Environ. Sci. Technol. 2009, 43, 3700–3704
Patterns of Bioaccumulation of Polybrominated Diphenyl Ether and Polychlorinated Biphenyl Congeners in Marine Mussels A D R I A N M . H . D E B R U Y N , * ,† LIZANNE M. MELOCHE,† AND CHRISTOPHER J. LOWE‡ Golder Associates Ltd., 500-4260 Still Creek Drive, Burnaby, British Columbia, Canada V5C 6C6, and Capital Regional District, P. O. Box 1000, 625 Fisgard Street, Victoria, British Columbia, Canada V8W 2S6
Received November 14, 2008. Revised manuscript received March 25, 2009. Accepted March 26, 2009.
Marine mussels (Modiolus modiolus) and sediment from 14 stations near a municipal outfall and three reference locations were analyzed for polybrominated diphenyl ethers (PBDEs) and polychlorinated biphenyls (PCBs) to evaluate and compare patterns of bioaccumulation of individual congeners between these two groups of chemicals. Of the 47 PBDEs and 209 PCBs analyzed, 34 PBDE and 153 PCB congeners or coeluting groups of congeners were detected in one or more matrices. The predominant PBDE congeners were BDEs 47, 99, 100, and 209, accounting for 80-90% of the total PBDEs in all matrices. PCBs and PBDEs exhibited a parabolic relationship of the biota-sediment accumulation factor (BSAF) versus the log octanol-water partition coefficient (KOW). Below KOW 105.5, BSAFs ranged between 1 and 3, reflecting approximate equilibrium between mussels and sediment for these relatively water soluble congeners. BSAFs increased with increasing KOW to maximum values of approximately 30-100 for congeners with KOW ∼107 and then declined at higher KOW to a value of approximately 1 for BDE 209. BSAFs for PBDEs were generally 2- to 3-fold higher than those for PCBs of a similar KOW. The calculated BSAFs for PBDE congeners indicate that PBDEs have a pattern of bioaccumulative behavior in mussels similar to that of the PCBs, and that some PBDE congeners may be more bioaccumulative in mussels than PCBs.
Evidence for the bioaccumulative potential of PBDEs comes from a range of sources. Similarities in structure and physicochemical properties between PBDEs and PCBs suggest that environmental fate may be governed by similar processes. However, the ether linkage of the PBDEs in place of the biphenyl linkage of the PCBs and differences in the properties of bromine and chlorine as substituents distinguish PBDEs from PCBs in several key ways relevant to bioaccumulation. Importantly, PBDEs exhibit a wider range of molecular size and hydrophobicity than that of PCBs, with reports of measured and calculated octanol-water partition coefficients (KOW) extending to 1010 or greater (3, 4). In addition, PBDEs appear to undergo debromination more readily than PCBs undergo dechlorination (5, 6). These characteristics would be expected to result in reduced bioaccumulation of the higher-substituted PBDE congeners relative to PCBs, but they may be expected to enhance the apparent bioaccumulative potential of intermediate-substituted congeners because of internal production from metabolic debromination of the higher congeners (7). Empirical estimates of PBDE bioaccumulation are available for a range of taxa, including invertebrates (8, 9), fish (9-12), mammals (12-16) and birds (13). Biomagnification factors reported in these studies are typically on the order of 5-20 for BDE 47, indicating a bioaccumulative potential of some PBDEs comparable to that of the most bioaccumulative PCBs. Gustafsson et al. (8) found that bioaccumulation factors for BDE 47 and BDE 99 in blue mussels were several-fold higher than for PCBs of similar hydrophobicity. In contrast, Kelly et al. (17) reported no biomagnification of seven PBDE congeners and a trophic magnification factor for BDE 47 of only 1.6, substantially lower than most PCBs. A limitation of the previously reported data is that even studies that sampled many taxa generally report only a few key PBDE congeners. This restricts our ability to develop and validate general models of bioaccumulation for PBDEs (7). Here, we report biota-sediment accumulation factors (BSAFs) for 27 detected congeners or coeluting pairs of congeners ranging in estimated KOW from 104.8 to 109.3. We compare these data to the patterns of bioaccumulation observed for 135 PCB congeners or coeluting sets of congeners measured in the same study organisms. Our objective is to describe the pattern of bioaccumulation among PBDE congeners relative to the well-known benchmark of the bioaccumulative PCBs to provide insight into the extent that a relatively good theoretical understanding of PCB bioaccumulation (e.g., ref 18) can be applied to modeling PBDEs.
Introduction
Experimental Section
The polybrominated diphenyl ethers (PBDEs) are a group of contaminants that have attracted widespread scientific and regulatory attention. Increasingly apparent similarities between PBDEs and many legacy pollutants, especially the polychlorinated biphenyls (PCBs), have prompted regulation and/or bans of some PBDE formulations in the European Union, Australia, Canada, Japan, and several U.S. states. Of particular concern is evidence that PBDEs have the combination of environmental persistence, bioaccumulative potential, and toxicity that first attracted attention to the PCBs and other substances listed under the Stockholm Convention (1, 2).
Sampling. Field sampling was conducted in September 2006 off the coast of Vancouver Island, British Columbia, Canada in the vicinity of the Capital Regional District’s Clover Point municipal wastewater outfall (48°23′67′ N, 123°20′68′′ W) adjacent to the city of Victoria. Preliminary treated (screened) wastewater has been discharged from this outfall since 1981, resulting in localized effects on sediment chemistry and biology (19, 20). A total of 17 stations were sampled, including one adjacent to the diffuser (1.5 km from shore), 13 arranged in a radial design at 100, 200, 400, and 800 m from the diffuser (Figure S1 of the Supporting Information), and three in a reference area approximately 5.5 km southeast of the outfall. At each station, three grabs with a 0.1 m2 Van Veen dredge were used to obtain a sample of surface sediment (top 2 cm) and 15 horse mussels (Modiolus modiolus), randomly selected from individuals >50 mm length (i.e., large enough that sufficient tissue mass would be available for all planned
* Corresponding author phone: 604-296-4200; fax: 604-298-5253; e-mail:
[email protected]. † Golder Associates Ltd. ‡ Capital Regional District. 3700
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ENVIRONMENTAL SCIENCE & TECHNOLOGY / VOL. 43, NO. 10, 2009
10.1021/es900472k CCC: $40.75
2009 American Chemical Society
Published on Web 04/14/2009
analyses). Field duplicates of mussel samples were collected at the outfall terminus station. Shell length, shell width, total weight, tissue weight, age, and sex were determined for each mussel prior to compositing and homogenizing all mussels from each station for chemical analysis. Mussels were aged by counting annuli in the inner nacreous layer of an acetate peel preparation of a cross section cut through the umbone. Wastewater samples were obtained from a wet well at the treatment plant quarterly in 2006 as 24 h composites; field triplicate composites were taken in April 2006. Chemical Analysis. Extraction, cleanup, and analysis of PBDEs and PCBs using high resolution gas chromatography-high resolution mass spectrometry (HRGC-HRMS) were conducted at AXYS Analytical Services Ltd. (Sidney, BC, Canada). Details of methods for PBDE and PCB determinations and quality assurance/quality control (QA/QC) procedures are provided in the U.S. Environmental Protection Agency (USEPA) Methods 1668A (21) and 1614 (22); modifications are described in the Supporting Information. Lipid content was determined gravimetrically. Organic carbon content was determined by USEPA Method 9060A (23) at the ALS Laboratory Group (Vancouver, BC, Canada). Data quality objectives were met for lipid (relative standard deviation of laboratory duplicates ) 5%) and organic carbon [certified reference material recovery ) 94 ( 1.1% (mean ( standard deviation, n ) 5)]. Data quality objectives for PCBs and PBDEs were met for matrix spike recovery (50-150%) in all cases and for relative standard deviation of all duplicate analyses (
