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Long-term increased bioaccumulation of mercury in largemouth bass follows reduction of waterborne selenium
Chemosphere 41 (2000) 1101±1105
Long-term increased bioaccumulation of mercury in largemouth bass follows reduction of waterborne selenium George R. Southworth *, Mark J. Peterson, Michael G. Ryon Environmental Sciences Division, Oak Ridge National Laboratory, Bldg. 1505, MS 6036, P.O. Box 2008, Oak Ridge, Tennessee 37831-6036, USA Received 12 June 1999; accepted 13 August 1999
Abstract Average mercury concentrations in largemouth bass from Rogers Quarry in east Tennessee were found to increase steadily following the elimination of selenium-rich discharges of ¯y ash to the quarry in 1989. From 1990 to 1998, mean mercury concentrations (adjusted to compensate for the covariance between individual ®sh weight and mercury concentration) in bass rose from 0.02 to 0.61 mg/kg. There was no indication that the rate increase was slowing or that mercury concentrations in ®sh were approaching a plateau or steady state. Mean selenium concentrations in bass declined from 3 to 1 mg/kg over the ®rst ®ve years of the study, but remained at 1±1.5 mg/kg (about twice typical concentrations in bass from local reference sites) for the last three years of the study. Gross physical abnormalities were common in ®sh from the site in the ®rst three years after elimination of ¯y ash discharges but disappeared after two more years. Although it remains possible that other chemical or physical changes related to ¯y ash disposal in the system were associated with increased mercury bioaccumulation, the most likely explanation is that selenium played a critical role. It appears as though aqueous selenium enrichment was capable of having a profound eect on mercury bioaccumulation in this system but at the cost of causing a high incidence of gross abnormalities in ®sh. However, it is possible that selenium concentrations between the national ambient water quality criterion for the protection of aquatic life, 5 lg/l, and that now found in Rogers Quarry (<2 lg/l) could reduce mercury bioaccumulation without causing adverse eects on aquatic biota and ®sh-eating wildlife. Ó 2000 Elsevier Science Ltd. All rights reserved. Keywords: Mercury; Bioaccumulation; Selenium; Deformities
1. Introduction The bioaccumulation of mercury in aquatic ecosystems appears to be diminished by exposure to waterborne selenium (Rudd et al., 1980, 1983; Turner and Rudd, 1983; Turner and Swick, 1983; Bjornberg, 1987; Bjornberg et al., 1988; Paulsson and Lundbergh, 1991). In a previous study, we reported that mercury concen-
*
Corresponding author. Tel.: +1-423-574-7240; fax: +1-423574-3989. E-mail address: [email protected] (G.R. Southworth).
trations in largemouth bass (Micropterus salmoides) increased ten-fold between 1990 and 1992 following the elimination of selenium rich discharges of slurried ¯y ash to an abandoned quarry pond (Southworth et al., 1994). In 1990, mercury concentrations in bass were unusually low, and in 1992 they remained slightly lower than concentrations typical of bass from large reservoirs in east Tennessee (Southworth et al., 1994). Monitoring of mercury and selenium bioaccumulation in bass at that site has continued through 1998. The results of that monitoring are reported in this study. Our monitoring objectives were to ascertain how long mercury bioaccumulation would continue to increase and how high
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G.R. Southworth et al. / Chemosphere 41 (2000) 1101±1105
concentrations in ®sh would rise before stabilizing. A secondary objective was to observe the time course of selenium bioaccumulation following the large reduction in selenium inputs.
assumptions of normality, homogeneity of variances, and parallelism of slopes.
2. Methods
Average mercury concentrations in bass in Rogers Quarry continued to increase steadily throughout the study period with no indication of approach to a steadystate concentration (Fig. 1). By summer of 1998, mercury in largemouth bass averaged 0.73 lg/g wet weight (0.63 lg/g adjusted for covariance with weight) and ranged from 0.45 to 0.98 lg/g. Linear regression of adjusted mean mercury concentration vs. time ®t the data well r2 0:95. The average mercury concentration in bass from Rogers Quarry in 1998 was well in excess of the mean concentration (0.3 lg/g) typical of bass from reservoirs in east Tennessee (Dycus, 1989) and also exceeded the average concentration for bass (0.4 lg/g) in a nationwide survey (Bahnick et al., 1994). Average mercury concentration in Rogers Quarry bass was similar to that found in bass from nearby Lambert Quarry (Southworth et al., 1994), suggesting that high mercury concentrations typify bass populations in oligotrophic quarries. One hypothetical explanation for increasing mercury concentrations in unexploited populations of long-lived ®sh in unproductive environments involves the possible lack of Ôgrowth dilutionÕ of accumulated mercury. If the population of ®sh is so large relative to its food supply that individuals grow slowly and utilize most of their food to meet metabolic needs, mercury ingested with food would be retained in ®sh that change little in size over time. However, growth rates of bass collected in
Rogers Quarry in Anderson County, Tennessee was used from 1967 to 1989 for the disposal of ¯y ash from a coal ®red steam plant. An aqueous ¯y ash slurry was pumped to the upper reaches of a small creek (McCoy Branch) that discharged into the quarry. The quarry served as a settling basin for the ash, and discharged via McCoy Branch into Melton Hill Reservoir, 400 m downstream. Selenium in the ¯y ash slurry averaged approximately 200 lg/l (Turner et al., 1986a) and produced aqueous selenium concentrations of 20±30 lg/l in Rogers Quarry (Southworth et al., 1994). Fly ash disposal in the system was phased out in 1989, and subsequently selenium concentrations in Rogers Quarry fell to the 2±5 lg/l range in 1990 and below the analytical detection limit (<2 lg/l) from 1991 on (Southworth et al., 1994). Water chemistry in Rogers Quarry is typi®ed by moderate alkalinity (2.0± 3.0 meq/l) and pH ranging from 7 to 9 (Turner et al., 1986a). Photosynthetic activity of phytoplankton in the quarry commonly drives epilimnetic pH to relatively high levels (8.5±9.5) in summer (Turner et al., 1986b). Largemouth bass (Micropterus salmoides) were collected yearly from Rogers Quarry in summer (late June± early August), 1990±98, by angling. The ®sh were placed on ice and brought to the laboratory, where they were weighed, measured, ®lleted and skinned. A 5 g portion of the anterior dorsal section of the ®llet was removed for analysis for mercury and selenium by the Lockheed Martin Energy Systems Corporation Analytical Services Organization. Mercury was analyzed by cold vapor atomic absorption spectrophotometry after acid digestion and chemical oxidation (EPA, 1991). Following digestion in nitric acid (EPA, 1991), selenium was analyzed by inductively coupled plasma mass spectrometry (EPA, 1991). Age and growth were determined by counting and measuring scale annulli. Statistical evaluation of the data was conducted using linear regression and analysis of covariance (SAS, 1985). Mercury concentrations in ®sh from the same waterbody are generally higher in larger ®sh than in smaller specimens of the same species. This covariance was observed in the Rogers Quarry collections and required that year-to-year comparisons be made after adjusting for dierences in the size of ®sh constituting the collections made in dierent years. Loge transformation of mercury concentration and ®sh weight was used before analysis of covariance in order to better approximate
3. Results and discussion
Fig. 1. Mean ( SE) concentration of mercury in ®llets of largemouth bass from Rogers Quarry (N 8 ®sh/date). Adjusted values were obtained by analysis of covariance of lnHgfish vs. ln wgt. Curve is linear regression of Hgadjusted vs. date, r2 0:95.
G.R. Southworth et al. / Chemosphere 41 (2000) 1101±1105
1998 in Rogers Quarry were typical of bass populations in Kentucky and Missouri (Carlander, 1997), providing ample additional body mass to prevent the undiluted accumulation of mercury. A single measurement of mercury speciation in Rogers Quarry in summer 1998 indicated that total mercury levels (1.1 ng/l) in the pond were quite low, typical of uncontaminated waters in the region. However, methylmercury, the microbially-produced substance that accumulates in aquatic biota, was present at a concentration (0.15 ng/l) that would be considered high for local reference sites (Bechtel Jacobs Company, 1999). If an assumed bioaccumulation factor for methylmercury of 3 106 (Allan et al., 1996) is applied to the aqueous measure, a mercury concentration of 0.45 lg/g is predicted. Thus, the observed methylmercury concentration in Rogers Quarry was consistent with the degree of mercury bioaccumulation in ®sh in that system. The steady increase in mercury bioaccumulation in bass in Rogers Quarry was ascribed to the reduction in selenium inputs when it was ®rst reported (Southworth et al., 1994), and the more recent data have not dispelled that explanation. We originally speculated as to whether the action of selenium was within the ®sh or in the aquatic habitat. Excess selenium in water does not appear to reduce methylmercury uptake by ®sh gills, and excess internal selenium actually increased the uptake of methylmercury across gill membranes (Pedersen et al., 1998). The limited data on mercury and methylmercury concentration in water suggest that, in the absence of excess aqueous selenium, mercury is eciently methylated in Rogers Quarry water. Selenium in bass remains a factor of two or more higher than is typical of ®sh in this region. Although we cannot reconstruct past conditions in the quarry, the fact that mercury bioaccumulation has increased despite elevated selenium (2X background) in ®sh, and methylmercury in water is high for an uncontaminated system, suggest that the action of selenium was to inhibit the production of methylmercury in the quarry rather than to block the accumulation of methylmercury by ®sh. It is probable that the continued increase in mercury concentrations in ®sh represent the gradual approach to a steady-state condition in this system. We hypothesize that methylmercury is produced, bioaccumulated and eciently recycled, building up in the biotic components of the ecosystem. In a closed, deep quarry where no ®sh are taken by angling, ®sh that die may be decomposed and ingested by smaller ®sh and invertebrates before they sink to he bottom and transfer their methylmercury burden to the sediments. Thus, high mercury concentrations in terminal predators may be a natural phenomenon in such systems, unrelated to mercury inputs other than those from geologic and atmospheric sources. Selenium concentrations in bass decreased following elimination of ¯y ash discharges (Fig. 2), but the con-
1103
Fig. 2. Mean concentration of selenium in ®llets of largemouth bass from Rogers Quarry, 1990±98 (N 8 ®sh/date). Curve ®t as ®rst-order approach to a steady state, Sefish 3.3 e ÿ0:24t + 0.71; r2 83.
centrations did not decrease to levels typical of bass from other sites in the region, leveling o at about 1±1.5 mg/kg. Like mercury, selenium is eciently bioaccumulated via the food chain pathway, and the steady concentration in ®sh may represent the ecient internal cycling of organo-selenium compounds in the biota of Rogers Quarry. Alternatively, the quarry may continue to receive selenium inputs, albeit at concentrations below the detection limit of routine monitoring (2 lg/l), from ¯y ash deposits in the watershed upstream or via recycling of selenium in sediments (Bowie et al., 1996; Mattice et al., 1997). When bass were ®rst sampled from Rogers Quarry in 1990, larger ®sh in the collection were grotesquely deformed with incomplete and deformed development of bony tissues in the head, ®ns and gill covers (Ryon, 1992). In 1991, an eort was made to census the prevalence of deformities in ®sh from Rogers Quarry. In 1991 and 1992, approximately 1/3 of ®sh collected (75 ®sh in each year) had severe deformities (Ryon, 1996). The typical severity of individual deformities was less in 1992 than 1991 even though the percentages deformed were similar. By 1993 the frequency of abnormalities had decreased substantially, to only 2 of 40 ®sh having mild deformities (Ryon, 1996). After 1993, gross abnormalities were not observed in any ®sh from the quarry. A high incidence of similar abnormalities in bony tissues was observed in sun®sh (L. auritus, L. macrochirus, and L. cyanellus) in McCoy Branch downstream from the quarry in 1989 and 1990 (Ryon, 1992). The proportion of abnormalities ranged from 10% to 70% of the sun®sh species in the creek. The existence of deformities in ®sh exposed to excess aqueous selenium derived from ¯y ash has been well documented (Lemly, 1997a,b). The types of abnormalities found in
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G.R. Southworth et al. / Chemosphere 41 (2000) 1101±1105
Rogers Quarry bass were also found by Lemly. In Rogers Quarry, high rates of abnormalities were observed when selenium concentrations in ®sh muscle were in the 3±3.5 lg/g wet weight range (roughly 15±18 lg/g dry weight) and disappeared when selenium in ®sh fell to 1±1.5 lg/g (5.0±7.5 lg/g dry weight). These observations agree well with those of Lemly (1997a), who found that the incidence of deformities increased strikingly as selenium concentrations in whole ®sh increased from 5±10 lg/g dry wt (<11% deformities) to 40±65 lg/g (55% deformed). 4. Conclusions The elimination of selenium-rich discharges of slurried ¯y ash to a deep quarry pond was followed by a steady increase in mercury concentrations in largemouth bass in the quarry. Over an 8 year period, mercury increased from 0.02 to 0.73 lg/g in muscle tissue in a steady, roughly linear increase. To date, there is no evidence that the rate of increase is slowing or that mercury concentrations in bass are approaching a saturation or steady-state level. The aqueous total mercury concentration in surface water of the quarry was typical of uncontaminated aquatic systems, but aqueous methylmercury was high enough to account for the mercury concentrations in bass. Selenium concentrations in bass muscle decreased in the ®rst ®ve years following the elimination of ¯y ash discharges, but then leveled o at 1±1.5 lg/g, about twice background levels. Gross physical abnormalities were common in adult bass and sun®sh in the early years of the study, but disappeared within four years after the ¯y ash discharges stopped. Although it remains possible that other chemical or physical changes related to ¯y ash disposal in the system were associated with increased mercury bioaccumulation, the most likely explanation is that selenium played a critical role. It appears as though aqueous selenium enrichment was capable of having a profound eect on mercury bioaccumulation in this system, but at the cost of causing a high incidence of gross abnormalities in ®sh. However, it is possible that selenium concentrations between the national ambient water quality criterion for the protection of aquatic life, 5 lg/l, and that now found in Rogers Quarry (<2 lg/l) could reduce mercury bioaccumulation without causing adverse eects on aquatic biota and ®sh-eating wildlife (Lemly, 1996).
Acknowledgements This work was sponsored by the Oak Ridge Y-12 Plant, Health, Safety, and Environment Division, and
Environmental Restoration Program. The Y-12 Plant is managed by Lockheed Martin Energy Systems, Inc., under contract DE-AC05-840R21400 with the US Department of Energy. Oak Ridge National Laboratory is managed by Lockheed Martin Energy Research Corp. for the US Department of Energy under contract number DE-AC05-96OR22464. Publication number 4935, Environmental Sciences Division, ORNL.
References Allan, M.A., Levin, L., Porcella, D., Yager, J., Wyzga, R., Chang, P., Chu, R., Nott., B. Toole-O'Neil., 1996. Mercury in the Environment-A Research Update. EPRI TR-107695. Electric Power Research Institute, Palo Alto, CA. Bahnick, D., Sauer, C., Butterworth, B., Kuehl, D.W., 1994. A national study of mercury contamination of ®sh. Chemosphere 29, 537±546. Bechtel Jacobs Company LLC, 1999. Determination of sitespeci®c aqueous concentration goals for controlling mercury bioaccumulation in ®sh. In: East Fork Poplar Creek Results of Studies Undertaken by the Y-12 Biological Monitoring and Abatement Program at the Oak Ridge Y-12 Plant, Oak Ridge, Tennessee, BJC/OR-272, Bechtel Jacobs, LLC, Oak Ridge, Tennessee. Bjornberg, A., 1987. Removal of mercury in ®sh in so-called black-listed lakes in Sweden by addition of selenium. In: Lindberg, S.E., Hutchinson, T.C. (Eds.), Heavy Metals in the Environment, CEP Consultants, Edinburgh, UK. Bjornberg, A., Hakanson, L., Lundbergh, K., 1988. A theory on the mechanisms regulating the bioavailability of mercury in natural waters. Environmental Pollution 49, 53±61. Bowie, G.L., Sanders, J.G., Riedel, G.F., Gilmour, C.C., Breitburg, D.L., Cutter, G.A., Porcella, D.B, 1996. Assessing selenium cycling and accumulation in aquatic ecosystems. Water, Air and Soil Pollution 90, 93±104. Carlander, K.D., 1977. Handbook of Freshwater Fishery Biology. Iowa State University Press, Ames, Iowa, 431 pp. Dycus, D.L., 1989. Results of Fish Screening Studies in the Tennessee and Cumberland River systems in 1987. TVA/ WR/AB-89/5, Tennessee Valley Authority, Division of Water Resources, Knoxville,TN, 42 pp. Environmental Protection Agency (EPA), 1991. Methods for the Determination of Metals in Environmental Samples. EPA-600/4-91-010. Environmental Monitoring Systems Laboratory, US EPA, Cincinnati, OH. Lemly, A.D., 1996. Assessing the toxic threat of selenium to ®sh and aquatic birds. Environmental Monitoring and Assessment 43, 19±35. Lemly, A.D., 1997a. A teratogenic deformity index for evaluating impacts of selenium on ®sh populations. Ecotoxicology and Environmental Safety 37, 259±266. Lemly, A.D., 1997b. Ecosystem recovery following selenium contamination in a freshwater reservoir. Ecotoxicology and Environmental Safety 36, 275±281. Mattice, J.S., Porcella, D.B., Brocksen, R.W., 1997. Sedimentwater interactions aect assessments of metals discharges at electric utilities. Water, Air and Soil Pollution 99, 187±199.
G.R. Southworth et al. / Chemosphere 41 (2000) 1101±1105 Paulsson, K., Lundbergh, K., 1991. Treatment of mercury contaminated ®sh by selenium addition. Water, Air and Soil Pollution 56, 833±841. Pedersen, T.V., Block, M., Part, P., 1998. Eect of selenium on the uptake of methylmercury across perfused gills of rainbow trout. Aquatic Toxicology 40, 361±373. Rudd, J.W.M., Turner, M.A., Furatani, A., Swick, A.L., Townsend, B.V., 1983. The English-Wabigoon river system:I. a synthesis of recent research with a view towards mercury amelioration. Can. J. Fish Aquat. Sci. 40, 2206± 2217. Rudd, J.W.M., Turner, M.A., Townsend, B.E., Swick, A., Furutani, A., 1980. Dynamics of selenium in mercurycontaminated experimental freshwater ecosystems. Can. J. Fish. Aquat. Sci. 37, 848±857. Ryon, M.G. (Ed.), 1992. Ecological Eects of Contaminants in McCoy Branch, 1989±1990 ORNL/TM-11926, Oak Ridge National Laboratory, Oak Ridge, TN. Ryon, M.G. (Ed.), 1996. Ecological Eects of Contaminants in McCoy Branch,1991±1993 ORNL/TM-13125, Oak Ridge National Laboratory, Oak Ridge, TN.
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SAS Institute, 1985. SAS User's Guide: Statistics, Version 5 Edition. SAS Institute, Cary, NC, 1290 pp. Southworth, G.R., Peterson, M.J., Turner, R.R., 1994. Changes in concentrations of selenium and mercury in largemouth bass following elimination of ¯y ash discharge to a quarry. Chemosphere 29, 71±79. Turner, M.A., Rudd, J.W.M., 1983. The English-Wabigoon river system: III. selenium in lake enclosures: its geochemistry, bioaccumulation, and ability to reduce mercury bioaccumulation. Can. J. Fish. Aquat. Sci. 40, 2228±2240. Turner, M.A., Swick, A.L., 1983. The English-Wabigoon river system:IV. interaction between mercury and selenium accumulated from waterborne and dietary sources by northern pike. Can. J. Fish. Aquat. Sci. 40, 2241±2250. Turner, R.R., Bogle, M.A., Kane, M.A., Mercier, TM., 1986a. Characterization of Y-12 plant coal ash discharge to McCoy branch. Y/TS-177. Oak Ridge Y-12 Plant, Oak Ridge, Tennessee. Turner, R.R., Bogle, M.A., Kimmel, B.L., Soballe, D.M., 1986b. Nature of pH variations at Rogers Quarry. Y/TS179. Oak Ridge Y-12 Plant, Oak Ridge, Tennessee.
Long-term increased bioaccumulation of mercury in largemouth bass follows reduction of waterborne selenium George R. Southworth *, Mark J. Peterson, Michael G. Ryon Environmental Sciences Division, Oak Ridge National Laboratory, Bldg. 1505, MS 6036, P.O. Box 2008, Oak Ridge, Tennessee 37831-6036, USA Received 12 June 1999; accepted 13 August 1999
Abstract Average mercury concentrations in largemouth bass from Rogers Quarry in east Tennessee were found to increase steadily following the elimination of selenium-rich discharges of ¯y ash to the quarry in 1989. From 1990 to 1998, mean mercury concentrations (adjusted to compensate for the covariance between individual ®sh weight and mercury concentration) in bass rose from 0.02 to 0.61 mg/kg. There was no indication that the rate increase was slowing or that mercury concentrations in ®sh were approaching a plateau or steady state. Mean selenium concentrations in bass declined from 3 to 1 mg/kg over the ®rst ®ve years of the study, but remained at 1±1.5 mg/kg (about twice typical concentrations in bass from local reference sites) for the last three years of the study. Gross physical abnormalities were common in ®sh from the site in the ®rst three years after elimination of ¯y ash discharges but disappeared after two more years. Although it remains possible that other chemical or physical changes related to ¯y ash disposal in the system were associated with increased mercury bioaccumulation, the most likely explanation is that selenium played a critical role. It appears as though aqueous selenium enrichment was capable of having a profound eect on mercury bioaccumulation in this system but at the cost of causing a high incidence of gross abnormalities in ®sh. However, it is possible that selenium concentrations between the national ambient water quality criterion for the protection of aquatic life, 5 lg/l, and that now found in Rogers Quarry (<2 lg/l) could reduce mercury bioaccumulation without causing adverse eects on aquatic biota and ®sh-eating wildlife. Ó 2000 Elsevier Science Ltd. All rights reserved. Keywords: Mercury; Bioaccumulation; Selenium; Deformities
1. Introduction The bioaccumulation of mercury in aquatic ecosystems appears to be diminished by exposure to waterborne selenium (Rudd et al., 1980, 1983; Turner and Rudd, 1983; Turner and Swick, 1983; Bjornberg, 1987; Bjornberg et al., 1988; Paulsson and Lundbergh, 1991). In a previous study, we reported that mercury concen-
*
Corresponding author. Tel.: +1-423-574-7240; fax: +1-423574-3989. E-mail address: [email protected] (G.R. Southworth).
trations in largemouth bass (Micropterus salmoides) increased ten-fold between 1990 and 1992 following the elimination of selenium rich discharges of slurried ¯y ash to an abandoned quarry pond (Southworth et al., 1994). In 1990, mercury concentrations in bass were unusually low, and in 1992 they remained slightly lower than concentrations typical of bass from large reservoirs in east Tennessee (Southworth et al., 1994). Monitoring of mercury and selenium bioaccumulation in bass at that site has continued through 1998. The results of that monitoring are reported in this study. Our monitoring objectives were to ascertain how long mercury bioaccumulation would continue to increase and how high
0045-6535/00/$ - see front matter Ó 2000 Elsevier Science Ltd. All rights reserved. PII: S 0 0 4 5 - 6 5 3 5 ( 9 9 ) 0 0 5 6 2 - 7
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G.R. Southworth et al. / Chemosphere 41 (2000) 1101±1105
concentrations in ®sh would rise before stabilizing. A secondary objective was to observe the time course of selenium bioaccumulation following the large reduction in selenium inputs.
assumptions of normality, homogeneity of variances, and parallelism of slopes.
2. Methods
Average mercury concentrations in bass in Rogers Quarry continued to increase steadily throughout the study period with no indication of approach to a steadystate concentration (Fig. 1). By summer of 1998, mercury in largemouth bass averaged 0.73 lg/g wet weight (0.63 lg/g adjusted for covariance with weight) and ranged from 0.45 to 0.98 lg/g. Linear regression of adjusted mean mercury concentration vs. time ®t the data well r2 0:95. The average mercury concentration in bass from Rogers Quarry in 1998 was well in excess of the mean concentration (0.3 lg/g) typical of bass from reservoirs in east Tennessee (Dycus, 1989) and also exceeded the average concentration for bass (0.4 lg/g) in a nationwide survey (Bahnick et al., 1994). Average mercury concentration in Rogers Quarry bass was similar to that found in bass from nearby Lambert Quarry (Southworth et al., 1994), suggesting that high mercury concentrations typify bass populations in oligotrophic quarries. One hypothetical explanation for increasing mercury concentrations in unexploited populations of long-lived ®sh in unproductive environments involves the possible lack of Ôgrowth dilutionÕ of accumulated mercury. If the population of ®sh is so large relative to its food supply that individuals grow slowly and utilize most of their food to meet metabolic needs, mercury ingested with food would be retained in ®sh that change little in size over time. However, growth rates of bass collected in
Rogers Quarry in Anderson County, Tennessee was used from 1967 to 1989 for the disposal of ¯y ash from a coal ®red steam plant. An aqueous ¯y ash slurry was pumped to the upper reaches of a small creek (McCoy Branch) that discharged into the quarry. The quarry served as a settling basin for the ash, and discharged via McCoy Branch into Melton Hill Reservoir, 400 m downstream. Selenium in the ¯y ash slurry averaged approximately 200 lg/l (Turner et al., 1986a) and produced aqueous selenium concentrations of 20±30 lg/l in Rogers Quarry (Southworth et al., 1994). Fly ash disposal in the system was phased out in 1989, and subsequently selenium concentrations in Rogers Quarry fell to the 2±5 lg/l range in 1990 and below the analytical detection limit (<2 lg/l) from 1991 on (Southworth et al., 1994). Water chemistry in Rogers Quarry is typi®ed by moderate alkalinity (2.0± 3.0 meq/l) and pH ranging from 7 to 9 (Turner et al., 1986a). Photosynthetic activity of phytoplankton in the quarry commonly drives epilimnetic pH to relatively high levels (8.5±9.5) in summer (Turner et al., 1986b). Largemouth bass (Micropterus salmoides) were collected yearly from Rogers Quarry in summer (late June± early August), 1990±98, by angling. The ®sh were placed on ice and brought to the laboratory, where they were weighed, measured, ®lleted and skinned. A 5 g portion of the anterior dorsal section of the ®llet was removed for analysis for mercury and selenium by the Lockheed Martin Energy Systems Corporation Analytical Services Organization. Mercury was analyzed by cold vapor atomic absorption spectrophotometry after acid digestion and chemical oxidation (EPA, 1991). Following digestion in nitric acid (EPA, 1991), selenium was analyzed by inductively coupled plasma mass spectrometry (EPA, 1991). Age and growth were determined by counting and measuring scale annulli. Statistical evaluation of the data was conducted using linear regression and analysis of covariance (SAS, 1985). Mercury concentrations in ®sh from the same waterbody are generally higher in larger ®sh than in smaller specimens of the same species. This covariance was observed in the Rogers Quarry collections and required that year-to-year comparisons be made after adjusting for dierences in the size of ®sh constituting the collections made in dierent years. Loge transformation of mercury concentration and ®sh weight was used before analysis of covariance in order to better approximate
3. Results and discussion
Fig. 1. Mean ( SE) concentration of mercury in ®llets of largemouth bass from Rogers Quarry (N 8 ®sh/date). Adjusted values were obtained by analysis of covariance of lnHgfish vs. ln wgt. Curve is linear regression of Hgadjusted vs. date, r2 0:95.
G.R. Southworth et al. / Chemosphere 41 (2000) 1101±1105
1998 in Rogers Quarry were typical of bass populations in Kentucky and Missouri (Carlander, 1997), providing ample additional body mass to prevent the undiluted accumulation of mercury. A single measurement of mercury speciation in Rogers Quarry in summer 1998 indicated that total mercury levels (1.1 ng/l) in the pond were quite low, typical of uncontaminated waters in the region. However, methylmercury, the microbially-produced substance that accumulates in aquatic biota, was present at a concentration (0.15 ng/l) that would be considered high for local reference sites (Bechtel Jacobs Company, 1999). If an assumed bioaccumulation factor for methylmercury of 3 106 (Allan et al., 1996) is applied to the aqueous measure, a mercury concentration of 0.45 lg/g is predicted. Thus, the observed methylmercury concentration in Rogers Quarry was consistent with the degree of mercury bioaccumulation in ®sh in that system. The steady increase in mercury bioaccumulation in bass in Rogers Quarry was ascribed to the reduction in selenium inputs when it was ®rst reported (Southworth et al., 1994), and the more recent data have not dispelled that explanation. We originally speculated as to whether the action of selenium was within the ®sh or in the aquatic habitat. Excess selenium in water does not appear to reduce methylmercury uptake by ®sh gills, and excess internal selenium actually increased the uptake of methylmercury across gill membranes (Pedersen et al., 1998). The limited data on mercury and methylmercury concentration in water suggest that, in the absence of excess aqueous selenium, mercury is eciently methylated in Rogers Quarry water. Selenium in bass remains a factor of two or more higher than is typical of ®sh in this region. Although we cannot reconstruct past conditions in the quarry, the fact that mercury bioaccumulation has increased despite elevated selenium (2X background) in ®sh, and methylmercury in water is high for an uncontaminated system, suggest that the action of selenium was to inhibit the production of methylmercury in the quarry rather than to block the accumulation of methylmercury by ®sh. It is probable that the continued increase in mercury concentrations in ®sh represent the gradual approach to a steady-state condition in this system. We hypothesize that methylmercury is produced, bioaccumulated and eciently recycled, building up in the biotic components of the ecosystem. In a closed, deep quarry where no ®sh are taken by angling, ®sh that die may be decomposed and ingested by smaller ®sh and invertebrates before they sink to he bottom and transfer their methylmercury burden to the sediments. Thus, high mercury concentrations in terminal predators may be a natural phenomenon in such systems, unrelated to mercury inputs other than those from geologic and atmospheric sources. Selenium concentrations in bass decreased following elimination of ¯y ash discharges (Fig. 2), but the con-
1103
Fig. 2. Mean concentration of selenium in ®llets of largemouth bass from Rogers Quarry, 1990±98 (N 8 ®sh/date). Curve ®t as ®rst-order approach to a steady state, Sefish 3.3 e ÿ0:24t + 0.71; r2 83.
centrations did not decrease to levels typical of bass from other sites in the region, leveling o at about 1±1.5 mg/kg. Like mercury, selenium is eciently bioaccumulated via the food chain pathway, and the steady concentration in ®sh may represent the ecient internal cycling of organo-selenium compounds in the biota of Rogers Quarry. Alternatively, the quarry may continue to receive selenium inputs, albeit at concentrations below the detection limit of routine monitoring (2 lg/l), from ¯y ash deposits in the watershed upstream or via recycling of selenium in sediments (Bowie et al., 1996; Mattice et al., 1997). When bass were ®rst sampled from Rogers Quarry in 1990, larger ®sh in the collection were grotesquely deformed with incomplete and deformed development of bony tissues in the head, ®ns and gill covers (Ryon, 1992). In 1991, an eort was made to census the prevalence of deformities in ®sh from Rogers Quarry. In 1991 and 1992, approximately 1/3 of ®sh collected (75 ®sh in each year) had severe deformities (Ryon, 1996). The typical severity of individual deformities was less in 1992 than 1991 even though the percentages deformed were similar. By 1993 the frequency of abnormalities had decreased substantially, to only 2 of 40 ®sh having mild deformities (Ryon, 1996). After 1993, gross abnormalities were not observed in any ®sh from the quarry. A high incidence of similar abnormalities in bony tissues was observed in sun®sh (L. auritus, L. macrochirus, and L. cyanellus) in McCoy Branch downstream from the quarry in 1989 and 1990 (Ryon, 1992). The proportion of abnormalities ranged from 10% to 70% of the sun®sh species in the creek. The existence of deformities in ®sh exposed to excess aqueous selenium derived from ¯y ash has been well documented (Lemly, 1997a,b). The types of abnormalities found in
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Rogers Quarry bass were also found by Lemly. In Rogers Quarry, high rates of abnormalities were observed when selenium concentrations in ®sh muscle were in the 3±3.5 lg/g wet weight range (roughly 15±18 lg/g dry weight) and disappeared when selenium in ®sh fell to 1±1.5 lg/g (5.0±7.5 lg/g dry weight). These observations agree well with those of Lemly (1997a), who found that the incidence of deformities increased strikingly as selenium concentrations in whole ®sh increased from 5±10 lg/g dry wt (<11% deformities) to 40±65 lg/g (55% deformed). 4. Conclusions The elimination of selenium-rich discharges of slurried ¯y ash to a deep quarry pond was followed by a steady increase in mercury concentrations in largemouth bass in the quarry. Over an 8 year period, mercury increased from 0.02 to 0.73 lg/g in muscle tissue in a steady, roughly linear increase. To date, there is no evidence that the rate of increase is slowing or that mercury concentrations in bass are approaching a saturation or steady-state level. The aqueous total mercury concentration in surface water of the quarry was typical of uncontaminated aquatic systems, but aqueous methylmercury was high enough to account for the mercury concentrations in bass. Selenium concentrations in bass muscle decreased in the ®rst ®ve years following the elimination of ¯y ash discharges, but then leveled o at 1±1.5 lg/g, about twice background levels. Gross physical abnormalities were common in adult bass and sun®sh in the early years of the study, but disappeared within four years after the ¯y ash discharges stopped. Although it remains possible that other chemical or physical changes related to ¯y ash disposal in the system were associated with increased mercury bioaccumulation, the most likely explanation is that selenium played a critical role. It appears as though aqueous selenium enrichment was capable of having a profound eect on mercury bioaccumulation in this system, but at the cost of causing a high incidence of gross abnormalities in ®sh. However, it is possible that selenium concentrations between the national ambient water quality criterion for the protection of aquatic life, 5 lg/l, and that now found in Rogers Quarry (<2 lg/l) could reduce mercury bioaccumulation without causing adverse eects on aquatic biota and ®sh-eating wildlife (Lemly, 1996).
Acknowledgements This work was sponsored by the Oak Ridge Y-12 Plant, Health, Safety, and Environment Division, and
Environmental Restoration Program. The Y-12 Plant is managed by Lockheed Martin Energy Systems, Inc., under contract DE-AC05-840R21400 with the US Department of Energy. Oak Ridge National Laboratory is managed by Lockheed Martin Energy Research Corp. for the US Department of Energy under contract number DE-AC05-96OR22464. Publication number 4935, Environmental Sciences Division, ORNL.
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