Environ. Sci. Technol. 2005, 39, 5584-5591
Polybrominated Diphenyl Ether Trends in Eggs of Marine and Freshwater Birds from British Columbia, Canada, 1979-2002 J O H N E . E L L I O T T , * ,† LAURIE K. WILSON,† AND BRYAN WAKEFORD‡ Canadian Wildlife Service, 5421 Robertson Road, Delta, British Columbia V4K 3N2, Canada, and National Wildlife Research Centre, Carleton University, Ottawa, Ontario K1A 0H3, Canada
Temporal, spatial, and interspecific trends in polybrominated diphenyl ether (PBDE) flame retardants were determined in eggs of marine and freshwater bird species from the province of British Columbia, Canada. Temporal trends in the Fraser River estuary, 1983-2002, were examined by analysis of eggs of great blue herons (Ardea herodias) and from the Strait of Georgia marine ecosystem, 1979-2002, in eggs of double-crested cormorants (Phalacrocorax auritus). Results were compared to those from eggs of the osprey (Pandion haliaetus) taken along the lower Fraser River and along the Columbia River near Castlegar, British Columbia, and of a pelagic seabird, the Leach’s stormpetrel (Oceanodroma leucorhoa), collected at a colony on the Queen Charlotte Islands. Mean concentration of ∑PBDE, 455 µg/kg w.w., were highest in heron eggs collected in 2002 from the Fraser estuary. Concentrations in eggs of cormorants and ospreys taken from sites of varying urban influence tended to be about half that value. Leach’s storm petrel eggs had only trace amounts of ∑PBDE (3.38 µg/kg), despite having similar concentrations of PCBs and organochlorine pesticides to the other species. PBDEs increased exponentially with a doubling time of 5.7 years in eggs of both herons and cormorants. Over this period of increasing PBDEs, major chlorinated hydrocarbons, such as PCBs and DDE, were stable or decreased. The PBDE pattern was relatively consistent in most years and sites, with BDEs 47 > 100 > 99 > 153 > 154 > 28 > 183. This was interpreted as evidence of technical pentaBDE formulations as primary sources of the contamination, with the octaBDE formulations as secondary. Higher resolution analysis of a subsample of the eggs revealed the presence of up to nine other congeners, including BDE209 (range: 0.9-1.8 µg/kg), indicating exposure and uptake of decaBDE sourced congeners in North American foodchains. At some locations, concentrations of pentabrominated congeners and mixtures in fish are approaching levels potentially toxic to fish-eating birds, based on rodent studies and calculations of dietary intake from fish data. * Corresponding author phone: (604)940-4680; fax: (604)946-7022; e-mail:
[email protected]. † Canadian Wildlife Service. ‡ Carleton University. 5584
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Introduction Polybrominated diphenyl ethers (PBDEs) are widely used as flame retardants in a large variety of textiles, plastics, and foams (1). PBDE compounds have been found in samples of wildlife from many areas of the globe, including deep sea marine mammals, alpine fish, birds of prey, and arctic seabirds (2-5). From the 1980s to the early 2000s, PBDE concentrations increased significantly in North American fish and wildlife samples (6-8). For example, the doubling time was less than 3 years for the sum of major PBDE congeners in eggs of herring gulls (Larus argentatus) from colonies throughout the Great Lakes (9). In addition to the herring gull, the Canadian Wildlife Service has used several other marine and freshwater bird species for monitoring spatial and temporal trends in persistent contaminants in specific ecosystems. Since the early 1970s, eggs of the great blue heron (Ardea herodias) have been collected for estuarine and the double-crested cormorant (Phalacrocorax auritus) for coastal monitoring of the Canadian portion of the Georgia Basin-Puget Sound ecosystem (10-12). Both species are resident year-round in the Georgia Basin, primarily in the vicinity of their breeding colonies, and eat principally smaller forage fish. In the recent past, investigations focused on exposure and health effects on herons and cormorants of polychlorinated dibenzo-pdioxin (PCDD) and dibenzofuran (PCDF) compounds released by pulp and paper mills and other forest industry operations into the Georgia Basin (10, 12, 13). The piscivorous osprey (Pandion haliaetus) is a long distance migrant wintering in Mexico and Central America but has still proved useful for monitoring persistent contaminants along the major river systems of the Pacific Northwest (14, 15). Ospreys return to the wintering site 3-4 weeks prior to egg laying and feed extensively on local fish before and during egg production, thus producing a largely local signal in egg lipids (16). The Leach’s storm-petrel (Oceanodroma leucorhoa) is a pelagic planktivore that feeds along the shelf break while breeding and then ranges widely outside of the breeding season; it has proven useful in previous studies for monitoring open ocean contamination (17). To examine spatial, temporal, and interspecific trends in PBDEs in the British Columbia environment, we retrieved archived egg samples for the above species and analyzed them using current methodology.
Methods Information on species collected along with some pertinent life history is summarized in Table 1. Sample Collection and Preparation. Samples of great blue heron eggs were taken from a colony at the University of British Columbia (UBC) in Vancouver (Figure 1). In 1983, heron eggs were collected from a colony at Crescent Beach, on Boundary Bay, approximately 40 km southeast of the UBC colony. Heron eggs were also collected from a colony at Quamichan Lake near the small town of Duncan on Vancouver Island. Eggs from that site contained relatively low levels of chlorinated hydrocarbons (10, 11). Cormorant eggs were taken from a colony on Mandarte Island, located some 25 km from the city of Victoria. Osprey eggs were collected from nests located on the Pitt River close to its confluence with the Fraser River and within the Greater Vancouver urban area and from upstream and downstream of the city of Castlegar. Eggs of Leach’s storm petrel were taken from nesting burrows on Hippa Island. The monitoring protocol for herons involve collection of 5-10 eggs from different nests in each of a series of 10.1021/es050496q CCC: $30.25
2005 American Chemical Society Published on Web 06/21/2005
TABLE 1. Information on Diet and Range of Marine and Freshwater Bird Species Collected for PBDE Monitoring, 1979-2002, from British Columbia, Canada species
scientific name
diet and feeding strategy
Small forage fish including: seaperch (Cymatogaster spp.), midshipman (Porichthys spp.), sculpin (Leptocottus spp.), gunnels (Pholis spp.), flounders (Platichthys spp.), sticklebacks (Gasterosteus spp.). Caught by stealth wading. double-crested Phalacrocorax Forage fish, including: gunnels, seaperch, prickleback cormorant auritus (Lumpenus spp.), sandlance (Ammodytes spp.), herring (Clupea spp.). Caught by pursuit diving. osprey Haliaetus Fish including suckers (Catostomidae), carp, chubs and pandion pikeminnow (Cyprinidae), trout, salmon and whitefish (Salmonidae) and catfishes (Ictaluridae). Caught by plunge diving. Leach’s storm Oceanodroma Pelagic plankton including amphipods and myctophid -petrel leucorhoa fishes. Caught by surface dabbling.
great blue heron
Ardea herodias
range Pacific coastal populations remain year-round residents near breeding colonies. Coastal, mainly local resident after reaching breeding age. April to September near nest, winters Mexico and Central America. April to October within foraging range of breeding colony. Winter ranges widely across Pacific.
Georgia region, pooled homogenates of heron and cormorant eggs collected from 1983 and 1979, respectively, to 2002 were retrieved from the specimen bank and analyzed for PBDEs. Eggs collected from ospreys in 1991 and 1997 at sites on the Columbia River and from 2000 near the lower Fraser River were retrieved from the Specimen Bank, as were eggs of Leach’s storm-petrel from a remote colony on the Queen Charlotte Islands. For all species, the number of eggs to analyze was constrained by availability of samples from the specimen bank, which accounts for some of the variability in sample size.
FIGURE 1. Collection locations for bird eggs in British Columbia, Canada, 1979-2002. Herons from UBC (1), Crescent Beach (2), and near Duncan (3); cormorants from Mandarte Island (4); osprey from Pitt River (5) and Castlegar upstream (6) and downstream (7); and Leach’s storm-petrels from Hippa Island (8). colonies, at intervals of 2-5 years around the Strait of Georgia. Osprey eggs (5-10 from individual nests) are collected approximately every 5 years from nests at specific sites along the Fraser and Columbia River systems. Cormorant and storm-petrel collections are part of the CWS seabird monitoring program and involve collection of 15 eggs from individual nests every 4 years along coastal BC and analysis of 5 pools of 3 eggs per pool. Subsamples of the eggs are archived individually and as equal weight pools at -40 °C at the Canadian Wildlife Service National Wildlife Specimen Bank (18). To determine temporal trends, in the Strait of
Chemical Analysis. Egg homogenates for herons, 19832000, ospreys from 1991 and 1997, storm-petrels, and for cormorants collected in 1979, 1994, and 1998 were analyzed at the National Wildlife Research Centre according to previously described methods (9). Briefly, each sample of egg pool homogenate was ground with anhydrous sodium sulfate and extracted with 1:1 dichloromethane:hexane spiked with a PBDE surrogate spiking solution (EO-4981, Cambridge Isotope Laboratories, Cambridge, MA). The final volume of extract was reduced by rotary evaporation. Lipid content was determined gravimetrically. Lipid was removed by gel permeation chromatography. Final cleanup was with a florisil column and dichloromethane:hexane, followed by further reduction under a nitrogen stream and an exchange of solvent to toluene, and further spiking with 13C12BDE77. Samples were analyzed with a VG AutoSpec double focusing gas chromatograph-mass spectrometer (GC-MS). Recoveries of the surrogate standards were calculated by comparison to an external standard solution in order to ensure accurate and precise functioning of the method. Minimum detection limits (MDL) were 0.01-0.05 µg/kg wet weight of the egg. Recoveries of the 13C12-BDE internal standards averaged 82 + 15%. Results from the recovery of surrrogates with the same number of bromines were used to correct the concentrations for each congener. Blank samples contained inconsequential concentrations ( 100 > 99 > 153 > 154 > 183 (Figure 3). The calculated doubling time, 1979-2002, for ∑PBDEs in cormorant eggs was 5.7 years (r2 ) 0.662, p ) 0.016) and for the individual BDE congeners as follows: BDE17 (NS); BDE28 (NS); BDE47, DT ) 6.0 (r2 ) 0.604, p ) 0.024); BDE49 (NS), BDE99, DT ) 6.4 (r2 ) 0.591, p ) 0.027); BDE100, DT ) 5.0 (r2 ) 0.724, p ) 0.01); BDE153, DT ) 5.5 (r2 ) -0.0742, p ) 0.008); BDE154, DT ) 5.4 (r2 ) 0.0663, p ) 0.016); BDE183 (NS).
TABLE 3. Polybrominated Diphenyl Ether (PBDE) Congeners and Sum of Congeners in Eggs of Great Blue Herons (µg/kg, Wet Weight) Collected from Colonies on the Southwest Coast of British Columbia, 1983-2002 location year N % fat % water BDE 28 BDE 49 BDE 47 BDE 100 BDE 99 BDE 154 BDE 153 BDE 183 ∑BDEsg ∑BDEsh
Duncan 2000a 10 6.15 81.5 NDd 0.69 15.5 11.9 9.40 4.41 5.69 ND 47.9 NA
Crescent Beach 1983a 1 6.93 80.5 ND 0.04 0.77 0.16 0.20 0.12 NQ ND 1.31 NA
UBC 1987a 27 6.04 81.5 0.05 0.09 4.37 1.41 2.16 1.59 2.63 NQ 12.5 NA
UBC 1988a 16 6.79 81.9 0.04 0.08 4.66 1.55 2.02 1.77 3.51 0.32 14.2 NA
UBC 1991a 5 6.68 81.3 0.08 0.21 20.1 8.97 12.3 4.58 6.96 0.07 53.6 NA
UBC 1992a 10 6.38 81.9 0.17 1.37 28.3 10.3 11.7 40.7 6.37 0.22 99.6 NA
UBC 1993a 6 5.82 82.9 0.17 1.37 42.9 21.8 21.4 8.20 11.8 0.30 109 NA
UBC 1994a 5 6.14 82.1 0.20 1.40 53.8 25.9 17.4 8.90 15.1 0.32 124 NA
UBC 1996a 5 6.04 82.4 0.41 1.99 120 56.1 54.5 18.8 34.3 0.44 288 NA
UBC 1998a 5 6.96 80.9 NQe 0.74 64.8 51.2 34.8 18.5 30.9 NQ 202 NA
UBC 2000a 10 5.71 81.7 0.16 1.73 53.9 56.2 28.9 19.0 32.9 0.29 194 NA
UBC 2002b 5 5.92 NAc 0.12f 2.50 82.8 88.6 174 35.0 67.7 1.43 455 457
a Chemical analysis conducted at NWRC, Ottawa, ON. b Chemical analysis conducted by AXYS Analytical, Sidney, BC. c NA ) not available. ND ) not detected. e NQ ) not quantifiable. f BDE congeners 28 and 33 coelute. g Sum of 18 congeners (BDEs 7, 8, 15, 17, 28, 47, 49, 66, 85, 99, 100, 119, 138, 140, 153, 154, 155, and 183). h Sum of 18 congeners listed in “g” plus additional 26 (BDEs 1, 2, 3, 10, 11, 12, 13, 25, 30, 32, 33, 35, 37, 71, 75, 77, 105, 116, 126, 166, 181, 190, 206, 207, 208, and 209). d
TABLE 4. Polybrominated Diphenyl Ether (PBDE) Congeners and Sum of Congeners (µg/kg Wet Weight) in Eggs of Double-Crested Cormorants Collected from Mandarte Island on the Coast of British Columbia, 1979-2002 year 1979a 1985b 1990b 1994a 1995b 1998a 2002b N 1 5 11 3 10 6 3 % fat 4.85 5.61 5.35 5.45 6.08 6.05 6.58 % water 83.8 NAc NA 83.7 NA 84.1 NA BDE 28 NDd NDe 0.01e 0.74 0.06e 0.06 0.05 BDE 49 ND 0.01 0.02 ND 0.07 ND 0.06 BDE 47 0.11 1.85 6.89 172 81.5 53.7 16.3 BDE 100 0.03 1.27 6.99 88.3 57.8 55.1 22.3 BDE 99 0.06 2.59 7.46 53.7 41.1 44.0 9.18 BDE 154 0.01 0.48 2.05 25.6 11.8 15.0 4.15 BDE 153 0.03 0.57 2.14 39.2 16.2 25.8 9.65 BDE 183 NQf 0.03 0.04 NQ 0.08 NQ 0.04 ∑BDEsg 0.24 6.93 26.0 385 210 195 62.5 ∑BDEsh NA 7.32 26.2 NA 211 NA 63.3 a Analysis conducted at NWRC, Ottawa, ON. b Analysis by Axys Analytical, Sidney, BC. c NA ) not available. d ND ) not detected. e BDEs 28 and 33 coelute. f NQ ) not quantifiable. g Sum 18 congeners (BDEs 7, 8, 15, 17, 28, 47, 49, 66, 85, 99, 100, 119, 138, 140, 153, 154, 155, and 183). h Sum of 18 congeners listed in “g” plus additional 26 (BDEs 1, 2, 3, 10, 11, 12, 13, 25, 30, 32, 33, 35, 37, 71, 75, 77, 105, 116, 126, 166, 181, 190, 206, 207, 208, and 209).
FIGURE 2. Trends in major PBDE compounds in eggs of great blue herons collected at a colony in the estuary of the Fraser River, British Columbia, Canada, 1983-2002 (no. 1, Figure 1). Chemical analysis at NWRC 1983-2000, at AXYS 2002 (see text for details). Leach’s Storm-Petrel. Six BDE congeners were quantified in the pooled homogenate of Leach’s storm-petrels analyzed by NWRC. Concentration of all congeners were 100. Analysis of a larger sample of osprey eggs in conjunction with fish sampling and stable isotope analysis could further elucidate the processes occurring in the Columbia River. Such a study could also be illuminating for the Fraser system. Interspecific Comparisons. The ∑PBDE concentrations reported here for herons, cormorants, and ospreys are comparable to those reported for herring gulls in the Great Lakes (9), when expressed on a lipid weight basis to take into account variation in mean lipid content of the different
species. For example, mean concentrations in heron eggs at UBC in 1996 at 5100 µg/kg lipid are greater than the concentration, 2700 µg/kg lipid, in Lake Ontario herring gulls, but less than the 6200 µg/kg lipid in samples from Lake Michigan. Concentrations of ∑PBDEs (w.w.) in eggs of ospreys, collected during 2000-2002 in the Delaware and Chesapeake Bay areas, ranged from 82 to 725 µg/kg, similar to those reported here and for other fish-eating birds in general (24, 25). Our PBDE data in ospreys may be biased upward somewhat, as samples for PBDE analysis were selected based on having higher PCB concentrations. In all of the species studied here, the PBDE congener pattern was dominated by pentabrominated BDEs, consistent with data for Great Lakes herring gulls (9), and harbor seals from San Francisco harbor (6). In guillemot (Uria algae) eggs from the Baltic sea, only tetra- and pentabrominated congeners were present (26). Swedish peregrine falcons, in contrast, which feed on both aquatic and terrestrial foodchains had a different pattern dominated by higher brominated congeners, BDEs 153 and 183. They also contained substantial concentrations of BDE209, thought to result from feeding on terrestrial foodchains (3). The potential for BDE209 to be released and to bioaccumulate to some degree is supported by our finding of low µg/kg quantities of that congener in fish-eating bird eggs. Toxicological Implications. Despite evidence of increasing concentrations of PBDEs in wildlife samples, there is a lack of pertinent toxicological literature. No data are currently available on critical effects levels either for dietary samples or wildlife tissues. Studies on laboratory rodents have reported effects of both pure pentabrominated congeners and of pentaBDE mixtures on neurobehavioral development and thyroid endpoints at doses as low as 0.6-0.8 mg/kg day (27). Using a broad assumption of comparable sensitivity for birds, a 1.5 kg osprey, for example, would need to ingest 0.9-1.2 mg per day of a pentaBDE mixture. Assuming a mean daily food intake of 275 g (large heron species) to 420 g (merganser species) and an intake efficiency of 0.8 (28), then the concentration in the diet would have to be 2.5-3.5 mg/kg pentaBDE to affect neurobehavioral endpoints based on the rodent data. Those concentrations are 3.8-5.4-fold more than the greatest concentration of total pentabrominated diphenyl ethers reported, for example for mountain whitefish collected in 1999 from the Columbia River (29). Most reported values for fish are lower. However, given the consistent evidence of exponential increases in biota, and potential variation in species sensitivity, there may be a risk to wildlife from PBDE exposure. Further field and laboratory studies are warranted. Of the species studied here, populations of ospreys generally have increased in recent years such as many other birds of prey. That increase is consistent with declining environmental concentrations of DDE and other chlorinated contaminants, combined with greater public awareness of their value and need of protection (30). This has led to less persecution and destruction at least of nesting habitat. Great blue heron populations in the Strait of Georgia may have declined in recent years, and the coastal subspecies is listed as a conservation concern in British Columbia (11). Although major threats are believed to be habitat fragmentation and disturbance during breeding, chlorinated hydrocarbons have likely impacted some breeding colonies (11). PBDEs should be considered as a potential emerging threat to populations of this species breeding in urban areas. Similarly, populations of both double crested and pelagic (P. pelagicus) have also decreased in recent years in the Strait of Georgia, and causative factors are unclear (22). Like herons, cormorant populations in the Strait of Georgia and elsewhere have exhibited biological effects associated with exposure to chlorinated hydrocarbons. Due to their more restricted breeding distribution and greater distance of main colonies VOL. 39, NO. 15, 2005 / ENVIRONMENTAL SCIENCE & TECHNOLOGY
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from urban sites, cormorants in the Strait of Georgia are likely at lower risk from any PBDE toxicity. Sources of PBDEs. Penta-BDE formulations are used almost entirely in polyurethane foam (PUF), much of which goes into furniture upholstery, while the deca and octa formulations are used primarily in the rigid thermoplastic housings of electronic equipment (1). The deca formulations comprise the greatest proportion of industrial PBDE use globally including North America, while octa formulations are used minimally (31). Those higher brominated formulations were considered less of an environmental threat due to lower bioavailability and no previous data on uptake by biota. The penta formulations comprise about 22% of North American industrial use (31); however, the congeners present in those mixtures, particularly BDE47, BDE99, and BDE101, appear to more readily escape to the environment, likely from rapid degradation of PUF products. The uptake of pentaBDEs by crickets raised on pieces of PUF provides a clear demonstration of bioavailability (1). In response to evidence of increasing environmental contamination by PBDEs, jurisdictions in Europe and North America and industrial associations in some countries have moved to severely restrict or ban the use at least of the pentaand octacommercial formulations. In Canada, PBDEs have been declared as toxic under the Canadian Environmental Protection Act, with a recommendation that the penta- and octaBDE formulations be slated for virtual elimination (31). Continued monitoring of PBDEs in indicator species will allow for tracking the success of regulatory actions.
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Acknowledgments S. Lee, P. Whitehead, I. Moul, and A. Breault assisted with sample collection. R. McNeil supervised sample archiving and retrieval. M. Simon analyzed samples at NWRC. S. Lee assisted with the preparation of graphics. R. Letcher made useful comments on an earlier version. Funding was provided by the Georgia Basin Ecosystem Initiative and Environmental Protection Branch of Environment Canada.
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Received for review March 14, 2005. Revised manuscript received May 16, 2005. Accepted May 24, 2005. ES050496Q
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