Environ. Sci. Technol. 2005, 39, 8243-8250
Polybrominated Diphenyl Ethers and Polychlorinated Biphenyls in a Marine Foodweb of Coastal Florida B O R I S J O H N S O N - R E S T R E P O , †,§ K U R U N T H A C H A L A M K A N N A N , * ,† RUDOLF ADDINK,† AND DOUGLAS H. ADAMS‡ Wadsworth Center, New York State Department of Health and Department of Environmental Health Sciences, State University of New York at Albany, Empire State Plaza, P.O. Box 509, Albany, New York 12201-0509, and Florida Fish & Wildlife Conservation Commission, Fish & Wildlife Research Institute, 1220 Prospect Avenue #285, Melbourne, Florida 32901
Nine species of marine fish, including teleost fishes, sharks, and stingrays, and two species of marine mammals (dolphins) collected from Florida coastal waters were analyzed for polybrominated diphenyl ethers (PBDEs) and polychlorinated biphenyls (PCBs) to evaluate biomagnification factors (BMF) of these contaminants in a coastal foodweb. In addition, bottlenose dolphins and bull sharks collected from the Florida coast during the 1990s and the 2000s were analyzed for evaluation of temporal trends in PBDE and PCB levels in coastal ecosystems. Mean concentrations of PBDEs in muscle tissues of teleost fishes ranged from 8.0 ng/g, lipid wt (in silver perch), to 88 ng/ g, lipid wt (in hardhead catfish), with an overall mean concentration of 43 ( 30 ng/g, lipid wt. Mean concentrations of PBDEs in muscle of sharks ranged from 37.8 ng/g, lipid wt, in spiny dogfish to 1630 ng/g, lipid wt, in bull sharks. Mean concentrations of PBDEs in the blubber of bottlenose dolphins and striped dolphins were 1190 ( 1580 and 660 ng/g, lipid wt, respectively. Tetra-BDE 47 (2,2′,4,4′-) was the major congener detected in teleost fishes and dolphin samples, followed by BDE-99, BDE-153, BDE-100, and BDE-154. In contrast, BDE-209 was the most abundant congener in sharks. Concentrations of PBDEs and PCBs in dolphins and sharks were 1-2 orders of magnitude greater than those in lower trophic-level fish species, indicating biomagnification of both of these contaminants in the marine foodweb. Based on the analysis of sharks and dolphins collected over a 10-year period, an exponential increase in the concentrations of PBDEs and PCBs has occurred in these marine predators. The doubling time of PBDE and PCB concentrations was estimated to be 2-3 years for bull sharks and 3-4 years for bottlenose dolphin.
Introduction Polybrominated diphenyl ethers (PBDEs) are synthetic organic compounds used extensively as additive flame* Corresponding author phone: (518)474-0015; fax: (518)473-2895; e-mail:
[email protected]. † State University of New York at Albany. ‡ Fish & Wildlife Research Institute. § Present address: Environmental and Computation Chemistry Group, University of Cartagena, Colombia. 10.1021/es051551y CCC: $30.25 Published on Web 10/05/2005
2005 American Chemical Society
retardants in a wide variety of consumer products. PBDEs have been produced chiefly as three commercial technical mixtures: pentabromodiphenyl ether (pentaBDE), octabromodiphenyl ether (octaBDE), and decabromodiphenyl ether (decaBDE). PentaBDE has been used mainly as an additive (up to 30% in weight) to meet the requirements in the manufacturing of flexible polyurethane foam for more than 25 years (1). The polyurethane foam is used in basic home products, including upholstered couches, chairs, curtains, carpet padding, and mattresses. OctaBDE is used in acrylonitrile-butadiene-styrene-based polymers applied to computer monitors, and in other related electronic appliances. DecaBDE makes up 83% of the PBDEs manufactured globally (2) and is used mainly in high-impact polystyrene for television sets, computer cases, and electronic equipment. Like polychlorinated biphenyls (PCBs), PBDEs are found in abiotic samples (e.g., air, water, and sediment), wildlife, and human tissues around the world (3-5). Although the sources of human exposures can be multiple and variable, it has been reported that fish and shellfish were the main contributors to human intake of PBDEs in the European countries and Japan, while meat products were the major contributors to the total intakes of PBDEs in Canada and the USA (6). Although studies have reported the occurrence of PBDEs in freshwater fish species from several locations (4, 7-11), little is known about PBDE concentrations in coastal marine fish. Furthermore, food-chain magnification of PBDEs in coastal marine ecosystems has not been studied in detail. The aim of this study was to determine PBDE concentrations in muscle tissue from several species of fishes including teleosts (bony fishes), sharks, and stingrays (cartilaginous fishes), and in blubber tissue from dolphins that occupy differing trophic levels in a coastal marine foodweb of Florida. Determination of both PBDE and PCB concentrations allowed comparison between the two classes of contaminants. In addition, we analyzed archived samples of shark muscle tissue and dolphin blubber collected in the 1990s and in the early 2000s to assess the patterns of temporal change for PBDEs and PCBs.
Material and Methods Sampling. A total of 88 specimens from nine species of marine fishes and two species of dolphins were analyzed in this study. Fish species included were: Atlantic sharpnose shark (Rhizoprionodon terraenovae; n ) 5), spiny dogfish (Squalus acanthias; n ) 5), bull shark (Carcharhinus leucas; n ) 13), Atlantic stingrays (Dasyatis sabina; n ) 7), striped mullet (Mugil cephalus; n ) 6), hardhead catfish (Arius felis; n ) 8), red drum (Sciaenops ocellatus; n ) 11), spotted seatrout (Cynoscion nebulosus; n ) 7), and silver perch (Bairdiella chrysoura; n ) 6). Samples were collected from estuarine waters of the Indian River Lagoon and adjacent offshore coastal waters of Florida in 2004 by the staff of the Florida Fish & Wildlife Conservation Commission-Fish and Wildlife Research Institute (FWC-FWRI). For all fishes, samples were placed directly on ice and transported to the laboratory, where gender, standard length (SL), and weight were recorded. Precaudal length (PCL) was recorded for shark species, and disk width (DW) was recorded for ray species. When possible, maturity of fish was determined by macroscopic examination of gonads, examination of claspers on male sharks and rays, or by comparison of size with known size-at-maturity estimates. A clean stainless steel knife was used to remove axial muscle tissue samples from the left dorsal area above the lateral line and anterior to the origin of the first dorsal fin. Tissue samples from stingrays were removed from the VOL. 39, NO. 21, 2005 / ENVIRONMENTAL SCIENCE & TECHNOLOGY
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406 (305-466) UN UN UN
538 (342-840)
20 (13-27) 76 (72-79) 93 (76-100) 179 (104-252) 214 (93-274) 225 3M, 3F, 1UN 5F 2M, 3F 5M, 6F, 2UN 11M, 9F F 2004 2004 2004 1993-2004 1991-2004 1994 Mean (range). UN ) unknown. a
7 5 5 13 20 1 Atlantic stingray spiny dogfish Atlantic sharpnose shark bull shark bottlenose dolphin striped dolphin
muscle muscle muscle muscle blubber blubber
132 (37-293) 1730 (547-3570) 533 (311-782) 13 (4-27) 44 (30-58) 31 (25-35) 2M, 1F, 4UN 6M, 5F 8F 2004 2004 2004 muscle muscle muscle 7 11 8
trophic level and feeding habits
carnivore (juvenile fishes, eggs of invertebrates) herbivore (grazing diatoms, microalgae, detritus, and inorganic sediment) carnivore (fishes and shrimp) carnivore (crustaceans and fishes) omnivore (fishes, mollusks, algae, seagrasses, and various invertebrates crustacean) carnivore (small fishes, mollusks, and crustaceans) carnivore (small fishes and crabs) carnivore (small fishes, shrimp, crabs, and mollusks) carnivore (small- and medium-sized fishes) carnivore (small- and medium-sized fishes) carnivore (small- and medium-sized fishes) 69 (54-100) 1002 (739-1171) 17 (15-20) 35 (31-38) 6UN 6F 2004 2004
weight (g)a length (cm)a gender date of collection tissue analyzed
muscle muscle 6 6
spotted seatrout red drum hardhead catfish
The measurement of tri- to hexa-BDE congeners was accomplished by use of a Finnigan Trace gas chromatograph Ultra coupled with a MAT95XP high-resolution mass spectrometer (GC-HRMS). Measurements were carried out at a resolution of R > 9000-10 000. The ion source temperature was kept at 280 °C. A DB-5MSITD capillary column coated with 5% phenyl methylpolysiloxane (30 m length, 0.25 mm
n
Identification and Quantification. Extracts were injected into an Agilent 6890 gas chromatograph coupled to an Agilent series 5973 mass selective detector (MSD) for the determination of PCB congener concentrations. A RTX-5MS capillary column coated with 5% phenyl methylpolysiloxane (30 m length × 0.25 mm i.d., 0.25 µm film thickness; Restek Corp., PA) was used for the separation of individual congeners. The MSD was operated in an electron impact (70 eV), selected ion monitoring mode. PCB congeners were monitored at the two most intense ions of the molecular cluster. An equivalent mixture of Kanechlor (KC300, 400, 500, and 600), with known PCB composition, was used in the identification of PCB congeners. Quantification of PCB congeners was based on external calibration standards containing known concentration of di- through deca-CB congeners. Concentrations of individually resolved peaks of PCB isomers were summed, to obtain total PCB concentrations.
species
Chemical Analysis. PCB and PBDE congeners were analyzed following the method described elsewhere (1214). Twenty grams of muscle tissue or 3 g of blubber was homogenized and mixed with anhydrous sodium sulfate and extracted in a Soxhlet apparatus for 16 h using dichloromethane and hexane (3:1; 400 mL). The extract was rotaryevaporated at 40 °C, and an aliquot of 1 mL was used for the determination of lipid by gravimetry. The remaining extract was spiked with chlorobiphenyl congeners 30 (2,4,6-) and 204 (2,2′,3,4,4′,5,6,6′-) as surrogate standards. Extracts were purified by passage through a multilayer silica gel packed glass column (Davisil, 100-200 mesh, Aldrich, Milwaukee, WI). Samples were then eluted at a rate of 1 mL/min with 15% dichloromethane in hexane (150 mL), rotary-evaporated, and concentrated to 100 µL under a gentle stream of N2.
TABLE 1. Attributes of Teleost Fishes, Sharks, Stingrays, and Dolphins Analyzed from Coastal Waters of Florida
Archived blubber samples from bottlenose dolphin (Tursiops truncatus; n ) 20) collected along the western (Gulf of Mexico) and eastern (Atlantic Ocean) coasts of Florida during 1991-2004 were analyzed. Blubber samples from the western coast of Florida came from offshore waters of Charlotte County (n ) 3), Manatee County (n ) 5), and Sarasota County (n ) 6), as a part of the Marine Mammal Stranding Network Program. Blubber samples from the east coast of Florida were collected from estuarine waters of the Indian River Lagoon (n ) 6) by Hubbs-Sea World Research Institute. Dolphin samples from the west coast of Florida were comprised of 11 adults, 3 subadults, and 1 calf, whereas those from the east coast were comprised of 1 adult, 2 subadults, and 3 calves/fetus. One blubber sample of adult striped dolphin (Stenella coeruleoalba; n ) 1) collected along the west coast (Sarasota County) of Florida was also included. Archived samples of dorsal muscle from bull shark (Carcharhinus leucas; n ) 13) were used in this study for the analysis of temporal trends. Six adult and one juvenile bull shark samples (n ) 7) collected by the FWC-FWRI in 20022004 were from coastal waters adjacent to the Indian River Lagoon, whereas those collected in 1993-1994 were all juveniles (n ) 6). Further details of the samples are given in Table 1.
silver perch striped mullet
left dorsal area distal to the vertebral column. Care was taken to ensure that the sample made no contact with skin, scales, or other surrounding surfaces during the extraction process. The muscle tissue samples were placed directly in sterile polyethylene bags, frozen, and stored at -20 °C until analyzed. Specific details of the samples are given in Table 1.
TABLE 2. ∑PBDE and ∑PCB Concentrations (ng/g, lipid wt) in Muscle Tissue of Teleost Fishes, Sharks, and Stingrays, and in Blubber of Dolphin from Coastal Waters of Florida PBDE congeners fata (%)
species
28
U-TBDEb
47
66
85
99
100
138
153
154
183
209
∑PBDEa
