Environ. Sci. Technol. 2008, 42, 1365–1370
Mercury Concentrations in Salmonids from Western U.S. National Parks and Relationships with Age and Macrophage Aggregates A D A M R . S C H W I N D T , * ,† JOHN W. FOURNIE,‡ DIXON H. LANDERS,§ C A R L B . S C H R E C K , 4,⊥ A N D MICHAEL L. KENT† Department of Microbiology, Center for Fish Disease Research, 220 Nash Hall, Oregon State University, Corvallis, Oregon 97331, Gulf Ecology Division, U.S. Environmental Protection Agency, Gulf Breeze, Florida, Western Ecology Division, U.S. Environmental Protection Agency, Corvallis, Oregon, Oregon Cooperative Fish and Wildlife Research Unit, U.S. Geological Survey, Corvallis, Oregon, and Department of Fisheries and Wildlife, Oregon State University, Corvallis, Oregon
Received September 17, 2007. Revised manuscript received October 30, 2007. Accepted November 20, 2007.
Mercury accumulation in aquatic foodwebs and its effects on aquatic biota are of growing concern both for the health of the fish and the piscivores that prey upon them. This is of particular concern for western U.S. National Parks because it is known that mountainous and Arctic areas are sinks for some contaminants. The Western Airborne Contaminants Assessment Project seeks, in part, to ascertain mercury concentrations and evaluate effects of contaminants on biota in 14 lakes from 8 National Parks or Preserves. In this paper we report that mercury has accumulated to concentrations in trout that may negatively impact some piscivorous wildlife, indicating potential terrestrial ecosystem effects. Additionally, we show that mercury concentrations increase with age in 4 species of trout, providing evidence of bioaccumulation. Finally, we demonstrate that mercury is associated with tissue damage in the kidney and spleen, as indicated by increases in macrophage aggregates. This finding suggests that mercury, and possibly other contaminants, are negativelyaffectingthetroutthatinhabittheseremoteandprotected ecosystems. Our results indicate that mercury is indeed a concern for the U.S. National Parks, from an organismic and potentially an ecosystem perspective.
Introduction A major goal of the Western Airborne Contaminants Assessment Project (WACAP) is to identify contaminants that * Corresponding author phone: +1-541-737-1858; fax: +1-541737-0496; e-mail:
[email protected]. † Department of Microbiology, Center for Fish Disease Research, Oregon State University. ‡ Gulf Ecology Division, U.S. Environmental Protection Agency. § Western Ecology Division, U.S. Environmental Protection Agency. 4 Oregon Cooperative Fish and Wildlife Research Unit, U.S. Geological Survey. ⊥ Department of Fisheries and Wildlife, Oregon State University. 10.1021/es702337m CCC: $40.75
Published on Web 01/18/2008
2008 American Chemical Society
may be ecologically significant for biota in western U.S. National Parks (NPs) (1). Long-range (2, 3) and regional atmospheric transport (4) of pollutants are an issue for the U.S. National Park Service because many semivolatile contaminants are bioactive (5) and they may also bioaccumulate and biomagnify in the food web (6). Mountainous and Arctic aquatic ecosystems, precisely the areas characterized by many western U.S. National Parks, were sampled during these studies and are of particular concern because they are sinks for semivolatile contaminants as has been reported in an earlier publication (7). The parks studied in the WACAP represent a latitudinal and elevational transect that is unprecedented in North America. Salmonids were chosen as sentinel species of contaminants for the WACAP because they are usually top predators in aquatic food webs and were the only common family of fishes to reside in the lakes we studied (1). Fishes are also intermediate in the foodweb, top predators in the aquatic environment, and prey to piscivorous birds and mammals. Biological effects observed in the fishes may then provide an early warning sign as to potential ecosystem effects. This study, unlike most other large-scale ecotoxicology studies, conducted chemical analyses on whole fish as well as physiological and pathological analyses on the same individuals. This allowed for direct determination of pathological and physiological changes coincident with contaminant concentrations. Mercury is of particular concern for WACAP because it bioaccumulates in fish tissues and biomagnifies in the foodweb (8). Efficient incorporation of mercury into the food web depends on microbial conversion of inorganic forms to methyl-Hg (9). Therefore, the deposition of inorganic Hg is an important input to the ecosystem but does not necessarily indicate that Hg will end up in the biota. Methylation is dependent on numerous abiotic factors such as organic carbon, pH, and sulfate (10), among others (9, 11). After accumulation in animals, methyl-Hg can affect nearly every body system and induces oxidative stress (12) leading to tissue damage (13, 14). Histopathological biomarkers can be used to assess the effects of prior or current exposure to contaminants at the level of the individual (15). One of these biomarkers is macrophage aggregates (MAs), which are focal accumulations of macrophages that are found in the spleen, kidney, and sometimes liver of teleost fishes. They contain three types of pigments: ceroid/lipofuscin, melanin, and hemosiderin and they are formed in response to tissue damage (16, 17). Macrophage aggregates scavenge cellular debris resulting from, for example, erythrocyte break-down and lipid peroxidation and are thought to be primitive analogs to mammalian lymph nodes (16, 17). Several studies have demonstrated a significant correlation between increased MAs in fishes from polluted waters (18–20) and fishes exposed to mercury (21, 22) and other metals (23, 24). Fish age is also a significant explanatory factor in MA accumulations (16, 17). The primary purpose of this study was to determine total Hg concentrations in salmonid fishes inhabiting remote lakes in U.S. National Parks. Second, we wanted to determine if fishes exposed to mercury showed any evidence of tissue damage. More specifically, we aimed to identify any possible relationships between Hg concentrations and accumulations of kidney and spleen MAs.
Experimental Section Fish Sample Collection. Fishes were collected from 8 western U.S. National Parks or Preserves for analysis of semivolatile VOL. 42, NO. 4, 2008 / ENVIRONMENTAL SCIENCE & TECHNOLOGY
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TABLE 1. Lakes, Species, Number of Fish Analyzed, and Geographic Variables in Western U.S. National Parks national park
lake (year)
species
N
latitude
longitude
elevation (m)
Noatak Gates of the Arctic Denali
Burial (2004) Matcharak (2004) Wonder (2004) McLeod (2004, 2005) Snyder (2005) Oldman (2005) PJ (2003, 2005) Hoh (2005) Golden (2005) LP19 (2005) Mills (2003) Lone Pine (2003) Pear (2003) Emerald (2003)
Salvelinus namaycush S. namaycush S. namaycush Lota lota Oncorhynchus clarki lewisi O. clarki bouvieri S. fontinalis S. fontinalis S. fontinalis S. fontinalis O. mykiss S. fontinalis S. fontinalis S. fontinalis
10 10 10 4 15 10 25 15 15 15 10 10 10 10
68.43N 67.75N 63.48N 63.38N 48.62N 48.50N 47.95N 47.90N 46.89N 46.82N 40.29N 40.22N 36.60N 36.58N
-159.18W -156.21W -150.88W -151.07W -113.79W -113.46W -123.42W -123.79W -121.90W -121.89W -105.64W -105.73W -118.67W -118.67W
427 488 610 609 1600 2026 1433 1384 1372 1373 3030 3024 2904 2800
Glacier Olympic Mount Rainier Rocky Mountain Sequoia
organic contaminants, metals including Hg, and fish health as part of WACAP. We sampled two lakes per park that were selected using the following criteria: (1) the lakes occupied relatively small catchments with no major inlets or outlets, (2) the lakes were not fed by glacial water, (3) lakes contained reproducing populations of nonanadromous salmonid fishes, and (4) had suitable bathymetry for the collection of sediment. The parks and lakes sampled ranged from north of the Arctic Circle in Alaska to southern California and east from the Olympics to parks in the Rocky Mountains. Lake elevation ranged from approximately 400 m in the Arctic to over 3000 m in Rocky Mountain NP (Table 1). Samples were collected between the months of July and September from 2003 to 2005. All lakes were sampled once during the study, except for PJ Lake, Olympic NP (2003 and 2005) and McLeod Lake, Denali NP (2004 and 2005). All fish were handled in accordance with Institutional Animal Care and Use Committee guidelines at Oregon State University. Angling, gill nets, or set-lines were used to capture brook (Salvelinus fontinalis), rainbow (Oncorhynchus mykiss), west slope cutthroat (O. clarki lewisi), yellowstone cutthroat (O. clarki bouvieri), or lake (S. namaycush) trouts from each lake. Burbot (Lota lota) were captured from one lake. Sample processing details are reported in the Supporting Information. Fish Analytical Methods. We measured total Hg rather than methyl-Hg to maintain consistency between Hg analyses in the other environmental compartments studied in WACAP. Mercury was analyzed in the whole-body homogenate by combustion atomic absorption spectrophotometry with a LECO AMA254 advanced mercury analyzer (LECO, St. Joseph, MI) according to USEPA Method 7473 (25). Results were reported as wet weight means of two replicate analyses. Quality assurance details are provided in the Supporting Information. Brook, rainbow, and cutthroat trouts were aged by examining annuli on otoliths along the sagittal axis as described by Hall (26). Sagittal otoliths from lake trout were aged along the lateral axis as described by Simoneau et al. (27). Otoliths from all fish were examined under transmitted compound light microscopy and 1 dark and 1 light band was counted as 1 year. After aging, fish were selected (N ) 10) for Hg analysis to obtain even sex, maturation, and age distributions. This was also to determine if Hg was agedependent and if sex or maturation effects were evident. In some instances all 15 fish were analyzed for Hg. PJ Lake, Olympic NP and McLeod Lake, Denali NP were sampled twice, where N ) 25 and N ) 4, respectively. Low fish availability limited the sample size at McLeod Lake (Table 1). Percent area of the tissue occupied by MAs was determined in all fish as described by Schwindt et al. (28). See the Supporting Information for the raw data. 1366
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Fish Consumption Criteria. Lazorchak et al. (29) developed fish consumption criteria for mink (Mustela vison), river otter (Lutra canadensis), and belted kingfisher (Ceryle alcyon) in the Mid-Atlantic States, United States and we used these values to identify NPs that contained fish with mercury concentrations above the various criteria. Although the criteria were developed for the Mid-Atlantic States, mink, otter, and kingfishers inhabit nearly all the field sites in this study. For assumptions made with the human criteria, see USEPA (30) and Peterson et al. (31) for converting the human threshold developed for filet to whole-body concentrations. Statistical Analysis. All data were inspected for normality prior to statistical analyses. Arcsine square-root transformations were used on the MA data for regression analysis with Hg concentrations, for among-lake comparisons, and for the Student’s T-test when looking for sex differences. Unequal variance in Hg data was detected using Levene’s test and was corrected by log10 transformation prior to ANOVA. Mean age, MAs, and Hg (log10) were compared among lakes with ANOVA or Kruskal–Wallis (KW) followed by a Bonferroni post hoc (at 95% confidence) because of skewed data. The slopes of the regressions for among-lake comparisons of MAs versus age and Hg were compared using analysis of covariance (ANCOVA). Statistical significance was set at P < 0.05 and the degrees of freedom are given as subscripts.
Results and Discussion Hg in Fish and Risk to Wildlife. Total Hg concentrations were determined on 169 fish from 14 lakes in 8 National Parks or Preserves from southern California to Arctic Alaska. Average total Hg concentrations ranged from 16.9 to 411 ng g-1 ww among lakes. Mercury concentrations exceeded consumption criteria as identified by Lazorchak et al. (29) assuming a diet entirely of fish or prey at similar trophic levels for the specified wildlife in most parks (Figure 1). Mercury concentrations exceeded criteria at several lakes, but Lazorchak et al. (29) indicated that deleterious effects on the wildlife may vary because effects are contingent upon numerous other factors. Individual differences in response to Hg depend on sex, reproductive strategy and status, exposure to other stressors, and the overall health of the animal. In addition, an unknown amount of error in the risk assessment could adjust the criteria up or down. In the Arctic at Burial Lake, Noatak NP, average Hg concentrations also exceeded consumption criteria for humans (sensitive populations) and individual Hg concentrations at several other sites were above the recommended thresholds for humans (Figure 1). Biomagnification of Hg has been observed in other mountain (32) and Arctic
FIGURE 1. Mean whole-body total Hg and 95% confidence intervals based on wet weight from all National Parks lakes and consumption criteria for various biota (see Experimental Section). Data start at 10 ng g-1 and are plotted on log10 scales. N ) 4-25. SEKI ) Sequoia, ROMO ) Rocky Mountain, MORA ) Mount Rainier, OLYM ) Olympic, GLAC ) Glacier, DENA ) Denali, and GAAR ) Gates of the Arctic National Parks, and NOAT ) Noatak Natural Preserve. Salmonid fishes (Salvelinus spp. and Oncorhynchus spp.) were captured at all lakes except McLeod where burbot (Lota lota) were captured. aquatic ecosystems (33), suggesting that Hg also poses a risk in ecosystems outside of NPs. In comparison to other studies, mercury concentrations in the trout from the parks in this study were lower than those reported for lakes in the Midwest and Northeast United States, including Lake Michigan and Lake Superior. See Supporting Information Table S1 for details. Mercury concentrations were lower in fish at all WACAP parks than in 1-year-old insectivorous yellow perch (Perca flavescens) at Voyageurs National Park in Minnesota. The same was true for lake trout and northern pike (Esox lucius) in northern lakes (50° N latitude and above) in Canada. In contrast, fish from our study showed higher Hg levels than Arctic char (Salvelinus alpinus), grayling (Thymallus arcticus), and brook trout from northern lakes in Canada. Also, mercury levels were higher in fish from this study than in brown trout (Salmo trutta) from similar mountain and sub-Arctic ecosystems in Europe. Juvenile sturgeon (Acipenser transmontanus) in the Columbia River, United States, had lower mercury concentrations than fish from the Arctic, Denali, Olympic, and Mount Rainier National Parks, although a 41-year-old adult female sturgeon had mercury concentrations well above all fish in this study. In lakes with brook trout, average Hg (log10) was significantly elevated at LP19, Mount Rainier NP and Hoh Lake, Olympic NP compared to Lone Pine Lake, Rocky Mountain NP and Golden Lake, Mount Rainier NP (F6,93 ) 4.33, P ) 0.0007). Mercury (log10) was significantly elevated at Burial Lake, Noatak Natural Preserve compared to the other lakes with lake trout in Alaska (F2,27 ) 7.61, P ) 0.002). In lakes with Oncorhynchus spp. mercury (log10) was elevated at Mills Lake, Rocky Mountain NP compared to Snyder Lake, Glacier NP (F2,32 ) 4.13, P ) 0.02). Within species, age was not different among any of the lakes (P > 0.05, Table S2). Mercury concentrations were age-dependent in brook, rainbow, and cutthroat trouts (Figure 2, Table S3). Mercury was agedependent in lake trout up to 15 y, after which Hg declined with age (Figure 2). The reasons for this are uncertain and cannot be resolved with the current data set. Methylation is the driving force in Hg bioaccumulation (9) however numerous factors regulate the rate of uptake and depuration. Variable rates of methylation may, in part, explain the
FIGURE 2. Scatterplot of fish age versus whole-body total Hg in trout from all lakes. Some data points are overlapping. differences observed within and among parks with the same species of fish (Figure 1). Species and Lake Effects on Hg Concentrations and MAs. Spleen MAs were significantly elevated in lake trout at Wonder Lake, Denali NP (F2,27 ) 32.98, P < 0.0001) compared to Matcharak and Burial Lake in the Arctic (Table S2). In the Oncorhynchus spp. spleen MAs were elevated at Snyder Lake, Glacier NP compared to Mills Lake, Rocky Mountain NP and Oldman Lake in Glacier NP (F2,32 ) 7.94, P ) 0.002). In brook trout, comparison of median spleen MAs by KW yielded a significant main effect (KW6,93 ) 14.31, P ) 0.03) but differences between individual lakes were not detected. Mercury has been associated with increased MAs in fish in both field (22) and experimental studies (21). In a polluted river in Germany, Meinelt et al. (22) found positive correlations between liver, kidney, and spleen MAs and mercury in individual northern pike. Handy and Penrice (21) induced MAs in the rainbow trout kidney by chronic per os exposure of 10 mg kg-1 HgCl- over 42 d. Although this is a high dose, it establishes the proof of concept that mercuric compounds can induce the formation of MAs in salmonid fishes. It should also be noted that the above cited studies used mercuric salts, as opposed to methyl-Hg. To our knowledge it remains to be determined if methyl-Hg also induces MAs. In terms of geographic variation, it is likely that the brook trout among lakes experienced differences in biotic and abiotic factors that, in addition to Hg, contributed to MAs. Indeed, dividing and analyzing brook trout by lake led to a dramatic increase in the variation explained by the regression model (Table S5). The among lakes slopes of the MA and Hg regression lines were not different (F1,6 ) 1.43, P ) 0.21) suggesting that spleen MAs in all brook trout responded similarly to whole-body Hg. This suggests that the mechanisms regulating spleen MA accumulations are reasonably consistent across brook trout in this study. In the lake trout, positive relationships between the sum of MAs and Hg were identified at Wonder Lake, Denali NP (Table S5) but only in lake trout 25 y) and MAs in lake trout were much less abundant than in the brook trout (Table S2), yet Hg was relatively high. Methyl-Hg, the most common form in fish (34), accumulates in numerous tissues to varying degrees (35) but is more concentrated in the skeletal muscle than the VOL. 42, NO. 4, 2008 / ENVIRONMENTAL SCIENCE & TECHNOLOGY
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FIGURE 3. Colinearity between percent area occupied by spleen MAs, Hg, and age in brook trout (A) and log-linear relationships between Hg and brook trout (Salvelinus fontinalis) spleen MAs (B). O and dotted line ) 1 – 3 y Log(X) regression; 9 and solid line ) 4 – 6 y Log(X) regression; ( and dashed line ) 7 – 13 y Log(X) regression. Some data points are overlapping and x-axis data are offset slightly in (A). whole body (31). It is possible that Hg sequestered in skeletal muscle was less available to visceral organs which may explain high concentrations of Hg but low densities of MAs. Hg Affects MAs Independent of Age. Mercury concentrations, MAs, and age were all colinear in brook trout (Figure 3A). This was expected because both MAs (28, 36–38) and Hg concentrations increase with age (Tables S3 and S6). Because MAs increase with age they may reflect past exposure to contaminants (39). Therefore, when comparing fish from polluted and reference sites they should be age matched (39). Additionally, no sex differences in MAs were found (T39female, 59male ) 1.12, P ) 0.26). The slopes of the regression lines between MAs and age were not different (F1,6 ) 0.81, P ) 0.56) among lakes, suggesting that age-dependent accumulations of MAs were consistent for the brook trout. Based on these procedures, no confounding relationships between sex, age, MAs, or Hg resulting from the location of particular field sites were observed; therefore, we grouped the brook trout data for regression analyses. We analyzed 100 brook trout from 7 different lakes for Hg and MAs which represented our largest and most geographically extensive data set for a single species (Table 1). A significant, positive relationship was found between spleen MAs and Hg in all brook trout (F1,98 ) 82.82, P < 0.0001, R2 ) 0.45). Over 90 current and historic pesticides and industrial and urban chemicals were measured in these fish (40). Positive relationships were found between MAs and the polychlorinated biphenyls (F1,68 ) 26.04, P < 0.0001, R2 ) 1368
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0.28) as well as the polybrominated diphenyl ethers F1,68 ) 17.14, P ) 0.0001, R2 ) 0.20). To identify potential relationships independent of age, we evaluated specific age classes. Spleen MAs in 4–6 year old brook trout were positively related to Hg (F1,46 ) 26.27, P < 0.0001, R2 ) 0.36) but 1–3 and 7–13 year old brook trout yielded only weak relationships, if at all (1–3 y F1,28 ) 6.03, P ) 0.02, R2 ) 0.18; 7–13 y F1,20 ) 2.59, P ) 0.12, R2 ) 0.11). See Table S4. Dividing the 7–13 y age classes further did not yield any significant relationships. In 4–6 year old brook trout, only 36% of the variance in the spleen MAs was explained by Hg, indicating that other stressors, including the effects of other chemicals, play a part in age-independent MA accumulation. However, that mercury alone explained over one-third of the variance in MAs suggests that the tissue damage resulting from mercury exposure (12, 13) is important for the formation of MAs in these fish. Feeding ecology may account for the rapid, non-ageassociated changes in contaminant concentrations. Forage availability shifts seasonally, forage basis is site specific, foraging itself changes based on size of the fish, and incorporation of Hg varies between life history stages of salmonids (41, 42). During periods of fast growth and increased food consumption per unit time, Hg accumulates rapidly (41, 42). Mercuric compounds have been associated with MAs (21) and, during periods of fast growth, MAs and Hg increase independently of age as was observed in our results for 4–6 year old brook trout. Rainbow trout were collected from a single lake (Mills Lake, Rocky Mountain NP) and 7 of 10 fish were between 4 and 6 y, so it was not possible to test other age classes. However, spleen and kidney MAs were significantly related to both Hg and age (Tables S5, S6). Similarly in the cutthroat trout from Glacier NP, it was not possible to test numerous age classes. However MAs are related to both age and Hg in both species (Tables S5, S6). The wide age distribution (5–33 y, Table S2) and small sample size (N ) 10) of lake trout prohibited the identification of age classes for Hg and MA regression. Macrophage aggregates were used as an indicator of degraded environments where fish were sampled from areas with differing degrees of pollution (19). We had no knowledge a priori of pollution in the NPs, although project collaborators have recently established that proximity to agricultural areas is associated with pesticides in the snow (7). To our knowledge, the association of MAs to any single compound has not been established on the geographic scale of WACAP. Our results indicate that brook trout MAs can be suggestive of Hg accumulation, and are easily identified during routine histological processing as we have demonstrated in an earlier publication (28). Because MAs respond to tissue damage and increase with age, we contend that MA proliferation might be due to agedependent increases of toxicants especially those that induce tissue damage such as Hg (12, 13). Additionally, other stressors such as starvation play a role in MA formation (43, 44) indicating that MA formation is more than a side effect of aging. This may be comparable to liver spots that develop on fair-skinned persons. Liver spots (senile lentigines) develop in exposed regions of the skin of older persons due to longterm cumulative effects of UV radiation, not due simply to age itself (45). To our knowledge, there are no studies describing the poststressor fate of MAs; therefore, it is possible that MAs persist long after the stressor has ceased or declined. The only significant histological abnormalities in the kidney and spleen were increases in the area of MAs. In the lake trout from Matcharak Lake, Gates of the Arctic NP we identified encysted worms (Raphidascaris sp.) in the liver. Macrophage aggregates were not congregated around the worms nor were they more numerous in fish with prolific
infections (data not shown). Mercury can cause other pathological changes in fishes (46–50). With salmonids, Handy and Penrice (21) observed sloughing of the gut epithelium in addition to increased kidney MAs following high doses of HgCl2. Corresponding Hg concentrations in the kidney ranged from approximately 2–9 µg g-1 (21) which is an order of magnitude higher that the whole-body concentrations determined in this study. In the flounder (Platichthys flesus) Pulsford et al. (24) observed the localization of metals in spleen MAs but no associations were made between the metals and changes in MAs. In summary, total whole-body Hg concentrations exceeded consumption criteria for wildlife at several sites which suggests that Hg is a geographically extensive, ecological problem. Measurements of mercury, MAs, and age in the same fish allowed dissection of covariates and demonstrated positive relationships between age, MAs, and Hg concentrations. It also advanced our understanding of the behavior of MAs, in relation to Hg, within specific year classes. Future studies should focus on relating the presence or absence of MAs to changes in parameters that indicate whether or not the animal is immunologically or physiologically impaired. Additionally, studies exposing fish to methyl-Hg and testing for relationships to MAs are also needed.
Acknowledgments We thank Drs. L. Curtis and J. Heidel, Oregon State University, and four anonymous referees for critical review of the manuscript. Tamara Blett, NPS-Air Resources Division, Lakewood, CO, and the WACAP sampling team are acknowledged for technical support. We thank Patagonia, Inc. and Marmot Mountain, Ltd. for contributing cold-weather gear. This work is part of WACAP (Western Airborne Contaminants Assessment Project), a collaborative venture between the National Park Service, the U.S. Environmental Protection Agency, the U.S. Geological Survey, Oregon State University, University of Washington, and the U.SDA Forest Service. It was funded primarily through cooperative and interagency agreements with the National Park Service, and also included in-kind contributions from all of the project partners. Further information about WACAP can be found on the web site at http://www2.nature.nps.gov/air/Studies/air_toxics/ wacap.cfm. This document has been subjected to appropriate institutional peer review and/or administrative review and approved for publication. Approval does not signify that the contents reflect the views of the U.S. Government, nor does mention of trade names or commercial products constitute endorsement or recommendation. This paper is contribution WED-07-163 of the U.S. Environmental Protection Agency, National Health and Environmental Effects Research Laboratory, Western Ecology Division, Corvallis, Oregon 97333.
Supporting Information Available Tables of fish biological data, mercury concentrations from other studies, and regression statistics for all comparisons made between MAs, age, and mercury. This material is available free of charge via the Internet at http://pubs.acs.org.
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