Environ. Sci. Technol. 2009, 43, 1750–1755
Trend Reversal of Mercury Concentrations in Piscivorous Fish from Minnesota Lakes: 1982-2006 BRUCE A. MONSON* Minnesota Pollution Control Agency, 520 Lafayette Road No., St. Paul, Minnesota
Received September 26, 2008. Revised manuscript received December 26, 2008. Accepted January 8, 2009.
The trend of mercury concentrations in standardized length northern pike (NP55) and walleye (WE40) was evaluated for a 25year period, 1982-2006, based on a data set of 1707 cases from 845 lakes throughout Minnesota. Two lines of evidence—changes within individual lakes and regression analyses for all lakes together—indicate a downward trend before the mid-1990s and an upward trend thereafter. Within lakes, the evidence is based on the difference between two years of data at least 5 years apart. Before 1995, 64% decreased and 31% increased; after 1995, 35% decreased and 60% increased. Three regression modelsslinear, quadratic, and twosegment linear piecewiseswere evaluated for best fit using the Akaike Information Criteria (AIC). The two-segment linear piecewise regression model, with a breakpoint of 1992, was the best fit, while the quadratic model, with an inflection point of 1995, also had substantial support. The linear model was not supported (∆AIC > 10). Based on least-squares linear regressions applied separately to 1982-1992 and 1992-2006, mercury concentrations in NP55 and WE40 decreased 4.6 ( 1.3% (95% CI) per year from 1982 to 1992 and increased 1.4 ( 0.8% per year from 1992 to 2006.
Introduction Consumption of fish is the primary route of exposure to methylmercury in most human populations and in wildlife (1). Mercury concentrations in fish respond to changes in mercury load (2), which is primarily from atmospheric deposition in most surface waters (3-5). Mercury deposition has increased by a factor of 2-3 over the last 150 years, although since the 1970s mercury deposition, as measured in lake sediment cores, has shown a substantial decline in many Minnesota lakes (4, 6). Mercury deposited directly to a lake can be methylated and bioaccumulated by biota within weeks, but export of mercury deposited on the watershed takes years (7). Long-term monitoring of mercury concentrations in fish from newly flooded reservoirs has shown peak production of new methylmercury was reached within a few years of flooding, while mercury concentrations in northern pike and walleye peaked 2-8 years later (8). Therefore, mercury concentrations in fish are expected eventually to respond to the changing atmospheric mercury deposition, but the lag time of the response is uncertain. Fish contaminant databases are maintained by states primarily for fish consumption advisories and related impaired waters assessment. Their use for other empirical * corresponding author phone: 1-651-757-2579; fax: 1-651-2978676; e-mail:
[email protected]. 1750
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analyses has been limited because these databases usually lack the statistical benefits of probability-based sample collection. Most often, they are used for correlation or regression analysis (9-11) rather than trend analysis. For those studies that have analyzed for long-term trends, they mainly found downward trends over the last 20-30 years (10, 12-14). Minnesota’s Fish Contaminant Monitoring Program has collected fish for mercury since the late 1960s, and the database contains mercury concentrations for more than 60 fish species. The ubiquitous top piscivore species, northern pike (Esox lucius) and walleye (Sander vitreus), are used as indicators of mercury contaminant levels. Mercury concentrations in northern pike and walleye sampled from Minnesota lakes were statistically examined to (1) determine if standardized lengths of the two species were equivalent indicators of mercury contamination and (2) characterize temporal trends in mercury concentrations between 1982 and 2006.
Materials and Methods Fish Collection, Processing, and Analysis. The Minnesota Department of Natural Resources (MDNR) has surveyed 4400 lakes over the last 50 years using gill nets and trap nets. The number of lakes surveyed per year has remained at 500-700 lakes per year. The fish survey rotation depends on lake size and angling use; large, heavily used lakes are surveyed more frequently than small, lightly used lakes. Some are surveyed in 1-3 year cycles, but most surveys are on a 5-year cycle, and remote lakes have rotations of over 20 years. A representative subset of the surveyed waters is selected for mercury analysis of fish tissue, which includes new and resampled sites. Site selection is a collaborative result of the Minnesota Department of Health’s development of fish consumption advisories, the Minnesota Pollution Control Agency’s interest in trends and compliance with water quality standards, and the MDNR’s responsibility for management of fish and fish-eating wildlife. Collected fish are wrapped in aluminum foil and stored frozen. Thawed fish are filleted (skin-on), ground, and refrozen in clean 125 mL glass jars until analyzed. Before 1997, fish of similar length were usually composited into several samples per site; beginning in 1997, predator fish were analyzed individually to improve the statistical power of the data. Three laboratories analyzed fish tissue samples for mercury: (1) Minnesota Department of Health, 1982-1989, (2) Braun Intertec Environmental, Inc., 1990-1998, and (3) Minnesota Department of Agriculture, 1998-2006. All laboratories analyzed for total mercury (wet weight), following the same sample quality control protocol. During each laboratory transition, split samples were analyzed by each laboratory to establish continued data comparability. At both transitions, the relative percent differences for the split samples were within the range seen for duplicate samples analyzed within laboratories. A summary of the representative accuracy and precision assessments of the laboratories is included in the Supporting Information (SI). Standardized Length Predator Fish. Mercury concentrations in 55 cm northern pike (NP55) and 40 cm walleye (WE40) were derived from weighted-average length-specific mercury concentrations. The calculation procedure and a comparison to the linear regression approach are described in the SI. SI includes plots of mercury concentration versus fish total length for each case (lake-species-year) where standardized length concentrations were determined. The plots show the 10.1021/es8027378 CCC: $40.75
2009 American Chemical Society
Published on Web 02/09/2009
and y2 are coefficients before and after the breakpoint time (T) respectively; tmin is 1982 and tmax is 2006. T is the threshold where the regression line changes slope, as determined by the Marquardt-Levenberg algorithm (eq 3). Statistical analyses were performed with SYSTAT 12.0 (Systat Software, Inc., 2007) and SigmaPlot 10.0 (Systat Software, Inc. 2006). The best-fit model was selected based on Akaike Information Criteria (AIC) (17). AIC is scaled as ∆AIC, where, ∆AIC ) AICi - AICmin. The best-fit model has ∆AIC ) 0. To assess the relative support for the fit of a model, models having ∆AIC e 2 have substantial support, whereas models with ∆AIC > 10 are not supported (17). Akaike weights (wi) are included to present the support levels in terms of probability.
Results
FIGURE 1. Map of Minnesota showing locations of lakes having sufficient data to calculate mercury concentrations in standardized length predator fish, SPFHg (NP55 or WE40). fish samples overlap the standardized length and indicate the number of fish per sample. NP55 and WE40 together are referred to as standardized predator fish mercury concentrations (SPFHg). They were evaluated for the statewide data set and for the Northern Lakes and Forest (NLF) ecoregion. The NLF, based on the Level III ecoregions (15), is the largest ecoregion in the state, covering 31% of the total area in Minnesota, 49% of the open water area, and 44% of the state’s wetland area (Figure 1). Before 1990, nearly all analysis of mercury in fish was collected in NLF because of its preponderance of fishable lakes and the expectation that most lakes impaired by mercury contamination in fish tissue were in northern Minnesota (16). For the period of record, 1982-2006, there were 1707 SPFHg cases (lake-species-year) from 845 lakes. The average number of cases per year increased from 44 (range 21-67) before 1990 to 82 (range 31-134) afterward because of an increased effort to collect samples throughout the state. Before 1990, 93% of the cases were in the NLF ecoregion; after 1990, 65% were in the NLF. Trend Analysis. The general modeling goal for trend analysis was to describe the pattern of SPFHg over time. Three regression models were evaluated for the best fit to temporal trends in mercury concentrations, having the following general forms: linear y ) y0 + at
(1)
quadratic y ) y0 + at + bt2
(2)
and two-segment linear piecewise
{
y1(T - t) + ymin(t - tmin) , tmin e t e T T - tmin f ) ymin(tmax - t) + y2(t - T) , T e t e tmax tmax - T
(3)
where, t ) year and y ) loge-transformed mercury concentration. In the two-segment piecewise regression model, y1
NP55 and WE40 were combined for part of the inferential statistical analysis because they have virtually identical distributions. Variances were not significantly different between the two species, based on an F-test for the equality of variances applied to the loge of WE40 and NP55 (F-ratio 0.939, p ) 0.360). Based on a two-sample t test, the means of WE40 (327 ppb) and NP55 (334 ppb) were not significantly different (t ) 0.756, p ) 0.450) and the same was true for the loge-transformed values (t ) 1.409, p ) 0.159). Accordingly, NP55 and WE40 were expected to give the same results if they were taken from the same waterbody. To evaluate this expectation of similarity, a major axis regression of the 393 lake-years where WE40 and NP55 coexisted resulted in the equation Log(NP55) ) 1.027((0.057)Log(WE40) - 0.047((0.136) (4) The 95% confidence intervals in parentheses indicate the slope and intercept were not significantly different from 1 and 0, respectively. Therefore, NP55 and WE40 had an evident 1:1 relationship where they coexist. Temporal trends are typically evaluated in terms of a linear regression model; however, diagnostic plots of SPFHg time series suggested a nonlinear pattern, decreasing from 1982 to the mid-1990s and then increasing. To test this ostensible nonlinearity, the three regression modelsslinear, twosegment linear piecewise, and quadraticswere applied to the statewide and NLF ecoregion data sets. For each data set, NP55 and WE40 were evaluated separately and together (Table 1). Comparison of AIC for the three regression models indicates that the two-segment piecewise model was the best fit for all but statewide NP55. The quadratic model was essentially equivalent to the piecewise model (∆AIC < 2) or had moderate support (∆AIC < 10). Akaike weights (wi) indicate the piecewise and quadratic models were of nearly equal weight (i.e., equal probability as the best fit model) for the SPFHg statewide. In the NLF ecoregion, however, the piecewise model was clearly superior to the quadratic model for SFPHg (Table 1). The linear model had ∆AIC > 10 for all data sets, except WE40 in NLF; therefore, the linear model is not supported for the trend in SFPHg. The best overall model, based on the information-theoretic approach, was the piecewise model (Figure 2). The breakpoint year, T, was 1992 for all data sets except statewide NP55, which had a breakpoint in 1995 (Table 2). Because of the nonrandom selection of lakes for resampling, there was a potential for bias caused by repeat sampling of high mercury concentration lakes. To test for the influence of repeated samples, the piecewise regression was calculated for NLF-NP55 and WE40 with no repeat years (i.e., only the first year for a given lake and species was used; years other than the first more likely represent biased samples). Sample size was reduced from 1199 to 812. VOL. 43, NO. 6, 2009 / ENVIRONMENTAL SCIENCE & TECHNOLOGY
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TABLE 1. Model Selection Results for Statewide and NLF Ecoregion Datasetsa data set
N
NP55
956
WE40
751
NP55 and WE40
1707
NP55
661
WE40
538
NP55 and WE40
1199
regression quadratic piecewise linear piecewise quadratic linear piecewise quadratic linear
RSS Statewide 313.6 313.9 328.4 262.7 264.1 270.2 577.8 578.5 599.8
piecewise quadratic linear piecewise quadratic linear piecewise quadratic linear
NLF 176.8 177.5 183.0 168.3 169.4 171.4 346.7 348.6 356.2
k
AIC
∆AIC
wi
4 5 3 5 4 3 5 4 3
1655.3 1658.3 1697.5 1352.3 1354.3 1369.5 3005.0 3005.2 3064.8
0.0 3.0 42.2 0.0 2.0 17.2 0.0 0.2 59.8
0.82 0.18 0.00 0.73 0.27 0.00 0.52 0.48 0.00
5 4 3 5 4 3 5 4 3
1014.3 1014.9 1032.8 911.6 913.2 917.4 1924.8 1929.5 1953.5
0.0 0.6 18.5 0.0 1.6 5.8 0.0 4.6 28.6
0.57 0.43 0.00 0.66 0.30 0.04 0.91 0.09 0.00
a RSS, residual sum of squares; k, number of coefficients; AIC, Akaike Information Criteria; ∆AIC ) AICi - AICmin; wi, Akaike weight.
FIGURE 2. Piecewise regression of natural log-transformed standardized predator fish mercury concentration (SPFHg) from 1982 to 2006, showing breakpoint in 1992: (a) State, (b) Northern Lakes and Forests (NLF) Ecoregion. SPFHg include 55 cm northern pike (NP55) and 40 cm walleye (WE40). Regression coefficients did not significantly change; the breakpoint year remained at 1992 (Table 2). 1752
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The piecewise model was linear on either side of the breakpoint, but annual percent change (APC) was not readily determined from the piecewise regression coefficients; therefore, APC was estimated from the slope of ordinary leastsquares regression applied separately to data before and after the breakpoint (Table 3). The regressions were significant (p < 0.05), except the slope for WE40, 1992-2006 (State, p ) 0.0850; NLF, p ) 0.1330). For all data combined, the APC for 1982-1992 was -4.6 ( 1.3% (95% CI) and for 1992-2006, 1.4 ( 0.8%. For just the NLF, the APC for 1982-1992 was -3.3 ( 1.3% and for 1992-2006, 1.5 ( 0.9%. The APCs for NP55 and WE40 separately were similar to the APCs when the two species were combined. Although the linear regression model for the 25-year period was not supported as a good fit, it is noteworthy that the linear model had a significant APC of -0.9 ( 0.4%. While the maximum likelihood estimate for the breakpoint in NP55 and WE40 was 1992 from the piecewise-linear regression, the inflection points for the quadratic regressions ranged from 1995 to 1996. If 1995 is selected as the breakpoint, the APC for all data 1982-1995 is -3.7 ( 0.9% and for 1995-2006, 2.1 ( 1.1%. This underscores the uncertainty in the specific breakpoint year, but supports the conclusion that the breakpoint occurred in the early to mid-1990s, with a downward trend before and an upward trend since the early to mid-1990s. An additional statistical test was pursued to corroborate the trend reversal indicated by the quadratic and piecewise regression models. Preferably, the test of the trend reversal would come from long-term temporal trends within individual lakes over the 25-year period. SPFHg from lakes with 4 or more years of data were evaluated and none had a sufficiently frequent time series over the 25 years to demonstrate any trend. Alternatively, if there was a trend reversal in the mid-1990s, SPFHg in a majority of lakes should have decreased before the mid-1990s and increased after the mid1990s. The trend reversal was tested by examining changes in SPFHg within lakes before and after 1995. Changes within lakes were based on differences between two years of data at least five years apart, both years occurring between 1982-1995 or 1995-2006. The changes were categorized as increasing, decreasing, or no change (no change defined as a difference of
