A global perspective on mercury cycling in the ocean

Journal Pre-proof A global perspective on mercury cycling in the ocean

Katlin L. Bowman, Carl H. Lamborg, Alison M. Agather PII:

S0048-9697(19)36162-5

DOI:

https://doi.org/10.1016/j.scitotenv.2019.136166

Reference:

STOTEN 136166

To appear in:

Science of the Total Environment

Received date:

1 August 2019

Revised date:

10 December 2019

Accepted date:

15 December 2019

Please cite this article as: K.L. Bowman, C.H. Lamborg and A.M. Agather, A global perspective on mercury cycling in the ocean, Science of the Total Environment (2019), https://doi.org/10.1016/j.scitotenv.2019.136166

This is a PDF file of an article that has undergone enhancements after acceptance, such as the addition of a cover page and metadata, and formatting for readability, but it is not yet the definitive version of record. This version will undergo additional copyediting, typesetting and review before it is published in its final form, but we are providing this version to give early visibility of the article. Please note that, during the production process, errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.

© 2019 Published by Elsevier.

Journal Pre-proof

A global perspective on mercury cycling in the ocean Katlin L. Bowmanab*, Carl H. Lamborgb, Alison M. Agatherc a

Moss Landing Marine Laboratories, 8272 Moss Landing Road, Moss Landing, California

95039, USA [email protected] b

University of California Santa Cruz, Ocean Sciences Department, 1156 High Street, Santa Cruz,

California 95064, USA [email protected] National Oceanic and Atmospheric Administration, 1325 East West Highway, Silver Spring,

of

c

ro

MD 20910, USA [email protected] *

Jo

ur

na

lP

re

-p

Corresponding author: 117 Handley Street, Santa Cruz, CA 95060, USA (Permanent address)

Journal Pre-proof Abstract Mercury (Hg) is a ubiquitous metal in the ocean that undergoes in situ chemical transformations in seawater and marine sediment. Most relevant to public health is the production of monomethyl-Hg, a neurotoxin to humans that accumulates in marine fish and mammals. Here we synthesize 30 years of Hg measurements in the ocean to discuss sources, sinks, and internal cycling of this toxic metal. Global-scale oceanographic survey programs (i.e.

of

CLIVAR and GEOTRACES), refined protocols for clean sampling, and analytical advancements

ro

have produced over 200 high-resolution, full-depth profiles of total Hg, methylated Hg, and

-p

gaseous elemental Hg throughout the Atlantic, Pacific, Arctic, and Southern Oceans. Vertical

re

maxima of methylated Hg were found in surface waters, near the subsurface chlorophyll maximum, and in low-oxygen thermocline waters. The greatest concentration of Hg in deep

lP

water was measured in Antarctic Bottom Water, and in newly formed Labrador Sea Water, Hg

na

showed a decreasing trend over the past 20 years. Distribution of Hg in polar oceans was unique relative to lower latitudes with higher concentrations of total Hg near the surface and vertical

ur

trends of Hg speciation driven by water column stratification and seasonal ice cover. Global

Jo

models of Hg in the ocean require a better understanding of biogeochemical controls on Hg speciation and improved accuracy of methylated Hg measurements within the international community.

Keywords: GEOTRACES, methylmercury, speciation, fluxes, sources, sinks

Journal Pre-proof

1. Introduction Initial measurements of mercury (Hg) in the open-ocean were mostly limited to the upper water column (< 1000 m) and high detection limits thwarted analysis of methylated Hg species (Gill and Fitzgerald, 1988; Mason et al., 1998; Mason and Sullivan, 1999; Mason and Fitzgerald, 1990). In the past 20 years, further development of clean sampling protocols, lower analytical

of

detection limits, and establishment of global-scale oceanographic survey programs (i.e. CLIVAR

ro

and GEOTRACES) advanced our understanding of the biogeochemical cycle of Hg in the global

-p

ocean. Today, more than 200 high-resolution, full-depth profiles of Hg speciation spanning the

re

Arctic, Atlantic, Pacific, and Southern Oceans are published (Figure 1). This review offers new insight garnered from this wealth of data and highlights remaining gaps in our understanding of

lP

ocean Hg cycling.

na

Mercury from natural and anthropogenic sources enters the ocean primarily through atmospheric deposition (precipitation and dust), but also via riverine and submarine groundwater

ur

discharge, and input from deep-sea hydrothermal vents (Amos et al., 2014; Ganguli et al., 2012;

Jo

Horowitz et al., 2017; Lamborg et al., 2006; Mason et al., 2017; Outridge et al., 2018; Streets et al., 2017). Air-sea exchange of Hg in the surface ocean is the largest gross source and sink, and therefore, controls oceanic concentrations (DiMento et al., 2019; Mason et al., 2017; Soerensen et al., 2014). Inorganic Hg (Hg2+) is photochemically and microbially reduced to gaseous elemental Hg (Hg0), often resulting in oversaturation of surface waters and evasion of Hg0 to the atmosphere (Mason et al., 2001). Mercury is also bound to particles and organic ligands and converted to monomethyl-Hg (MMHg), gaseous dimethyl-Hg (DMHg), or Hg0 below the surface (Lamborg et al., 2004; Lamborg et al., 2016; Lehnherr et al., 2011). Methylation reactions are

Journal Pre-proof thought to occur where heterotrophic organisms are active, particularly in low-oxygen thermocline waters (Sunderland et al., 2009). Production of MMHg in the thermocline is concerning as this neurotoxin biomagnifies in marine food webs (Lavoie et al., 2013). Humans are exposed to Hg primarily as MMHg through seafood consumption (Kim et al., 2016; Lavoie et al., 2018; Sunderland et al., 2018), and globally, more than 60% of seafood is harvested from the ocean (FAO, 2018). Anthropogenic emissions have increased Hg concentrations in the

of

thermocline by 150 % since pre-industrial times (Lamborg et al., 2014); therefore, our

ro

understanding of the marine Hg cycle is important to uncover the impact human emissions have

-p

on seafood resources.

re

2. Analytical challenges of Hg analysis in seawater

The merit of comparing Hg concentrations from various oceanic datasets relies on the

lP

assumption that different collection and analytical methods accurately quantify each chemical

na

form of Hg. As with other trace-elements, the logistics of generating large open-ocean datasets often requires less favorable practices, such as quantifying dissolved gaseous Hg (DGM = Hg0 +

ur

DMHg) and total methylated Hg (MeHgT = MMHg + DMHg), rather than analyzing each

Jo

chemical species separately. Intercalibration exercises facilitated by the international GEOTRACES program (geotraces.org) have shown improvement in the accuracy of picomolar total Hg measurements in seawater; however, intercomparison of open-ocean methylated Hg needs improvement (Figure A.1). Poor intercomparison of methylated Hg stems from low (femtomolar) ambient concentrations in the ocean and a variety of analytical methods. In seawater, total Hg (the concentration of all Hg species in a sample) is analyzed by a standard redox reaction using BrCl and SnCl2. The resulting gaseous Hg0 is purged from solution with Hg-free gas and quantified by cold vapor atomic fluorescence spectrometry (CVAFS), or

Journal Pre-proof cold vapor atomic absorption spectrometry (CVAAS) (Bloom and Crecelius, 1983; Fitzgerald and Gill, 1979; Freimann and Schmidt, 1982). This method is used routinely by the U.S. Environmental Protection Agency and has been updated for clean analysis techniques by the GEOTRACES community (Cutter et al., 2017; EPA, 2002). Some earlier oceanic studies report reactive Hg (HgR), analyzed by direct reduction with SnCl2, which underestimates total Hg concentrations (Gill and Fitzgerald, 1988; Mason et al., 1995a).

of

Gaseous species of Hg (Hg0 and DMHg) are stripped from seawater by purging with Hg-

ro

free gas, typically N2, within 1–2 hours of collection. Effluent gas first passes through a soda

-p

lime column to remove water vapor and neutralize acidity, then through a solid phase adsorption

re

column to concentrate DHMg, and finally a Au-packed column to concentrate Hg0 (Agather et al., 2019; Bowman et al., 2015; Bowman et al., 2016; Munson et al., 2015). Solid phase

lP

adsorption traps used to collect DMHg include Bond-Elut (Agather et al., 2019; Baya et al.,

na

2013; Bowman et al., 2016), Tenax (Bowman and Hammerschmidt, 2011; Bowman et al., 2015; Bratkič et al., 2016), and Carbotrap (Lehnherr et al., 2011). Dimethylmercury is quantified by

ur

gas-chromatographic CVAFS (GC-CVAFS) or GC-inductively coupled plasma mass

Jo

spectrometery (GC-ICP-MS). Elimination of the solid phase adsorption column (Au-packed column only) quantifies DGM. After sample collection, Au traps are analyzed for either DGM or Hg0 by CVAFS.

Acidified seawater is analyzed for MeHgT and MMHg by first rendering the Hg species volatile so they can be purged from solution. This can be done by hydride generation or organic derivatization (usually ethylation, propylation or phenylation). Both approaches can be done directly from preserved seawater (Bowman and Hammerschmidt, 2011; Cossa et al., 2011; Munson et al., 2014), but the organic derivatization approaches are conventionally performed on

Journal Pre-proof MMHg extracted from seawater by distillation or into a non-aqueous phase (e.g., Horvat et al., 1993; Monperrus et al., 2005). Because DMHg is demethylated to MMHg upon acidification, it must first be purged from seawater to quantify only MMHg (Bowman and Hammerschmidt, 2011; Coale et al., 2018). Alternatively, un-purged samples subjected to MMHg analysis can provide a value for MeHgT. Seawater analyzed via direct aqueous ethylation is neutralized after acidification and amended with an ethylating agent such as sodium tetraethylborate. The

of

efficiency of the ethylation reaction is pH dependent and can be improved with addition of

ro

ascorbic acid (Bowman and Hammerschmidt, 2011; Munson et al., 2014). Resulting

-p

methylethyl-Hg is sparged onto a solid phase adsorption trap (Tenax) and analyzed by GC-

re

CVAFS (Agather et al., 2019; Bowman et al., 2015; Bowman et al., 2016; Bratkič et al., 2016) or GC-ICP-MS (Heimbürger et al., 2015; Lehnherr et al., 2011). Organic derivatization performed

lP

on extracted MMHg is analogous, but also frequently accompanied by isotope dilution to

na

account for inefficiencies during extraction (e.g., Monperrus et al., 2005). For hydride generation, acidified samples are analyzed directly with addition of a reducing agent such as

ur

sodium borohydride to form Hg0 and MeHgH (e.g., Cossa et al., 2011; Stoichev et al., 2002).

Jo

These species are sparged from the sample with He gas onto a cooled quartz column. After removing the column from liquid nitrogen, Hg-free gas carries thermally desorbed Hg for analysis either by GC-AFS (Cossa et al., 2011; Živković et al., 2017) or GC-ICP-IMS (Heimbürger et al., 2015). Particulate total Hg and MMHg concentrations are quantified by analysis of the particles or by subtraction. Direct measurement quantifies particles collected on quartz fiber filters and digested in acid prior to analysis by CVAFS and GC-CVAFS (Agather et al., 2019; Bowman et al., 2015; Bowman et al., 2016). Quantification by subtraction requires collection of an unfiltered

Journal Pre-proof and filtered sample, the difference in these two concentrations representing the particulate phase (Cossa et al., 2018). Fluxes into and out of the ocean from the atmosphere are determined using essentially the same approach analytically, but with different sample collection approaches. Precipitation Hg over the ocean or at coastal land stations is generally collected on an ad hoc basis into rigorously cleaned funnels/condensors of various designs (e.g., Fogg and Fitzgerald, 1979; Mason et al.,

of

1992; Weiss-Penzias et al., 2016). Such samples can be processed as seawater samples

ro

mentioned above, but limited sample sizes mean that most cited data are merely total Hg,

-p

without speciation. There are some examples of MMHg data as well (Conaway et al., 2010; Lamborg et al., 1999; Marumoto and Matsuyama, 2014; e.g., Mason et al., 1992), but no

re

examples of precipitation Hg0 or DMHg. These concentration measurements are then converted

lP

to a flux with knowledge, from a variety of sources, of regional and global precipitation depths

na

for a time interval of interest. In addition to precipitation phases, “dry” forms of atmospheric deposition can also contribute to Hg fluxes to the ocean and these include both particulate and

ur

gaseous forms of Hg. The aerosol/particulate forms are much easier to collect and quantify, and

Jo

there are a few examples of such samples being collected over the ocean and at coastal sites, by pulling large volumes of air through a variety of filtering materials (Bowman et al., 2015; Morton et al., 2013). As to the gaseous forms of Hg that may engage in dry deposition, there is only one approach that seems to have found favor amongst researchers, which is the use of a “denuder,” functionally the opposite of filter in that it allows reactive gases to be collected while allowing particles to pass (Feng et al., 2003; Lu et al., 2003; Soerensen et al., 2010). In the case of Hg species that might deposit to the ocean, they are thought to be gas-phase forms of Hg2+ compounds, and thus denuders coated with KCl or similar ionic solution thought to be capable of

Journal Pre-proof absorbing Hg2+ species are used. These dry fluxes of Hg are calculated by typically multiplying concentrations with a deposition velocity thought to be characteristic of that phase or through the application of micrometeorological measurements, and is likely a substantial source of uncertainty in estimating this term in the Hg cycle (Lindberg and Stratton, 1998; Skov et al., 2006). With regard to the flux of Hg out of the ocean, recent deployments of equilibrator

of

approaches have proved very successful, fed with water from ship’s clean surface water intakes

ro

otherwise used for measuring CO2 and other properties while underway or from clean intakes

-p

deployed over the side of the ship (e.g., Andersson et al., 2011; DiMento et al., 2019; Kuss et al.,

re

2011; Mason et al., 2017). In this approach, water is continuously pumped through a large volume degassing system with water/gas flow ratios set so that the gas leaving the system is at

lP

equilibrium with the amount of Hg0 in the water. The amount of Hg0 in the effluent gas is then

na

monitored, and in this way high resolution transects of Hg0 in surface water can be developed. The flux to the atmosphere is then estimated by multiplying concentrations by an evasion piston

ur

velocity, which like the dry deposition velocity, is uncertain and usually estimated using

Jo

functions of wind speed (e.g., Nightingale et al., 2000). A final phase of oceanic Hg that might contribute to air-sea exchange of Hg is the surface microlayer (SML). This represents the ocean’s “skin” and is a location of chemical properties that are dramatically different from bulk surface seawater. This layer is extremely difficult to sample, but such samples are treated like those mentioned above. The impact of this layer on Hg cycling is the topic of active and on-going research (Coale et al., 2018).

Journal Pre-proof 3. Distribution and speciation in the upper water column 3.1 Total Hg Vertical profiles of total Hg have nutrient-like, scavenged, and transient (a combination of nutrient-like and scavenged) characteristics controlled by external sources of Hg to the surface ocean and scavenging by biomass and inorganic particles. In the Atlantic and Pacific Oceans, total Hg concentrations in the thermocline (150–1000 m) exceeded those of the upper water

of

column (<150 m) from release of Hg during organic matter respiration (Bowman et al., 2015;

ro

Bowman et al., 2016; Bratkič et al., 2016; Hammerschmidt and Bowman, 2012; Munson et al.,

-p

2015; Sunderland et al., 2009). This is not the case in the Arctic Ocean and Southern Ocean near

re

Antarctica where concentrations of total Hg were greater in the upper water column compared to thermocline waters (Agather et al., 2019; Cossa et al., 2011; Heimbürger et al., 2015;

lP

Mastromonaco et al., 2017). Trapped DGM in ice-covered surface waters, input of Hg from

na

melting ice and rivers, and lack of respiration due to low productivity contributed to this trend. Coastal upwelling, sea ice, submarine groundwater discharge, and riverine inputs

ur

increase concentrations of total Hg over the continental shelf and slope (Black et al., 2009; Bone

Jo

et al., 2007; Bowman et al., 2016; Bratkič et al., 2016; Cossa et al., 2011; Ganguli et al., 2012; Gionfriddo et al., 2016; Heimbürger et al., 2015). However, some regions such as the Chukchi shelf and northwest Atlantic margin had total Hg concentrations similar to the open ocean (Agather et al., 2019; Bowman et al., 2015). Riverine flux of Hg to the ocean can be reduced by scavenging and deposition in estuaries, particle settling on the continental shelf, and photochemical reduction followed by re-emission back to the atmosphere (Amos et al., 2014; Buck et al., 2015; Sonke et al., 2018).

Journal Pre-proof The lowest concentrations of total Hg (< 1.0 pM) were found in the upper 1000 m of the central and eastern tropical Pacific Ocean and the Labrador Sea (Table 1; Bowman et al., 2016; Cossa et al., 2018; Munson et al., 2015). The Atlantic, Arctic, and Southern Oceans, as well as the northeast Pacific had average total Hg concentrations >1.0 pM in the upper 1000 m (Table 1; Bowman et al., 2015; Bratkič et al., 2016; Cossa et al., 2004; Cossa et al., 2011; Sunderland et

these basins (Agather et al., 2019; Lamborg et al., 2014).

ro

3.2 Vertical profiles of methylated Hg

of

al., 2009); anthropogenic Hg has been estimated to contribute to thermocline waters in each of

-p

The first measurements of methylated Hg (as DMHg) in the open-ocean were achieved in

re

the equatorial Pacific more than 30 years ago (Kim and Fitzgerald, 1988). The authors of this study hypothesized that bacterial methylation of inorganic Hg occurs in the oxygen minimum

lP

zone (OMZ), an explanation that has been tested through decades of water column measurements

na

and seawater methylation studies. Low-oxygen thermocline waters, however, are not the only depth region in the ocean where methylated Hg accumulates. Vertical profiles across the global

ur

ocean reveal three important depth regions: 1) surface ocean (0–2 m depth), 2) subsurface

Jo

chlorophyll maximum (SCM; <150 m), and 3) thermocline waters depleted of oxygen during microbial respiration (<1000 m). Photodegradation and gas evasion remove MMHg and DMHg (respectively) from surface waters; however, the surface ocean is not devoid of methylated Hg (DiMento and Mason, 2017; Mason et al., 2017). Average MeHgT concentrations represented 3–34% of total Hg in surface waters (0–2 m) across the globe. In Arctic surface waters MeHgT was 3–13% (n = 3) of total Hg, with MMHg as the dominant species (Agather et al., 2019). In the eastern North Pacific, only MMHg was present in surface water representing 4% (n = 1) of HgT (Hammerschmidt and

Journal Pre-proof Bowman, 2012). In the North Atlantic, %MeHgT was relatively high and variable (34 ± 22%, n = 9; Bowman et al., 2015). Monomethyl-Hg was the dominant species across the North Atlantic except near Africa where dust deposition from the Sahara Desert scavenged MMHg, leaving DMHg as the dominant methylated species (Bowman et al., 2015). In the South Atlantic, MeHgT represented 4–5% of total Hg (Bratkič et al., 2016). Potential sources of methylated Hg in surface waters are in situ methylation (Lehnherr et al., 2011; Monperrus et al., 2007; Munson et

of

al., 2018), upward diffusion from subsurface waters (Kim et al., 2017), and atmospheric

ro

deposition (Mason et al., 2017).

-p

The SCM is found in the oxygenated euphotic zone (<150 m) where optimal light and

re

nutrient conditions fuel phytoplankton growth (Cullen, 2015). Discovery of MeHgT maxima coincident with the SCM was unexpected, as heterotrophic microorganisms, rather than

lP

autotrophs, are assumed to control net Hg methylation in the ocean. Though less common than

na

maxima in the thermocline, MeHgT maxima at the SCM were found in the Atlantic and Pacific Oceans (Bowman et al., 2015; Bowman et al., 2016; Bratkič et al., 2018). Maxima of MeHgT in

ur

the euphotic zone were first reported in the Mediterranean Sea where temporal data revealed the

Jo

highest concentrations during periods dominated by nano- and pico-phytoplankton communities (Heimbürger et al., 2010).

Vertical maxima of MMHg and MeHgT are consistently found in low-oxygen thermocline waters where heterotrophic microorganisms respire sinking organic matter. Proxies for organic matter respiration have been used, to varying degrees of success, to predict concentrations of MeHgT in the ocean (Kim et al., 2017; Semeniuk and Dastoor, 2017). In productive regions such as the Southern Ocean, northwestern Pacific, and Mediterranean Sea, significant linear correlations were found between apparent oxygen utilization (AOU) and

Journal Pre-proof MeHgT concentrations (Table A.1; Bowman et al., 2016; Cossa et al., 2009; Cossa et al., 2011; Heimbürger et al., 2010; Kim et al., 2017; Lehnherr et al., 2011; Munson et al., 2015). Organic carbon remineralization rate (OCRR; or its oxygen equivalent, apparent oxygen utilization rate; AOUR), a less frequently explored proxy for microbial respiration that accounts for water mass age, correlated with MeHgT in the north and western Pacific, but not in the central Pacific (Kim et al., 2017; Munson et al., 2015; Sunderland et al., 2009). In less productive regions, such as the

of

oligotrophic North Atlantic and Arctic Oceans, there was no significant correlation between

ro

AOU and MeHgT (Agather et al., 2019; Bowman et al., 2015; Heimbürger et al., 2015). The

-p

Arctic Ocean lacks an OMZ, and AOU is a shelf-advected signal not indicative of in situ

re

respiration (Agather et al., 2019; Heimbürger et al., 2015; Wang et al., 2012; Wang et al., 2018). Proxies for microbial respiration (AOU and OCRR), therefore, are not suitable for all ocean

lP

regions and cannot be the sole factor used to predict oceanic MeHgT concentrations.

na

Depth regions of MeHgT accumulation in the Arctic Ocean are unique to other basins due to ice cover and distinct water column stratification. Shallow subsurface maxima of MeHgT

ur

(100–300 m) were found in Arctic marginal seas (Wang et al., 2012; Wang et al., 2018), and the

Jo

marginal ice zone (MIZ) of the Arctic Ocean where broken first-year ice transitions to solid multi-year ice (Agather et al., 2019; Heimbürger et al., 2015). Ice-covered waters near the central Arctic Ocean had deeper MeHgT maxima between 350–600 m depth (Agather et al., 2019; Heimbürger et al., 2015) despite shoaling of the halocline with increasing latitude from firstyear/MIZ to multi-year ice. Ice-covered waters also had greater concentrations of MMHg near the surface (upper 20 m) compared to open-water stations (Agather et al., 2019). Studies in the Arctic Ocean and Arctic marginal seas agree that isopycnal transport of MeHgT produced over broad continental shelves surrounding the basin is insignificant, and in situ methylation is likely

Journal Pre-proof responsible for MeHgT maxima in the upper water column (Agather et al., 2019; Heimbürger et al., 2015; Lehnherr et al., 2011; Wang et al., 2012; Wang et al., 2018). Remineralization of slowly sinking particles in the shallow halocline, Hg methylation by microbial communities associated with sea ice, and transport of metabolite-enriched shelf water are hypothesized to stimulate MMHg production in the Arctic Ocean (Agather et al., 2019; Heimbürger et al., 2015; Wang et al., 2012; Wang et al., 2018).

of

3.3 Basin-wide distribution of methylated Hg

ro

Concentrations of MeHgT varied regionally across the global ocean with averages of

-p

%MeHgT ranging from 4–19% in subsurface waters (>150 m) and 3–41% in thermocline waters

re

(150–1000 m; Table 1). In the Arctic Ocean %MeHgT was relatively low (<20%) in the upper 1000 m of the water column, unlike the Southern Ocean where %MeHgT averaged 18% in

lP

subsurface waters and 41% in the thermocline (Table 1). Microbial activity in the Southern

na

Ocean is fueled by upwelling of nutrients with Circumpolar Deep Water and a strong correlation between MeHgT and AOU (r2 = 0.722, p < 0.001) suggests in situ methylation by heterotrophic

ur

microorganisms, rather than external inputs are responsible for elevated MeHgT in this region

Jo

(Cossa et al., 2011). Sea ice MeHgT concentrations in the Southern Ocean were enriched compared to underlying seawater, and MeHgT in sea ice and brine correlated with Chla, suggesting sea ice phytoplankton communities play a role in inorganic Hg methylation (Agather et al., 2019; Cossa et al., 2011; DiMento and Mason, 2017; Gionfriddo et al., 2016). There was a striking contrast between %MeHgT in subsurface and thermocline waters of the Atlantic Ocean with lower %MeHgT (~ 4%) in the South compared to the North (~20%) (Table 1). Both trans-Atlantic sections revealed higher concentrations of MeHgT in the western side of the basin, however, there is no significant difference in %MeHgT between the eastern

Journal Pre-proof and western side of both the North and South Atlantic (p = 0.41 and p = 52 respectively, MannWhitney Rank Sum; Bowman et al., 2015; Bratkič et al., 2016). With the exception of upwelling stations, there was less regional variability in the Pacific Ocean and average %MeHgT was ~20% in subsurface and thermocline waters (Table 1). Coastal and equatorial upwelling regions generated higher %MeHgT in the Pacific Ocean (Table 1) compared to adjacent stations (Bowman et al., 2016; Munson et al., 2015), however,

of

%MeHgT was not significantly elevated in the Mauritanian upwelling region in the North

ro

Atlantic (Bowman et al., 2015). Coastal upwelling stations near Peru and Mauritanian had

-p

MMHg and DMHg maxima in the oxycline (<100 m depth) where decreasing oxygen

re

concentrations are driven by heterotrophic microbial respiration (Figure 2; Bowman et al., 2015; Bowman et al., 2016). In the central Pacific equatorial upwelling station, only MMHg was

lP

elevated in the oxycline, perhaps due to evasion of DMHg to the atmosphere (Munson et al.,

na

2015). Deeper in the OMZ, 1–2 maxima of MMHg and DMHg were observed in each upwelling region (Figure 2; Bowman et al., 2015; Bowman et al., 2016; Munson et al., 2015).

ur

The ratio of MMHg:DMHg in the upper 1000 m of the water column was highly variable.

Jo

In the Arctic and Atlantic Oceans, MMHg was the dominant methylated species (Agather et al., 2019; Bowman et al., 2015; Bratkič et al., 2016), but in the Pacific Ocean, concentrations of MMHg and DMHg were often similar (Bowman et al., 2016; Munson et al., 2015). Formation of DMHg has been linked to reduced sulfur compounds in seawater (Jonsson et al., 2016), and MMHg can be methylated to create DMHg (Lehnherr et al., 2011), but overall the interconnectivity of MMHg and DMHg is understudied.

Journal Pre-proof 3.4 Elemental Hg Gaseous Hg0 has a nutrient-type profile in the ocean created by evasion to the atmosphere from surface waters, production in subsurface waters, and accumulation at depth. In the surface ocean, Hg0 is the product of photochemical Hg2+ reduction and MMHg decomposition (Lee and Fisher, 2019; Monperrus et al., 2007; Poulain et al., 2007; Whalin et al., 2007). In the upper water column, production of Hg0 has been associated with microbial density and planktonic

of

biomass (Bratkič et al., 2018; Lee and Fisher, 2019; Mason et al., 1995a; Mason et al., 1995b).

ro

The proportion of total Hg as Hg0 varied spatially throughout the global ocean, but was

-p

similar between subsurface and thermocline waters in each study basin. Elemental Hg

re

represented 9–47% of HgT in subsurface waters (<150 m), and 6–39% in thermocline waters (150–1000 m). The greatest regional variability was found in the North Atlantic Ocean where

lP

%Hg0 was significantly greater in the western basin (p < 0.001, Mann-Whitney Rank Sum;

na

Bowman et al., 2015). Subsurface waters were enriched in Hg0 in the Peru and equatorial upwelling regions of the Pacific Ocean (Bowman et al., 2016; Munson et al., 2015), but not the

ur

Mauritanian upwelling region (Bowman et al., 2015).

Jo

Most studies measure dissolved gaseous Hg (DMG = Hg0 + DMHg) with the assumption that DMHg represents an insignificant proportion of DGM. However, recent work revealed that DMHg is ~20% of DMG in subsurface waters, and 20–60% in thermocline waters (Table A.2; Agather et al., 2019; Bowman et al., 2015; Bowman et al., 2016; Munson et al., 2015). This is significant because, as studies in coastal California found, DMHg evaded from the surface ocean decomposes to MMHg in acidic fog (Coale et al., 2018; Weiss-Penzias et al., 2016; Weiss‐ Penzias et al., 2012). Acidolysis of DMHg in the marine boundary layer may be a source of

Journal Pre-proof MMHg in other coastal environments where wind-driven upwelling is prominent, and could contribute to MMHg found in open-ocean surface waters and precipitation. 4. Hg in the deep ocean Deep water masses acquire Hg from their source regions in the Labrador, Weddell, and Ross Seas, and continue to accumulate Hg from vertical mixing and remineralization of sinking particles during thermohaline circulation. The highest and most variable concentrations of Hg in

of

deep water were found in relatively young Labrador Sea Water (LSW) and Antarctic Bottom

ro

Water (AABW; Figure 3). These high concentrations are attributed to atmospheric deposition of

-p

anthropogenic Hg and enhanced Hg deposition on snow and ice surfaces (i.e. atmospheric

re

mercury depletion events; Cossa et al., 2011; Cossa et al., 2018; Lamborg et al., 2014). Average Hg concentrations in LSW declined ~25% during the past 20 years (Cossa et al.,

lP

2004; Cossa et al., 2018; Mason et al., 1998; Wang et al., 2018), consistent with a decline in

na

atmospheric Hg0 in the North Atlantic troposphere (Cossa et al., 2018; Soerensen et al., 2012). Total Hg varied regionally in LSW measured during 1993–1994 and 2014–2015 (Figure 4).

ur

Similar to the LSW, total Hg in AABW varied regionally with higher concentrations in the

Jo

Weddell Sea (2.1 ± 1.1 pM, n = 36) compared to the Adelie Coast (1.35 ± 0.39 pM, n = 14) measured in 2013 and 2008, respectively (Cossa et al., 2011; Mastromonaco et al., 2017). Circumpolar Deep Water (CDW), a mixture of upwelled deep water from the Atlantic, Pacific, and Indian Oceans, had total Hg concentrations similar to AABW. In the Atlantic, LSW becomes North Atlantic Deep Water (NADW) as it flows south and accumulates Hg. From the Southern Ocean, AABW flows north into the Atlantic and Indian Oceans, and CDW flows north into the Pacific and becomes Pacific Deep Water (PDW; Figure 3).

Journal Pre-proof Nutrient-rich upper CDW shoals to the surface, moving south towards Antarctica, fueling primary productivity and consequently Hg methylation. In the Southern Ocean, CDW had the greatest %MeHgT measured anywhere in the ocean (~50%; Cossa et al., 2011). In the North Atlantic, LSW (~50 years old) had elevated %MeHgT and %Hg0 (Figure 3). Older PDW had lower %MeHgT and %Hg0 compared to relatively younger NADW (Figure 3). This could indicate net oxidative demethylation of MeHgT in aging deep water and a shrinking pool of

of

bioavailable Hg for methylation and reduction.

ro

The ratio of MMHg:DMHg varied throughout the deep ocean. In the North Atlantic and

-p

Arctic Oceans, MMHg was the dominant methylated species while DMHg represented a larger

re

fraction of MeHgT in older deep waters of the Pacific Ocean (Agather et al., 2019; Bowman et al., 2015; Bowman et al., 2016; Munson et al., 2015). In the South Atlantic, MMHg and DMHg

lP

concentrations were similar (Bratkič et al., 2018). Methylation of MMHg proceeds slowly

na

(Lehnherr et al., 2011), but on the timescale of thermohaline circulation (~1000 years) it’s plausible that DMHg is produced from MMHg in aging deep water. With the stability of DMHg

ur

decreasing with pH (Coale et al., 2018), demethylation of DMHg in older, more corrosive deep

Jo

water could contribute to lower %MeHgT in PDW. Greater %Hg0 in LSW likely results from downwelling of surface waters saturated with Hg0 during deep-water formation. Oxidation of Hg0 in aging deep-water decreased %Hg0 from 30–40% in NADW to ~15% in PDW (Figure 3). In the open-ocean, benthic sources of Hg are localized, having little impact on deep water concentrations. Though uncommon, an increase in total Hg and sometimes MMHg near the sediment-water interface was observed in the Arctic, Atlantic, and Pacific Oceans (Agather et al., 2019; Bowman et al., 2015; Bowman et al., 2016; Bratkič et al., 2018; Mason and Sullivan, 1999). Deep-sea hydrothermal fluids were enriched with total Hg (15–11,000 pM) and MMHg

Journal Pre-proof (4–16 pM) in the northeast Pacific, though transport of Hg away from vents within buoyant plumes is understudied (Crepo-Medina et al., 2009; Lamborg et al., 2006). Over the Mid Atlantic Ridge in the North Atlantic Ocean, a buoyant plume extending from the TAG hydrothermal vent field had 10× higher dissolved total Hg concentrations than surrounding deep water with an average of 42 ± 24% as MMHg (Bowman et al., 2015). However, at the East Pacific Rise in the South Pacific, Hg enrichment was absent in a buoyant metal-rich plume that carried dissolved

of

iron, aluminum, and manganese 4000 km west from the rise (Bowman et al., 2016; Resing et al.,

ro

2015). Metal oxides and sulfur released from the vent could scavenge and mineralize excess Hg

-p

released from the vent preventing long-range transport. Though hydrothermal vents may

re

represent a small source of Hg to deep water masses, they are a significant localized source of Hg to benthic food webs (Martins et al., 2006; Martins et al., 2001).

lP

5. Internal cycling of Hg in the ocean

na

5.1 Particulate scavenging and burial

Removal to marine sediments is the long-term sink for Hg in Earth’s active reservoirs

ur

(e.g., Amos et al., 2013), and this process is made possible by Hg associations with ocean

Jo

particles. How this association arises is not well understood, but likely includes sorption to various non-living phases of particles and cell surfaces, and uptake into living organisms and several resulting fates. In general, particulate Hg phases represent a small fraction of all Hg in the open ocean, but can represent the majority in coastal and freshwater settings (Fitzgerald et al., 2007). When particulate Hg concentrations are combined with particulate mass data, the apparent distribution coefficient, or Kd, value is between 105.4 to 107.6 liters per kilogram (Lamborg et al., 2016). These values can rival that of quintessentially “sticky” metals like thorium, but particle

Journal Pre-proof concentrations in the ocean are generally so low that the amount of Hg therefore associated with particles also remains low. Through examination of GEOTRACES data, we recently reported that Kd values are fairly uniform vertically (away from bottom nepheloid layers) and horizontally in the North Atlantic Ocean, though samples came from a range of ocean productivities and particle concentrations (Lamborg et al., 2016). The rate of removal and burial of Hg associated with particles is currently estimated at 3

of

Mmoles per year, which would imply a residence time with respect to this process occurring in

ro

the deep ocean of about 500 years (Outridge et al., 2018). Such a residence time is seemingly

-p

inconsistent with the observation that Hg in the deep ocean is macronutrient-like in its

re

distribution. This would require a residence time in the deep ocean, with respect to scavenging and burial, of a few thousand years at a minimum. A resolution to this seeming discrepancy

lP

requires Hg associated with particles in the deep ocean sink very slowly (<5 m per year) and that

na

most of the Hg buried in deep ocean sediments became associated with particles in the surface, and is thus part of the small proportion of surface productivity that reaches the ocean floor via

ur

the biological pump. Our recent first-order modeling suggests that Hg partitioning between

Jo

solution and solid phases, the Kd value mentioned above, is best explained not by an equilibriumlike reaction where Hg is free to move back and forth between the phases, but by a process that has been described as “regenerative scavenging” (John and Conway, 2014). In this mechanism, Hg becomes associated with particles in the surface through uptake, but does not leave the particle phase until that material has been remineralized by the action of marine heterotrophs. Some fraction the Hg forced back into solution in this way is then re-scavenged by particles in deeper water, probably through simple sorption, but then sinks very slowly.

Journal Pre-proof 5.2 Microbial controls on Hg speciation in the ocean The distribution of MMHg and Hg0 in the ocean suggests that microorganisms play a key role in the chemical cycling of Hg, however, the specific organisms and reactions involved in Hg methylation and reduction in seawater are poorly understood. Microbial reduction of Hg2+ can be facilitated by the mer operon, a suite of genes that, when activated, shuttle Hg into the cytoplasm where mercuric reductase enzyme (MerA) catalyzes Hg0 production. Reductive demethylation of

of

MMHg (yielding Hg0) can also be mediated by genes of the mer operon (i.e. merE and merB)

ro

(Boyd and Barkay, 2012). Expression of merA is associated with high (> 50 pM) Hg

-p

concentrations (Morel et al., 1998), however, merA transcripts have been found in microbial

re

mats from an Arctic coastal lagoon at seawater Hg concentrations ~10 pM (Poulain et al., 2007), and mer genes have been identified in the Arctic basin at Hg concentrations < 1 pM (Bowman et

lP

al. in press). Laboratory incubations of bacterioplankton possessing merA from the Atlantic

na

Ocean produced Hg0 at Hg concentrations as low as 5 pM (Lee and Fisher, 2019), though gene transcription was not measured.

ur

Expression of mer genes at open-ocean Hg concentrations (~1 pM) has not been tested,

Jo

and unidentified microbial pathways to Hg reduction that do not involve mer genes likely exist. For example, growth rates of cultured purple non-sulphur bacteria increased with addition of Hg2+, which was used as an electron sink under redox stress, increasing Hg0 concentrations during phototrophic growth (Grégoire and Poulain, 2016). Elevated Hg0 also coincided with denitrification at some stations in the South Pacific Ocean (Bowman et al., 2016; Munson et al., 2015). Methylation studies using enriched Hg isotopes found that Hg methylation and MMHg demethylation occur simultaneously in seawater through both abiotic and biotic pathways

Journal Pre-proof (Lehnherr et al., 2011; Monperrus et al., 2007; Munson et al., 2018). In the Pacific Ocean, significant quantities of 202Hg2+ were methylated instantaneously and filtered water (0.2 μm to remove cells) had higher methylation rates than unfiltered water (Munson et al., 2018). Rapid (<30 minutes) methylation of 202Hg2+ was also observed in the Arctic Ocean. The authors hypothesized that abiotic or extracellular methylation occurs in the central Pacific Ocean (Munson et al., 2018). Biotic methylation in anoxic environments is controlled by the hgcAB

of

gene cluster (Parks et al., 2013), which is present in Hg-methylating organisms including iron-

ro

and sulfate-reducing bacteria, and methanogens (Gilmour et al., 2018; Gilmour et al., 2013).

-p

HgcA has been found in marine sediments, but only homologs of hgcA (hgcA-like genes) have

re

been identified, at low abundance, in the Pacific Ocean and Antarctic sea ice (Gionfriddo et al., 2016; Podar et al., 2015). The methylation capacity of hgcA-like genes and their importance to

lP

marine Hg methylation is unknown (Bowman et al., in press; Gionfriddo et al., 2016; Podar et

na

al., 2015). If the hgcAB gene cluster has any control over Hg methylation in the water column, the only plausible pathway would be through anoxic microenvironments of sinking particles

ur

(Bianchi et al., 2018), shown in laboratory studies to be sites of Hg methylation (Ortiz et al.,

Jo

2015). 6. Future directions

Modeling global ocean Hg has taken many forms and has been enormously useful in testing the consistency of field and laboratory data, formulating and testing hypotheses, and highlighting gaps in understanding. For example, relatively simple box models have been used to examine the Hg cycle’s sensitivity to sources and sinks, to infer rate laws for Hg species transformations, and to reconstruct and predict changes in the cycle in the past and future (Amos et al., 2014; Amos et al., 2013; Amos et al., 2015; Archer and Blum, 2018; Kim et al., 2017;

Journal Pre-proof Mason et al., 1994; Semeniuk and Dastoor, 2017). Mercury biogeochemistry has also been incorporated into medium- and high-resolution global circulation models that allow regional differences to be examined (Selin et al., 2008; Zhang et al., 2014). Where these models have notably struggled is in accurately re-creating the distributions of methylated Hg species. This is perhaps not surprising as much of the underlying biogeochemistry of the formation and destruction of these forms is not understood at all, not to mention in a way that could be

of

parameterized for inclusion in a model. Progress is being made, however, in the topics of

ro

conversion rates (Lehnherr et al., 2011; Monperrus et al. 2007; Munson et al., 2018), potential

-p

mechanisms (Jonsson et al., 2016) and dependencies to microbial genomics (Bowman et al., in

re

press; Gionfriddo et al., 2016; Podar et al., 2015). The success of future modeling efforts for methylated Hg relies on continued intercalibration efforts within the international community

lP

and development of temporal datasets to examine the seasonality of Hg methylation in the ocean.

na

7. Acknowledgements

This paper is part of a virtual special issue on advances in Hg research. We thank our

ur

GEOTRACES collaborators Chad Hammerschmidt and Rob Mason, as well as Fei Wang and

Jo

Lars-Eric Heimbürger who contributed data. Thank you to the U.S. and International GEOTRACES programs and administrators. The research of the Lamborg, Hammerschmidt, and Mason laboratories has been supported by the U.S. National Science Foundation (Chemical Oceanography).

Journal Pre-proof References

Jo

ur

na

lP

re

-p

ro

of

Agather AM, Bowman KL, Lamborg CH, Hammerschmidt CR. Distribution of mercury species in the Western Arctic Ocean (US GEOTRACES GN01). Marine Chemistry 2019: 103686. Amos HM, Jacob DJ, Kocman D, Horowitz HM, Zhang Y, Dutkiewicz S, et al. Global biogeochemical implications of mercury discharges from rivers and sediment burial. Environmental science & technology 2014; 48: 9514-9522. Amos HM, Jacob DJ, Streets DG, Sunderland EM. Legacy impacts of all-time anthropogenic emissions on the global mercury cycle. Global Biogeochemical Cycles 2013: 410-421. Amos HM, Sonke JE, Obrist D, Robins N, Hagan N, Horowitz HM, et al. Observational and Modeling Constraints on Global Anthropogenic Enrichment of Mercury. Environmental Science & Technology 2015; 49: 4036-4047. Andersson ME, Sommar J, Gardfeldt K, Jutterstrom S. Air-sea exchange of volatile mercury in the North Atlantic Ocean. Marine Chemistry 2011; 125: 1-7. Archer DE, Blum JD. A model of mercury cycling and isotopic fractionation in the ocean. Biogeosciences 2018; 15: 6297. Baya PA, Hollinsworth JL, Hintelmann H. Evaluation and optimization of solid adsorbents for the sampling of gaseous methylated mercury species. Analytica chimica acta 2013; 786: 61-69. Bianchi D, Weber TS, Kiko R, Deutsch C. Global niche of marine anaerobic metabolisms expanded by particle microenvironments. Nature Geoscience 2018; 11: 263. Black FJ, Paytan A, Knee KL, De Sieyes NR, Ganguli PM, Gray E, et al. Submarine groundwater discharge of total mercury and monomethylmercury to central California coastal waters. Environmental science & technology 2009; 43: 5652-5659. Bloom NS, Crecelius EA. Determination of mercury in seawater at sub-nanogram per liter levels. Marine Chemistry 1983; 14: 49-59. Bone SE, Charette MA, Lamborg CH, Gonneea ME. Has submarine groundwater discharge been overlooked as a source of mercury to coastal waters? Environmental science & technology 2007; 41: 3090-3095. Bowman K, Hammerschmidt CR. Extraction of monomethylmercury from seawater for lowfemtomolar determination. Limnology and Oceanography-Methods 2011; 9: 121-128. Bowman KL, Collins E, Agather A, Lamborg CH, Hammerschmidt CR, Kaul D, et al. Distribution of mercury-cycling genes in the Arctic and Equatorial Pacific Oceans and their relationship to mercury speciation. Limnology and Oceanography in press. Bowman KL, Hammerschmidt CR, Lamborg CH, Swarr G. Mercury in the North Atlantic Ocean: The U.S. GEOTRACES zonal and meridional sections. Deep Sea Research Part II: Topical Studies in Oceanography 2015; 116: 251-261. Bowman KL, Hammerschmidt CR, Lamborg CH, Swarr GJ, Agather AM. Distribution of mercury species across a zonal section of the eastern tropical South Pacific Ocean (US GEOTRACES GP16). Marine Chemistry 2016; 186: 156-166. Boyd E, Barkay T. The mercury resistance operon: from an origin in a geothermal environment to an efficient detoxification machine. Frontiers in microbiology 2012; 3: 349. Bratkič A, Tinta T, Koron N, Guevara SR, Begu E, Barkay T, et al. Mercury transformations in a coastal water column (Gulf of Trieste, northern Adriatic Sea). Marine Chemistry 2018; 200: 57-67.

Journal Pre-proof

Jo

ur

na

lP

re

-p

ro

of

Bratkič A, Vahčič M, Kotnik J, Obu Vazner K, Begu E, Woodward EMS, et al. Mercury presence and speciation in the South Atlantic Ocean along the 40° S transect. 2016; 30: 105-119. Buck CS, Hammerschmidt CR, Bowman KL, Gill GA, Landing WM. Flux of total mercury and methylmercury to the northern Gulf of Mexico from US estuaries. Environmental science & technology 2015; 49: 13992-13999. Coale K, Heim W, Negrey J, Weiss-Penzias P, Fernandez D, Olson A, et al. The distribution and speciation of mercury in the California current: Implications for mercury transport via fog to land. Deep Sea Research Part II: Topical Studies in Oceanography 2018; 151: 77-88. Conaway CH, Black FJ, Weiss-Penzias P, Gault-Ringold M, Flegal AR. Mercury speciation in Pacific coastal rainwater, Monterey Bay, California. Atmospheric Environment 2010; 44: 1788-1797. Cossa D, Averty B, Pirrone N. The origin of methylmercury in open Mediterranean waters. Limnology and Oceanography 2009; 54: 837-844. Cossa D, Cotté-Krief M-H, Mason RP, Bretaudeau-Sanjuan JJMC. Total mercury in the water column near the shelf edge of the European continental margin. 2004; 90: 21-29. Cossa D, Heimbürger L-E, Lannuzel D, Rintoul SR, Butler EC, Bowie AR, et al. Mercury in the southern ocean. 2011; 75: 4037-4052. Cossa D, Heimburger L-E, Pérez FF, Garcia-Ibanez MI, Sonke JE, Planquette H, et al. Mercury distribution and transport in the North Atlantic Ocean along the GEOTRACES-GA01 transect. 2018; 15: 2309-2323. Crepo-Medina M, Chatziefthimiou AD, Bloom NS, Luther GWI, Wright DD, Reinfelder JR, et al. Adaptation of chemosynthetic microorganisms to elevated mercury concentrations in deep‐ sea hydrothermal vents. Limnology and Oceanography 2009; 54: 41-49. Cullen JJ. Subsurface chlorophyll maximum layers: enduring enigma or mystery solved? 2015. Cutter G, Casciotti K, Croot P, Geibert W, Heimbürger L-E, Lohan M, et al. Sampling and Sample-handling Protocols for GEOTRACES Cruises. Version 3, August 2017. 2017. DiMento BP, Mason RP. Factors controlling the photochemical degradation of methylmercury in coastal and oceanic waters. Marine chemistry 2017; 196: 116-125. DiMento BP, Mason RP, Brooks S, Moore C. The impact of sea ice on the air-sea exchange of mercury in the Arctic Ocean. Deep Sea Research Part I: Oceanographic Research Papers 2019; 144: 28-38. EPA. Method 1631, Revision E: Mercury in water by oxidation, purge and trap, and cold vapor atomic fluorescence spectrometry. US Environmental Protection Agency Washington, DC 2002. FAO. The state of world fisheries and aquaculture 2018 - Meeting the sustainable development goals. , Rome, 2018. Feng XB, Sommar J, Lindqvist O, Zhu YX. Determination of gaseous divalent mercury in ambient air using KCl coated denuders. Chinese Journal of Analytical Chemistry 2003; 31: 682-685. Fitzgerald WF, Gill GA. Subnanogram determination of mercury by two-stage gold amalgamation and gas phase detection applied to atmospheric analysis. Analytical Chemistry 1979; 51: 1714-1720. Fitzgerald WF, Lamborg CH, Hammerschmidt CR. Marine biogeochemical cycling of mercury. Chemical Reviews 2007; 107: 641-662.

Journal Pre-proof

Jo

ur

na

lP

re

-p

ro

of

Fogg TR, Fitzgerald WF. Mercury in southern New England coastal rains. Journal of Geophysical Research-Oceans and Atmospheres 1979; 84: 6987-6989. Freimann P, Schmidt D. Determination of mercury in seawater by cold vapour atomic absorption spectrophotometry. Fresenius' Zeitschrift für analytische Chemie 1982; 313: 200-202. Ganguli P, Conaway C, Swarzenski P, Izbicki J, Flegal A. Mercury speciation and transport via submarine groundwater discharge at a southern California coastal lagoon system. Environmental science & technology 2012; 46: 1480-1488. Gill GA, Fitzgerald WF. Vertical mercury distributions in the oceans. Geochimica et Cosmochimica Acta 1988; 52: 1719-1728. Gilmour CC, Bullock AL, McBurney A, Podar M, Elias DA. Robust mercury methylation across diverse methanogenic archaea. MBio 2018; 9: e02403-17. Gilmour CC, Podar M, Bullock AL, Graham AM, Brown SD, Somenahally AC, et al. Mercury methylation by novel microorganisms from new environments. Environmental science & technology 2013; 47: 11810-11820. Gionfriddo CM, Tate MT, Wick RR, Schultz MB, Zemla A, Thelen MP, et al. Microbial mercury methylation in Antarctic sea ice. Nature microbiology 2016; 1: 16127. Grégoire D, Poulain A. A physiological role for Hg II during phototrophic growth. Nature Geoscience 2016; 9: 121. Hammerschmidt CR, Bowman KL. Vertical methylmercury distribution in the subtropical North Pacific Ocean. Marine Chemistry 2012; 132: 77-82. Heimbürger L-E, Cossa D, Marty J-C, Migon C, Averty B, Dufour A, et al. Methyl mercury distributions in relation to the presence of nano-and picophytoplankton in an oceanic water column (Ligurian Sea, North-western Mediterranean). Geochimica et Cosmochimica Acta 2010; 74: 5549-5559. Heimbürger L-E, Sonke JE, Cossa D, Point D, Lagane C, Laffont L, et al. Shallow methylmercury production in the marginal sea ice zone of the central Arctic Ocean. 2015; 5: 10318. Horowitz HM, Jacob DJ, Zhang Y, Dibble TS, Slemr F, Amos HM, et al. A new mechanism for atmospheric mercury redox chemistry: implications for the global mercury budget. Atmospheric Chemistry and Physics 2017; 17: 6353-6371. Horvat M, Liang L, Bloom NS. Comparison of Distillation with Other Current Isolation Methods for the Determination of Methyl Mercury-Compounds in Low-Level EnvironmentalSamples. 2. Water. Analytica Chimica Acta 1993; 282: 153-168. John SG, Conway TM. A role for scavenging in the marine biogeochemical cycling of zinc and zinc isotopes. Earth and Planetary Science Letters 2014; 394: 159-167. Jonsson S, Mazrui NM, Mason RP. Dimethylmercury formation mediated by inorganic and organic reduced sulfur surfaces. Scientific reports 2016; 6: 27958. Kim H, Soerensen AL, Hur J, Heimbürger L-E, Hahm D, Rhee TS, et al. Methylmercury mass budgets and distribution characteristics in the Western Pacific Ocean. Environmental science & technology 2017; 51: 1186-1194. Kim J, Fitzgerald W. Gaseous mercury profiles in the tropical Pacific Ocean. Geophysical Research Letters 1988; 15: 40-43. Kim S-A, Kwon Y, Kim S, Joung H. Assessment of dietary mercury intake and blood mercury levels in the Korean population: results from the Korean national environmental health survey 2012–2014. International journal of environmental research and public health 2016; 13: 877.

Journal Pre-proof

Jo

ur

na

lP

re

-p

ro

of

Kuss J, Zülicke C, Pohl C, Schneider B. Atlantic mercury emission determined from continuous analysis of the elemental mercury sea-air concentration difference within transects between 50°N and 50°S. Global Biogeochemical Cycles 2011; 25: GB3021. Lamborg CH, Fitzgerald WF, Skoog A, Visscher PT. The abundance and source of mercurybinding organic ligands in Long Island Sound. Marine Chemistry 2004; 90: 151-163. Lamborg CH, Hammerschmidt CR, Bowman KL. An examination of the role of particles in oceanic mercury cycling. Philosophical Transactions of the Royal Society A: Mathematical, Physical and Engineering Sciences 2016; 374: 20150297. Lamborg CH, Hammerschmidt CR, Bowman KL, Swarr GJ, Munson KM, Ohnemus DC, et al. A global ocean inventory of anthropogenic mercury based on water column measurements. Nature 2014; 512: 65. Lamborg CH, Rolfhus KR, Fitzgerald WF, Kim G. The atmospheric cycling and air-sea exchange of mercury species in the South and equatorial Atlantic Ocean. Deep-Sea Research Part II-Topical Studies in Oceanography 1999; 46: 957-977. Lamborg CH, Von Damm KL, Fitzgerald WF, Hammerschmidt CR, Zierenberg R. Mercury and monomethylmercury in fluids from Sea Cliff submarine hydrothermal field, Gorda Ridge. Geophysical Research Letters 2006; 33. Lavoie RA, Bouffard A, Maranger R, Amyot M. Mercury transport and human exposure from global marine fisheries. Scientific reports 2018; 8: 6705. Lavoie RA, Jardine TD, Chumchal MM, Kidd KA, Campbell LM. Biomagnification of mercury in aquatic food webs: a worldwide meta-analysis. Environmental science & technology 2013; 47: 13385-13394. Lee CS, Fisher NS. Microbial generation of elemental mercury from dissolved methylmercury in seawater. Limnology and Oceanography 2019; 64: 679-693. Lehnherr I, Louis VLS, Hintelmann H, Kirk JL. Methylation of inorganic mercury in polar marine waters. Nature geoscience 2011; 4: 298. Lindberg SE, Stratton WJ. Atmospheric mercury speciation: Concentrations and behavior of reactive gaseous mercury in ambient air. Environmental Science & Technology 1998; 32: 49-57. Lu JYL, Feng X, Hao Y, Banic C, Schroeder WH. Development of a diffusion type of Reactive Gaseous Mercury (RGM) source and evaluation of the RGM collecting efficiency by KCl-coated annular denuders. Journal De Physique IV 2003; 107: 1431-1431. Martins I, Costa V, Porteiro F, Colaço A, Santos R. Mercury concentrations in fish species caught at Mid-Atlantic Ridge hydrothermal vent fields. Marine Ecology Progress Series 2006; 320: 253-258. Martins I, Costa V, Porteiro F, Cravo A, Santos R. Mercury concentrations in invertebrates from Mid-Atlantic Ridge hydrothermal vent fields. Journal of the Marine Biological Association of the United Kingdom 2001; 81: 913-915. Marumoto K, Matsuyama A. Mercury speciation in wet deposition samples collected from a coastal area of Minamata Bay. Atmospheric Environment 2014; 86: 220-227. Mason R, Morel Fa, Hemond H. The role of microorganisms in elemental mercury formation in natural waters. Water, Air, and Soil Pollution 1995b; 80: 775-787. Mason R, Rolfhus K, Fitzgerald W. Methylated and elemental mercury cycling in surface and deep ocean waters of the North Atlantic. Water, Air, and Soil Pollution 1995a; 80: 665677. Mason R, Rolfhus Ka, Fitzgerald WJMC. Mercury in the north Atlantic. 1998; 61: 37-53.

Journal Pre-proof

Jo

ur

na

lP

re

-p

ro

of

Mason Ra, Sullivan KJDSRPITSiO. The distribution and speciation of mercury in the South and equatorial Atlantic. 1999; 46: 937-956. Mason RP, Fitzgerald WF, Morel FMM. The biogeochemical cycling of elemental mercury anthropogenic influences. Geochimica et Cosmochimica Acta 1994; 58: 3191-3198. Mason RP, Fitzgerald WF, Vandal GM. The sources and composition of mercury in Pacific Ocean rain. Journal of Atmospheric Chemistry 1992; 14: 489-500. Mason RP, Hammerschmidt CR, Lamborg CH, Bowman KL, Swarr GJ, Shelley RU. The air-sea exchange of mercury in the low latitude Pacific and Atlantic Oceans. Deep Sea Research Part I: Oceanographic Research Papers 2017; 122: 17-28. Mason RP, Lawson Na, Sheu G-R. Mercury in the Atlantic Ocean: factors controlling air–sea exchange of mercury and its distribution in the upper waters. Deep Sea Research Part II: Topical Studies in Oceanography 2001; 48: 2829-2853. Mason R, Fitzgerald W. Alkylmercury species in the equatorial Pacific. Nature 1990; 347: 457. Mastromonaco MGN, Gårdfeldt K, Assmann KM, Langer S, Delali T, Shlyapnikov YM, et al. Speciation of mercury in the waters of the Weddell, Amundsen and Ross Seas (Southern Ocean). Marine Chemistry 2017; 193: 20-33. Monperrus M, Tessier E, Amouroux D, Leynaert A, Huonnic P, Donard O. Mercury methylation, demethylation and reduction rates in coastal and marine surface waters of the Mediterranean Sea. Marine Chemistry 2007; 107: 49-63. Monperrus M, Tessier E, Veschambre S, Amouroux D, Donard O. Simultaneous speciation of mercury and butyltin compounds in natural waters and snow by propylation and speciesspecific isotope dilution mass spectrometry analysis. Analytical and Bioanalytical Chemistry 2005; 381: 854-862. Morel FM, Kraepiel AM, Amyot M. The chemical cycle and bioaccumulation of mercury. Annual review of ecology and systematics 1998; 29: 543-566. Morton PL, Landing WM, Hsu SC, Milne A, Aguilar-Islas AM, Baker AR, et al. Methods for the sampling and analysis of marine aerosols: results from the 2008 GEOTRACES aerosol intercalibration experiment. Limnology and Oceanography-Methods 2013; 11: 62-78. Munson K, Babi D, Lamborg CH. Determination of monomethylmercury from seawater with ascorbic acid-assisted direct ethylation. Limnology and Oceanography-Methods 2014; 12: 1-9. Munson KM, Lamborg CH, Boiteau RM, Saito MA. Dynamic mercury methylation and demethylation in oligotrophic marine water. Biogeosciences 2018; 15: 6451-6460. Munson KM, Lamborg CH, Swarr GJ, Saito MA. Mercury species concentrations and fluxes in the Central Tropical Pacific Ocean. Global Biogeochemical Cycles 2015; 29: 656-676. Nightingale PD, Malin G, Law CS, Watson AJ, Liss PS, Liddicoat MI, et al. In situ evaluation of air-sea gas exchange parameterizations using novel conservative and volatile tracers. Global Biogeochemical Cycles 2000; 14: 373-387. Ortiz VL, Mason RP, Ward JE. An examination of the factors influencing mercury and methylmercury particulate distributions, methylation and demethylation rates in laboratory-generated marine snow. Marine chemistry 2015; 177: 753-762. Outridge PM, Mason R, Wang F, Guerrero S, Heimbürger-Boavida L. Updated global and oceanic mercury budgets for the United Nations Global Mercury Assessment 2018. Environmental science & technology 2018; 52: 11466-11477. Parks JM, Johs A, Podar M, Bridou R, Hurt RA, Smith SD, et al. The genetic basis for bacterial mercury methylation. Science 2013; 339: 1332-1335.

Journal Pre-proof

Jo

ur

na

lP

re

-p

ro

of

Podar M, Gilmour CC, Brandt CC, Soren A, Brown SD, Crable BR, et al. Global prevalence and distribution of genes and microorganisms involved in mercury methylation. Science advances 2015; 1: e1500675. Poulain AJ, Chadhain SMN, Ariya PA, Amyot M, Garcia E, Campbell PG, et al. Potential for mercury reduction by microbes in the high arctic. Appl. Environ. Microbiol. 2007; 73: 2230-2238. Resing JA, Sedwick PN, German CR, Jenkins WJ, Moffett JW, Sohst BM, et al. Basin-scale transport of hydrothermal dissolved metals across the South Pacific Ocean. Nature 2015; 523: 200. Selin NE, Jacob DJ, Yantosca RM, Strode S, Jaegle L, Sunderland EM. Global 3-D land-oceanatmosphere model for mercury: Present-day versus preindustrial cycles and anthropogenic enrichment factors for deposition. Global Biogeochemical Cycles 2008; 22: GB2011, doi:10.1029/2007GB003040. Semeniuk K, Dastoor A. Development of a global ocean mercury model with a methylation cycle: Outstanding issues. Global Biogeochemical Cycles 2017; 31: 400-433. Skov H, Brooks SB, Goodsite ME, Lindberg SE, Meyers TP, Landis MS, et al. Fluxes of reactive gaseous mercury measured with a newly developed method using relaxed eddy accumulation. Atmospheric Environment 2006; 40: 5452-5463. Soerensen AL, Jacob DJ, Streets DG, Witt ML, Ebinghaus R, Mason RP, et al. Multi‐ decadal decline of mercury in the North Atlantic atmosphere explained by changing subsurface seawater concentrations. 2012; 39. Soerensen AL, Mason RP, Balcom PH, Jacob DJ, Zhang Y, Kuss J, et al. Elemental mercury concentrations and fluxes in the tropical atmosphere and ocean. Environmental science & technology 2014; 48: 11312-11319. Soerensen AL, Skov H, Jacob DJ, Soerensen BT, Johnson MS. Global Concentrations of Gaseous Elemental Mercury and Reactive Gaseous Mercury in the Marine Boundary Layer. Environmental Science & Technology 2010; 44: 7425-7430. Sonke JE, Teisserenc R, Heimbürger-Boavida L-E, Petrova MV, Marusczak N, Le Dantec T, et al. Eurasian river spring flood observations support net Arctic Ocean mercury export to the atmosphere and Atlantic Ocean. Proceedings of the National Academy of Sciences 2018; 115: E11586-E11594. Stoichev T, Martin-Doimeadios RCR, Amouroux D, Molenat N, Donard OFX. Application of cryofocusing hydride generation and atomic fluorescence detection for dissolved mercury species determination in natural water samples. Journal of Environmental Monitoring 2002; 4: 517-521. Streets DG, Horowitz HM, Jacob DJ, Lu Z, Levin L, Ter Schure AF, et al. Total mercury released to the environment by human activities. Environmental science & technology 2017; 51: 5969-5977. Sunderland EM, Krabbenhoft DP, Moreau JW, Strode SA, Landing WM. Mercury sources, distribution, and bioavailability in the North Pacific Ocean: Insights from data and models. Global Biogeochemical Cycles 2009; 23. Sunderland EM, Li M, Bullard K. Decadal changes in the edible supply of seafood and methylmercury exposure in the United States. Environmental health perspectives 2018; 126: 017006.

Journal Pre-proof

Jo

ur

na

lP

re

-p

ro

of

Wang F, Macdonald RW, Armstrong DA, Stern GA. Total and methylated mercury in the Beaufort Sea: The role of local and recent organic remineralization. Environmental science & technology 2012; 46: 11821-11828. Wang K, Munson KM, Beaupré-Laperrière A, Mucci A, Macdonald RW, Wang FJSr. Subsurface seawater methylmercury maximum explains biotic mercury concentrations in the Canadian Arctic. 2018; 8: 14465. Weiss-Penzias P, Coale K, Heim W, Fernandez D, Oliphant A, Dodge C, et al. Total-and monomethyl-mercury and major ions in coastal California fog water: Results from two years of sampling on land and at sea. Elementa: Science of the Anthropocene 2016; 4. Weiss‐ Penzias PS, Ortiz C, Acosta RP, Heim W, Ryan JP, Fernandez D, et al. Total and monomethyl mercury in fog water from the central California coast. Geophysical Research Letters 2012; 39. Whalin L, Kim E-H, Mason R. Factors influencing the oxidation, reduction, methylation and demethylation of mercury species in coastal waters. Marine Chemistry 2007; 107: 278294. Zhang YX, Jaegle L, Thompson L, Streets DG. Six centuries of changing oceanic mercury. Global Biogeochemical Cycles 2014; 28: 1251-1261. Živković I, Fajon V, Tulasi D, Vazner KO, Horvat M. Optimization and measurement uncertainty estimation of hydride generation–cryogenic trapping–gas chromatography– cold vapor atomic fluorescence spectrometry for the determination of methylmercury in seawater. Marine Chemistry 2017; 193: 3-7.

Journal Pre-proof Table 1. Concentrations of total Hg and the proportion of total Hg as methylated Hg (%MeHgT) and gaseous elemental Hg (%Hg0) in the upper 1000 meters of the ocean. Data includes both filtered and unfiltered samples. Total Hg (pM) <150 m >150–1000 m

%Hg0

%MeHgT

Study region <150 m >150–1000 m <150 m >150–1000 m Arctic Ocean Western Arctica 1.1 ± 0.42 (n = 103) 0.71 ± 0.30 (n = 95) 7 ± 6 (n = 74) 14 ± 10 (n = 70) 23 ± 21 (n = 100) 24 ± 25 (n = 91) Central Arcticb 1.3 ± 1.3 (n = 23) 0.81 ± 0.24 (n = 31) 10 ± 9 (n = 18) 18 ± 11 (n = 31) Canadian Arcticc 15 ± 13 (n = 101) 19 ± 11 (n = 65) Atlantic Ocean North Atlanticd 0.69 ± 0.39 (n = 155) 0.96 ± 0.34 (n = 255) 19 ± 18 (n = 61) 23 ± 16 (n = 98) 25 ± 14 (n = 146) 39 ± 15 (n = 234) South Atlantice 1.3 ± 0.62 (n = 132) 1.4 ± 0.66 (n = 93) 4 ± 3 (n = 38) 3 ± 1 (n = 31) Pacific Ocean Northeast Pacificf 0.99 ± 0.32 (n = 48) 1.35 ± 0.37 (n = 32) 10 ± 5 (n = 48) 19 ± 6 (n = 32) Northeast Pacificg 0.36 ± 0.10 (n = 5) 0.74 ± 0.17 (n = 10) 6 ± 2 (n = 6) 7 ± 3 (n = 10) Central North Pacifich 0.47 ± 0.36 (n = 19) 1.1 ± 0.29 (n = 19) 15 ± 8 (n = 7) 19 ± 7 (n = 7) 47 ± 34 (n = 7) 17 ± 12 (n = 19) Equatorial Pacifich 0.45 ± 0.31 (n = 7) 0.93 ± 0.23 (n = 25) 19 ± 7 (n = 7) 15 ± 5 (n = 25) 36 ± 15 (n = 7) 12 ± 14 (n = 32) Central South Pacifich -0.61 ± 0.19 (n = 21) -11 ± 3 (n = 21) -18 ± 16 (n = 66) Peru upwelling regioni 0.69 ± 0.62 (n = 67) 0.88 ± 0.45 (n = 112) 22 ± 23 (n = 60) 26 ± 15 (n = 109) 13 ± 12 (n = 67) 8 ± 9 (n = 112) Eastern tropical Pacifici 0.19 ± 0.065 (n = 91) 0.59 ± 0.25 (n = 144) 14 ± 21 (n = 27) 17 ± 16 (n = 62) 9 ± 9 (n = 87) 6 ± 10 (n = 137) Southern Ocean 140o–150o Eastj 18 ± 22 (n = 15) 41 ± 20 (n = 24) Agather et al. 2019a; Heimbürger et al. 2015b; Wang et al. 2018c; Bowman et al. 2015 d; Bratkič, et al. 2016e; Sunderland et al. 2011 f; Hammerschmidt & Bowman, 2012 g; Munson et al. 2015 h; Bowman et al. 2016 i; Cossa et al., 2011 j

f o

l a

Jo

n r u

r P

e

o r p

Journal Pre-proof

Figure 1. Ocean transects where published Hg data is available. Full depth Hg speciation data is available at stations outlined in yellow boxes. Stations with only surface ocean dissolved gasoues Hg data are not plotted. Figure 2. Methylated Hg in upwelling regions. Vertical profiles for filtered monomethyl-Hg (MMHg), dimethyl-Hg (DMHg), and filtered total methylated Hg (MeHgT) in upwelling regions of the central Pacific (Munson et al. 2015), eastern North Atlantic (Bowman et al. 2015), and tropical South Pacific (Bowman et al. 2016).

re

-p

ro

of

Figure 3. Mercury in deep water masses. Total Hg (HgT) and the proportion of Hg as methylated Hg (%MeHgT) and elemental Hg (%Hg0) in Labrador Sea Water (LSW), Canada Basin Deep Water (CBDW), North Atlantic Deep Water (NADW), Antarctic Bottom Water (AABW), Circumpolar Deep Water (CDW), and Pacific Deep Water (PDW). Data includes both filtered and unfiltered data from the subpolar North Atlantic and Labrador Sea (Cossa, et al. 2018; Cossa, et al. 2004; Mason, et al. 1998; Wang, et al. 2018), western Arctic (Agather 2019), Atlantic (Bowman, et al. 2015; Bratkič, et al. 2016; Pohl, et al. 2011), Southern (Cossa, et al. 2011; Mastromonaco, et al. 2017), and Pacific Oceans (Bowman, et al. 2016; Laurier, et al. 2004; Munson, et al. 2015).

Jo

ur

na

lP

Figure 4. Temporal and regional variability of total Hg in Labrador Sea Water. Total Hg in Labrador Sea Water measured in the subpolar North Altantic Ocean (1993 unfiltered seawater, Mason et al. 1998), European continental margin (1994 filtered seawater, Cossa et al. 2004), eastern Labrador Sea (2014 unfiltered seawater, Cossa et al. 2018b), and western Labrador Sea (2015 unfiltered seawater, Wang et al. 2018).

Journal Pre-proof

Conflict of interest

Jo

ur

na

lP

re

-p

ro

of

We have no conflict of interests to report.

Journal Pre-proof

Highlights Mercury, a ubiquitous metal in the ocean, accumulates in marine fish and mammals



30 years of marine mercury data are synthesized



Distribution of Hg is unique in polar seas



Max. methylated Hg in surface waters associated with low-oxygen thermocline waters



Global scale models require a better understanding of biogeochemical controls

Jo

ur

na

lP

re

-p

ro

of



Figure 1

Figure 2

Figure 3

Figure 4