Article pubs.acs.org/est
Trophodynamic Behavior of Hydrophobic Organic Contaminants in the Aquatic Food Web of a Tidal River Mohammed A. Khairy,†,‡ Michael P. Weinstein,§ and Rainer Lohmann*,‡ †
Graduate School of Oceanography, University of Rhode Island, Narragansett, Rhode Island 02882, United States Department of Environmental Sciences, Faculty of Science, Alexandria University, 21511 Moharam Bek, Alexandria, Egypt § Center for Natural Resources Development and Protection, New Jersey Institute of Technology, Newark, New Jersey 07102-1982, United States ‡
S Supporting Information *
ABSTRACT: The bioaccumulation and biomagnification of sediment-bound hydrophobic organic contaminants (HOCs) are of major concern for environmental and human health. In dynamic estuaries, HOCs can be taken up from sediments, porewater, or the overlying water column concentrations directly or via the diet. The transfer of HOCs including polycyclic aromatic hydrocarbons (PAHs), polychlorinated biphenyls (PCBs), and polychlorinated dibenzo-p-dioxins/ furans (PCDD/Fs) to resident/migratory biota was investigated in 11 finfish species and blue crabs (Callinectes sapidus) in the Passaic River estuary. Concurrently, passive samplers were deployed to assess porewater and overlying water column concentrations. Biota were assigned to three trophic levels based on their tissue 15N isotope values and published life history strategies. There were no significant differences in trophic magnification factors (TMFs) calculated based on life-history scenarios, implying that the migratory species, mostly juveniles, had equilibrated with in situ sources of pollutants at the time they were sampled. Bioaccumulation factors and TMFs were >1 for most PCBs and tetra- and penta-CDD/DFs, indicating that they underwent biomagnification in the food web. All PAHs, PCB 11, and other lower chlorinated PCBs and PCDD/Fs did not magnify. Results from the analysis of HOC profiles implied that biota accumulated HOCs from sediments, porewater, and diet but not from overlying water.
■
INTRODUCTION
By combining active and passive measurements we can begin to address whether it is the ingestion of the contaminated sediments directly that is causing the trophic enrichment of HOCs in the foodweb, or whether porewater, water column, and diet are also involved as key matrices. Studying the fate and transport of contaminants in highly dynamic coastal estuaries, however, is confounded by the observation that some biota are only transient members of the estuarine fauna, further complicating foodweb and HOC transfer dynamics. Here, we investigated the trophic transfer and biomagnification of HOCs in the oligohaline-fresh portion of the tidal Passaic River estuary, a tributary of the Hudson River Harbor complex, extending from the Dundee Dam (river km 29) to its entrance at Newark Bay, New Jersey, USA (river km 0). We deployed passive samplers in the overlying water column and used them to derive porewater concentrations and profiles of sedimentary HOCs. This was combined with extensive sampling of sediment and nekton to establish the trophic position of targeted finfish and blue crabs (Callinectes sapidus)
The transfer of hydrophobic organic contaminants (HOCs) from sediments into aquatic biota is of global concern especially where human activities have resulted in highly elevated concentrations of pollutants in the ecosystem. Depending on the level of lipophilicity and resistance to metabolism, some HOCs can biomagnify in fauna at increasing trophic levels resulting in higher concentrations in top predators. 1,2 Consumption of the latter also poses a threat to human health.3 The results of previous studies have established the trophic transfer (bioconcentration, bioaccumulation, and biomagnification) of HOCs in lakes and coastal waters where human populations and industrial activities predominate.1−10 In these settings, coupling to sediments is the likely driver for the transfer of HOCs into aquatic food webs. Yet apportioning the exact sources of HOCs (i.e., uptake from overlying water, porewater, diet or sediment ingestion) remained elusive so far. More recently, passive sampling approaches have enabled probing porewater concentrations and profiles of HOCs directly (and those of the overlying water column).11−13A great body of literature has emerged based on passive sampling, teasing apart the fraction of sediment-bound contaminants that are actually bioavailable.11,14,15 © 2014 American Chemical Society
Received: Revised: Accepted: Published: 12533
June 13, 2014 September 30, 2014 October 1, 2014 October 1, 2014 dx.doi.org/10.1021/es502886n | Environ. Sci. Technol. 2014, 48, 12533−12542
Environmental Science & Technology
Article
by using 15 N stable isotope values of their muscle tissue.1,3,5,16−23 Stable isotopes of carbon and sulfur were also used to address potential dietary sources from primary producers.24 Historically, the aquatic environment of the lower Passaic River and estuary was severely degraded in the late 19th and early 20th centuries by industrial and municipal waste disposal in the Newark, New Jersey, metropolitan region.25 Elevated concentrations of polycyclic aromatic hydrocarbons (PAHs), polychlorinated biphenyls (PCBs), chlorinated pesticides, chlorinated herbicides, and heavy metals were detected in sediments, water, and biota collected from the Hudson River Estuary (including the Passaic portion)26−30 that have consistently been among the highest values measured at US sites.31 The region was also heavily contaminated with polychlorinated dibenzo-p-dioxins and furans (PCDD/Fs) including the highly toxic 2,3,7,8-TCDD congener28,32,33 in the region adjacent to the former Diamond Alkali pesticide manufacturing facility (river km 5.6) in Newark, NJ (1948− 1969).32 Due to the high sedimentary concentrations of PCDD/Fs, this site was added to the U.S. EPA Superfund list in 1984 and is currently undergoing a two-phase remediation effort that includes removal of 153,000 m3 of sediment via dredging.34 The Superfund program recently proposed extending remedial dredging to the entire lower 13 kms of the Passaic River. Although concentrations of PCDD/Fs have greatly decreased in sediments in the estuary over time,28,33 marine organisms collected from the Passaic and nearby locations have continued to exhibit high PCDD/Fs body burdens.35 Contamination of fish with PCDD/Fs, metals, and other organic pollutants prompted the NJ Department of Environmental Protection (NJDEP) to issue fish, shellfish, and blue crab consumption bans for all of the lower Passaic River and estuary.36 Iannuzzi et al.37 suggested that conventional biota-sediment accumulation factor (BSAF) models to predict body burdens were not a reliable way of predicting concentrations of HOCs in resident biota. Additionally, Friedman and Lohmann34 concluded that porewater and bottom water concentrations of PCCDD/Fs in the estuary were better predictors of concentrations in benthic species than sediment concentrations. This suggests that the Passaic River continues to discharge dissolved PCDD/Fs and possibly other HOCs that are available for bioaccumulation. A major question driving this work was to assess how important historically contaminated sediments were as a source of HOCs to taxa, as opposed to ongoing discharges of pollutants into the Passaic River. In the present study, we investigated the bioaccumulation and biomagnification of HOCs in 11 finfish species and the blue crab, Callinectes sapidus, collected from the fresh-brackish portion of the Passaic River estuary. First, we developed a conceptual framework for the Passaic River estuary food web using tissue concentrations of the three stable isotopes. Once nekton were assigned to their respective trophic positions, our further aims were to (i) determine the concentrations of PCDD/Fs, PCBs, and PAHs in fish and blue crab tissues with different feeding strategies and estimated trophic position including taxa that are marine transients (the latter, however, are generally resident during their first year of life in the estuary, often displaying substantial site fidelity38−41), (ii) assess whether benthic and pelagic biota displayed different body burdens and profiles of HOCs and whether these pollutant concentrations stemmed from sediment, porewater, diet, or
overlying water, and (iii) assess the extent of trophic transfer and biomagnification (or biodilution) of these HOCs.
■
MATERIALS AND METHODS Samples Collection, Extraction, Analysis, and Quality Control. Detailed description of the sampling and chemical analysis methodologies, preparation of the LDPE passive samplers, stable isotope analysis methods, and quality control data are given in the Supporting Information (SI); a summary description is given below. Calculations of the freely dissolved concentrations of HOCs based on LDPE are described in the SI. Nekton collected as target species in this study were selected to represent different life history strategies and trophic positions. Feeding strategies were further classified as “benthic”, “bentho-pelagic”, and “pelagic” based on feeding position in the water column according to recorded stable isotopic data for nekton and plants presented in our previous work and by a general review of the literature.40,41 For purposes of this study, blue crabs were considered to be benthic species although they are highly mobile and can sometimes be found swimming in the water column. Marine transients whose young-of-year are generally estuarine resident 42 included juvenile Morone saxatilis (∼100−300 mm FL43), juvenile Dorosoma cepedianum, Menidia menidia, and taxa that are typically year-round residents of the estuary or freshwaters - Callinectes sapidus, Fundulus heteroclitus, Fundulus diaphanus, Lepomis gibbosus, Lepomis macrochirus, Hybognthus regius, Esox americanus, Morone americana, and Anguilla rostrata (prespawning stages). All specimens were collected during several weekly sampling events in AugustNovember, 2011 at three locations (Figure S1): (i) a site above the Dundee Dam (river km 28.0) that served as a “reference” station above the main limits of contamination in the lower tidal River; (ii) lower Riverside Park (river km 16.1), and (iii) the Port Authority of NY&NJ Rail Maintenance Yard (river km 7.4). The downstream locations were established as tidal freshwater and brackish (oligohaline) sampling sites, respectively (Figure S1 and the SI for more detail). Passive LDPE samplers were deployed at six different locations along the lower Passaic River covering the region from the Dundee Dam to Newark Bay (Figure S1). Water samplers were fastened to an anchored rope and suspended in water ∼1−2 m below the surface. Six sampling campaigns (∼2 months each) were performed during September, 2011 through November, 2012 (Table S1). LDPE samplers were extracted and analyzed for PAHs and PCBs according to Khairy and Lohmann.44,45 For PCDD/Fs analysis, extracts were passed over an activated carbon column using U.S. EPA method 161346 with some modifications. Homogenized fish tissues were analyzed for PAHs by methods describe in Wretling et al.47 Extraction and cleanup of tissues for the analysis of PCBs and PCDD/Fs was performed according to the U.S. EPA method 161346 with modifications. Details on the analysis are given in the SI. Procedural blanks, field blanks (LDPE), matrix spikes, and duplicate samples (20% of the total samples) were included with each sample batch and were carried throughout the entire analytical procedure in a manner identical to the samples. PAHs were detected in the blanks, and samples were corrected for blanks. Recoveries of the surrogate standards in the LDPE and biota samples generally ranged from 72 to 104%. Matrix spikes recoveries were always >90% and 1 indicates that contaminants are biomagnifying, whereas values 15‰) were observed in larger Anguilla rostrata (>120 cm) and Morone saxatilis (28−33 cm) (third level), suggesting that both species were the top (or tertiary) predators in this food web. The only “surprise” in this study was the location of the Hybognathus regius, another omnivore that we predicted a priori to be at or near the level of Fundulus heteroclitus but turned out to occupy a position about a trophic level higher. Two potential reasons for this observation are the copious amounts of sediment ingested by this species while feeding and the observation that H. regius also ingests more animal matter than usually reported in the literature.56 Trophic positions for all organisms calculated using δ15N values according to eq 3 are given in Table S8. Fundulus heteroclitus, the base of our food web, had a value of 2. Trophic positions of the remaining nekton samples varied from 2.4 (Dorosoma cepedianum) to 4.0 (Morone saxatilis, 28.2−32.5 cm). As expected, results for S and C stable isotopes were generally not conclusive in discriminating between species’ trophic positions but were useful for separating allochthonous and autochthonous sources of primary producer inputs to the system (see the SI and Figure S4 for more details).
C lip CW
(2)
Bioaccumulation here refers to the accumulation of contaminants in biota irrespective of the route of exposure, whereas bioconcentration refers to the uptake from water only. Stable Isotope Composition. Stable isotope analysis of finfish and blue crab tissue (muscle samples or whole smaller specimens) was performed according to Weinstein et al.52 Although primary producers were not sampled in the Passaic River estuary, the authors have collected extensive data on benthic microalgae, phytoplankton as suspended particulate matter (SPM), smooth cordgrass (Spartina alternif lora), common reed (Phragmites australis), and other C3 plants. These data are derived from numerous estuaries in the region including the Hudson River, Mullica River, and Delaware Bay.36,42,52,53 Their 15N isotopic signatures form the baseline for this study, and as noted in Figure S2, there is relatively little distinction among 15N signatures in these plant taxa. Because δ14N/ δ15N ratios in consumers increased about 3.0−4.0‰ relative to prey eaten,54 the fractionation of N in the food web was used to approximate the trophic position of constituent species. In addition, 13C and 34S tissue concentrations allowed for additional water column nutrient source considerations that reflected inputs of these nutrients along the long axis of the estuary, vegetation type (13C), and benthic (sulfide) or water column (sulfate) sources of 34S. We examined feeding habits of all species sampled herein, and because they were considered omnivores consuming both vegetation and animal matter,55 we assumed a priori that the resident species Fundulus heteroclitus would comprise the base of the local food web. Similarly, we predicted the relative trophic levels of the other taxa examined, prior to constructing the food web based on tissue isotope values, and noted exceptional congruence between our predictions and actual trophic status (with one exception, see below). For each individual used in the study, trophic position was determined by the following relationship:54 trophic position = 2 +
δ15 Nconsumer − δ15 NFundulus heteroclitus 3.4 (3)
The trophic magnification factors (TMFs) were derived from the slope of the plots of natural log concentrations (lipid normalized) versus TP. The slope b was used to calculate TMF 12535
dx.doi.org/10.1021/es502886n | Environ. Sci. Technol. 2014, 48, 12533−12542
Environmental Science & Technology
Article
concentrations of the pelagic species (27 μg/g lipid) collected were comparable to those of the benthic fish (24 μg/g lipid) (Figure 1). Concentrations of ∑29PCBs and ∑20 PCDD/Fs ranged from 3.0 to 80 μg/g lipid and 2.0−31 ng/g lipid, respectively. Similar to PAHs, average PCB concentrations in benthic feeders (8.0−24 μg/g lipid) were slightly higher than tissue concentrations of bentho-pelagic feeders (6.0−17 μg/g lipid) at river km 16.1 and above the dam. Average concentrations of PCBs (at river km 7.4) and PCDD/Fs (at the three sampling sites) were higher in the bentho-pelagic compared to benthic taxa (see Figures S5 and S6 and SI for more information on the concentrations of PAHs, PCBs, and PCDD/Fs in the nekton and water samples). Overall, there was no consistent difference between sampling sites below the dam, implying species were locally mobile in the lower Passaic River. Source of HOCs to Nekton. Profiles of PAHs, PCBs, and PCDD/Fs in the benthic, pelagic, and bentho-pelagic nekton were compared with profiles of the freely dissolved fraction of each pollutant class (obtained from passive samplers) and profiles of porewater and sediments collected from the same locations as the nekton (Khairy and Lohmann, Graduate School of Oceanography, University of Rhode Island, unpublished data) (Figure 2). There was an overall similarity in the profiles of PAHs, PCBs, and PCDD/Fs between the benthic, pelagic, and bentho-pelagic nekton at the three sampling locations. Additionally, profiles were in close agreement between nekton and the freely dissolved fraction and/or porewater for the lower molecular weight PAHs (Figure 2 a-c). However, the detection of 5- and 6-rings PAHs, 7−10 chlorinated biphenyls (Figure 2 d-f), and 4−8 chlorinated dioxins/furans (Figure 2 g-i) in all the nekton was of particular interest since all these contaminants were either not detected or at very low concentrations in the freely dissolved fraction and porewater (Figure 2 a-i). These higher molecular weight PAHs and higher chlorinated PCBs and dioxins/furans were detected in the sediment samples at relatively high concentrations. An overall similarity was observed between profiles of PCBs and PCDD/Fs in the nekton and sediments suggesting that the uptake of pollutants from sediments is significant in the Passaic River either directly (as in case of benthic species) or through a dietary source. For the three classes of pollutants, sediment concentrations at the two downstream sites were significantly higher than concentrations observed in sediments from above Dundee Dam (Friedman Repeated measures ANOVA on Ranks, p < 0.001), which was similar to trends in tissue concentrations. This finding together with the similarity in pollutants profiles in sediments and nekton suggested that sediments continue to be a source of pollutants to the biota, even at higher trophic levels. To gain additional knowledge on the sources of organic pollutants in nekton, a MLR analysis was performed. The output of the MLR (see Figure 4) indicated that the uptake of the organic pollutants in Morone americana, Anguilla rostrata (56−110 cm), and Lepomis gibbosus (river km 16.1) is mainly from a dietary source, which identified 67−89% of the total variability in tissue concentrations. Similarly, dietary sources represented the major source of organic pollutants (53−94%) in Morone saxatilis, Lepomis macrochirus, L. gibbosus (both collected above the dam), Anguilla rostrata (28−45 cm), and Fundulus diaphanus (above dam and river km 16.1), followed by either porewater (22−40%), sediments (17−20% in Anguilla rostrata), or the freely dissolved fraction (6.0−37% in Fundulus diaphanus). In all the other species, including blue crab,
HOC Concentrations in Nekton. Concentrations of HOCs in the biota normalized to lipid content are shown in Figure 1. We observed the highest concentrations of all
Figure 1. Total concentrations of PAHs (a), PCBs (b), and PCDD/Fs (c) in biota samples collected from three different locations along the lower Passaic River. Blue crab collected from river km 16.1 was plotted separately from the other benthic species.
pollutants in Callinectes sapidus (blue crab). Additionally, detected concentrations of all pollutants in benthic and bentho-pelagic samples collected from above Dundee Dam (nontidal fresh water) were significantly lower (Kruskal−Wallis One Way ANOVA, p < 0.05) than samples collected from the two estuarine sites. High PAH (∑45PAHs) concentrations were generally observed in all the investigated species ranging from 1.0−71 μg/g lipid. Tissue PAH average concentrations were generally higher in the benthic species (7.0−24 μg/g lipid) compared to the bentho-pelagic species (2.0−8.0 μg/g lipid) at the three sampling sites. At river km 7.4, average tissue 12536
dx.doi.org/10.1021/es502886n | Environ. Sci. Technol. 2014, 48, 12533−12542
Environmental Science & Technology
Article
Figure 2. Profiles of PAHs (a-c), PCBs (d-f), and PCDD/Fs (g-i) in nekton, water, porewater, and sediments collected from the lower Passaic River. Pelagic fish was only collected from river km 7.4; C-Nap: alkylated naphthalenes; DBT: dibenzothiophene; Flr: fluorene; Phn/Ant: phenanthrene/ anthracene.
sediments and porewater were better predictors of the tissue concentrations and explained 40−82% of the total variability in the data (Table S9). Diet could still be an important uptake source for the latter nekton, but we lack data for the levels of organic pollutants in their food items. As shown in Figure 2, different profiles of PAHs, PCBs, and PCDD/Fs were observed in the freely dissolved fraction, porewater, nekton, and sediments. The freely dissolved fraction and porewater exhibited profiles that showed a decline in relative abundance with degree of chlorination (PCBs and PCDD/Fs) and molecular weight (for PAHs), which was not observed in the nekton and sediments. If bioconcentration was the main route of exposure, similarity between profiles of the freely dissolved fraction and nekton would be expected. Based on the profiles and the output of the MLR, we hence conclude that sediments and food should be considered the major sources of organic pollutants in the Passaic River estuary, whereas overlying water was a minor source. This has the obvious implications that removing contaminated sediments will go a long way in reducing the transfer of HOCs into the food-chain. Benthic and pelagic species exhibited PCB and PCDD/Fs profiles which more closely matched that of the bulk
sediment and porewater. A likely explanation is that the dietary sources (both the pelagic and benthic community) are dominated by desorbed pollutants from the sediment/ particulates fraction.19 Except for blue crab, mummichog, and silvery minnow, all the species investigated do not directly ingest the sediments/particulate fraction. To resolve the issue, further direct study of prey species and other food items in the Passaic River should be performed. Bioaccumulation Factors. We derived bioaccumulation factors (BAFs) from the ratio of lipid-normalized concentrations of the target analytes and their dissolved concentrations derived from the LDPEs (see Tables S10−S12). Calculated BAFs for PAHs ranged from 2.2 × 104−8.6 × 106 in pelagic fish, 2.5 × 103−2.1 × 107 in bentho-pelagic fish, and 1.5 × 103− 1.5 × 107 in benthic fish and Callinectes sapidus (Table S10). PAH BAFs in the benthic species (Callinectes sapidus, Hybognathus regius, Fundulus heteroclitus) and Menidia menidia (pelagic) collected from the two downstream sites were significantly greater (Kruskal−Wallis One Way ANOVA, p < 0.05) than in all the other species. BAFs were plotted against lipid−water partition coefficients (Klip‑w) calculated using eq 1 (Figure 3a). Except for Morone saxatilis (a top predator), all the 12537
dx.doi.org/10.1021/es502886n | Environ. Sci. Technol. 2014, 48, 12533−12542
Environmental Science & Technology
Article
Figure 3. Bioaccumulation factors (L/kg lipid) for PAHs (a), PCBs (b), and PCDD/Fs (c) plotted against lipid−water partitioning coefficient (Klip‑w). Error bars represent the standard deviation of the combined pooled samples.
data were fit to a cubic polynomial curve with r2 values ranging from 0.25 to 0.70 (p < 0.05). The lower molecular weight PAHs seemed to be linearly related to log Klip‑w ≤ 4.1 (log KOW = 4.0) and BAFs were 1−2 times higher than Klip‑w. This is possibly related to (i) the greater solubility and the lower biotransformation efficiency of LMW PAHs in fish causing them to be more bioavailable57−59 and/or (ii) uptake kinetics are faster than depuration, leading to apparent accumulation at contaminated sites.57 Log BAFs then tended to level off for PAHs with 4.1 < log Klip‑w < 5.4. This was previously observed in other studies16,54 and could be attributed to the higher biotransformation rates of larger PAHs in fish compared to the LMW ones60,61 although it varies widely among the different species.58 Finally, a linear increase for PAHs with log Klip‑w > 5.4 (log KOW = 5.3) was observed in benthic and pelagic species, an observation that might be the result of (i) the truly dissolved HOC concentrations measured by the passive samplers, which are significantly lower than results based on conventional water sampling techniques leading to higher BAF values especially for the higher molecular weight PAHs and (ii) ingestion of sediment particles (benthic feeders) and contaminated particles from the water column (pelagic species)19,58 (see the SI for more details). However, this linear increase in the higher molecular weight PAHs was less obvious at higher trophic levels; i.e., in Morone saxatilis, Anguilla rostrata, and M. americana, which also displayed lower BAFs compared to species at lower trophic levels (Table S10). This suggests that bioaccumulation was less important and/or biomagnification was likely absent. This
observation was probably related to the higher biotransformation rates observed in species located at higher trophic levels.58 Calculated BAFs for PCBs and PCDD/Fs (Tables S11 and S12) ranged from 2.0 × 103−2.0 × 109 and 4.0 × 103−6.0 × 108, respectively. PCB BAFs were within and/or slightly lower than previously calculated BAFs in marine and freshwater food webs.19,62 We observed significant positive log−linear relationships (Figure 3b, c) between Klip‑w and BAFs of PCBs and PCDD/Fs (r2 = 0.80−0.93, p < 0.001 for PCBs; r2 = 0.63−0.80, p = 0.003 for PCDD/Fs) in all the investigated species. This is often interpreted as indicating that equilibrium partitioning with the water column controls the bioaccumulation of PCBs and PCDD/Fs in tissues (see the SI for more details). In turn, this would imply that biomagnification (i.e., the enrichment of HOCs above their chemical activity in the water column) should not be observed. We investigated this next. Biomagnification of HOCs in the Food Web. Calculated TMFs for HOCs based on lipid-normalized tissue concentrations and estimated trophic level of each target species are given in Tables S13−S15. Samples (pooled or single specimens) were entered separately in the TMF calculations. Different sample sizes within the same species were also entered separately. Only samples collected from the two downstream locations were used in the TMF calculations. Blue crabs were excluded from the calculations of the TMFs because of their high HOC concentrations, despite their low trophic position, which we assume was from direct sediment ingestion. Marine transients were included in the calculations because the majority of specimens collected were young-of-the-year and were anticipated to be in the system for most or all of their first 12538
dx.doi.org/10.1021/es502886n | Environ. Sci. Technol. 2014, 48, 12533−12542
Environmental Science & Technology
Article
Figure 4. Output of the multiple linear regression showing the % contribution of the investigated contamination sources in biota tissues. P: pelagic; BP: bentho-pelagic; B: benthic. Food was investigated as a source of contamination only in secondary consumers and top predators.
the only PCDD/F congeners that underwent biomagnification in the food web of the lower Passaic River. TMFs previously reported for 2,3,7,8-CDF, 1,2,3,7,8-CDF, and 2,3,4,7,8-CDF in the marine food web of Bohai Bay,23 China were >1 but insignificant. TMF ∑17 PCDD/Fs was insignificantly >1. However, TEQ concentrations increased linearly with the increase in the trophic level (R2 = 0.83, p < 0.001) indicating the preferential accumulation of the potentially more toxic congeners in the food web. Calculated TMFs for all the HOCs were plotted against log KOW as shown in Figure 5. All HOCs that had log KOW < 5.9 displayed trophic dilution. Although log KOW for PAHs, PCBs, and PCDD/Fs overlapped in the range from 5.9 to 6.6, different patterns emerged in the data. While all the PCB and the majority of PCDD/F congeners in this range showed significant biomagnification, all PAHs and 2,3,7-CDF showed
year. This observation was also supported by their C and S isotopic signatures, which suggested that their primary food source was from freshwater primary production, similar to the species that are year-round residents in the Passaic estuary. In particular, we did not observe an enriched signature for C and S that is characteristic of a marine source of C or S (We note that the turnover of stable isotopes is faster than pollutant dynamics, which could result in lower body burdens of HOCs in transient species, and hence lead to an underestimation of TMFs.). TMFs were considered significant when p values of the ln concentration−TL regression relationships were 1. However, they were only significant for 2,3,7,8-CDD (2.7), 2,3,7,8-CDF (2.4), 1,2,3,7,8CDF (4.2), and 2,3,4,7,8-CDF (2.5) suggesting that these are
Figure 5. Relationship between TMFs and log KOW for PAHs, PCBs, and PCDD/Fs. The quadratic polynomial curve is drawn only for calculated TMFs of PCBs. TMFs of PAHs and PCDD/Fs did not show any significant relationship with log KOWs. 12539
dx.doi.org/10.1021/es502886n | Environ. Sci. Technol. 2014, 48, 12533−12542
Environmental Science & Technology
Article
and size (PAH concentrations and BAFs decreased with an increase in the size of Anguilla rostrata and Morone saxatilis). The largest eels and the age-2 striped bass collected in this study were highly mobile, less susceptible to predation, and potentially capable of moving into and out of this small estuary over time. Future studies should therefore concentrate on the influence of sex, size, and age (but accounting for reproductive status of individuals) on the body burdens of HOCs in the fish. As concerns the Passaic River, our results confirm the need to remediate the sediments from the lower 13 km (8 mi) of the Passaic River and thus remove the dominant source of HOCs to the food web.
significant biodilution. The different patterns for these chemicals with similar log KOW indicates that lipophilicity was not the only factor to predict the bioaccumulation potential and that metabolic transformation was likely a key factor. Fish are well-known for their ability to biotransform PAHs, and the biotransformation rate becomes higher in fish occupying higher trophic levels. Accordingly, the observed pattern in the current study may be attributed to the efficient metabolic transformation of PAHs relative to PCBs66,67 and the lower assimilation efficiencies of PAHs in the guts of fish compared to PCBs.68 No significant correlation was observed between TMFs of PCDD/Fs and log KOW, which may be attributed to the insignificance of the TMFs calculated for the majority of the congeners, and the limited number of congeners (n = 17) as all the hexa-chlorinated dioxins were < LOD. In contrast, a significant quadratic-polynomial relationship was observed for PCBs (r2 = 0.47, p = 0.0003), where TMFs increased with lipophilicity up to log KOW = 7.2 and then decreased with the increase in log KOW (Figure 5). A similar pattern was previously observed for PCBs in freshwater food webs.3 Hepta- and octachlorinated dioxins and furans displayed lower TMF values as well. This observation may be attributed to the larger molecular sizes of those congeners, which restrict their permeation through the cell membrane depressing their partitioning into the tissues, and the greater elimination through feces in the fish species.2 Implications. Previous studies investigating the bioaccumulation and biomagnification of HOCs in coastal settings have rarely been able to apportion how exactly the HOCs enter the food web. In dynamic regions, such as the Passaic River estuary, sediments play a major role in contaminant cycling. By deploying passive samplers in overlying water and porewater, we could demonstrate the importance of sediment ingestion, uptake from porewater, and diet, but not overlying water, as the likely origins for the bioaccumulation of organic pollutants in biota. This implies that removing contaminated sediments will be very effective in reducing the transfer of HOCs into the food-chain. Sediment and porewater measurements should be included in future studies investigating the bioaccumulationbiomagnification patterns of organic pollutants, especially in shallow, well mixed rivers and estuaries with a historical sediment contamination record. Most conveniently, this should be done using passive samplers. The other unknown in dealing with estuaries is linked to establishing trophic dynamics in the presence of migratory species. We observed no statistically significant difference between concentrations and BAFs calculated for marine transient and estuarine residents. TMFs calculated on a transient-resident (PAHs: 0.1−0.8; PCBs: 0.3−3.4; PCDD/ Fs: 0.4−4.1) and resident only scenarios (PAHs: 0.1−0.9; PCBs: 0.1−3.8; PCDD/Fs: 0.2−3.5) for all HOCs did not demonstrate any significant difference. This confirms the observation that marine transients, most of which were young-of-year, had been residing and feeding for some time within the Passaic River estuary, and their tissue burdens reflected its contamination status, which was also reflected in their stable isotopic signatures (see also Litvin and Weinstein 200427). Tissue concentrations were also influenced by metabolic transformation rates (as in the case of PAHs and lower chlorinated biphenyls and dioxins/furans), feeding habits (benthic feeders displaying higher body burdens of HOCs),
■
ASSOCIATED CONTENT
S Supporting Information *
Details on the sampling, chemical analysis, calculations of freely dissolved concentrations of HOCs, and BAFs. This material is available free of charge via the Internet at http://pubs.acs.org.
■
AUTHOR INFORMATION
Corresponding Author
*Phone: 401-874-6612. Fax 401-874-6811. E-mail: rlohmann@ mail.uri.edu. Notes
The authors declare no competing financial interest.
■
ACKNOWLEDGMENTS We acknowledge the Hudson River Foundation for funding this project (Hudson River Award # HRF 2011-5). We thank Dave Adelman (URI) and Kirk Barrett (Manhattan College) for passive sampler deployments in the Passaic River, and Paul Lerin (NJIT) for assistance in the fish collections.
■
REFERENCES
(1) Broman, D.; Rolff, C.; Näf, C.; Zebühr, Y.; Fry, B.; Hobbie, J. Using ratios of stable nitrogen isotopes to estimate bioaccumulation and flux of polychlorinated dibenzo-p-dioxins (PCDDs) and dibenzofurans (PCDFs) in two food chains from the Northern Baltic. Environ. Toxicol. Chem. 1992, 11 (3), 331−345. (2) Fisk, A. T.; Norstrom, R. J.; Cymbalisty, C. D.; Muir, D. C. Dietary accumulation and depuration of hydrophobic organochlorines: bioaccumulation parameters and their relationship with the octanol/ water partition coefficient. Environ. Toxicol. Chem. 1998, 17 (5), 951− 961. (3) Wu, J.-P.; Luo, X.-J.; Zhang, Y.; Yu, M.; Chen, S.-J.; Mai, B.-X.; Yang, Z.-Y. Biomagnification of polybrominated diphenyl ethers (PBDEs) and polychlorinated biphenyls in a highly contaminated freshwater food web from South China. Environ. Pollut. 2009, 157 (3), 904−909. (4) Burkhard, L. P.; Cook, P. M.; Lukasewycz, M. T. Biota−sediment accumulation factors for polychlorinated biphenyls, dibenzo-p-dioxins, and dibenzofurans in southern Lake Michigan lake trout (Salvelinus namaycush). Environ. Sci. Technol. 2004, 38 (20), 5297−5305. (5) Fisk, A. T.; Hobson, K. A.; Norstrom, R. J. Influence of chemical and biological factors on trophic transfer of persistent organic pollutants in the Northwater Polynya marine food web. Environ. Sci. Technol. 2001, 35 (4), 732−738. (6) Goerke, H.; Weber, K.; Bornemann, H.; Ramdohr, S.; Plötz, J. Increasing levels and biomagnification of persistent organic pollutants (POPs) in Antarctic biota. Mar. Pollut. Bull. 2004, 48 (3−4), 295−302. (7) Houde, M.; Muir, D. C.; Kidd, K. A.; Guildford, S.; Drouillard, K.; Evans, M. S.; Wang, X.; Whittle, D. M.; Haffner, D.; Kling, H. Influence of lake characteristics on the biomagnification of persistent organic pollutants in lake trout food webs. Environ. Toxicol. Chem. 2008, 27 (10), 2169−2178. 12540
dx.doi.org/10.1021/es502886n | Environ. Sci. Technol. 2014, 48, 12533−12542
Environmental Science & Technology
Article
Tittabawassee and Saginaw Rivers, Michigan, USA. Sci. Total Environ. 2010, 408 (11), 2394−2401. (24) McCutchan, J. H.; Lewis, W. M.; Kendall, C.; McGrath, C. C. Variation in trophic shift for stable isotope ratios of carbon, nitrogen, and sulfur. Oikos 2003, 102 (2), 378−390. (25) Iannuzzi, T. J.; Ludwig, D. F. Historical and current ecology of the lower Passaic River. Urban Habitats 2004, 2 (1), 147−173. (26) Adams, D. A.; O’Connor, J.; Weisberg, S. Sediment quality of the NY/NJ harbor system. An Investigation under the Regional Environmental Monitoring and Assessment Program (REMAP); 1998. (27) Armstrong, T. N.; Iannuzzi, T. J.; Thelen, J. B.; Ludwig, D. F.; Firstenberg, C. E. Characterization of chemical contamination in shallow-water estuarine habitats of an industrialized river. Part II. metals. Soil Sediment Contam. 2005, 14 (1), 35−52. (28) Bopp, R. F.; Chillrud, S. N.; Shuster, E. L.; Simpson, H. J.; Estabrooks, F. D. Trends in chlorinated hydrocarbon levels in Hudson River basin sediments. Environ. Health Perspect. 1998, 106 (Suppl 4), 1075. (29) Iannuzzi, T. J.; Armstrong, T. N.; Thelen, J. B.; Ludwig, D. F.; Firstenberg, C. E. Characterization of chemical contamination in shallow-water estuarine habitats of an industrialized river. Part 1: organic compounds. Soil Sediment Contam. 2005, 14 (1), 13−33. (30) Long, E. R.; Wolfe, D.; Scott, K.; Thursby, G.; Stern, E.; Peven, C.; Schwartz, T. Magnitude and Extent of Sediment Toxicity in the Hudson-Raritan Estuary; Coastal Monitoring and Bioeffects Assessment Division, Office of Ocean Resources Conservation Assessment, National Ocean Service, National Oceanic and Atmospheric Administration, US Department of Commerce: 1995; Vol. 88. (31) Wolfe, D. A.; Long, E. R.; Thursby, G. B. Sediment toxicity in the Hudson-Raritan Estuary: Distribution and correlations with chemical contamination. Estuaries 1996, 19 (4), 901−912. (32) Bopp, R. F.; Gross, M. L.; Tong, H.; Simpson, H. J.; Monson, S. J.; Deck, B. L.; Moser, F. C. A major incident of dioxin contamination: sediments of New Jersey estuaries. Environ. Sci. Technol. 1991, 25 (5), 951−956. (33) Lambert, M. K.; Friedman, C.; Luey, P.; Lohmann, R. Role of black carbon in the sorption of polychlorinated dibenzo-p-dioxins and dibenzofurans at the diamond alkali superfund site, Newark Bay, New Jersey. Environ. Sci. Technol. 2011, 45 (10), 4331−4338. (34) Friedman, C. L.; Lohmann, R. Comparing sediment equilibrium partitioning and passive sampling techniques to estimate benthic biota PCDD/F concentrations in Newark Bay, New Jersey (USA). Environ. Pollut. 2014, 186, 172−179. (35) Fernandez, M. P.; Ikonomou, M. G.; Courtenay, S. C.; Wirgin, I. I. Spatial variation in hepatic levels and patterns of PCBs and PCDD/ Fs among young-of-the-year and adult Atlantic tomcod (Microgadus tomcod) in the Hudson River estuary. Environ. Sci. Technol. 2004, 38 (4), 976−983. (36) Buchanan, G. A.; Hayton, A. G.; MacGregor, J. Comment on Urban et al.“Assessment of Human Health Risks Posed by Consumption of Fish f rom the Lower Passaic River (LPR), New Jersey”. Sci. Total Environ. 2010, 408 (8), 2002−2003. (37) Iannuzzi, J.; Butcher, M.; Iannuzzi, T. Evaluation of potential relationships between chemical contaminants in sediments and aquatic organisms from the lower Passaic River, New Jersey, USA. Environ. Toxicol. Chem. 2011, 30 (7), 1721−1728. (38) Deegan, L. A.; Garritt, R. H. Evidence for spatial variability in estuarine food webs. Mar. Ecol.: Prog. Ser. 1997, 147 (1), 31−47. (39) Litvin, S. Y.; Weinstein, M. P. Multivariate analysis of stableisotope ratios to infer movements and utilization of estuarine organic matter by juvenile weakfish (Cynoscion regalis). Can. J. Fish. Aquat. Sci. 2004, 61 (10), 1851−1861. (40) Litvin, S. Y.; Weinstein, M. P. Life history strategies of estuarine nekton: the role of marsh macrophytes, benthic microalgae, and phytoplankton in the trophic spectrum. Estuaries 2003, 26 (2), 552− 562. (41) Weinstein, M. P.; Litvin, S. Y.; Krebs, J. M. Restoration ecology: Ecological fidelity, restoration metrics, and a systems perspective. Ecol. Eng. 2014, 65, 71−87.
(8) McKinney, M. A.; McMeans, B. C.; Tomy, G. T.; Rosenberg, B.; Ferguson, S. H.; Morris, A.; Muir, D. C.; Fisk, A. T. Trophic transfer of contaminants in a changing arctic marine food web: Cumberland Sound, Nunavut, Canada. Environ. Sci. Technol. 2012, 46 (18), 9914− 9922. (9) Morrison, H. A.; Whittle, D. M.; Metcalfe, C. D.; Niimi, A. J. Application of a food web bioaccumulation model for the prediction of polychlorinated biphenyl, dioxin, and furan congener concentrations in Lake Ontario aquatic biota. Can. J. Fish. Aquat. Sci. 1999, 56 (8), 1389−1400. (10) Wu, W.; Schramm, K.-W.; Kettrup, A. Bioaccumulation of polychlorinated dibenzo-p-dioxins and dibenzofurans in the foodweb of Ya-Er Lake area, China. Water Res. 2001, 35 (5), 1141−1148. (11) Lohmann, R.; Burgess, R. M.; Cantwell, M. G.; Ryba, S. A.; MacFarlane, J. K.; Gschwend, P. M. Dependency of polychlorinated biphenyl and polycyclic aromatic hydrocarbon bioaccumulation in Mya arenaria on both water column and sediment bed chemical activities. Environ. Toxicol. Chem. 2004, 23 (11), 2551−2562. (12) Morgan, E. J.; Lohmann, R. Detecting air−water and surface− deep water gradients of PCBs using polyethylene passive samplers. Environ. Sci. Technol. 2008, 42 (19), 7248−7253. (13) McLeod, P. B.; Luoma, S. N.; Luthy, R. G. Biodynamic modeling of PCB uptake by Macoma balthica and Corbicula f luminea from sediment amended with activated carbon. Environ. Sci. Technol. 2007, 42 (2), 484−490. (14) Bucheli, T. D.; Gustafsson, Ö . Ubiquitous observations of enhanced solid affinities for aromatic organochlorines in field situations: are in situ dissolved exposures overestimated by existing partitioning models? Environ. Toxicol. Chem. 2001, 20 (7), 1450−1456. (15) Tracey, G.; Hansen, D. Use of biota-sediment accumulation factors to assess similarity of nonionic organic chemical exposure to benthically-coupled organisms of differing trophic mode. Arch. Environ. Contam. Toxicol. 1996, 30 (4), 467−475. (16) Helm, P. A.; Gewurtz, S. B.; Whittle, D. M.; Marvin, C. H.; Fisk, A. T.; Tomy, G. T. Occurrence and biomagnification of polychlorinated naphthalenes and non-and mono-ortho PCBs in Lake Ontario sediment and biota. Environ. Sci. Technol. 2008, 42 (4), 1024−1031. (17) Hu, G.-c.; Dai, J.-y.; Xu, Z.-c.; Luo, X.-j.; Cao, H.; Wang, J.-s.; Mai, B.-x.; Xu, M.-q. Bioaccumulation behavior of polybrominated diphenyl ethers (PBDEs) in the freshwater food chain of Baiyangdian Lake, North China. Environ. Int. 2010, 36 (4), 309−315. (18) Ikemoto, T.; Tu, N. P. C.; Watanabe, M. X.; Okuda, N.; Omori, K.; Tanabe, S.; Tuyen, B. C.; Takeuchi, I. Analysis of biomagnification of persistent organic pollutants in the aquatic food web of the Mekong Delta, South Vietnam using stable carbon and nitrogen isotopes. Chemosphere 2008, 72 (1), 104−114. (19) Morgan, E. J.; Lohmann, R. Dietary uptake from historically contaminated sediments as a source of PCBs to migratory fish and invertebrates in an urban estuary. Environ. Sci. Technol. 2010, 44 (14), 5444−5449. (20) Takeuchi, I.; Miyoshi, N.; Mizukawa, K.; Takada, H.; Ikemoto, T.; Omori, K.; Tsuchiya, K. Biomagnification profiles of polycyclic aromatic hydrocarbons, alkylphenols and polychlorinated biphenyls in Tokyo Bay elucidated by δ13C and δ15N isotope ratios as guides to trophic web structure. Mar. Pollut. Bull. 2009, 58 (5), 663−671. (21) Walters, D. M.; Fritz, K. M.; Johnson, B. R.; Lazorchak, J. M.; McCormick, F. H. Influence of trophic position and spatial location on polychlorinated biphenyl (PCB) bioaccumulation in a stream food web. Environ. Sci. Technol. 2008, 42 (7), 2316−2322. (22) Wan, Y.; Hu, J.; Yang, M.; An, L.; An, W.; Jin, X.; Hattori, T.; Itoh, M. Characterization of trophic transfer for polychlorinated dibenzo-p-dioxins, dibenzofurans, non-and mono-ortho polychlorinated biphenyls in the marine food web of Bohai Bay, North China. Environ. Sci. Technol. 2005, 39 (8), 2417−2425. (23) Wan, Y.; Jones, P. D.; Holem, R. R.; Khim, J. S.; Chang, H.; Kay, D. P.; Roark, S. A.; Newsted, J. L.; Patterson, W. P.; Giesy, J. P. Bioaccumulation of polychlorinated dibenzo-p-dioxins, dibenzofurans, and dioxin-like polychlorinated biphenyls in fishes from the 12541
dx.doi.org/10.1021/es502886n | Environ. Sci. Technol. 2014, 48, 12533−12542
Environmental Science & Technology
Article
PBDEs and PCBs in Lake Michigan. Environ. Sci. Technol. 2006, 40 (23), 7263−7269. (63) Nakata, H.; Sakai, Y.; Miyawaki, T.; Takemura, A. Bioaccumulation and toxic potencies of polychlorinated biphenyls and polycyclic aromatic hydrocarbons in tidal flat and coastal ecosystems of the Ariake Sea, Japan. Environ. Sci. Technol. 2003, 37 (16), 3513−3521. (64) Wan, Y.; Jin, X.; Hu, J.; Jin, F. Trophic dilution of polycyclic aromatic hydrocarbons (PAHs) in a marine food web from Bohai Bay, North China. Environ. Sci. Technol. 2007, 41 (9), 3109−3114. (65) Mizukawa, K.; Takada, H.; Takeuchi, I.; Ikemoto, T.; Omori, K.; Tsuchiya, K. Bioconcentration and biomagnification of polybrominated diphenyl ethers (PBDEs) through lower-trophic-level coastal marine food web. Mar. Pollut. Bull. 2009, 58 (8), 1217−1224. (66) Forbes, V. E.; Andreassen, M. S.; Christensen, L. Metabolism of the polycyclic aromatic hydrocarbon fluoranthene by the polychaete Capitella capitata species I. Environ. Toxicol. Chem. 2001, 20 (5), 1012−1021. (67) Gardinali, P. R.; Sericano, J. L.; Wade, T. L. Uptake and depuration of toxic halogenated aromatic hydrocarbons by the American oyster (Crassostrea virginica): a field study. Chemosphere 2004, 54 (1), 61−70. (68) Thomann, R. V.; Komlos, J. Model of biota-sediment accumulation factor for polycyclic aromatic hydrocarbons. Environ. Toxicol. Chem. 1999, 18 (5), 1060−1068.
(42) Weinstein, M. P.; Litvin, S. Y.; Guida, V. G. Stable isotope and biochemical composition of white perch in a Phragmites dominated salt marsh and adjacent waters. Wetlands 2010, 30 (6), 1181−1191. (43) Able, K. W.; Fahay, M. P. First Year in the Life of Estuarine Fishes in the Middle Atlantic Bight; 1998. (44) Khairy, M. A.; Lohmann, R. Field validation of polyethylene passive air samplers for parent and alkylated PAHs in Alexandria, Egypt. Environ. Sci. Technol. 2012, 46 (7), 3990−3998. (45) Khairy, M. A.; Lohmann, R. Field calibration of low density polyethylene passive samplers for gaseous POPs. Environ. Sci.: Processes Impacts 2014, 16, 414−421. (46) U.S.EPA, Tetra-through Octa-Chlorinated Furans by Isotope Dilution HRGC/HRMS; 1994. (47) Wretling, S.; Eriksson, A.; Eskhult, G.; Larsson, B. Polycyclic aromatic hydrocarbons (PAHs) in Swedish smoked meat and fish. J. Food Compos. Anal. 2010, 23 (3), 264−272. (48) Ma, Y.-G.; Lei, Y. D.; Xiao, H.; Wania, F.; Wang, W.-H. Critical review and recommended values for the physical-chemical property data of 15 polycyclic aromatic hydrocarbons at 25 C. J. Chem. Eng. Data 2009, 55 (2), 819−825. (49) Schenker, U.; MacLeod, M.; Scheringer, M.; Hungerbühler, K. Improving data quality for environmental fate models: A least-squares adjustment procedure for harmonizing physicochemical properties of organic compounds. Environ. Sci. Technol. 2005, 39 (21), 8434−8441. (50) Åberg, A.; MacLeod, M.; Wiberg, K. Physical-chemical property data for dibenzo-p-dioxin (DD), dibenzofuran (DF), and chlorinated DD/Fs: a critical review and recommended values. J. Phys. Chem. Ref. Data 2008, 37 (4), 1997−2008. (51) Endo, S.; Escher, B. I.; Goss, K.-U. Capacities of membrane lipids to accumulate neutral organic chemicals. Environ. Sci. Technol. 2011, 45 (14), 5912−5921. (52) Weinstein, M. P.; Litvin, S. Y.; Guida, V. G. Essential fish habitat and wetland restoration success: a tier III approach to the biochemical condition of common mummichog Fundulus heteroclitus in common reed Phragmites australis- and smooth cordgrass Spartina alternif loradominated salt marshes. Estuaries Coasts 2009, 32 (5), 1011−1022. (53) Weinstein, M. P.; Litvin, S. Y.; Bosley, K. L.; Fuller, C. M.; Wainright, S. C. The role of tidal salt marsh as an energy source for marine transient and resident finfishes: a stable isotope approach. Trans. Am. Fish. Soc. 2000, 129 (3), 797−810. (54) Post, D. M. Using stable isotopes to estimate trophic position: models, methods, and assumptions. Ecology 2002, 83 (3), 703−718. (55) Kneib, R.; Stiven, A. Growth, reproduction, and feeding of Fundulus heteroclitus (L.) on a North Carolina salt marsh. J. Exp. Mar. Biol. Ecol. 1978, 31 (2), 121−140. (56) MacAvoy, S. E.; Garman, G. C.; Macko, S. A. Anadromous fish as marine nutrient vectors. Fish. Bull. 2009, 107 (2), 165−174. (57) Baumard, P.; Budzinski, H.; Garrigues, P.; Sorbe, J.; Burgeot, T.; Bellocq, J. Concentrations of PAHs (polycyclic aromatic hydrocarbons) in various marine organisms in relation to those in sediments and to trophic level. Mar. Pollut. Bull. 1998, 36 (12), 951−960. (58) Baussant, T.; Sanni, S.; Jonsson, G.; Skadsheim, A.; BøRSETH, J. F. Bioaccumulation of polycyclic aromatic compounds: 1. Bioconcentration in two marine species and in semipermeable membrane devices during chronic exposure to dispersed crude oil. Environ. Toxicol. Chem. 2001, 20 (6), 1175−1184. (59) Porte, C.; Albaiges, J. Bioaccumulation patterns of hydrocarbons and polychlorinated biphenyls in bivalves, crustaceans, and fishes. Arch. Environ. Contam. Toxicol. 1994, 26 (3), 273−281. (60) Broman, D.; Näuf, C.; Lundbergh, I.; Zebühr, Y. An in situ study on the distribution, biotransformation and flux of polycyclic aromatic hydrocarbons (pahs) in an aquatic food chain (seston - Mytilus edulis L. - Somateria mollissima L.) from the baltic: An ecotoxicological perspective. Environ. Toxicol. Chem. 1990, 9 (4), 429−442. (61) Varanasi, U.; Stein, J. E. Disposition of xenobiotic chemicals and metabolites in marine organisms. Environ. Health Perspect. 1991, 90, 93. (62) Streets, S. S.; Henderson, S. A.; Stoner, A. D.; Carlson, D. L.; Simcik, M. F.; Swackhamer, D. L. Partitioning and bioaccumulation of 12542
dx.doi.org/10.1021/es502886n | Environ. Sci. Technol. 2014, 48, 12533−12542
