Article pubs.acs.org/est
Novel Flame Retardants in Urban-Feeding Ring-Billed Gulls from the St. Lawrence River, Canada Marie-Line Gentes,† Robert J. Letcher,‡ Élyse Caron-Beaudoin,† and Jonathan Verreault*,† †
Centre de recherche en toxicologie de l’environnement (TOXEN), Département des sciences biologiques, Université du Québec à Montréal, Montreal, QC, Canada ‡ Wildlife and Landscape Science Directorate, Science and Technology Branch, Environment Canada, National Wildlife Research Centre, Carleton University, Ottawa, ON, Canada S Supporting Information *
ABSTRACT: This study investigated the occurrence of a comprehensive suite of polybrominated diphenyl ethers (PBDEs) and current-use flame retardants (FRs) in ring-billed gulls breeding in a highly industrialized section of the St. Lawrence River, downstream from Montreal (QC, Canada). Despite major point-sources and diffuse contamination by FRs, nearly no FR data have been reported in birds from this area. Bis(2-ethylhexyl)-2,3,4,5-tetrabromophthalate (BEHTBP) was detected in 89% of ring-billed gull livers (mean: 2.16 ng/g ww; max: 17.6 ng/g ww). To our knowledge, this is the highest detection frequency and highest concentrations reported thus far in any avian species or populations. Dechlorane Plus (DP) isomers were also particularly abundant (anti-DP detected in 100% and syn-DP in 93% of livers). Other detected FR compounds (3−14% detection) included 2-ethylhexyl-2,3,4,5-tetrabromobenzoate (EHTBB), hexachlorocyclopentenyl-dibromocyclooctane (HCDBCO) and β-1,2-dibromo-4-(1.2-dibromoethyl)-cyclohexane (β-TBECH). Mean BDE-209 (57.2 ± 12.2 ng/g ww) in ring-billed gull livers was unexpectedly high for this midtrophic gull species, exceeding levels reported in several apex raptors such as peregrine falcons. BDE-209’s relative contribution to ∑PBDEs was on average 25% (exceeding BDE-47 and BDE-99) and contrasted with profiles typically reported for fish-eating gull species. The present study highlighted preoccupying gaps in upcoming FR regulations and stressed the need for further investigation of the sources of FR exposure in highly urbanized areas.
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INTRODUCTION A large suite of nonreactive flame retardants (FRs) are routinely added to consumer products such as electronic circuitry, upholstered furniture, and construction materials to comply with fire safety standards. These include the largely restricted polybrominated diphenyl ethers (PBDEs), which are now ubiquitous in the environment and have been detected in virtually all ecosystems and taxa, as well as numerous as yet unregulated halogenated compounds. 1 Mounting environmental concerns have led to the worldwide phaseout of Pentaand Octa-BDEs between 2004 and 2010, 2 and Deca-BDE was restricted in Europe in 2008. 3 In North America, industry members of the Bromine Science and Environmental Forum (BSEF) have agreed to voluntarily phase out production and use of Deca-BDE in Canada and the United States by the end of 2013.4,5 The increasing restrictions on PBDE production and use are resulting in the increased use of alternative FRs to meet flammability standards. Consequently, environmental levels of replacement or alternative FRs have been on the rise worldwide. For instance, the alternative FRs bis(2-ethylhexyl)-2,3,4,5-tetrabromophthalate (BEHTBP, also known as TBPH) and 2-ethylhexyl-2,3,4,5-tetrabromobenzoate © 2012 American Chemical Society
[(EHTBB, also known as TBB) (major compounds in Firemaster-550; replacing Penta-BDE)], 1.2-bis(2,4,6tribromophenoxy)ethane [(BTBPE) (major compound in FF680; replacing Octa-BDE)], and decabromodiphenyl ethane [(DBDPE) (major compound in Firemaster-2100; replacing Deca-BDE)] are already being detected in humans, as well as in a few captive and wild bird, marine mammal, and fish species, along with a series of other emerging FRs such as pentabromoethylbenzene (PBEB) and α- and β-isomers of 1,2-dibromo-4-(1,2-dibromoethyl)cyclohexane (TBECH).1 The chlorinated FR Dechlorane-Plus (DP), commercialized in the 1960s as a substitute for the pesticide Mirex has also been suggested as a possible replacement product for DecaBDE.6 DP is now classified as a high production volume chemical in the United States and is being detected globally in air, sediments, water, and biota.7 Recent research confirms that a number of these current-use FRs (e.g., BTBPE, β-TBECH, PBEB, and EHTBB) exhibit high bioaccumulation and Received: Revised: Accepted: Published: 9735
May 30, 2012 July 26, 2012 July 30, 2012 July 30, 2012 dx.doi.org/10.1021/es302099f | Environ. Sci. Technol. 2012, 46, 9735−9744
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Figure 1. Study site. Deslauriers Island is a 600 m long island in the St. Lawrence River downstream from Montreal, QC, Canada. It hosts one of the largest ring-billed gull colonies (48 000 nesting pairs) in North America.
1377.4 ng/g ww and 776.9 ng/g ww ∑PBDEs,15 falling within the higher range of PBDE contamination for the Great Lakes and St. Lawrence River Basin. A recent pan-Canadian study investigating FRs in several gull species reported that ∑PBDEs in herring gull eggs (781 ng/g ww) collected in 2008 just downstream from Montreal (Deslauriers Island) not only exceeded levels reported in Great Lakes colonies (134−440 ng/ g ww) but were the highest concentrations reported in Canada.16 Thus, both these studies support that the greater Montreal area is a potentially major “hotspot” with respect to FR contamination in avian species, but the exact sources of exposure for these birds have never been investigated. Furthermore, a more comprehensive screening of emerging FRs of potential environmental concern is critically needed. The present study addressed these knowledge gaps using the ring-billed gull (Larus delawarensis) as model species. The ringbilled gull was selected because of its omnivorous diet, which encompasses terrestrial prey items as well as aquatic organisms, and because of its important utilization of both urban and nonurban habitats.17 These characteristics make this mediumsize gull particularly well suited for investigating bioaccumulation of historical (Penta-BDE and Octa-BDE) and emerging, unregulated halogenated FRs that may not otherwise bioaccumulate in species feeding exclusively upon aquatic food webs.
biomagnification factors8 and undergo long-range atmospheric transport.9 Despite growing evidence that they may constitute substances of potential environmental concern to humans and wildlife, as demonstrated for PBDEs,2 current regulatory frameworks are lagging behind and do not provide adequate international oversight of these emerging or less-studied compounds. Birds represent ideal models to investigate the occurrence and fate of FRs in both terrestrial and aquatic ecosystems; resident species can be used as local sentinels, while those that migrate may provide insights from broader-scale exposure scenarios.10 Gulls (Larids) specifically have been extensively used in research focusing on aquatic ecosystems as the majority of gull species feed at high trophic levels and have been shown to accumulate FRs. In Canada and the United States, a considerable amount of research investigating spatial and temporal trends of FRs has focused on herring gulls (Larus argentatus) from the Laurentian Great Lakes. Contaminant levels in Great Lakes herring gull eggs have been closely monitored since the early 1970s, producing a wealth of invaluable data for a large suite of halogenated organics and trace elements.11−14 Conversely, only two studies on FRs in avian species breeding in the highly industrialized and densely populated sections of the St. Lawrence River (downstream from the Great Lakes) have been published. Blue herons eggs collected from colonies near Montreal in 2001−2002 contained 9736
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Table 1. Concentrations (ng/g wwa) of Current and Historical Use Halogenated FRs in Liver (n = 28) and Plasma (n = 30) of Ring-Billed Gulls Breeding in the St. Lawrence River Downstream from Montreal, QC, Canada liver samples >MLOD (%)
plasma
meanb ± S.E.
range
samples >MLOD
± ± ± ± ±
2.02−6.83 ND-64.0 0.70−38.4 ND-15.2 ND-19.8 ND-0.02 ND-0.37 ND-1.55 ND-0.23 ND-0.30 ND-17.6 ND-0.57 22.4−682 2.74−283
0 0 0 0 0 3 0 0 0 0 0 100 100
meanb ± S.E.
range
0.74 ± 0.02
0.55−1.08 ND ND ND ND ND ND-0.38 ND ND ND ND ND 3.54−90.3 0.70−23.8
lipids lipid content (%) ∑20non-PBDEsc,d anti-DP syn-DP total-HBCDe HCDBCO OBIND (or OBTMI) EHTBB α-TBECH β-TBECH/BDE-15 BEHTBP BB-101 ∑45PBDEsf BDE-209
100 100 93 89 4 4 11 3 14 89 18 100 100
3.79 16.0 6.06 2.38 5.22
0.20 3.0 1.64 0.67 1.02
2.16 ± 0.59 205 ± 32.0 57.2 ± 12.2
27.0 ± 4.05 6.99 ± 1.17
a Conversion of ng/g ww into ng/g lw can be found in Table S2, Supporting Information. bMeans were calculated if at least 50% of the samples had FR concentrations greater than the MLOQ. c∑20Non-PBDEs: sum of BB-101(2,2′,4,5,5′-pentabromobiphenyl), BTBPE (1,2.-bis(2,4,6tribromophenoxy)ethane), BEHTBP (bis(2-ethylhexyl)-2,3,4,5-tetrabromophthalate), DBDPE (decabromodiphenyl ethane), DP (Dechlorane Plus), DPTE (2,3-dibromopropyl tribromophenyl ether), EHTBB (2-ethylhexyl-2,3,4,5-tetrabromobenzoate), HBB (hexabromobenzene), HCDBCO (hexachlorocyclopentenyl-dibromocyclooctane), HBCD (hexabromocyclododecane), OBIND/OBTMI (octabromo-1.3.3-trimethyl-1phenyl Indane), PBBA (pentabromobenzyl acrylate), PBEB (pentabromoethyl benzene), PBPAE (pentabromophenyl allyl ether), TBCT (tetrabromo-o-chlorotoluene), TBECH (1,2-dibromo-4-(1,2-dibromoethyl)-cyclohexane), TBPAE (2,4,6-tribromophenyl allyl ether), pTBX (tetrabromo-p-xylene). dScreened for, but not detected: BTBPE, DBDPE, DPTE, HBB, PBBA, PBEB, PBPAE, TBCT, TBPAE, and pTBX . e Total-HBCD: sum of α-, β-, γ-HBCD after thermal isomerization into α-HBCD. f∑45PBDEs: see Table S3 in Supporting Information for a complete list of screened PBDE congener concentrations in liver and plasma.
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distance by a remote control system. 20 Birds were blood sampled immediately after capture using heparinized syringes, then euthanized by cervical dislocation for tissue collection. Liver and blood samples were kept on ice until the end of daily fieldwork (maximum 10 h). In the laboratory, liver was transferred to a −20 °C freezer and blood was centrifuged at 2500g during 7 min. Resulting plasma was stored at −20 °C until chemical analysis (see next section). Capture and handling methods were approved by the Institutional Committee on Animal Care (CIPA) of the Université du Québec à Montréal and comply with the guidelines issued by the Canadian Council on Animal Care (CCAC). Chemical Standards and Materials. Plasma (n = 30) and liver samples (n = 28) were screened for 47 PBDE congeners and 23 emerging FRs (Table S1 in Supporting Information). All PBDE congeners, α-HBCD, and 13C- labeled BDE-209 were purchased from Wellington Laboratories (Guelph, ON, Canada), as well as BTBPE, DBDPE, α- and β-TBECH, tetrabromo-o-chlorotoluene, pentabromoethylbenzene, hexabromobenzene, tetrabromo-p-xylen, and polybrominated biphenyl congeners (BB-101 and -153). Reference standards for 2,4,6-tribromophenyl allyl ether, pentabromophenyl allyl ether, pentabromotoluene, pentabromobenzyl acrylate and pentabromobenzyl bromide were purchased from SigmaAldrich (Mississauga, ON, Canada). 13C-Dechlorane Plus (DP) isomers (syn and anti) were purchased from Cambridge Isotope Laboratories (Cambridge, MA). Octabromo-1,3,3trimethyl-1-phenylindane was kindly donated by Dr. Åke Bergman (University of Stockholm, Sweden). Chemical analyses were performed at the National Wildlife Research Centre, Environment Canada (Ottawa, ON, Canada). Sample Preparation. Extraction and cleanup of plasma and liver samples were performed as described elsewhere,14,21
EXPERIMENTAL SECTION Study Area and Sample Collection. Fieldwork was conducted from April through June 2010 on Deslauriers Island (45°42′45″ N, 73°26′25″ W), that is, the site identified by Chen and co-workers16 as the most FR-contaminated gull colony in Canada. Deslauriers Island is a 600 m long island located ∼3.2 km downstream from the tip of Montreal in the St. Lawrence River (Figure 1). It hosts one of the largest ringbilled gull colonies in Eastern Canada with approximately 48 000 breeding pairs (2009 survey; P. Brousseau, Environment Canada; personal communication). It is located amidst a mosaic of landscape features, some of which represent significant point sources of FRs: Montreal’s densely populated urban core and industrial parks, the largest landfill within the province of Quebec (∼30 km from Montreal), and Canada’s largest wastewater treatment plant (primary-treated effluent released directly into the St. Lawrence River). The region also encompasses a number of low-exposure areas to FRs such as forests, lakes, and agricultural lands on which no sewage sludge is applied. At the beginning of the incubation period (i.e., mid-April to early May), ring-billed gull nests containing one or two eggs were randomly selected within the different sections of the colony and marked with a unique number. This preliminary step was repeated five times over a three week period so that a large number of nests (n > 300) with a known clutch initiation date would be available for the study based on the assumption that one egg is laid every second day.18,19 From mid-May to mid-June, i.e., once a sufficient number of preidentified nests had a complete clutch (3 eggs), randomly selected ring-billed gulls (males and females) were live-captured on their nest while incubating using a dip net or a nest trap triggered from a 9737
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been shown for various tissues that FRs do not necessary correlate with extractable lipid content and likely bind, at least in part, to proteins.23 Nevertheless, lipid-normalized data are presented in the text and in Supporting Information (Table S2) to facilitate comparisons with other studies.
with minor modifications. Briefly, thawed liver (1.5 g) and plasma (1 g) samples were homogenized with diatomaceous earth (DE; J.T. Baker, NJ), spiked with 100 μL of internal standards (BDE-30, BDE-156, 13C-BDE-209, 13C-syn-DP, and 13 C-anti-DP), and extracted using Accelerated Solvent Extraction (ASE 200, Dionex, Sunnyvale, CA) with 175 mL of 50:50 dichloromethane:n-hexanes (DCM:HEX). For liver samples, 10% of the extract was removed for lipid determination by gravimetry, and samples were cleaned up using gel permeation chromatography (GPC; O.I. Analytical, College Station, TX). Final sample cleanup on the remaining GPC fraction was performed using disposable solid-phase extraction (SPE) silica gel (SiOH) cartridges (Bakerbond SPE, 6 mL/500 mg, VWR, Mississauga, ON, Canada). Quantification. Identification and quantification of target FRs was performed using a gas chromatograph (GC) coupled to a single quadrupole mass spectrometer (MS) (Agilent Technologies 5890, Palo Alto, CA) operating in the electron capture negative ionization mode (GC/MS-ECNI). The analytical column (15 m × 0.25 mm × 0.10 μm) was a fused-silica DB-5 HT capillary column (J & W Scientific, Brockville, ON, Canada). Details on the injection mode, gas flow, and temperature ramping program have been described in details elsewhere.13,14 Quantification of PBDEs and current-use FRs was achieved using selected ion monitoring (SIM) mode for isotopic bromine anions 79Br- and 81Br-, except for BDE209 (m/z 487) and 13C-BDE-209 (m/z 495). The molecular ion m/z 652 was used for quantifying DP isomers and was also chromatographically resolved.22 Total-HBCD represents the sum of α-, β-, and γ-HBCD isomers as temperatures above 160 °C in the injection port caused the thermal isomerization of all isomers into α-HBCD. Quality Control and Assurance. Procedures included method blanks (DE) and injection of standard reference material (SRM 1947; Lake Michigan fish tissue) for each batch of ten samples (n = 3 batches). Background contamination of method blanks was negligible, and no blank correction was necessary except for BDE-170 in liver (ND-4.56 ng/g ww in blanks) and BDE-209 also in liver (0.95−2.62 ng/g ww in blanks). Hence, concentrations in liver samples were blankcorrected for those two congeners. Concentrations of FRs in all samples were quantified using an internal standard approach, and thus all analyte concentrations were inherently recoverycorrected. Method limits of quantification (MLOQs) and method limits of detection (MLODs) were based on replicate analyses (n = 8) of matrix samples spiked at a concentration of 3−5 times the estimated detection limit. MLOQs (defined as a minimum amount of analyte producing a peak with a signal-tonoise ratio (S/N) of 10) and MLODs (defined as S/N = 3) can be found in Table S1 of the Supporting Information section. Data Treatment. The arithmetic mean concentration of a given compound was calculated only if at least 50% of the samples (plasma or liver) had concentrations above the compound-specific MLOQ (Tables 1 and S1 in Supporting Information). When this criterion was respected, samples with FR concentrations below the MLOD were assigned a random value between zero and the compound-specific MLOD, while samples with concentrations below the MLOQ were assigned a random value between the MLOD and the MLOQ. Since no differences in FR concentrations were found between males and females (p = 0.96 and p = 0.65 for plasma and liver, respectively), all individuals were merged into one group. All data presented in tables are in ng/g wet weight (ww) as it has
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RESULTS AND DISCUSSION Non-PBDE Flame Retardants. Screening of liver samples for current-use FRs (Table 1) revealed high (>50% of samples) detection frequency of the following compounds: BEHTBP, DP (anti- and syn- isomers), and total-HBCD. Other detected compounds (ranging between 3 and 14% detection) included EHTBB, HCDBCO, OBIND, β-TBECH, and BB-101. Sum concentrations of current-use FRs and historical FRs (i.e., BB101) in liver were approximately one order of magnitude lower than PBDEs (∑45PBDEs: 205 ng/g ww; ∑20non-PBDEs: 16.0 ng/g ww). Current-use FRs were all below MLODs in plasma, with the exception of OBIND which was detected in one bird only (0.38 ng/g ww). BEHTBP and EHTBB. Possibly the most striking finding in the current-use FR liver data was the unexpectedly high occurrence of BEHTBP, which was detected in nearly all samples (89%), as well as its high concentrations (mean: 2.16 ng/g ww; max: 17.6 ng/g ww) relative to the other non-PBDE FRs. To our knowledge, this represents the highest detection frequency and the highest concentrations of BEHTBP reported thus far in avian species worldwide. This compound, along with EHTBB (detected in 11% of liver samples), is found in Firemaster 550, Firemaster BZ-54, and DP-45 and currently marketed by Chemtura Corporation (formerly Great Lakes Chemicals) as replacement products for the banned Penta-BDE. 24 They contain varying proportions of BEHTBP (15% in FM-550, 30% in FM-BZ54, 100% in DP-45) and EHTBB (35% in FM-550, 70% in FM-BZ54, 0% in DP45).25,26 Firemaster is mostly used in polyurethane foam while DP-45 serves as a plasticizer in polyvinylchloride (PVC), neoprene, and electrical coating.27 The higher detection frequency and higher concentrations of BEHTBP compared to EHTBB in ring-billed gull liver samples could therefore be indicative of DP-45 as a local source. Slower photodegradation of BEHTBP compared to EHTBB has also been suggested as a factor explaining its higher concentrations in environmental samples.28,29 Since their initial detection in house dust from the Boston area in 2006,30 BEHTBP and EHTBB have been found in sewage sludge of a few locations in the United States,24,31 as well as in gas and particle phase air samples collected near the shores of the Great Lakes from 2008 to 2010.25 The environmental fate of these compounds is largely unknown, and reports of BEHTBP and EHTBB in biota are still very scarce: only three studies documenting their occurrence in wildlife have been published at present. BEHTBP has been reported in eggs of peregrine falcons from Canada and from Spain,32 with fairly low detection frequency (33% in Canada and 8% in Spain). The Norwegian Climate and Pollution Agency recently reported on the occurrence of EHTBB and BEHTBP in birds (eider liver, kittiwake liver, and guillemot’s eggs), mammals (ringed seal liver, arctic fox liver, polar bear plasma), and fish (capelin) from Svalbard in the Norwegian Arctic.33 Detection frequencies of BEHTBP in bird eggs from Svalbard (50−70%) were lower than in present ring-billed gull livers, while EHTBB was detected more frequently (90−100%) in eggs from Svalbard than in ring-billed gull livers. The only 9738
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commercial product and indicated that no stereoselective enrichment is occurring in ring-billed gulls breeding in Montreal area. Published data on DP in avian species are still too scarce and heterogeneous (i.e., different tissues and species sampled) to draw robust conclusions about global spatial trends, but limited comparisons between European and North American studies suggest that North American birds generally exhibit greater DP body burdens than European birds. DP in eggs from Spanish storks (urban: 0.401 ng/g ww; national park: 0.105 ng/g ww)36 was 20- to 80-fold lower in comparison to ring-billed gull livers from the present study; comparisons between those storks’ eggs and Great Lake herring gull eggs revealed similar trends. Furthermore, eggs of Spanish peregrine falcons (1.78 ng/g lw) contained ∼20 times lower DP than eggs of Canadian peregrines (36.4 ng/g lw)37 and ∼80 times lower than ringbilled gull liver. In contrast, differences between our ring-billed gulls and Canadian peregrines were only 4-fold (peregrine > ring-billed gull). Apart from the discrepancies due to the different tissues sampled (i.e., eggs vs liver), it is possible that differences in dietary habits among the species sampled would partly explain the higher DP burden of Canadian birds, but Guerra et al.37 suggested that greater historical use of DP in North America and relative proximity of Canadian study sites to the DP production facility in Niagara Falls could be driving such trends. Information on the potential toxicity of DP is very scarce and critically needed. Available data on mammalian toxicity (i.e., Wistar rats and rabbits) originate from the manufacturer’s HPV (high production volume) test challenge report to the EPA39 and from an OxyChem-sponsored study.40 Both these reports concluded that the toxicity of DP was minimal (except for a dose-related decrease in liver and ovary weights in female rabbits in the challenge report). Only one study investigating avian toxicity has been published thus far.41 DP was not cytotoxic up to a maximum concentration of 3 μM in chicken embryonic hepatocytes, and no effect on pipping success was observed up to the highest nominal dose group of 500 ng/g egg. There are, however, no published data on potential endocrine-disrupting effects of DP in any species, chronic exposure studies for mammals and birds are lacking, and toxicity to aquatic species has never been investigated for this compound. Total-HBCD. Total-HBCD was the second most frequently detected (89%) current-use FR in ring-billed gull livers (equal with BEHTBP). HBCD has been used internationally as an additive FR in polystyrene foam, upholstery textiles, and electrical equipment for over 30 years.42 As PBDEs were gradually withdrawn from the global market, production and use of HBCD kept increasing worldwide (in North America particularly),43 and HBCD is now considered a high production volume by the EPA.44 Despite evidence of bioaccumulation, long-range atmospheric transport, and toxicity, it historically received much less attention than PBDEs and until now eluded international restrictions. However, at the seventh meeting of the Stockholm Convention (October 10−14, 2011, Geneva, Switzerland), HBCD was recommended for listing as a POP, aiming at the eventual elimination of this compound from the international market.45 Canada’s Risk Management Plan for HBCD (released jointly with the Final Risk Assessment for HBCD on November 12, 2011) concluded that this compound meets the criteria for virtual elimination from the environment and proposed the prohibition of manufacture, use, sale, offer for
other report of BEHTBP and EHTBB in wildlife is from marine mammals (blubber of humpback dolphins and finless porpoises) stranded near Hong Kong.34 Detection frequencies in that study were also lower (40% for BEHTBP and 12% for EHTBB) than in the liver of Montreal-breeding ring-billed gulls. Average concentrations of BEHTBP in the present ringbilled gull livers (2.16 ng/g ww or 58.3 ng/g lw) were more than 25-fold greater in comparison to peregrine falcon eggs from Canada (2.10 ng/g lw), and almost 50-fold greater compared to those from Spain (1.20 ng/g lw).32 EHTBB in ring-billed gull livers also surpassed levels reported for peregrine eggs from Canada (4.10−7.20 ng/g lw) and Spain (0.63−3.10 ng/g lw). BEHTBP in ring-billed gulls was up to 4fold greater than in Norwegian Arctic species (lowest in ringed seal liver: 0.57 ng/g ww; highest in guillemot’s eggs: 1.80 ng/g ww). EHTBB concentrations in ring-billed gulls (ND−1.55 ng/ g ww) and Arctic species overlapped (from 0.38 ng/g ww in capelin to 3.46 ng/g ww in polar bear plasma).33 Although BEHTBP in ring-billed gull livers was more than 100-fold higher than in blubber of stranded Hong Kong dolphins (0.51 ng/g lw), concentrations reported in the present study were far lower compared to those determined in porpoises’ blubber from the same area (342 ng/g lw)the highest levels found in biota thus far.34 Similarly, EHTBB was higher in ring-billed gull livers (ND−1.55 ng/g ww = ND−8.64 ng/g lw) than in dolphins’ blubber (
