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 concentrations 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

Chemosphere 41 (2000) 1101±1105

* Corresponding author. Tel.: +1-423-574-7240; fax: +1-423-

574-3989.

E-mail address: sgr@urnl.gov (G.R. Southworth).

0045-6535/00/$ - see front matter Ó 2000 Elsevier Science Ltd. All rights reserved.

PII: S 0 045-6535(99)00562-7
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.

2. Methods

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

assumptions of normality, homogeneity of variances,

and parallelism of slopes.

3. Results and discussion

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

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

lnHg

fish vs. lnwgt. Curve is linear regression of Hgadjusted

vs. date, r2  0:95.

1102 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 concentrations 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

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, Se

fish  3.3

eÿ0:24t + 0.71; r2  83.

G.R. Southworth et al. / Chemosphere 41 (2000) 1101±1105 1103
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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