Article pubs.acs.org/est
Temporal and Spatial Trends in Freshwater Fish Tissue Mercury Concentrations Associated with Mercury Emissions Reductions Michael S. Hutcheson,*,† C. Mark Smith,† Jane Rose,† Carol Batdorf,‡ Oscar Pancorbo,‡ Carol Rowan West,† Joseph Strube,§ and Corey Francis§ †
Office of Research and Standards, Massachusetts Department of Environmental Protection, 1 Winter Street, Boston, Massachusetts 02108, United States ‡ Senator William X. Wall Experiment Station, Massachusetts Department of Environmental Protection, 37 Shattuck Street, Lawrence, Massachusetts 01843-1398, United States § Normandeau Associates, 25 Nashua Road, Bedford, New Hampshire 03110-5500, United States S Supporting Information *
ABSTRACT: Mercury (Hg) concentrations were monitored from 1999 to 2011 in largemouth bass (LMB) and yellow perch (YP) in 23 lakes in Massachusetts USA during a period of significant local and regional Hg emissions reductions. Average LMB tissue Hg concentration decreases of 44% were seen in 13 of 16 lakes in a regional Hg “hotspot” area. YP in all lakes sampled in this area decreased 43% after the major emissions reductions. Comparative decreases throughout the remainder of the state were 13% and 19% for LMB and YP respectively. Annual tissue mercury concentration rate decreases were 0.029 (LMB) and 0.016 mg Hg/kg/yr (YP) in the hotspot. In lakes around the rest of the state, LMB showed no trend and YP Hg decreased 0.0068 mg Hg/kg/yr. Mercury emissions from major point sources in the hotspot area decreased 98%, and 93% in the rest of the state from the early 1990s to 2008. The significant declines in fish Hg concentrations in many lakes occurred over the second half of a two decade decrease in Hg emissions primarily from municipal solid waste combustors and, secondarily, from other combustion point sources. In addition to the substantial Hg emissions reductions achieved in Massachusetts, further regional, national and global emissions reductions are needed for fish Hg levels to decrease below fish consumption advisory levels.
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INTRODUCTION Mercury (Hg) is a potent toxin that adversely affects the neurological system, kidneys, immune system and cardiovascular systems of humans and wildlife.1 The brains and developing neurological systems of the fetus and children are particularly sensitive to Hg and can be damaged by low levels of exposure.2 Human exposures to Hg, principally the monomethylated form, are largely attributable to the consumption of fish that have accumulated Hg.3 Mercury sources can be natural or anthropogenic with the latter greatly increasing Hg levels in the global environment.3 Efforts to control anthropogenic Hg inputs have been driven by the noted environmental and human health concerns. These efforts have focused on a variety of Hg emission sources including coal-fired electric generating units, municipal solid waste combustors (MSWC), medical waste incinerators and industrial facilities, among others.3 Efforts to reduce the use and disposal of Hg-added products are being implemented. Work throughout North America over the past decade has documented some, though not consistent, downturns in Hg concentrations in various environmental compartments4,5 generally attributed to global and regional efforts to reduce the use, production (since about 1970)6 and releases of Hg. © 2014 American Chemical Society
There has been limited documentation or understanding of the temporal and quantitative relationships between tissue burdens of Hg in fish and changes in atmospheric loadings of Hg.7 Several field studies that experimentally manipulated Hg loading have shown that lake ecosystems can respond rapidly to increases in atmospheric Hg deposition rates.8 However, uncertainty exists regarding the length of time that it would take for aquatic ecosystem resources to reflect decreases in Hg inputs7,9 in part because of the large reservoirs of Hg already existing in aquatic environments and catchment areas.3 We present coupled time series data on local and regional Hg emissions to the atmosphere, and edible tissue Hg concentrations in two widely fished freshwater fish species, largemouth bass (LMB, Micropterus salmoides) and yellow perch (YP, Perca f lavescens). This study was conducted over a period when major reductions in Hg emissions, particularly from local point sources, occurred. The work focused on a regional Hg emissions and deposition “hotspot” in northeastern MassachuReceived: Revised: Accepted: Published: 2193
September 26, 2013 January 15, 2014 January 21, 2014 February 4, 2014 dx.doi.org/10.1021/es404302m | Environ. Sci. Technol. 2014, 48, 2193−2202
Environmental Science & Technology
Article
Figure 1. Study area lakes.
setts10−12 that also extends into southeastern New Hampshire.13 We estimated local and state Hg emissions from major point sources before and after the implementation of state14 and regional15 Hg reduction policies. Key components of these efforts included the imposition of stringent Hg emission control requirements on MSWCs, which took effect in 2000,16 and on coal-fired electric generating units which took effect in 2008;17 regional agreement to stringently control emissions from medical waste incinerators, which resulted in the closure of all these units in Massachusetts by 2003; and the adoption of laws limiting Hg use in products and discharges from dental offices. This study’s objective was to document the magnitude and direction of changes in dorsal muscle total Hg concentrations in LMB and YP in lakes in the hotspot area and elsewhere across Massachusetts during this period of local Hg emission reductions. Because MSWC Hg emissions are substantially comprised of Hg species with relatively short atmospheric half-lives, these facilities can significantly contribute to locally elevated Hg deposition. Much of the hotspot Hg deposition in 1996 was attributed to local MSWCs and medical waste incinerators.11 Based upon a comparison of 1996 to 2002 Hg emissions, Hg deposition was predicted to decrease by up to 90% in the hotspot area.11,18 Emission reductions under the Massachusetts and northeastern regional Hg reduction strategies have thus provided an opportunity to assess environmental responses associated with reduced Hg emissions.
were not known to receive point source discharges of Hgcontaining wastes and were chosen to provide representative geographic coverage across the study areas. Samples were collected over an extended time frame to minimize the potential impact of localized events or conditions (e.g., algal blooms, fish kills, aquatic weed control treatments, etc.) that could uniquely influence fish Hg tissue concentrations. Sample Collection and Processing. Fish sampling and preparation of skinless muscle samples for analysis were as described elsewhere.10 Fish were collected in the spring of each year to control for the variability which can be introduced by seasonal changes in fish tissue Hg concentrations.19 Thirty YP and 12−15 LMB of various sizes per lake per sampling event were sought, determined on the basis of sample variance estimates from prior sampling work and desired power to detect differences in means. The following water quality parameters were measured: water temperature, pH, dissolved oxygen concentration, conductivity, major cations and anions (Na, K, Ca, Mg, Fe, Mn, SO4, Cl), dissolved organic carbon and total organic carbon contents, nitrate+nitrite nitrogen, total phosphorus, and ammonia. Further details of water sampling are in the Supporting Information (SI). Analytical Methods. Fish tissue Hg concentrations expressed on a wet weight basis were determined in accordance with U.S. Environmental Protection Agency (EPA) procedures20 as described elsewhere.10 Method details, and water quality analytical techniques and associated detection limits are all provided in the SI. Hg Emissions Data. Hg emission inventory estimates were derived for MSWCs, medical waste incinerators, coal-fired electric generating units and sewage sludge incinerators for 1991−2008. They were based on stack emission tests using standard U.S. EPA methods performed under MassDEP supervision as required by state regulations. Emission
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EXPERIMENTAL SECTION Study and Sampling Locations. We sampled edible dorsal muscle from YP and LMB from two to eight times between 1999 and 2011 from 23 lakes. Sixteen lakes were in a Hg deposition hotspot area and seven were throughout the rest of Massachusetts in areas distant from large airborne Hg emissions point sources (Figure 1). Lakes had surface areas ≥4 ha, were known to have supported the targeted fish species, 2194
dx.doi.org/10.1021/es404302m | Environ. Sci. Technol. 2014, 48, 2193−2202
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Figure 2. Time series of LMB and YP Hg concentrations (mg Hg/kg wet wt) in lakes in northeastern hotspot and rest of state.
factors21,22 from other source categories were used to calculate their emissions. Further details are presented in the SI.
Meteorological Data. Meteorological data for 1991−2011 on rainfall amounts and chemical characteristics of wet 2195
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Table 1. Fish Tissue Hg Concentration (mg Hg/kg wet wt) Change Summary ≤2002 to 2003−2011 species:
LMB
YP
area
lake
% Δ Hg
npre
npost
NE
Baldpate Pond Chadwicks Pond Lake Cochichewick Haggetts Pond Johnsons Pond Kenoza Lake Lake Attitash Lake Pentucket Lake Saltonstall Long Pond Lowe Pond Millvale Reservoir Newfield Pond Pomps Pond Rock Pond Stevens Pond area mean
−41 −13 −47 −12 −8 −35 −22 −87 −35 −65 −40 −65 −84 −62 −45 −43 −44 ± 24
8 12 21 8 9 5 9 10 9 9 9 9 9 9 9 18
57 54 74 84 59 58 54 4 12 15 18 15 15 38 74 38
−14 −14 35 −31
8 9 9 21
72 57 69 52
−25 −30 −13 ± 25
14 30
59 68
rest
Bare Hill Pond Massapoag Pond N. Watuppa Pond Onota Lake Upper Reservoir Lake Wampanoag Wequaquet Lake area mean
% Δ Hg
npre
npost
−58 −35 −41 −22 −29 −35 −26
9 9 65 9 9 56 9
7 48 150 180 123 120 120
−51 −30
9 9
30 80
−46 −63 −50 −67 −43 ± 15
9 7 9 9
30 34 148 8
−17 −13 −0.1 −23 36 −30 −14 −19 ± 12
9 9 60 54 50 30 60
150 120 137 150 48 120 150
NOTE: for lake means bold = significant at p = 0.05.
precipitation were obtained from online sources for two National Atmospheric Deposition Program network stations located to the west of the study area. One was in urban Waltham, MA (Station MA13) located 40 km southwest of the hotspot area and the other at the rural Quabbin Reservoir (Station MA09) 100 km to the west southwest.23 More details are provide in the SI. Statistical Analyses. The confounding effect of fish size on Hg concentrations was controlled for by deriving predicted Hg concentrations for a “standard-sized fish”10 of each individual of each species in each lake at each sampling time. This procedure facilitates comparisons between groups of fish. Standardization may not reflect Hg concentration differences at size extremes. The data for one lake, Johnsons Pond, were standardized to a different sized fish for reasons explained in the SI. One objective of the study was to determine if fish tissue Hg concentrations in lakes in a known Hg emissions hotspot had changed between the periods before and after the implementation of strict emissions controls on MSWCs. We first performed a step trend24 two-period comparison of data for each species and lake grouped from the periods 1998−2002 and 2003−2011. Through grouping years, we sought to average out the interannual variability seen within the individual time series at many of the lakes during the periods so that any major overall differences between the 2 time periods could be identified. The 2002/2003 breakpoint was visually identified from time series plots of size-standardized tissue Hg concentrations for each species, even though the emissions controls were implemented in 2000. Mean differences between the grouped fish tissue concentrations for each lake and species were calculated as percent changes. The Student’s t test applied
to log10-transformed size-standardized Hg concentrations was used to test for differences in species mean Hg concentrations between the two groups. The Regional Kendall Trends Test25,26 was used to test for consistent regional trends across lakes throughout the entire state, the northeastern part of the state and the rest of the state. This nonparametric test assesses trends in the data regardless of whether those trends are linear and makes no assumptions about the statistical attributes of the data. Mann-Kendall test statistics are first calculated using annual species mean sizestandardized Hg concentrations for each lake within defined geographical areas. These test statistics are then combined in the Regional Test to determine whether mean Hg concentrations change in consistent directions over time. Kendall’s tau nonparametric correlation coefficient, its significance and annual regional median rate of change in tissue Hg concentrations are calculated. All other statistical evaluations in this study were performed with the Statistica©, Version 10.0 or 12.0 software package (StatSoft, Tulsa, OK).
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RESULTS Fish Hg Levels and Trends. Although temporal changes in fish tissue Hg concentrations were not uniform, nor linear in all Massachusetts lakes monitored, a downward trend between 1999 and 2011, most strongly and generally from greater initial concentrations in the hotspot area of northeastern Massachusetts (Figure 2), was observed. In the two period comparisons, YP Hg concentrations in the majority of the lakes throughout the state decreased significantly (p < 0.05) between the first and second phases
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decade, the contribution from the northeast declined to 51% of the state total, reflecting closure of one of four operating MSWCs in the hotspot area and likely decreased Hg levels in combusted trash resulting in part from the Hg reductions in batteries and other products and wastes attributable to state and federal actions.27 During the second phase of Hg emissions reductions after 2000, MSWC emissions further decreased to 130 kg/yr statewide by 2008 and to 40 kg/yr in the hotspot area. Emissions rates from these facilities throughout the state decreased by 96% over the period starting in 1991, with the 98% decline in the northeast part of the state accounting for the majority of the state’s reductions in atmospheric emissions of Hg from these sources. The fish Hg monitoring in this study occurred during the later phase of Hg emissions reductions (Figure 3).
of monitoring (Table 1). YP Hg concentrations in all 13 lakes in the hotspot area decreased significantly (p < 0.05) 22−67%. The mean decrease over all the lakes was 43 ± 15% (Table 1). Five of the seven lakes around the remainder of the state had significant (p < 0.05), but smaller tissue Hg concentration decreases over the same period (range: 14−36%) with a mean decrease across all seven of the lakes of 19 ± 15%. The data trends for LMB were similar. Fish Hg concentrations in 16 of the 22 lakes with LMB throughout the state decreased significantly (p < 0.05) between the two time periods, though not always linearly within the time periods (Figure 2, Table 1). The LMB in 13 of the 16 lakes in northeastern Massachusetts exhibited significant (p < 0.05) declines between the two periods of 22−87%. The mean decrease over all the lakes in this area was 44 ± 24%. Fish in three of the remaining seven lakes around the remainder of the state had significant Hg decreases of 25− 31%. The mean decrease over all lakes in the rest of the state was 13 ± 25%. The group averaging over sampling years performed to calculate percent changes between time periods obscured some interannual changes (Figure 2) within the groups. The Regional Trends Analysis provided a complementary picture of the results from the two time period comparisons. When all lakes in the state were considered together, the trends test found significant (p = 0.05; Kendall’s tau correlation coefficients of −0.39 and −0.44 for LMB and YP) downward fish Hg concentration trends over the study period, with LMB and YP Hg concentrations decreasing at annual median rates of change of 0.021 and 0.013 mg Hg/kg/yr respectively. In the northeast, both species had significant (p = 0.05; taus of −0.50 and −0.48 for LMB and YP) and large rates of Hg concentration decrease with annual median rates of 0.029 (LMB) and 0.016 mg Hg/kg/yr (YP). LMB from lakes in the rest of the state did not show any significant trend in their Hg concentrations (tau = −0.20), whereas YP had a much smaller, but statistically significant (p = 0.05; tau= −0.39) annual median decrease of 0.0068 mg Hg/kg/yr. Temporal Responses of Fish Hg Concentrations to Emissions Changes. MSWCs have represented the largest single source category for Hg emissions in Massachusetts. They accounted for 83%, 47% and 40% of total Hg emissions in Massachusetts in the periods 1991−1994, 2002 and 2008, respectively (SI Table S-3). However, in each period their total Hg emissions were significantly decreased. During the first phase of Hg emissions reductions in the state (from an early 1990s baseline [1991−1994] to the late 1990s prior to the implementation of more strict MSWC Hg emissions limits in 2000), their emissions throughout the whole state decreased by approximately 1740 kg (54%) (Table 2). In the baseline years, 62% of the total statewide emissions of Hg came from the northeastern part of the state (Table 2). By the end of the
Figure 3. Municipal solid waste combustor Hg emissions throughout Massachusetts and in northeastern deposition hotspot area from 1991 to 2008.
Massachusetts fish tissue Hg data over the earlier period are insufficient to allow for longer-term trends to be assessed. In this study, the earliest decreases in fish tissue concentrations compared to a 1999 fish tissue baseline were seen in a few lakes by 2002−2003, 2−3 years after the large 2000 emissions reductions. Further fish Hg concentration decreases were seen thereafter. These reductions were 4−10 years after the significant first phase emissions reductions that occurred between 1993 and 1998 (Figure 3). More and greater changes in fish Hg were seen in the lakes in the northeast hotspot area than around the remainder of the state (Figure 2). Mercury deposition modeling in the hotspot area had predicted large decreases up to 90% in Hg wet deposition following the emissions reductions.11,18
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DISCUSSION We documented area mean fish Hg concentrations decreases of 13 to 44% in two recreationally important freshwater fish species in Massachusetts after significant local and regional Hg emissions reductions. Interannual changes varied more widely within individual lakes. These decreases were correlated with large reductions in local and regional mercury air emissions attributable to state regulatory efforts. Chalmers et al.28 identified national trends (1969−2005) in freshwater fish tissue Hg for a variety of species. Thirty-two percent of the water bodies sampled had concentration
Table 2. Massachusetts Municipal Solid Waste Combustor Annual Hg Stack Emission Rates, kg Hg/yr (Source: NESCAUM 201122 and MassDEP as described in the SI) averaging period
a
region
1991−1994
1998−1999
2001−2003
2008
northeastern MA rest of state state total
1990 1240 3230
760 730 1490
40 190 230
40 90 130
Emissions figures rounded to nearest ten. 2197
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deposition inputs of Hg, cycling of Hg in the ecosystem and its appearance in biota.45,46 Experimentally added Hg simulating atmospheric deposition was preferentially incorporated into fish tissues over older Hg cycled through upland and wetland habitats into lake waters.8,39,47 The mesocosm studies demonstrated that lake biota Hg levels can increase rapidly and linearly in response to increases in simulated atmospheric Hg inputs.8 The theoretical converse of this conclusion is that when recently added, atmospherically deposited Hg is reduced, fish Hg accumulation should also be rapidly reduced. This is the result seen frequently in our study. The reductions in fish tissue Hg levels observed to date are less than the model predicted decrements in overall Hg deposition in the hotspot area. This is not surprising given other possible reservoir sources of Hg in the area (sediments and watershed soils), consistent with elevated atmospheric depositional inputs over many years. Our results and those from the Everglades indicate that changes in atmospheric deposition (increases or decreases) can be reflected in biota Hg levels on a fairly short time frame.7,47 Fish Hg concentration fluctuations may be influenced by a number of scale-dependent factors: global climate and temperature changes; global and upwind out-of-area atmospheric Hg inputs, changes in the amounts and chemical composition of precipitation and alterations in the trophodynamics of the lakes. Global and hemispheric temperature and climate changes have been hypothesized to have effects on Hg and other contaminant levels in fish tissue through a variety of mechanisms.34,36 During our study, these types of large-scale fluctuations would have been a constant factor across our study areas. Global Hg emissions decreased from 2428 to 1930 tonnes/yr (−20.5%) between 1995 and 2005 after peaks in the late 1970s to early 1980s.48−50 While North American emissions have decreased markedly,51 substantial increased inputs to the global atmospheric Hg pool have come primarily from Asia,49 moderating the influence of the North American reductions. Atmospheric Hg concentrations in the northern hemisphere between 1996 and 2009 have trended downward (−1.4 to −2.2%/yr),50,52,53 also reflected in a mean change in Hg flux to Great Lakes sediments after the 1980s of approximately −20%.54 At the regional level, from 47 to 60% of the total atmospheric Hg deposition in the northeast in the mid 1990s was estimated to come from regional, primarily point sources with the remainder from upwind continental and global sources.11,55 With the large reductions in local emissions by the 2000s, the figures had changed substantially with 17−32% coming from the regional and point sources. When large Hg point sources are present, the local (
Temporal and Spatial Trends in Freshwater Fish Tissue Mercury Concentrations Associated with Mercury Emissions Reductions Michael S. Hutcheson,*,† C. Mark Smith,† Jane Rose,† Carol Batdorf,‡ Oscar Pancorbo,‡ Carol Rowan West,† Joseph Strube,§ and Corey Francis§ †
Office of Research and Standards, Massachusetts Department of Environmental Protection, 1 Winter Street, Boston, Massachusetts 02108, United States ‡ Senator William X. Wall Experiment Station, Massachusetts Department of Environmental Protection, 37 Shattuck Street, Lawrence, Massachusetts 01843-1398, United States § Normandeau Associates, 25 Nashua Road, Bedford, New Hampshire 03110-5500, United States S Supporting Information *
ABSTRACT: Mercury (Hg) concentrations were monitored from 1999 to 2011 in largemouth bass (LMB) and yellow perch (YP) in 23 lakes in Massachusetts USA during a period of significant local and regional Hg emissions reductions. Average LMB tissue Hg concentration decreases of 44% were seen in 13 of 16 lakes in a regional Hg “hotspot” area. YP in all lakes sampled in this area decreased 43% after the major emissions reductions. Comparative decreases throughout the remainder of the state were 13% and 19% for LMB and YP respectively. Annual tissue mercury concentration rate decreases were 0.029 (LMB) and 0.016 mg Hg/kg/yr (YP) in the hotspot. In lakes around the rest of the state, LMB showed no trend and YP Hg decreased 0.0068 mg Hg/kg/yr. Mercury emissions from major point sources in the hotspot area decreased 98%, and 93% in the rest of the state from the early 1990s to 2008. The significant declines in fish Hg concentrations in many lakes occurred over the second half of a two decade decrease in Hg emissions primarily from municipal solid waste combustors and, secondarily, from other combustion point sources. In addition to the substantial Hg emissions reductions achieved in Massachusetts, further regional, national and global emissions reductions are needed for fish Hg levels to decrease below fish consumption advisory levels.
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INTRODUCTION Mercury (Hg) is a potent toxin that adversely affects the neurological system, kidneys, immune system and cardiovascular systems of humans and wildlife.1 The brains and developing neurological systems of the fetus and children are particularly sensitive to Hg and can be damaged by low levels of exposure.2 Human exposures to Hg, principally the monomethylated form, are largely attributable to the consumption of fish that have accumulated Hg.3 Mercury sources can be natural or anthropogenic with the latter greatly increasing Hg levels in the global environment.3 Efforts to control anthropogenic Hg inputs have been driven by the noted environmental and human health concerns. These efforts have focused on a variety of Hg emission sources including coal-fired electric generating units, municipal solid waste combustors (MSWC), medical waste incinerators and industrial facilities, among others.3 Efforts to reduce the use and disposal of Hg-added products are being implemented. Work throughout North America over the past decade has documented some, though not consistent, downturns in Hg concentrations in various environmental compartments4,5 generally attributed to global and regional efforts to reduce the use, production (since about 1970)6 and releases of Hg. © 2014 American Chemical Society
There has been limited documentation or understanding of the temporal and quantitative relationships between tissue burdens of Hg in fish and changes in atmospheric loadings of Hg.7 Several field studies that experimentally manipulated Hg loading have shown that lake ecosystems can respond rapidly to increases in atmospheric Hg deposition rates.8 However, uncertainty exists regarding the length of time that it would take for aquatic ecosystem resources to reflect decreases in Hg inputs7,9 in part because of the large reservoirs of Hg already existing in aquatic environments and catchment areas.3 We present coupled time series data on local and regional Hg emissions to the atmosphere, and edible tissue Hg concentrations in two widely fished freshwater fish species, largemouth bass (LMB, Micropterus salmoides) and yellow perch (YP, Perca f lavescens). This study was conducted over a period when major reductions in Hg emissions, particularly from local point sources, occurred. The work focused on a regional Hg emissions and deposition “hotspot” in northeastern MassachuReceived: Revised: Accepted: Published: 2193
September 26, 2013 January 15, 2014 January 21, 2014 February 4, 2014 dx.doi.org/10.1021/es404302m | Environ. Sci. Technol. 2014, 48, 2193−2202
Environmental Science & Technology
Article
Figure 1. Study area lakes.
setts10−12 that also extends into southeastern New Hampshire.13 We estimated local and state Hg emissions from major point sources before and after the implementation of state14 and regional15 Hg reduction policies. Key components of these efforts included the imposition of stringent Hg emission control requirements on MSWCs, which took effect in 2000,16 and on coal-fired electric generating units which took effect in 2008;17 regional agreement to stringently control emissions from medical waste incinerators, which resulted in the closure of all these units in Massachusetts by 2003; and the adoption of laws limiting Hg use in products and discharges from dental offices. This study’s objective was to document the magnitude and direction of changes in dorsal muscle total Hg concentrations in LMB and YP in lakes in the hotspot area and elsewhere across Massachusetts during this period of local Hg emission reductions. Because MSWC Hg emissions are substantially comprised of Hg species with relatively short atmospheric half-lives, these facilities can significantly contribute to locally elevated Hg deposition. Much of the hotspot Hg deposition in 1996 was attributed to local MSWCs and medical waste incinerators.11 Based upon a comparison of 1996 to 2002 Hg emissions, Hg deposition was predicted to decrease by up to 90% in the hotspot area.11,18 Emission reductions under the Massachusetts and northeastern regional Hg reduction strategies have thus provided an opportunity to assess environmental responses associated with reduced Hg emissions.
were not known to receive point source discharges of Hgcontaining wastes and were chosen to provide representative geographic coverage across the study areas. Samples were collected over an extended time frame to minimize the potential impact of localized events or conditions (e.g., algal blooms, fish kills, aquatic weed control treatments, etc.) that could uniquely influence fish Hg tissue concentrations. Sample Collection and Processing. Fish sampling and preparation of skinless muscle samples for analysis were as described elsewhere.10 Fish were collected in the spring of each year to control for the variability which can be introduced by seasonal changes in fish tissue Hg concentrations.19 Thirty YP and 12−15 LMB of various sizes per lake per sampling event were sought, determined on the basis of sample variance estimates from prior sampling work and desired power to detect differences in means. The following water quality parameters were measured: water temperature, pH, dissolved oxygen concentration, conductivity, major cations and anions (Na, K, Ca, Mg, Fe, Mn, SO4, Cl), dissolved organic carbon and total organic carbon contents, nitrate+nitrite nitrogen, total phosphorus, and ammonia. Further details of water sampling are in the Supporting Information (SI). Analytical Methods. Fish tissue Hg concentrations expressed on a wet weight basis were determined in accordance with U.S. Environmental Protection Agency (EPA) procedures20 as described elsewhere.10 Method details, and water quality analytical techniques and associated detection limits are all provided in the SI. Hg Emissions Data. Hg emission inventory estimates were derived for MSWCs, medical waste incinerators, coal-fired electric generating units and sewage sludge incinerators for 1991−2008. They were based on stack emission tests using standard U.S. EPA methods performed under MassDEP supervision as required by state regulations. Emission
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EXPERIMENTAL SECTION Study and Sampling Locations. We sampled edible dorsal muscle from YP and LMB from two to eight times between 1999 and 2011 from 23 lakes. Sixteen lakes were in a Hg deposition hotspot area and seven were throughout the rest of Massachusetts in areas distant from large airborne Hg emissions point sources (Figure 1). Lakes had surface areas ≥4 ha, were known to have supported the targeted fish species, 2194
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Figure 2. Time series of LMB and YP Hg concentrations (mg Hg/kg wet wt) in lakes in northeastern hotspot and rest of state.
factors21,22 from other source categories were used to calculate their emissions. Further details are presented in the SI.
Meteorological Data. Meteorological data for 1991−2011 on rainfall amounts and chemical characteristics of wet 2195
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Table 1. Fish Tissue Hg Concentration (mg Hg/kg wet wt) Change Summary ≤2002 to 2003−2011 species:
LMB
YP
area
lake
% Δ Hg
npre
npost
NE
Baldpate Pond Chadwicks Pond Lake Cochichewick Haggetts Pond Johnsons Pond Kenoza Lake Lake Attitash Lake Pentucket Lake Saltonstall Long Pond Lowe Pond Millvale Reservoir Newfield Pond Pomps Pond Rock Pond Stevens Pond area mean
−41 −13 −47 −12 −8 −35 −22 −87 −35 −65 −40 −65 −84 −62 −45 −43 −44 ± 24
8 12 21 8 9 5 9 10 9 9 9 9 9 9 9 18
57 54 74 84 59 58 54 4 12 15 18 15 15 38 74 38
−14 −14 35 −31
8 9 9 21
72 57 69 52
−25 −30 −13 ± 25
14 30
59 68
rest
Bare Hill Pond Massapoag Pond N. Watuppa Pond Onota Lake Upper Reservoir Lake Wampanoag Wequaquet Lake area mean
% Δ Hg
npre
npost
−58 −35 −41 −22 −29 −35 −26
9 9 65 9 9 56 9
7 48 150 180 123 120 120
−51 −30
9 9
30 80
−46 −63 −50 −67 −43 ± 15
9 7 9 9
30 34 148 8
−17 −13 −0.1 −23 36 −30 −14 −19 ± 12
9 9 60 54 50 30 60
150 120 137 150 48 120 150
NOTE: for lake means bold = significant at p = 0.05.
precipitation were obtained from online sources for two National Atmospheric Deposition Program network stations located to the west of the study area. One was in urban Waltham, MA (Station MA13) located 40 km southwest of the hotspot area and the other at the rural Quabbin Reservoir (Station MA09) 100 km to the west southwest.23 More details are provide in the SI. Statistical Analyses. The confounding effect of fish size on Hg concentrations was controlled for by deriving predicted Hg concentrations for a “standard-sized fish”10 of each individual of each species in each lake at each sampling time. This procedure facilitates comparisons between groups of fish. Standardization may not reflect Hg concentration differences at size extremes. The data for one lake, Johnsons Pond, were standardized to a different sized fish for reasons explained in the SI. One objective of the study was to determine if fish tissue Hg concentrations in lakes in a known Hg emissions hotspot had changed between the periods before and after the implementation of strict emissions controls on MSWCs. We first performed a step trend24 two-period comparison of data for each species and lake grouped from the periods 1998−2002 and 2003−2011. Through grouping years, we sought to average out the interannual variability seen within the individual time series at many of the lakes during the periods so that any major overall differences between the 2 time periods could be identified. The 2002/2003 breakpoint was visually identified from time series plots of size-standardized tissue Hg concentrations for each species, even though the emissions controls were implemented in 2000. Mean differences between the grouped fish tissue concentrations for each lake and species were calculated as percent changes. The Student’s t test applied
to log10-transformed size-standardized Hg concentrations was used to test for differences in species mean Hg concentrations between the two groups. The Regional Kendall Trends Test25,26 was used to test for consistent regional trends across lakes throughout the entire state, the northeastern part of the state and the rest of the state. This nonparametric test assesses trends in the data regardless of whether those trends are linear and makes no assumptions about the statistical attributes of the data. Mann-Kendall test statistics are first calculated using annual species mean sizestandardized Hg concentrations for each lake within defined geographical areas. These test statistics are then combined in the Regional Test to determine whether mean Hg concentrations change in consistent directions over time. Kendall’s tau nonparametric correlation coefficient, its significance and annual regional median rate of change in tissue Hg concentrations are calculated. All other statistical evaluations in this study were performed with the Statistica©, Version 10.0 or 12.0 software package (StatSoft, Tulsa, OK).
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RESULTS Fish Hg Levels and Trends. Although temporal changes in fish tissue Hg concentrations were not uniform, nor linear in all Massachusetts lakes monitored, a downward trend between 1999 and 2011, most strongly and generally from greater initial concentrations in the hotspot area of northeastern Massachusetts (Figure 2), was observed. In the two period comparisons, YP Hg concentrations in the majority of the lakes throughout the state decreased significantly (p < 0.05) between the first and second phases
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Article
decade, the contribution from the northeast declined to 51% of the state total, reflecting closure of one of four operating MSWCs in the hotspot area and likely decreased Hg levels in combusted trash resulting in part from the Hg reductions in batteries and other products and wastes attributable to state and federal actions.27 During the second phase of Hg emissions reductions after 2000, MSWC emissions further decreased to 130 kg/yr statewide by 2008 and to 40 kg/yr in the hotspot area. Emissions rates from these facilities throughout the state decreased by 96% over the period starting in 1991, with the 98% decline in the northeast part of the state accounting for the majority of the state’s reductions in atmospheric emissions of Hg from these sources. The fish Hg monitoring in this study occurred during the later phase of Hg emissions reductions (Figure 3).
of monitoring (Table 1). YP Hg concentrations in all 13 lakes in the hotspot area decreased significantly (p < 0.05) 22−67%. The mean decrease over all the lakes was 43 ± 15% (Table 1). Five of the seven lakes around the remainder of the state had significant (p < 0.05), but smaller tissue Hg concentration decreases over the same period (range: 14−36%) with a mean decrease across all seven of the lakes of 19 ± 15%. The data trends for LMB were similar. Fish Hg concentrations in 16 of the 22 lakes with LMB throughout the state decreased significantly (p < 0.05) between the two time periods, though not always linearly within the time periods (Figure 2, Table 1). The LMB in 13 of the 16 lakes in northeastern Massachusetts exhibited significant (p < 0.05) declines between the two periods of 22−87%. The mean decrease over all the lakes in this area was 44 ± 24%. Fish in three of the remaining seven lakes around the remainder of the state had significant Hg decreases of 25− 31%. The mean decrease over all lakes in the rest of the state was 13 ± 25%. The group averaging over sampling years performed to calculate percent changes between time periods obscured some interannual changes (Figure 2) within the groups. The Regional Trends Analysis provided a complementary picture of the results from the two time period comparisons. When all lakes in the state were considered together, the trends test found significant (p = 0.05; Kendall’s tau correlation coefficients of −0.39 and −0.44 for LMB and YP) downward fish Hg concentration trends over the study period, with LMB and YP Hg concentrations decreasing at annual median rates of change of 0.021 and 0.013 mg Hg/kg/yr respectively. In the northeast, both species had significant (p = 0.05; taus of −0.50 and −0.48 for LMB and YP) and large rates of Hg concentration decrease with annual median rates of 0.029 (LMB) and 0.016 mg Hg/kg/yr (YP). LMB from lakes in the rest of the state did not show any significant trend in their Hg concentrations (tau = −0.20), whereas YP had a much smaller, but statistically significant (p = 0.05; tau= −0.39) annual median decrease of 0.0068 mg Hg/kg/yr. Temporal Responses of Fish Hg Concentrations to Emissions Changes. MSWCs have represented the largest single source category for Hg emissions in Massachusetts. They accounted for 83%, 47% and 40% of total Hg emissions in Massachusetts in the periods 1991−1994, 2002 and 2008, respectively (SI Table S-3). However, in each period their total Hg emissions were significantly decreased. During the first phase of Hg emissions reductions in the state (from an early 1990s baseline [1991−1994] to the late 1990s prior to the implementation of more strict MSWC Hg emissions limits in 2000), their emissions throughout the whole state decreased by approximately 1740 kg (54%) (Table 2). In the baseline years, 62% of the total statewide emissions of Hg came from the northeastern part of the state (Table 2). By the end of the
Figure 3. Municipal solid waste combustor Hg emissions throughout Massachusetts and in northeastern deposition hotspot area from 1991 to 2008.
Massachusetts fish tissue Hg data over the earlier period are insufficient to allow for longer-term trends to be assessed. In this study, the earliest decreases in fish tissue concentrations compared to a 1999 fish tissue baseline were seen in a few lakes by 2002−2003, 2−3 years after the large 2000 emissions reductions. Further fish Hg concentration decreases were seen thereafter. These reductions were 4−10 years after the significant first phase emissions reductions that occurred between 1993 and 1998 (Figure 3). More and greater changes in fish Hg were seen in the lakes in the northeast hotspot area than around the remainder of the state (Figure 2). Mercury deposition modeling in the hotspot area had predicted large decreases up to 90% in Hg wet deposition following the emissions reductions.11,18
■
DISCUSSION We documented area mean fish Hg concentrations decreases of 13 to 44% in two recreationally important freshwater fish species in Massachusetts after significant local and regional Hg emissions reductions. Interannual changes varied more widely within individual lakes. These decreases were correlated with large reductions in local and regional mercury air emissions attributable to state regulatory efforts. Chalmers et al.28 identified national trends (1969−2005) in freshwater fish tissue Hg for a variety of species. Thirty-two percent of the water bodies sampled had concentration
Table 2. Massachusetts Municipal Solid Waste Combustor Annual Hg Stack Emission Rates, kg Hg/yr (Source: NESCAUM 201122 and MassDEP as described in the SI) averaging period
a
region
1991−1994
1998−1999
2001−2003
2008
northeastern MA rest of state state total
1990 1240 3230
760 730 1490
40 190 230
40 90 130
Emissions figures rounded to nearest ten. 2197
dx.doi.org/10.1021/es404302m | Environ. Sci. Technol. 2014, 48, 2193−2202
Environmental Science & Technology
Article
deposition inputs of Hg, cycling of Hg in the ecosystem and its appearance in biota.45,46 Experimentally added Hg simulating atmospheric deposition was preferentially incorporated into fish tissues over older Hg cycled through upland and wetland habitats into lake waters.8,39,47 The mesocosm studies demonstrated that lake biota Hg levels can increase rapidly and linearly in response to increases in simulated atmospheric Hg inputs.8 The theoretical converse of this conclusion is that when recently added, atmospherically deposited Hg is reduced, fish Hg accumulation should also be rapidly reduced. This is the result seen frequently in our study. The reductions in fish tissue Hg levels observed to date are less than the model predicted decrements in overall Hg deposition in the hotspot area. This is not surprising given other possible reservoir sources of Hg in the area (sediments and watershed soils), consistent with elevated atmospheric depositional inputs over many years. Our results and those from the Everglades indicate that changes in atmospheric deposition (increases or decreases) can be reflected in biota Hg levels on a fairly short time frame.7,47 Fish Hg concentration fluctuations may be influenced by a number of scale-dependent factors: global climate and temperature changes; global and upwind out-of-area atmospheric Hg inputs, changes in the amounts and chemical composition of precipitation and alterations in the trophodynamics of the lakes. Global and hemispheric temperature and climate changes have been hypothesized to have effects on Hg and other contaminant levels in fish tissue through a variety of mechanisms.34,36 During our study, these types of large-scale fluctuations would have been a constant factor across our study areas. Global Hg emissions decreased from 2428 to 1930 tonnes/yr (−20.5%) between 1995 and 2005 after peaks in the late 1970s to early 1980s.48−50 While North American emissions have decreased markedly,51 substantial increased inputs to the global atmospheric Hg pool have come primarily from Asia,49 moderating the influence of the North American reductions. Atmospheric Hg concentrations in the northern hemisphere between 1996 and 2009 have trended downward (−1.4 to −2.2%/yr),50,52,53 also reflected in a mean change in Hg flux to Great Lakes sediments after the 1980s of approximately −20%.54 At the regional level, from 47 to 60% of the total atmospheric Hg deposition in the northeast in the mid 1990s was estimated to come from regional, primarily point sources with the remainder from upwind continental and global sources.11,55 With the large reductions in local emissions by the 2000s, the figures had changed substantially with 17−32% coming from the regional and point sources. When large Hg point sources are present, the local (
