Elsevier

Environmental Research

Volume 119, November 2012, Pages 101-117
Environmental Research

Mercury biogeochemical cycling in the ocean and policy implications

https://doi.org/10.1016/j.envres.2012.03.013Get rights and content

Abstract

Anthropogenic activities have enriched mercury in the biosphere by at least a factor of three, leading to increases in total mercury (Hg) in the surface ocean. However, the impacts on ocean fish and associated trends in human exposure as a result of such changes are less clear. Here we review our understanding of global mass budgets for both inorganic and methylated Hg species in ocean seawater. We consider external inputs from atmospheric deposition and rivers as well as internal production of monomethylmercury (CH3Hg) and dimethylmercury ((CH3)2Hg). Impacts of large-scale ocean circulation and vertical transport processes on Hg distribution throughout the water column and how this influences bioaccumulation into ocean food chains are also discussed. Our analysis suggests that while atmospheric deposition is the main source of inorganic Hg to open ocean systems, most of the CH3Hg accumulating in ocean fish is derived from in situ production within the upper waters (<1000 m). An analysis of the available data suggests that concentrations in the various ocean basins are changing at different rates due to differences in atmospheric loading and that the deeper waters of the oceans are responding slowly to changes in atmospheric Hg inputs. Most biological exposures occur in the upper ocean and therefore should respond over years to decades to changes in atmospheric mercury inputs achieved by regulatory control strategies. Migratory pelagic fish such as tuna and swordfish are an important component of CH3Hg exposure for many human populations and therefore any reduction in anthropogenic releases of Hg and associated deposition to the ocean will result in a decline in human exposure and risk.

Introduction

Monomethylmercury (CH3Hg) is a neurotoxin that can cause long-term developmental delays in children and has been linked to impaired cardiovascular health in adults (Axelrad et al., 2007, Choi et al., 2009, Grandjean et al., 1997: Roman et al., 2010, Karagas et al., in review, Fitzgerald and Clarkson, 1991). For most fish eating populations, marine fish are the major source of human exposure to CH3Hg globally. For example, in the United States over 90% of the population-wide CH3Hg intake is from marine and estuarine fish species (Carrington and Bolger, 2002, Sunderland, 2007, U.S. EPA, 2002). In an effort to reduce risks associated with human and wildlife exposures, the United Nations Environment Program (UNEP) is currently leading negotiations toward a global legally binding instrument on reducing global anthropogenic mercury (Hg) emissions and use in products (UNEP, 2010). One uncertainty in understanding the potential effectiveness of such agreements relates to how emissions reductions on a global scale will affect concentrations in marine fish. Better constraints on estimated lifetimes of different Hg forms in the ocean and biogeochemical factors driving interspecies conversions are needed to understand factors controlling accumulation in marine food webs. Here we review the sources of Hg and CH3Hg to open ocean regions, their areal and vertical distributions and synthesize information on temporal and spatial trends of the dominant species in seawater. Additionally, we review available data on CH3Hg concentrations in biological tissues and discuss potential impacts from anthropogenic emissions of Hg on human exposures and risks from marine fish.

The majority of Hg inputs to open ocean regions are from wet and dry atmospheric deposition (Mason et al., 1994a, Mason and Sheu, 2002, Sunderland and Mason, 2007, Soerensen et al., 2010). This inorganic mercury (HgII) can be transported laterally and vertically by ocean circulation and settling of suspended particulate matter, or may be reduced to dissolved gaseous elemental mercury (Hg0) and evaded to the atmosphere. Physical and biological characteristics of ocean basins determine both the lifetime of anthropogenic inorganic Hg in upper ocean waters and its relative conversion to the more toxic and bioaccumulative CH3Hg. Generally, model simulations have suggested that anthropogenic impacts are greatest in the surface mixed layer of the ocean (54 m annual modeled average; Soerensen et al., 2010, Strode et al., 2011; Fig. 1(A)). Note that throughout this manuscript we use the terms surface waters/mixed layer to refer to the top 100 m of the ocean while the term subsurface waters refers to those waters below the mixed layer but above the permanent thermocline, typically<1000 m. In the subsurface waters, penetration of anthropogenic Hg is varied and complicated by the lateral and vertical movement of water masses through upwelling and deep-water formation in different ocean basins, and with differences in the intensity of vertical transport processes (Sunderland and Mason, 2007, Strode et al., 2011, Mason and Sheu, 2002). Estimates of anthropogenic Hg enrichment vary among models that have different spatial and temporal resolution and consider different transport processes and evaluation of these models is constrained by limited measurements. Overall, anthropogenic Hg enrichment of deep ocean water (>1500 m) is smaller than surface and subsurface waters due to the long timescales for lateral and vertical transport to the deep ocean (Sunderland and Mason, 2007). Understanding the impacts of human activities on fish CH3Hg concentrations requires combining our knowledge of the time-scales required for penetration of anthropogenic Hg in the vertical marine water column with the dominant regions where inorganic Hg is converted to CH3Hg.

Both CH3Hg and dimethylmercury ((CH3)2Hg) are present in the ocean at detectable concentrations (e.g., Mason and Fitzgerald, 1990). While, as discussed below, there is the potential for different pathways for the formation and degradation of the methylated Hg forms, there is little concrete evidence for such differences in the literature. Additionally, analytical methods for methylated Hg species used do not always distinguish between CH3Hg and (CH3)2Hg (e.g., Cossa et al., 2011, Sunderland et al., 2009). Therefore, when comparing data in the literature, we compare and contrast the total methylated concentration to make use of all available data and denote the sum of these two species as ΣCH3Hg.

Hypothesized sources of CH3Hg for uptake into the marine food web include production in coastal and shelf sediments (Hammerschmidt and Fitzgerald, 2004, 2006a, b), hydrothermal vents and deep-sea sediments (Kraepiel et al., 2003), and in situ water column methylation processes (Mason and Fitzgerald, 1990, Heimburger et al., 2010, Lehnherr et al., 2011, Cossa et al., 2011, Sunderland et al., 2009). Here we review current understanding of these processes and their magnitude to identify plausible locations for the formation of CH3Hg that is bioaccumulated into marine food webs.

Risks associated with CH3Hg in marine fish can be managed over the short term by dietary interventions for sensitive groups, such as women of childbearing age and young children, by switching from high to low CH3Hg fish (Carrington et al., 2004) to effectively reduce CH3Hg exposure (Mahaffey et al., 2011, Oken et al., 2012). However, because of the health benefits of consuming fish (Oken et al., 2012), reducing the environmental Hg burden and associated accumulation in fish is the preferred long term approach for managing exposure. This review focuses on the physical and biological processes in open ocean regions that drive the timing and magnitude of changes in fish CH3Hg levels in response to changes in atmospheric Hg loadings. We review the best available knowledge of spatial, vertical and temporal patterns of Hg and CH3Hg in the major oceans and discuss the major gaps in process-level understanding and measurements, and their implications for ongoing regulatory efforts for Hg and CH3Hg.

Section snippets

Inorganic mercury sources and sinks

Sources of Hg to open ocean regions include inputs from ocean margins (rivers, estuaries), groundwater, benthic sediments, and hydrothermal vents and direct atmospheric deposition. Models and measurements suggest that direct atmospheric deposition is the dominant source of Hg with global inputs to the ocean ranging from 14 to 29 Mmol over the past decade (Dastoor and Larocque, 2004, Holmes et al., 2010, Mason and Sheu, 2002, Selin et al., 2007, Selin et al., 2008, Soerensen et al., 2010, Strode

Spatial trends in Hg concentrations

Concentrations of total dissolved Hg (<0.45 μm) in ocean waters vary by location horizontally and vertically. A compilation of information on the ranges of Hg and its various forms in coastal (excluding estuaries) and open ocean environments is shown in Table 1. For offshore water masses, measurements suggest that the total dissolved Hg is typically<3 pM. Developing an understanding of spatial variation of Hg in the ocean from available data is complicated by the wide timespan over which samples

Temporal trends in mercury inputs

Anthropogenic Hg emissions have increased atmospheric concentrations by at least a factor of three over the last century (e.g., Fitzgerald et al., 2005, Schuster et al., 2002, Lamborg et al., 2002b, Fain et al., 2009). Additionally, there is evidence of inputs of Hg into the atmosphere prior to the rapid industrialization in the last century due to the use of Hg in precious metal mining (Cooke et al., 2009, Schuster et al., 2002, Streets et al., In review) and these sources should have further

Bioaccumulation and concentrations in marine biota

Individuals in North America are exposed to CH3Hg primarily from the consumption of marine seafood (Mahaffey et al., 2004, U.S. EPA, 2002, Sunderland, 2007). Despite the toxicological significance of CH3Hg in oceanic biota, there is limited understanding of factors controlling accumulation in marine food webs, especially into primary producers and consumers. Available data are collated in Table 2. Because CH3Hg is biomagnified at every level of the food web (Mason et al., 1996, Wiener et al.,

Future directions and research needs

Trace metal clean measurements of Hg species in the ocean span about 30 years and there is substantial variability in seawater Hg concentrations due to changes related to anthropogenic input variations over time and space during this period, as noted above. This applies to other trace metals (e.g., Pb, Ag; Wu and Boyle, 1997, Bruland and Lohan, 2004). The temporal and distributional data regarding concentration and speciation of Hg in the ocean is somewhat spotty (Mason et al., 1998, Mason and

Summary and policy implications

Anthropogenic Hg emissions have impacted ocean ecosystems at varying levels globally. Estimates of human impacts on total Hg levels range from negligible changes in concentrations in the deep ocean waters (>1500 m) of the Pacific to an expected doubling of concentrations in the North Pacific surface and subsurface waters over the next few decades due to the growth of Asian emissions (Sunderland et al., 2009). Changes of this magnitude have been seen in the last 30 years for the upper North

Acknowledgments

This paper is part of a special issue that originated from meetings and activities coordinated through Dartmouth University as part of NIH Grant Number P42 ES007373 from the National Institute of Environmental Health Sciences. We acknowledge the efforts of the students, technicians and post-docs involved in our studies discussed here and their help in data synthesis. The ocean and atmospheric research of Mason, Fitzgerald, Hammerschmidt, Lamborg and Sunderland has been supported by the National

References (192)

  • D. Cossa et al.

    Total mercury in the water column near the shelf edge of the european continental margin

    Mar. Chem.

    (2004)
  • D. Cossa et al.

    Mercury in the Southern Ocean

    Geochim. Cosmochim. Acta

    (2011)
  • S. Covelli et al.

    Porewater distribution and benthic flux measurements of mercury and methylmercury in the Gulf of Trieste (northern Adriatic Sea). Estuar. Coast

    Shelf Sci.

    (1999)
  • J.A. Dalziel

    Reactive mercury in the Eastern North-Atlantic and Southeast Atlantic

    Mar. Chem.

    (1995)
  • A. Dastoor et al.

    Global circulation of atmospheric mercury: a modelling study

    Atmos. Environ.

    (2004)
  • J.A. Davis et al.

    Reducing methylmercury accumulation in the food webs of San Francisco Bay and its local watersheds

    Environ. Res.

    (2012)
  • V.M. Dekov

    Native Hg-liq. in the metalliferous sediments of the East Pacific Rise (21° S)

    Mar. Geol.

    (2007)
  • S.C. Doney et al.

    A chlorofluorocarbon section in the eastern North-Atlantic

    Deep-Sea Res.

    (1992)
  • C.T. Driscoll et al.

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

    Environ. Res.

    (2012)
  • G.A. Gill et al.

    Vertical mercury distributions in the oceans

    Geochim. Cosmochim. Acta

    (1988)
  • P. Grandjean

    Cognitive deficit in 7-year-old children with prenatal exposure to methylmercury

    Neurotoxicol. Teratol.

    (1997)
  • J.S. Gray

    Biomagnification in marine systems: the perspective of an ecologist

    Mar. Poll. Bull.

    (2002)
  • C.R. Hammerschmidt et al.

    Methylmercury cycling in sediments on the continental shelf of southern New England

    Geochim. Cosmochim. Acta

    (2006)
  • C.R. Hammerschmidt et al.

    Sediment–water exchange of methylmercury determined from shipboard benthic flux chambers

    Mar. Chem.

    (2008)
  • C.R. Hammerschmidt et al.

    Biogeochemistry of methylmercury in sediments of Long Island Sound

    Mar. Chem.

    (2004)
  • C.R. Hammerschmidt et al.

    Organic matter and sulfide inhibit methylmercury production in sediments of New York/New Jersey Harbor

    Mar. Chem.

    (2008)
  • R. Harris et al.

    Mercury in the Gulf of Mexico: Sources to Receptors

    Environ. Res.

    (2012)
  • L.E. Heimburger

    Methyl mercury distributions in relation to the presence of nano- and picophytoplankton in an oceanic water column (Ligurian Sea, North-Western Mediterranean)

    Geochim. Cosmochim. Acta

    (2010)
  • A. Heyes et al.

    Mercury methylation in estuaries: insights from using measuring rates using stable mercury isotopes

    Mar. Chem.

    (2006)
  • A. Heyes et al.

    Mercury and methylmercury in Hudson River sediment: impact of tidal resuspension on partitioning and methylation

    Mar. Chem.

    (2004)
  • T.A. Hollweg et al.

    Methylmercury production in sediments of Chesapeake Bay and the mid-Atlantic continental margin

    Mar. Chem.

    (2009)
  • N.C. Kamman et al.

    Historical and present fluxes of mercury to Vermont and New Hampshire lakes inferred from Pb-210 dated sediment cores

    Atmos. Environ.

    (2002)
  • E.H. Kim et al.

    The impact of resuspension on sediment mercury dynamics, and methylmercury production and fate: a mesocosm study

    Mar. Chem.

    (2006)
  • M. Amyot et al.

    Dark oxidation of dissolved and liquid elemental mercury in aquatic environments

    Environ. Sci. Technol.

    (2005)
  • M. Andersson et al.

    A description of an automatic continuous equilibrium system for the measurement of dissolved gaseous mercury

    Anal. Bioanal.Chem.

    (2008)
  • A. Antia et al.

    Basin-wide particulate organic carbon flux in the Atlantic Ocean: regional export patterns and potential for CO2 sequestration

    Global Biogeochem. Cycles

    (2001)
  • L. Atwell et al.

    Biomagnification and bioaccumulation of mercury in an arctic marine food web: insights from stable nitrogen isotope analysis

    Can. J. Fish. Aquat. Sci.

    (1998)
  • D.A. Axelrad et al.

    Dose-response relationship of prenatal mercury exposure and IQ: an integrative analysis of epidemiologic data

    Environ. Health Perspect.

    (2007)
  • Balcom, P.H., Fitzgerald, W.F., Mason, R.P., 2010. Synthesis and assessment of heavy metal contamination in the Hudson...
  • W. Baeyens et al.

    Bioconcentration and biomagnification of mercury and methylmercury in North Sea and Scheldt estuary fish

    Arch. Environ. Contam. Toxicol.

    (2003)
  • R.T. Barber et al.

    Mercury concentrations in recent and ninety-year-old benthopelagic fish

    Science

    (1972)
  • J.M. Benoit et al.

    Effect of bioirrigation on sediment–water exchange of methylmercury in Boston Harbor, Massachusetts

    Environ. Sci. Technol.

    (2009)
  • F.J. Black et al.

    Submarine groundwater discharge of total mercury and monomethylmercury to central California coastal waters

    Environ. Sci. Technol.

    (2009)
  • F.J. Black et al.

    Stability of dimethyl mercury in seawater and its conversion to monomethyl mercury

    Environ. Sci. Technol.

    (2009)
  • N.S. Bloom et al.

    Speciation and cycling of mercury in Lavaca Bay, Texas, sediments

    Environ. Sci. Technol.

    (1999)
  • S.E. Bone et al.

    Has submarine groundwater discharge been overlooked as a source of mercury to coastal waters?

    Environ. Sci. Technol.

    (2007)
  • G.M. Boush et al.

    Total mercury content in yellowfin and bigeye tuna

    Bull. Enviorn. Contam. Toxicol.

    (1983)
  • Bowman, K.L., Hammerschmidt, C.R., Lamborg, C.H., 2012. U.S. GEOTRACES: distribution of mercury species across a zonal...
  • W.S. Broeker et al.

    Tracers in the Sea.

    (1982)
  • K.W. Bruland et al.

    Controls of trace metals in seawater

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    This publication was made possible by NIH Grant Number P42 ES007373 from the National Institute of Environmental Health Sciences. Support also was provided by the U.S. National Science Foundation’s Atmospheric Chemistry and Chemical Oceanography Divisions.

    This research has not involved human subjects or experimental animals.

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