Mercury in the Anthropocene Ocean

. The toxic metal mercury is present only at trace levels in the ocean, but it accumulates in fish at concentrations high enough to pose a threat to human and environmental health. Human activity has dramatically altered the global mercury cycle, resulting in loadings to the ocean that have increased by at least a factor of three from pre-anthropogenic levels. Loadings are likely to continue to increase as a result of higher atmospheric emissions and other factors related to global environmental change. The impact that these loadings will have on the production of methylated mercury (the form that accumulates in fish) is unclear. In this article, we summarize the biogeochemistry of mercury in the ocean and use this information to examine past impacts that human activity has had on the cycling of this toxic metal. We also highlight ways in which the mercury cycle may continue to be affected and its potential impact on mercury in fish.


INTRODUCTION
Mercury is a notoriously toxic trace metal that has received global attention since the poisoning of thousands of people in southern Japan (Minamata and Niigata) in the mid-1950s. Ingestion of fish laden with monomethylmercury (CH 3 Hg + ) caused those tragic circumstances and inspired researchers worldwide to examine mercury toxicity to humans and wildlife, measure concentrations in terrestrial and aquatic biota, and understand the biogeochemical cycling of the element's multiple forms.
Mercury (Hg) would be of little toxicological concern if it were not for its microbial and abiotic Oceanography | Vol. 27, No. 1 transformation to CH 3 Hg + , which is the form that most readily bioaccumulates and biomagnifies in marine food webs.
These processes result in CH 3 Hg + concentrations in predatory fish and marine mammel species, including many species eaten by humans (e.g., tuna, swordfish, shark, pilot whale) that regularly exceed guidelines for safe consumption. Indeed, 5-10% of US women of childbearing age have blood CH 3 Hg + levels that increase the risk of neurodevelopmental problems in their children (Mahaffey et al., 2009), presumably as a result of eating seafood (Selin et al., 2010). While the effects of current mercury exposures may not be as overt as those experienced in Minamata, the size of the worldwide population exposed to potentially harmful levels of CH 3 Hg + via seafood consumption is likely in the hundreds of millions.
In addition to the impact on human health, we are just beginning to understand how elevated concentrations of mercury can affect the health and sustainability of food webs. Several studies document developmental and behavioral effects of CH 3 Hg + on fish and other animals at concentrations commonly found in the environment but at levels well below those that cause acute toxicity (e.g., Scheuhammer et al., 2007). Indeed, some studies suggest that the sustainability of some animal populations may already be threatened by impaired reproductive success as a result of mercury exposure (e.g., Tartu et al., 2013).
These disturbing ecological findings come in the context of geochemical research that indicates human activities have significantly perturbed the mercury cycle on local, regional, and global scales. Mercury loadings to the atmosphere, for example, have increased at least three-fold since the Industrial Revolution and are expected to continue to rise (e.g., Driscoll et al., 2013). Some research even suggests that anthropogenic impacts on the mercury cycle extend back well before industrialization, largely as a result of the use of mercury in gold and silver mining.
Here, we review the environmental pathways of mercury from its introduction to the ocean to its accumulation in seafood, focusing on what is known and unknown about key microbial transformations of mercury in the sea, and how this cycle may change in the future.

MERCURY SPECIES CONCENTR ATIONS AND TR ANSFORMATIONS IN THE OCEAN
Mercury exists primarily as four chemical species in the ocean: elemental Hg (Hg 0 ), mercuric ion (Hg 2+ , also written as Hg(II)) in a variety of inorganic and organic complexes, and methylated forms that include both CH 3 Hg + and dimethylmercury ((CH 3 ) 2 Hg; Table 1; Figure 1). As with most trace metals, both biological and physical processes govern the distribution of total mercury in the ocean. Combined influences of bioaccumulation and organic matter remineralization, as well as inputs from the atmosphere, scavenging, and horizontal advection, result in mercury displaying nutrient-and scavenged-type profiles with depth in the ocean. At any location, the profile will be dependent upon the relative strength of each of these processes (e.g., Mason et al., 2012). and release during remineralization of soft tissues in the thermocline likely cause nutrient-type distributions of mercury, as is often observed for trace metals that are biologically essential (e.g., zinc, cobalt, cadmium). Thus, increased concentrations of total dissolved mercury in the thermocline are a result of vertical transport from above and a slow rate of removal by either scavenging or microbial uptake.
Although distributions of total mercury are important to establish, the story of mercury cycling in the ocean is fundamentally connected to its proclivity to change chemical and physical forms.
Natural and anthropogenic sources emit elemental Hg (as well as a lesser amount of gaseous Hg(II)). Direct atmospheric deposition is presumed to be the principal source of Hg(II) (mercury is oxidized to Hg(II) in the atmosphere) to most of the ocean (e.g., Driscoll et al., 2013), although rivers and groundwater can be more important in nearshore systems and the confined Arctic Ocean. This flux amounts to about 7 Mmol yr -1 net (Amos et al., 2013). Once in the marine environment, Hg(II) has a complex biogeochemistry, resulting in one of three fates ( Figure 1): (1) reduction to Hg 0 and evasion to the atmosphere, (2) methylation to either CH 3 Hg + or (CH 3 ) 2 Hg, and (3) scavenging from the water column.

Reduction
Net reduction of Hg(II) to Hg 0 proceeds strongly enough that Hg 0 is often supersaturated in seawater with respect to the atmosphere (Mason et al., 2012). Subsequent evasion of Hg 0 to the atmosphere is half of the air-sea cycling loop and is a unique aspect of the biogeochemistry of this metal. The reduction and evasion process is a major component of the marine Hg cycle, with evasion fluxes removing 50-80% of gross loadings from the atmosphere. Mercury reduction in seawater is thought to occur rapidly and to include both abiotic (photo chemical) reactions as well as reduction by biota. Most mercury reduction in productive coastal waters is likely accomplished by a biological mechanism that is driven by any one of several mercury-reducing bacteria. In contrast, photo chemical reduction is more likely the dominant pathway in the open ocean, where light penetration is deeper and biological productivity less.

Methylation and Demethylation
Sediments External sources of the methylated forms of mercury are too low to explain their concentrations and fluxes in the ocean (e.g., Fitzgerald et al., 2007), suggesting that the primary source is internal production in sediments or the water column.
In nearshore environments and likely for continental shelves, in situ sediment production accounts for most of the CH 3 Hg + present. Other significant sources of CH 3 Hg + to nearshore systems include tidal marshes, wastewater treatment facilities, submarine groundwater discharge, and mangroves that have exceptionally high rates of mercury methylation (e.g., Driscoll et al., 2013).
Principal losses of CH 3 Hg + from these waters include sedimentation, photochemical decomposition, harvesting of seafood, and export to the wider ocean.
In a recent breakthrough, Parks et al. is oxidized in the atmosphere to complexes of divalent mercury Hg(II) and deposited to land and the surface ocean. Hg(II) can be either reduced to Hg 0 or methylated to form monomethylmercury (CH 3 Hg + ) and dimethylmercury ((CH 3 ) 2 Hg). Blue arrows highlight biogeochemical transformations of mercury. Black arrows denote fluxes among the atmosphere, water, sediments, and biota. All of the mercury species can be transported hydrologically between the coastal zone, surface ocean, and deep sea, with bioaccumulative CH 3 Hg + also transported by bioadvection (white arrows; Fitzgerald et al., 2007).    (e.g., SO 4 2or Fe(III)) as well as labile organic matter appear to be sufficient to fuel organisms' mercury methylation even in the sandiest of marine deposits.
Accordingly, geochemical factors that influence sediment-water partitioning and the chemical speciation of Hg(II) substrate greatly affect benthic production of CH 3 Hg + . Maximum rates of CH 3 Hg + production are observed in coastal sediments that have relatively low levels of both solid-phase organic matter and sulfide, which favors partitioning of Hg(II) species into pore water and therefore uptake by microbes (Fitzgerald et al., 2007). In contrast, CH 3 Hg + production can be inhibited in sediments with enhanced levels of either organic matter (greater particle binding) or sulfide, which shifts speciation of dissolved Hg−S species to ionically charged complexes that are less bioavailable (e.g., Benoit et al., 1999 and Hg(II) are the end products or by use of the organomercurial lyase protein, MerB, encoded on the mer operon (Barkay et al., 2003). However, microbial demethylation via the mer operon is likely not the dominant mechanism of CH 3 Hg + loss in anoxic sediment.

Water Column
Hg(II) also can be methylated to matter (e.g., Mason and Fitzgerald, 1993), the process that also is partly responsible for the oxygen minimum, in addition to a slow rate of ventilation in the thermocline. Sectional oceanographic studies have observed associations between methylated mercury species and either apparent oxygen utilization (AOU) or the rate of organic carbon remineralization (Sunderland et al., 2009), which suggests that production of methylated mercury in the marine water column is limited by methylation potential more than it is by Hg(II) availability.   Balcom et al. (2004) ocean. We can make a first order estimate using studies that observed correlations between mercury and organic matter in sediments (e.g., Fitzgerald et al., 2007) 1970s, 1980s, and 1990s. This key component of the method, which has been subsequently refined, allows pico-and femtomolar concentrations of mercury to be isolated and determined from seawater. The form of gold (Au) can vary, but it is usually quartz sand with a thin coating of Au 0 . In a bit of chemical irony, this method represents the converse of the way in which mercury has long been used in gold mining, where mercury is added to a sediment/rock/water slurry, the mixture is agitated, and the gold is allowed to amalgamate to the mercury. Later, the dense mercury is recovered from the slurry through settling and then boiled off to reveal the precious gold.
Thus, today, Hg analysts use essentially the same technology that resulted in contamination in the past to study the impact of that contamination. The organomercury compounds are determined in a similar process, by derivitization rather than reduction, purge, and trap onto organic-trapping Tenax instead of gold, and separation by gas chromatography prior to analysis to isolate the methylated forms from Hg 0 and Hg(II). As part of the US GEOTRACES program, all of these analyses are performed at sea in a self-contained Hg lab (see figure). However, our current understanding of the dependencies of various aspects of mercury biogeochemistry on these various forcings is too limited to make firm predictions. For example, Table 2 shows a few of the forcings that have been considered, some of which display competing impacts on the mercury cycle. Thus, as with many aspects of global change science, the impact on the mercury cycle is very uncertain, which complicates the job of planning for or mitigating the impact of future mercury loadings to the ocean.

REGIONAL IMPACT CASE STUDIES
The  and receives a total areal Hg load that is less than half that of the SCS. Indeed, the SCS is closer in areal loading to urbanized embayments like Long Island Sound than the Mediterranean (Table 3).

ATMOSPHERE-RELATED
So much Hg is in the air over the SCS that in winter, when winds are from the northwest, Hg 0 invades the sea in a situation rarely observed anywhere else (evasion is the norm; Tseng et al., 2013).
At most times of the year, the evasional flux of Hg from the SCS is virtually the same as that from the Mediterranean and other ocean regions, implying that evasion may not be proportional to total Hg, as is frequently assumed (e.g., Amos et al., 2013). If this is the case, then progressively larger percentages of Hg loadings to the wider ocean can be expected to remain there than current models predict. If the future of most ocean regions is anything like the SCS, the impact of human emissions may be more serious than we currently appreciate.

The Arctic
There are two reasons that the Arctic is of concern with respect to global mer- The events themselves may not be new phenomena (Drevnick et al., 2012), but with the loss of sea ice in the Arctic, the process of re-emission of Hg deposited by Depletion Events may decrease in the future, dramatically increasing the net load to the Arctic Ocean (assuming snow is better at reducing/evading Hg than the ocean).
A second cause for concern is the impact that global change is having on Arctic animals appear to be threatened by Hg-induced loss of fecundity (Tartu et al., 2013), and others are likely to follow (AMAP, 2011). As with global warming, the Arctic may be the "canary in the coal mine" for the impact of our past, present, and future releases of mercury to the environment.

WHAT CAN BE DONE?
The   Moving forward, several lessons emerge for future mercury policy. Experience with regional mercury management suggests that future policy should take into account transboundary influences, coordinate across environmental media, and better assess human and ecological impacts in regulatory analyses. With the new Minamata Convention, coordinating policies across scales-ensuring that national, regional, and international actions are consistent and reinforcing-will become more important. In addition, because mercury is a legacy pollutant, population risks could be further minimized by improved adaptive measures, such as fish advisories, before the benefits of international policy are fully realized.