Geochemical Factors Controlling Dissolved Elemental Mercury and

4 days ago - U.S. Geological Survey, Boulder , Colorado 80303 , United States. ‡ Department of Civil, Environmental, and Architectural Engineering, ...
0 downloads 0 Views 2MB Size
Download PDF
Article Cite This: Environ. Sci. Technol. XXXX, XXX, XXX−XXX

pubs.acs.org/est

Geochemical Factors Controlling Dissolved Elemental Mercury and Methylmercury Formation in Alaskan Wetlands of Varying Trophic Status Brett A. Poulin,*,†,‡ Joseph N. Ryan,‡ Michael T. Tate,§ David P. Krabbenhoft,§ Mark E. Hines,∥,$ Tamar Barkay,⊥ Jeffra Schaefer,# and George R. Aiken†,$ †

U.S. Geological Survey, Boulder, Colorado 80303, United States Department of Civil, Environmental, and Architectural Engineering, University of Colorado Boulder, Boulder, Colorado 80309, United States § U.S. Geological Survey, Middleton, Wisconsin 53562, United States ∥ Department of Biological Sciences, University of Massachusetts Lowell, Lowell, Massachusetts 01854, United States ⊥ Department of Biochemistry and Microbiology, Rutgers University, New Brunswick, New Jersey 08901, United States # Department of Environmental Sciences, Rutgers University, New Brunswick, New Jersey 08901, United States

Environ. Sci. Technol. Downloaded from pubs.acs.org by UNIV OF ROCHESTER on 05/16/19. For personal use only.

‡

S Supporting Information *

ABSTRACT: The transformations of aqueous inorganic divalent mercury (Hg(II)i) to volatile dissolved gaseous mercury (Hg(0)(aq)) and toxic methylmercury (MeHg) govern mercury bioavailability and fate in northern ecosystems. This study quantified concentrations of aqueous mercury species (Hg(II)i, Hg(0)(aq), MeHg) and relevant geochemical constituents in pore waters of eight Alaskan wetlands that differ in trophic status (i.e., bog-to-fen gradient) to gain insight on processes controlling dark Hg(II)i reduction and Hg(II)i methylation. Regardless of wetland trophic status, positive correlations were observed between pore water Hg(II)i and dissolved organic carbon (DOC) concentrations. The concentration ratio of Hg(0)(aq) to Hg(II)i exhibited an inverse relationship to Hg(II)i concentration. A ubiquitous pathway for Hg(0)(aq) formation was not identified based on geochemical data, but we surmise that dissolved organic matter (DOM) influences mercury retention in wetland pore waters by complexing Hg(II)i and decreasing the concentration of volatile Hg(0)(aq) relative to Hg(II)i. There was no evidence of Hg(0)(aq) abundance directly limiting mercury methylation. The concentration of MeHg relative to Hg(II)i was greatest in wetlands of intermediate trophic status, and geochemical data suggest mercury methylation pathways vary between wetlands. Our insights on geochemical factors influencing aqueous mercury speciation should be considered in context of the long-term fate of mercury in northern wetlands.

■

surface connectivity)15,16 that modulates the availability of terminal electron acceptors (e.g., sulfate) and availability of DOM as an electron source to heterotrophic methylating microorganisms.11,17,18 The dynamic competition between Hg(II)i reduction to Hg(0)(aq) and methylation to MeHg as a function of wetland trophic status is unknown. It is unclear if Hg(0)(aq) formation occurs through dark biotic19−21 or abiotic Hg(II)i reduction pathways22−24 or if Hg(0)(aq) formation directly20,25,26 or indirectly7,24,27 limits MeHg formation at the environmental level.

INTRODUCTION The cycling of mercury in northern ecosystems has implications for human and environmental health.1 Northern freshwater wetlands receive inorganic mercury from atmospheric deposition and plant uptake of primarily gaseous elemental mercury (Hg(0)(g)),2−4 which is oxidized to inorganic divalent mercury (Hg(II)i).3,5 The atmospheric re-emission of mercury is controlled by photoreduction of Hg(II)i to Hg(0)(g) at the peat surface6 and dark reduction of Hg(II)i to volatile dissolved gaseous mercury (Hg(0)(aq)) in pore waters containing dissolved organic matter (DOM).7,8 Anoxic pore waters of wetlands are also important locations for conversion of Hg(II)i to bioavailable methylmercury (MeHg),9−12 which can be hydrologically mobilized downstream.11,13,14 Mercury methylation is influenced by wetland trophic status, a property governed by hydrologic factors (e.g., groundwater contributions, © XXXX American Chemical Society

Received: October 26, 2018 Revised: February 22, 2019 Accepted: May 6, 2019

A

DOI: 10.1021/acs.est.8b06041 Environ. Sci. Technol. XXXX, XXX, XXX−XXX

Article

Environmental Science & Technology Table 1. Properties of Sampled Wetlands in Interior and Southcentral Alaskaf Location

ID

Tentative Wetland Type

Eightmile bogb,c,d

EB

Bog

Goldstream bogb,e

GB

Bog

Black Spruce bogb,e

BSB

Bog

Twin Lakes poor fene

TLPF

Poor Fen

Sheep Creek fenb,e

SCF

Poor Fen

Ballaine fenb,e Twin Lakes rich fene

BF TLRF

Poor Fen Rich Fen

Frozen Pond fenb,d

FPF

Rich Fen

2016 # of PW samples

Range in PW pH

6

3.9−4.2

1

7

3.7−4.2

W147.83571

6

6

3.7−5.1

N61.16025

W149.74605

5

N64.90963

W147.94514

4

N64.87000 N61.16095

W147.82800 W149.74300

2 6

N64.91417

W147.83487

6

Dominant Vegetationa Sphagnum sp. Carex sp. Eriophorum sp. Sphagnum riparium Eriophorum vaginatum Sphagnum rubrum Sphagnum fuscum Sphagnum angustifolium Eriophorum vaginatum Sphagnum squarrosum Sphagnum angustifolium Carex aquatilis Sphagnum squarrosum Carex aquatilis Carex canescens Menyanthes trifoliata Calliergon sp. Scorpidium revolvens Carex aquatalis

Latitude

Longitude

N63.87856

W149.25887

N64.91237

W147.83903

N64.91494

2015 # of PW samples

4.9−5.1

6

5.2−5.6

5.3−5.5 5.7−6.0

12

5.1−7.1

a

Plant species with coverage >25% of sampling location49 arranged in order of abundance. bUnderlaid by permafrost. cSpecies-level identification of vegetation not available. dWater table above peat surface at the time of sampling. eWater table below peat surface at the time of sampling. f Tabulated properties include the name, identification abbreviation (ID), wetland type, dominant vegetation, latitude, longitude, the number of pore water (PW) samples collected in 2015 and 2016, and range in pore water pH.

primarily attributed to sulfate-reducing bacteria at locations of sulfate inputs, most notably from groundwater contributions.10,13,17 However, MeHg formation by other microbial guilds (e.g., metal-reducing bacteria, methanogens) across wetland trophic gradients is supported by field methylation experiments using guild-specific inhibitors,17,38 evidence of hgcA gene expression in both bacteria and methanogens in northern soils,39 and knowledge of cometabolic interactions (i.e., syntropy) enhancing methylation in laboratory coculture.40 Geochemical factors also influence the availability of Hg(II)i for methylation. Numerous studies propose that Hg(0) (aq) formation may limit methylation,7,20,24,26,27 in part, due to the necessary oxidation of Hg(0)(aq) to Hg(II)i prior to methylation.26 Inorganic dissolved sulfide limits Hg(II)i methylation by bacteria41 and archea42 via formation of nanoparticulate mercuric sulfide (β-HgS) that limits Hg(II)i bioavailability.43,44 DOM composition influences the bioavailability of Hg(II)i associated with nanoparticulate β-HgS to methylation by decreasing the size or crystalline order of nanoparticulate βHgS.45 Forecasting the fate of mercury in northern wetlands necessitates an understanding of the interplay between factors controlling Hg(II)i reduction and methylation, particularly given projections of increased hydrologic connectivity and shifts in wetland trophic status in response to a warming climate.36,46,47 Here, the geochemical factors controlling the concentrations of Hg(II)i, Hg(0)(aq), and MeHg were studied across Alaskan wetlands of varying trophic status. Pore waters were analyzed for a suite of geochemical conditions and constituents from eight Alaskan wetlands ranging from ombrotrophic bogs to minerotrophic fens. We report the first effort to link the

Interactions between mercury and DOM are hypothesized to influence the distribution of Hg(II)i and Hg(0)(aq). DOM forms strong complexes with Hg(II)i that dominate aqueous mercury speciation under nonsulfidic conditions28,29 and limit the reduction of Hg(II)i to Hg(0)(aq).23,24 DOM can also facilitate Hg(II)i reduction22 and Hg(0)(aq) oxidation; the latter is favored when DOM is in a reduced state.23,24 In a northern bog, pore water Hg(0)(aq) concentration coincided with Hg(0)(g) evasion rates and net mercury efflux, and the formation of Hg(0)(aq) was attributed to dark reduction of Hg(II)i by DOM.7 In wetlands of varied trophic status, the balance between DOM promoting or inhibiting Hg(0)(aq) formation may differ due to shifts in DOM concentration, composition,30,31 and electron exchange capacity.32 The pore waters of ombrotrophic bogs (pH < 4.2) accumulate DOM of high aromatic30,31,33 and redox-active quality32 from the leaching of Sphagnum mosses and inhibition of enzymatic degradation of DOM by phenol oxidases under anoxic conditions.34,35 Fens vary in trophic status (poor fens < rich fen), pore water pH (from 4.2 to 7.0), and vegetation due to differences in the degree of minerotrophic groundwater contribution relative to precipitation. Fens are sites for the processing and mineralization of DOM;30,36,37 they tend to contain DOM of lower aromaticity30,36 and electron exchange capacity than bogs.32 The ability of DOM to provide electrons to heterotrophs could influence dark biotic Hg(0)(aq) formation by metal-reducing19,20 and fermentative bacteria.21 Questions remain on the factors influencing dark Hg(0)(aq) formation in anoxic wetlands and the relative importance of Hg(0)(aq) in mercury cycling in northern environments. MeHg formation in northern wetlands is influenced by both microbial and geochemical factors. Mercury methylation is B

DOI: 10.1021/acs.est.8b06041 Environ. Sci. Technol. XXXX, XXX, XXX−XXX

Article

Environmental Science & Technology

ion-selective electrode. Major cation composition (Ca, Mg, Mn, Fe, Na) was determined by inductively coupled plasma-optical emission spectrometry. Inorganic anions (Cl−, NO3−, SO42−) and simple organic acids (acetate, formate, butyrate, propanoate, oxalate; only performed in 2016) were quantified by ion chromatography. Total iron and Fe(II) were quantified by a ferrozine assay;52 Fe(III) was determined as the difference between total iron and Fe(II). DOC concentration was determined by persulfate oxidation. UV−vis absorption spectra were measured from 190 to 800 nm and decadic absorbance values were converted to absorption coefficients as

geochemical processes controlling Hg(0)(aq) formation in northern wetlands of varied trophic status to the retention and methylation of Hg(II)i.

■

EXPERIMENTAL SECTION Field Locations. Eight wetlands in Interior and Southcentral Alaska spanning a continuum from ombrotrophic bogs to minerotrophic fens were sampled in 2015 (17 July−22 July) and 2016 (12 July−16 July). Wetlands were not influenced by historic mining activities48 and were classified using pore water pH15,16 and plant species.49 Three wetlands were classified as bogs (Eightmile bog (EB), Goldstream bog (GB), Black Spruce bog (BSB); pore water pH < 4.2), three wetlands were classified as poor fens (Twin Lakes poor fen (TLPF), Sheep Creek fen (SCF), Ballaine fen (BF); pH from 4.2 to 5.8), and two wetlands were classified as rich fens (Twin Lakes rich fen (TLRF), Frozen Pond fen (FPF); pH > 5.8).15,16 The sampling sites included five wetlands in Interior Alaska near Fairbanks, one thermokarst wetland near Denali National Park, and two wetlands in Southcentral Alaska near Anchorage (Table 1; Figure S1 in the Supporting Information (SI)). Table 1 provides information on the wetlands (names, identification abbreviations, wetland type, dominant vegetation,49 latitudes and longitudes, and pore water pH range). The wetlands near Fairbanks (GB, BSB, SCF, BF, FPF) and one of the wetlands near Anchorage (EB) were underlain by permafrost. For the wetlands near Fairbanks sampled in both 2015 and 2016, a comparison of air temperature and cumulative precipitation between sampling years is provided in the SI (SI Figures S2 and S3).50 The water table was below the peat surface in six wetlands and above the peat surface in Frozen Pond fen and Eightmile bog. Pore Water Sampling. A complete account of pore water sampling procedures is provided in the SI. A Teflon sipper and peristaltic pump were used to collect shallow (10−15 cm below water table) and deep (20−35 cm below water table) pore waters. For wetlands underlain by permafrost, pore water sampling depths targeted the thawed, water-saturated active layer at the time of sampling. For most wetlands, shallow and deep pore water samples were collected at three sublocations separated laterally by approximately 2 m. At each location, pore water temperature, conductivity, pH, dissolved oxygen (DO) concentration, and oxidation−reduction potential (ORP) were measured using a flow-through cell and multiparameter meters. Next, pore waters were filtered directly into vessels using a 0.45 μm disk filter (Aquaprep 50 mm, Pall Corporation) or a quartz fiber filter (precombusted; Whatman) for the two respective sets of analyses: (1) major cations, inorganic anions, simple organic acids, inorganic dissolved sulfide, iron oxidation state, dissolved organic carbon (DOC), ultraviolet and visible light (UV−vis) absorption, DOM fluorescence, and measurement of electron release from DOM and Fe(II) and (2) filter-passing total mercury (HgT) and MeHg. The abiotic reduction of Hg(II)i to Hg(0)(aq) by DOM and Fe(II)24,51 was evaluated by measuring the release of electrons from pore waters on samples collected by filling vessels from the bottom and leaving no headspace to preserve pore water redox state. For Hg(0)(aq) quantification, unfiltered pore water (approximately 750 mL) was collected directly into 1 L gas-wash bottles with minimal agitation and bottles were immediately capped with Teflon plugs and stored in the dark at ambient temperature until sample processing. Pore Water Sample Processing and Analyses. Information on analytical methods is summarized in Table S1. The concentration of inorganic dissolved sulfide was measured by

αλ =

Aλ l

(1) −1

where αλ is the decadic absorption coefficient (cm ), Aλ is the absorbance, and l is the path length (cm). Due to oxidation of Fe(II) between sample collection and UV−vis spectra measurement, decadic absorption coefficients at 254 nm (α254) were corrected for Fe(III) interference.53 The specific ultraviolet absorbance at 254 nm (SUVA 254), a proxy for DOM aromaticity,54 was calculated by dividing the Fe(III)-corrected α254 by DOC concentration. For the fluorescence spectra, the fluorescence index (FI) was defined as the ratio of emission intensities measured at 470 and 520 nm at excitation 370 nm.55 A colorimetric assay was used to quantify the release of electrons associated with DOM and Fe(II).56,57 A complete account of electron release measurement and details on the evaluation of the electron release method are provided in the SI (SI Figures S4−S7).58−61 Mercury species were measured at the U.S. Geological Survey Mercury Research Laboratory (Middleton, WI). HgT was quantified by cold vapor atomic fluorescence spectroscopy (CVAFS) following EPA method 1631 (average daily detection limit (DDL) of 42 pg L−1). MeHg was measured by isotope dilution, isothermal gas chromatography separation, and detection by inductively coupled plasma-mass spectrometry (average DDL of 6 pg L−1). Samples for Hg(0)(aq) quantification were processed ≤6.5 h after sample collection (average hold time of 3 h); no trend was observed between sample hold time and the Hg(0)(aq) concentration or relative concentration of Hg(0)(aq) to Hg(II)i (p-value ≥ 0.56). Hg(0)(aq) was purged from pore waters with ultrahigh-purity nitrogen onto precleaned gold-coated sand traps and analyzed within 7 d of collection by thermal desorption and CVAFS detection. The limit of quantification (LOQ) for pore water Hg(0)(aq) was determined by measurement of bubbler blanks (average of 14 pg L−1, n = 4). The degree of Hg(0)(aq) saturation of pore waters was calculated using the measured Hg(0)(aq) concentration, Henry’s law constant (corrected for pore water temperature),62 and a typical atmospheric Hg(0)(g) concentration for the Northern Hemisphere (1.5 ng m−3) (details in SI).2,3,7 The pore water concentration of Hg(II)i was calculated as 0 Hg(II)i = Hg T − MeHg − Hg(aq)

(2)

We compared concentrations of mercury species as a function of pore water sample depth for each sublocation within wetlands as [Hg]shallow [Hg]deep

(3)

where [Hg]shallow and [Hg]deep are the concentrations of Hg(II)i, MeHg, or Hg(0)(aq) measured at shallow (10−15 cm below water table) and deep (20−35 cm below water table) depths, C

DOI: 10.1021/acs.est.8b06041 Environ. Sci. Technol. XXXX, XXX, XXX−XXX

Article

Environmental Science & Technology

Figure 1. Field pore water measurements of (a) pH, (b) conductivity (Cond.), (c) dissolved oxygen (DO), (d) temperature (Temp.), and concentrations of (e) ferrous iron (Fe(II)), (f) manganese (Mn), (g) sulfate (SO42−), and (h) inorganic dissolved sulfide (S(-II)) of bogs (brown symbols), poor fens (blue symbols), and rich fens (yellow symbols) in Alaska. Black-filled and color-filled symbols denote samples from July 2015 and July 2016, respectively.

All wetland pore waters were hypoxic or anoxic (Figure 1c), exhibited nitrate levels below the limit of detection (0.3 μM) in pore waters from all poor and rich fens and deep (30 cm depth) pore water samples within the Black Spruce bog (Figure 1h). We attribute the presence of inorganic dissolved sulfide to dissimilatory sulfate reduction. In general, sulfate and inorganic dissolved sulfide concentrations increased with increasing wetland trophic status (Figure 1). Simple organic acids (acetate, formate, oxalate), the end products of fermentation67,68 or the products of homoacetogenesis,69 were above the limit of detection in all bogs and

respectively. Data generated during this study are available at https://doi.org/10.5066/P9KHR2B1.63

■

RESULTS Wetland Pore Water Chemistry. With increasing wetland trophic status (bogs < poor fens < rich fens), pore waters show trends of increasing pH, conductivity, and concentrations of major inorganic anions (Cl−, SO42−) and cations (Ca, Mg, Na) (Figure 1, SI Figure S8). Concentrations of major inorganic anions and cations in two wetlands (Eightmile bog, Goldstream bog) were similar to those reported for bogs in Interior Alaska15 and only moderately higher than that of rainwater,64 which suggests that these wetlands are ombrotrophic. In the other six wetlands, the pH was higher and concentrations of major ions were elevated compared to rainwater,64 which we attribute to groundwater discharge into these wetlands.15,16 The range in pore water pH and Ca concentration (SI Figure S8e), which are geochemical indicators of wetland trophic status,15,16,65 support that the wetlands span a wide trophic distribution. In comparison to wetlands previously surveyed in Sweden for mercury methylation,11,17 pore water pH and Ca concentrations spanned a greater range of conditions (comparison shown in SI Figure S8e). The sampled wetlands exhibit a decrease in abundance of nonvascular plants (e.g., Sphagnum spp.) and an increase in abundance of sedge species (e.g., Carex spp.) with increased trophic status (Table 1), which is consistent with geochemical trends between pore waters and supports wetland classifications. D

DOI: 10.1021/acs.est.8b06041 Environ. Sci. Technol. XXXX, XXX, XXX−XXX

Article

Environmental Science & Technology Frozen Pond fen (SI Figure S10); acetate concentrations were elevated compared to all other wetlands in Black Spruce bog. The concentration and composition of DOM showed distinct trends with wetland trophic status, presented here as a function of pore water pH. In general, bogs contained higher concentrations of DOC and DOM of greater aromatic carbon content, as indicated by higher SUVA254 and lower FI values (SI Figure S11).54,55 With increasing trophic status, the concentration of DOC decreased and DOM was of lower aromaticity as indicated by lower SUVA254 and higher FI values (SI Figure S11). An exception to this general trend was observed in the Frozen Pond fen, where DOC levels were elevated in wetland pore waters of high pH and locations of minerotrophic groundwater inputs (Figure 1, SI Figure S8). The release of electrons from pore water DOM and Fe(II) was measured colorimetrically56,57 to evaluate the possibility of dark formation of Hg(0)(aq) by abiotic Hg(II)i reduction by DOM or Fe(II).24,51 Laboratory experiments confirmed that the colorimetric method only quantifies electron contribution from DOM and Fe(II) (SI Figure S6).56 The quantity of electrons released from pore waters was higher in samples with elevated DOC and Fe(II) concentration, and the concentration of electrons positively correlated with pore water DOC concentration (SI Figure S12). Mercury Concentration and Speciation in Wetland Pore Waters. Inorganic divalent mercury (Hg(II)i) concentrations in wetland pore waters ranged from 0.5 to 26.2 ng L−1. Most wetlands exhibited similar Hg(II)i concentrations between shallow and deep pore water samples (data not shown). Regardless of wetland type, pore waters with low DOC coincided with low Hg(II)i levels (Figure 2). Pore water Hg(II)i concentration correlated linearly and significantly with DOC concentration (p-value < 0.05) for three wetlands, and the slopes of the regressions decreased with trophic status (Black Spruce Bog > Sheep Creek fen > Frozen Pond fen) (Figure 2). Concentrations of Hg(0)(aq) varied within and between wetlands (Figure 3a) from below the limit of quantification (14 pg L−1; n = 9) to as high as 187 pg L−1. The average pore water Hg(0)(aq) concentration across all wetlands was 46 pg L−1 (n = 66). Elevated pore water Hg(0)(aq) concentrations were often observed at higher Hg(II)i concentrations. Pore water Hg(0)(aq) concentration positively correlated significantly with Hg(II)i concentration in two of the eight wetlands (Black Spruce bog, Frozen Pond fen) (Figure 3a). Across all wetlands, the concentration ratio of Hg(0)(aq) to Hg(II)i (Hg(0)(aq)/Hg(II)i) exhibited an inverse relationship with Hg(II)i concentration (Figure 3b;

[Hg(0)(aq)] [Hg(II)i ]

Figure 2. Scatter plot presents linear correlations between the pore water concentrations of inorganic divalent mercury (Hg(II)i) and dissolved organic carbon (DOC). The dashed brown, blue, and yellow lines presents linear fits of data of statistical significance (p-value < 0.05) for Black Spruce bog (BSB), Sheep Creek fen (SCF), and Frozen Pond fen (FPF). Black-filled and color-filled symbols denote samples from July 2015 and July 2016, respectively.

Methylmercury (MeHg) in pore waters varied in concentration (0.04 to 4.5 ng L−1) and fraction of HgT (1 to 47%) and exhibited trends with pore water Hg(II)i concentration and wetland trophic status (Figure 4). Low MeHg concentrations were observed in wetland pore waters with low Hg(II)i levels (Twin Lakes poor fen) and ombrotrophic bogs (Eightmile bog, Goldstream bog) (Figure 4a). Wetlands with appreciable MeHg exhibited general trends of higher MeHg at higher Hg(II)i concentrations. Significant site-specific correlations between MeHg and Hg(II)i were observed for Black Spruce bog and Frozen Pond fen (Figure 4a; p-value < 0.05). The ratio of MeHg to Hg(II)i concentration (MeHg/Hg(II)i) increased systematically with wetland trophic status from bogs to poor fens and then decreased from poor fens to rich fens (Figure 4b). Sheep Creek fen, a poor fen of intermediate trophic status, had the highest pore water MeHg/Hg(II)i (median = 30%, n = 10). Across all wetlands, the MeHg/Hg(II)i correlated positively to MeHg concentration (SI Figure S13e). No clear trend was observed in MeHg concentration with pore water sample depth (SI Figure S13f). Across all wetlands, no correlation was observed between the concentrations of Hg(0)(aq) and MeHg (p-value = 0.71, n = 66), but a site-specific positive correlation between Hg(0)(aq) and MeHg was observed for Frozen Pond fen in 2016 (p-value < 0.001, n = 12; Figure S14).

= 3.1e−0.2 ×[Hg(II)i ]; p-value < 0.001).

Further, higher Hg(0)(aq)/Hg(II)i was observed in pore waters with lower DOC concentration (Figure 3b inset) and higher Hg(0)(aq) concentration (SI Figure S13a). Neither the concentration of Hg(0)(aq) nor Hg(0)(aq)/Hg(II)i could be explained across all wetlands by (1) other differences in pore water chemistry (e.g., DOM composition (SUVA254, FI), quantified electron release from DOM and Fe(II)), (2) conditions during pore water sampling (e.g., pore water temperature, presence of standing water) (Figure 1d), (3) wetland trophic status (SI Figures S13c and S13d), or (4) sampling depth (SI Figure S13b). Pore waters were supersaturated with respect to Hg(0)(aq) in 95% of samples, with Hg(0)(aq) concentrations exceeding the calculated Hg(0)(aq) concentration at equilibrium with atmospheric Hg(0)(g).

■

DISCUSSION Geochemical Factors Controlling Dark Hg(0)(aq) Formation. This study is the first investigation of dark Hg(0)(aq) concentrations in northern wetlands of varied trophic status. Dark Hg(0)(aq) formation has been proposed to be an important E

DOI: 10.1021/acs.est.8b06041 Environ. Sci. Technol. XXXX, XXX, XXX−XXX

Article

Environmental Science & Technology

Figure 3. Scatter plots present (a) positive correlations between the concentrations of pore water dissolved gaseous mercury (Hg(0)(aq)) and inorganic divalent mercury (Hg(II)i) and (b) the inverse relationship between the ratio of Hg(0)(aq) to Hg(II)i concentration (%) and the Hg(II)i concentration for bogs (brown symbols), poor fens (blue symbols), and rich fens (yellow symbols). In plot a, the inset shows a close-up of the x- and y-axis intercept; colored dashed lines present linear fits of data for individual wetlands of statistical significance (p-value < 0.05), and the horizontal dotted gray line is the limit of quantification (LOQ) for Hg(0)(aq) (based on analysis of bubbler blanks). In plot b, the equation of the exponential function is [Hg(0)(aq)] [Hg(II)i ]

= 3.1e−0.2 ×[Hg(II)i ] (p-value < 0.001), and the inset shows the inverse relationship between Hg(0)(aq) to Hg(II)i concentration (%) and

dissolved organic carbon (DOC) concentration. Black-filled and color-filled symbols denote samples from July 2015 and July 2016, respectively. Note that data points at or below the LOQ (n = 9) are shown in plots a and b as gray-filled symbols.

Figure 4. (a) Scatter plot presents the linear correlations between concentrations of pore water methylmercury (MeHg) and inorganic divalent mercury (Hg(II)i) for bogs (brown symbols), poor fens (blue symbols), and rich fens (yellow symbols). (b) Box plots present median and quartile ranges of the ratio of pore water MeHg to Hg(II)i (%) for each wetland arranged in order of increasing wetland trophic status. In plot a, colored dashed lines present linear fits of data for individual wetlands of statistical significance (p-value < 0.05). In plot b, error bars represent 10−90% percentiles, outliers are shown as data points, and the order in wetland trophic status is based on geochemical indicators of pH and calcium concentration (SI Figure S8e). Black-filled and color-filled symbols denote samples from July 2015 and July 2016, respectively.

mercury retention in wetland pore waters by complexing Hg(II)i (Figure 2)28,29 and decreasing the concentration of volatile Hg(0)(aq) relative to Hg(II)i (Figure 3b). Our conclusion is supported by the observed inverse relationship between the

phenomenon contributing to mercury evasion from northern systems.7,8 Mercury is delivered to northern wetlands from predominantly dry atmospheric deposition and plant uptake of Hg(0)(g),2−4 and our results suggest that DOM influences F

DOI: 10.1021/acs.est.8b06041 Environ. Sci. Technol. XXXX, XXX, XXX−XXX

Article

Environmental Science & Technology

correlations observed between Hg(0)(aq) and Hg(II)i concentrations in two wetlands (Black Spruce bog, Frozen Pond fen; Figure 3a) suggest that Hg(II)i availability was a limiting factor in Hg(0)(aq) formation and the rate of Hg(II)i reduction exceeded rates of dark Hg(0)(aq) oxidation and atmospheric Hg(0)(g) evasion. Notably, both of these wetlands exhibited (1) geochemical evidence of groundwater inputs (higher pH and Ca concentration; Figure 1, SI Figure S8) and anaerobic microbial activity (e.g., acetate accumulation, autochthonous DOM production; SI Figures S10 and S11) and (2) similar correlations between concentrations of Hg(0)(aq) versus Hg(II)i (Figure 3a) and MeHg versus Hg(II)i (Figure 4a). These observations lend support to a dark biotic Hg(0)(aq) formation pathway, which has been proposed to explain Hg(0)(aq) presence at depth in a northern lake.27 Hg(0)(aq) formation by dissimilatory metalreducing bacteria, a prominent anaerobic pathway for Hg(II)i reduction,19,20 cannot be confirmed in Black Spruce bog and Frozen Pond fen because our analysis suggests that pore water Fe(II) and Mn could arise from in situ metal reduction or inputs of reduced groundwater (SI Figure S9).16 Alternatively, acetate accumulation in these wetlands (SI Figure S10a) suggest that fermentative bacteria could be responsible for dark Hg(II)i reduction,21 though we cannot discount the possibility of homoacetogenesis contributing to acetate formation.69 Geochemical data did not support dark biotic Hg(0)(aq) formation in the other six wetlands. This observation may be a result of alternative Hg(II)i reduction pathways or differences in relative rates of Hg(II)i reduction versus Hg(0)(aq) oxidation. Stable mercury isotope measurements of northern soils support that abiotic reduction of Hg(II)i by DOM is responsible for mercury evasion.8 Here, measurement of electron shuttle from pore water DOM (SI Figure S12) did not explain Hg(0)(aq) behavior, even in the two ombrotrophic bogs (Eightmile bog, Goldstream bog) where Hg(0)(aq) and DOC were elevated (Figure 3a, SI Figures S11a and S13c), and we infer low microbial activity.36 However, it is worth noting that the colorimetric method used to measure electron shuttle from DOM quantified differences between pore waters predominantly based on variance in DOC concentration but did not identify clear differences based on DOM composition (SUVA254 and DOM electron exchange capacity covary).32 This may reflect the greater differences in DOC concentration compared to DOM composition between pore waters (SI Figure S11) or a limitation of the colorimetric approach. These observations and the evidence discussed above on DOM limiting the concentration of Hg(0)(aq) relative to Hg(II)i do not preclude the possibility of Hg(II)i reduction by DOM. Rather, the multifaceted role of DOM on mercury behavior (Hg(II)i complexation28,29 and reduction23 and Hg(0)(aq) oxidation)24 may confound measurement of Hg(II)i reduction by DOM in the environment. Several additional explanations for Hg(0)(aq) production were considered. Hg(0)(aq) formation by other abiotic reductants (e.g., Fe(II))51 is unlikely in DOM-rich waters. Similarly, MeHg demethylation is not a likely explanation of Hg(0) (aq) production because oxidative demethylation, which produces Hg(II)i, is understood to occur under anaerobic conditions.77 Though, the lability of Hg(II)i produced through anaerobic MeHg demethylation to subsequent transformations (e.g., reduction) is unknown. The photoreduction of Hg(II)i to Hg(0)(aq) at the peat surface and the downward diffusion of Hg(0)(aq) are also considered unlikely because (1) pore waters were supersaturated with Hg(0)(aq), (2) no trend was observed

Hg(0)(aq)/Hg(II)i and (1) Hg(II)i concentration (Figure 3b) and (2) DOC concentration (Figure 3b inset). Because Hg(0)(aq) is volatile and susceptible to oxidation, we interpret these trends to reflect the summation of processes influencing dark Hg(II) i reduction, dark Hg(0) (aq) oxidation, and atmospheric evasion of Hg(0)(g). Below we propose two nonmutually exclusive explanations for these observations and discuss the geochemical evidence regarding processes controlling Hg(0)(aq) formation. First, the inverse trend between Hg(0)(aq)/Hg(II)i and Hg(II)i concentration (Figure 3b) may reflect the atmospheric evasion of Hg(0)(g) from wetland pore waters, as wetland pore waters were supersaturated with respect to Hg(0)(aq) in almost all cases. This interpretation is consistent with the observation in a northern bog of maximum Hg(0)(g) evasion rates coincident with maximum pore water Hg(0)(aq) concentrations that exceed Hg(0)(aq) saturation7 and is in agreement with observations between Hg(0)(aq) photoproduction and evasion from limnologic surface waters.70,71 Pore water Hg(0)(aq) concentrations measured here (187 pg L−1 maximum; 46 pg L−1 average; n = 66) were comparable to those reported in a northern bog (82 pg L−1 maximum, summer average = ∼ 40 pg L−1) attributed to the net efflux of mercury.7 Pore waters were supersaturated with Hg(0)(aq) suggesting that diffusion limitation could influence mercury evasion from pore water depths in this study (10−35 cm below the water table). We cannot discount, however, the possible influence of other driving forces not measured that influence mercury evasion (e.g., wind speed) or the total mercury budgets of wetlands (e.g., hydrologic transport).7,11 Second, we interpret the inverse trend between Hg(0)(aq)/ Hg(II)i and DOC concentration (Figure 3b inset) to reflect the influence of DOM on the distribution of mercury between Hg(II)i and Hg(0)(aq). A higher Hg(0)(aq)/Hg(II)i was observed under conditions of lower DOC concentration (Figure 3b inset). At higher DOC concentration, Hg(0)(aq) may exhibit low concentration relative to Hg(II)i because DOM (1) complexes Hg(II)i,28,29 in turn inhibiting Hg(II)i reduction by dark biotic19,72 or abiotic pathways,22−24 and (2) promotes the oxidation of Hg(0)(aq) to Hg(II)i, either by direct oxidation24 or by stabilizing the reaction product (i.e., Hg(II)i).73,74 Further, DOM in a reduced state, as was observed universally in pore waters (SI Figure S12), exhibits enhanced ability to oxidize Hg(0)(aq) to Hg(II)i.23,24 Elevated DOC concentrations were observed under contrasting trophic conditions (Figure 1, SI Figure S11). The bog pore waters exhibited high DOC concentration and DOM of more aromatic quality (higher SUVA254, lower FI; SI Figure S11), which has been attributed to accumulation of phenols that inhibit enzymatic decomposition of DOM.34,35 In contrast, Frozen Pond fen exhibited elevated DOC as a result of nutrient inputs (Figure 1, SI Figure S8) that stimulate DOM leaching from Sphagnum mosses and in situ DOM production,30,31 as reflected by DOM of lower aromatic quality (SI Figure S11). Our interpretation of the influence of DOM compositional differences between wetlands on DOM electron exchange capacity32 is discussed separately below. It is also possible that pore waters with higher Hg(II)i concentration, and therefore less Hg(0)(aq), reflect an older pool of mercury that is less reactive to reduction due to Hg(II)i aging,75 analogous to mercury accumulation in surface soils and litter.8,76 Ultimately, we report the first provisional environmental evidence of DOM controlling Hg(0)(aq) abundance in the absence of sunlight. A ubiquitous pathway for dark Hg(0)(aq) formation was not identified across all wetlands. However, the significant positive G

DOI: 10.1021/acs.est.8b06041 Environ. Sci. Technol. XXXX, XXX, XXX−XXX

Article

Environmental Science & Technology

as an electron source.17,18,36 Alternatively, methylation could also be facilitated by methanogens39,42 or through syntrophic interactions involving sulfate-reducing bacteria under sulfatelimitation40 that prevent acetate accumulation.88 Further, inorganic dissolved sulfide, which can inhibit methylation41,42 via formation of nanoparticulate β-HgS,43,44 was low at this site supporting MeHg accumulation. Though, the formation of FeS, through interactions between Fe(II) and inorganic dissolved sulfide, could mask evidence of dissimilatory sulfate reduction and influence Hg(II)i availability to methylation.89 Interestingly, the lowest concentration and MeHg/Hg(II)i were observed in the ombrotrophic bogs (Eightmile bog, Goldstream bog; Figure 4) with similar pore water chemistries (negligible sulfate and inorganic dissolved sulfide, elevated Fe(II)) but lower pH ( 5; Figure 1a)90 suggest that sulfate-reducing bacteria may be responsible for MeHg formation. The similar behaviors of MeHg and Hg(0)(aq) for the Frozen Pond fen (Figures 3 and 4, SI Figure 14) further present the possibility that the same microbes may be responsible for both Hg(II)i methylation and reduction.26 Intermediate levels of methylation in the Black Spruce bog may also be a result of the influence of DOM composition (elevated SUVA254) and low inorganic dissolved sulfide concentration that produce poorly crystalline nanoparticulate β-HgS43,44 which renders Hg(II)i more bioavailable to methylating organisms.41,45 In summary, these interpretations are consistent with previous studies suggesting multiple potential pathways for mercury methylation across a northern wetland trophic gradient.11,17 Ultimately, the relative importance of mercury methylation by a single microbial clade42,87 versus cometabolic processes40 remains enigmatic at the environmental level, emphasizing the need for future studies that employ a combination of geochemical and genomic approaches to fill knowledge gaps on pathways for mercury methylation.

between Hg(0)(aq) and sample depth (SI Figure S13b), and (3) the two wetlands with standing water (Frozen Pond fen, Eightmile bog), where photoreduction of Hg(II)i is expected to be greatest, exhibited contrasting Hg(0)(aq) behavior. Similarly, Hg(0)(aq) inputs from groundwater are unlikely because Hg(0)(aq) concentration did not correlate with geochemical indicators of groundwater (e.g., Ca). Regardless of the Hg(0)(aq) formation pathway(s), we surmise that DOM controls inorganic mercury abundance and speciation in wetland pore waters by binding Hg(II)i and limiting the relative abundance of volatile Hg(0)(aq). In the coming decades, DOC concentration in wetland pore waters are expected to increase in response to water table fluctuations78 and warmer temperatures79 as a result of a warming climate. Carbon mineralization rates and greenhouse gas production, which are used to model the flux of mercury from terrestrial landscapes to the atmosphere,80,81 increase with the progression of permafrost thaw82 and wetland trophic status36 and are intimately linked to shifts in DOC concentration and DOM composition.31 Future investigations should explore linkages between carbon mineralization in northern wetlands in response to warming and atmospheric mercury exchange. Geochemical Insights on Mercury Methylation. The relative concentration of MeHg to Hg(II)i in Alaskan wetland pore waters (Figure 4b) was highest in a poor fen (Sheep Creek fen) of intermediate trophic status. The observed trends in the MeHg/Hg(II)i with wetland trophic status (Figure 4b; poor fen > rich fens > bogs) are consistent with a conceptual model for net MeHg production in northern wetlands from Sweden11 and previous surveys of northern wetlands9−12 and receiving waters11,13,14 that identify fens as locations for MeHg production. In fact, Sheep Creek fen exhibited the highest MeHg/Hg(II)i and shows similar geochemical conditions of pore waters to that associated with maximum net methylation in Sweden (comparison shown in SI Figure S8e).11,17 We interpret the MeHg/Hg(II)i in pore waters to reflect rates of net in situ mercury methylation,10 akin to measurements of sediments.17,83−85 This interpretation is supported by positive agreement between the measured aqueous surface export of MeHg from northern wetlands and in situ mercury methylation rates in wetland sediments.11 The concentration of MeHg in pore waters was, in part, limited by the concentration of Hg(II)i (Figure 4a). Our results do not support a direct limitation of Hg(0)(aq) formation on mercury methylation in northern wetlands (SI Figure S14),25,26 explained by the low levels of Hg(0)(aq) in wetland pore waters and the greater availability of Hg(II)i to methylation than Hg(0)(aq).26 Rather, under the premise that dark Hg(0)(aq) formation and mercury efflux7 decrease Hg(II)i concentrations in northern wetlands (Figure 3b), our results point to an indirect limitation of Hg(0)(aq) accumulation on mercury methylation by decreasing the Hg(II)i pool available to methylation. The geochemistry of pore waters suggests that Hg(II)i availability and methylation pathways may differ over the range of wetland trophic conditions surveyed. The highest concentration of MeHg relative to Hg(II)i was observed at intermediate trophic status (Sheep Creek Fen, Figure 4b) under pore water conditions of low sulfate (