Methylmercury in Freshwater Fish
Linked to Atmospheric Mercury
Deposition
C H A D R . H A M M E R S C H M I D T * ,† A N D
WILLIAM F. FITZGERALD‡
Department of Marine Chemistry and Geochemistry,
Woods Hole Oceanographic Institution, Woods Hole,
Massachusetts 02543, and Department of Marine Sciences,
University of Connecticut, Groton, Connecticut 06340
A connection between accumulation of methylmercury
(MeHg) in wild fish populations and atmospheric mercury
deposition has not been made. Large databases for
both MeHg in fish and atmospheric mercury deposition
have been assimilated from monitoring efforts spanning the
contiguous United States. Here, we compare results of
these data sets and show that state-wide average
concentrations of MeHg in a cosmopolitan freshwater
fish, the largemouth bass Micropterus salmoides, are related
positively to wet atmospheric Hg fluxes among most of
the 25 states that are analyzed, which span a 5-fold range
in Hg deposition. Differences in largemouth bass MeHg
concentrations among states are unrelated to average
precipitation depth, wet atmospheric acid deposition, or
interstate variations in the type of water body (river, lake,
reservoir) from which the fish were sampled. There are
modest correlations between MeHg in bass and surface
water pH, temperature, and wet atmospheric deposition of
sulfate. However, when fish and atmospheric mercury
results are combined at the state level, wet atmospheric
Hg deposition accounts for about two-thirds of the variation
in bass MeHg among most states, and stepwise multiple
regression analysis reveals that these variables do not improve
the linear model significantly. This suggests the accumulation
of MeHg in wild fish populations is linked to atmospheric
Hg loadings, two-thirds of which are estimated to be from
anthropogenic sources.
Introduction
Accumulation of methylmercury (MeHg) in aquatic biota is
a primary toxicological concern related to mercury in the
environment. MeHg is produced from inorganic mercury
(Hg) by microorganisms in aquatic systems, presumably
sulfate-reducing bacteria (1), and it accumulates and biomagnifies in food webs to levels that may pose a health threat
to wildlife (2) and humans who consume fish (3). The
production and bioaccumulation of MeHg in aquatic ecosystems can be influenced by a variety of environmental
factors (e.g., organic material, pH, sulfur cycling, biological
productivity, temperature) that affect either the availability
of inorganic Hg for methylation, the activity of methylating
organisms, or the uptake and trophic transfer of MeHg (e.g.,
* Corresponding author phone:
508-289-3551;
[email protected].
† Woods Hole Oceanographic Institution.
‡ University of Connecticut.
10.1021/es061480i CCC: $33.50
Published on Web 10/24/2006
 xxxx American Chemical Society
e-mail:
2, 4-9). The complex biogeochemistry of Hg species in
aquatic ecosystems has overshadowed the underlying importance of the supply of reactant inorganic Hg for MeHg
production. The significance of Hg loadings is evidenced by
exceedingly high levels of MeHg in biota of aquatic systems
polluted with inorganic Hg from mining (e.g., Clear Lake,
CA; 10) and industrial point sources (e.g., Clay Lake, Ontario,
Canada; 11). Atmospheric deposition is the principal source
of inorganic Hg in most aquatic systems (12), and a potential
connection between wet atmospheric Hg fluxes and MeHg
in aquatic organisms was apparent in our recent study with
mosquitoes (10). More recently, a mesocosm study in
northwestern Ontario (13) and our own investigation in arctic
Alaskan lakes (9) have indicated MeHg production is directly
proportional to loadings of inorganic Hg. Accordingly, there
should be a positive relationship between atmospheric Hg
deposition and MeHg in fish, if the supply of inorganic Hg
were an important control on the production and subsequent
bioaccumulation of MeHg in aquatic systems.
Here, we examine this hypothesis by comparing MeHg in
fillets of a widely distributed fish species, the largemouth
bass Micropterus salmoides, to wet atmospheric Hg fluxes
across the 5-fold range in Hg deposition that exists within
the contiguous United States. Wet atmospheric Hg fluxes,
for example, are generally lowest in the western states, greater
in the Midwest and Northeast, and greatest in the southeastern United States. Largemouth bass were selected
because they are distributed throughout much of the United
States and frequently monitored for Hg by state environmental agencies. Many such programs have contributed to
an extensive national database for Hg levels in freshwater
fish (14) that complements results from a national atmospheric Hg deposition network (15). This novel assessment
is possible because the data bases are not only comprehensive, but there are more than 8 years of standardized Hg
deposition measurements at many locations (15). Essentially
all of the Hg in fish fillets is MeHg (16). Thus, and with
individual states as the experimental unit, these data sources
were used to compare average levels of MeHg in largemouth
bass with mean annual wet atmospheric Hg fluxes among
the American states.
Experimental Section
Largemouth Bass. MeHg concentrations in fish typically
increase with age and body size within a particular population
(2). Accordingly, comparisons of MeHg accumulation among
fish populations must normalize for either fish age or size
(length or body weight). Only largemouth bass between 30
and 40 cm total length were used for this study. Length was
used to normalize MeHg comparisons because age often is
not determined for each fish, and this slot length was selected
because it encompasses the average-sized largemouth bass
sampled in most states.
Most largemouth bass information in this study is from
a U.S. Environmental Protection Agency database (14)
compiled from state monitoring efforts of fish sampled mostly
between 1990 and 1995, which includes 39 states reporting
levels in largemouth bass (see Table A in the Supporting
Information). This data set was vetted carefully to include
only (1) individual largemouth bass between 30 and 40 cm
total length or composites of comparably sized bass with a
mean length between 30 and 40 cm (samples with no reported
total length or number of fish in the composite were
excluded), (2) concentrations for skinless or skin-on fillets,
(3) fish from watersheds with no known point sources of Hg
(e.g., geological, mining, industrial), (4) samples with meaVOL. xx, NO. xx, xxxx / ENVIRON. SCI. & TECHNOL.
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9
A
sured concentrations greater than the reported detection
limit, and (5) fish analyzed with acceptable quality control
results. These criteria resulted in the exclusion of several
states for lack of sufficient or acceptable data for the purpose
of this study (see Table A in Supporting Information).
Largemouth bass from South Carolina, for example, were
not used because the unusually high analytical detection
limit for these samples (0.25 µg g-1 wet weight) eliminated
many low-Hg fish leading to a positively biased mean
concentration. Results from additional reports or databases
were used and/or combined with the U.S. EPA data if they
met the above criteria and were available by either a search
of the Internet or shared upon request from states’ environmental departments (see Table A in Supporting Information). The combined data set used in this analysis includes
9169 largemouth bass sampled from 1043 water bodies (lakes,
reservoirs, and rivers) in 25 states. Weighted-mean concentrations of MeHg in largemouth bass were calculated for
each state because some states analyzed composite samples.
It is assumed that sample means determined from this data
set represent reasonably the population mean for 30-40 cm
total length largemouth bass in each state.
Wet Atmospheric Hg Deposition. Wet atmospheric Hg
fluxes were estimated for each state with results from the
Mercury Deposition Network (MDN; 15) and peer-reviewed
literature (see Table B in Supporting Information). The
sampling periods for atmospheric Hg deposition are variable
(1992-2004), and, although many records extend to the mid1990s, there often is little overlap between the periods of fish
and Hg deposition sampling (see Tables A and B in Supporting
Information). There appears to be, however, no significant
temporal change in either largemouth bass MeHg or atmospheric Hg deposition at locations where either parameter
has been monitored continuously during this time period.
Levels of MeHg in largemouth bass from four Michigan lakes,
for example, show no significant temporal trend between
1990 and 2004 (p ) 0.10-0.70; see Figure A in Supporting
Information). There also is no consistent, and in most cases
significant, temporal trend for MeHg in largemouth bass from
11 Louisiana water bodies where more than 7 years of timeseries data are available (see Figure B in Supporting
Information). Moreover, and while wet atmospheric Hg
deposition can vary inter-annually at a particular location,
there are no significant changes at 13 of 15 locations, spanning
the contiguous United States (Vermont, Maine, North
Carolina, Florida, Minnesota, Wisconsin, Texas, Washington),
where there is eight or more years of Hg deposition
information (p ) 0.11-0.99; see Figure C in Supporting
Information). Decreasing trends of Hg deposition at one site
in Minnesota (p ) 0.05) and Wisconsin (p ) 0.05) are not
consistent with results from other locations in each state
during the same time period (p ) 0.22-0.99). Hence, and for
states where periods of fish and Hg deposition sampling do
not coincide or overlap, the more recent estimates of
atmospheric Hg deposition should represent reasonably the
atmospheric flux when the fish were sampled.
Additional Physicochemical Factors. As noted, biogeochemical factors other than Hg deposition also can affect
the production and/or bioaccumulation of MeHg (e.g.,
organic material, pH, sulfur cycling, biological productivity).
These factors, as well as the transport and fate of Hg, are
influenced by both atmospheric/climatic phenomena (e.g.,
precipitation amount, temperature, acid and sulfate deposition) and watershed characteristics that can include watershed/wetland area, vegetation/soil type, and land use (1719). While terrestrial characteristics vary within and among
watersheds, the spatial scale of this study is wider ranging,
with individual states as the experimental unit. Thus, we
limited our comparison of MeHg in largemouth bass to only
physicochemical factors that are readily generalized and
B
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relatively uniform within most states, including the average
pH of surface water, annual precipitation amount, annual
air temperature (a proxy for water temperature), and wet
atmospheric deposition of acid (H+) and sulfate (SO42-; see
Table C in Supporting Information for summary characteristics). Such comparisons are possible because there are
extensive databases for wet atmospheric deposition (20),
annual temperature (21), and surface water pH (22).
Largemouth bass were sampled from lakes, reservoirs,
and rivers for this study. The relative distribution of sampling
effort among these three water body types varied among
states (see Table A in Supporting Information), likely a result
of differences in geography and surface water hydrology. In
North Carolina, for example, 34% of the sampled water bodies
are lakes, 4% are reservoirs, and 62% are rivers. This is in
contrast to many other states where lakes comprised greater
than 80% of the surface waters sampled for largemouth bass.
We tested for a potential influence of water body type (lakes,
reservoirs, rivers), and inferred watershed characteristics, on
state-wide average levels of MeHg in largemouth bass by
comparing bass MeHg with the fraction of sampled water
bodies in each state that are either lakes, reservoirs, or rivers.
For this analysis, ponds and marshes were considered lakes,
and bayous were included in the number of rivers.
Statistical Analysis. All statistical analyses were performed
with commercially available software (SigmaStat for Windows, version 3.1) and without data transformation. Leastsquares linear regression and correlation analyses were used
to identify factors related to MeHg levels in largemouth bass
and examine temporal trends in both bass MeHg and
atmospheric Hg deposition. Spearman rank order correlation
analysis (rs) was used when data were not distributed normally
with constant variance. Forward-stepwise multiple regression
analysis was used to examine the relationship between MeHg
in largemouth bass and several independent variables among
statesswater body type, surface water pH, precipitation
depth, air temperature, and wet atmospheric deposition of
Hg, acid, and sulfate. Variables were included in the model
only if they reduced the unexplained sum of squares
significantly (p e 0.05).
Results and Discussion
Bass MeHg versus Atmospheric Hg Deposition. Mean levels
of MeHg in largemouth bass are related positively to the
average annual wet atmospheric Hg flux among 22 of the 25
states analyzed (Figure 1); New Hampshire, Maine, and
Georgia are not included in the regression analysis (see
below). This relationship is striking given the many environmental factors other than Hg loadings, noted previously,
that are known or suspected to influence the production
and/or bioaccumulation of MeHg. Differences in the wet
atmospheric flux of Hg account for about two-thirds of the
variability in mean MeHg concentrations in largemouth bass
among states. Moreover, bass MeHg concentrations are
relatively similar among geographical regions that receive
comparable wet atmospheric Hg fluxes (Figure 1), including
the west coast states (CA, OR, WA), upper Midwest (MN, WI,
MI), Northeast (NY, CT, MA, VT), mid-Atlantic (WV, NJ, KY,
NC), and southeastern states (AL, LA, FL). A comparable
relationship is observed when periods of fish and atmospheric
Hg sampling coincide in a limited number of states (r2 )
0.68, p < 0.01; see Figure D in Supporting Information). The
relationship in Figure 1 suggests that dry atmospheric
deposition, including reactive gaseous Hg (23), which may
enhance Hg loadings compared to measured wet fluxes, either
is relatively proportional to wet atmospheric deposition for
sites in this study or does not have a large effect on the
bioaccumulation of MeHg at most locations.
FIGURE 1. Relation between weighted-mean concentration of MeHg
in fillets of largemouth bass (30-40 cm total length) and average
annual wet atmospheric deposition of total Hg among 22 of 25
American states: AL, Alabama; AR, Arkansas; CA, California; CT,
Connecticut; FL, Florida; GA, Georgia; IA, Iowa; KS, Kansas; KY,
Kentucky; LA, Louisiana; ME, Maine; MA, Massachusetts; MI,
Michigan; MN, Minnesota; NH, New Hampshire; NJ, New Jersey;
NY, New York; NC, North Carolina; OK, Oklahoma; OR, Oregon; TX,
Texas; VT, Vermont; WA, Washington; WV, West Virginia; WI,
Wisconsin. Results for GA, NH, and ME (shown circled; see text)
are not included in the regression analysis. Error bars are ( 1 SE.
Mean values are distributed normally (p ) 0.76) with constant
variance (p ) 0.83).
Largemouth bass in Georgia, New Hampshire, and Maine
are outliers to the relationship shown in Figure 1 and are not
included in the regression analysis. The average level of MeHg
in Georgia bass is much lower than expected based on both
the wet atmospheric Hg flux and mean concentrations in
bass from adjoining states of Florida and Alabama (Figure
1). It is unclear why the mean MeHg concentration in Georgia
bass is one of the lowest in the country (Figure 1), especially
given that the biogeochemistry and ecology of surface waters
in this state most probably are comparable to those in
Alabama and Florida. However, when only results from 1994
and 1995 are considered for the Georgia bass (161 fish, 15
water bodies), the mean MeHg concentration is 0.37 µg g-1
wet weight, which is in good agreement with results from
other states with respect to wet atmospheric Hg deposition.
In contrast to Georgia, largemouth bass in the neighboring
states of New Hampshire and Maine have average MeHg
levels that are nearly 3-fold greater than expected based on
measured wet atmospheric Hg fluxes alone (Figure 1). A
potential explanation for this result is that atmospheric Hg
deposition measured at the MDN sites in New Hampshire
and Maine is not representative of Hg fluxes at locations
where most of the fish were sampled. It has been suggested
that atmospheric Hg deposition may be enhanced considerably in southern New Hampshire and southwestern Maine,
potentially as a result of waste incineration and coal-burning
facilities in industrialized regions of southern New Hampshire
and northeastern Massachusetts (24). This is supported by
recent observations of elevated MeHg levels in fish and birds
of southern New Hampshire and southwestern Maine relative
to those of other New England locations (25, 26). While the
majority of MDN sites in these states are in rural locations
(15), and presumably distant from such local emission
sources, most of the largemouth bass analyzed in this study
were sampled from ponds within the suspected region of
locally enhanced MeHg bioaccumulation and Hg deposition.
Indeed, more than two-thirds of the bass analyzed from each
state were sampled from either the southwestern corner of
Maine or the five southeastern counties of New Hampshire.
Hence, there is good reason to suspect that atmospheric Hg
deposition at locations where largemouth bass were sampled
in New Hampshire and Maine may be considerably different
from what is indicated by results from the MDN stations in
each state. Results for MeHg in Massachusetts bass, which
are in good agreement with the other states relative to
measured wet atmospheric Hg fluxes (Figure 1), are not biased
from these potential local Hg emission sources because fish
sampling locations are more broadly distributed throughout
the state and not concentrated in the northeast corner.
Hg Deposition and Other Biological Indicators. The
observed relationship between MeHg in largemouth bass
and wet atmospheric Hg deposition (Figure 1) is supported
by results from studies with other widely distributed aquatic
organisms that occupy both lower and comparable trophic
levels. We have observed previously that MeHg in mosquitoes,
which have aquatic life stages, is related positively to wet
atmospheric Hg deposition among regions of North America
that span a 10-fold range in wet Hg deposition (10).
Additionally, a unique geographical survey of Hg in blood of
fish-eating common loons Gavia immer also suggests a
linkage between atmospheric Hg deposition and MeHg
bioaccumulation in aquatic systems. In the mid-1990s, Evers
and co-workers (27) measured total Hg in blood of adult and
juvenile common loons sampled during summer breeding
seasons in Alaska and the Pacific Northwest (Washington
and Montana), Upper Great Lakes (northern Wisconsin,
Minnesota, Michigan), and New England (New Hampshire
and Maine) regions of the United States. They observed that
total Hg in loon blood, which reflects exposure of the birds
to MeHg from their diet at the time of sampling (28), increased
considerably from west to east across North America, and
suggested that the trend resembled modeled predictions of
Hg deposition at the time (27). Wet atmospheric Hg fluxes
have since been measured at these locations. Figure 2 shows
the loon blood results of Evers et al. (27) versus measured
wet atmospheric Hg fluxes. Although the number of sampling
locations is limited, there are strong correlations between
wet atmospheric Hg deposition and total Hg in the blood of
both adult (r2 ) 0.97) and juvenile (r2 ) 1.00) loons for Alaska,
the Pacific Northwest, and Upper Great Lakes regions.
Moreover, and similar to the pattern observed for largemouth
bass in this study, adult and juvenile loons in New Hampshire
and Maine are outliers to the correlation observed among
the other locations. Results from the loon study appear to
support our hypothesis that MeHg bioaccumulation is linked
to atmospheric Hg deposition among most locations, and
that MeHg in biota of New Hampshire and Maine is enhanced
considerably relative to wet atmospheric Hg fluxes measured
at the MDN sites.
Additional Physicochemical Factors. As noted, a variety
of biogeochemical factors other than Hg inputs are known
or suspected to influence the production and/or bioaccumulation of MeHg in aquatic systems. Figure 3 shows
relationships between state-wide mean concentrations of
MeHg in largemouth bass and average annual precipitation
depth, wet atmospheric deposition of acid and sulfate, surface
water pH, and air temperature for the 25 states analyzed in
this study. Of these factors, only surface water pH is correlated
significantly with MeHg in largemouth bass when results
from all states are considered (Table 1). We have suggested
that bass MeHg levels in New Hampshire, Maine, and Georgia
may be anomalous with respect to wet atmospheric Hg
deposition. Mean concentrations of MeHg in bass from these
states also may be anomalous with respect to several of the
factors shown in the Figure 3. Linear regression statistics
improve modestly when results from these three states are
excluded from the regression analyses (Table 1). However,
and even when New Hampshire, Maine, and Georgia are
excluded from analysis, none of the independent variables
shown in Figure3 can account for more than 40% of the
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C
FIGURE 2. Variation of total Hg in blood of adult and juvenile common
loons during summer breeding seasons (27) as a function of measured
wet atmospheric Hg deposition among regions of North America.
Wet atmospheric Hg fluxes are estimated for the respective breeding
areas: Alaska (mean, 3.1 µg m-2 y-1), average between arctic (1.5
µg m-2 y-1; 48) and southeastern coastal locations (4.6 µg m-2 y-1;
W. F. Fitzgerald, unpublished data); Pacific Northwest (5.1 µg m-2
y-1), average between two sites in Washington (Table B in
Supporting Information) and a site in western Montana (15); Upper
Great Lakes (7.7 µg m-2 y-1), average for nine sites in northern
Minnesota, Wisconsin, and Michigan (Table B in Supporting
Information); Maine/New Hampshire (5.9 µg m-2 y-1; Table B in
Supporting Information). Error bars are ( 1 SE.
variation in average bass MeHg concentrations among states
(Table 1).
The type of water body sampled for largemouth bass varied
among states (see Table A in Supporting Information).
However, differences in the relative number of lakes,
reservoirs, or rivers sampled for bass had no discernible effect
on variations in MeHg concentration among states (see Figure
E in Supporting Information). There is no significant correlation between state-wide average concentrations of MeHg
in largemouth bass and the percentage of sampled water
bodies that are either lakes (r ) -0.01, p ) 0.97), reservoirs
(rs ) 0.16, p ) 0.44), or rivers (r < 0.01, p ) 0.99) among
states. The relationships also are not significant when results
for New Hampshire, Maine, and Georgia are excluded (p )
0.24-0.53). Thus, and based on the variables considered in
this study, relative differences in the types of water bodies
sampled among states appear to have minimal influence on
state-wide average levels of MeHg in largemouth bass.
Forward-stepwise multiple regression analysis was used
to evaluate the relationship between MeHg in largemouth
bass and several independent variables among states. These
variables included water body types (fraction of sampled
water bodies in each state that are either lakes, rivers, or
reservoirs), surface water pH, precipitation depth, temperature, and wet atmospheric deposition of Hg, acid, and
sulfate. Results for New Hampshire, Maine, and Georgia were
D
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not considered in the stepwise regression analysis because
most of the variables noted above were related most strongly
and independently to bass MeHg when these states were
excluded (Figure 1, Table 1). The stepwise regression analysis
revealed that MeHg in largemouth bass was influenced
significantly by only wet atmospheric Hg deposition (p <
0.001). No other factors improve the linear model significantly
(p ) 0.32-0.93). Accordingly, and among these variables,
wet atmospheric Hg deposition, which describes about 70%
of the variation in bass MeHg among most states (Figure 1),
appears to be a primary factor influencing MeHg bioaccumulation.
Temperature. Previous studies have found, most notably,
that temperature, surface water pH, and sulfate availability
are important factors related to the cycling of MeHg.
Temperature can affect MeHg production and bioaccumulation by influencing the activity of methylating bacteria (e.g.,
4, 7) and potentially the uptake of MeHg by fish via effects
on metabolism and growth. It is apparent from Figure 3 (panel
e), however, that mean air temperature, which is a proxy for
surface water temperature, has no substantial effect on MeHg
in largemouth bass across the broad geographical range
examined in this study. Moreover, and if geographical
differences in the growth rate of largemouth bass affect MeHg
bioaccumulation, then they do not influence the relationship
in Figure 1 positively. Comparative studies of bioaccumulation in wild fish populations have shown that differences
in MeHg production and subsequent dietary exposure of
fish, not their rate of growth, are the dominant source of
variation in fish MeHg concentrations (29, 30). It has been
hypothesized, however, that more rapidly growing fish will
have lower MeHg concentrations than slower-growing fish
at a given length (31). While it is not practical to examine
growth rates of largemouth bass in each of the 1043 water
bodies analyzed in this study, it is reasonable to infer that
the growth rate of bass varies largely as a function of climate/
temperature (32). This would suggest, for example, that 3040 cm largemouth bass in subtropical southeastern states
(e.g., Florida, Alabama) that are 3-4 y old (33) should have
lower MeHg levels than comparably sized, but slower-growing
bass (i.e., 5-6 y old; 34) in temperate Midwestern states (e.g.,
Minnesota, Wisconsin). This is in contrast to the results shown
in Figure 1, which indicate that largemouth bass in Florida
and Alabama have, on average, nearly 2-fold more MeHg
than those in Minnesota and Wisconsin. Accordingly, and if
differences in growth rate do influence the bioaccumulation
of MeHg, they presumably would attenuate the relationship
in Figure 1.
pH. There is a statistically significant correlation between
state-wide average levels of MeHg in largemouth bass and
mean surface water pH for the states analyzed in this study,
especially when New Hampshire, Maine, and Georgia are
excluded from analysis (Table 1). Surface water acidity often
is associated with enhanced production and/or bioaccumulation of MeHg (e.g., 4, 5, 25, 29), although the mechanism
by which a reduced pH influences MeHg cycling remains
unclear. Within the normal range of pH values found in nature
(pH 5-9), there is no substantial effect of H+ activity on
either the speciation, and presumed bioavailability, of
dissolved Hg-sulfide and Hg-organic ligand complexes (3537), or the activity of sulfate-reducing bacteria (38), the
presumed primary methylators of Hg (1). Inverse correlations
between pH and MeHg bioaccumulation may be related to
greater facilitated uptake of inorganic Hg by methylating
organisms when H+ activity is increased (39), or these
relationships may exist because surface water pH simply covaries with Hg species and acid delivered from either the
watershed or atmosphere. Indeed, and among the 25 states
included in this analysis, average surface water pH is
correlated with wet atmospheric deposition of Hg (r ) -0.56,
FIGURE 3. Weighted-mean MeHg concentration in fillets of largemouth bass (30-40 cm total length) versus average biogeochemical
characteristics for each state: (a) annual precipitation depth, (b) wet atmospheric acid (H+) deposition, (c) wet atmospheric flux of sulfate
(SO42-), (d) pH of surface water, and (e) annual air temperature. Symbols are the same as those in Figure 1.
p ) 0.004), acid (r ) -0.59, p ) 0.002), and sulfate (r ) -0.53,
p ) 0.006), all of which are derived in part from anthropogenic
combustion sources (40, 41). While it is obvious how the
supply of inorganic Hg substrate may affect MeHg production, there is limited mechanistic information to explain how
acidity influences MeHg production or bioaccumulation,
except that it may co-vary with the supply of substrate Hg
or sulfate.
Sulfate. Microbial SO42- reduction can be sulfate-limited
(42), and in studies of temperate aquatic systems, experimental additions of sulfate increase MeHg production (e.g.,
1, 43). These results point to SO42- availability as a potentially
important factor influencing MeHg production in freshwater
systems (5). Atmospheric deposition can be a major source
of sulfate to some aquatic systems (44, 45). However, there
is no relationship between MeHg in largemouth bass and
wet SO42- deposition when all of the states are considered,
and only a moderate correlation when New Hampshire,
Maine, and Georgia and excluded (Table 1). Total loadings
of sulfate to aquatic systems, including dry deposition and
weathering reactions in the watershed, can vary considerably
and independently of wet atmospheric SO42- deposition, yet
these results suggest that wet atmospheric fluxes of sulfate
may not be a major control on the net production and
bioaccumulation of MeHg. Alternatively, there is recent
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TABLE 1. Linear Regression Statistics for Relationships
between Mean MeHg Concentrations in Largemouth Bass and
Average Physicochemical Characteristics for the 25 States
Considered in This Analysis (i.e., Figure 3), With and Without
Results from New Hampshire (NH), Maine (ME), and Georgia
(GA)
including ME,
NH, GA
excluding ME,
NH, GA
variable
r2
p
r2
p
precipitation depth
wet acid deposition
wet sulfate deposition
surface water pH
air temperature
0.06
0.12
0.10
0.25
0.01
0.25
0.09
0.12
0.01
0.60
0.11
0.15
0.21
0.39
0.26
0.13
0.08
0.03
0.002
0.02
evidence that suggests MeHg production may be independent of SO42-. Iron-reducing bacteria can methylate Hg (46),
and we have observed that there were no relationships
between sulfate and either sediment MeHg concentration,
potential rate of Hg methylation, or benthic MeHg flux among
four arctic Alaskan lakes spanning a 10-fold range of ambient
sulfate (9).
The results of this study suggest that inputs of atmospherically derived Hg may be an important factor influencing
MeHg bioaccumulation in wild fish populations remote from
direct industrial or geologic sources of Hg. As noted, a variety
of environmental factors can influence the transport, transformation, and fate of Hg species in aquatic systems, and
many of these factors vary among individual watersheds.
This is readily apparent, for example, by comparison of the
long-term monitoring results for MeHg in largemouth bass
from Michigan and Louisiana surface waters (Figures A and
B in Supporting Information). Bass MeHg concentrations
vary considerably among individual lakes, rivers, bayous,
and reservoirs that receive comparable wet atmospheric Hg
fluxes within each state. However, and on average, differences
in wet atmospheric Hg deposition can account for about
70% of the variation in bass MeHg levels among most states
(Figure 1). Thus, and while watershed-specific factors can
result in considerable differences of MeHg bioaccumulation
locally, this analysis integrates intra-state variations of
bioaccumulation and suggests that the ultimate supply of
inorganic Hg may be an important factor influencing MeHg
bioaccumulation on local and broader geographic scales.
This result is novel, but not unprecedented; comparable
investigations, spanning a 3-10× range of wet atmospheric
Hg deposition, have found significant positive relationships
between wet atmospheric Hg fluxes and MeHg in both
mosquitoes (10) and common loons (Figure 2; 27). However,
the MeHg cycle is more complex than portrayed by these
linear relationships, and future research should reveal more
fully the biogeochemical mechanisms linking these two end
members of the cycle.
We found that the state-wide average concentration of
MeHg in largemouth bass is correlated with wet atmospheric
Hg deposition among many American states. This suggests
that the supply of inorganic Hg to freshwater systems, most
of which is derived from the atmosphere, is an important
factor influencing the accumulation of MeHg in aquatic
organisms. Anthropogenic Hg emissions, largely from the
combustion of fossil fuels (41), have been estimated to have
increased atmospheric loadings 3-fold globally since the
Industrial Revolution (47). This implies that levels of MeHg
in aquatic food webs worldwide may have been substantially
lower in the pre-industrial past, and also suggests that future
reductions in anthropogenic Hg emissions to the atmosphere
may resultin proportionately lower levels of MeHg in aquatic
organisms, including fishes consumed by humans.
F
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Acknowledgments
We thank the many researchers who contributed data for
this study, particularly David Evers, Neil Kamman, Ken Krier,
Richard Langdon, John Olson, Dave Stone, and Jay Wright.
We are grateful to Carl Lamborg, Mark Sandheinrich, and
four anonymous reviewers for providing helpful reviews of
earlier versions of this manuscript. Support was provided by
the NSF (0425562) and the Postdoctoral Scholar Program at
the Woods Hole Oceanographic Institution, with funding
from the Doherty Foundation.
Supporting Information Available
Five figures and three tables with references. This material
is available free of charge via the Internet at http://
pubs.acs.org.
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