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Variations of mercury in the inflow and outflow of a constructed treatment wetland in south Florida, USA
Ecological Engineering 61 (2013) 419–425
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Variations of mercury in the inflow and outflow of a constructed treatment wetland in south Florida, USA Shimei Zheng a,b,c , Binhe Gu d,∗ , Qixing Zhou b,∗∗ , Yuncong Li c a
College of Chemistry and Environmental Engineering, Weifang University, Shandong 261061, China College of Environmental Science and Engineering, Nankai University, Tianjin 300071, China c Department of Soil and Water Science, Tropical Research and Education Center, IFAS, University of Florida, Homestead, FL, 32611, USA d Water Quality Bureau, South Florida Water Management District, West Palm Beach, FL 33406, USA b
a r t i c l e
i n f o
Article history: Received 16 May 2013 Received in revised form 30 September 2013 Accepted 12 October 2013 Available online 7 November 2013 Keywords: Constructed wetlands Environmental variables Methylmercury (MeHg) Seasonal trend Total mercury (THg)
a b s t r a c t Variations of total mercury (THg) and methylmercury (MeHg) concentrations at the inflow and outflow of a constructed treatment wetland, Stormwater Treatment Area 2 (STA-2) in south Florida were investigated from 2000 to 2011. The linkages between inflow water quality parameters and outflow THg and MeHg concentrations were assessed. THg and MeHg concentrations at the outflow in 2001 (2.88 and 0.95 ng L−1 ) and 2002 (2.33 and 0.87 ng L−1 ) were significantly greater than those (1.14 and 0.14 ng L−1 , 1.16 and 0.12 ng L−1 , respectively) at the inflow during the same time period. This was due to dryout and rewetting which may lead to Hg release from soil and promote Hg methylation. The average concentrations (0.75 and 0.11 ng L−1 ) of THg and MeHg at the outflow from 2005 to 2011 (except 2007) were lower than those (1.00 and 0.13 ng L−1 ) at the inflow, indicating that net THg and MeHg retention occurred in STA-2 during those years, which ranged from 0.35% to 49% for THg and from 3.5% to 37% for MeHg, respectively. Stepwise regression identified several inflow water quality parameters which explained 68% and 58% of the variances in the outflow THg and MeHg concentrations from 2000 to 2011. Certain inflow quality parameters were strong predictors of the variations in outflow THg and MeHg concentrations. These parameters included sulfate, chloride, dissolved organic carbon (DOC), dissolved oxygen (DO), pH, and temperature for outflow THg; and sulfate, chloride, DOC, and DO for outflow MeHg. Inflow sulfate and DO concentrations separately exhibited significant correlations with outflow THg and MeHg concentrations only prior to 2004. The results indicate that STA-2 was a source of THg and MeHg during early years of operation and a sink for THg and MeHg when the wetland passed the initial operation period and especially as water management improved to prevent dryout from occurring. Findings from this study also underscore the important role of inflow water quality to the variations of the outflow THg and MeHg concentrations. © 2013 Elsevier B.V. All rights reserved.
1. Introduction Inorganic mercury (Hg) can be transformed to a highly toxic form, methylmercury (MeHg), which readily accumulates to harmful levels in organisms at higher trophic levels (Abernathy and Cumbie, 1977; Bodaly et al., 1984). Sulfate-reducing bacteria (SRB) are generally recognized as the primary driver of Hg methylation (Compeau and Bartha, 1985; Gilmour et al., 1992; Ullrich et al., 2001), which thrive in carbon-rich anaerobic environments, degrade organic matter (OM), and reduce sulfate to sulfide in both
∗ Corresponding author. Tel.: +1 561 682 2556; fax: +1 561 682 5318. ∗∗ Corresponding author. Tel.: +86 22 23507800; fax: +86 22 23507800. E-mail addresses: [email protected], [email protected] (B. Gu), [email protected] (Q. Zhou). 0925-8574/$ – see front matter © 2013 Elsevier B.V. All rights reserved. http://dx.doi.org/10.1016/j.ecoleng.2013.10.015
freshwater and estuarine sediments. In the south Florida region, Gilmour et al. (1998) demonstrated that SRB were mediators of Hg methylation in the Everglades sediments. More broadly, Branfireun et al. (1999) reported that the in situ addition of sulfate to peat and associated pore water resulted in a significant increase in pore water MeHg concentrations in northwestern Ontario, Canada. Jeremiason et al. (2006) also found that enhanced sulfate loading increased Hg methylation in an experimental wetland at the Marcell Experimental Forest located in northeastern Minnesota, USA. Historic surface water monitoring data demonstrate that sulfate is present in Everglades Agricultural Area (EAA) runoff at 60–100 times that of background levels (Orem, 2004). The large treatment wetlands, Stormwater Treatment Areas (STAs) in the Everglades have been constructed primarily to remove total phosphorus (TP) from EAA runoff before entering the Everglades Protection Area (Chimney et al., 2000), and their role in removing excess sulfate
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is very limited (i.e., providing only about 11% sulfate reduction) (Orem, 2004; Orem et al., 2011). Notably, recent studies have found high Hg levels in fish and wildlife from the Everglades (Orem, 2004; Rumbold and Fink, 2006). The levels frequently exceeded U.S. Environmental Protection Agency (USEPA) and U.S. Fish and Wildlife Service (USFWS) predator protection criteria for wildlife protection, with 83% of fish Hg found to be in the MeHg form (Kannan et al., 1998). In addition to sulfate, numerous studies have shown that other factors can also influence Hg methylation. These include, but are not limited to, dissolved organic carbon (DOC) (Aiken et al., 2011); chloride (Ullrich et al., 2001); redox condition (Compeau and Bartha, 1985; Gilmour et al., 1992; Ullrich et al., 2001); temperature (Ullrich et al., 2001); and pH (Ullrich et al., 2001). These factors influence the efficiency of microbial Hg methylation by imposing an effect on the activity of SRB or the Hg bioavailability for SRB (Ullrich et al., 2001). Although wetlands are known to be net sinks for total mercury (THg) (Galloway and Branfireun, 2004; St. Louis et al., 1996), these areas can also facilitate MeHg production and produce MeHg hot spots (Hall et al., 2008) and therefore can frequently be sources of MeHg to the downstream environment (Driscoll et al., 1998; Galloway and Branfireun, 2004; Grigal et al., 2000; St. Louis et al., 1996). However, Stormwater Treatment Areas (STAs) are constructed primarily for the removal of nutrients but may also trap metals associated with suspended solids. Yet even if these constructed treatment wetlands are assumed to capture Hg associated with solids, it is still unknown whether the effects on THg and MeHg are similar to natural wetlands. The purpose of this study was to investigate the variations of THg and MeHg concentrations at the inflow and outflow of Stormwater Treatment Area 2 (STA-2) in south Florida, USA and explore the relationship between inflow water quality and outflow THg and MeHg concentrations. Overall, this study provides insight into the temporal trend of Hg and discusses potential factors controlling Hg variations in STAs. Specifically, it is intended to provide a better understanding of the role that a constructed treatment wetland plays on the processing and removal of THg and MeHg, and the influence of inflow water quality on outflow THg and MeHg, especially inflow sulfate loading on the Hg methylation. 2. Materials and methods 2.1. Study area Stormwater Treatment Area 2 (STA-2) is located in western Palm Beach County, Florida, immediately west of Water Conservation Area 2 (WCA-2) (Fig. 1), and is divided into four parallel north-south treatment cells with a total surface area of approximately 8000 acres as of 2012 (Cell 4, approximately 2000 acres, was constructed in 2007). Water from flow structures S-6 and G-328 enter the supply canal and is conveyed southward to the inflow canal, which extends across the northern perimeter of STA-2. A series of inflow culverts convey water from the inflow canal to the respective treatment cells. Water then flows southward through the treatment cells and eventually discharges into the discharge canal via culverts or gated spillways. The outflow pump station G-335 conveys water to WCA-2. 2.2. Data collection and quality assurance All THg and MeHg data at the STA-2 inflow and outflow and the inflow water quality parameters used in this analysis were obtained from the South Florida Water Management District’s DBHYDRO database (www.sfwmd.gov/dbhydro). Selected water
Fig. 1. Schematic diagram of structures and flows at Stormwater Treatment Area 2 (STA-2) before 2012, not to scale; S-6 and G-328 are the inflow structures, and G-335 is the outflow station.
quality parameters—chloride, dissolved organic carbon (DOC), dissolved oxygen (DO), pH, sulfate, and water temperature (Table 1) were also obtained from the same database to assess the influence of inflow water quality on the variations in outflow THg and MeHg concentrations. Sample collection and determinations of THg and MeHg concentrations have been described by Rumbold and Fink (2006). Briefly, unfiltered water samples of inflow (S-6 and G-328) and outflow (G-335) were collected biweekly to quarterly for water quality analysis (including THg and MeHg). A total of 218 and 224 data values were obtained for THg and MeHg concentrations, respectively, during the study period. THg determination in surface water was carried out using USEPA Method 1631 (Mercury in Water by Oxidation, Purge and Trap, and Cold Vapor Atomic Fluorescence Spectrometry) or a modification of Method 1631. MeHg analysis in surface water was used modified USEPA Draft Method 1630 (Methylmercury in Water and Tissues by Distillation, Extraction, Aqueous Phase Ethylation, Purge and Trap, Isothermal GC Separation, and Cold Vapor Atomic Fluorescence Spectrometry). The method detection limit for THg and MeHg are 0.1 ng L−1 and 0.022 ng L−1 , respectively. Quality assurance (QA) measures were incorporated during the sample collection and laboratory analysis to evaluate the quality of the data. All of the above methods use performance-based standards employing the appropriate levels of QA/QC (quality control) required by the National Environmental Laboratory Accreditation Conference, the specific reference method, and the Protocol. Laboratory QC samples included method blanks, lab-fortified blanks, matrix spikes, standard reference materials, and laboratory duplicates. Field QC samples included trip blanks, field blanks, equipment blanks, both of pre-cleaned equipment at the start of sampling and of field-cleaned equipment at the end of sampling, container and processing equipment blanks and field duplicates (Rumbold and Fink, 2006). 2.3. Statistical analysis All statistical analyses were conducted using PASW® Statistics 18.0 (SPSS Inc., Chicago, USA). The differences in THg and MeHg concentrations between the inflow and outflow were evaluated using the Mann–Whitney U test. Prior to correlation analysis and stepwise regression analysis, all data were log-transformed to approximate a normal distribution. The relationships among individual inflow water quality parameter (sulfate, pH, temperature,
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Table 1 Characteristics of multiple inflow water quality parameters (sulfate, chloride, DO, DOC, pH, temperature) from 2000 to 2011. Inflow water quality parameters −1
Sulfate (mg L ) Chloride (mg L−1 ) DO (mg L−1 ) DOC (mg L−1 ) pH Temperature (◦ C)
Range 39.3–110.1 87.62–301.53 0.71–8.23 20.8–43.9 6.77–8.06 14.3–32.5
Median
Mean
SD
57.6 193.1 3.44 34.9 7.47 25.6
59.5 192.6 3.73 33.9 7.46 24.9
14.8 50.2 1.71 6.1 0.21 3.9
DO, DOC, and chloride, respectively) and outflow THg and MeHg were evaluated using Pearson product-moment correlation coefficient analysis. Stepwise multivariate regression was applied to investigate the influence of multiple inflow water quality parameters on the outflow THg and MeHg concentrations. 3. Results 3.1. Comparison of THg and MeHg in inflow and outflow During the entire monitoring period at STA-2 from 2000 to 2011, the inflow THg concentration varied from 0.28 to 3.95 ng L−1 with a median value of 1.03 ng L−1 , while the outflow THg concentration ranged from 0.05 to 5.43 ng L−1 with a median value of 1.35 ng L−1 (Fig. 2a). The inflow MeHg concentration varied from 0.02 to 0.65 ng L−1 with a median value of 0.11 ng L−1 , while the outflow MeHg concentration ranged from 0.01 to 3.55 ng L−1 with a median value of 0.22 ng L−1 (Fig. 2b). Significant decreasing 6
Inflow Outflow
4 3 2 1
a
Inflow Outflow
4
Total Mercury (ng L-1)
-1
Total mercury (ng L )
5
56.0–62.9 180.3–204.8 3.46–4.00 31.8–36.0 7.43–7.50 24.4–25.4
trends were observed in inflow (r = −0.288, p = 0.0026) and outflow THg concentrations (r = −0.503, p < 0.001) over the monitoring period. A significant decreasing trend was also found in the outflow MeHg concentration (r = −0.364, p < 0.001) but not in the inflow MeHg concentration (r = −0.147, p = 0.128). The outflow THg and MeHg concentrations were significantly higher than the inflow THg and MeHg concentrations over the monitoring period, respectively (Mann–Whitney U test, p < 0.001). When the data were averaged by year, outflow THg and MeHg concentrations from 2001 to 2004 and in 2007 were greater than the inflow THg and MeHg concentrations, respectively (Fig. 3a and b). This was especially evident in 2001 and 2002 when outflow THg concentrations (2.88 and 2.33 ng L−1 ) were twofold higher than inflow THg concentrations (1.14 and 1.16 ng L−1 ), and outflow MeHg concentrations (0.95 and 0.87 ng L−1 ) were six to seven times greater than inflow MeHg concentrations (0.14 ng L−1 and 0.12 ng L−1 ). The average concentrations of THg and MeHg (0.75
5
a
95% confidence interval
3
2
1
0 0 1999 2000 2001 2002 2003 2004 2005 2006 2007 2008 2009 2010 2011 2012
2000 2001 2002 2003 2004 2005 2006 2007 2008 2009 2010 2011 2012 4
1.8
b
Inflow Outflow
1.6
2
1
0
Inflow Outflow
1.4
Methylmercury (ng L-1)
-1
Methylmercury (ng L )
3
b
1.2 1.0 .8 .6 .4 .2 0.0
2000 2001 2002 2003 2004 2005 2006 2007 2008 2009 2010 2011 2012 Year Fig. 2. Temporal variations of total mercury (THg) and methylmercury (MeHg) concentrations in inflow and outflow at STA-2.
1999 2000 2001 2002 2003 2004 2005 2006 2007 2008 2009 2010 2011 2012
Year Fig. 3. Annual averages (SD) of total mercury (THg) and methylmercury (MeHg) concentrations in the inflow and outflow at STA-2.
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Table 2 Results of Pearson product-moment correlation between inflow water parameters and outflow THg and MeHg. All data were log-transformed prior to correlation analysis. Inflow water quality parameters
Correlation coefficient (R) Before year 2004
Chloride DOC DO pH Sulfate Temperature *
Year 2000–2011
Outflow THg
Outflow MeHg
Outflow THg
Outflow MeHg
−0.085 −0.125 −0.405* −0.193 −0.379* 0.305
−0.049 −0.177 −0.347* −0.149 −0.368* 0.208
−0.089 −0.125 0.272 −0.13 −0.001 0.332*
−0.023 −0.149 0.236 −0.219 0.013 0.04
p < 0.05.
and 0.11 ng L−1 ) from 2005 to 2011 (except 2007) at the outflow were lower than those at the inflow (1.00 and 0.13 ng L−1 ), showing THg and MeHg retention by STA-2. Specifically, THg and MeHg retention in STA-2 after 2004 (except 2007) ranged from 0.35% to 49% with an average value of 21% and from 3.5% to 37% with a mean value of 22%, respectively. 3.2. Relationship between inflow water quality and outflow THg and MeHg At STA-2, the difference in MeHg between the inflow and outflow was significant before 2004 (p < 0.05), indicating that Hg methylation during this period was also significant. To evaluate how the factors affected Hg methylation in the constructed treatment wetland, Pearson product-moment correlation coefficient analyses between inflow water quality parameters and outflow THg and MeHg were assessed both prior to 2004 and from 2000 to 2011. Among the inflow water quality parameters before 2004, sulfate and DO were significantly correlated with both outflow THg and MeHg (Table 2). Inflow sulfate concentration was negatively correlated with both outflow THg and MeHg (Fig. 4a), which explained 37.9% and 36.8% of the THg and MeHg variations at the outflow, respectively. Inflow DO concentration was also negatively correlated with both outflow THg and MeHg concentrations (Fig. 4b), which accounted for 40.5% and 34.7% of THg and MeHg variations at the outflow, respectively. From 2000 to 2011, only the inflow temperature showed a positive, significant correlation with the outflow THg (Table 2), which accounted for 33.2% of the outflow THg variation, and no inflow water quality parameters exhibited a significant correlation with outflow MeHg concentration. Stepwise multivariate regression analysis was used to investigate whether outflow THg and MeHg variances would be better explained by combinations of the inflow water quality parameters. During the entire monitoring period from 2000 to 2011, several inflow water quality parameters were strong predictors of outflow THg and MeHg variations. Collectively, inflow chloride, sulfate, DO, DOC, pH, and temperature explained 68.4% of the outflow THg concentration variance, and inflow chloride, sulfate, DO, and DOC accounted for 58.4% of the outflow MeHg concentration variance (Table 3). The standardized coefficients (ˇ) of the stepwise regression in Table 3 represent the independent contributions of each inflow water quality parameter to the prediction of R. For each equation, they are directly comparable to one another and can be used to approximately evaluate the relative importance of individual inflow water quality parameter included in that equation. The inflow water quality parameter associated with a larger absolute value of ˇ suggests that this parameter contributes more to the variation of the dependent variable (outflow THg or MeHg). A negative ˇ means that R decreases with an increase in the inflow water quality parameters. In the equation of stepwise regression (Table 3), chloride negatively affected both outflow THg and MeHg
Fig. 4. Correlations between inflow DO and sulfate and outflow THg and MeHg at STA-2 before 2004.
concentrations and contributed more to outflow THg and MeHg variations than any of the other inflow water quality parameters, which included sulfate, DOC, DO, pH, and temperature. The contributions of the inflow sulfate, DOC, and DO to the variations of the outflow THg and MeHg were at the same level, negative effects of sulfate and DO and positive effect of DOC on outflow THg and MeHg variations. Furthermore, compared to other water quality parameters, the inflow pH and temperature contributed the least to the outflow THg variation. 4. Discussion 4.1. Comparison of THg and MeHg concentrations between inflow and outflow Over the 12-year monitoring period, STA-2 acted as a source and sink of both THg and MeHg in five and seven years, respectively.
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Table 3 Stepwise regression results between inflow water quality parameters and outflow THg and MeHg from 2000 to 2011. All data were log-transformed prior to correlation analysis. Dependent
Independent (inflow water quality parameters)
Standardized coefficient (ˇ)
R2
Significance
Outflow THg
Chloride Sulfate DO DOC pH Temperature
−1.028 −0.833 −0.806 0.7 0.102 0.103
0.684
p = 0.023
Outflow MeHg
Chloride DOC Sulfate DO
−1.093 0.878 −0.835 −0.626
0.584
p = 0.016
STA-2 often acted as a source in several years after the wetland was constructed and operated. Actually, STA-2 served as a significant source of both THg and MeHg in 2001 and 2002 only (Fig. 3). This is likely attributed to the severe drought during 2000 and 2001 that occurred in both Cells 1 and 2 (Fink et al., 2005). The process of drying and rewetting has been found to provide fuel for Hg methylation and microbial sulfate reduction, thereby causing increased Hg methylation in the wetland (Dmytriw et al., 1995; Gilmour et al., 2004). Dryout and rewetting can also enhance the release of trace metals from soil to the water column, including Hg release from the inorganic and organic binding sites in soil (Dmytriw et al., 1995). Soil dryout leads to the oxidation of OM, iron (II), and sulfide in the surficial soil to labile OM, iron(III), and sulfate, respectively (Dmytriw et al., 1995; Gilmour et al., 2004). The reinundation of soils after dryout is accompanied by a flush release of sulfate, iron, and labile OM (Gilmour et al., 2004). Following the flush release of sulfate and nutrients under anoxic conditions, the metabolic activity of SRB is likely to be stimulated to produce additional MeHg. Before 2004, the dryout and rewetting events in STA-2 provided a favorable condition for the growth of SRB and subsequently enhanced MeHg production. This is evident by the significantly higher outflow vs. inflow MeHg concentrations. The small difference of MeHg between inflow and outflow since 2004 suggests that the conditions in STA-2 since 2004 were no longer suitable for the growth of SRB or MeHg production. Over the 12-year monitoring period, STA-2 acted as a sink for both THg and MeHg during the last four to six years of operation. This suggests that the ability of the constructed treatment wetland to capture both THg and MeHg was improved when it matured and especially after water management was improved to prevent dryout. Such findings are somewhat contrary to some previous studies on the effect of wetlands on Hg retention. For instance, various studies have identified wetlands as a sink of THg but often as a net source of MeHg (Driscoll et al., 1998; Galloway and Branfireun, 2004; Grigal et al., 2000; St. Louis et al., 1996). The level of THg retention in STA-2 (0.35–49%, mean value 21%) was slightly lower than other wetland and upland systems reported in the literature, including 18–80% retention in different types of wetlands over three years (St. Louis et al., 1996), 74% in a beaver pond/riparian wetland (Driscoll et al., 1998), 95% in an upland catchment (Scherbatskoy et al., 1998), and the mean of 69% retention in a temperate forested wetland (Galloway and Branfireun, 2004). In comparison to the literature values of THg retention in other wetlands, STA-2 acted as a modest sink for THg. Hg is known to have a strong affinity for OM (Hurley et al., 1995), which supports the wetland soil retention of THg. Wetland THg retention may also be due to deep leaching to groundwater and considerable rates of Hg0 evasion (Galloway and Branfireun, 2004; Grigal et al., 2000). MeHg retention in STA-2 ranged from 3.5% to 37% (mean value 22%); MeHg retention data in other wetlands for comparison were
not found in literature. The work by Sellers et al. (1996) demonstrates that MeHg is photolytically decomposed in surface waters, and that this process is potentially an important step in the aquatic Hg cycle. Thereby, the photolytic decomposition of MeHg may be one of reasons for the MeHg removal in STA-2. 4.2. Influence of inflow water quality on outflow THg and MeHg The stepwise regression results indicate that inflow chloride, sulfate, DOC, and DO appear in the regression models of both outflow THg and MeHg, suggesting that they are critical inflow water quality parameters influencing outflow THg and MeHg concentrations. Except for the above inflow water quality parameters, only inflow pH and temperature had slightly positive effects on the outflow THg concentration. Among the inflow water quality parameters, sulfate loading to STA-2 was of the most concern in this study. The significant correlation between inflow sulfate load and outflow MeHg illustrated that sulfate input to STA-2 likely stimulated the activity of SRB and played a crucial role in the Hg methylation in the constructed treatment wetland. The buildup of sulfide, the reduced product of sulfate, in sediment porewater appears to inhibit Hg methylation through formation of insoluble HgS, which decreases the Hg availability to SRB (Benoit et al., 1999; Gilmour et al., 1992; Orem et al., 2011). The dual effect of sulfur on Hg methylation, that is, the stimulation effect of sulfate and the inhibition effect of sulfide, is termed the “Goldilocks effect” (Orem, 2007). This conceptual model for the role of sulfur in MeHg production has been verified for the Everglades by field, laboratory, and mesocosm experiments (Orem, 2007). Orem (2004) stated that in the Everglades the areas of highest MeHg production occur where sulfate contamination is moderate (2–10 mg L−1 ) and sulfide levels are low enough to avoid the inhibition of MeHg formation. Gilmour and Henry (1991) proposed an optimal sulfate concentration range of 19–48 mg L−1 (optimum concentration was approximately 29 mg L−1 ) for Hg methylation by SRB in sediments, above which methylation is inhibited and below which sulfate becomes limiting for Hg methylation and sulfate-reduction processes, and Weber (1993) found Hg methylation stops completely at a sulfate concentration exceeding approximately 48 mg L−1 . Gilmour et al. (1992) reported that MeHg production increases with sulfate concentrations up to 10 mg L−1 and declines when porewater sulfide exceeds 0.6 mg L−1 . King et al. (1999) observed active MeHg formation in the presence of 2.88 g L−1 sulfate and millimolar concentrations of dissolved sulfide. In this study, the negatively correlated relationship between inflow sulfate and outflow MeHg indicates that the sulfate concentration in the inflow was much greater than the optimal concentration for MeHg production in STA-2. Similarly, Selvendiran et al. (2008) also demonstrated a significant, negative correlation between MeHg and sulfate concentrations (6.33 ± 0.9 mg L−1 )
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during the growing season in a forested wetland, along with an increase in MeHg concentrations concomitant with the decrease in sulfate in wetland stream waters. In such case, the cycle of drying and rewetting likely promoted the production of MeHg accompanied by the release of THg, leading to the significant correlated relationship between inflow sulfate and outflow THg. Sulfate loading is an important factor in causing increased Hg methylation in the Everglades (Gilmour et al., 2007; Orem et al., 2011). In general, sulfate concentration decreases from north to south in the Everglades ecosystem (Orem, 2004; Orem et al., 2011). The dual effect of sulfur on MeHg production and the north-tosouth gradient in sulfate concentrations in the Everglades provide geographic context to MeHg distributions (Orem et al., 2011). Unenriched areas of the ecosystem with sulfate concentrations less than 1 mg L−1 exhibit low levels of MeHg due to sulfate limitation on Hg methylation (Orem et al., 2011). In sulfate-enriched areas (concentration more than 20 mg L−1 ) buildup of sulfide inhibits MeHg production (Orem et al., 2011). Areas with intermediate concentrations of sulfate (1–20 mg L−1 ) have sulfate levels that promote maximum MeHg production (Gilmour et al., 2007), where porewater sulfide concentrations are moderate (5–150 g L−1 ) (Gilmour et al., 1998; Orem et al., 2011). The influence of chloride on Hg methylation could be attributable to the competition of chloride for binding Hg, forming chloride–mercury complexes with the negatively charged forms (e.g., HgCl3 − , HgCl4 2− ). The neutral form (HgCl2 ) is more bioavailable for microbes than negatively charged forms because its uptake by microbes is likely a passive diffusion process (Barkay et al., 1997; Ullrich et al., 2001). So, the inverse correlation between inflow chloride and outflow MeHg in the stepwise regression indicates that inflow chloride concentration favored the formation of negatively charged chlorine–mercury complexes, which is consistent with other studies. Barkay et al. (1997) reported that when chloride concentrations were above 1 mM, a decreased bioavailability of Hg(II) to the bioindicator was attributed to an increased proportion of negatively charged chlorine–mercury complexes. A previous study has shown that increasing chloride from 0.01 to 0.1 mM sharply reduced Hg adsorption on clay particles (Newton et al., 1976), indicating a positive relationship between chloride and Hg in the watershed under a range of low chloride concentrations. However, the high chloride concentrations in STA-2 and the negative impact on MeHg production are in line with the majority of the studies that high chloride concentration favors the formation of negatively charged chlorine–mercury complex and reduces bioavailability of inorganic mercury. The influence of DOC on Hg availability for SRB methylation is complicated. DOC can act as energy source for microbial activity to stimulate methylation (Ullrich et al., 2001) and can decrease and enhance the bioavailability of Hg to SRB (Gorski, 2004). Hg bioavailability can be reduced by DOC through photochemical reduction of Hg(II) to Hg0 (Ravichandran, 2004) or can be enhanced by the mixed complexes that contain both DOC and reduced sulfur groups (DOC–Hg–SH) (Hsu-Kim and Sedlak, 2005; Miller et al., 2007). DOC also can interact strongly with THg and MeHg, facilitating the mobility of Hg from soils and sediments into watersheds (Ravichandran, 2004). In the Florida Everglades, the DOC concentration is high due to the high natural production of organic carbon in the peat soils (Aiken et al., 2011; Liu et al., 2008), and DOC has been found to be strongly correlated to THg and MeHg in this region (Liu et al., 2008). The observed positive relationship between inflow DOC and outflow THg and MeHg in this study suggests that inflow DOC was an important controlling factor influencing the THg and MeHg concentrations in the watershed of the constructed treatment wetland, either by controlling the bioavailability of Hg or controlling Hg transport and concentration.
Anaerobic conditions favor the activity of SRB and subsequently Hg methylation, while oxygen deficiency is widely known to enhance Hg mobility (Compeau and Bartha, 1985; Gilmour et al., 1992; Kim, 1995; Ullrich et al., 2001); therefore, the significantly negative effects of inflow DO on the outflow THg and MeHg were expected to occur. Generally, Hg methylation in an acidic environment is prone to be enhanced in comparison to alkaline surroundings, and elevated Hg levels in fish are commonly found in acidified lakes (Ullrich et al., 2001). It is uncertain whether the stimulation of methylation in lake water is a direct effect of low pH on the methylation process, or if it is related to other factors that are influenced by pH, such as the loss of volatile Hg species from the water surfaces, or changes in Hg solubility and partitioning (Ullrich et al., 2001). In the laboratory, the maximum rate of Hg methylation occurred at a pH of 4.5 and the formation of Hg hydroxides at higher pH (>8) inhibits the formation of MeHg by reducing inorganic Hg availability to bacteria (Leng and Nies, 1999). Xun et al. (1987) found that net MeHg production in lake water was seven times faster at pH 4.5 than at pH 8.5. As the inflow in STA-2 was slightly alkaline, and there was no significant relationship between inflow pH and outflow MeHg, this may suggest that the range of inflow pH was possibly too small to influence the availability of Hg to methylating microorganisms or to impose any effect on the microbial community. However, the stepwise regression results showed that inflow pH had a slight positive effect on outflow THg, indicating the narrow inflow pH produced little effect on the mobility of THg between the soil and water column. This is consistent with other study finding that showed the pH dependency of Hg solubility and mobility in the watershed (Lee and Hultberg, 1990). Moderately high temperatures have been found to provide a stimulating effect on Hg methylation, which is most likely due to the enhanced microbial activity by the increase in temperature (Ullrich et al., 2001). However, no significant relationship between inflow temperature and outflow MeHg was observed in this study. The seasonal change in water temperature may not impose a significant impact on the microbial activity. But, the significant positive correlation for inflow temperature with the outflow THg suggests that inflow temperature affected the THg mobility between the soil and the water column. 5. Conclusion Results from this study show that STA-2 served as a source of both THg and MeHg at the early stages of operation and as a sink for both THg and MeHg when the constructed treatment wetland became mature and especially as water management was improved to prevent dryout from occurring. The net output of both THg and MeHg during the early years of operation, especially in 2001 and 2002, was primarily attributed to the dryout and rewetting cycles which promoted the Hg methylation and the releases of both THg and MeHg from the soil to the surface water. Stepwise regression results suggest that inflow water quality played an important role on the variations of THg and MeHg at the outflow from 2000 to 2011. Sulfate, chloride, DOC, DO, pH, and temperature were among the biogeochemical parameters at the inflow that significantly impacted outflow THg variation, and only inflow sulfate, chloride, DOC, and DO showed significant effects on outflow MeHg variation. Acknowledgements We greatly appreciate the support for this work from Nankai University, China; University of Florida–Institute of Food and
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Agricultural Sciences, Tropical Research and Education Center; and the South Florida Water Management District. We also appreciate Comments from Dr. Larry Schwartz and Dr. Garth Redfield, and editorial improvements from Ms. Stacey Ollis. References Abernathy, A.R., Cumbie, P.M., 1977. Mercury accumulation by largemouth bass (Micropterus salmoides) in recently impounded reservoirs. Bull. Environ. Contam. Toxicol. 17, 595–602. Aiken, G.R., Gilmour, C.C., Krabbenhoft, D.P., Orem, W.H., 2011. Dissolved organic matter in the Florida Everglades: implications for ecosystem restoration. Crit. Rev. Environ. Sci. Technol. 41, 217–248. Barkay, T., Gillman, M., Turner, R.R., 1997. Effects of dissolved organic carbon and salinity on bioavailability of mercury. Appl. Environ. Microbiol. 63, 4267–4271. Benoit, J.M., Gilmour, C.C., Mason, R.P., Heyes, A., 1999. Sulfide controls on mercury speciation and bioavailability in sediment pore waters. Environ. Sci. Technol. 33, 951–957. Bodaly, R.A., Hecky, R.E., Fudge, R.J.P., 1984. Increases in fish mercury levels in lakes flooded by the Churchill River Diversion, Northern Manitoba. Can. J. Fish. Aquat. Sci. 41, 682–691. Branfireun, B.A., Roulet, N.T., Kelly, C.A., Rudd, J.W.M., 1999. In situ sulphate stimulation of mercury methylation in a boreal peatland: toward a link between acid rain and methylmercury contamination in remote environments. Global Biogeochem. Cycles 13, 743–750. Chimney, M.J., Nungesser, M., Newman, J., Pietro, K., Germain, G., Lynch, T., Goforth, G., Moustafa, M.Z., 2000. Chapter 6: stormwater treatment areas-status of research and monitoring to optimize effectiveness of nutrient removal and annual report on operational compliance. In: 2000 Everglades Consolidated Report. South Florida Water Management District, West Palm Beach, FL. Compeau, G.C., Bartha, R., 1985. Sulfate-reducing bacteria: principal methylators of mercury in anoxic estuarine sediment. Appl. Environ. Microbiol. 50, 498–502. Dmytriw, R., Mucci, A., Lucotte, M., Pichet, P., 1995. The partitioning of mercury in the solid components of dry and flooded forest soils and sediments from a hydroelectric reservoir, Quebec (Canada). Water Air Soil Pollut. 80, 1099–1103. Driscoll, C.T., Holsapple, J., Schofield, C.L., Munson, R., 1998. The chemistry and transport of mercury in a small wetland in the Adirondack region of New York, USA. Biogeochemistry 40, 137–146. Fink, L.E., King, J., Adak, P., Matson, F., 2005. Appendix 2B-2: STA-2 Mercury Special Studies Project Report. In: 2005 South Florida Environmental Report. South Florida Water Management District, West Palm Beach, FL. Galloway, M.E., Branfireun, B.A., 2004. Mercury dynamics of a temperate forest wetland. Sci. Total Environ. 325, 239–254. Gilmour, C.C., Henry, E.A., 1991. Mercury methylation in aquatic systems affected by acid deposition. Environ. Pollut. 71, 131–169. Gilmour, C.G., Henry, E.A., Mitchell, R., 1992. Sulfate stimulation of mercury methylation in freshwater sediments. Environ. Sci. Technol. 26, 2281–2287. Gilmour, C.C., Riedel, G.S., Ederington, M.C., Bell, J.T., Benoit, J.M., Gill, G.A., Stordal, M.C., 1998. Methymercury concentrations and production rates across a trophic gradient in the Northern Everglades. Biogeochemistry 40, 327–345. Gilmour, C., Krabbenhoft, D., Orem, W., Aiken, G., 2004. Appendix 2B-1: Influence of drying and rewetting on mercury and sulfur cycling in Everglades and STA soils. In: 2004 Everglades Consolidated Report. South Florida Water Management District and Florida Department of Environmental Protection, West Palm Beach, FL. Gilmour, C., Krabbenhoft, D., Orem, W., Aiken, G., Roden, E., 2007. Appendix 3B-2: Status report on ACME studies on the control of Hg methylation and bioaccumulation in the Everglades. In: 2007 South Florida Environmental Report. South Florida Water Management District, West Palm Beach, FL. Gorski, P.R., 2004. An assessment of bioavailability and bioaccumulation of mercury species in freshwater food chains. Limnology and Marine Science, University of Wisconsin – Madison, Madison, WI. Grigal, D.F., Kolka, R.K., Flech, J.A., Nater, E.A., 2000. Mercury budget of an uplandpeatland watershed. Biogeochemistry 50, 95–109. Hall, B.D., Aiken, G.R., Krabbenhoft, D.P., Marvin-Dipasquale, M., Swarzenski, C.M., 2008. Wetlands as principal zones of methylmercury production in
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Ecological Engineering journal homepage: www.elsevier.com/locate/ecoleng
Variations of mercury in the inflow and outflow of a constructed treatment wetland in south Florida, USA Shimei Zheng a,b,c , Binhe Gu d,∗ , Qixing Zhou b,∗∗ , Yuncong Li c a
College of Chemistry and Environmental Engineering, Weifang University, Shandong 261061, China College of Environmental Science and Engineering, Nankai University, Tianjin 300071, China c Department of Soil and Water Science, Tropical Research and Education Center, IFAS, University of Florida, Homestead, FL, 32611, USA d Water Quality Bureau, South Florida Water Management District, West Palm Beach, FL 33406, USA b
a r t i c l e
i n f o
Article history: Received 16 May 2013 Received in revised form 30 September 2013 Accepted 12 October 2013 Available online 7 November 2013 Keywords: Constructed wetlands Environmental variables Methylmercury (MeHg) Seasonal trend Total mercury (THg)
a b s t r a c t Variations of total mercury (THg) and methylmercury (MeHg) concentrations at the inflow and outflow of a constructed treatment wetland, Stormwater Treatment Area 2 (STA-2) in south Florida were investigated from 2000 to 2011. The linkages between inflow water quality parameters and outflow THg and MeHg concentrations were assessed. THg and MeHg concentrations at the outflow in 2001 (2.88 and 0.95 ng L−1 ) and 2002 (2.33 and 0.87 ng L−1 ) were significantly greater than those (1.14 and 0.14 ng L−1 , 1.16 and 0.12 ng L−1 , respectively) at the inflow during the same time period. This was due to dryout and rewetting which may lead to Hg release from soil and promote Hg methylation. The average concentrations (0.75 and 0.11 ng L−1 ) of THg and MeHg at the outflow from 2005 to 2011 (except 2007) were lower than those (1.00 and 0.13 ng L−1 ) at the inflow, indicating that net THg and MeHg retention occurred in STA-2 during those years, which ranged from 0.35% to 49% for THg and from 3.5% to 37% for MeHg, respectively. Stepwise regression identified several inflow water quality parameters which explained 68% and 58% of the variances in the outflow THg and MeHg concentrations from 2000 to 2011. Certain inflow quality parameters were strong predictors of the variations in outflow THg and MeHg concentrations. These parameters included sulfate, chloride, dissolved organic carbon (DOC), dissolved oxygen (DO), pH, and temperature for outflow THg; and sulfate, chloride, DOC, and DO for outflow MeHg. Inflow sulfate and DO concentrations separately exhibited significant correlations with outflow THg and MeHg concentrations only prior to 2004. The results indicate that STA-2 was a source of THg and MeHg during early years of operation and a sink for THg and MeHg when the wetland passed the initial operation period and especially as water management improved to prevent dryout from occurring. Findings from this study also underscore the important role of inflow water quality to the variations of the outflow THg and MeHg concentrations. © 2013 Elsevier B.V. All rights reserved.
1. Introduction Inorganic mercury (Hg) can be transformed to a highly toxic form, methylmercury (MeHg), which readily accumulates to harmful levels in organisms at higher trophic levels (Abernathy and Cumbie, 1977; Bodaly et al., 1984). Sulfate-reducing bacteria (SRB) are generally recognized as the primary driver of Hg methylation (Compeau and Bartha, 1985; Gilmour et al., 1992; Ullrich et al., 2001), which thrive in carbon-rich anaerobic environments, degrade organic matter (OM), and reduce sulfate to sulfide in both
∗ Corresponding author. Tel.: +1 561 682 2556; fax: +1 561 682 5318. ∗∗ Corresponding author. Tel.: +86 22 23507800; fax: +86 22 23507800. E-mail addresses: [email protected], [email protected] (B. Gu), [email protected] (Q. Zhou). 0925-8574/$ – see front matter © 2013 Elsevier B.V. All rights reserved. http://dx.doi.org/10.1016/j.ecoleng.2013.10.015
freshwater and estuarine sediments. In the south Florida region, Gilmour et al. (1998) demonstrated that SRB were mediators of Hg methylation in the Everglades sediments. More broadly, Branfireun et al. (1999) reported that the in situ addition of sulfate to peat and associated pore water resulted in a significant increase in pore water MeHg concentrations in northwestern Ontario, Canada. Jeremiason et al. (2006) also found that enhanced sulfate loading increased Hg methylation in an experimental wetland at the Marcell Experimental Forest located in northeastern Minnesota, USA. Historic surface water monitoring data demonstrate that sulfate is present in Everglades Agricultural Area (EAA) runoff at 60–100 times that of background levels (Orem, 2004). The large treatment wetlands, Stormwater Treatment Areas (STAs) in the Everglades have been constructed primarily to remove total phosphorus (TP) from EAA runoff before entering the Everglades Protection Area (Chimney et al., 2000), and their role in removing excess sulfate
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is very limited (i.e., providing only about 11% sulfate reduction) (Orem, 2004; Orem et al., 2011). Notably, recent studies have found high Hg levels in fish and wildlife from the Everglades (Orem, 2004; Rumbold and Fink, 2006). The levels frequently exceeded U.S. Environmental Protection Agency (USEPA) and U.S. Fish and Wildlife Service (USFWS) predator protection criteria for wildlife protection, with 83% of fish Hg found to be in the MeHg form (Kannan et al., 1998). In addition to sulfate, numerous studies have shown that other factors can also influence Hg methylation. These include, but are not limited to, dissolved organic carbon (DOC) (Aiken et al., 2011); chloride (Ullrich et al., 2001); redox condition (Compeau and Bartha, 1985; Gilmour et al., 1992; Ullrich et al., 2001); temperature (Ullrich et al., 2001); and pH (Ullrich et al., 2001). These factors influence the efficiency of microbial Hg methylation by imposing an effect on the activity of SRB or the Hg bioavailability for SRB (Ullrich et al., 2001). Although wetlands are known to be net sinks for total mercury (THg) (Galloway and Branfireun, 2004; St. Louis et al., 1996), these areas can also facilitate MeHg production and produce MeHg hot spots (Hall et al., 2008) and therefore can frequently be sources of MeHg to the downstream environment (Driscoll et al., 1998; Galloway and Branfireun, 2004; Grigal et al., 2000; St. Louis et al., 1996). However, Stormwater Treatment Areas (STAs) are constructed primarily for the removal of nutrients but may also trap metals associated with suspended solids. Yet even if these constructed treatment wetlands are assumed to capture Hg associated with solids, it is still unknown whether the effects on THg and MeHg are similar to natural wetlands. The purpose of this study was to investigate the variations of THg and MeHg concentrations at the inflow and outflow of Stormwater Treatment Area 2 (STA-2) in south Florida, USA and explore the relationship between inflow water quality and outflow THg and MeHg concentrations. Overall, this study provides insight into the temporal trend of Hg and discusses potential factors controlling Hg variations in STAs. Specifically, it is intended to provide a better understanding of the role that a constructed treatment wetland plays on the processing and removal of THg and MeHg, and the influence of inflow water quality on outflow THg and MeHg, especially inflow sulfate loading on the Hg methylation. 2. Materials and methods 2.1. Study area Stormwater Treatment Area 2 (STA-2) is located in western Palm Beach County, Florida, immediately west of Water Conservation Area 2 (WCA-2) (Fig. 1), and is divided into four parallel north-south treatment cells with a total surface area of approximately 8000 acres as of 2012 (Cell 4, approximately 2000 acres, was constructed in 2007). Water from flow structures S-6 and G-328 enter the supply canal and is conveyed southward to the inflow canal, which extends across the northern perimeter of STA-2. A series of inflow culverts convey water from the inflow canal to the respective treatment cells. Water then flows southward through the treatment cells and eventually discharges into the discharge canal via culverts or gated spillways. The outflow pump station G-335 conveys water to WCA-2. 2.2. Data collection and quality assurance All THg and MeHg data at the STA-2 inflow and outflow and the inflow water quality parameters used in this analysis were obtained from the South Florida Water Management District’s DBHYDRO database (www.sfwmd.gov/dbhydro). Selected water
Fig. 1. Schematic diagram of structures and flows at Stormwater Treatment Area 2 (STA-2) before 2012, not to scale; S-6 and G-328 are the inflow structures, and G-335 is the outflow station.
quality parameters—chloride, dissolved organic carbon (DOC), dissolved oxygen (DO), pH, sulfate, and water temperature (Table 1) were also obtained from the same database to assess the influence of inflow water quality on the variations in outflow THg and MeHg concentrations. Sample collection and determinations of THg and MeHg concentrations have been described by Rumbold and Fink (2006). Briefly, unfiltered water samples of inflow (S-6 and G-328) and outflow (G-335) were collected biweekly to quarterly for water quality analysis (including THg and MeHg). A total of 218 and 224 data values were obtained for THg and MeHg concentrations, respectively, during the study period. THg determination in surface water was carried out using USEPA Method 1631 (Mercury in Water by Oxidation, Purge and Trap, and Cold Vapor Atomic Fluorescence Spectrometry) or a modification of Method 1631. MeHg analysis in surface water was used modified USEPA Draft Method 1630 (Methylmercury in Water and Tissues by Distillation, Extraction, Aqueous Phase Ethylation, Purge and Trap, Isothermal GC Separation, and Cold Vapor Atomic Fluorescence Spectrometry). The method detection limit for THg and MeHg are 0.1 ng L−1 and 0.022 ng L−1 , respectively. Quality assurance (QA) measures were incorporated during the sample collection and laboratory analysis to evaluate the quality of the data. All of the above methods use performance-based standards employing the appropriate levels of QA/QC (quality control) required by the National Environmental Laboratory Accreditation Conference, the specific reference method, and the Protocol. Laboratory QC samples included method blanks, lab-fortified blanks, matrix spikes, standard reference materials, and laboratory duplicates. Field QC samples included trip blanks, field blanks, equipment blanks, both of pre-cleaned equipment at the start of sampling and of field-cleaned equipment at the end of sampling, container and processing equipment blanks and field duplicates (Rumbold and Fink, 2006). 2.3. Statistical analysis All statistical analyses were conducted using PASW® Statistics 18.0 (SPSS Inc., Chicago, USA). The differences in THg and MeHg concentrations between the inflow and outflow were evaluated using the Mann–Whitney U test. Prior to correlation analysis and stepwise regression analysis, all data were log-transformed to approximate a normal distribution. The relationships among individual inflow water quality parameter (sulfate, pH, temperature,
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Table 1 Characteristics of multiple inflow water quality parameters (sulfate, chloride, DO, DOC, pH, temperature) from 2000 to 2011. Inflow water quality parameters −1
Sulfate (mg L ) Chloride (mg L−1 ) DO (mg L−1 ) DOC (mg L−1 ) pH Temperature (◦ C)
Range 39.3–110.1 87.62–301.53 0.71–8.23 20.8–43.9 6.77–8.06 14.3–32.5
Median
Mean
SD
57.6 193.1 3.44 34.9 7.47 25.6
59.5 192.6 3.73 33.9 7.46 24.9
14.8 50.2 1.71 6.1 0.21 3.9
DO, DOC, and chloride, respectively) and outflow THg and MeHg were evaluated using Pearson product-moment correlation coefficient analysis. Stepwise multivariate regression was applied to investigate the influence of multiple inflow water quality parameters on the outflow THg and MeHg concentrations. 3. Results 3.1. Comparison of THg and MeHg in inflow and outflow During the entire monitoring period at STA-2 from 2000 to 2011, the inflow THg concentration varied from 0.28 to 3.95 ng L−1 with a median value of 1.03 ng L−1 , while the outflow THg concentration ranged from 0.05 to 5.43 ng L−1 with a median value of 1.35 ng L−1 (Fig. 2a). The inflow MeHg concentration varied from 0.02 to 0.65 ng L−1 with a median value of 0.11 ng L−1 , while the outflow MeHg concentration ranged from 0.01 to 3.55 ng L−1 with a median value of 0.22 ng L−1 (Fig. 2b). Significant decreasing 6
Inflow Outflow
4 3 2 1
a
Inflow Outflow
4
Total Mercury (ng L-1)
-1
Total mercury (ng L )
5
56.0–62.9 180.3–204.8 3.46–4.00 31.8–36.0 7.43–7.50 24.4–25.4
trends were observed in inflow (r = −0.288, p = 0.0026) and outflow THg concentrations (r = −0.503, p < 0.001) over the monitoring period. A significant decreasing trend was also found in the outflow MeHg concentration (r = −0.364, p < 0.001) but not in the inflow MeHg concentration (r = −0.147, p = 0.128). The outflow THg and MeHg concentrations were significantly higher than the inflow THg and MeHg concentrations over the monitoring period, respectively (Mann–Whitney U test, p < 0.001). When the data were averaged by year, outflow THg and MeHg concentrations from 2001 to 2004 and in 2007 were greater than the inflow THg and MeHg concentrations, respectively (Fig. 3a and b). This was especially evident in 2001 and 2002 when outflow THg concentrations (2.88 and 2.33 ng L−1 ) were twofold higher than inflow THg concentrations (1.14 and 1.16 ng L−1 ), and outflow MeHg concentrations (0.95 and 0.87 ng L−1 ) were six to seven times greater than inflow MeHg concentrations (0.14 ng L−1 and 0.12 ng L−1 ). The average concentrations of THg and MeHg (0.75
5
a
95% confidence interval
3
2
1
0 0 1999 2000 2001 2002 2003 2004 2005 2006 2007 2008 2009 2010 2011 2012
2000 2001 2002 2003 2004 2005 2006 2007 2008 2009 2010 2011 2012 4
1.8
b
Inflow Outflow
1.6
2
1
0
Inflow Outflow
1.4
Methylmercury (ng L-1)
-1
Methylmercury (ng L )
3
b
1.2 1.0 .8 .6 .4 .2 0.0
2000 2001 2002 2003 2004 2005 2006 2007 2008 2009 2010 2011 2012 Year Fig. 2. Temporal variations of total mercury (THg) and methylmercury (MeHg) concentrations in inflow and outflow at STA-2.
1999 2000 2001 2002 2003 2004 2005 2006 2007 2008 2009 2010 2011 2012
Year Fig. 3. Annual averages (SD) of total mercury (THg) and methylmercury (MeHg) concentrations in the inflow and outflow at STA-2.
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Table 2 Results of Pearson product-moment correlation between inflow water parameters and outflow THg and MeHg. All data were log-transformed prior to correlation analysis. Inflow water quality parameters
Correlation coefficient (R) Before year 2004
Chloride DOC DO pH Sulfate Temperature *
Year 2000–2011
Outflow THg
Outflow MeHg
Outflow THg
Outflow MeHg
−0.085 −0.125 −0.405* −0.193 −0.379* 0.305
−0.049 −0.177 −0.347* −0.149 −0.368* 0.208
−0.089 −0.125 0.272 −0.13 −0.001 0.332*
−0.023 −0.149 0.236 −0.219 0.013 0.04
p < 0.05.
and 0.11 ng L−1 ) from 2005 to 2011 (except 2007) at the outflow were lower than those at the inflow (1.00 and 0.13 ng L−1 ), showing THg and MeHg retention by STA-2. Specifically, THg and MeHg retention in STA-2 after 2004 (except 2007) ranged from 0.35% to 49% with an average value of 21% and from 3.5% to 37% with a mean value of 22%, respectively. 3.2. Relationship between inflow water quality and outflow THg and MeHg At STA-2, the difference in MeHg between the inflow and outflow was significant before 2004 (p < 0.05), indicating that Hg methylation during this period was also significant. To evaluate how the factors affected Hg methylation in the constructed treatment wetland, Pearson product-moment correlation coefficient analyses between inflow water quality parameters and outflow THg and MeHg were assessed both prior to 2004 and from 2000 to 2011. Among the inflow water quality parameters before 2004, sulfate and DO were significantly correlated with both outflow THg and MeHg (Table 2). Inflow sulfate concentration was negatively correlated with both outflow THg and MeHg (Fig. 4a), which explained 37.9% and 36.8% of the THg and MeHg variations at the outflow, respectively. Inflow DO concentration was also negatively correlated with both outflow THg and MeHg concentrations (Fig. 4b), which accounted for 40.5% and 34.7% of THg and MeHg variations at the outflow, respectively. From 2000 to 2011, only the inflow temperature showed a positive, significant correlation with the outflow THg (Table 2), which accounted for 33.2% of the outflow THg variation, and no inflow water quality parameters exhibited a significant correlation with outflow MeHg concentration. Stepwise multivariate regression analysis was used to investigate whether outflow THg and MeHg variances would be better explained by combinations of the inflow water quality parameters. During the entire monitoring period from 2000 to 2011, several inflow water quality parameters were strong predictors of outflow THg and MeHg variations. Collectively, inflow chloride, sulfate, DO, DOC, pH, and temperature explained 68.4% of the outflow THg concentration variance, and inflow chloride, sulfate, DO, and DOC accounted for 58.4% of the outflow MeHg concentration variance (Table 3). The standardized coefficients (ˇ) of the stepwise regression in Table 3 represent the independent contributions of each inflow water quality parameter to the prediction of R. For each equation, they are directly comparable to one another and can be used to approximately evaluate the relative importance of individual inflow water quality parameter included in that equation. The inflow water quality parameter associated with a larger absolute value of ˇ suggests that this parameter contributes more to the variation of the dependent variable (outflow THg or MeHg). A negative ˇ means that R decreases with an increase in the inflow water quality parameters. In the equation of stepwise regression (Table 3), chloride negatively affected both outflow THg and MeHg
Fig. 4. Correlations between inflow DO and sulfate and outflow THg and MeHg at STA-2 before 2004.
concentrations and contributed more to outflow THg and MeHg variations than any of the other inflow water quality parameters, which included sulfate, DOC, DO, pH, and temperature. The contributions of the inflow sulfate, DOC, and DO to the variations of the outflow THg and MeHg were at the same level, negative effects of sulfate and DO and positive effect of DOC on outflow THg and MeHg variations. Furthermore, compared to other water quality parameters, the inflow pH and temperature contributed the least to the outflow THg variation. 4. Discussion 4.1. Comparison of THg and MeHg concentrations between inflow and outflow Over the 12-year monitoring period, STA-2 acted as a source and sink of both THg and MeHg in five and seven years, respectively.
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Table 3 Stepwise regression results between inflow water quality parameters and outflow THg and MeHg from 2000 to 2011. All data were log-transformed prior to correlation analysis. Dependent
Independent (inflow water quality parameters)
Standardized coefficient (ˇ)
R2
Significance
Outflow THg
Chloride Sulfate DO DOC pH Temperature
−1.028 −0.833 −0.806 0.7 0.102 0.103
0.684
p = 0.023
Outflow MeHg
Chloride DOC Sulfate DO
−1.093 0.878 −0.835 −0.626
0.584
p = 0.016
STA-2 often acted as a source in several years after the wetland was constructed and operated. Actually, STA-2 served as a significant source of both THg and MeHg in 2001 and 2002 only (Fig. 3). This is likely attributed to the severe drought during 2000 and 2001 that occurred in both Cells 1 and 2 (Fink et al., 2005). The process of drying and rewetting has been found to provide fuel for Hg methylation and microbial sulfate reduction, thereby causing increased Hg methylation in the wetland (Dmytriw et al., 1995; Gilmour et al., 2004). Dryout and rewetting can also enhance the release of trace metals from soil to the water column, including Hg release from the inorganic and organic binding sites in soil (Dmytriw et al., 1995). Soil dryout leads to the oxidation of OM, iron (II), and sulfide in the surficial soil to labile OM, iron(III), and sulfate, respectively (Dmytriw et al., 1995; Gilmour et al., 2004). The reinundation of soils after dryout is accompanied by a flush release of sulfate, iron, and labile OM (Gilmour et al., 2004). Following the flush release of sulfate and nutrients under anoxic conditions, the metabolic activity of SRB is likely to be stimulated to produce additional MeHg. Before 2004, the dryout and rewetting events in STA-2 provided a favorable condition for the growth of SRB and subsequently enhanced MeHg production. This is evident by the significantly higher outflow vs. inflow MeHg concentrations. The small difference of MeHg between inflow and outflow since 2004 suggests that the conditions in STA-2 since 2004 were no longer suitable for the growth of SRB or MeHg production. Over the 12-year monitoring period, STA-2 acted as a sink for both THg and MeHg during the last four to six years of operation. This suggests that the ability of the constructed treatment wetland to capture both THg and MeHg was improved when it matured and especially after water management was improved to prevent dryout. Such findings are somewhat contrary to some previous studies on the effect of wetlands on Hg retention. For instance, various studies have identified wetlands as a sink of THg but often as a net source of MeHg (Driscoll et al., 1998; Galloway and Branfireun, 2004; Grigal et al., 2000; St. Louis et al., 1996). The level of THg retention in STA-2 (0.35–49%, mean value 21%) was slightly lower than other wetland and upland systems reported in the literature, including 18–80% retention in different types of wetlands over three years (St. Louis et al., 1996), 74% in a beaver pond/riparian wetland (Driscoll et al., 1998), 95% in an upland catchment (Scherbatskoy et al., 1998), and the mean of 69% retention in a temperate forested wetland (Galloway and Branfireun, 2004). In comparison to the literature values of THg retention in other wetlands, STA-2 acted as a modest sink for THg. Hg is known to have a strong affinity for OM (Hurley et al., 1995), which supports the wetland soil retention of THg. Wetland THg retention may also be due to deep leaching to groundwater and considerable rates of Hg0 evasion (Galloway and Branfireun, 2004; Grigal et al., 2000). MeHg retention in STA-2 ranged from 3.5% to 37% (mean value 22%); MeHg retention data in other wetlands for comparison were
not found in literature. The work by Sellers et al. (1996) demonstrates that MeHg is photolytically decomposed in surface waters, and that this process is potentially an important step in the aquatic Hg cycle. Thereby, the photolytic decomposition of MeHg may be one of reasons for the MeHg removal in STA-2. 4.2. Influence of inflow water quality on outflow THg and MeHg The stepwise regression results indicate that inflow chloride, sulfate, DOC, and DO appear in the regression models of both outflow THg and MeHg, suggesting that they are critical inflow water quality parameters influencing outflow THg and MeHg concentrations. Except for the above inflow water quality parameters, only inflow pH and temperature had slightly positive effects on the outflow THg concentration. Among the inflow water quality parameters, sulfate loading to STA-2 was of the most concern in this study. The significant correlation between inflow sulfate load and outflow MeHg illustrated that sulfate input to STA-2 likely stimulated the activity of SRB and played a crucial role in the Hg methylation in the constructed treatment wetland. The buildup of sulfide, the reduced product of sulfate, in sediment porewater appears to inhibit Hg methylation through formation of insoluble HgS, which decreases the Hg availability to SRB (Benoit et al., 1999; Gilmour et al., 1992; Orem et al., 2011). The dual effect of sulfur on Hg methylation, that is, the stimulation effect of sulfate and the inhibition effect of sulfide, is termed the “Goldilocks effect” (Orem, 2007). This conceptual model for the role of sulfur in MeHg production has been verified for the Everglades by field, laboratory, and mesocosm experiments (Orem, 2007). Orem (2004) stated that in the Everglades the areas of highest MeHg production occur where sulfate contamination is moderate (2–10 mg L−1 ) and sulfide levels are low enough to avoid the inhibition of MeHg formation. Gilmour and Henry (1991) proposed an optimal sulfate concentration range of 19–48 mg L−1 (optimum concentration was approximately 29 mg L−1 ) for Hg methylation by SRB in sediments, above which methylation is inhibited and below which sulfate becomes limiting for Hg methylation and sulfate-reduction processes, and Weber (1993) found Hg methylation stops completely at a sulfate concentration exceeding approximately 48 mg L−1 . Gilmour et al. (1992) reported that MeHg production increases with sulfate concentrations up to 10 mg L−1 and declines when porewater sulfide exceeds 0.6 mg L−1 . King et al. (1999) observed active MeHg formation in the presence of 2.88 g L−1 sulfate and millimolar concentrations of dissolved sulfide. In this study, the negatively correlated relationship between inflow sulfate and outflow MeHg indicates that the sulfate concentration in the inflow was much greater than the optimal concentration for MeHg production in STA-2. Similarly, Selvendiran et al. (2008) also demonstrated a significant, negative correlation between MeHg and sulfate concentrations (6.33 ± 0.9 mg L−1 )
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during the growing season in a forested wetland, along with an increase in MeHg concentrations concomitant with the decrease in sulfate in wetland stream waters. In such case, the cycle of drying and rewetting likely promoted the production of MeHg accompanied by the release of THg, leading to the significant correlated relationship between inflow sulfate and outflow THg. Sulfate loading is an important factor in causing increased Hg methylation in the Everglades (Gilmour et al., 2007; Orem et al., 2011). In general, sulfate concentration decreases from north to south in the Everglades ecosystem (Orem, 2004; Orem et al., 2011). The dual effect of sulfur on MeHg production and the north-tosouth gradient in sulfate concentrations in the Everglades provide geographic context to MeHg distributions (Orem et al., 2011). Unenriched areas of the ecosystem with sulfate concentrations less than 1 mg L−1 exhibit low levels of MeHg due to sulfate limitation on Hg methylation (Orem et al., 2011). In sulfate-enriched areas (concentration more than 20 mg L−1 ) buildup of sulfide inhibits MeHg production (Orem et al., 2011). Areas with intermediate concentrations of sulfate (1–20 mg L−1 ) have sulfate levels that promote maximum MeHg production (Gilmour et al., 2007), where porewater sulfide concentrations are moderate (5–150 g L−1 ) (Gilmour et al., 1998; Orem et al., 2011). The influence of chloride on Hg methylation could be attributable to the competition of chloride for binding Hg, forming chloride–mercury complexes with the negatively charged forms (e.g., HgCl3 − , HgCl4 2− ). The neutral form (HgCl2 ) is more bioavailable for microbes than negatively charged forms because its uptake by microbes is likely a passive diffusion process (Barkay et al., 1997; Ullrich et al., 2001). So, the inverse correlation between inflow chloride and outflow MeHg in the stepwise regression indicates that inflow chloride concentration favored the formation of negatively charged chlorine–mercury complexes, which is consistent with other studies. Barkay et al. (1997) reported that when chloride concentrations were above 1 mM, a decreased bioavailability of Hg(II) to the bioindicator was attributed to an increased proportion of negatively charged chlorine–mercury complexes. A previous study has shown that increasing chloride from 0.01 to 0.1 mM sharply reduced Hg adsorption on clay particles (Newton et al., 1976), indicating a positive relationship between chloride and Hg in the watershed under a range of low chloride concentrations. However, the high chloride concentrations in STA-2 and the negative impact on MeHg production are in line with the majority of the studies that high chloride concentration favors the formation of negatively charged chlorine–mercury complex and reduces bioavailability of inorganic mercury. The influence of DOC on Hg availability for SRB methylation is complicated. DOC can act as energy source for microbial activity to stimulate methylation (Ullrich et al., 2001) and can decrease and enhance the bioavailability of Hg to SRB (Gorski, 2004). Hg bioavailability can be reduced by DOC through photochemical reduction of Hg(II) to Hg0 (Ravichandran, 2004) or can be enhanced by the mixed complexes that contain both DOC and reduced sulfur groups (DOC–Hg–SH) (Hsu-Kim and Sedlak, 2005; Miller et al., 2007). DOC also can interact strongly with THg and MeHg, facilitating the mobility of Hg from soils and sediments into watersheds (Ravichandran, 2004). In the Florida Everglades, the DOC concentration is high due to the high natural production of organic carbon in the peat soils (Aiken et al., 2011; Liu et al., 2008), and DOC has been found to be strongly correlated to THg and MeHg in this region (Liu et al., 2008). The observed positive relationship between inflow DOC and outflow THg and MeHg in this study suggests that inflow DOC was an important controlling factor influencing the THg and MeHg concentrations in the watershed of the constructed treatment wetland, either by controlling the bioavailability of Hg or controlling Hg transport and concentration.
Anaerobic conditions favor the activity of SRB and subsequently Hg methylation, while oxygen deficiency is widely known to enhance Hg mobility (Compeau and Bartha, 1985; Gilmour et al., 1992; Kim, 1995; Ullrich et al., 2001); therefore, the significantly negative effects of inflow DO on the outflow THg and MeHg were expected to occur. Generally, Hg methylation in an acidic environment is prone to be enhanced in comparison to alkaline surroundings, and elevated Hg levels in fish are commonly found in acidified lakes (Ullrich et al., 2001). It is uncertain whether the stimulation of methylation in lake water is a direct effect of low pH on the methylation process, or if it is related to other factors that are influenced by pH, such as the loss of volatile Hg species from the water surfaces, or changes in Hg solubility and partitioning (Ullrich et al., 2001). In the laboratory, the maximum rate of Hg methylation occurred at a pH of 4.5 and the formation of Hg hydroxides at higher pH (>8) inhibits the formation of MeHg by reducing inorganic Hg availability to bacteria (Leng and Nies, 1999). Xun et al. (1987) found that net MeHg production in lake water was seven times faster at pH 4.5 than at pH 8.5. As the inflow in STA-2 was slightly alkaline, and there was no significant relationship between inflow pH and outflow MeHg, this may suggest that the range of inflow pH was possibly too small to influence the availability of Hg to methylating microorganisms or to impose any effect on the microbial community. However, the stepwise regression results showed that inflow pH had a slight positive effect on outflow THg, indicating the narrow inflow pH produced little effect on the mobility of THg between the soil and water column. This is consistent with other study finding that showed the pH dependency of Hg solubility and mobility in the watershed (Lee and Hultberg, 1990). Moderately high temperatures have been found to provide a stimulating effect on Hg methylation, which is most likely due to the enhanced microbial activity by the increase in temperature (Ullrich et al., 2001). However, no significant relationship between inflow temperature and outflow MeHg was observed in this study. The seasonal change in water temperature may not impose a significant impact on the microbial activity. But, the significant positive correlation for inflow temperature with the outflow THg suggests that inflow temperature affected the THg mobility between the soil and the water column. 5. Conclusion Results from this study show that STA-2 served as a source of both THg and MeHg at the early stages of operation and as a sink for both THg and MeHg when the constructed treatment wetland became mature and especially as water management was improved to prevent dryout from occurring. The net output of both THg and MeHg during the early years of operation, especially in 2001 and 2002, was primarily attributed to the dryout and rewetting cycles which promoted the Hg methylation and the releases of both THg and MeHg from the soil to the surface water. Stepwise regression results suggest that inflow water quality played an important role on the variations of THg and MeHg at the outflow from 2000 to 2011. Sulfate, chloride, DOC, DO, pH, and temperature were among the biogeochemical parameters at the inflow that significantly impacted outflow THg variation, and only inflow sulfate, chloride, DOC, and DO showed significant effects on outflow MeHg variation. Acknowledgements We greatly appreciate the support for this work from Nankai University, China; University of Florida–Institute of Food and
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