Seasonal Dynamics of PCB and Toxaphene Bioaccumulation within a Lake Michigan Food Web

J. Great Lakes Res. 28(1):52–64 Internat. Assoc. Great Lakes Res., 2002

Seasonal Dynamics of PCB and Toxaphene Bioaccumulation within a Lake Michigan Food Web Heather M. Stapleton1, John Skubinna2,†, and Joel E. Baker1,* 1Chesapeake

Biological Laboratory University of Maryland Solomons, Maryland 20688 2Michigan

State University Dept. of Fisheries and Wildlife Sciences East Lansing. Michigan 48864 ABSTRACT. Seasonal variations in PCB and toxaphene concentrations were measured in bulk zooplankton, mysid shrimp, benthic amphipods, alewife, and bloater chub collected from Grand Traverse Bay, Lake Michigan between April and September of 1997 and 1998. Concentrations of PCBs in the dissolved phase of the water column were consistent over time; however, seasonal changes in contaminant concentrations within the biota were significant. Seasonal changes were most pronounced in zooplankton, which displayed highest PCB burdens in April and decreased by as much as 75% through September, coincident with changes in phytoplankton biomass, species composition, and changes in the particulate pools of PCBs within the water column. Mysis sp. display a similar PCB trend as zooplankton, while Diporeia sp. displayed maximal PCB concentrations in late summer during 1997. PCB trends in the primary forage fish alewife (Alosa pseudoharengus) and bloater (Coregonus hoyi) were correlated more to shifts in lipid content and seasonal diet preferences. PCB concentrations were higher (p < 0.01) in bloater (310 ± 98 ng/g wet weight) than alewife (233 ± 70 ng/g wet weight), however alewife possessed higher toxaphene burdens (198 ± 72 ng/g wet weight) than bloater (88 ± 36 ng/g wet weight). Alewife contaminant burdens were high in spring and fall of both years, decreasing by as much as 60% in midsummer, and were reflective of changes measured in their lipid content associated with gamete production and spawning. These results suggest that despite invariant concentrations of the dissolved pool of PCBs within the lake, accumulation of PCBs by the biota on seasonal scales is controlled appreciably by growth and lipid dynamics, and foraging behavior. INDEX WORDS:

PCBs, toxaphene, Grand Traverse Bay, bioaccumulation.

INTRODUCTION Seasonal changes in hydrophobic organic contaminants (HOCs) burdens within aquatic food webs are rarely investigated due to the extensive sampling and analyses required. However, seasonal dynamics in HOC accumulation have been observed and vary among systems dependent upon many factors, including temperature and biota densities (Crane and Sonzogni 1992, Harding et al. 1997, Roe and MacIsaac 1998, Hargrave et al. 2000). In Lake Michigan, higher zooplankton polychlorinated biphenyl (PCB) burdens were observed in January

compared to July, reflecting seasonal changes in surface water PCB concentrations (Offenberg and Baker 2000). In Lake Erie, observed PCB concentrations in plankton were highest during June when monitored from May through October and were correlated to relative abundances of zooplankton and phytoplankton (Epplett et al. 2000). Seasonal fluctuations in HOC burdens within lower trophic level aquatic biota are often influenced more by changes within HOC pools in their exposure media than are upper trophic levels. Changes in the dissolved phase of HOCs throughout the season are often influenced by volatilization rates, advection of water masses, partitioning with suspended and settling solids, and any inputs from local sources (Swackhamer et al. 1988; Jeremiason

*Corresponding

author. E-mail: [email protected] Address: Michigan Dept. of Environmental Quality, Monie, Michigan 48857 †Current

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PCBs and Toxaphene in Lake Michigan et al. 1994, 1999; Hargrave et al. 1997). For example, in Lake Superior, Hornbuckle et al. (1994) observed the highest volatilization fluxes of PCBs in late summer/early fall which were strongly correlated to surface water temperature and atmospheric vapor pressure. These processes can influence the bioavailability of HOCs to the lower trophic levels. Additionally, changes in the growth rates of plankton can affect their ability to accumulate HOCs from the dissolved phase (Stange and Swackhamer 1994, Skoglund and Swackhamer 2000). However, in higher trophic levels, exposure to HOCs is typically via dietary sources, and therefore any effects from fluctuating concentrations of dissolved HOCs become diminished relative to the importance of fish tissue turnover time. Most modeling efforts have shown that HOC accumulation in fish, especially piscivorous fish, is a result of dietary accumulation (Thomann and Connolly 1984, Madenjian et al. 1993, Madenjian et al. 1998). On seasonal time scales, fish will experience changes in their diet through ontogeny, migration patterns, and availability of food (Eck andWells 1986, Jude et al. 1987). Changes in lipid content that occurs seasonally in some fish due to spawning and growth can also affect the assimilation of HOCs from their diet since these contaminants are lipophilic. Modeling simulations have suggested that changes in the lipid content of a prey item can affect the lipid content of the predator, thus affecting the predator ’s ability to assimilate HOCs (Borgmann and Whittle 1991, Madenjian et al. 2000). Additionally, egg production can act as a vector for depuration of HOCs from the mother (Larsson et al. 1993, Miller 1993). Therefore, seasonal dynamics in lipid composition, growth, and diet can be important for understanding the dynamics of HOC accumulation in food webs. Numerous studies have attempted to predict and model PCB concentrations within biota based upon physical properties of the water column and bioenergetics processes (Thomann 1989, Jackson and Carpenter 1995, Eby et al. 1997). Most of these models lack seasonal dynamics that can affect assimilation of HOCs. These models could be improved by incorporating seasonal dynamics in water column processes and accumulation capacities, especially at the base of the food chain where plankton and other invertebrates are prone to seasonal changes in contaminant exposure and assimilation. The data presented in this paper were collected as part of an extensive study investigating PCB transport and accumulation in Lake Michigan food webs

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on seasonal time scales to elucidate ecosystem response times. Previous publications resulting from this study have demonstrated seasonality in water column characteristics (McCusker et al. 1999), differences in the transfer of PCBs between the pelagic and benthic environments (Stapleton et al. 2001a), PCB metabolism in deepwater sculpin (Stapleton et al. 2001b) and have calculated the response times of contaminants as recorded in sediment cores (Schneider et al. 2001). This project has provided an excellent data set in which to examine seasonal dynamics due to the numerous food web members collected simultaneously every month, from April through September, within the same area. The purpose of this paper is to examine the variations in HOC burdens within the food web on a seasonal scale, with the objectives of: 1) determining how seasonal HOCs in the invertebrate populations vary with changes in HOC pools of the water column, and 2) determining how seasonal HOCs within the forage fish populations change with respect to their lipid dynamics and seasonal feeding preferences. MATERIALS AND METHODS Sample Collection This study was conducted between April of 1997 and September of 1998 in Grand Traverse Bay (Fig. 1), located on the northeast coast of Lake Michigan. Sample collection and experimental methods employed for the food web samples were discussed in a previous publication (Stapleton et al. 2001a). Information on composites and number of individuals sampled can be found through the supplementary material of this manuscript and by clicking on supporting information at http://pubs.acs.org/journals/ esthag/index.html. Briefly, bulk zooplankton were collected using plankton nets with a 1-m diameter and a 153-µm mesh and obliquely towed with steps between 0 and 80 m. Visual inspection of the plankton was performed and an approximation of species composition was conducted using a dissecting microscope. Benthic amphipods (Diporeia hoyi) and opposum shrimp (Mysis relicta) were collected primarily using a benthic sled towed along the bottom of the lake while alewife (Alosa pseudoharengus) and bloater chub (Coregonus hoyi) were collected using gill nets and otter trawls. Alewife and bloater chub were composited by month of collection and contained between 5 and 15 individuals per composite. Water samples were collected for dissolved and

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Stapleton et al. extracted using a 50:50 mixture of acetone:hexane for 24 hours followed by a liquid/liquid extraction with hexane in separatory funnels. Individual PCB congeners were quantified according to the method by Mullin et al. (1984) using a Hewlett Packard 5890 gas chromatograph equipped with a 63Ni detector. Toxaphene was quantified using a Hewlett Packard 5890 gas chromatograph connected to a Hewlett Packard 5989A mass spectrometer operated in select ion mode and employing negative chemical ionization according to the method by Glassmeyer et al. (1999). To review, toxaphene is quantified by homolog groups monitored by the base m/z peaks in a series of windows and the isotopic ratios of the compounds are compared to an accepted value developed by Glassmeyer et al. (1999). This automated method for toxaphene is a conservative method that considers possible interfering compounds such as chlordanes.

FIG. 1. Map of sampling sites within Grand Traverse Bay, Lake Michigan.

particulate PCB analyses at depths of approximately 5 m every month from April through September in 1997. Approximately 200 L of water was pumped from a depth of 5 m below the surface using a submersible Teflon pump, and filtered through a 293 mm glass fiber filter to remove particulate matter. The filtrate was collected in precleaned stainless steel tanks and later pumped through a packed XAD-2 resin at a flow rate of 120 mL/min using a peristaltic pump. The XAD-2 resin and glass fiber filter were extracted separately to quantify PCBs, and toxaphene in the dissolved and particulate phases, respectively. XAD-2 was stored in pre-cleaned glass containers at 4°C while glass fiber filters were folded and stored in aluminum foil at –4°C until extraction. Procedures for extracting and quantifying water and biota samples are reported in Offenberg and Baker (2000). Briefly, biota samples were ground with sodium sulfate and Soxhlet extracted for 24 hours with dichloromethane. Extracts were then cleaned up using gel permeation chromatography to remove the lipids and then eluted through a precleaned Florisil column to separate PCBs from pesticides. XAD-2 resin samples were Soxhlet

Quality Assurance As a measure of analytical precision and accuracy, quality assurance methods were employed by extracting laboratory matrix blanks spiked with PCBs, standard reference material, and performing replicate analyses. Laboratory matrix blanks consisted of approximately 30 g of granulated Na2SO4 spiked with surrogate PCB compounds and extracted adjacent to biota samples. Average percent recoveries for the surrogates were 80 ± 12% and 79 ± 11% for IUPAC PCB congeners 14 (3,5dichlorobiphenyl) and 166 (2,3,4,4′,5,6-hexachlorobiphenyl) respectively. Analytical precision on replicate samples varied between 5 and 15% of the total. The standard reference material was obtained from the National Institute of Standards and Technology (NIST) (1974a; Organics in Mussel Tissue). Laboratory extraction of this material resulted in PCB concentrations averaging 101 ± 27% of the certified values. Standard reference materials were not available for toxaphene analyses at the time of sample processing. As a measure of quality assurance in toxaphene analyses, laboratory blanks were extracted and quantified for toxaphene. The standards used for the quantification were Hercules toxaphene (courtesy Dr. Ron Hites Laboratory, Indiana University). Blanks were the same as for PCBs and consisted of approximately 30 g sodium sulfate extracted alongside biota samples. Limits of detection were 2 ng total toxaphene.

PCBs and Toxaphene in Lake Michigan

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RESULTS AND DISCUSSION Individual PCB congeners were quantified for all samples in this study. Reported here are concentrations of total PCBs to examine seasonal dynamics. Congener patterns change between media (i.e., from air to water; from water to biota) and are a factor of their physical properties such as log Kow and depuration rates in biotic tissues (Fisk et al. 2000). From this data set we have shown that congener patterns change significantly from the base of the food web, zooplankton, to the top predators such as lake trout (Stapleton et al. 2001b). For example, the proportion of hexachlorobiphenyls increases with increasing δ 15 N (R 2 = 0. 81), an indicator of trophic position. However, the changes in PCB congener patterns among media and species is much more pronounced than any changes within a species, which was ascertained by a principal component analyses (PCA) on this entire data set. PCA revealed that there was little change in PCB congener patterns on seasonal time scales relative to differences in PCB congener patterns among species. Therefore, for the purposes of this paper, changes were described in total PCBs. Seasonal PCB Dynamics in Surface Waters Dissolved and particulate PCB surface water concentrations were measured at sites GT1 and GT3 during the experimental time periods and are presented in Figure 2. Total PCBs in Figure 2 represent the total of 70 individual PCB congeners quantified (see Stapleton (2000) for congener details). Water samples were not quantified for toxaphene due to limitations on detection (L.O.D. = 20 pg/L). Dissolved PCB concentrations are relatively constant from April through September of 1997 and 1998, ranging from 85 to 150 ng/L, with no apparent temporal pattern. However, particulate PCB concentrations (ng/g dry) are highest in the spring of both years and decrease significantly through late summer. Particulate PCB levels were much higher in 1997 relative to 1998. The total suspended particulate matter in the water column in 1997 was 0.7 ± 0.3 mg/L, as opposed to 0.4 ± 0.04 mg/L in 1998. Fluorescence measurements taken concurrently in this study indicated a higher phytoplankton abundance and higher primary productivity during the spring period that declined linearly throughout the summer into early fall (McCusker et al. 1999). This suggests that seasonal changes in the particulate PCB concentrations may be driven by changes in

FIG. 2. Seasonal dissolved (A) and particulate (B) PCB concentrations in Grand Traverse Bay during the 1997 to 1998 sampling seasons. Sampling depth was 5 m. (Error bars represent standard deviation of two samples; one from GT1 and the other from GT3.) the plankton abundance and/or the amount of labile organic carbon available. Seasonal Contaminant Dynamics in Invertebrates Invertebrates are important vectors for contaminant transfer between abiotic matrices and forage fish (DePinto and Coull 1997, Zaranko et al. 1997). In this study, PCB concentrations in zooplankton were highest in April, decreasing by as much as 70% through September in both 1997 and 1998 (Fig. 3A; top). Offenberg and Baker (2000) observed a significant decrease in zooplankton PCB concentrations from January to July in southern Lake Michigan, similar to the trend observed here. In contrast, lipid content was lowest in April 1997

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FIG. 3. Seasonal PCB (top) and toxaphene (bottom) concentrations in (A) bulk zooplankton, (B) Mysis relicta, and (C) Diporeia hoyi composite samples collected from Grand Traverse Bay, 1997 and 1998. Error bars represent standard deviation of replicate composite samples. and increased 4-fold through early fall of 1997 (lipid content is not available for all invertebrate species in 1998). The increasing lipid content of zooplankton between April and August may be related to shifts in species composition within the bulk zooplankton. During the sampling period Copepoda sp. dominated the zooplankton assemblage in April 1997 and a decreasing proportion was observed throughout the summer as an increasing proportion of Cladocera sp. was collected in the tows (Table 1). Changes in zooplankton PCB burdens reflect changes in the surface water particulate PCB conTABLE 1. Approximate percent of species composition, by weight, observed in zooplankton tows collected in Grand Traverse Bay during 1997 sampling season. April May Copepoda sp. 100 60 Cladocera sp. 15 Diatoms 25 Filamentous Algae Bythotrephes

June July August Sept. 75 75 60 45 25 25 30 40 10 15

centrations. This coupling between particulate PCBs and zooplankton PCB body burdens is most likely associated with zooplankton feeding upon fresh and labile phytoplankton material which adsorbs a greater amount of PCBs during the spring. High springtime PCB concentrations within plankton has been observed previously and in marine systems as well. Harding et al. (1997) observed highest concentrations of PCBs in a marine pelagic food web during the spring that decreased through late fall. In Lake Erie, Epplett et al. (2000) observed highest concentrations of PCBs during June, which was coincident with changes in the observed lipid content of the zooplankton. PCB burdens within zooplankton in GTB were not correlated with lipid content and this disparity may be driven by different nutritional sources available to the systems. A majority of the samples collected during this study possessed significantly lower lipid contents than previously recorded in the literature and may reflect the introduction of zebra mussels (Dreissena polymorpha) in the Great Lakes. Previous studies have suggested that the presence of zebra mussels may be responsible for decreased primary productivity and the population declines of the benthic amphipod in Lake Michigan (Nalepa et al. 1998; Landrum et al. 2000).

PCBs and Toxaphene in Lake Michigan During 1997, toxaphene concentrations in zooplankton were highest in July (42 ng/g), and lowest in June (13 ng/g), corresponding to shifts in the lipid content measured in zooplankton (Fig. 3A; bottom). In 1998 the highest toxaphene concentrations observed were in April and lowest in September. Toxaphene concentrations within zooplankton are unavailable for April of 1997 making it difficult to compare the PCB and toxaphene seasonal trends throughout the year. The similar log Kow values of these two organochlorine mixtures would suggest similar transport mechanisms. Mysis relicta PCB burdens were highest during May and June 1997, and decreased in August. In 1998, the highest levels of PCBs were observed in March and decreased through June from 15 to 3 ng/g (Fig. 3B; top). Toxaphene also decreased in Mysis relicta from the spring through late summer, from 6.5 to 1.3 ng/g (Fig. 3B; bottom). The lipid content of Mysis was highest in the spring months (1.6 to 1.9%) and decreased throughout the summer (0.6%), in a trend similar to observations made by Gardner et al. (1985). Seasonal alterations in the lipid biomass of Mysis associated with feeding and metabolism may influence the assimilation of these hydrophobic contaminants seasonally. Mysis migrate vertically in the water column, inhabiting the deep water during the day and moving up in the water column at night (Bowers et al. 1990). They are opportunistic feeders, and depending on prey availability and density, can switch between predatory raptorial feeding and filter-feeding on suspended particles (Grossnickle 1982). If Mysis were feeding heavily upon zooplankton, the PCB body burden of Mysis would be equivalent to or greater than the PCB body burden of zooplankton. However, this is not the case in this system, as Mysis PCB body burdens are on average 50% lower than zooplankton PCB levels, similar to other reported values (Swackhamer et al. 1998). Additionally, toxaphene burdens in Mysis relicta are on average 75% lower than the burdens observed in bulk zooplankton. Therefore, seasonal shifts in PCB and toxaphene burdens in Mysis may be linked to feeding upon suspended and settling particulate matter that displays similar seasonal shifts in contaminant concentrations. The benthic amphipod Diporeia hoyi resides near the sediment-water interface. Previous studies have suggested that settling phytoplankton material, especially lipid-rich diatoms, are an important food source to amphipods and important in the benthicpelagic coupling of organic carbon (Fitzgerald and

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Gardner 1993). During 1997, PCB body burdens within Diporeia were relatively low in April and May (13 ± 4 ng/g) and doubled by the end of summer (32 ± 2 ng/g)(Fig. 3A; top). This enrichment in PCBs and corresponding increase in lipid content may be related to incorporation of settling diatoms associated with the spring bloom that was recorded in May 1997 (McCusker et al. 1999). Average PCB burdens are significantly different (p < 0.05) between low lipid (< 2.0%) and high lipid (> 2.0%) Diporeia composite samples. In 1998 PCB burdens were relatively high from March through June, however it is uncertain if the increasing trend observed in August 1997 would have occurred in 1998, since no samples were collected during late summer. Average PCB concentrations in zooplankton were 30% higher in April of 1998 compared to April 1997 which might suggest higher seasonal PCB concentrations in Diporeia during 1998 as well. Toxaphene levels measured in Diporeia display no systematic trend throughout the season and are not correlated to shifts in their lipid content. These levels fluctuate from April through September, ranging from 8 to 29 ng/g wet weight. Average toxaphene levels in Diporeia are 18 ± 9 ng/g wet weight, significantly higher than the average in Mysis ( 5 ± 3 ng/g wet weight), but comparable to the observed bulk zooplankton levels (25 ± 12 ng/g wet weight). Seasonal Contaminants in Forage Fish Alewife (Alosa pseudoharengus) and bloater chub (Coregonus hoyi) are the predominant forage fish in Lake Michigan and compete for food resources (Crowder and Binkowski 1983). Alewife samples collected ranged in size from approximately 120 to 210 mm in length while bloater ranged from 74 to 260 mm in length. Both fish species were composited by month. As seen in Figures 4 and 5, PCB congener patterns were consistent within a species over the sampling season and both fish possessed higher concentrations of hexaand heptachlorobiphenyls. Alewife composites of lengths 160 to 210 mm were quantified for PCB and toxaphene concentrations from April through September 1997 and 1998 (Fig. 6A). In both years, measured alewife PCB burdens were highest in April (300 ng/g ww), and decreased through June and July (200 ng/g ww). In 1998 alewife PCB burdens increased from July to September in a trend similar to changes in their

FIG. 4.

PCB congener patterns normalized to total PCB level within alewife composites during the 1998 sampling season.

58 Stapleton et al.

FIG. 5.

PCB congener concentration normalized to total PCB levels within bloater composites during the 1998 sampling season.

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FIG. 6. Seasonal PCB (top) and toxaphene (bottom) concentrations in (A) alewife (size 120–200mm) and (B) bloater chub (size 200 to 260 mm) composites from Grand Traverse Bay 1997–1998. Error bars represent standard deviation of replicate samples. lipid content. Toxaphene changes followed a trend similar to PCBs. From April through June of both years toxaphene burdens decreased and then increased in late summer. Seasonal changes in alewife PCB burdens appear to reflect changes in their lipid content from April through September. Average PCB burdens between alewife samples with low (< 4%) and high (> 7%) lipid contents are significantly different (p < 0.01), suggesting that lipid dynamics affect PCB concentrations. Field studies conducted by Madenjian et al. (2000) also reported the same trend in seasonal alewife lipid fluctuations in Lake Michigan. Alewifes increase their lipid content in the fall as they build-up energy reserves to sustain them over the harsh conditions of winter (Flath and Diana 1985). During the winter alewives feed sparingly and rely upon lipid reserves for energy and then in the spring they began to feed more heavily. Lipid reserves are transferred to gonad growth in early

summer as alewives prepare to spawn. Both lipid content and PCB burdens decreased between May to August of both years sampled and may be related to spawning events during this period which are known to occur (Flath and Diana 1985). Spawning will act as a depuration pathway for fish as they release lipid-rich biomass (Miller 1993). Bio-energetics modeling of zooplanktivory by alewives in Lake Michigan has shown that 73% of the total annual consumption by alewife populations occurs between July and October, and 45% occurs in August and September alone (Hewett and Stewart 1989). This high consumption is also linked to higher growth rates in early fall (Stewart and Binkowski 1986). Increased feeding rates should expose them to higher concentrations of PCBs in their diet, however growth dilution should compensate for body burdens. This suggests that perhaps the assimilation efficiency of PCBs within alewife increases during dynamic shifts in lipid contents.

PCBs and Toxaphene in Lake Michigan The strong dependence upon lipid content for nutrition, the re-mobilization of lipid reserves for energy and spawning efforts, and observations of lipid to PCB correlation, suggest that alewife PCB assimilation is sensitive to lipid dynamics. PCB burdens in bloater composites were relatively consistent throughout the sampling periods in both years, except for June of both years when a 25% increase in PCB burdens was measured (Fig. 6B; top). Bloater chub spawn in the early spring, around February to March (Dr. Thomas Miller, personal communication) and therefore the effects of spawning on contaminant concentrations was not observed. Bloater composite samples measured for PCB concentrations in June were significantly higher (p < 0.025) than the composite samples collected the rest of the year. The lipid content of bloater was low, 2.2 ± 0.5%, and did not change significantly throughout the sampling season. Relative to other studies that have measured the lipid content of bloater in Lake Michigan (Hesselberg et al. 1990, Madenjian et al. 2000) these values are low and may indicate poor nutrition and growth requirements for bloater. The average bloater toxaphene concentration was 92 ± 32 ng/g wet weight, while alewife toxpahene burdens average 198 ± 70 ng/g. It was expected that there would be elevated toxaphene burdens in bloater relative to alewife, similar to the PCB burdens between the two species. However, this difference may indicate differential uptake and assimilation of toxaphene compared to PCBs between alewife and bloater. Correlating Diet to Contaminant Burdens Stomach content analyses was performed on alewife and bloater collected between April through September in 1997 to identify primary food items and determine seasonal changes in diet (Table 2). Alewives fed predominantly upon the zooplankton fraction of the food web, which consists primarily of Copepoda sp. and Cladocera sp. (Table 1). A minor component of Diporeia and Mysis was observed in the diets of alewife during the summer months, and in July and August 1997 a significant fraction from Bythotrephes invertebrates was found. Bythotrephes has only recently invaded the Great Lakes area. This crustacean is large and pigmented, making it a visual target for forage fish such as alewife and bloater. However the presence of a rigid tail-spine results in a gape-limitation on feeding by alewife and bloater smaller than 50 mm in size (Branstrator and Lehman 1996).

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TABLE 2. Diet analysis of alewife and bloater from Grand Traverse Bay during 1997 as a percentage of dry weight. Numbers in parenthesis following the month of sampling indicate the number of fish analyzed.

Zooplankton Mysis relicta Diporeia hoyi Bythotrephes Other

Zooplankton Mysis relicta Diporeia hoyi Bythotrephes Other

Alewife April May June (14) (0) (7) 87.0 4.9 66.0 28.5 13.0

0.5

April (30) 0.4 98.0

Bloater May June (3) (29) 0.2 0.4 98.6 28.6 34.8

1.6

1.2

36.2

July Aug. Sept. (15) (17) (15) 16.6 18.3 88.9 47.8 10.0 83.3 14.9 0.1 19.0

1.1

July Aug. Sept. (29) (30) (30) 0.1 1.0 0.8 30.2 40.1 85.5 65.8 6.3 5.9 0.1 0.6 0.2 3.8 52. 7.5

Previous studies have also found that alewives diet consists primarily of zooplankton most of the year with a minor contribution from amphipods and other invertebrates (Janssen and Brandt 1980), similar to this study. Zooplankton PCB concentrations decrease by 50 to 70% from spring through September (Fig. 3A; top). As mentioned previously, alewife are known to feed more heavily during the late summer/early fall, and despite low HOC concentrations within the zooplankton during these months, alewife still accumulate large body burdens. The stomach content analysis of bloater (Coregonus hoyi) reveals that a high proportion of their diet between April through September 1997 consists of Mysis relicta (Table 2). A significant contribution from the amphipod Diporeia hoyi is seen in midsummer. The increase in bloater PCB burdens evident in June 1997 and 1998 is coincident with the increase in Diporeia presence in the stomach content analyses (Table 2). This may indicate that bloaters are moving to deeper parts of the water column during the stratified summer months, perhaps to locate more abundant food sources. The inclusion of amphipods in the diet would be the most logical route by which bloaters assimilate greater concentrations of PCBs in their tissues. Mysis PCB burdens are very low and decrease throughout the summer (Fig. 3B; top). By contrast, amphipods are on average twice as enriched in PCBs relative to Mysis.

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To sustain the relatively high concentrations of PCBs in their tissues, bloaters must be feeding upon a more highly contaminated source than Mysis relicta throughout the summer to fall. Stable isotope analyses of nitrogen and carbon within tissues of Mysis and bloater also support the idea that bloaters are receiving their food and PCBs through a source other than Mysis, most likely amphipods and zooplankton (Stapleton et al. 2001a). Laboratory and field studies have both investigated prey selection of juvenile and adult bloaters, and have shown dynamic shifts in the diet of bloaters due to competition with alewife and changes in zooplankton community structure (Crowder and Crawford 1984, Crowder et al. 1987). If bloater continue to feed heavily upon Mysis, the rate of decline in PCB bloater burdens should be expected to increase, since Mysis are on average 50% less contaminated than their other prey. CONCLUSIONS This study examined the seasonal changes in PCB and toxaphene concentrations, total lipid content, and in the case of bloater and alewife, diet over the 1997 to 1998 sampling season. Although the measurements recorded here may not be average conditions for these food chain dynamics over larger time scales, they do suggest seasonal effects. Assessing the relative influence of lipid content versus diet on seasonal HOC burdens is difficult but in this study, seasonal changes were species specific. Bulk zooplankton and Mysis PCB burdens were positively correlated to changes in the suspended particulate matter PCB concentrations in the water. During these sampling seasons, alewife and Diporeia PCB burdens appear to be sensitive to lipid dynamics, while bloater PCB burdens were reflective of changes in their diet. However, the bloater in GTB did not experience any dynamic changes in their lipid content making it difficult to determine how sensitive PCB assimilation would be to lipid changes. Despite evidence suggesting that lipid content is not a variable in PCB body burdens among species (Stow et al. 1997), lipid content does appear to be influential in PCB assimilation over seasonal time scales, as we observed in this study. ACKNOWLEDGMENTS We would like to thank the following for their contributions to this paper: Dr. Thomas Coon and

Dr. Thomas Miller for their insight on fish ecology; Jeff McDonald of Indiana University for his guidance and assistance in toxaphene analysis; the captain and crew of the RV Shenehon for the use of their vessel and aid in collection of samples; Tom Callison and Erik Olsen of the Grand Traverse Band of Ottawa and Chippewa Indians for assisting in collection of alewife and bloater; Dr. Jeff Jeremiason for his continued support in this project, the USEPA STAR program and the Michigan Sea Grant program for funding, and all the members of the Baker Lab at the Chesapeake Biological Laboratory. This is the University of Maryland Center for Environment Science Contribution #3540. REFERENCES Borgmann, U., and Whittle, D.M. 1991. Contaminant concentration trends in Lake Ontario lake trout (Salvelinus namaycush): 1977 to 1988. J. Great Lakes Res. 17(3):368–381. Bowers, J.A., Cooper, W.E., and Hall, D.J. 1990. Midwater and epibenthic behaviours of Mysis relicta Loven: observations from the Johnson-Sea-Link II submersible in Lake Superior and from a remotely operated vehicle in northern Lake Michigan. J. Plankton Res. 12:1279–1286. Branstrator, D.K., and Lehman, J.T. 1996. Evidence for predation by young-of-the-year alewife and bloater chub on Bythotrephes cederstroemi in Lake Michigan. J. Great Lakes.Res. 22(4):917–924. Crane, J.L., and Sonzogni, W.C. 1992. Temporal distribution and fractionation of polychlorinated biphenyl congeners in a contaminated Wisconsin lake. Chemosphere. 24(12):1921–1941. Crowder, L.B., and Binkowski, F.P. 1983. Foraging behaviors and the interaction of alewife, Alosa pseudoharengus, and bloater, Coregonus hoyi. Environ. Bio. Fishes 8:105–113. ———, and Crawford, H.L. 1984. Ecological shifts in resource use by bloater in Lake Michigan. Trans. Amer. Fish. Soc. 113:694–700. ———, McDonald, M.E., and Rice, J.A. 1987. Understanding recruitment of Lake Michigan fishes: the importance of size-based interactions between fish and zooplankton. Can. J. Fish. Aquat. Sci. 44(Suppl. 2):141–147. DePinto, L.M., and Coull, B.C. 1997. Trophic transfer of sediment-associated polychlorinated biphenyls from meiobenthos to bottom-feeding fish. Environ. Toxicol. and Chem. 16(12):2568–2575. Eby, L.A., Stow, C.A., Hesselberg, R.J., and Kitchell, J.F. 1997. Modeling change in growth and diet on polyclorinated biphenyl bioaccumulation in Coregonus hoyi. Ecol. Applic. 7(3):981–990 Eck, G.W., and Wells, L. 1986. Depth distribution, diet,

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