Environ. Sci. Technol. 1998, 32, 3063-3067
Net Trophic Transfer Efficiency of PCBs to Lake Michigan Coho Salmon from Their Prey C H A R L E S P . M A D E N J I A N , * ,† ROBERT F. ELLIOTT,‡ LARRY J. SCHMIDT,† TIMOTHY J. DESORCIE,† ROBERT J. HESSELBERG,† RICHARD T. QUINTAL,† LINDA J. BEGNOCHE,† PATRICK M. BOUCHARD,‡ AND MARK E. HOLEY‡ U.S. Geological Survey, Biological Resources Division, Great Lakes Science Center, 1451 Green Road, Ann Arbor, Michigan 48105, and U.S. Fish and Wildlife Service, Green Bay Fishery Resources Office, 1015 Challenger Court, Green Bay, Wisconsin 54311
Most of the polychlorinated biphenyl (PCB) body burden accumulated by coho salmon (Oncorhynchus kisutch) from the Laurentian Great Lakes is from their food. We used diet information, PCB determinations in both coho salmon and their prey, and bioenergetics modeling to estimate the efficiency with which Lake Michigan coho salmon retain PCBs from their food. Our estimate was the most reliable estimate to date because (a) the coho salmon and prey fish sampled during our study were sampled in spring, summer, and fall from various locations throughout the lake, (b) detailed measurements were made on the PCB concentrations of both coho salmon and prey fish over wide ranges in fish size, and (c) coho salmon diet was analyzed in detail from April through November over a wide range of salmon size from numerous locations throughout the lake. We estimated that coho salmon from Lake Michigan retain 50% of the PCBs that are contained within their food.
Introduction For the purpose of assessment of risk to wildlife and humans consuming contaminated fish, computer models have been used to predict changes in PCB accumulation rates in fish associated with changes in the food web structure (1). The efficiency at which fish assimilate PCBs from their food is one of the most important factors regulating PCB accumulation rates in fish (2). Therefore, an accurate estimate of the efficiency at which fish retain PCBs from their food is critical for predicting future risk to both people and wildlife eating contaminated fish. Coho salmon (Oncorhynchus kisutch) was introduced into Lake Michigan during the 1960s to control the population of alewife (Alosa pseudoharengus), which had become a nuisance to public health (3), and to establish a sport fishery (4). Also beginning in the 1960s, lake trout (Salvelinus namay* Corresponding author phone: (734)994-3331, ext. 259; fax: (734)994-8780; e-mail:
[email protected]. † U.S. Geological Survey. ‡ U.S. Fish and Wildlife Service. S0013-936X(98)00277-6 Not subject to U.S. Copyright. Publ. 1998 Am. Chem. Soc. Published on Web 09/10/1998
cush), a native salmonine, was planted into Lake Michigan in an attempt to restore the population, which had been extirpated from the lake due to overfishing and sea lamprey (Petromyzon marinus) predation (3). Coho salmon movements within Lake Michigan have been characterized as extensive, with a general trend to traverse large portions of the lake during the fish’s lifetime (5), whereas movements of lake trout in Lake Michigan are believed to be considerably more restricted (6). To estimate the efficiency with which the net trophic transfer of PCBs from prey to salmonines occurred, Jackson and Schindler (7) used the equation
γ)
[PCBPRED]R
(1)
[PCBPREY]
where γ ) net trophic transfer efficiency of PCBs from the prey to the predator, [PCBPRED] ) PCB concentration of predator (mg/kg), [PCBPREY] ) PCB concentration of the predator’s food (mg/kg), and R ) gross growth efficiency (gge) of the predator. Gross growth efficiency (gge) was equal to the weight gained by the predator divided by the amount of food eaten by the predator. During 1994 through 1995, the Great Lakes National Program Office (GLNPO) of the U.S. Environmental Protection Agency sponsored the Lake Michigan Mass Balance (LMMB) project; the ultimate objective was to develop a model for flow of contaminants, such as PCBs, through the Lake Michigan ecosystem. Coho salmon and lake trout were chosen to represent the top predators of the ecosystem (8, 9). The diet and PCB concentration of coho salmon of various sizes and at numerous locations throughout Lake Michigan was investigated during April through November of 1994 and 1995. Additionally, PCB determinations were made on prey fish of various sizes and from several nearshore locations in Lake Michigan during spring, summer, and fall of the same time period. Thus, data from the LMMB project was wellsuited for the calculation of net trophic transfer efficiency of PCBs to coho salmon from their prey. Using LMMB data, Madenjian et al. (10) estimated the net trophic transfer efficiency of PCBs from prey fish to lake trout to be 80%. Net trophic transfer efficiencies of PCBs from prey to coho salmon have been estimated in the previous study by Jackson and Schindler (7); however, no previous study has made use of a data set with such extensive spatial and temporal coverage of the lake as was done in the LMMB project. The objective of the present study was to calculate the net trophic transfer efficiency to coho salmon from their prey, using the LMMB project data set, and then to compare our estimate with previous estimates of this efficiency. We also compared the estimate for coho salmon with that for lake trout.
Methods Field Sampling. From April-November during 1994 and 1995, we sampled 1383 coho salmon from throughout Lake Michigan for diet analysis, and 301 of these 1383 fish were also used in PCB determinations. Hook-and-line sampling was used to collect fish from throughout the lake each year, and the state-operated harvest weirs were used to collect fish returning to rivers in the fall of each year. The times and locations of capture coincided with the major migrations and congregations of coho salmon throughout Lake Michigan. Overall, coho were sampled from 28 different regions of the lake during 229 collection days over the two-year period. VOL. 32, NO. 20, 1998 / ENVIRONMENTAL SCIENCE & TECHNOLOGY
9
3063
Soon after collection, all coho salmon were measured to the nearest millimeter total length and weighed to the nearest 0.01, 0.025, or 0.05 kg depending on their size and the scale available. The stomach from each fish was then removed and either preserved in a 10% formalin solution or frozen. Scales were taken from each fish for age determination. After their stomachs were removed, coho salmon being kept for PCB determination were individually wrapped in solventrinsed aluminum foil, placed in a plastic bag, and frozen. Additionally, in 1994, 25 yearling coho salmon were obtained from the Platte River Hatchery (near Frankfort, MI) just prior to when they were to be planted into the lake. These fish were processed in the same manner but were weighed to the nearest 0.1 g, and they did not have their stomachs removed. To catch prey fish, bottom trawling was performed at depths ranging from 10 to 50 m. During the spring, summer, and fall of 1994 as well as the spring and fall of 1995, prey fish were caught in the vicinities of three different nearshore locations: Saugatuck, MI; Port Washington, WI; and Sturgeon Bay, WI. The prey fish species included alewife (Alosa pseudoharengus), bloater (Coregonus hoyi), rainbow smelt (Osmerus mordax), slimy sculpin (Cottus cognatus), and deepwater sculpin (Myoxocephalus thompsoni). Prey fish were removed from the bottom trawl, packaged in solventrinsed aluminum foil, placed in plastic bags, and then frozen. For more details on field sampling, refer to Holey and Elliott (9), Elliott et al. (11), and Brown and Eck (8). Coho Salmon Stomach Processing. We followed the protocol established by the Lake Michigan Technical Committee for processing the stomachs of the coho salmon (11). Refer to Holey and Elliott (9) for more details. Analysis of Coho Salmon Diet Data. Again, we followed the Lake Michigan Technical Committee’s protocol for analyzing and summarizing the diet data for coho salmon (11). For each age class of coho and each month, we calculated the proportion, on a wet weight basis, that each prey type contributed to the total amount of food in the diet. These proportions were based on the total weight of food contained in the stomachs. We then constructed lengthfrequency distributions of prey fish found in the coho stomachs by month. From these, we determined the modal lengths for each size class of each prey fish species consumed during each month. For more details of data analysis and summary, refer to Elliott et al. (11) and Elliott and Holey (12). PCB Determinations. In the laboratory, coho salmon were thawed and then composited into groups of three to five fish of the same age, same sex, similar size, and similar time and location of sampling. In total, 67 composites were derived from the 301 coho salmon selected for PCB determinations. Prey fish were composited into groups of five fish by species, length, location, and time of sampling. Mean total length for each coho salmon and prey fish composite was calculated. All composited fish were homogenized using an industrial-strength mixer. The concentrations of 80 different PCB congeners were determined in each composite sample using the procedure described by Schmidt and Hesselberg (13). Summing the PCB concentrations of all 80 congeners yielded a reasonable estimate of total PCB concentration in the sample (10). Although certain PCB congeners are of particular interest to aquatic toxicologists because these congeners display relatively high toxicities, many present-day computer models concerned with flow of contaminants through the food web still focus on total PCBs (14). Moreover, we wanted to compare our results with previous model applications involving total PCB concentrations. Therefore, the analyses presented in our study will be applied to data for total PCB concentrations only. The PCB concentrations were expressed on a wet weight basis. 3064
9
ENVIRONMENTAL SCIENCE & TECHNOLOGY / VOL. 32, NO. 20, 1998
Analysis of PCB Data. The determination of the PCB concentration of a coho salmon without its stomach was assumed to be an accurate estimate of its whole-body PCB concentration. This appeared to be a reasonable assumption, based on the arguments presented by Madenjian et al. (10). For coho salmon and each of the prey species, we examined the relationship between PCB concentration and fish total length using regression analysis. We considered both straight line and exponential functions, and we used the criteria outlined by Draper and Smith (15) to choose the most appropriate regression model. These regression equations were then used in calculating γ. Estimation of γ. We used eq 1 to calculate the net trophic transfer efficiency of PCBs from prey to Lake Michigan coho salmon, γ. We calculated γ for coho salmon of ages 24 months and 29 months. The three quantities appearing on the righthand side of eq 1 were PCB concentration of the prey of the coho salmon, gross growth efficiency of the coho salmon, and PCB concentration of the coho salmon. The regression equation for coho salmon PCB concentration as a function of coho salmon length in 1995 was not significantly different than that for 1994 (P > 0.05), and therefore we pooled all coho salmon from both years to represent the PCB concentration of coho salmon from Lake Michigan during 1994 through 1995. Based on 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 Lake Michigan during the same time period. Most coho salmon are stocked as yearlings into Lake Michigan, typically around the first of April (16). Most coho salmon mature during their second year in the lake (16). During late September of the second year, coho salmon begin to congregate near river mouths; and most spawning migration up the rivers occurs during October (5). Coho salmon die shortly after spawning. Thus, we simulated the consumption and growth of coho salmon from April 1 as planted yearlings to September 15 of the following year. Data from the Platte River Hatchery indicated an average weight of 33 g at time of planting in Lake Michigan during the early 1990s, and we used this weight as the initial weight in our simulations. Our length and weight observations for anglercaught coho salmon in April and September of 1994-1995 yielded an average length of 484 mm and an average weight of 872 g for 24-month old fish and an average length of 636 mm and an average weight of 3020 g for 29-month old fish. We used the coho salmon bioenergetics model developed by Stewart et al. (16) to estimate the gross growth efficiency (gge) for coho salmon from Lake Michigan. See Hewett and Johnson (17) and Madenjian et al. (10, 18) for more details on this procedure. We inputted our coho salmon diet and growth data from the LMMB project into the bioenergetics model; the diet schedule is summarized in Table 1. We then used the estimates of gge in our calculations of γ. The PCB concentrations of coho salmon of ages 24 months and 29 months were estimated by substituting average lengths at these ages into our regression model presented in Table 2. We did not obtain yearling coho salmon in Lake Michigan from April through June during our sampling for the LMMB project, and therefore we used diet information for these young coho salmon from previous studies (19). We assumed that the overwinter diet composition of coho salmon was an average of the diet during the late fall and the diet during the early spring of the following year. To estimate the PCB concentration of prey, our agespecific monthly diet data for coho salmon was inputted into the bioenergetics model to estimate the amounts of the various prey categories consumed by coho salmon each month. The modal length of each prey fish category was substituted into the appropriate equation in Table 2 to
TABLE 1. Percent Diet Composition, on a Wet-Weight Basis, for Coho Salmon in Lake Michigan during 1994-1995a prey category year in lake
time period
1 1 1 1 2 2 2 2 2 2
1 Apr-30 Jun 1 Jul-30 Sep 1 Oct-15 Nov 16 Nov-31 Mar 1 Apr-30 Apr 1 May-31 May 1 Jun-30 Jun 1 Jul-31 Jul 1 Aug-31 Aug 1 Sep-15 Sep
terrestrial insects
benthic invertebrates
80
20 12 1 5 9 15 5
Bythotrephes cederstromi
small alewife
large alewife
1 35 18
67 29 23 17 13 3 5 3 19
19
3
35 69 54 91 95 91 78
rainbow smelt
5 5 4 15 1 5
bloater
other fish
1 5 1 1 2
25 13 1
1
a Diet of coho salmon during April through June of their first year in the lake was taken from Elliott (19). The winter diet was estimated by averaging the diet composition from the preceding fall with that from the following spring. Benthic invertebrates included Mysis and Diporeia. Small alewife were e120 mm in total length, and large alewife were >120 mm in total length. The other fish category chiefly included threespine stickleback. This diet schedule was used in the bioenergetics modeling of food consumption by coho salmon. We simulated food consumption by coho salmon from the time of planting as yearlings into Lake Michigan on April 1 through September 15 of the following year.
TABLE 2. Fitted Regression Equations for PCB Concentration (Y, in mg/kg) as a Function of Mean Total Length (X, in mm) for Coho Salmon and Prey Fish Found in Lake Michigan, 1994-1995a species
regression equation
R2
N
range in mean total length (mm)
alewife bloater coho salmon deepwater sculpin slimy sculpin rainbow smelt
Y ) 0.00360X - 0.060 Y ) 0.00375X + 0.079 Y ) 0.03725e0.00515X Y ) 0.00384X - 0.030 Y ) 0.00423X + 0.108 Y ) 0.00249X - 0.023
0.571 0.292 0.704 0.121 0.154 0.130
132 139 67 74 69 73
68-206 115-236 137-775 55-149 45-95 109-153
a PCB concentrations of most of the coho salmon were based on whole-fish composites, without stomachs, of three to five fish. The only exceptions were whole-fish composites, complete with stomachs, of yearling coho salmon, which were less than 200 mm in total length, from the Platte River Hatchery. PCB concentrations of prey fish were based on whole-fish composites of five fish. The PCB concentration of the composite was matched with the mean total length of the fish comprising the composite. N ) the number of composites used to calculate the regression equation.
calculate the PCB concentration of that prey category for that month. Over 90% of the ingested biomass in the other fish category was comprised of threespine stickleback (Gasterosteus aculeatus). We are unaware of any PCB determinations for threespine stickleback in Lake Michigan. Because this fish presumably has a benthic orientation in Lake Michigan (20), as do sculpins (21), we averaged the regression line for slimy sculpin with that for deepwater sculpin to estimate the PCB concentration for threespine stickleback of a given length. Threespine sticklebacks contributed less than 2.5% to the total amount of food eaten by coho salmon during their 17month duration in the lake during the 1994-1995 period. The average PCB concentrations of adult Mysis and adult Diporeia in Lake Michigan during the 1994-1995 period were 0.04 mg/kg (A. Trowbridge, University of Minnesota, Minneapolis, MI, personal communication) and 0.08 mg/kg (P. Van Hoof, NOAA Great Lakes Environmental Research Laboratory, Ann Arbor, MI, personal communication; A. Trowbridge, University of Minnesota, St. Paul, MN, personal communication). Averaging these two values yielded a PCB concentration of 0.06 mg/kg for benthic invertebrate prey of coho salmon during the 1994-1995 period. The average PCB concentration for Bythotrephes cederstromi in Lake Michigan during 1994-1995 was 0.03 mg/kg (A. Trowbridge, University of Minnesota, St. Paul, MN, personal communication). PCB concentration of terrestrial insects was assigned a value of 0.07 mg/kg (22).
Results Coho salmon PCB concentration increased exponentially with increasing coho salmon length (Figure 1). The regression
FIGURE 1. PCB concentrations of coho salmon from Lake Michigan, 1994-1995. Each point represents a composite of three to five whole fish of the same age and similar size. Stomachs of all of the coho salmon, with the exception of the yearlings (total length
