Environ. Sci. Technol. 1998, 32, 886-891
Estimate of Net Trophic Transfer Efficiency of PCBs to Lake Michigan Lake Trout from Their Prey CHARLES P. MADENJIAN,* ROBERT J. HESSELBERG, TIMOTHY J. DESORCIE, LARRY J. SCHMIDT, RALPH M. STEDMAN, RICHARD T. QUINTAL, LINDA J. BEGNOCHE, AND DORA R. PASSINO-READER U.S. Geological Survey, Biological Resources Division, Great Lakes Science Center, 1451 Green Road, Ann Arbor, Michigan 48105
Most of the polychlorinated biphenyl (PCB) body burden accumulated by lake trout (Salvelinus namaycush) from the Laurentian Great Lakes is from their food. We used diet information, PCB determinations in both lake trout and their prey, and bioenergetics modeling to estimate the efficiency with which Lake Michigan lake trout retain PCBs from their food. Our estimates were the most reliable estimates to date because (a) the lake trout and prey fish sampled during our study were all from the same vicinity of the lake, (b) detailed measurements were made on the PCB concentrations of both lake trout and prey fish over wide ranges in fish size, and (c) lake trout diet was analyzed in detail over a wide range of lake trout size. Our estimates of net trophic transfer efficiency of PCBs to lake trout from their prey ranged from 0.73 to 0.89 for lake trout between the ages of 5 and 10 years old. There was no evidence of an upward or downward trend in our estimates of net trophic transfer efficiency for lake trout between the ages of 5 and 10 years old, and therefore this efficiency appeared to be constant over the duration of the lake trout’s adult life in the lake. On the basis of our estimates, lake trout retained 80% of the PCBs that are contained within their food.
Introduction Polychlorinated biphenyls (PCBs) may pose a health threat to people consuming fish contaminated with these chemicals (1) and have been suspected of interfering with reproduction in some fish (2) and wildlife populations (3). Computer models to predict changes in PCB accumulation rates in fish associated with changes in the food web structure are useful in assessing risk to wildlife and humans consuming the contaminated fish. The efficiency at which fish assimilate PCBs from their food has been identified as one of the most important factors regulating PCB accumulation rates in fish (4, 5). Therefore, an accurate estimate of PCB assimilation efficiency from food by fish is critical in predicting future risk to wildlife and humans eating the contaminated fish. Jackson and Schindler (6) estimated the net trophic transfer efficiency, γ, of PCBs to Lake Michigan lake trout * Corresponding author telephone: (734) 994-3331, ext. 259; fax: (734) 994-8780; e-mail address: chuck
[email protected]. 886 9 ENVIRONMENTAL SCIENCE & TECHNOLOGY / VOL. 32, NO. 7, 1998
(Salvelinus namaycush) from their prey by using
γ)
[PCBLT]R [PCBPREY]
(1)
where [PCBLT] is the PCB concentration of lake trout (mg/ kg), [PCBPREY] is the PCB concentration of lake trout food (mg/kg), and R is the gross growth efficiency of lake trout. Gross growth efficiency (gge) was equal to the weight gained by the lake trout divided by the amount of food eaten. Jackson and Schindler (6) estimated γ ) 0.55 for Lake Michigan lake trout, using lake trout diet information presented by Stewart et al. (7) and Stewart and Ibarra (8) and using PCB determinations of lake trout and prey fish from Wisconsin waters of Lake Michigan from 1975 through 1990. In contrast, on the basis of diet schedules for lake trout and PCB determinations of lake trout and prey fish from Wisconsin waters of the lake (4, 5), γ can be calculated to be approximately 0.80. The PCB determinations of lake trout were from fish caught during 1985 (4). One weakness in the data used by Jackson and Schindler (6) was that the diet information was not geographically matched with the PCB data. The diet schedules presented by Stewart et al. (7) and Stewart and Ibarra (8) represented an averaging of diet composition between lake trout caught near Saugatuck, MI, along the southeastern shore of the lake, and lake trout caught near Port Washington, WI, along the lake’s western shore (9). The PCB data used by Jackson and Schindler (6) were from fish caught chiefly in Wisconsin waters of the lake. The diets of lake trout less than 6 years old differed substantially between the two locations (9); and the most appropriate diet data for the calculation in eq 1 would have been the Wisconsin diet information rather than an averaging of diet between Michigan and Wisconsin waters. In the computer simulation model by Madenjian et al. (4, 5), lake trout were exposed to a Wisconsin diet, and the model predictions agreed with PCB data for lake trout from Wisconsin waters. To resolve the issue of which estimate of net trophic transfer efficiency (γ) was more accurate, a new set of detailed diet and PCB data from one region of the lake would be instructive. Such a detailed data set has become available as a result of the Lake Michigan Mass Balance (LMMB) project, sponsored by the Great Lakes National Program Office of the U.S. Environmental Protection Agency. The intent of the LMMB project was to develop a model for flow of contaminants, such as PCBs, through the Lake Michigan ecosystem. The diet of lake trout over a wide range of sizes was investigated in the nearshore waters of Sturgeon Bay, WI, during 1994 and 1995. From the same location and during the same sampling dates, PCB determinations were made on lake trout and prey fish of various sizes. Our estimate would be the most reliable estimate of net trophic transfer efficiency to date because (a) the diet and PCB observations were made simultaneously at the same location during 19941995 over wide ranges in sizes of both prey fish and lake trout; (b) the lake trout diet observations were very detailed, including the mean size of prey fish in the lake trout stomachs over a wide range in lake trout size, during 1994-1995; (c) general patterns in lake trout diet in the vicinity of Sturgeon Bay have been tracked since 1982 (10); and (d) PCB concentrations of prey fish in the Wisconsin waters of Lake Michigan, albeit limited data, have been measured by the Wisconsin Department of Natural Resources since 1976 (4). Thus, our available data set to estimate γ using eq 1 would be the most complete data set to date for such a calculation. S0013-936X(97)00832-8 Not subject to U.S. copyright. Publ. 1998 Am. Chem.Soc. Published on Web 02/14/1998
The objective of the present study was to calculate the net trophic transfer efficiency to lake trout from their prey, using the LMMB project data set, and then to compare our estimate with previous estimates of this efficiency.
Methods Field Sampling. We caught lake trout and prey fish in Lake Michigan in the nearshore vicinity of Sturgeon Bay, WI, during spring (April-May), summer (July), and fall (SeptemberOctober) 1994 and during spring and fall 1995. All sampling was restricted to within 7 km of shore. Most of the lake trout that were examined in this study were captured in gill nets, although bottom trawling yielded a small (less than 15%) proportion of the total catch. We set gill nets at depths ranging from 9 to 40 m. To supplement the catch of lake trout 0.05); therefore, we pooled all lake trout from both years to represent the PCB concentration of lake trout from Sturgeon Bay in 1994. On the basis of similar reasoning, the PCB data for prey fish were pooled for both years 1994 and 1995 to represent the PCB concentration of prey fish from the Sturgeon Bay vicinity in 1994. Madenjian et al. (10), using the lake trout bioenergetics model developed by Stewart et al. (7), calculated the gge for lake trout caught in the vicinity of Sturgeon Bay during the 1994-1995 time period. We used these estimates of gge in our calculations of γ. The PCB concentration of lake trout was estimated for each of the ages 2-10 using the regression model presented in Table 1. We converted the average weight of lake trout at ages 2-10, as presented by Madenjian et al. (10), into lengths at age based on the length-weight regression for Lake Michigan lake trout developed by Madenjian et al. (4). These lengths were then substituted into our regression model to yield PCB concentrations. To estimate the PCB concentration of prey, the PCB concentrations of the various prey categories had to be weighted by their percent contribution, on a wet weight basis, to the lake trout diet. The results of the bioenergetics modeling performed by Madenjian et al. (10) were used to estimate the amounts of the various prey categories consumed by lake trout. See Hewett and Johnson (18) and Madenjian et al. (10) for more details on this procedure. The prey categories included small alewife, large alewife, rainbow smelt, sculpins (both slimy sculpin and deepwater sculpin), bloater, and invertebrates (mainly Mysis and Diporeia). In many cases, sculpins in the stomachs of the lake trout could not be further identified as to whether they were slimy sculpin or deepwater sculpin. To simplify the estimation of PCB concentrations of sculpins in the diet of lake trout, we averaged the regression equation of PCB concentration as a function of length for deepwater sculpin with that for slimy sculpin. We used this average equation to estimate PCB concentrations of sculpin prey in lake trout diet. VOL. 32, NO. 7, 1998 / ENVIRONMENTAL SCIENCE & TECHNOLOGY
9
887
TABLE 1. Fitted Regression Equations for PCB Concentration (Y, in mg/kg) as a Function of Mean Total Length (X, in mm) for Lake Trout and Prey Fish Found in the Vicinity of Sturgeon Bay, WI, 1994-1995a species
regression equation
R2
N
range in mean total length (mm)
alewife bloater deepwater sculpin lake trout rainbow smelt slimy sculpin
Y ) 0.00436X - 0.159 Y ) 0.00264X + 0.208 Y ) 0.00254X + 0.043 Y ) 0.103e0.0048X Y ) 0.00406X - 0.203 Y ) 0.00835X - 0.125
0.648 0.190 0.432 0.940 0.268 0.350
40 44 23 70 24 25
68-185 126-235 82-139 205-889 113-153 45-74
a PCB concentrations of lake trout were based on whole-fish composites, without stomach linings, of one to five fish. PCB concentrations of prey fish were based on whole-fish composites of five fish. PCB concentration of the composite was matched with the mean length of the fish comprising the composite. N is the number of composites used to calculate the regression equation.
Next, PCB concentrations in lake trout prey were estimated for each season and year of the lake trout’s life in the lake. For an example, consider a 10-year-old lake trout caught near Sturgeon Bay in 1994. This lake trout was planted in the lake as a yearling in 1985. Therefore, to estimate the PCB concentration in the food of this lake trout during its time spent in the lake, we had to estimate the PCB concentrations in its food as a yearling from spring 1985 to spring 1986, the PCB concentrations in its food as a 2-year-old from spring of 1986 to spring 1987, and so on. We determined the modal length for each category of the prey fish found in the stomachs of the lake trout for a particular combination of season and age of lake trout, based on our diet data at Sturgeon Bay from 1994 through 1995 (10). We then substituted this modal length into the appropriate equation from Table 1 to yield an estimate of the PCB concentration for each combination of prey fish category and prey fish modal length. We used the same equation from Table 1 for both small and large alewife. These regression equations were based on data from 1994 to 1995. Because the PCB concentrations in most prey fish populations from the Wisconsin side of Lake Michigan have declined from 1985 to 1994, we had to adjust the PCB concentrations calculated from the regression equations in Table 1 for the appropriate year of the lake trout’s life in the lake. We multiplied the PCB concentrations that were estimated from the regression equations by a weighting factor to make this adjustment. The weighting factor was calculated as follows. In 1985, the PCB concentrations observed in prey fish from the Wisconsin side of Lake Michigan were 1.0 mg/kg for a 175mm alewife, 1.0 mg/kg for a 205-mm bloater, 0.5 mg/kg for a 75-mm sculpin, and 0.35 mg/kg for a 135-mm rainbow smelt (4). For prey fish of the same lengths in 1994-1995, the PCB concentrations were 0.6 mg/kg for alewife, 0.75 mg/ kg for bloater, 0.37 mg/kg for sculpins, and 0.35 mg/kg for rainbow smelt. Only rainbow smelt showed no decline in PCB concentration from 1985 to 1994; therefore, the weighting factor for rainbow smelt was 1.0 for all years between 1985 and 1994. For the other three prey fish groups, we assumed that PCB concentration decreased exponentially from 1985 to 1994. An exponential decrease was a reasonable approximation, based on the findings of Madenjian et al. (4). We calculated the weighting factor by dividing the PCB concentration in the target year by the PCB concentration in 1994. Thus, the weighting factors for 1985 were 1.67 for alewife, 1.33 for bloater, and 1.35 for sculpins. Estimation of the PCB concentration for the invertebrate prey category was simpler than that for prey fish. The average PCB concentrations of adult Mysis and adult Diporeia in the vicinity of Sturgeon Bay during the 1994-1995 period were 0.04 mg/kg (A. Trowbridge, University of Minnesota, Minneapolis, MN, personal communication) and 0.08 mg/kg (P. Van Hoof, NOAA Great Lakes Environmental Research Laboratory, Ann Arbor, MI, personal communication; A. 888
9
ENVIRONMENTAL SCIENCE & TECHNOLOGY / VOL. 32, NO. 7, 1998
FIGURE 1. PCB concentrations of lake trout from Lake Michigan in the vicinity of Sturgeon Bay, WI, 1994-1995. Each point represents a composite of one to five whole fish, without the stomach linings, of the same age. PCB concentrations are expressed on a wet weight basis. Fitted exponential curve is also shown. See Table 1 for more details on the fitted curve. Trowbridge, University of Minnesota, St. Paul, MN, personal communication). Averaging these two values yielded a PCB concentration of 0.06 mg/kg for invertebrate prey of lake trout from the Sturgeon Bay vicinity during 1994. In 1985, the average PCB concentration of invertebrate prey was 0.1 mg/kg (4). Again, we assumed an exponential decline in PCB concentration between 1985 and 1994, and weighting factors were calculated accordingly. To complete the estimation procedure, we calculated the amount of PCB in each of the prey categories eaten by a lake trout for a particular season and year by multiplying the PCB concentration of the prey category by the amount of that prey consumed by the lake trout. We then added up all of these PCB amounts to yield the total amount of PCB in the food of the lake trout over its course of existence in the lake. Dividing the total amount of PCB in the food by the total amount of food eaten by the lake trout yielded the PCB concentration of the lake trout prey. Then, we used eq 1 to estimate γ. We estimated γ for lake trout of ages 2-10 in 1994 from the vicinity of Sturgeon Bay. We inspected the values of γ to determine whether γ increased, decreased, or remained relatively constant as the lake trout grew in size.
Results Lake trout PCB concentrations increased exponentially with increasing lake trout length (Figure 1). PCB concentrations for the lake trout composites ranged from 0.2 to nearly 8.0 mg/kg. The regression model explained 94% of the variation in lake trout PCB concentrations (Table 1). The PCB concentration of a large adult (175-mm) alewife averaged 0.6 mg/kg, whereas a small (85-mm) alewife averaged about 0.2 mg/kg (Figure 2). The PCB concentrations
TABLE 2. Estimates of Net Trophic Transfer Efficiency (γ) of PCBs to Lake Trout from Their Preya
FIGURE 2. PCB concentrations of alewife from Lake Michigan in the vicinity of Sturgeon Bay, WI, 1994-1995. Each point represents a composite of five whole fish of similar lengths. PCB concentrations are expressed on a wet weight basis. Fitted regression line is also shown. See Table 1 for more details on the fitted regression line.
age (yr)
mean total length (mm)
gross growth efficiency
PCB concn in lake trout (mg/kg)
PCB concn in food (mg/kg)
γ
2 3 4 5 6 7 8 9 10
244 361 468 554 646 691 710 751 794
0.177 0.178 0.188 0.169 0.157 0.142 0.122 0.113 0.107
0.331 0.580 0.969 1.465 2.278 2.827 3.097 3.773 4.635
0.094 0.170 0.287 0.340 0.402 0.470 0.510 0.543 0.570
0.619 0.607 0.636 0.728 0.886 0.856 0.742 0.788 0.868
a Estimates were based on sampling lake trout and prey fish from Lake Michigan in the vicinity of Sturgeon Bay, WI, 1994-1995.
of Table 2. Estimates of γ for age-4 and younger lake trout were substantially lower than the estimates for lake trout between the ages of 5 and 10. The overall mean of all nine values of γ listed in Table 2 was 0.75, and the 95% confidence interval for this mean ranged from 0.66 to 0.83. In contrast, γ averaged 0.81 for lake trout between the ages of 5 and 10. The 95% confidence interval for this mean spanned from 0.74 to 0.88. There was no upward or downward trend in the values of γ between the ages of 5 and 10 (Table 2).
Discussion
FIGURE 3. PCB concentrations of rainbow smelt from Lake Michigan in the vicinity of Sturgeon Bay, WI, 1994-1995. Each point represents a composite of five whole fish of similar lengths. PCB concentrations are expressed on a wet weight basis. Fitted regression line is also shown. See Table 1 for more details on the fitted regression line. of alewife ranged from about 0.05 to nearly 0.9 mg/kg. There was a relatively high degree of variability in PCB concentrations of larger alewives (Figure 2). The smallest average length for an alewife composite was 68 mm (Table 1). The PCB concentration of a large adult (135-mm) rainbow smelt averaged 0.35 mg/kg (Figure 3). Rainbow smelt PCB concentrations ranged from 0.2 to about 0.45 mg/kg. Whereas the regression model of PCB concentration as a function of fish length explained 65% of the variation in alewife PCB concentrations, the regression model for rainbow smelt explained only 27% of the variation in smelt PCB concentrations (Table 1). Small alewife dominated the diet of small (
