Dietary Uptake from Historically Contaminated Sediments as a Source

Jun 17, 2010 - To determine the sources of PCBs to Bay fish and invertebrates, it was necessary to characterize and .... urban impacted area (25-27), ...
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Environ. Sci. Technol. 2010, 44, 5444–5449

Dietary Uptake from Historically Contaminated Sediments as a Source of PCBs to Migratory Fish and Invertebrates in an Urban Estuary ERIC J. MORGAN AND RAINER LOHMANN* Graduate School of Oceanography, University of Rhode Island, Narragansett, Rhode Island 02882

Received February 9, 2010. Revised manuscript received May 1, 2010. Accepted May 7, 2010.

Migratory fish and invertebrate samples were analyzed for polychlorinated biphenyls (PCBs) to study bioaccumulation in an urbanized estuary in the northeastern USA. Fish were also analyzed for 13C, 15N, and 34S ratios. Results from several approaches (stable isotopes, total PCB concentrations, congener ratios, and bioaccumulation factors, BAFs) suggested that the fish and invertebrates fell into two distinct dietary groups: the more planktonic butterfish and squid versus a benthic group composed of lobsters, scups, and crabs. Both benthic and pelagic fish obtained the majority of their PCB body burdens from the sediments. Lobsters seemed to have an additional uptake from sediment particles, as observed by an increase in highly chlorinated congeners’ bioaccumulation. BAFs were calculated relative to passive sampling-derived dissolved concentrations of PCBs. BAFs exceeded Kow values, implying that PCBs were accumulated beyond equilibrium partitioning with the water column. This was supported by comparison of chemical activity gradients, which suggested chemical activities of hexa- and heptachlorobiphenyls in biota exceeded those in water and porewater, but not for tetra- and pentachlorobiphenyls in squids and butterfish.

result was surprising. It could indicate that local factors caused the elevated concentrations of PCBs in fish, although a major PCB superfund site is located nearby at New Bedford Harbor. NB is a relatively small, heavily urbanized temperate estuary on the northeastern coast of the US, Rhode Island. It is characterized by a long history of pollution, including historical deposition of PCBs (7, 8). To determine the sources of PCBs to Bay fish and invertebrates, it was necessary to characterize and understand the potential for bioconcentration, generally defined as the presence of PCBs in tissue through uptake from water (3, 9). To this end, we utilized data from polyethylene (PE) passive samplers deployed in NB in a vertical array (surface air, surface water, bottom water) as part of a larger study to provide directly comparable measurements of PCB activity (10). As passive samplers rely on diffusion to accumulate analytes of interest, they sample only the fraction of PCBs that are freely dissolved and not the portion that may be sorbed to other matrices (11), such as dissolved or particulate organic carbon. Beyond simply measuring PCBs in biota, we opted to use stable isotopes to characterize their dietary sources, namely stable isotopes of carbon (C), nitrogen (N), and sulfur (S). We hypothesized that fish feeding in the water column (pelagic species) would display lower PCB concentrations than species feeding in/near the sediments (benthic biota). In contrast to previous studies in the Great Lakes, where fish cannot escape the influence of sediments (9, 12), biota in NB are migratory and are affected by “dilution” with cleaner ocean water. Furthermore, we hypothesized that benthic and pelagic species would be characterized by different PCB profiles reflective of their typical diets, which we characterized using stable isotopes. In summary, we undertook a major sampling and measurement campaign in the summer of 2006 to (i) determine the concentrations of PCBs in different migratory fish and invertebrates in NB; (ii) assess whether benthic and pelagic biota displayed different PCB body burdens and profiles; (iii) compare activities of PCBs in fish/invertebrates with those in atmosphere, water and sediments, which we derived using PE samplers, and (iv) understand the current sources of PCBs to fish and invertebrates in NB.

Methods Introduction Polychlorinated biphenyls (PCBs) are a class of ubiquitous hydrophobic organic legacy pollutants that were banned in the U.S.A. some 40 years ago and in 2001 by the United Nations Environmental Programme (1). Nonetheless, PCBs have been found to continue to bioaccumulate in organisms all over the planet. Coastal environments are particularly impacted as they represent a sink for PCBs (2). The number of variables controlling bioaccumulation, the enrichment of a contaminant in an organism relative to its environment from all routes of exposure, is considerable. The degree of bioaccumulation in any given organism is affected by temperature, lipid and protein content, size, age, feeding strategy, sex, depuration rates, and extent of metabolic or biotransformative processes (3-5). Fish in Narragansett Bay (NB), RI, have been found to consistently exceed safe-eating guidelines by the U.S. EPA (6). In light of the migratory nature of most fish in NB, this * Corresponding author. E-mail: [email protected]. Tel.: (401) 874-6612. Fax: (401) 874-6811. 5444

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Details on Narragansett Bay, fish, and invertebrate abundances during the study period, stable isotope and GCanalysis can be found in the Supporting Information. Target Species. We selected several demersal fish and invertebrate species based on their ubiquity, range of physiologies, diets, and commercial interest. Two schooling fish, Stenotomus chrysops (scup) and Peprilus triacanthus (American butterfish), were chosen, as they tend to dominate the landings of trawls during the study period (summer and fall) and reflected two different feeding strategies: S. chrysops preys mostly upon benthic invertebrates (13), whereas P. tiracanthus feeds mostly upon plankton (as a juvenile), gelatinous macrozooplankton (14), and the abundant ctenophore Mnemiopsis leidyi (15). Both fish demonstrate a seasonal inshore-offshore migrational pattern, coming into the Bay during the summer months as water temperatures warm (14). For comparison, we also chose Cancer spp. (crabs), Homarus americanus (American lobster), and Loligo pealei (long-finned squid) as they represented different phyla and a range of physiologies, and exhibited the seasonal inshoreoffshore migrational pattern (16, 17). 10.1021/es100450f

 2010 American Chemical Society

Published on Web 06/17/2010

Collection of Fish and Invertebrate Samples. Fish and invertebrate samples were collected on alternate weeks with PE deployment/retrieval from a research trawl conducted by URI-GSO from May to November of 2006. Fish were caught via an otter tow (a slow bottom trawl to monitor the abundance of demersal fish) in the West Passage of the Bay (41°26′55′′ N, 71°25′10′′ W) aboard the R/V Cap’n Bert (18). We analyzed 121 individuals from these selected species, resulting in 65 discrete samples (smaller fish were pooled for analysis; for details on fish sizes and weights, see Table SI 3 in the Supporting Information). Preparation and Deployment of PE Samplers. PEs were cut from commercial sheeting (Carlisle Plastics, Inc., Minneapolis, MN) with a thickness of 51 µm, yielding an ∼10 × 30 cm strip of ∼1-2 g each and pretreated as described elsewhere (10). PEs were deployed off a monitoring buoy near Quonset Point in the West Passage of NB, close to the site of the trawl (41°35.288′ N, 71°22.839′ W). PEs were deployed from May to November 2006, for an average period of 15 days, although deployment times of individual PEs varied from 11 to 22 days. For further information, see Morgan and Lohmann (10). Extraction of PEs. Prior to extraction, PEs were wiped clean with Kimwipes and 50 µL of an internal standard containing 13C-labeled PCBs (PCBs 8, 28, 52, 118, 138, 180, 209; 3 ng µL-1 in nonane) was added to the PEs. They were twice extracted in dichloromethane overnight; the resulting extracts were combined and concentrated to ∼1 mL on a rotary evaporator, solvent exchanged to hexane and concentrated to ∼50 µL. Five microliters of 2,4,6-tribromobiphenyl in nonane (15 ng µL-1), was added as an injection standard before analysis. Extraction of Fish and Invertebrate Tissues. Fish and invertebrate tissues were homogenized in a precleaned stainless steel blender. For fish less than 10 cm in length, the whole animal was homogenized. For larger fish, the bones, skin, and viscera were discarded, the rationale being that bones were not blendable, the skin often had organic matter (OM) and sediment on it and was considered a possible source of contamination (small amounts of OM and sediments could yield erroneously high PCB concentrations), and the gut of fish often contains unassimilated prey tissues (and in some cases sediment), which could be later egested and thus cannot be considered part of the body burden of the organism. Invertebrates with a carapace (lobsters, crabs) were dissected; the carapace was scraped clean and discarded. Fish yielding under 10 g of tissue were combined into a composite sample of several individuals to provide a more general indication of trends of interest (see Table SI 1 in the Supporting Information for general fish data and more details). Sediment and Porewater PE Experiments. Sediments were obtained from the study site with a grab sampler midway through the study period and incubated with passive samplers to derive the porewater activity of PCBs. Approximately 80 g of surface sediment was sealed in a 500 mL round-bottom flask with 400 mL of pre-extracted Milli-Q water, in triplicate. Each flask contained a precleaned PE strip (ranging from 0.1 to 0.5 g), as detailed in Lohmann et al. (19). Flasks were then foil-covered and placed into a modified metabolic shaker and agitated for 3 weeks at room temperature. Instrument Analyses and QC. Analysis for 29 PCBs was conducted on an Agilent 6800 gas chromatograph (GC) coupled to an Agilent 5973N mass spectrometer (MS) operated in the negative electronic ionization mode. In this study, we report the results for PCBs 52, 66, 101, 118, 138, 153, 187, 180, and 209. Physico-chemical Properties. We chose KOW values from the review by Li et al. (20) who presented a set of internally consistent physicochemical properties. Other partitioning

constants were derived and corrected for salinity and temperature as detailed in Morgan and Lohmann (10). Klip-w was estimated from KOW by the method detailed in ref 9 0.91 Klip-w ) 3.2KOW

(1)

Calculation of Activities and Bioaccumulation Factors. Bioaccumulation factors (BAFs) were calculated as the ratio of the PCB concentration in the organism’s tissue (Clip, in pg kg-1 lipid) to the freely dissolved concentration CW (pg L-1) in the bottom water BAF )

Clip Cw

(2)

where BAF is in L kg-1 lipid (9). Bioaccumulation here refers to the accumulation of contaminants in biota irrespective of the route of exposure, whereas bioconcentration is reserved for those cases in which the route of exposure is uptake from water. To easily compare the presence of PCBs between fish, invertebrates, and environmental compartments, we derived the PCBs’ chemical activities as a common reference state. PCB concentrations in tissue were converted to a hypothetical CW by assuming equilibrium with the water using the lipid-water partitioning coefficients (Klip-w) Cw )

Clip Klip-w

(3)

PCB concentrations in PE (from the bottom waters and sediment tumbling experiment) were converted to CW using the respective PE-water partitioning constants, KPE-W. All CW were normalized to the aqueous solubility (C sat w ) of the PCB congener, yielding hypothetical aqueous activities, a. This took the form of (9) a)

Cw sat Cw

)

Cphase

(4)

sat Kphase-wC w

where Cphase is the concentration in either PE or the tissue’s lipids in pg kg-1 (PE or lipid) and Kphase-w is the tissue/ PE-water equilibrium partitioning coefficient in L kg-1. For further details on the derivation of Cw from CPE, see the Supporting Information.

Results and Discussion Isotopic Evidence of Dietary Composition. δ13C values of the entire data set ranged from ∼ -14.0‰ to -18.5‰, a typical range for a temperate estuary (21, 22). Two groups of fish/invertebrates emerged based on their δ13C values (p > 0.05, two-tailed test): butterfish and squid on the one hand, and lobsters, crabs, and scups on the other hand (for details, see the Supporting Information, Figure SI 3). We interpret these two groups as separating those with planktonic-based diets (butterfish and squid) from benthic-based diets (lobster, crab, and scup). Mean δ15N values were highest for lobsters (17.8‰), followed by scup (16.8‰), with the other three species being ∼16‰. Results for N isotopes were not conclusive in discriminating between species. δ34S values served as a control to C and N isotopes, because sulfur isotopes have been found to fractionate only slightly with increasing trophic level (23). Butterfish and squid were found to be closer to the expected value for marine plankton (usually between -21 and 18‰, see the Supporting Information and ref 24), whereas results for scup, lobsters, and crabs were closer to benthic values (12, 25). Overall, results from the C and S isotope analysis suggest that the fish and invertebrates sampled in this study fell into two distinct groups, supporting what was expected given VOL. 44, NO. 14, 2010 / ENVIRONMENTAL SCIENCE & TECHNOLOGY

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FIGURE 1. Bioaccumulation factors for different congeners plotted as a function of the octanol-water partitioning coefficient, KOW. BAF (L/kg lipid) was calculated as [PCB] in pg/ kg lipid/CW in pg/L. Dashed line is the 1:1 line. PCB 209 is not plotted because it was not detected in the water column. Congener numbers are given in the gray boxes. their typical dietary composition: the more planktonic butterfish and squid versus a benthic group composed of lobsters, scups, and crabs. Bioaccumulation Factors. Typical concentrations of individual congeners in butterfish ranged from ∼0.1 to 30 ng/g dry wt (average 24 ng/g dry wt), from ∼0.05 to 80 ng/g dry wt in scup (average 91 ng/g dry wt), and from ∼0.2 to 90 ng/g dry wt in lobsters (average 140 ng/g dry wt; see Table SI 1 in the Supporting Information). Concentrations of most congeners in crab were typically higher than in other species, ranging from ∼0.5 to 185 ng/g dry wt (average 240 ng/g dry wt), and lowest in squid tissues ranging from ∼0.08 to 15 ng/g dry wt (average 26 ng/g dry wt). Concentrations in all fish and invertebrates were determined to be independent of time, temperature, and isotopic compositions over the course of the study. Bioaccumulation factors (BAFs), based on the dissolved concentrations derived from the PEs and lipid-normalized PCB concentrations were moderate to high for a coastal or urban impacted area (25-27), averaging on the order of 1 × 106 for PCB 52, 1 × 107 for PCB 66, 1 × 108 for PCB 101 and PCB 118, and 1 × 109 for PCB 153, PCB 138, PCB 187, and PCB 180 (see Table SI 6 in the Supporting Information). Wetweight BAFs (see Table SI 7 in the Supporting Information) were lower than results for PCBs in lake trout from the Great Lakes (26). We opted to normalize results to % lipids, as this is the fraction that generally contains the majority of PCBs. When plotted against the octanol-water equilibrium partitioning coefficient, KOW (Figure 1), lipid-normalized averaged BAFs exhibited a strong positive log-linear relationship for butterfish (r2 ) 0.993, p ) 1 × 10-7, n ) 8, R ) 0.05), squid (r2 ) 0.99, p ) 3 × 10-8, n ) 8, R ) 0.05), lobsters (r2 ) 0.98, p ) 2 × 10-6, n ) 8, R ) 0.05), crabs, (r2 ) 0.81, p ) 0.002, n ) 8, R ) 0.05), and scup (r2 ) 0.90, p ) 0.0002, n ) 8, R ) 0.05). In the entire data set, only one individual organism had r2 < 0.9 (a crab). Generally, this implies that bioaccumulation is a result of equilibrium partitioning with the water column if the BAFs are corrected for lipid content (9, 27). These results were surprising, given the many variables present in a field study such as this, particularly when one considers the migratory nature of these estuarine species. However, BAFs exceeded log KOW values by 1-2 orders of magnitude, implying an additional source of PCBs beyond equilibrium partitioning, most likely due to PCB biomagnification in the food chain. Finally, the BAFs confirmed previous trends seen in isotope data and PCB tissue concentrations such that BAFs of the “pelagic” dietary 5446

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FIGURE 2. PCB profiles for fish, invertebrates, and porewater (“sediment PE”). Prominent congeners are represented as the average fraction of the total; error bars represent 1 standard deviation.

grouping (butterfish and squid) were lower on average than those species identified as having a “benthic” diet (Figure 1). The comparison above is based on the assumption that octanol is a good model for the biota’s lipid composition. The lipid-water equilibrium partitioning coefficient, Klip-w, could be more useful for discussing the degree of equilibrium than KOW because it directly reflects the distribution of PCBs between lipids and water, rather than a proxy, octanol (see the Supporting Information, Figure SI 1). Klip-w values are lower than KOW values for the higher chlorinated congeners, leading to an interpretation of higher bioaccumulation than one would observe from comparing BAFs to KOW. This suggests that the Klip-w values we derived based on ref 9 might be too low and/or not appropriate for the range of organisms we covered in our study or that the highest chlorinated PCB congeners are strongly biomagnified. BAFs were also variable, with total ranges typically encompassing up to 2 log units for a given congener and fish, which is not too surprising in fast-growing migratory species. The BAFs derived in this study did not show the parabolalike shape that has been often observed in bioaccumulation studies, with a maximum at KOW ≈ 6 (e.g., ref 28). In contrast to previous studies, we used passive samplers that only sample the truly dissolved fraction of PCBs in the water column, and not the fraction of PCBs that are adsorbed to dissolved organic matter (DOM). Truly dissolved concentrations are likely significantly lower than results based on classical pump-operated filter-adsorbent sampling approaches. This would lead to enhanced BAFs, especially for the higher log KOW PCBs, which are more strongly associated with DOM. A similar reasoning was presented recently by Jonkers and van der Heiden (29). Additionally, elevated BAFs for higher chlorinated PCBs could result from biomagnification or the ingestion of sediment and/or particulate material, since the higher chlorinated congeners have lower diffusivities (9). The potential role of biomagnification leading to elevated PCB concentrations was also demonstrated by comparing the slopes of the relationship between KOW and BAF. Squids, butterfish, crab and scup had parallel slopes (2.4, 2.5, 2.5, and 2.5 respectively), while lobsters possessed skew relative to the others (3.1), indicating higher bioaccumulation at higher levels of KOW. Congener Profiles and Ratios. PCB profiles or signatures were established for each species by calculating PCB fractions. There was remarkable constancy both within and between species (Figure 2). In all captured fish and invertebrate specimens the hexachlorobiphenyl PCB 153 was at the highest concentration, and hexachlorobiphenyls dominated the homologue groups.

FIGURE 3. Average fractions of PCB congeners 52 and 209, calculated as [52]/([52] + [209]) for different species of fish and invertebrates, as compared to values obtained from bottom water PEs, the PE tumbling experiment (“Sed PE”), and a sediment extraction (“Bulk Sed”). Error bars represent single standard deviations. Of particular interest was the regular detection of PCB 206 and PCB 209 in all fish and invertebrate specimens, two unusual congeners found in only trace levels in Aroclors with a degree of chlorination below 1262 (7). Indeed, PCB 209 is sometimes used as a surrogate or internal standard in the extraction of PCBs from tissues and other matrices (30-32). The presence of these congeners in the Bay has been detected for some time (33) and has been linked to historical contamination of sediments from local industry (7). On the basis of our results, it seems that these two congeners might be a useful tracer of PCBs in NB and could be used to identify migrants when offshore, for instance. Neither PCBs 206 or 209 were ever detected in the PEs suggesting that their passive (diffusive) uptake by biota would be insignificant relative to their ingestion with particles/food. Hence we assumed that PCB 209 could be used as an indicator of sediment ingestion-whether direct or through a dietary source-when found in tissues. The ratios or fractions between different PCB congeners have been utilized by other authors as tracers of food web phenomena in fish with excellent success (34). As PCB 153 is not readily metabolized and was found to be the dominant congener (35, 36), we made comparisons of its relative concentration to other prominent congeners. The ratios of 153:118, 153:138, 153:180, 153:187 and 153:209 showed no appreciable difference between species. This was interpreted to mean that penta-, hexa- and heptachlorobiphenyls were not only supplied by the same source, but underwent similar (slow) rates of biotransformation/depuration. The similarity in PCB profiles between available PCBs in the sediment, the fish, and invertebrate species considered in this study suggests a common source of PCBs, presumably the PCBs residing in the sediments. Fraction of PCB [52]/([52] + [209]). We also examined the ratio of two congeners, PCB 52 and PCB 209 in fish and invertebrate samples. We calculated this as a fraction, [52]/ ([52] + [209]). This approach was able to resolve the different species into three groups: butterfish (average fraction of 0.8) and squid (0.8), statistically indistinguishable from one another (Mann-Whitney U test, two tailed test) which had higher relative concentrations of PCB 52. Crabs (0.6) and scups (0.7) were not statistically different from one another having very low concentrations of 52 and higher concentrations of 209 (Figure 3). Finally, there were the lobsters (0.3), which were statistically different from all of the other species except crabs. The [52]/([52] + [209]) of all species in this study were in-between values of the abiotic reservoirs: A fraction close to 1 for the water column, at the other extreme

FIGURE 4. PCB profiles for passive samplers deployed at the study site. Congeners are represented as the average fraction of the total; error bars represent single standard deviations. Data from ref 10.

a fractional value of 0.3 for bulk sediment, with the sediment porewater displaying a value of 0.7 (Figure 3). We suggest that the higher fraction of [52]/([52] + [209]) in butterfish and squid reflect their more pelagic-based diet, as indicated by the similarly elevated fraction of PCB [52]/ ([52] + [209]) in bottom water PEs (Figure 3). Butterfish and scup are both schooling fish of similar size and habitat, yet differ in PCB concentrations and fractions due to dietary composition and feeding strategy. The other extreme are lobsters that align closely with the fraction of the bulk sediments (Figure 3), with crab and scup displaying [52]/ ([52] + [209]) values in-between sediments and bottom water. It is interesting to note the difference in PCB profiles between the PEs and the fish/invertebrates and sediment. The bottom waters exhibited a profile that showed a decline in relative abundance with degree of chlorination, instead of the maximum at hexachlorobiphenyls (Figure 4). It should also be noted that the congener profile one would expect to see based on the diffusive uptake of PCBs into a hydrophobic matrix, such as PE, and biota should be the same if bioconcentration was the main route of exposure. This has been suggested by numerous authors and is one of the major rationales for employing passive sampling in bioaccumulation studies (37). The profile of bioavailable PCBs (as measured in the PEs) did not match the profiles detected in the five species analyzed in this study. We hence conclude that bioconcentration of PCBs from the water column is insufficient to account for the PCB body burdens of fish and invertebrates with the exception of the tetrachlorinated PCBs, for which gill exchange dominates uptake and depuration. Similar results have been observed by Moermond et al. (38). Prest et al. (39) also found a discrepancy between the profiles of PCBs as measured by semipermeable membrane devices (SPMDs) and mussels, but attributed it to differences in uptake kinetics; this was later shown to be erroneous by the work of Verweij et al. (37) who found some agreement between SPMDs and caged carp. In fact, fish and invertebrates’ congener profiles closely matched that of the sediment, particularly that of the porewater (see Figure 2). This is strong evidence for the sediments being the source of PCBs to Bay fish. Yet this must be weighed against the difference in the [52]/([52] + [209]) fraction between porewater, as was measured in the PE experiment, and the bulk sediment extractions (Figure 3 and Table SI 2). Lobsters exhibited a PCB profile which more closely matched that of the bulk sediment extractions, whereas crabs, scup, butterfish, and squid more closely matched the PE-derived profile. A likely explanation is that the dietary sources (both the pelagic and benthic community) VOL. 44, NO. 14, 2010 / ENVIRONMENTAL SCIENCE & TECHNOLOGY

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FIGURE 5. Chemical activities (a) derived for fish and invertebrates and plotted against a given congener’s KOW. The solid line displays the upper limit for PCB congeners’ a in the porewater, with lower a present in bottom, surface waters, and atmosphere as derived from the PEs (not shown).

of scup, butterfish, and squid are dominated by desorbed PCBs from the sediment/particulate fraction of PCBs. These three species do not directly ingest the sediments/particulate fraction themselves, whereas lobsters (and potentially crabs) do (e.g., ref 38). To resolve the issue, further direct study of prey species in the Bay is warranted, which would also aid in directly determining evidence for biomagnification in the Bay’s food chains. Activity Gradients and the Potential for Transfer. One of the advantages of passive sampling is that it allows for direct comparisons of the PCB’s chemical activities between different media (e.g., water, air, sediment etc.). A more detailed discussion of PE-derived activities in Narragansett Bay can be found in Morgan and Lohmann (10). We detected activity gradients of PCBs in the Bay from bottom to surface, and from water to atmosphere, which should be balanced by fluxes of PCBs to establish equilibrium. Similarly, gradients of PCB activities between living organisms and their surrounding should be eliminated by chemical fluxes given efficient exchange across the biota-water interface. As evidenced by biomagnification in aquatic food webs, and supported by theoretical work (e.g., ref 40), this is not always observed. To better understand the gradients driving diffusive fluxes, we calculated the chemical activity of each congener for fish and invertebrates. This number represented the lipid normalized tissue concentrations converted to a hypothetical aqueous concentration using a given congener’s Klip-w normalized to its aqueous solubility (eq 4). These were then compared to the PCB’s chemical activities in sediment porewater, air, surface, and bottom water, as derived from the PEs (Figure 5). On average, the activity gradients were from (low to high): Air < bottom waters < surface waters < surface sediments < fish for all hexa- and heptachlorobiphenyls. For tetra- and pentachlorobiphenyls, squids and butterfish had lower activities than the abiotic reservoirs. Surface, bottom water, and sediments were on average close to equilibrium for the less chlorinated congeners. For these abiotic reservoirs, as the degree of chlorination increases, the degree of disequilibrium increased. Fish and invertebrates showed a similar trend, albeit lessened, of increasing disequilibrium with increasing degree of chlorination. Thus, fish and invertebrates exceeded their potential to receive higher chlorinated PCBs from the Bay, a requisite for “true” bioaccumulation (9). For these species, the dominating route of exposure is dietary or through the ingestion of sediments and particles. In this case, PCB desorption from particulates in the fish/invertebrate’s 5448

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gut will determine bioaccumulation, not uptake of dissolved PCBs from the water column (40). Our results offer some suggestions for further bioaccumulation work in estuaries. Passive samplers, in our case PE, were useful for understanding bioaccumulation, as they provided a time-averaged easy quantification of the available fraction of PCBs in the sediment and water column, facilitating BAF calculations. Passive samplers also offer a means of verifying whether the often observed hydrophobicity cutoff in BAFs is due to errors in adequately determining dissolved concentrations using active sampling approaches. PEs also enabled an activity comparison, which suggest that the heaviest PCBs displayed true bioaccumulation, i.e., PCB activities in biota > water column. Porewater measurements were useful in establishing matching profiles between sediments and most species-implying sediments/their desorbing PCBs as the likely cause for PCB bioaccumulation in biota in NB. Indeed, our data imply that much like in the Great Lakes, historically contaminated sediments continue to be the dominant source of PCBs to biota in partially wellmixed NB, and most likely in other shallow estuaries with a legacy of PCB contamination.

Acknowledgments Kelly Henry, Tom Puckett, and Jeremy Collie kindly helped us to obtain samples from the GSO fish trawl. Mark Cantwell and Becky Robinson assisted with stable isotope analysis, and Dave Adelman with lipid analysis. Funding for sulfur analysis came from the GSO Alumni Association and The Atlantic Center for the Environment and the Quebec/ Labrador Foundation. We thank the anonymous reviewers for their constructive comments.

Supporting Information Available Details on biota preparation and their analysis, the study site, and additional tables and figures (PDF). This material is available free of charge via the Internet at http:// pubs.acs.org/.

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