NetTHg and MeHg loadings to this remote landscape were lower than at any other previously studied forested site globally. This study shows that THg and MeHg loading can be extremely variable within a heterogeneous boreal landscape and that processes such as Hg photoreduction and emission from foliage should be considered when estimating dry deposition of Hg.

Whole-ecosystem study shows rapid fish-mercury response to changes in mercury deposition.

Methylmercury contamination of fisheries from centuries of industrial atmospheric emissions negatively impacts humans and wildlife worldwide. The response of fish methylmercury concentrations to changes in mercury deposition has been difficult to establish because sediments/soils contain large pools of historical contamination, and many factors in addition to deposition affect fish mercury. To test directly the response of fish contamination to changing mercury deposition, we conducted a whole-ecosystem experiment, increasing the mercury load to a lake and its watershed by the addition of enriched stable mercury isotopes. The isotopes allowed us to distinguish between experimentally applied mercury and mercury already present in the ecosystem and to examine bioaccumulation of mercury deposited to different parts of the watershed. Fish methylmercury concentrations responded rapidly to changes in mercury deposition over the first 3 years of study. Essentially all of the increase in fish methylmercury concentrations came from mercury deposited directly to the lake surface. In contrast, <1% of the mercury isotope deposited to the watershed was exported to the lake. Steady state was not reached within 3 years. Lake mercury isotope concentrations were still rising in lake biota, and watershed mercury isotope exports to the lake were increasing slowly. Therefore, we predict that mercury emissions reductions will yield rapid (years) reductions in fish methylmercury concentrations and will yield concomitant reductions in risk. However, a full response will be delayed by the gradual export of mercury stored in watersheds. The rate of response will vary among lakes depending on the relative surface areas of water and watershed.

Effect of loading rate on the fate of mercury in littoral mesocosms.

The effects of changes in atmospheric mercury (Hg) deposition on aquatic ecosystems are poorly understood. In this study, we examined the biogeochemical cycling of Hg in littoral mesocosms receiving different loading rates (7-107 microg Hg m(-2) year(-1)). We added a 202Hg-enriched preparation to differentiate the experimentally added Hg from the ambient Hg in the environment. This approach allowed us to follow the distribution and methylation of the isotopically enriched ("spike") Hg in the mesocosms. Within 3 weeks, spike Hg was distributed throughout the main environmental compartments (water, particles, periphyton, and sediments) and began to be converted to methylmercury (MeHg). Concentrations of spike total Hg and MeHg in these compartments, measured after 8 weeks, were directly proportional to loading rates. Thus, Hg(II) availability was the limiting factor for the major processes of the biogeochemical Hg cycle, including methylation. This is the first study to demonstrate a proportional response of in situ MeHg production to atmospherically relevant loading levels. On the basis of mass balances, we conclude that loading rate had no effect on the relative distribution of spike Hg among the main compartments or on the fraction of spike Hg converted to MeHg. Therefore, loading rate did not change the relative magnitude of biogeochemical pathways competing for Hg within the mesocosms. These data suggest that reductions of Hg deposition to lake surfaces would be equally effective across a broad range of deposition rates.

The rise and fall of mercury methylation in an experimental reservoir.

For the past 9 years, we experimentally flooded a wetland complex (peatland surrounding an open water pond) at the Experimental Lakes Area (ELA), northwestern Ontario, Canada, to examine the biogeochemical cycling of methyl mercury (MeHg) in reservoirs. Using input-output budgets, we found that prior to flooding, the wetland complex was a net source of approximately 1.7 mg MeHg ha(-1) yr(-1) to downstream ecosystems. In the first year of flooding, net yields of MeHg from the reservoir increased 40-fold to approximately 70 mg MeHg ha(-1) yr(-1). Subsequently, annual net yields of MeHg from the reservoir declined (10-50 mg MeHg ha(-1) yr(-1)) but have remained well above natural levels. The magnitude and timing of Hg methylation in the flooded peat portion of the wetland reservoir were very different than in the open water region of the reservoir. In terms of magnitude, net Hg methylation rates in the peat in the first 2 years of flooding were 2700 mg ha(-1) yr(-1), constituting over 97% of the MeHg produced at the whole-ecosystem level. But in the following 3 years, there was a large decrease in the mass of MeHg in the flooded peat due to microbial demethylation. In contrast, concentrations of MeHg in the open water region and in zooplankton, and body burdens of Hg in cyprinid fish, remained high for the full 9 years of this study. Microbial activity in the open water region also remained high, as evidenced by continued high concentrations of dissolved CO2 and CH4. Thus, the large short-term accumulation of MeHg mass in the peat appeared to have only a small influence on concentrations of MeHg in the biota; rather MeHg accumulation in biota was sustained by the comparatively small ongoing net methylation of Hg in the flooded pond where microbial activity remained high. In large reservoirs, where the effects of wind and fetch are greater than in the small experimental reservoir we constructed, differences can occur in the timing and extent of peat and soil erosion, effecting either transport of MeHg to the food chain or the fueling of microbial activity in open water sediments, both of which could have important long-term implications for MeHg concentrations in predatory fish.

Effect of pH on mercury uptake by an aquatic bacterium: implications for Hg cycling.

We studied the effect of increasing hydrogen ion (H+) concentration on the uptake of mercury (Hg(II)) by an aquatic bacterium. Even small changes in pH (7.3-6.3) resulted in large increases in Hg(II) uptake, in defined media. The increased rate of bioaccumulation was directly proportional to the concentration of H+ and could not be explained by assuming that the source of Hg to the bacteria was diffusion of neutrally charged species such as HgCl2. Thus, pH appeared to affect a facilitated mechanism by which Hg(II) is taken up by the cells. Lowering the pH of Hg solutions mixed together with natural dissolved organic carbon, or with whole lake water, also increased bacterial uptake of Hg(II). These findings have several potential implications for mercury cycling, including effects on elemental mercury production, mercury sedimentation, and microbial methylation of Hg(II), and could be part of the explanation for the observed positive correlation between lake acidity and methyl mercury levels in fish.

Reactivity and mobility of new and old mercury deposition in a boreal forest ecosystem during the first year of the METAALICUS study. Mercury Experiment To Assess Atmospheric Loading In Canada and the US.

The METAALICUS (Mercury Experiment To Assess Atmospheric Loading In Canada and the US) project is a whole ecosystem experiment designed to study the activity, mobility, and availability of atmospherically deposited mercury. To investigate the dynamics of mercury newly deposited onto a terrestrial ecosystem, an enriched stable isotope of mercury (202Hg) was sprayed onto a Boreal forest subcatchment in an experiment that allowed us, for the first time, to monitor the fate of 'new' mercury in deposition and to distinguish it from native mercury historically stored in the ecosystem. Newly deposited mercury was more reactive than the native mercury with respect to volatilization and methylation pathways. Mobility through runoff was very low and strongly decreased with time because of a rapid equilibration with the large native pool of "bound" mercury. Over one season, only approximately 8% of the added 212Hg volatilized to the atmosphere and less than 1% appeared in runoff. Within a few months, approximately 66% of the applied 202Hg remained associated with above ground vegetation, with the rest being incorporated into soils. The fraction of 202Hg bound to vegetation was much higher than seen for native Hg (<5% vegetation), suggesting that atmospherically derived mercury enters the soil pool with a time delay, after plants senesce and decompose. The initial mobility of mercury received through small rain events or dry deposition decreased markedly in a relatively short time period, suggesting that mercury levels in terrestrial runoff may respond slowly to changes in mercury deposition rates.