Environmental Management DOI 10.1007/s00267-015-0486-0
Response to Julian et al. (2015) ‘‘Comment on and Reinterpretation of Gabriel et al. (2014) ‘Fish Mercury and Surface Water Sulfate Relationships in the Everglades Protection Area’’’ Mark C. Gabriel1 • Don Axelrad2 • William Orem3 • Todd Z. Osborne4,5
Received: 23 December 2014 / Accepted: 30 March 2015 Springer Science+Business Media New York (outside the USA) 2015
Abstract The purpose of this forum is to respond to a rebuttal submitted by Julian et al., Environ Manag 55:1–5, 2015 where they outlined their overall disagreement with the data preparation, methods, and interpretation of results presented in Gabriel et al. (Environ Manag 53:583–593, 2014). Here, we provide background information on the research premise presented in Gabriel et al. (Environ Manag 53:583–593, 2014) and provide a defense for this work using five themes. In spite of what Julian et al. perceive as limitations in the sampling methods and analytical tools used for this work, the relationships found between fish total mercury and surface water sulfate concentrations in Gabriel et al. (Environ Manag 53:583–593, 2014) are comparable to relationships between pore water methylmercury (MeHg) and pore water sulfate found in past studies indicating that sulfate is important to MeHg production and bioaccumulation in the Everglades. Julian et al. state ‘‘…there is no way to justify any ecosystemwide sulfur strategy as a management approach to reduce
& Mark C. Gabriel [email protected] 1
International Joint Commission, 2000 L Street NW, Suite 615, Washington, DC 20440, USA
2
Institute of Public Health, Florida A&M University, 1515 S. Martin Luther King, Jr. Blvd., Tallahassee, FL 32307, USA
3
U.S. Geological Survey, 12201 Sunrise Valley Dr., Reston, VA 20192, USA
4
Wetland Biogeochemistry Laboratory, Soil and Water Science Department, University of Florida, 2181 McCarty Hall A, P.O. Box 11029, Gainesville, FL 32611, USA
5
Whitney Laboratory for Marine Bioscience, University of Florida, 9505 N Ocean Shore Blvd, St. Augustine, FL 32080, USA
mercury risk in the (Everglades) as suggested by Gabriel et al. (Environ Manag 53:583–593, 2014), Corrales et al. (Sci Tot Environ 409:2156–2162, 2011) and Orem et al. (Rev Environ Sci Technol 41 (S1):249–288, 2011).’’ We disagree, and having stated why sulfate input reduction to the Everglades may be the most effective means of reducing mercury in Everglades fish, it is important that research on sulfur and mercury biogeochemistry continues. If further studies support the relationship between sulfate loading reduction and MeHg reduction, sulfur mass balance studies should commence to (1) better quantify agricultural and connate seawater sulfate inputs and (2) define opportunities to reduce sulfate inputs to the Everglades ecosystem. Keywords
Everglades Sulfate Mercury Fish
Julian et al. (2015) provided a detailed evaluation of our publication (Gabriel et al. 2014) and outlined their overall disagreement with our data preparation, methods, and interpretation of results. We, however, believe their evaluation of our paper is flawed and it is in the best interest of the mercury and sulfur research field to defend our work and provide additional supporting information. As stated, the primary objectives of our paper were to (1) compare fish THg (total mercury) and surface water sulfate concentrations across multiple monitoring stations within the Everglades Protection Area (EvPA) and (2) provide interpretation of our results. In support of the original work and interpretation, we first identify how and why the research initiative for our publication was developed. In 2008, at an Everglades Mercury and Sulfur technical meeting held at the South Florida Water Management District (SFWMD), expert
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researchers in the field of mercury and sulfur science from multiple agencies including the Florida Department of Environmental Protection, collectively agreed on a simple and valuable approach to further understand the relative importance of sulfate on methylmercury (MeHg) production in the Everglades ecosystem. This agreed approach consisted in mining available datasets on fish THg and surface water sulfate across Everglades monitoring stations, pairing these data on a station-by-station basis, and plotting these data across space and time (FDEP 2008). It was suggested that these data could then be compared to plots involving sediment pore water sulfate vs. MeHg concentration generated by past field and laboratory studies. The research premise for this comparison was that if data plots for surface water sulfate versus fish THg were similar in form to pore water sulfate versus pore water MeHg, this result would further highlight the significance of sulfate to MeHg production. In addition to investigating the importance of sulfate to MeHg production, these data plots could also be used to highlight the sulfate conditions that contained the highest fish THg concentrations. Past research has shown that sulfate has a dual effect on MeHg production (Gilmour et al. 1992, 2007a; Benoit et al. 1999a, b, 2003; Axelrad et al. 2008). Low sulfate concentration limits MeHg production and high sulfate concentration produces sulfide which suppresses microbial MeHg production. This dual effect of sulfur on mercury methylation results in maximum MeHg production in so-called ‘‘Goldilocks’’ zones where sulfate and sulfide levels are just right for mercury methylation (Frederick et al. 2005). Conversely, if plots of sulfate versus fish THg did not present a data pattern that resembled a ‘‘Goldilocks’’ curve (i.e., unimodal trend), this result would point to the cumulative importance of other processes in generating/limiting MeHg, e.g., iron reduction, methanogenesis, pH effects, dissolved organic carbon (DOC). As discussed by researchers at the 2008 meeting, what prevented this type of comparison from being developed previously was the difficulty in obtaining long-term sulfate and fish THg data for multiple species over an entire ecosystem. The results of our study (Gabriel et al. 2014) were that peak fish THg levels for all fish species occurred in *1–12 mg/L surface water sulfate which is a similar sulfate range (2–20 mg/L) for peak MeHg production in sediments as determined by others (Gilmour et al. 1992, 2007a; Benoit et al. 1999a, b). Our findings for fish THg versus surface water sulfate were evident for three fish trophic levels: mosquitofish, sunfish, and large-mouth bass. Julian et al. (2015) examined our publication and discussed their disagreement with our methods, data interpretation, and discussion of results. Here, we respond to the main themes of their disagreements, as follows.
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Importance of Sulfate Reduction We fully agree with Julian et al. (2015) that there are several factors that can limit MeHg production. But even with the limitations in our methods and data preparation, as they perceive them, we show that peak THg concentrations for three trophic levels of fish occurred between *1 and 12 mg/L surface water sulfate which is in agreement with past studies showing peak MeHg production occurs over 2–20 mg/L pore water sulfate (Gilmour et al. 2007a). We do not believe this similarity in peak fish THg and MeHg production is coincidental. The fish data used in this study were collected throughout multiple biogeochemical conditions in the Everglades and, as expected, the fish THg concentration data demonstrate significant variability across the sulfate range. What is causing the variability in fish THg concentrations are spatiotemporal variations in factors that influence mercury methylation (e.g., pH, DOC, competing ions, bioavailable mercury) and factors that influence bioaccumulation (feeding patterns and source, fish age and type, food chain dynamics, etc.,). Even with the large number of factors that can impact MeHg production and bioaccumulation, the ‘‘Goldilocks’’ signature is evident in our plots, indicating the importance of sulfate reduction on MeHg production. Plots of MeHg production in sediment versus sulfate concentrations across the ecosystem also follow such unimodal ‘‘Goldilocks’’ form (Gilmour et al. 1992, 2007a; Benoit et al. 1999a, b). This type of response to sulfate occurs despite large variability in other factors such as pH, DOC, competing ions, and bioavailable mercury concentrations, suggesting that these other factors are secondary to the importance of sulfate levels.
Data Preparation The methods we used to standardize/normalize fish THg concentrations for data analysis are the same as those accepted and used by SFWMD (see Chapter 3 in past SFWMD Reports), which is the state agency where our raw data were obtained. The only difference in our study was the use of age-1 large-mouth bass, instead of the commonly used age-3. We used age-1 because it was the most abundant age group for the period of record (1998–2009). For standardization and comparability reasons, we did not combine age-1 and 3 fish data or any other age. We agree with Julian et al. (2015) that fish THg concentration can vary by gender and species, but we maximized the use of our large data sets by combining these factors. We recognize that this approach likely added data variability in our plots. Even so, the familiar ‘‘Goldilocks’’ relationship between surface water sulfate and fish THg is evident.
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Station Selection and Pairing Julian et al. (2015) question why we paired certain monitoring stations and used stations that were outside the EvPA marsh areas. As mentioned in our paper, fish and sulfate monitoring stations were matched based on their proximity and hydrologic connection to each other over the analysis period of 1998–2009. Using stations outside the natural wetlands ecosystem, i.e., in canals, was beneficial because we added data from sites with contrasting flow regimes and sediment biogeochemistry, thus providing a more comprehensive assessment. All of our sites are within the Everglades watershed, and the watershed is the relevant boundary for fish and mercury data. We recognize that using stations within and outside the jurisdictional boundaries of the EvPA, this also likely increased the data variability in our plots, nonetheless peak fish THg occurred in *1–12 mg/L surface water sulfate.
Quantitative Statistics Julian et al. (2015) mention that no quantitative statistics were used to identify trends. We did not apply their suggested quantitative statistics, (i.e., fitting a non-linear trend to our data) because our intention was not to develop a predictive model(s), but rather to highlight the general trends in our data. We believe the use of running averages for our purpose was suitable. Julian et al. (2015) also argue that by presenting the interquartile ranges, we eliminated 50 % of the data variability. Their point was misleading as detailed. The median and inner quartile reflect the central tendency of all data in a population, in this case, each station. It is important for the reader to know that each median and inner quartile in our study reflect tens to hundreds of data points (see Fig. 3 caption in Gabriel et al. 2014); therefore, there is substantial power in both statistical measures. We log-transformed the data at the request of one of the manuscript peer reviewers purely for visual clarity which facilitated illustration of the data spread and increase in fish THg above 1 mg/L sulfate.
Ecosystem Management Implications As it pertains to microbial-mediated sulfate reduction, the primary factors involved in regulating MeHg production are pH, water temperature, electron acceptors (in this case sulfate), labile organic carbon, redox potential, competing ions (and their interactions), and bioavailable mercury. There is little that can be done to limit atmospheric mercury deposition because most deposition originates outside
Florida. Therefore, out of these regulating factors, sulfate is the only factor that could be directly altered through management practices in some capacity, and its alteration would impact MeHg production in Everglades sediments. We agree in theory that there could be biogeochemical factors other than sulfur that have a large impact on MeHg production and might be more practical to manage for the purposes of curbing MeHg production, but to date, no such factors have been identified conclusively. Further, much Everglades research links sulfate concentrations in the Everglades to MeHg production (Gilmour et al. 1992, 2007a; Benoit et al. 1999a, b, 2003; Axelrad et al. 2008). Recent research demonstrates a unimodal relationship between sulfate concentrations in Everglades surface water and fish THg (Pollman 2014; Pollman and Axelrad 2014). Even with sulfate’s clear impact on MeHg production, we still encourage future development of studies to explore the potential importance of non-sulfate-related factors on MeHg production. Julian et al. criticize the proposition that the implementation of an ecosystem strategy to reduce sulfate loading to the ecosystem, as a way to reduce mercury levels in fish has no merit. Their criticism ignores a wealth of evidence clearly linking sulfate loading to MeHg production and bioaccumulation in the Everglades (Axelrad et al. 2007, 2008, 2009, 2011; Bates et al. 2001, 2002; Benoit et al. 2003; Gabriel et al. 2008, 2010; Gilmour et al. 1992, 1998, 2007a, b; Orem 2004, 2007, 2011) and in other ecosystems (e.g., Harmon et al. 2004, 2007; Jeremiason et al. 2006). These field studies from across the Everglades show the unimodal link between sulfate loading and MeHg production. Mesocosm experiments in the ecosystem conducted at five different sites also clearly demonstrate that the addition of sulfate stimulates MeHg production and bioaccumulation up to a point when buildup of sulfide from excessive sulfate loading inhibits mercury methylation (Orem et al. 2011). Laboratory microcosm experiments using Everglades soil also demonstrate this relationship (Orem et al. 2011). Perhaps more useful commentary by our colleagues would have begun with recognition of the role of sulfate in MeHg production followed by discussion of the logistical constraints of conducting sulfur control programs in the EvPA. Julian et al. (2015), also fail to mention the other known benefits of reducing sulfate loading to the ecosystem. Sulfate loading has dramatically changed the basic microbial ecology of the ecosystem, from one dominated by methanogenesis to a system dominated by sulfate reduction. Sulfate reduction, a far more efficient biodegradation mechanism, may reduce organic soil accretion in the Everglades compared to the historical methanogenic conditions. Sulfide, a principal by-product of microbial sulfate reduction, is a toxic substance. Portions of the ecosystem
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heavily impacted by sulfate loading have surface water sulfide levels that exceed USEPA guidelines for levels of sulfide toxic to aquatic fauna (Orem et al. 2011). Studies also suggest that sulfide buildup in organic soils in the Everglades may be toxic to some types of aquatic macrophytes (Chabbi et al. 2000; Koch and Mendelssohn 1989; Koch et al. 1990; Li et al. 2009; Lissner et al. 2003). Several estimates of sulfur inputs to the Everglades from or through the Everglades Agricultural Area (EAA) to the Everglades have been made (Schueneman 2001, Gabriel et al. 2010; Corrales et al. 2011; Gu et al. 2012; James and McCormick 2012; Landing 2014). Three main sources of sulfur input from or through the 700,000 acre EAA to the Everglades are soil oxidation in the EAA, inputs from Lake Okeechobee, and agricultural sulfur applications in the EAA. In a recent paper, Ye et al. (2010) have shown that one of the biggest sources of sulfate loading from agriculture amendments, addition of elemental sulfur to adjust pH for more efficient phosphorus uptake by sugarcane in the EAA (Boswell and Friesen 1993), is not producing the desired effect. This result is from high levels of carbonate in EAA soils buffering the intended effect of elemental sulfur additions. Eliminating this source of sulfur to the ecosystem could save farmers money by removing an agricultural chemical that is not having the intended beneficial effect to sugarcane. Other potential strategies for mitigating sulfate loading could include reducing groundwater flux from leaky canal bottoms, reducing soil oxidation in the EAA or modifying existing STAs to remove more sulfate.
Conclusions We appreciate the critical review provided by Julian et al. (2015); however, in spite of what our colleagues perceive as limitations in our sampling methods and analytical tools, the relationships found between fish THg and Everglades surface water sulfate in our study (Gabriel et al. 2014) are comparable to trends between sediment MeHg and sulfate found in many past studies, and the methods we used to generate our data plots are scientifically valid. Considering the large number of ecosystem factors that can impact MeHg production and bioaccumulation, including the challenges related to the collection, standardization, and presentation of these data, our plots show peak fish THg occurred in *1–12 mg/L surface water sulfate. This ‘‘Goldilocks’’ signature indicates that sulfate is an important factor in MeHg production and bioaccumulation in fish in the Everglades, an ecosystem of international significance that is threatened by very high levels of mercury in the food chain. Our findings support the need for continued research in order to determine anthropogenic sources of sulfur to the
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Everglades and sulfate reductions necessary to reduce mercury to safe levels (Landing 2014). Acknowledgments Drs. Mark C. Gabriel and Todd Z. Osborne once again thank the South Florida Water Management District for providing the data used in this study and the anonymous reviewers for their helpful comments and suggestions. We also thank Curt Pollman for providing helpful technical insight toward the development of this forum. Financial support was provided by the University of Florida to publish this manuscript.
References Axelrad DM, Atkeson TD, Lange T, Gilmour CC, Pollman CD, Orem WH, Mendelssohn IA, Frederick PC, Krabbenhoft DP, Aiken GR, Rumbold DG, Scheidt DJ, Kalla PI (2007) Mercury monitoring, research and environmental assessment in South Florida. 2007 South Florida Environmental Report, Chapter 3B. South Florida Water Management District, West Palm Beach Axelrad DM, Lange T, Gabriel M, Atkeson TD, Pollman CD, Orem WH, Scheidt DJ, Kalla PI, Frederick PC, Gilmour CC (2008) Mercury and sulfur monitoring, research and environmental assessment in South Florida. South Florida Environmental Report, Chapter 3B. South Florida Water Management District, West Palm Beach Axelrad DM, Lange T, Atkeson TD, Gabriel MC (2009) Mercury and sulfur monitoring research and environmental assessment in South Florida. South Florida Environmental Report, Chapter 3B. South Florida Water Management District, West Palm Beach Axelrad DM, Gabriel MC, Lange T, Aiken GR, Brandon A, Cunningham MW, DeBusk T, Dierberg F, Donner BA, Frederick P, Gilmour C, Harris R, Jansen D, Krabbenhoft DP, McCray JM, Orem WH, Oronato DP, Pollman CD, Rumbold DG, White G, Wright AL, Ye R (2011) Mercury and Sulfur Monitoring, Research and Environmental Assessment in South Florida. South Florida Environmental Report, Chapter 3B. South Florida Water Management District, West Palm Beach Bates AL, Orem WH, Harvey JW, Spiker EC (2001) Geochemistry of Sulfur in the Florida Everglades; 1994 through 1999. U.S. Geological Survey Open-File Report 01-0007 Bates AL, Orem WH, Harvey JW, Spiker EC (2002) Tracing sources of sulfur in the Florida Everglades. J Environ Qual 31:287–299 Benoit JM, Gilmour CC, Mason RP, Heyes A (1999a) Sulfide controls on mercury speciation and bioavailability in sediment pore waters. Environ Sci Technol 33:951–957 Benoit JM, Mason RP, Gilmour CC (1999b) Estimation of mercury sulfide speciation in sediment pore waters using octanol–water partitioning and implications for availability to methylating bacteria. Environ Toxicol Chem 18:2138–2141 Benoit J, Gilmour CC, Heyes A, Mason RP, Miller C (2003) Geochemical and biological controls over methylmercury production and degradation in aquatic ecosystems. In: Y Chai, OC Braids (eds) Biogeochemistry of environmentally important trace elements. ACS Symposium Series #835, pp. 262–297. American Chemical Society, Washington, DC Boswell CC, Friesen DK (1993) Elemental sulfur fertilizers and their use on crops and pastures. Fertil Res 35:127–149 Chabbi A, McKee KL, Mendelssohn IA (2000) Fate of oxygen losses from Typha domingensis (Typhaceae) and Cladium jamaicense (Cyperaceae) and consequences for root metabolism. Am J Bot 87:1081–1090 Corrales J, Naja GM, Dziuba C, Rivero RG, Orem W (2011) Sulfate threshold target to control methylmercury levels in wetland ecosystems. Sci Tot Environ 409:2156–2162
Environmental Management Florida Department of Environmental Protection (FDEP) (2008) Everglades Mercury and Sulfur Workshop Notes. February 13, 2008 Frederick P, Axelrad D, Atkeson T, Pollman C (2005) Contaminants research and policy: the Everglades mercury story. Natl WetlNewsl 27:3–6 Gabriel MC, Redfield G, Rumbold D (2008) Sulfur as a regional water quality concern in South Florida, South Florida Environmental Report, Appendix 3B-2. South Florida Water Management District, West Palm Beach Gabriel MC, Axelrad D, Lange T, Dirk L (2010) Mercury and sulfur monitoring, research and environmental assessment in South Florida. 2010 South Florida Environmental Report, Chapter 3B. South Florida Water Management District, West Palm Beach Gabriel MC, Howard N, Osborne TZ (2014) Fish mercury and surface water sulfate relationships in the Everglades protection area. Environ Manag 53:583–593 Gilmour CC, Henry EA, Mitchell R (1992) Sulfate stimulation of mercury methylation in freshwater sediments. Environ Sci Technol 26:2281–2287 Gilmour C, Riedel GS, Ederington MC, Bell JT, Benoit JM, Gill GA, Stordal MC (1998) Methylmercury concentrations and production rates across a trophic gradient in the northern Everglades. Biogeochem 40:327–345 Gilmour CC, Krabbenhoft D, Orem W, Aiken G, Roden E (2007a) Appendix 3B-2: status report on ACME studies on the control of mercury methylation and bioaccumulation in the everglades. 2007 South Florida Environmental Report—vol I. South Florida Water Management District, West Palm Beach Gilmour C, Orem W, Krabbenhoft D, Roy S, Mendelssohn I (2007b) Preliminary assessment of sulfur sources, trends and effects in the Everglades. 2007 South Florida Environmental Report, Appendix 3B-3. South Florida Water Management District, West Palm Beach Gu B, Axelrad D, Lange T (2012) Chapter 3B: regional mercury and sulfur monitoring and environmental assessment. 2012 South Florida environmental report—vol I. South Florida Water Management District, West Palm Beach Harmon SM, King JK, Gladden JB, Chandler GT, Newman LA (2004) Methylmercury formation in a wetland mesocosm amended with sulfate. Environ Sci Technol 38:650–656 Harmon SM, King JK, Gladden JB, Newman LA (2007) Using sulfate amended sediment slurry batch reactors to evaluate mercury methylation. Arch Environ Contam Toxicol 52:326–331 James RT, McCormick PV (2012) The sulfate budget of a shallow subtropical lake. Fundam Appl Limnol 181:253–269 Jeremiason JD, Engstrom DR, Swain EB, Nater EA, Johnson BM, Almendinger JE, Monson BA, Kolka RK (2006) Sulfate addition
increases methylmercury production in an experimental wetland. Environ Sci Technol 40:3800–3806 Julian P, Gu B, Redfield G (2015) Comment on and reinterpretation of Gabriel et al. (2014) fish mercury and surface water sulfate relationships in the Everglades protection area. Environ Manag 55:1–5 Koch MS, Mendelssohn IA (1989) Sulfide as a soil phytotoxic: differential responses in two marsh species. J Ecol 77:565–578 Koch MS, Mendelssohn IA, McKee KL (1990) Mechanism for the hydrogen sulphide-induced growth limitation in wetland macrophytes. Limnol Oceanogr 35:399–408 Landing WM (2014) Peer review report on the Everglades agricultural area regional sulfur mass balance: technical Webinar: November 20, 2013. South Florida Water Management District, West Palm Beach Li S, Mendelssohn IA, Chen H, Orem WH (2009) Does sulfate enrichment promote Typha domingensis (cattail) expansion into the Cladium jamaicence (sawgrass)-dominated Florida Everglades? Freshw Biol 54:1909 Lissner J, Mendelssohn IA, Lorenzen B, Brix H, McKee KL, Miao S (2003) Interactive effects of redox intensity and phosphate availability on growth and nutrient relations of Cladium jamaicense (Cyperaceae). Am J Botany 90:736–748 Orem WH (2004) Impacts of sulfate contamination on the Florida Everglades ecosystem. USGS Fact Sheet FS 109-03 Orem W (2007) Sulfur contamination in the Florida Everglades: Initial examination of mitigation strategies: U.S. Geological Survey Open-File Report 2007-1374. http://sofia.usgs.gov/pub lications/ofr/2007-1374/ Orem W, Gilmour C, Axelrad D, Krabbenhoft D, Scheidt D, Kalla P, McCormick P, Gabriel M, Aiken G (2011) Sulfur in the South Florida ecosystem: distribution, sources, biogeochemistry, impacts, and management for restoration. Rev Environ Sci Technol 41(S1):249–288 Pollman CD (2014) Mercury cycling in aquatic ecosystems and trophic-state related variables—implications from structural equation modeling. Sci Tot Environ 499:62–73 Pollman CD, Axelrad DM (2014) Mercury Bioaccumulation and Bioaccumulation factors for Everglades Mosquitofish as Related to sulfate: a reanalysis of Julian II (2013). Bull Environ Contam Toxicol 93:509–516 Schueneman TJ (2001) Characterization of sulfur sources in the EAA. Soil Crop Sci Soc Fla 60:49–52 Ye R, Wright AL, Orem WH, McCray JM (2010) Sulfur distribution and transformations in Everglades agricultural area soil as influenced by sulfur amendment. Soil Sci 175:263–269
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Response to Julian et al. (2015) ‘‘Comment on and Reinterpretation of Gabriel et al. (2014) ‘Fish Mercury and Surface Water Sulfate Relationships in the Everglades Protection Area’’’ Mark C. Gabriel1 • Don Axelrad2 • William Orem3 • Todd Z. Osborne4,5
Received: 23 December 2014 / Accepted: 30 March 2015 Springer Science+Business Media New York (outside the USA) 2015
Abstract The purpose of this forum is to respond to a rebuttal submitted by Julian et al., Environ Manag 55:1–5, 2015 where they outlined their overall disagreement with the data preparation, methods, and interpretation of results presented in Gabriel et al. (Environ Manag 53:583–593, 2014). Here, we provide background information on the research premise presented in Gabriel et al. (Environ Manag 53:583–593, 2014) and provide a defense for this work using five themes. In spite of what Julian et al. perceive as limitations in the sampling methods and analytical tools used for this work, the relationships found between fish total mercury and surface water sulfate concentrations in Gabriel et al. (Environ Manag 53:583–593, 2014) are comparable to relationships between pore water methylmercury (MeHg) and pore water sulfate found in past studies indicating that sulfate is important to MeHg production and bioaccumulation in the Everglades. Julian et al. state ‘‘…there is no way to justify any ecosystemwide sulfur strategy as a management approach to reduce
& Mark C. Gabriel [email protected] 1
International Joint Commission, 2000 L Street NW, Suite 615, Washington, DC 20440, USA
2
Institute of Public Health, Florida A&M University, 1515 S. Martin Luther King, Jr. Blvd., Tallahassee, FL 32307, USA
3
U.S. Geological Survey, 12201 Sunrise Valley Dr., Reston, VA 20192, USA
4
Wetland Biogeochemistry Laboratory, Soil and Water Science Department, University of Florida, 2181 McCarty Hall A, P.O. Box 11029, Gainesville, FL 32611, USA
5
Whitney Laboratory for Marine Bioscience, University of Florida, 9505 N Ocean Shore Blvd, St. Augustine, FL 32080, USA
mercury risk in the (Everglades) as suggested by Gabriel et al. (Environ Manag 53:583–593, 2014), Corrales et al. (Sci Tot Environ 409:2156–2162, 2011) and Orem et al. (Rev Environ Sci Technol 41 (S1):249–288, 2011).’’ We disagree, and having stated why sulfate input reduction to the Everglades may be the most effective means of reducing mercury in Everglades fish, it is important that research on sulfur and mercury biogeochemistry continues. If further studies support the relationship between sulfate loading reduction and MeHg reduction, sulfur mass balance studies should commence to (1) better quantify agricultural and connate seawater sulfate inputs and (2) define opportunities to reduce sulfate inputs to the Everglades ecosystem. Keywords
Everglades Sulfate Mercury Fish
Julian et al. (2015) provided a detailed evaluation of our publication (Gabriel et al. 2014) and outlined their overall disagreement with our data preparation, methods, and interpretation of results. We, however, believe their evaluation of our paper is flawed and it is in the best interest of the mercury and sulfur research field to defend our work and provide additional supporting information. As stated, the primary objectives of our paper were to (1) compare fish THg (total mercury) and surface water sulfate concentrations across multiple monitoring stations within the Everglades Protection Area (EvPA) and (2) provide interpretation of our results. In support of the original work and interpretation, we first identify how and why the research initiative for our publication was developed. In 2008, at an Everglades Mercury and Sulfur technical meeting held at the South Florida Water Management District (SFWMD), expert
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researchers in the field of mercury and sulfur science from multiple agencies including the Florida Department of Environmental Protection, collectively agreed on a simple and valuable approach to further understand the relative importance of sulfate on methylmercury (MeHg) production in the Everglades ecosystem. This agreed approach consisted in mining available datasets on fish THg and surface water sulfate across Everglades monitoring stations, pairing these data on a station-by-station basis, and plotting these data across space and time (FDEP 2008). It was suggested that these data could then be compared to plots involving sediment pore water sulfate vs. MeHg concentration generated by past field and laboratory studies. The research premise for this comparison was that if data plots for surface water sulfate versus fish THg were similar in form to pore water sulfate versus pore water MeHg, this result would further highlight the significance of sulfate to MeHg production. In addition to investigating the importance of sulfate to MeHg production, these data plots could also be used to highlight the sulfate conditions that contained the highest fish THg concentrations. Past research has shown that sulfate has a dual effect on MeHg production (Gilmour et al. 1992, 2007a; Benoit et al. 1999a, b, 2003; Axelrad et al. 2008). Low sulfate concentration limits MeHg production and high sulfate concentration produces sulfide which suppresses microbial MeHg production. This dual effect of sulfur on mercury methylation results in maximum MeHg production in so-called ‘‘Goldilocks’’ zones where sulfate and sulfide levels are just right for mercury methylation (Frederick et al. 2005). Conversely, if plots of sulfate versus fish THg did not present a data pattern that resembled a ‘‘Goldilocks’’ curve (i.e., unimodal trend), this result would point to the cumulative importance of other processes in generating/limiting MeHg, e.g., iron reduction, methanogenesis, pH effects, dissolved organic carbon (DOC). As discussed by researchers at the 2008 meeting, what prevented this type of comparison from being developed previously was the difficulty in obtaining long-term sulfate and fish THg data for multiple species over an entire ecosystem. The results of our study (Gabriel et al. 2014) were that peak fish THg levels for all fish species occurred in *1–12 mg/L surface water sulfate which is a similar sulfate range (2–20 mg/L) for peak MeHg production in sediments as determined by others (Gilmour et al. 1992, 2007a; Benoit et al. 1999a, b). Our findings for fish THg versus surface water sulfate were evident for three fish trophic levels: mosquitofish, sunfish, and large-mouth bass. Julian et al. (2015) examined our publication and discussed their disagreement with our methods, data interpretation, and discussion of results. Here, we respond to the main themes of their disagreements, as follows.
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Importance of Sulfate Reduction We fully agree with Julian et al. (2015) that there are several factors that can limit MeHg production. But even with the limitations in our methods and data preparation, as they perceive them, we show that peak THg concentrations for three trophic levels of fish occurred between *1 and 12 mg/L surface water sulfate which is in agreement with past studies showing peak MeHg production occurs over 2–20 mg/L pore water sulfate (Gilmour et al. 2007a). We do not believe this similarity in peak fish THg and MeHg production is coincidental. The fish data used in this study were collected throughout multiple biogeochemical conditions in the Everglades and, as expected, the fish THg concentration data demonstrate significant variability across the sulfate range. What is causing the variability in fish THg concentrations are spatiotemporal variations in factors that influence mercury methylation (e.g., pH, DOC, competing ions, bioavailable mercury) and factors that influence bioaccumulation (feeding patterns and source, fish age and type, food chain dynamics, etc.,). Even with the large number of factors that can impact MeHg production and bioaccumulation, the ‘‘Goldilocks’’ signature is evident in our plots, indicating the importance of sulfate reduction on MeHg production. Plots of MeHg production in sediment versus sulfate concentrations across the ecosystem also follow such unimodal ‘‘Goldilocks’’ form (Gilmour et al. 1992, 2007a; Benoit et al. 1999a, b). This type of response to sulfate occurs despite large variability in other factors such as pH, DOC, competing ions, and bioavailable mercury concentrations, suggesting that these other factors are secondary to the importance of sulfate levels.
Data Preparation The methods we used to standardize/normalize fish THg concentrations for data analysis are the same as those accepted and used by SFWMD (see Chapter 3 in past SFWMD Reports), which is the state agency where our raw data were obtained. The only difference in our study was the use of age-1 large-mouth bass, instead of the commonly used age-3. We used age-1 because it was the most abundant age group for the period of record (1998–2009). For standardization and comparability reasons, we did not combine age-1 and 3 fish data or any other age. We agree with Julian et al. (2015) that fish THg concentration can vary by gender and species, but we maximized the use of our large data sets by combining these factors. We recognize that this approach likely added data variability in our plots. Even so, the familiar ‘‘Goldilocks’’ relationship between surface water sulfate and fish THg is evident.
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Station Selection and Pairing Julian et al. (2015) question why we paired certain monitoring stations and used stations that were outside the EvPA marsh areas. As mentioned in our paper, fish and sulfate monitoring stations were matched based on their proximity and hydrologic connection to each other over the analysis period of 1998–2009. Using stations outside the natural wetlands ecosystem, i.e., in canals, was beneficial because we added data from sites with contrasting flow regimes and sediment biogeochemistry, thus providing a more comprehensive assessment. All of our sites are within the Everglades watershed, and the watershed is the relevant boundary for fish and mercury data. We recognize that using stations within and outside the jurisdictional boundaries of the EvPA, this also likely increased the data variability in our plots, nonetheless peak fish THg occurred in *1–12 mg/L surface water sulfate.
Quantitative Statistics Julian et al. (2015) mention that no quantitative statistics were used to identify trends. We did not apply their suggested quantitative statistics, (i.e., fitting a non-linear trend to our data) because our intention was not to develop a predictive model(s), but rather to highlight the general trends in our data. We believe the use of running averages for our purpose was suitable. Julian et al. (2015) also argue that by presenting the interquartile ranges, we eliminated 50 % of the data variability. Their point was misleading as detailed. The median and inner quartile reflect the central tendency of all data in a population, in this case, each station. It is important for the reader to know that each median and inner quartile in our study reflect tens to hundreds of data points (see Fig. 3 caption in Gabriel et al. 2014); therefore, there is substantial power in both statistical measures. We log-transformed the data at the request of one of the manuscript peer reviewers purely for visual clarity which facilitated illustration of the data spread and increase in fish THg above 1 mg/L sulfate.
Ecosystem Management Implications As it pertains to microbial-mediated sulfate reduction, the primary factors involved in regulating MeHg production are pH, water temperature, electron acceptors (in this case sulfate), labile organic carbon, redox potential, competing ions (and their interactions), and bioavailable mercury. There is little that can be done to limit atmospheric mercury deposition because most deposition originates outside
Florida. Therefore, out of these regulating factors, sulfate is the only factor that could be directly altered through management practices in some capacity, and its alteration would impact MeHg production in Everglades sediments. We agree in theory that there could be biogeochemical factors other than sulfur that have a large impact on MeHg production and might be more practical to manage for the purposes of curbing MeHg production, but to date, no such factors have been identified conclusively. Further, much Everglades research links sulfate concentrations in the Everglades to MeHg production (Gilmour et al. 1992, 2007a; Benoit et al. 1999a, b, 2003; Axelrad et al. 2008). Recent research demonstrates a unimodal relationship between sulfate concentrations in Everglades surface water and fish THg (Pollman 2014; Pollman and Axelrad 2014). Even with sulfate’s clear impact on MeHg production, we still encourage future development of studies to explore the potential importance of non-sulfate-related factors on MeHg production. Julian et al. criticize the proposition that the implementation of an ecosystem strategy to reduce sulfate loading to the ecosystem, as a way to reduce mercury levels in fish has no merit. Their criticism ignores a wealth of evidence clearly linking sulfate loading to MeHg production and bioaccumulation in the Everglades (Axelrad et al. 2007, 2008, 2009, 2011; Bates et al. 2001, 2002; Benoit et al. 2003; Gabriel et al. 2008, 2010; Gilmour et al. 1992, 1998, 2007a, b; Orem 2004, 2007, 2011) and in other ecosystems (e.g., Harmon et al. 2004, 2007; Jeremiason et al. 2006). These field studies from across the Everglades show the unimodal link between sulfate loading and MeHg production. Mesocosm experiments in the ecosystem conducted at five different sites also clearly demonstrate that the addition of sulfate stimulates MeHg production and bioaccumulation up to a point when buildup of sulfide from excessive sulfate loading inhibits mercury methylation (Orem et al. 2011). Laboratory microcosm experiments using Everglades soil also demonstrate this relationship (Orem et al. 2011). Perhaps more useful commentary by our colleagues would have begun with recognition of the role of sulfate in MeHg production followed by discussion of the logistical constraints of conducting sulfur control programs in the EvPA. Julian et al. (2015), also fail to mention the other known benefits of reducing sulfate loading to the ecosystem. Sulfate loading has dramatically changed the basic microbial ecology of the ecosystem, from one dominated by methanogenesis to a system dominated by sulfate reduction. Sulfate reduction, a far more efficient biodegradation mechanism, may reduce organic soil accretion in the Everglades compared to the historical methanogenic conditions. Sulfide, a principal by-product of microbial sulfate reduction, is a toxic substance. Portions of the ecosystem
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heavily impacted by sulfate loading have surface water sulfide levels that exceed USEPA guidelines for levels of sulfide toxic to aquatic fauna (Orem et al. 2011). Studies also suggest that sulfide buildup in organic soils in the Everglades may be toxic to some types of aquatic macrophytes (Chabbi et al. 2000; Koch and Mendelssohn 1989; Koch et al. 1990; Li et al. 2009; Lissner et al. 2003). Several estimates of sulfur inputs to the Everglades from or through the Everglades Agricultural Area (EAA) to the Everglades have been made (Schueneman 2001, Gabriel et al. 2010; Corrales et al. 2011; Gu et al. 2012; James and McCormick 2012; Landing 2014). Three main sources of sulfur input from or through the 700,000 acre EAA to the Everglades are soil oxidation in the EAA, inputs from Lake Okeechobee, and agricultural sulfur applications in the EAA. In a recent paper, Ye et al. (2010) have shown that one of the biggest sources of sulfate loading from agriculture amendments, addition of elemental sulfur to adjust pH for more efficient phosphorus uptake by sugarcane in the EAA (Boswell and Friesen 1993), is not producing the desired effect. This result is from high levels of carbonate in EAA soils buffering the intended effect of elemental sulfur additions. Eliminating this source of sulfur to the ecosystem could save farmers money by removing an agricultural chemical that is not having the intended beneficial effect to sugarcane. Other potential strategies for mitigating sulfate loading could include reducing groundwater flux from leaky canal bottoms, reducing soil oxidation in the EAA or modifying existing STAs to remove more sulfate.
Conclusions We appreciate the critical review provided by Julian et al. (2015); however, in spite of what our colleagues perceive as limitations in our sampling methods and analytical tools, the relationships found between fish THg and Everglades surface water sulfate in our study (Gabriel et al. 2014) are comparable to trends between sediment MeHg and sulfate found in many past studies, and the methods we used to generate our data plots are scientifically valid. Considering the large number of ecosystem factors that can impact MeHg production and bioaccumulation, including the challenges related to the collection, standardization, and presentation of these data, our plots show peak fish THg occurred in *1–12 mg/L surface water sulfate. This ‘‘Goldilocks’’ signature indicates that sulfate is an important factor in MeHg production and bioaccumulation in fish in the Everglades, an ecosystem of international significance that is threatened by very high levels of mercury in the food chain. Our findings support the need for continued research in order to determine anthropogenic sources of sulfur to the
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Everglades and sulfate reductions necessary to reduce mercury to safe levels (Landing 2014). Acknowledgments Drs. Mark C. Gabriel and Todd Z. Osborne once again thank the South Florida Water Management District for providing the data used in this study and the anonymous reviewers for their helpful comments and suggestions. We also thank Curt Pollman for providing helpful technical insight toward the development of this forum. Financial support was provided by the University of Florida to publish this manuscript.
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