Environ. Sci. Technol. 2004, 38, 1667-1674
Congener-Specific Accumulation and Food Chain Transfer of Polybrominated Diphenyl Ethers in Two Arctic Food Chains H A N S W O L K E R S , * ,† B E R T V A N B A V E L , ‡ A N D R E W E . D E R O C H E R , †,§ ØYSTEIN WIIG,| KIT M. KOVACS,† CHRISTIAN LYDERSEN,† AND GUNILLA LINDSTRO ¨ M‡ Norwegian Polar Institute, N-9296 Tromsø, Norway, Department of Natural Sciences, O ¨ rebro University, 701 82 O ¨ rebro, Sweden, and Zoological Museum, Natural History Museum and Botanical Garden, University of Oslo, P.O. Box 1172, Blindern, N-0318 Oslo, Norway
Congener-specific accumulation and prey to predator transfer of 22 polybrominated diphenyl ethers (PBDEs) were assessed in polar cod, ringed seal, polar bear, and beluga whale. Although the concentrations found were relatively low, these results show that PBDEs have reached the Arctic. PBDE congeners 47, 99, and 100 were dominant in all species studied. The pattern in ringed seal was somewhat simpler than in polar cod, with PBDE 47 accounting for more than 90% of the total PBDEs. In contrast, beluga whales, feeding on prey similar to that of ringed seals, showed higher PBDE levels and a more complex PBDE pattern than ringed seals. In contrast, polar bears contained only PBDE 47 in relatively small amounts. These differences in levels and patterns are likely due to species-specific differences in PBDE metabolism and accumulation. The metabolic index suggested that PBDEs 47 and 99 accumulate to the same magnitude as PCB 153 (PCB ) polychlorinated biphenyl) in ringed seals and beluga whales. In contrast to beluga whales, ringed seals can metabolize PBDE 100 to some extent. Polar bears are seemingly capable of metabolizing virtually all PBDEs and are therefore unsuitable as indicators for PBDE contamination in the environment.
Introduction Polybrominated diphenyl ethers (PBDEs) are man-made chemicals used as flame retardants in a variety of consumer products such as electronic equipment, building materials, plane and car seats, and clothing (1). About 75% of the PBDEs produced consist of 10-BDE, but possibly due to selective uptake into food chains (2) or debromination of the 10-BDEs (3, 4) predominantly 4- and 5-BDEs accumulate (5). Sources of environmental PBDE contamination include leakage from consumer products and industrial facilities that manufacture * Corresponding author phone: +47-77750521; fax: +47-77750501; e-mail:
[email protected]. † Norwegian Polar Institute. ‡ O ¨ rebro University. § Current address: Department of Biological Sciences, University of Alberta, Edmonton, Canada T6G 2E9. | University of Oslo. 10.1021/es030448a CCC: $27.50 Published on Web 02/14/2004
2004 American Chemical Society
PBDEs, but also from disposal sites of PBDE-containing products (6, 7). PBDEs are closely related to polychlorinated biphenyls (PCBs), and these compounds share physical-chemical properties of high stability and lipid solubility, resistance to enzymatic degradation, and low vapor pressure (6-8). Consequently, these compounds are transported into remote areas, such as the Arctic, where they accumulate through the food chain and ultimately reach top predators such as seals, whales, and polar bears (Ursus maritimus) (5-7). Similar to PCBs, the bioaccumulative potential varies by congener. In particular, bioacumulation of PBDEs 47, 99, and 153 in blue mussles (Mytilus edulis) appeared to be similar to or higher than that of PCBs (2). In marine mammals PBDEs preferentially accumulate in the lipid-rich blubber, similar to PCBs, but also occur in organs such as liver, adrenals, ovaries, and brain (7). PBDE congeners 47, 99, and 100 show particularly high biomagnification in fish-eating birds and mammals (1, 7-10). While compounds such as PCBs and chlorinated pesticides seem to be stabilizing or declining in Arctic wildlife (11, 12), PBDEs are considered an increasing pollution problem worldwide. A few years ago these “PCBs of the 21st century” were discovered in sperm whales (Physeter macrocephalus) beached along the coast of Denmark and The Netherlands (8), indicating that PBDEs had reached the deep sea and were transported through the food chain. It has been estimated that PBDE concentrations in biota are doubling every 5 years (13, 14). A variety of biological effects similar to those of PCBs have been described for PBDEs, such as cytochrome P450 enzyme induction (15-18), effects on thyroid and steroid hormone homeostasis (6, 19), immunotoxicity (20), and estrogenic effects (21). Marine mammals including seals, whales, and polar bears are considered to be particularly sensitive to the effects of contaminant exposure because they are long-lived and feed high in the food chain. As a result, they are exposed to relatively high contaminant levels and can accumulate increasing concentrations in their body tissues during their entire life span. The mobilization of blubber lipids during annual events, such as mating, molting, and lactation, when food intake might be reduced, may result in dramatic effects because accumulated contaminants suddenly may become bioavailable by entering the circulation. Although information on contaminant concentrations in arctic marine mammals is quite extensive (11, 22), information on brominated fire retardants in most arctic top predators is scarce and is usually focused on a limited number of congeners. In addition, virtually no information is available on food chain transfer and congener-specific accumulation/ metabolism of PBDEs in different arctic species. Therefore, in the current paper we aim to assess congener-specific transfer and accumulation of a comprehensive selection of PBDEs in a few key species within the arctic food web, i.e., polar cod (Boreogadus saida), ringed seal (Phoca hispida), beluga whale (Delphinapterus leucas), and polar bears.
Experimental Section Sample Collection and Preparation. Polar cod was caught in eastern Svalbard in Storfjorden in summer 2001 using professional fishing equipment. Samples were wrapped in aluminum foil and stored at -20 °C until analysis. Ringed seals were shot northeast of Svalbard, approximately at 82°N, 13°90′-33°23′E, during a legal Norwegian hunt in 1999. A full blubber core was sampled dorsally at 60% of VOL. 38, NO. 6, 2004 / ENVIRONMENTAL SCIENCE & TECHNOLOGY
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the total body length, wrapped in aluminum foil, and stored at -20 °C until analysis. Beluga whales were live-captured in Storfjorden, Svalbard, between Aug 22 and Aug 24, 1998 using a “trawl” net (150 × 8 m, mesh size 15 cm) set from the beach at an angle of about 45°. The whales were herded into the net opening using two Zodiacs. Following capture, the whales were untangled from the net and restrained in shallow water with a hoop net held around the head and a cushioned rope tied around the caudal peduncle that was anchored to shore. The standard length was measured to the nearest 5 cm, and the sex was determined on the basis of examination of the genitalia. Animals were classified into age groups on the basis of body size and skin color (23). Blubber samples (whole cores) were collected from an area about 10 cm in front of the mid dorsal ridge, using a custom-made, hollow, stainless steel metal rod (diameter 6 mm, length 150 mm). All samples were wrapped in aluminum foil and stored at -20 °C until analysis. Polar bears were captured using a projectile syringe containing the drug Zoletil (Verbac, Carros, France) fired from a helicopter (24). Standardized morphometric measurements were collected from each captured bear. Fat biopsies were collected from the rump using an 8 mm biopsy punch. All capture and sampling protocols were approved by the National Animal Research Authority of Norway (NARA; Norwegian Animal Health Authority, P.O. Box 8147 Dep., N-0033 Oslo, Norway). Chemical Analyses. The samples were analyzed for 22 different PBDEs (4-BDE a, b, c, d, 47, e, 66, g; 5-BDE a, b, c, 100, e, f, 99, g, 85; 6-BDE a, 154, c, 153, 138) and 5 methoxylated metabolites (4-BDE-O-methoxy a, b, c; 5-BDE-O-methoxy a, b), as described previously (9, 25). Briefly, samples were homogenized in a mortar with sodium sulfate (1:5). About 1 g of the homogenized tissue was packed in a Suprex standard extraction vessel (10 mL). An internal standard consisting of 13C-labeled PBDE 77 and PCB 153 was added before the SFE extraction. On the top of the sample around 4.5 g of basic aluminum oxide (AlOx) was added as a fat retainer. The extractions were carried out on a Suprex Autoprep/Accutrap SFE using CO2 as the supercritical fluid. The chamber temperature was 40 °C and the pressure 280 bar during extraction at a flow rate of 2 mL/min for 25 min. All the analytes were trapped on a C18 solid sorbent (ODS, Octadecylsilica). The restrictor and trap temperatures were kept at 45 and 40 °C, respectively. After completion of the extraction the trap was rinsed with 3.5 mL of hexane and 3.5 mL of methylene chloride at a rate of 2 mL/min. After addition of the recovery standard containing 13C-labeled PCBs 128 and 178 in tetradecane the sample volume was reduced to 30 µL, producing an extract ready for GC/MS analysis. Separate lipid determination was performed by applying a part (∼1 g) of the homogenate on a small column and quantitatively extracting with methylene chloride and hexane (1:1). The weight of the extracted lipids was determined gravimetrically. Selected ion SIR HRGC/MS spectra were recorded using an Agilent 6890 gas chromatograph coupled to an Agilent 5973 mass spectrometer. Chromatographic separation was achieved by splitless injection of 2 µL on a nonpolar DB-5 column (30 m, 0.25 mm, internal diameter 0.25 µm) using helium as the carrier gas. The GC oven was programmed as follows: 180 °C initial hold for 2 min, increase at a rate of 15 °C/min to 205 °C, followed by an increase of 3.7 °C/min to 300 °C, final hold at 300 °C for 15 min. The injector temperature was kept at 250 °C and the GC interface temperature at 275 °C. The two most intense ions of the molecular ion cluster were monitored using electron impact (EI) ionization for 4-BDE (m/z 483.7, 485.7), 5-BDE (m/z 563.6, 1668
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565.6), and 6-BDE (m/z 641.5, 643.5) in addition to masses for the 13C-labeled internal standard (m/z 495.71, 497.68). The quantification standard consisted of 4-BDE 47, 5-BDEs 99 and 100, and 6-BDE 153, and detected PBDEs were quantified against a PBDE of the same bromination level closest to its retention time. PCB 153 was quantified against a quantification mix containing several PCBs at each chlorination level of which only PCB 153 was used. The detection limit (DL) was calculated at a signal-tonoise ratio of 3 (S/N > 3) and depended on the amount of lipids extracted. The cod and the ringed seal samples containing less lipids were rerun on the GC/MS system using negative chemical ionization (NCI) with methane as a reagent gas while monitoring masses 79 and 81 to achieve acceptable detection limits. The DLs for the cod, ringed seal, and white whale samples were 0.05-0.1 ng/g depending on the sample size. A somewhat higher DL was calculated for the polar bear samples (1-5 ng/g). Laboratory blanks were all well under 10% of the levels in the samples. PBDE congeners not present in the quantification mix were positively identified as PBDEs when the retention time was within the expected time window in addition to a bromine isotope ratio of the two most abundant ions in the molecular ion cluster within 10% of the theoretical ratio. The unidentified BDEs were numbered according to Lindstro¨m et al. (9). No standards for methoxylated BDEs (BDE-O-Me) were available at the time of analysis; BDE-O-Me’s were positively identified by acquiring full scan GC/MS mass spectra. BDE-O-Me was found to elute just after the BDE with the same number of bromine atoms. During routine analysis of BDE-O-Me the two most abundant ions in the molecular bromine cluster were analyzed in the EI mode. Quantification of the BDE-O-Me was done against a BDE with the same number of bromine atoms assuming a similar response during EI ionization. Data Analyses. The geometric mean concentrations and 95% confidence intervals were calculated for individual PBDE congeners in the different species. The total of the different contaminant groups was calculated by summing the raw data for each animal, calculating the ln-transformed mean of the animals, and taking the exponent of this mean. The contribution of each congener to the total PBDEs measured was assessed in all four species, while the relative presence of each congener, expressed as a percent of PCB 153, was calculated in each species as well. PCB 153 has been used as a reference congener because it is one of the most persistent PCB congeners and hardly is metabolized in animals. The ratio between the relative presence in predator and prey (percent of PCB 153 predator/percent of PCB 153 prey), the metabolic index (MI), indicates if the particular compound accumulates more (MI > 1) or less (MI < 1) than PCB 153 (26). This value in addition indicates biomagnification from prey to predator (27) and is as such a quantitative measure for food chain accumulation. Differences in the relative presence between species were calculated using a t-test, after logarithmic transformation of the individual data.
Results PBDE Concentrations and Patterns in the Polar CodRinged Seal-Polar Bear Food Chain. From the 22 brominated compounds measured, only 4-BDE 47, 5-BDEs 85, 99, and 100, 6-BDE 154, and a methoxylated 4-BDE were found above the detection limit in polar cod (Table 1). Ringed seals contained in addition 4-BDEs d and 66, but 5-BDE 85, 6-BDE 154, and the methoxy 4-BDE were below detection (Table 1). Concentrations of PBDEs in ringed seals were overall higher than in polar cod, with almost an order of magnitude higher values for PBDEs 47 and 99 (Table 1). Only 4-BDE 47 was detected in polar bears. The level of this congener was 1.5
TABLE 1. Geometric Mean Concentrations (ng/g of Lipid) and 95% Confidence Intervals for Selected BDEs in the Polar Bear Food Chaina 4-BDE d mean 95% low 95% high
nd nd nd
mean 95% low 95% high
0.13 0.10 0.15
mean 95% low 95% high mean 95% low 95% high a
47 2.09 1.33 3.28
5-BDE 66
85
99
100
Polar Cod (n ) 3) 0.10 0.31 0.10 0.18 0.10 0.55
6-BDE 154
4-BDE-O-ME a
∑PBDE
0.16 0.10 0.25
0.72 0.58 0.91
3.55 2.53 4.98
nd nd nd
nd nd nd
18.3 14.1 23.7
nd nd nd
0.13 0.08 0.20
16.8 12.1 23.3
0.07 0.03 0.20
nd nd nd
nd nd nd
27.4 13.0 57.7
nd nd nd
Polar Bear Male (n ) 10) nd nd nd nd nd nd nd nd nd
nd nd nd
nd nd nd
27.4 13.0 57.7
nd nd nd
45.6 29.5 70.3
nd nd nd
Polar Bear Female (n ) 10) nd nd nd nd nd nd nd nd nd
nd nd nd
nd nd nd
45.6 29.5 70.3
Ringed Seal (n ) 9) 0.66 0.39 0.42 0.27 1.04 0.58
nd ) not detectable
FIGURE 1. PBDE pattern (percent of total PBDEs measured) in polar cod, ringed seal, polar bear, and beluga whales. times higher in male polar bears and about 3 times higher in female bears compared to ringed seal (Table 1). The contribution of each PBDE congener to the total PBDEs measured showed that in polar cod, ringed seal, and polar bear 4-BDE 47 dominated (Figure 1). In polar cod this congener comprised about 60% of the total PBDEs, while the remaining 40% consisted of methoxylated 4-BDE (20%) and smaller fractions of 5-BDEs 85, 99, and 100 and 6-BDE 154 (Figure 1). In ringed seal PBDE 47 comprised more than 90% of the total PBDEs, but also minor fractions of an unidentified tetra-BDE congener and 4-BDEs 99 and 100 were found (Figure 1). PBDE Concentrations and Patterns in the Polar CodBeluga Whale Food Chain. Thirteen out of 22 brominated compounds were detected in white whales, with overall the highest levels in the calf and lowest levels in adult females (Table 2). Juvenile and adult male beluga whales had a substantially more complex PBDE pattern as compared to
polar cod, ringed seal, and polar bears. Male beluga whales had somewhat lower blubber PBDE concentrations than the subadult animals, but differences were relatively small (Table 2). Methoxylated 4-BDE c dominated in both juveniles and adult males, followed by PBDE 47 (Figure 1). Unidentified 4-BDE congener b, 5-BDEs 99 and 100, and the methoxylated 4-BDE b also made a small but significant contribution to the total PBDE concentration (Figure 1). Adult females were surprisingly different from the males and the juveniles; only 4-BDE 47 and the methoxylated 4-BDE c were detected in quantifiable amounts. Food Chain Transfer and Bioaccumulation of PBDEs. In the polar cod-ringed seal-polar bear food chain polar cod showed a relative presence for PBDE congeners 47 and 99 (expressed as a fraction of PCB 153) similar to that of ringed seal, while 4-BDEs d and 66 were only present as minor fractions of PCB 153 in ringed seals (Figure 2a). 5-BDEs 85 and 100 and 6-BDEs 153 and 154 had a lower relative VOL. 38, NO. 6, 2004 / ENVIRONMENTAL SCIENCE & TECHNOLOGY
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TABLE 2. Geometric Mean Concentrations (ng/g of Lipid) and 95% Confidence Intervals for Selected BDEs in Juvenile Beluga Whale Blubbera 4-B DE
5-B DE
a
c
d
47
66
1.40
0.89
6.20
147
0.88
0.23 0.03 1.78
0.26 0.03 2.21
1.42 0.87 2.32
90.0 60.8 133
0.36 0.03 3.83
g
a
99
100
2.70
8.90
6.40 3.92 10.4
8.77 5.93 13.0
4- BDE- O-Me b
c
∑ PBDE
1.41 1.52
18.8
89.2
279
0.21 0.40 0.01 0.03 6.38 4.68
13.8 10.3 18.5
106 79.1 142
234 174 314
6-BDE 154
a
Calf (n ) 1) nd 0.46
Juveniles (n ) 4) mean 95% low 95% high
0.09 0.03 0.01 0.0 1.03 0.19
Males (n ) 2) mean (sd) 27.4 (0.4) 0.26 (0.4) 1.50 (0.1) 69.7 (12) 0.43 (0.6) nd
nd 2.97 (0.5) 7.26 (0.4)
nd
nd 5.16 (7.3) 73.2 (16) 161 (23)
nd
nd
Females (n ) 2) mean (sd) a
nd
nd
nd
17.1 (0.6)
nd
nd
nd
nd
nd
nd
11.8 (17) 28.9 (17)
Mean and standard deviation for male and female beluga whales. nd ) not detectable.
presence, or were completely absent, in ringed seals as compared to polar cod (p < 0.001 for PBDE 100) (Figure 2a). Polar bear males and females showed a significantly lower relative presence of PBDE 47 compared to ringed seals (p < 0.001 for both sexes) (Figure 2a). There was no difference between male or female polar bear in terms of the relative presence of this congener. Despite a low but quantifiable presence of 5-BDEs 99 and 100 in ringed seals, these compounds were below detection in polar bears (Table 1, Figure 2a). The short beluga whale food chain (polar cod-beluga whale) showed a substantially different transfer and accumulation of PBDEs than the polar bear food chain. A roughly similar relative presence in polar cod and beluga whales (juveniles and males) was found for 4-BDE 47 and for 5-BDEs 99 and 100 (Figure 2b). Unidentified 4-BDE congeners a, c, d, and 66 had a low but quantifiable relative presence in beluga whales, but were nondetectable in polar cod (Table 2, Figure 2b). In contrast, the relative presence of 5-BDE 85 and 6-BDEs 153 and 154 was lower in beluga whales than in polar cod. The MI showed values close to 1 for PBDE 47 in ringed seal and beluga whale (Figure 3). In contrast, MI for this congener was far below 1 in polar bears (p < 0.001). PBDEs 99 and 100 showed a metabolic index of about 0.7 and 0.2, respectively, in ringed seals, while in beluga whales these values were significantly higher than in ringed seals, i.e., 1.4 (p < 0.05) and 0.7 (p < 0.001), respectively (Figure 3).
Discussion The detection of a variety of PBDEs in arctic fish and marine mammals indicates that these compounds have reached even remote arctic areas and, like PCBs, are long-range transported and transported through the arctic marine food web. Although levels in the arctic animals studied were relatively low, there is reason for concern since PBDEs are being produced and used in increasing amounts and are transported northward (10, 28). This will result in an increasing exposure of arctic wildlife in many years to come. A documented increase in blubber PBDE concentrations in Canadian beluga whales between 1982 and 1997 illustrates the increasing exposure in the Arctic (28). Consequently, PBDEs pose an increasing environmental threat for the Arctic. Relating contaminant levels in animals from different geographical locations may be somewhat tricky mainly because differences in contaminant sources, contaminant transport pathways, diet, and species may confound such comparisons. Therefore, such associations should preferably be made between animals from similar taxonomic families. Levels of PBDEs in all animals from the current study were low compared to those in animals from other areas, probably 1670
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reflecting larger distances from contaminant sources. Liver concentrations of PBDE 47 in herring (Clupea harengus) and cod (Gadus morua) from the North Sea were 15 and 60 times higher, respectively, than those of the arctic cod in this study (29). Similarly, sole (Solea spp.) from different locations from Canada’s west coast also showed 15-60 times higher PBDE 47 levels (5). Similar to the PBDE concentration pattern in herring and cod liver from the North Sea (29), PBDEs 47, 99, and 100 were quantitatively most important in the polar cod from the present study. Ringed seals from the Canadian Arctic showed substantially lower PBDE concentrations than the ringed seals from the present study (14), about 20 times lower for PBDEs 47, 99, and 100, and may reflect differences in PBDE transportation routes. In general the PBDEs in seals show a geographic trend similar to that of the PBDEs in fish. Substantially higher PBDE levels were found in animals from more southern areas compared to the Svalbard ringed seal, but all have PBDEs 47, 99, and 100 as dominant congeners. Ringed seals from the Baltic had almost 20 times higher concentrations of PBDE 47 and almost 10 times higher levels of PBDE 99 (1). Harbor seals from the North Sea sampled in 2000 showed an even more dramatic difference compared to the arctic seals: PBDE 47 was almost 2 orders of magnitude higher, while PBDEs 99 and 100 were more than 600 and 200 times higher, respectively (29). In harbor seals from the North Sea 16-70 times higher PBDE 47 and more than 150 times higher PBDE 99 were reported (8). In contrast to the Svalbard ringed seal, Baltic ringed seals also contained quantifiable amounts of the methoxylated 4-BDEs b and c (1). Primary sources for these methoxylated PBDEs (which were also found in appreciable amounts in the Svalbard beluga whales) are currently unknown, but one of the possibilities is that these compounds originate from metabolism or natural formation by microorganisms in the environment. Another possibility is that these compounds are the result of contaminant metabolism in the liver of vertebrates; in a first reaction a hydroxy-PBDE is formed (phase I reaction), followed by methylation (phase II reaction) in the liver or intestine to form a methoxylated PBDE (1, 6). Compared to beluga whales from the Canadian Arctic (27), the levels in Svalbard beluga whales were high. For PBDEs 47, 99, and 100 about 9 times higher levels were recorded in juvenile beluga whales from Svalbard. In contrast, similar to the ringed seals from Svalbard, PBDE levels in Svalbard beluga whales were substantially lower than in cetaceans from the Southern Atlantic Ocean and the North Sea area. However, similar to the Svalbard beluga whales, the PBDE pattern was also rather complex in the southern cetaceans. Levels of PBDEs 47, 99, and 100 in harbor porpoise (Phocoena phocoena) from the U.K. were more than 15, 45,
FIGURE 2. (a, top) Relative presence (percent of PCB 153) of different PBDEs in the polar bear food chain: polar cod-ringed seal-polar bear. (b, bottom) Relative presence (percent of PCB 153) of different PBDEs in beluga whales and their main prey (polar cod). and 25 times higher, respectively (10), than those of the beluga whales. Analyses of PBDEs in pilot whale (Globicephala melas) juveniles, males and females from the Faeroe Islands, revealed 19 quantifiable compounds (9), but similar to the beluga whales from Svalbard, most PBDE concentrations were low in these animals, with the exception of 4-BDE 47 and 5-BDEs 99 and 100. These congeners were about 20, 100, and 30 times higher, respectively, than in juvenile beluga whales. Similar to the beluga whales, the highest PBDE levels were found in the juvenile pilot whales and porpoises, and the lowest in the females (9, 10). Although the sample sizes for the adult Svalbard beluga whales were low, the large concentration differences between males and females probably reflect transfer from mother to calf during lactation and suggest a selective transfer of these compounds from mother to offspring in cetaceans. A similar favorable mother-
offspring transfer was confirmed in a previous study in rodents, where PBDEs were effectively transferred from females to their young (30). Contaminant concentrations and patterns in wildlife may be influenced by the total amount of body fat (31-33) and qualitative and quantitative differences in diet, while speciesspecific contaminant metabolism also plays a crucial role (24, 34). For example, the fact that only a few PCB congeners are found in polar bears is thought to be due to their exceptional metabolic capacity (35), while the more limited ability of cetaceans to metabolize contaminants is reflected in a more complex contaminant pattern. Consequently, it appears that PBDE persistence is highly congener- and species-specific. Compared to polar cod, ringed seals contained a simpler PBDE pattern with higher concentrations of some congeners, especially PBDEs 47, 99, and 100. This VOL. 38, NO. 6, 2004 / ENVIRONMENTAL SCIENCE & TECHNOLOGY
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FIGURE 3. Metabolic index for PBDE congeners 47, 99, 100, and 154 in ringed seal, beluga whale, and polar bear male and female: *, significant difference at p < 0.05 (ringed seal vs beluga whale); ***, significant difference at p < 0.001 (ringed seal vs beluga whale, polar bear vs ringed seal, polar bear vs beluga whale). suggests that some PBDE congeners (i.e., PBDEs 85 and 154) can be metabolized by this species. On the other hand, the presence of PBDEs in ringed seal that were below detection in polar cod (i.e., 4-BDEs d and 66) suggests accumulation of these compounds in seals. Polar bears, the apex predator of the arctic food web, feeds predominantly on ringed seals, but in this species only PBDE 47 could be detected. However, due to the relatively high detection limit, the presence of trace amounts of other PBDEs cannot be excluded. However, the relatively low amounts of the dominant congener PBDE 47 in polar bears, especially in comparison to PCB 153, indicate that the accumulation and persistence of this relatively stable PBDE congener is low in this species. The relatively high contaminant concentrations and more complex PBDE pattern in beluga whales compared to ringed seals is surprising since these species occupy similar trophic levels and have dietary overlap, with polar cod being an important prey species for both predators (36, 37). Some of the differences might be related to differences in size and relative blubber content between seals and whales. Differences in size result in differences in metabolic rate (MR) and thus food intake. The average weight of the ringed seals in this study was about 50 kg, while the whales weighed around 1000 kg. MR (KJ) in whales and seals can be expressed as
MR ) 4.19 × 70(body mass)0.75 (38)
(1)
This difference in body mass means that ringed seals need almost twice as much food per kilogram of body mass compared to the whales and are therefore, assuming similar pollution load in the food, exposed to twice the amount of contaminants on a mass-specific basis. However, since blubber is the main storage site for pollutants (39) and since the surface-to-volume ratio is much lower in the large whales than the small seals, the whales need less blubber per kilogram of body mass to maintain thermal balance. The sculp mass (blubber and skin) relates to body mass as 1672
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sculp ) 0.70(body mass)-0.146 (40)
(2)
This gives a 1000 kg whale a blubber mass of about 255 kg (0.25 kg of blubber/kg of body mass) and a 50 kg ringed seal a blubber mass of about 20 kg (0.40 kg of blubber/kg of body mass). Thus, the seals are ingesting more pollutants via food on a mass-specific basis, but they store these pollutants in a blubber depot that is considerably larger on a mass-specific basis than that of the whales. On the basis of a combination of these two opposing influences, the contaminant levels in the blubber of ringed seals would be expected to be about 1.25× that found in the whales. The finding that the total PBDE concentrations were more than 15 times higher in beluga whales compared to ringed seals suggests a substantial reduced PBDE metabolism in whales relative to seals. Indeed, several authors have indicated that whales have a reduced metabolism for compounds requiring cytochrome P450 2B/3A-like action, such as the meta,para-unsubstituted PCBs (41-43). The observation that toothed whales in general have relatively high PBDE levels and a more complex PBDE pattern compared to seals (7, 8, 34, 44) supports the suggestion that these species have a more limited metabolic capacity for these compounds than seals. Biomagnification of PBDEs is considered to be particularly large from fish to marine mammals (13, 34). Biomagnification through the food chain is often expressed as the biomagnification factor (BMF): the ratio between contaminant concentrations in predator and prey (32). Often, the lipidnormalized concentrations of a single tissue are used; however, these results may be seriously biased, particularly in marine mammals where contaminants are concentrated in the blubber. Additionally, the pronounced lipid cycles of this tissue result in large changes in lipid-normalized contaminant concentrations (45). Wet weight concentrations based on the total body mass are thus essential to calculate BMF properly. Since measuring wet weight-based contami-
nant concentrations in marine mammals is quite complicated (27), the current study used MI instead of BMF. The results from MI and BMF correspond well in seals (27). Assuming a similar uptake through the gut for the different PBDE congeners and PCB 153 within a species, MI expresses the accumulation of that congener relative to PCB 153 (26). An MI above 1 reflects a higher relative presence of a PBDE congener in predator than in prey and therefore indicates accumulation larger than that of PCB 153; an MI below 1 indicates a lower accumulation than PCB 153 and may imply a higher metabolism than that of PCB 153. The relatively high MI for congeners 47 and 99 in ringed seals suggested a relatively low metabolism of these congeners, while an MI of less than 0.2 for PBDE 100 suggested some metabolism. The persistence of these three congeners in seals was confirmed in a previous study (34), which also suggested that PBDEs 47 and 99 are probably persistent, while PBDE 100 might be metabolized in harbor seals. Beluga whales had an MI exceeding 1 for PBDEs 47 and 99, indicating a strong tendency of these compounds to accumulate. Likewise, PBDE 100 with an MI of about 0.7 probably accumulates more in beluga whales than in seals, while 6-BDE 154 showed an MI around 0.2, indicating that this compound may be metabolized to some extent by beluga whales. The presence of 4-BDEs a, c, d, and 66 in beluga whales but not in polar cod indicates that also these congeners accumulate in beluga whales. The MI also confirmed the high metabolic capacity in polar bears. PBDE 47 is generally considered persistent (7, 8, 13), but rats and mice exposed to radio-labeled PBDE 47 showed some metabolism (46). However, the rate of metabolism and excretion varies considerably between these species. The low MI for PBDE 47 in polar bears illustrated that this species, like some rodents, are capable of metabolizing this congener. However, the structure of PBDEs 47, 99, 100, and 154 does not support metabolism of any of these congeners. PBDEs 47 (2,2′,4,4′-BDE), 99 (2,2′,4,4′,5-BDE), 100 (2,2′,4,4′,6BDE), and 154 (2,2′,4,4′,6,6′-BDE) all have at least two o-bromines and two p-bromines. In PCBs such a Cl substitution pattern blocks the orhto,meta and the meta,para areas to enzyme attack, making them stable, even in polar bears (26, 34). Clearly, the criteria for persistence in PCBs with a certain Cl substitution pattern do not apply to the same extent to PBDEs with a similar Br substitution pattern. Possibly, differences in bond strength and more tension in the molecule because of the presence of the larger Br atoms between PCBs and PBDEs result in different persistence of congeners with similar substitution patterns. However, differences in uptake between the two compound classes can at present not be ruled out and might be responsible for the observed differences in persistence. In conclusion, PBDEs are present at low, but detectable, concentrations in arctic cod and marine mammals, including polar bears. These contaminants have found their way into the Arctic and are transferred and accumulated through the food chain. PBDEs 47 and 99 selectively accumulate in ringed seals, while beluga whales accumulated a wider range of PBDE congeners, probably due to their relatively low capacity to metabolize these compounds. Only PBDE 47 was detected in polar bears, indicating metabolism of most congeners in this species. However, a low MI for PBDE 47 indicated that in polar bears accumulation of this relatively persistent congener is low relative to that of PCB 153. Therefore, to assess time trends for PBDE accumulation in arctic animals, polar bears are less suitable as study animals because of metabolism of most, if not all, PBDEs in this species. Beluga whales and, to a lesser extent, ringed seals offer far better possibilities to monitor these contaminants because of their lower PBDE metabolism.
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Received for review April 29, 2003. Revised manuscript received November 12, 2003. Accepted November 18, 2003. ES030448A
