Environ. Sci. Technol. 2006, 40, 4916-4921
Perfluorinated Contaminants in Sediments and Aquatic Organisms Collected from Shallow Water and Tidal Flat Areas of the Ariake Sea, Japan: Environmental Fate of Perfluorooctane Sulfonate in Aquatic Ecosystems H A R U H I K O N A K A T A , * ,†,‡ KURUNTHACHALAM KANNAN,‡ T E T S U Y A N A S U , † H Y E O N - S E O C H O , ‡,§ EWAN SINCLAIR,‡ AND AKIRA TAKEMURA| Graduate School of Science and Technology, Kumamoto University, 2-39-1 Kurokami, Kumamoto 860-8555, Japan, Wadsworth Center, New York State Department of Health and Department of Environmental Health Sciences, School of Public Health, State University of New York at Albany, Empire State Plaza, P.O. Box 509, Albany, New York 12201-0509, Ocean Environment System Program, Yosu National University, San 96-1, Dundeok-dong, Yeosu 550-749, Korea, and Faculty of Fishery, Nagasaki University, 1-14 Bunkyo-machi, Nagasaki 852-8521, Japan
Perfluorinated compounds (PFCs), such as perfluorooctane sulfonate (PFOS), perfluorooctanoate (PFOA), perfluorononanoate (PFNA), perfluorohexane sulfonate (PFHS), and perfluorooctane sulfonamide (PFOSA) are widely distributed in aquatic ecosystems. Despite studies reporting the occurrence of PFCs in aquatic organisms, the fate of PFCs in tidal flat and marine coastal ecosystems is not known. In this study, we determined concentrations of PFOS, PFOA, PFNA, PFHS, and PFOSA in sediments; benthic organisms, including lugworm, mussel, crab, clam, oyster, and mudskipper fish from tidal flat; and shallow water species, such as filefish, bream, flounder, shark, finless porpoise, gull, and mallard collected from the Ariake Sea, Japan. PFOS and PFOA were detected in most of the samples analyzed, followed by PFNA, PFOSA, and PFHS. In shallow water species, PFOS was the dominant contaminant, and elevated concentrations were found in higher trophic level species, such as marine mammals and omnivorous birds. These results suggest biomagnification of PFOS through the coastal food chain. In contrast, PFOA was the most abundant compound in tidal flat organisms and sediments. PFOA concentrations in sediments, lugworms, and omnivorous mudskippers in tidal flat were approximately 1 order of magnitude greater than the levels of PFOS. This indicates differences in exposure pattern and bioavailability of PFOS and PFOA between * Corresponding author phone/fax: +81-96-342-3380; e-mail:
[email protected]. † Kumamoto University. ‡ State University of New York at Albany. § Yosu National University. | Nagasaki University. 4916
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ENVIRONMENTAL SCIENCE & TECHNOLOGY / VOL. 40, NO. 16, 2006
shallow water and tidal flat organisms. The accumulation profiles of PFCs were compared with those of organochlorines (polychlorinated biphenyls, PCB), organotin (tributyltin, TBT), and polycyclic aromatic hydrocarbons (PAHs) in tidal flat and shallow water samples collected from the Ariake Sea. Concentrations of PFCs in sediments and in tidal flat organisms were significantly lower than that found for PCBs, TBT, and PAHs. Nevertheless, PFOS concentrations in shallow water species were comparable to and/or significantly greater than those of other classes of contaminants. This implies that the aqueous phase is a major sink for PFCs, which is different from what was observed for nonpolar organic pollutants.
Introduction Perfluorinated compounds, such as perfluorooctane sulfonate (PFOS) and perfluorooctanoate (PFOA), have been recognized as widespread contaminants in the environment (1-3). The detection of PFOS in wildlife in and around pelagic and polar regions suggests long-range transport and global distribution of this compound and its precursors (1, 4). The occurrence of other fluorinated compounds, perfluoroalkane sulfonamides, and fluorinated telomer alcohols has been reported in various environmental matrixes. Recent studies have indicated that PFOS can bioaccumulate in higher trophic level organisms through the aquatic food chain (5-7). The concentrations of PFOS in marine mammals and omnivorous birds from the Eastern Arctic were approximately 10-20fold greater than those found in zooplankton and clam (5). Similarly, PFOS concentrations in amphipods and mussels from the Great Lakes were 3 orders of magnitude higher than those in the surrounding water (7). Whereas most of the earlier studies have focused on water or biological matrixes, little information is available on the concentrations of perfluorinated compounds (PFCs) in soil and sediment. The soil and sediment compartments have been suggested as a final sink for neutral organic pollutants. Hydrophobic compounds, such as polychlorinated biphenyls (PCBs) and organochlorine pesticides tend to partition from water into suspended solids and sediment, due to their propensity to absorb to organic carbon. Significant correlation was found between DDT concentrations and organic carbon content in soils and sediments (8). On the other hand, PFCs have amphiphilic profiles such that they exhibit both hydrophobic and hydrophilic properties (9, 10), and they are expected to behave differently in sediment. Relatively low concentrations of PFOS were found in sediments collected from the Detroit River (11), Baltimore harbor (12), and Niagara River (13) in the United States. In this study, we analyzed PFCs in a foodweb represented by sediment-associated tidal flat benthic species to evaluate the influence of sediments on the transfer of PFCs to benthic organisms. It is known that tidal flat organisms live in burrows filled with pore water containing large amounts of nutrient and suspended matter. Because the diet of tidal flat organisms ranges from seaweed to zoobenthos with sediment particles, the tidal flat ecosystem may be a good indicator to examine the role of sediments on the fate of PFCs in the environment. On the basis of this background, PFOS, PFOA, perfluorononanoate (PFNA), perfluorohexane sulfonate (PFHS), and perfluorooctane sulfonamide (PFOSA) were analyzed in sediments and benthic organisms, such as clam, mussel, lugworm, crab, herbivorous, and omnivorous mudskippers 10.1021/es0603195 CCC: $33.50
2006 American Chemical Society Published on Web 07/13/2006
for crabs. All biological samples were stored at -20 °C until chemical analysis. Chemical Analysis. Perfluorinated compounds were analyzed following the method described previously (7, 14). Approximately 0.5-1 g of tissue was homogenized with 5 mL of Milli-Q water, and a portion of this homogenate (1 mL) was transferred into a polypropylene tube. One milliliter of 0.5 M tetrabutylammonium hydrogen sulfate solution and 2 mL of sodium carbonate buffer (0.25 M, pH 10) were added to the tube containing the extracts. One hundred nanograms of perfluruotobutane sulfonate (PFBS) was spiked into the sample as a surrogate standard, and the sample was thoroughly mixed for extraction. Five milliliters of methyl tert-butyl ether (MTBE) was added to the above mixture and the mixture was shaken for 20 min. After shaking, the homogenate was centrifuged at 3500 rpm for 25 min to separate organic aqueous layers. The supernatant (MTBE layer) was transferred and evaporated under nitrogen, and the residue was transferred with 1 mL of methanol. This extract was passed through a nylon mesh filter (0.2 µm) into a HPLC vial. The analysis of PFCs in sediment was similar to that described elsewhere (11). Sediment was dried at room temperature and approximately 5 g of sediment was placed in a 50-mL polypropylene tube. PFBS (5 ng) was spiked as a surrogate standard. Ten milliters of methanol was added and the mixture was shaken for 10 min and then sonicated using an ultrasonicator for 30 min. The extract was decanted after centrifugation at 3000 rpm for 15 min. Another 10 mL of methanol was added to the sample and extracted. The extract was evaporated to 1 mL using a gentle nitrogen stream and then filtered using a 0.2-µm nylon filter. Quantitative analyses were performed with a highperformance liquid chromatograph equipped with an electrospray tandem mass spectrometer (HPLC/MS/MS). Details of the analytical conditions, quality assurance, and quality control measures have been described previously (14, 15). The limit of detection (LOD) of target compounds was evaluated for each sample on the basis of the maximum blank concentration, the concentration factor, and a signalto-noise ratio of 2. The LODs of target chemicals were 0.3, 3.0, and 1.5 ng/g for PFOS, PFOA, and other PFCs (PFNA, PFHS, PFOSA), respectively. Recoveries of the surrogate standard, PFBS, ranged from 79 to 118% in samples; concentrations of PFCs in samples were not corrected for the recovery percentages.
FIGURE 1. Map showing the sampling location for sediments and organisms analyzed in this study. collected from a tidal flat in the Ariake Sea, Japan. In the same region, shallow water organisms, comprising five species of fish (filefish, sea bream, red sea bream, right eye flounder, and hammerhead shark), marine mammals (finless porpoise), and birds (mallard and black-headed gull) were also analyzed. The accumulation pattern of PFCs was compared with those of other class of contaminants, such as PCBs, tributyltin (TBT), and aromatic hydrocarbons (PAHs), to examine the potential sink for PFCs in the aquatic ecosystem.
Materials and Methods Samples. Eighty-three samples of sediments and organisms were collected from shallow water and tidal flat areas of the Ariake Sea off the coast of Japan during 1999 and 2004 (Figure 1). Details of the samples analyzed in this study are shown in Table 1. Five species of fish, marine mammals, and omnivorous birds were collected from shallow waters of the Ariake Sea. Liver tissues were analyzed for fish, marine mammal, and birds. Samples of oyster, mussel, clam, lugworm, crab, and herbivorous and omnivorous mudskippers were collected from the tidal flat at the Tojin River estuary (Figure 1). Liver, soft tissue, and whole body samples were analyzed for fish, shellfish, and lugworm, respectively. Soft tissues of shellfish from several individuals were pooled on the basis of individual species. Hepatopancrea was analyzed
TABLE 1. Details of Samples Analyzed in This Study sample name
collection date
filefish sea bream red sea bream right eye flounder hammerhead shark finless porpoise mallard blackheaded gull
Oct 2003 Oct 2003 Oct 2003 Oct 2003 June 2000 Oct 1999-Oct 2002 Feb 2000-Feb 2001 Feb 2001
oyster mussel clam lugworm crab mudskipper (herbivourous)a mudskipper (omnivorous)b sedimentc
Oct 2003 Oct 2003 Oct 2003 Oct 2003 Oct 2003 Oct 2003 Oct 2003 Jan 2004
a
body length (cm)
n
Shallow Water 5 20 ( 0.6 5 21 ( 1.4 5 23 ( 1.1 5 28 ( 0.6 1 >100 5 107 ( 19 11 51 ( 2.0 2 36 Tidal Flat 5 5 6 5 2 10 6 5
6.9 ( 1.6 5.3 ( 0.2 3.4 ( 1.6 na 3.0 11 ( 1.3 6.2 ( 0.4 na
body weight (g) 273 ( 23 240 ( 48 377 ( 54 353 ( 38 nad 22 400 ( 13 000 1 100 ( 110 270 45 ( 33 25 ( 4.3 6.1 ( 1.0 na 8.8 15 ( 5.5 3.5 ( 0.6 na
tissues analyzed liver liver liver liver liver liver liver liver soft tissue soft tissue soft tissue whole hepatopancrea liver liver na
Boleophthalmus pectinirostris. b Periophthalmus modestus. c Average and std of water content in. d na: not available. VOL. 40, NO. 16, 2006 / ENVIRONMENTAL SCIENCE & TECHNOLOGY
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TABLE 2. Mean Concentrations and Range (ng/g wet wt) of Fluorinated Contaminants in Samples from the Ariake Sea sample name
n
tissue analyzed
PFOS
filefish
5
liver
sea bream
5
liver
red sea bream
5
liver
right eye flounder
5
liver
hammerhead shark finless porpoise
1 5
liver liver
11
liver
blackheaded gull
2
liver
oyster
5
soft tissue
