Environ. Sci. Technol. 2003, 37, 3513-3521
Introduction
aquatic food chain. In numerous field studies, special attention has been focused on the concentration and distribution of PCBs, especially non- and mono-ortho coplanar congeners which have toxicological properties similar to 2,3,7,8-tetrachlorodibenzo-p-dioxin (2378-TCDD) (1, 2). These congeners are known to bind to Ah receptor (AhR) and induce liver microsomal aryl hydrocarbon hydroxylase (AHH) in laboratory animals (3) and wildlife (4, 5). The World Health Organization (WHO) assigned toxic equivalency factors (TEFs) for four non-ortho (IUPAC 77, 81, 126, and 169) and eight mono-ortho (IUPAC 105, 114, 118, 123, 156, 157, 167, and 189) coplanar PCBs to evaluate their toxic potencies in the environment (6). Polycyclic aromatic hydrocarbons (PAHs) are another class of hydrophobic environmental contaminants that tend to adsorb rapidly on suspended materials and sediment (7). Recently, several studies have shown that some PAHs are capable of inducing dioxin-like responses in vitro, and the dioxin-like relative potencies (REPs) of PAHs ranged from 10-9 to 10-2 relative to TCDD with benzo[k]fluoranthene being the most potent dioxin-like PAH (8-10). To understand the relative contribution of dioxin-like toxicity posed by halogenated aromatic hydrocarbons (HAHs) and PAHs in the environment, PCDDs, PCDFs, PCNs, PCBs, and PAHs were analyzed in sediments from Tokyo Bay (11). PAHs were the predominant contributors to ∑TEQs in sediments, contributing 10-240 times greater TEQs than those by PCDDs/DFs. Similar results were also reported in marine sediments from the Mediterranean Sea (12). In recent years, the relative contribution of PCDDs/DFs, PCBs, and PCNs to ∑TEQs has been reported in wildlife (13, 14), but little information is available on the relative contribution of PAHs to ∑TEQs in tissues. The greater accumulation of PAHs and their metabolites were reported in lower trophic organisms, such as mussel (7), earthworm (15), and fish (16). Our recent study also indicated the occurrence of high concentrations of PAHs in benthic tidal flat organisms from the Ariake Sea, Japan (17). These facts suggest that PAHs could accumulate in tidal flat food chain and may pose great risk to these organisms. The Ariake Sea, located in western Japan, has large tidal ranges (up to 5 m) and a tidal flat (approximately 230 km2). This tidal flat ecosystem inhabits several unique benthic organisms, such as mudskipper fishes, crabs, clams, and lugworms. Recently, PCB contamination was reported in tidal flat organisms from the Ariake Sea, and a growth-dependent accumulation of PCBs was found in herbivore mudskippers (18). However, little information is available on the concentrations and bioaccumulation profiles of PAHs in tidal flat and coastal water organisms in this region. The aim of this study was to determine PCBs and PAHs residue levels in sediments, tidal flat species (crab, lugworm, clam, oyster, and tidal flatfishes including mudskipper), and coastal water organisms (horse mackerel, mackerel, sardine, flatfish, squid, finless porpoise) from the Ariake Sea to understand their status of contamination and bioaccumulation properties. In addition, TEQ concentrations of PCBs and PAHs were calculated for sediments and organisms to evaluate their contribution to ∑TEQs and toxic potencies.
Polychlorinated biphenyls (PCBs) are persistent and hydrophobic organic contaminants known to accumulate in
Experimental Section
* Corresponding author telephone/fax: +81-96-342-3380, e-mail:
[email protected]. † Kumamoto University. ‡ Ehime University. § Nagasaki University.
Sample Collection. Surficial sediment and tidal flat organisms such as clams (Cyclina sinensis), oysters (Crassostrea gigas), lugworms, crabs (Macrophthalmus japonicus), herbivore mudskippers (Boleophthalmus pectinirostris), omnivore mudskippers (Periophthalmus modestus), and tidal flatfishes
Bioaccumulation and Toxic Potencies of Polychlorinated Biphenyls and Polycyclic Aromatic Hydrocarbons in Tidal Flat and Coastal Ecosystems of the Ariake Sea, Japan H A R U H I K O N A K A T A , * ,† YASUFUMI SAKAI,† T A K A S H I M I Y A W A K I , †,‡ A N D AKIRA TAKEMURA§ Graduate School of Science and Technology, Kumamoto University, 2-39-1 Kurokami, Kumamoto 860-8555, Japan, Faculty of Agriculture, Ehime University, 3-5-7 Tarumi, Matsuyama 790-8566, Japan, and Faculty of Fishery, Nagasaki University, Bunkyo-machi, Nagasaki 852-8521, Japan
Sediment and marine biota comprising several species of tidal flat and coastal organisms were analyzed for polychlorinated biphenyls (PCBs) including non- and monoortho coplanar congeners and polycyclic aromatic hydrocarbons (PAHs) to examine bioaccumulation profiles and toxic potencies of these contaminants. Concentrations of PCBs in tidal flat organisms ranged from 3.6 ng/g (wet wt) in clams to 68 ng/g (wet wt) in omnivore tidal flatfishes, a discernible trend reflecting concentrations and trophic levels. In contrast, PAHs concentrations were the highest in lower trophic organisms, such as crabs and lugworms from tidal flat, whereas those in coastal fishes, squid, and finless porpoises were less than detection limit. Greater bioaccumulation of PAHs was found in lugworms and crabs, which might be due to their direct ingestion of sediment particulates absorbed with PAHs. TCDD toxic equivalents (TEQs) were calculated for PCBs and PAHs in sediments and biota. PCBs accounted for a greater proportion of total TEQs (∑TEQs: sum of TEQPCB and TEQPAH) in coastal and tidal flatfishes (>95%), while PAHs occupied a considerable portion of ∑TEQs in sediment (>97%). Interestingly, TEQPAH accounted for 37% and 81% of the ∑TEQs in crabs and clams, respectively. Benzo[b]fluoranthene was the dominant contributor to TEQPAH in both the species. Considering these observations, the environmental risks of PAHs may not be ignored in benthic tidal flat organisms due to their greater bioaccumulation through sediments.
10.1021/es021083h CCC: $25.00 Published on Web 07/19/2003
2003 American Chemical Society
VOL. 37, NO. 16, 2003 / ENVIRONMENTAL SCIENCE & TECHNOLOGY
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FIGURE 1. Map showing the sampling sites in the Ariake Sea, western Japan. (Taenioides rubicundus) were collected from the Tojin River Estuary in the Ariake Sea during 1999 and 2001 (Figure 1). Squid and coastal water fishes (horse mackerel, mackerel, sardine, flatfish) collected from the Ariake Sea were purchased at a fishery market in Kumamoto. Finless porpoises (Nephocoena phocoenoides) stranded along the Ariake Sea and the Yatsushiro Sea coasts were transported to the laboratory and dissected. All the samples were sealed in plastic bags and stored at -20 °C until analysis. Chemical Analysis. PCBs including non- and mono-ortho coplanar congeners were analyzed following the methods described previously (19, 20) with some modifications. The whole bodies of fishes, crabs, squids, and lugworms; the soft tissues of clams and oysters; and the blubber of finless porpoises were homogenized with Na2SO4 and extracted in dichloromethane:hexane (8:1) using a Soxhlet apparatus for 7-10 h. The extract was concentrated, an aliquot was refluxed for 1-2 h in 1 N KOH-ethanol, and the solution was transferred to hexane. Lipid content was determined gravimetrically from an aliquot of the Soxhlet extract. The hexane solution was concentrated to approximately 5 mL and sequentially subjected to cleanup by eluting through 1.5 g of silica gel (Wako-gel S-1, Wako Pure Chemical Co. Ltd) packed in a glass column with 150 mL of hexane. This eluant was concentrated to 6 mL, and after being cleaned with sulfuric acid and hexane-washed water, an aliquot was injected into a gas chromatograph-mass spectrometer (GCMSD). The 5 mL of the hexane eluted from the 1.5-g silica gel column was passed through a glass column packed with 125 mg of active carbon to separate non-ortho coplanar PCBs from other congeners. Quantification of PCB congeners was made by GC-MSD (Hewlett-Packard 6890 and 5973MSD) with 30-m fused silica capillary column (DB-1, J&W Scientific). Sediment samples were air-dried, sieved through 500-µm mesh, and analyzed by following the procedures described above. Total organic carbon of the sediment was determined by using a CHN analyzer (Yanaco MT-5). 3514
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Twenty-four PAHs including 16 priority compounds identified by the U.S. EPA such as naphthalene (NA), benzothiophene (BT), 1- and 2-methlynaphthalenes (1-MM, 2-MM), acenaphthylene (ANTHY), acenaphthene (ANTN), fluorene (FLU), 1,2- and 1,8-dimethylnaphthalene (1,2-DMN, 1,8-DMN), phenanthrene (PHE), anthracene (AN), dibenzothiophene (DBT), fluoranthene (FLR), pyrene (PY), chrysene (CHRY), benz[a]anthracene (B[a]A), benzo[b]fluoranthene (B[b]F), benzo[k]fluoranthene (B[k]F), benzo[e]pyrene (B[e]P), benzo[a]pyrene (B[a]P), perylene (PERY), indeno[1,2,3-cd]pyrene (I[cd]P), benzo[ghi]perylene (B[ghi]P), dibenz[a,h]anthracene (D[ah]A) were determined in this study. PAHs were analyzed following the method reported previously (21) with slight modification. The procedure of extraction is similar to that described for PCB analysis. Briefly, tissue homogenates and air-dried sediment samples were Soxhlet-extracted with a mixture of DCM and hexane (8:1). An appropriate volume of perdeuterated PAH surrogate mixture (acenaphthene-d10, phenanthrene-d10, chrysene-d12, and perylene-d14) was spiked into sample extract as a surrogate standard. The extract was subjected to acetonitrile partitioning to remove lipid. A total of 4 or 5 mL of the extract was added to a separatory funnel containing 50 mL of hexane-saturated acetonitrile and 20 mL of hexane. After the solution was shaken and partitioned, the acetonitrile layer was collected. This procedure was repeated, and totally 100 mL of hexane-saturated acetonitrile was collected. Five milliliters of hexane was added to the funnel and shaken gently. The acetonitrile layer was transferred to a 1-L separation funnel containing 500 mL of 5% NaCl solution and 50 mL of hexane. After the solution was shaken, the water layer was removed and hexane was collected. These procedures were repeated, and totally 100 mL of hexane was obtained. Several 10 g of Na2SO4 was added to the hexane to remove moisture. After filtration, hexane was concentrated to 5 mL and passed through a glass column containing 5 g of 5% H2O-deactivated silica gel. This column was eluted with 150 mL of hexane for cleanup. The eluate
g
a Concentration unit: ng/g dry wt. b A sample of sediment was measured for carbon percent. c Number of pooled samples. Mackerel, horse mackerel, sardine, and flatfish. h na, not analyzed. i Blubber tissues were analyzed.
d
Boleophthalmus pectinirostris. e Periophthalmus modestus. f Taenioides rubicundus.
280 ( 190 400 28 000 ( 6 600 30 ( 26 3.4 24 000 ( 5 100 na na na na na na nah na na Coastal Water 0.18 ( 0.26
