Environ. Sci. Technol. 1998, 32, 1192-1198
Organochlorines in Lake Superior’s Food Web JOHN R. KUCKLICK* AND JOEL E. BAKER Chesapeake Biological Laboratory, University of Maryland, P.O. Box 38, Solomons, Maryland 20688
Lake Superior’s food web was analyzed in 1994 for hydrophobic organochlorine contaminants (OCs) including toxaphene, chlordane and metabolites, hexachlorocyclohexanes, hexachlorobenzene, dieldrin, and polychlorinated biphenyl congeners. Toxaphene was the dominant organochlorine contaminant in the Lake Superior food web, with concentrations 2-15 times higher than total PCBs. Among the biota studied, wet weight toxaphene levels were highest in bloaters (Coregonus hoyi) at 1100 ( 270 ng/g (mean ( 1 standard deviation) and lowest in Mysis relicta (32 ( 804 ng/g). Total PCB concentrations ranged more than a factor of 20 on a wet weight basis but less than a factor of 6 on a lipid weight basis. The lipid content of the organisms explains 81% of the variability in wet weight t-PCB, with trophic position exerting a smaller influence. Using path analysis and regression techniques, the main influence of trophic position on t-PCBs was shown to be due to the concurrent increase in lipid content with trophic position. The relative distributions of organochlorines among trophic levels were very similar, despite the 3 orders of magnitude range in OC hydrophobicity. Unlike our work in Lake Baikal, the accumulation of OCs in the Lake Superior food web was not significantly (p < 0.05) related to the log octanol/water (Kow) partition coefficient, suggesting either that organochlorines in this food web equilibrate with surrounding dissolved OCs rapidly relative to dietary uptake or that the OC assimilation efficiency of predators does not vary with log Kow. Based on OC concentrations in benthic amphipods, we conclude that settling particles are an important source of OCs to deep water organisms in Lake Superior.
Introduction The production and use of many persistent, bioaccumulative organochlorine compounds (OCs) have been banned in developed countries. Compounds such as chlordanes, polychlorinated biphenyls (PCBs), DDTs, dieldrin, and toxaphene (chlorobornanes) persist in the environment and continue to contaminate aquatic food webs, often to levels thought to be hazardous to both human and ecosystem health. Concentrations of OCs in fish from the Great Lakes have initially decreased as a result of these restrictions (1, 2) but have more recently begun to show signs of leveling off (3). PCB levels in Lake Michigan lake trout, for example, initially declined at a rate of 0.28 year-1, but have apparently stabilized at 1.7 mg/kg during the past decade (3). Nonpoint sources of contamination, such as atmospheric deposition, * Corresponding author present address: National Institute of Standards and Technology, Charleston Laboratory, 219 Fort Johnson Road, Charleston, SC 29412. E-mail:
[email protected]. 1192
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may maintain existing concentrations in Great Lakes food webs. However, a number of factors within a lake also may affect biota OC concentrations and must be considered to provide a complete understanding of food web responses to changing OC loadings (4). The lipid content of an organism influences the bioaccumulation of OCs, consistent with the paradigm of OC storage in lipid-rich tissues within biota. A number of recent investigations have shown that wet weight OC concentrations are highly correlated with lipid both within a single species (5) and also across the entire food web (6-8). The most comprehensive examination between wet weight OC concentrations and lipid within a single species was that done by Bentzen et al. (5) using lake trout OC concentrations from a number of North American lakes. These authors demonstrated that the slope of the relationship between log percent lipid and log wet weight total PCB (t-PCB) and total DDT was not significantly different among lakes grouped by trophic status, implying that the OC-lipid affinity is similar among these lakes. However, the intercepts of these plots were significantly different (p < 0.05), which was attributed to differences in both food web length and OC loading. Within a food web, wet weight OC concentrations are also highly correlated with lipid, which is a combined result of increasing lipid with trophic position and bioaccumulation (7, 8). The structure and dynamics of the food web also influence OC concentrations in biota (4, 9). Top predator species in lakes with longer food webs tend to have higher organochlorine concentrations than those in lakes with fewer trophic levels (10). Changes in diet during the predator’s lifetime to more or less contaminated prey also may affect OC concentrations (11, 12). The effect of food web length on OC concentrations has been best demonstrated by the relationship between δ15N, a surrogate measure of trophic position, and wet weight OC concentrations (6, 11). For example, Kidd et al. (6) used δ15N to show that toxaphene levels in lake trout across a series of Canadian lakes were due primarily to differences in food web length rather than to variations in toxaphene inputs into the lakes. Aside from food web structure and lipid content, benthic food webs may possibly facilitate the transfer of contaminants stored in lake sediments, thereby maintaining concentrations at their present levels. Benthic-pelagic coupling, in which sedimentary organic carbon is recycled back to water column organisms, may transfer organic carbon-associated contaminants from the sediments (13, 14). Such benthic transfer could potentially maintain OC levels in water column predators, such as the lake trout, with contaminants deposited in sediments decades ago. The objectives of this study were (a) to quantify organochlorine concentrations in Lake Superior’s food web, with emphasis on the infrequently studied lower trophic level organisms; (b) to examine how lipid content and trophic position influence the accumulation and transfer of OCs in this lake’s food web; and (c) to evaluate the relative importance of sedimentary and water column OC sources to the Lake Superior food web.
Experimental Section Sample Collection. Organisms were collected from both the benthos and the water column of Lake Superior during summer 1994 using the R/V Edwin Link and the Clelia research submersible (June 25-July 1) and by U.S. Fish and Wildlife Service (USFWS) trawls in July. Planktonic organisms, including Mysis relicta (Mysis) and copepods (Limnocalanus sp.) were sampled from three sites along the S0013-936X(97)00794-3 CCC: $15.00
1998 American Chemical Society Published on Web 03/26/1998
Keweenaw Peninsula that we have previously studied (15), NOAA3 [47°20′ N, 89°15′ W], NEO80 [47°7.5′ N, 89°15′ W] and 1383 [47°39.5′ N, 87°57.5′ W], by making successive vertical or diagonal plankton tows of a 0.5 m diameter, 63 µm mesh plankton net. Large Mysis were removed using forceps, and the remaining sample was passed through a 63-µm sieve. Smaller Mysis remained on the net, and other plankton, primarily the copepod Limnocalanus along with some cladocerans, passed through the sieve to a collection vessel. Amphipods (Diporeia hoyi) were collected from site NEO80 using a surface-ship-deployed Ponar grab and a submersible-deployed box core. Deepwater sculpins (Myoxocephalus thompsoni; 86-101 mm) were collected from the submersible using a pilot-operated suction device at sites 1383 and NOAA3. Zooplankton, amphipods, and sculpins were transferred to precleaned glass/Teflon jars and frozen until analysis. Smelt (Osmerus mordax), herring (Coregonus artedii), bloater (Coregonus hoyi), slimy sculpin (Cottus congatus), spoonhead sculpin (Cottus ricei), and 50-99 mm size class of the deepwater sculpin were obtained from trawls made by the USFWS in July 1994 on the western side of the Keweenaw Peninsula near site NEO80 (Table 1). Gutted lake trout (Salvelinus namaycush) samples ranging in length from 42 to 48 cm were obtained from a commercial fishery on the Keweenaw Peninsula. Fish were wrapped in aluminum foil and immediately frozen after collection, remaining frozen until analysis. Extraction and Analysis. USFWS fish samples were sorted by size in the field, and composite samples of two to 10 individual fish were analyzed for OCs and stable isotopes (Table 1). Samples of muscle were taken from individual lake trout fillets after removing the skin. Zooplankton, amphipod, and sculpin samples were composited before homogenization. All samples except Limnocalanus were homogenized (Tekmar). Between 2 and 20 g (wet weight) of the homogenized composite sample was Soxhlet extracted, and lipids were first quantified and then removed as in ref 8. The sample extracts were purified using a two-fraction Florisil technique (8). PCBs were quantified in the first fraction by gas chromatography with electron-capture detection (GC-ECD), and the remaining organochlorines (Table 1) were quantified by negative-chemical ionization mass spectrometry (GC-NIMS) after the two fractions were recombined. Details of OC quantification and quality control are given in ref 8. Total toxaphene is represented as the sum of the hepta-, octa-, and nona-chlorobornanes in the sample that was quantified relative to technical toxaphene using 2,2′,3,4,4′,5,6,6′-octachlorobiphenyl (PCB 204) as the internal standard. Six-chlorinated bornanes, which were not quantified here, comprised 16%, 23%, and 19% of total toxaphene in an analytical standard, a lake sediment sample, and a Lake Superior fish sample, respectively (16, 17). Since the percent contribution of the hexa-chlorobornanes in the fish and the standard have been shown to be similar, this should not greatly bias the total toxaphene result in our study. Stable nitrogen isotopes were analyzed as described in ref 8. Quality Control. Quality control information is detailed in ref 8 and summarized below. The limit of detection (LOD) for the GC-ECD was determined from four blanks that consisted of 40 g of Na2SO4 that was treated as a sample. The LOD was defined as the mean blank plus three standard deviations. Samples exceeding the LOD were blank corrected and reported. The LOD for GC-NIMS analysis was defined as three times the signal-to-noise ratio. If the sample exceeded this value, the average noise was subtracted. The average blank for total PCB (t-PCB, sum of 74 congeners) was 10.8 ng (blank concentration depends on sample size). Mean blanks for GC-NIMS ranged from 0.1 ng for HCB to 92 ng for toxaphene. Surrogates were used to monitor extraction efficiency and losses during sample preparation,
and recoveries from biological samples averaged (mean ( standard deviation) 91 ( 9.2% and 89 ( 7.9% for PCBs 14 and 65 (n ) 34). Analyte concentrations were adjusted to the percent recovery of PCB 65. Recovery experiments were performed to evaluate the effectiveness of sample preparation and analysis methods (8).
Results and Discussion Organochlorine Concentrations. Concentrations of organochlorines on a wet weight basis and the lipid content of all samples are presented in Table 1. Most of the major trophic positions in Lake Superior, except phytoplankton and microplankton (bacteria, etc.), and infauna from the sediment were sampled. Toxaphene was the OC present in the highest concentration (Table 1). Wet weight concentrations ranged from 21 ng/g in large Mysis from station NOAA 3 to 1360 ng/g in the 150-199 mm bloater size class. Toxaphene concentrations were 6.2 ( 3.6 (mean ( 1 standard deviation) times higher than those of total PCBs. Toxaphene levels in Lake Superior fish measured here in 1994 are comparable to those previously measured in by Newsome et al. (18), where wet weight concentrations ranged from 458 ng/g in herring up to 936 ng/g in lake trout. However, toxaphene concentrations in Lake Superior lake trout reported recently by Glassmeyer et al. (19) are considerably higher than ours (4900 ( 1400 ng/g versus 390 ( 110 ng/g). The difference is attributed partly to a higher lipid content in that study’s lake trout (19%) versus ours (9%), and our fish samples being filets rather than whole fish. The analytical techniques used for measuring toxaphene were comparable. The present and historical sources of toxaphene to Lake Superior are not entirely known but arise partly from the atmospheric deposition of volatilized toxaphene from areas of past use, such as the southeastern United States (20, 21). Toxaphene was once the most heavily used pesticide in the United States with the peak production estimated at 55 × 106 kg in 1974 (20). Worldwide toxaphene usage since 1950 is estimated to be 1.33 × 106 t (22). Polychlorinated biphenyls were the next most abundant group of organochlorines in Lake Superior organisms (Table 1). The t-PCB concentrations on a wet weight basis ranged from 5.6 ng/g in small Mysis from station NOAA3 to 180 ng/g in 250-300 mm bloater size class (Table 1). The t-PCB concentrations in Lake Superior fish (bloater and lake trout) were lower than observed in the other Great Lakes (e.g., refs 1, 12, and 23) and lower than reported by Devault et al. (2) for Lake Superior Lake trout collected in 1990 (120 ( 28 ng/g versus 450 ( 140 ng/g). Total PCBs in all biota were dominated hexa-, penta-, and heptachlorobiphenyl congeners, with only minor contributions from the di-, tri-, and tetrachlorobiphenyl congeners that dominate the lake’s water column PCB inventory (24). Other organochlorines that were detected in Lake Superior include dieldrin, DDT and metabolites, chlordane and metabolites, hexachlorobenzene, and R- and γ-hexachlorocyclohexane (Table 1). All of these compounds were lower in concentration relative to t-PCBs and toxaphene. Dieldrin and 4,4′-DDE were the two compounds present in the highest concentration aside from t-PCBs and toxaphene with wet weight concentrations ranging up to 81 ( 19 ng/g in bloaters. (Table 1). Structure of Lake Superior’s Food Web. Feeding relationships among organisms in the Lake Superior food web were determined using δ15N. These were measured on most of the samples (Table 1); however, due to sample size limitations, values are not available for some organisms. Previous studies of aquatic food webs suggest a 3-3.5‰ increase δ15N for a predator feeding on a discrete prey item VOL. 32, NO. 9, 1998 / ENVIRONMENTAL SCIENCE & TECHNOLOGY
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TABLE 1. Organochlorine Concentrations (ng/g wet weight), δ15N (‰), and Lipid Content of Biota Collected from Lake Superior sample
no. or mass composited
δ15N
% lipid
t-PCBs
toxaph
r-HCH
HCB
γ-HCH
dieldrin
4,4′-DDE
hept
t-chl
c-chl
t-nona
c-nona
hept-epox
oxy-chl
1-49 mm 50-99 mm 100-149 mm 150-199 mm
11 10 5 5
NAa NA 6.27 6.98
2.9 2.6 4.0 4.6
21 28 41 53
99 140 210 200
1.5 2.6 5.7 6.5
0.8 1.3 1.3 1.8
Smeltb
