Bioaccumulation and Biomagnification of Mercury in Two Warmwater Fish Communities

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1 Journal of Freshwater Ecology ISSN: (Print) (Online) Journal homepage: Bioaccumulation and Biomagnification of Mercury in Two Warmwater Fish Communities Robert M. Neumann & Scott M. Ward To cite this article: Robert M. Neumann & Scott M. Ward (1999) Bioaccumulation and Biomagnification of Mercury in Two Warmwater Fish Communities, Journal of Freshwater Ecology, 14:4, , DOI: / To link to this article: Published online: 06 Jan Submit your article to this journal Article views: 168 Citing articles: 14 View citing articles Full Terms & Conditions of access and use can be found at

2 Bioaccumulation and Biomagnification of Mercury in Two Warmwater Fish Communities Robert M. Neumann and Scott M. Ward Department of Natural Resources Management and Engineering 1376 Storrs Road, Box U-87 University of Connecticut Storrs, Connecticut USA ABSTRACT Total mercury concentrations were determined in two Connecticut lakes for six fish species representing a range of trophic levels -- largemouth bass (Micropterus salmoides), chain pickerel (Esox niger), black crappie (Pornoxis nigromaculatus), bluegill (Lepomis macrochirus), smallmouth bass (M. dolomieu), and yellow perch (Perca flavescens). Total mercury concentrations in all fishes increased with length and age. Slopes of log,o mercury concentration-age regressions, which were used to compare bioaccumulation rates, were different among species in both lakes. In both lakes, no difference in bioaccumulation rate was found between top-level predators. Top-level predators and intermediate trophic level species (black crappie and yellow perch) accumulated mercury at a faster rate than bluegills. Intermediate trophic level species had bioaccumulation rates comparable to top-level predators over the range of ages sampled. Differences in mercury concentrations between a toplevel predator (largemouth bass) and intermediate trophic level species decreased with age, while differences between largemouth bass and bluegill increased with age. INTRODUCTION Several studies have shown that mercury bioaccumulates in fish tissue and that concentrations typically increase with increasing size and age (Phillips et al. 1980, Lange et al. 1993, Driscoll et al. 1994, Stafford and Haines 1997). Approximately 95-99% of mercury in fish tissue is methylmercury (Grieb et al. 1990, Bloom 1992). which is obtained predominantly from the diet, rather than through waterborne sources (Phillips and Buhler 1978). The rate of bioaccumulation in fishes may change with age due to ontogenetic changes in the diet (Mathers and Johansen 1985). Mercury concentrations in some fish species were shown to increase sharply at sizes when fish shifted from a diet of invertebrates to fish (MacCrimrnon et al. 1983, Driscoll et al. 1994), and Wren and MacCrirnmon (1986) observed that piscivorous fish species had higher concentrations of mercury than prey fish species of comparable age. While biomagnification of mercury in aquatic food chains has been documented, little information exists on quantifying the differences in mercury concentrations among fish species inhabiting different trophic positions. Moreover, differences in mercury concentrations among species are not likely to remain constant across ages due to changes in diet as fish grow. Thus, the objectives of this study were to: 1) determine and compare rates of mercury Journal of Freshwater Ecology, Volume 14, Number 4 - December 1999

3 bioaccumulation among fish species in two warmwater fish communities; and 2) quantify differences in concentrations of mercury among fish species representing different trophic levels. METHODS AND MATERIALS During the summer of 1996, 24 or 25 individuals of six fish species representing a range of trophic levels were collected from two Connecticut lakes. Largemouth bass (Micropterus salmoides), chain pickerel (Esox niger), black crappie (Pomoxis nigromaculatus), and bluegill (Lepomis rnacrochirus) were collected from Pickerel Lake; largemouth bass, smallmouth bass (M. dolomieu), yellow perch (Percaflavescens), and bluegill were collected from Lake Lillinonah. Largemouth bass, chain pickerel and smallmouth bass were considered to represent top-level predators. Black crappie and yellow were considered to be intermediate trophic level species between the top-level predators and bluegill (planktivore/insectivore). Pickerel Lake is an impoundment with a surface area of 35.9 ha, a maximum depth of 3.0 m, and a mean depth of 1.8 m. Lake Lillinonah is an impoundment with a surface area of 769 ha, a maximum depth of 30.5 m, and a mean depth of 7.6 m (Healy and Kulp 1995). Fish were collected by nighttime electrofishing using a 5.0-m boat equipped with a VVP-15 control unit (Coffelt Electronics) and a 5,000-W gasoline generator. Fish were netted and immediately placed in a clean, covered polyethylene tank filled with ambient lake water. To avoid contamination of fish by outboard motor exhaust plumes, the motor was shut off before processing fish and the person operating the motor did not assist in fish processing. After the sample was collected, fish were measured to the nearest mm (total length) on a clean plastic-wrapped measuring board, rinsed in ambient lake water, doublesealed in clean polyethylene bags, and stored on dry ice in clean cooiers for transport to the laboratory for mercury analysis. Detailed fish collection and sample preparation protocol can be found in Neumann et al. (1996). The total time from fish capture to mercury analysis was no longer than 28 d, and the analyses followed standard procedures (USEPA 1993). Fish were dissected in a positive pressure laminar flow hood on acid-washed surfaces. Stainless-steel instruments were thoroughly cleaned with laboratory-grade detergent and acid-washed before and after dissecting each fish specimen. Scales were removed from each fish near the tip of the pectoral fin for age determination; scales were imprinted on acetate slides and age was determined from projections of scale images on a 48X microfiche reader. Fish were rinsed with deionized water and placed on their left side. Three incisions were made to peel the skin anteriorly to expose the muscle and a boneless fillet of axial muscle was removed. Whole fillets were homogenized in a stainless-steel grinder. Fish tissue was digested by placing a 1.O- to 1.5-g sample of homogenate in a biological oxygen demand bottle with 8 ml of sulfuric acid and 2 ml of nitric acid and heating it on a hot plate (USEPA 1992). The tissue was then analyzed for total mercury (pglg wet weight) with atomic absorption spectrophotometry (USEPA

4 1992) using a Perkin Elmer flow injection mercury system with the AS90 autosampler. A four-point calibration curve was run at the beginning of each analysis. The calibration curve was verified with a certified external quality control sample from Ricca Chemical Company (Arlington, Texas). The initial calibration check demonstrated that the instrument was capable of acceptable performance at the beginning of the analysis. In order to ensure continuing acceptable performance, a calibration verification and procedural calibration blank were run at least every tenth sample. For every twenty samples, a procedural spiked-fish sample, a duplicate fish sample, a control spike, and a preparation blank were analyzed. Precision of analysis (relative percent difference) was calculated from duplicate analyses of fish (mean = 5.8%; SD = 7.6; N = 14). Accuracy (percent recovery) was determined from spiked fish samples (mean = 106.5%; SD = 9.9; N = 13). Data analyses were conducted with the Statistical Analysis System (SAS Institute 1990). Log,, transformation of mercury concentration values was used to improve normality of data. Relationships between log,$nercury concentration and length and age were tested using regression. The slope of log,,,mercury concentration-age regression was used as an indicator of mercury bioaccumulation rate for each species. Differences in slopes among species within each lake were tested by examining interaction of log,$nercury concentration-age regressions using an extension of analysis of covariance (GLM procedure, SAS Institute 1990). Where significant interaction of regressions occurred, differences in slopes among species were tested through contrasts (GLM procedure, SAS Institute 1990). Biomagnifications of mercury among species in each lake were examined by predicting mercury concentrations at various ages using log,dnercury concentration-age regressions, and concentrations of mercury at age were compared among species. RESULTS AND DISCUSSION Bioaccumulation Total mercury concentrations in axial muscle tissue significantly (P9.05) increased with length and age for all species from Pickerel Lake and Lake Lillinonah (Figures 1 and 2). Mercury concentrations exceeded the U. S. Food and Drug Administration (FDA) guideline of 0.5 pglg in all species except chain pickerel and bluegill from Pickerel Lake. Only largemouth bass from both lakes and smallrnouth bass from Lake Lillinonah exceeded mercury concentrations of 1.0 pglg. According to loglomercury concentration-age regressions, the mean lengths (rnm) of fishes that began to exceed the FDA guideline (0.5 yglg) in Pickerel Lake were 364, 578, and 330 for largemouth bass, chain pickerel, and black crappie, respectively. In Lake Lillinonah, these mean lengths were 319, 258, and 244 for largemouth bass, smallmouth bass, and yellow perch, respectively. Concentrations of mercury in black crappie and yellow perch reached the FDA guideline of 0.5 pglg at shorter mean lengths than they did in the top-level predators (largemouth bass, smallmouth bass, and chain pickerel) in both lakes.

5 3.0 Pickerel Lake Lake Lillinonah Largemouth bass o.l! Largemouth bass - - Chain pickerel I I I I I -. r - Black crappie I I I I I , 'fl :. & Bluegill Bluegill I I I I I 0.0 I I I I I Length (mm) Figure 1. Relationships between total mercury concentrations (pglg wet weight) and total length (mrn) for fishes collected from Pickerel Lake and Lake Lillinonah, Connecticut. Horizontal line indicates the U. S. Food and Drug Administration action level of 0.5 pglg wet weight.

6 Pickerel Lake Lake Lillinonah i 0.0 Largemouth bass 1 :argemouth bass c o Chain pickerel.eo.oi I 1, I 1 1 I I lu z 3.0 t: 8 1.0: c 0 W = lu - r" z Black crappie 0.0 I I I I I I I I : 0.1?. a. t. - "..: o 0.1 -, o- 0.1 Smallmouth bass. Yellow perch I I I I I I I I. 0.0 Bluegill I I I I I I I I Bluegill I I I I I I I I Age (years) Figure 2. Relationships between total mercury concentrations (pglg wet weight) and age (years) for fishes coliected from Pickerel Lake and Lake LiIlinonah, Connecticut. Horizontal line indicates the U. S. Food and Drug Administration action level of 0.5 pglg wet weight.

7 However, black crappie and yellow perch were one to two years older than toplevel predators at lengths where mercury concentrations began to exceed 0.5 pglg. These results demonstrate that mercury concentrations in large black crappie and yellow perch can surpass those of top-level predators of similar lengths. Because of wide differences in ages between species at the same lengths, comparison of bioaccumulation among species should be based on differences in rates of mercury accumulation with age (Wren and MacCrirnmon 1986). Slopes of log,, mercury concentration-age regressions were significantly different among species in both lakes (Pickerel Lake, P=0.003; Lake Lillinonah, P=0.047). In Pickerel Lake, no significant difference in slopes was found between largemouth bass and chain pickerel, suggesting that bioaccumulation rates were similar between these species (Table 1). Bluegill had significantly lower slopes than largemouth bass and black crappie, but not chain pickerel. Black crappie had a significantly greater slope than all other species in Pickerel Lake. In Lake Lillinonah, no differences in slopes were found among largemouth bass, smallrnouth bass, and yellow perch, but all three species had greater slopes than bluegill (P<0.10). As expected, bioaccumulation in bluegills was slower relative to other species and was most likely related to low mercury concentrations of their prey. Probable bluegill foods, such as zooplankton and macroinvertebrates, were shown to have lower mercury concentrations than prey fishes (Meili 1991). Phillips et al. (1980) found that in a Montana reservoir, northern pike (E. lucius) and sauger (Stizostedion canadense) accumulated mercury nearly twice as fast as did white crappie (P. annularis) and black crappie, which fed almost exclusively on zooplankton. Our results suggested that black crappie and yellow perch had bioaccumulation rates comparable to top-level predators over the range of ages sampled. However, mercury concentrations in black crappie and yellow perch were not necessarily greater than top-level predators of comparable age. For example, at early ages (two and three years), mercury concentrations in largemouth bass were over three times those of black crappie, but by age 5, mercury concentrations in largemouth bass were approximately two times those of black crappie (Table 2). Thus, differences in mercury concentrations between intermediate consumers and top-level predators declined at older ages. Although foods eaten by fishes in this study were not determined, we suspect that at early ages, mercury concentrations of intermediate trophic level species may be lower than those of top-level predators because of differences in diet of young fish. Black crappie and yellow perch may be relying on invertebrates longer than top-level predators, thus limiting their mercury concentrations for a longer time period compared to top-level predators. The fraction of total mercury that exists as methylmercury in aquatic organisms increases progressively from primary producers to fish. If black crappie and yellow perch shift from a diet of invertebrates to predominantly fish, their mercury concentrations may increase sharply, thus causing comparable or greater bioaccumulation rates relative to top-level predators that might be entirely piscivorous over the range of ages sampled. Driscoll et al. (1994) found that mercury concentrations in yellow perch increased sharply after age 5 in

8 Adirondack lakes, which was attributed to the size at which yellow perch became predominantly piscivorous at a length of approximately 200 rnm. In Lake Lillinonah, yellow perch attained a mean length of 200 mm at approximately age 4; in Pickerel Lake, black crappie attained a mean length of 200 mm at age 4 (Jacobs and O'Do~ell 1996). In Pickerel Lake and Lake Lillinonah, fish composed a substantial part of the diet of largemouth bass less than 200 rnm (Ward and Neumann 1998). Table 1. Comparison of log,,,mercury concentration (uglg wet weight)-age regression slopes among species within Pickerel Lake and Lake Lillinonah, Connecticut. Listed are probability (P) values associated with testing whether there was significant interaction among regression lines (i.e., homogeneity of regressions) based on contrasts. Pickerel Lake Species Largemouth bass Chain pickerel Black crappie Chain pickerel Black crappie Bluegill Lake Lillinonah Species Largemouth bass Smallmouth bass Yellow perch Smallmouth bass Yellow perch Bluegill Biornaanification There is a general lack of information regarding quantification of mercury biomagnification among fish species within lake systems. Piscivorous fishes usually have higher mercury concentrations than lower trophic level species from the same water body (Phillips et al. 1980, Wren et al. 1983). Biomagnification of mercury has been documented by comparing mean mercury concentrations among groups of organisms inhabiting different trophic levels (Wren et al. 1983). Because of the oversimplification of comparing mean mercury concentrations of groups of organisms. Wren and MacCrimmon (1986) refined their analysis by demonstrating that tissue mercury concentrations in predatory fish were higher than prey fishes of comparable age. However, quantification of biomagnification among fish species can become complex, especially for fishes that demonstrate ontogenetic shifts in diet (trophic position). For example, the rate of mercury accumulation in lake trout (Salvefinus namqcrrsh) increases sharply when they become large enough to shift from a diet of invertebrates to fish (MacCrimmon et al. 1983).

9 Table 2. Total mercury concentrations (pglg wet weight) at ages 2-5 for fish species'sampled from Pickerel Lake and Lake Lillinonah, Connecticut. Listed in parentheses are biomagnification levels between largemouth bass and each species at that age (i.e., Hg concentration in largemouth bass divided by Hg concentration of other species). Species Pickerel Lake Largemouth bass Chain pickerel 0.24(1.1) 0.30(1.0) 0.36(1.1) 0.44(1.1) Black crappie 0.07(3.7) O.lO(3.1) 0.14(2.7) 0.21(2.2) Bluegill O.ll(2.4) 0.12(2.6) 0.13(2.9) 0.14(3.4) Lake Lillinonah Largemouth bass Smallmouth bass 0.39 (0.8) 0.51 (0.9) 0.68 (0.9) 0.91 (1.0) Yellow perch 0.23 (1.4) 0.34 (1.4) 0.50 (1.3) 0.74 (1.2) Bluegill 0.17(1.9) 0.20(2.3) 0.24(2.7) 0.28(3.2) We observed that the concentrations of mercury in top-level predators from the same lake were similar across ages, as would be expected for species inhabiting the same trophic level (Table 2). In both lakes, the difference in mercury concentrations between largemouth bass and bluegill became progressively greater between ages 2 and 5. In Pickerel Lake, concentrations of mercury in largemouth bass were 2.4 and 3.4 times those in bluegill at ages 2 and 5, respectively. Similar results were observed in Lake Lillinonah where concentrations of mercury in largemouth bass were 1.9 and 3.2 times those in bluegill at ages 2 and 5, respectively. The increase in magnitude of biomagnification reflected the slow rate of mercury bioaccumulation in bluegill compared to largemouth bass. Our findings were consistent with those of Wren and MacCrimmon (1986) who found that the mean concentration of mercury in largemouth bass was 3.4 times that in pumpkinseed (L. gibbosus) at a comparable age of approximately 4.5 years. Differences in mercury concentrations between largemouth bass and intermediate trophic level species (black crappie and yellow perch) became progressively smaller between ages 2 and 5; this observation was most pronounced for largemouth bass and black crappie in Pickerel Lake (Table 2). In Pickerel Lake, concentrations of mercury in largemouth bass were 3.7 and 2.2 times those in black crappie at ages 2 and 5, respectively. In Lake Lillinonah, concentrations of mercury in largemouth bass were 1.4 and 1.2 times those in yellow perch at ages 2 and 5, respectively. Again, our findings were consistent with those of Wren and MacCrirnmon (1986) who found that the mean

10 concentration of mercury in largemouth bass was 1.4 times that in yellow perch at a comparable age of approximately 4.5 years. The large decrease in the magnitude of differences between largemouth bass and black crappie at increasing ages may reflect a shift in the diet of black crappie from invertebrates to fish. Concentrations of mercury in black crappie were similar to those of bluegill up to age 4, after which concentrations in black crappie increased sharply. Thus, black crappie and bluegill may have been consuming similar diet items up to age 4, after which fish may have become a more dominant diet item for black crappie. Differences in concentrations of mercury among fish species representing different trophic positions was not constant, probably reflecting species-specific changes in diet across age. However, concentrations of mercury were similar among top-level predators across age. Differences in concentrations of mercury increased with increasing age between top-level predators and low trophic level species (bluegill), reflecting the slow rate of bioaccumulation compared to toplevel predators. Differences in mercury concentrations between top-level predators and intermediate trophic level species decreased with increasing age, probably reflecting a shift in diet of intermediate trophic level species from invertebrates to fish. Species-specific ontogenetic changes in trophic position, prey type and availability, and consumption rates should be considered when assessing differences in mercury concentrations among fishes in an individual water body. ACKNOWLEDGEMENTS Funding for this research was provided by the Connecticut Department of Environmental Protection and the Environmental Research Institute at the University of Connecticut. We thank R. Hanten, C. Perkins, and D. Thompson for assistance in the field and laboratory. T. Strakosh, M. Anderson, and S. Jordan reviewed this manuscript. This manuscript represents scientific contribution number 1905 of the Storrs Agricultural Experiment Station. LITERATURE CITED Bloom, N. S On the chemical form of mercury in edible fish and marine invertebrate tissue. Canadian Journal of Fisheries and Aquatic Sciences 49: Driscoll, C. T., C. Yan, C. L. Schofield, R. Munson, and J. Holsapple The mercury cycle and fish in the Adirondack lakes. Environmental Science Technology 28: Grieb, T. M., C. T. Driscoll, S. P., Gloss, C. L. Schofield, G. L. Bowie, and D. B. Porcella Factors affecting mercury accumulation in fish in the upper Michigan Peninsula. Environmental Toxicology and Chemistry 9: Heally, D. F. and K. P. Kulp Water-quality characteristics of selected public recreational lakes and ponds in Connecticut. U. S. Geological

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12 Wren, C. D. and H. R. MacCrimmon Comparative bioaccumulation of mercury in two adjacent freshwater ecosystems. Water Research 20: Wren, C. D., H. R. MacCrirnmon, and B. R. Loescher Examination of bioaccurnulation and biomagnification of metals in a Precambrian Shleld lake. Water, Air, and Soil Pollution 19: Received: 9 May 1999 Accepted: 3 October 1999