Mercury biogeochemical cycling in the ocean and policy implications☆
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
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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.