Novel Flame Retardants in Urban-Feeding Ring-Billed Gulls from theSt. Lawrence River, CanadaMarie-Line Gentes,† Robert J. Letcher,‡ Elyse Caron-Beaudoin,† and Jonathan Verreault*,†

† Centre de recherche en toxicologie de l’environnement (TOXEN), Departement des sciences biologiques, Universite du Quebec a Montreal, Montreal, QC, Canada‡ Wildlife and Landscape Science Directorate, Science and Technology Branch, Environment Canada, National Wildlife ResearchCentre, Carleton University, Ottawa, ON, Canada

*S Supporting Information

ABSTRACT: This study investigated the occurrence of a comprehensive suiteof 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 majorpoint-sources and diffuse contamination by FRs, nearly no FR data have beenreported 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/gww; max: 17.6 ng/g ww). To our knowledge, this is the highest detectionfrequency and highest concentrations reported thus far in any avian species orpopulations. Dechlorane Plus (DP) isomers were also particularly abundant(anti-DP detected in 100% and syn-DP in 93% of livers). Other detected FRcompounds (3−14% detection) included 2-ethylhexyl-2,3,4,5-tetrabromoben-zoate (EHTBB), hexachlorocyclopentenyl-dibromocyclooctane (HCDBCO)and β-1,2-dibromo-4-(1.2-dibromoethyl)-cyclohexane (β-TBECH). MeanBDE-209 (57.2 ± 12.2 ng/g ww) in ring-billed gull livers was unexpectedly high for this midtrophic gull species, exceedinglevels reported in several apex raptors such as peregrine falcons. BDE-209’s relative contribution to ∑PBDEs was on average25% (exceeding BDE-47 and BDE-99) and contrasted with profiles typically reported for fish-eating gull species. The presentstudy highlighted preoccupying gaps in upcoming FR regulations and stressed the need for further investigation of the sources ofFR exposure in highly urbanized areas.

■ INTRODUCTION

A large suite of nonreactive flame retardants (FRs) are routinelyadded to consumer products such as electronic circuitry,upholstered furniture, and construction materials to complywith fire safety standards. These include the largely restrictedpolybrominated diphenyl ethers (PBDEs), which are nowubiquitous in the environment and have been detected invirtually all ecosystems and taxa, as well as numerous as yetunregulated halogenated compounds. 1 Mounting environ-mental concerns have led to the worldwide phaseout of Penta-and Octa-BDEs between 2004 and 2010, 2 and Deca-BDE wasrestricted in Europe in 2008. 3 In North America, industrymembers of the Bromine Science and Environmental Forum(BSEF) have agreed to voluntarily phase out production anduse of Deca-BDE in Canada and the United States by the endof 2013.4,5

The increasing restrictions on PBDE production and use areresulting in the increased use of alternative FRs to meetflammability standards. Consequently, environmental levels ofreplacement or alternative FRs have been on the riseworldwide. For instance, the alternative FRs bis(2-ethyl-hexyl)-2,3,4,5-tetrabromophthalate (BEHTBP, also known asTBPH) and 2-ethylhexyl-2,3,4,5-tetrabromobenzoate

[(EHTBB, also known as TBB) (major compounds inFiremaster-550; replacing Penta-BDE)], 1.2-bis(2,4,6-tribromophenoxy)ethane [(BTBPE) (major compound in FF-680; replacing Octa-BDE)], and decabromodiphenyl ethane[(DBDPE) (major compound in Firemaster-2100; replacingDeca-BDE)] are already being detected in humans, as well as ina few captive and wild bird, marine mammal, and fish species,along with a series of other emerging FRs such aspentabromoethylbenzene (PBEB) and α- and β-isomers of1,2-dibromo-4-(1,2-dibromoethyl)cyclohexane (TBECH).1

The chlorinated FR Dechlorane-Plus (DP), commercializedin the 1960s as a substitute for the pesticide Mirex has alsobeen suggested as a possible replacement product for Deca-BDE.6 DP is now classified as a high production volumechemical in the United States and is being detected globally inair, sediments, water, and biota.7 Recent research confirms thata number of these current-use FRs (e.g., BTBPE, β-TBECH,PBEB, and EHTBB) exhibit high bioaccumulation and

Received: May 30, 2012Revised: July 26, 2012Accepted: July 30, 2012Published: July 30, 2012

Article

pubs.acs.org/est

© 2012 American Chemical Society 9735 dx.doi.org/10.1021/es302099f | Environ. Sci. Technol. 2012, 46, 9735−9744

biomagnification factors8 and undergo long-range atmospherictransport.9 Despite growing evidence that they may constitutesubstances of potential environmental concern to humans andwildlife, as demonstrated for PBDEs,2 current regulatoryframeworks are lagging behind and do not provide adequateinternational oversight of these emerging or less-studiedcompounds.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 thatmigrate may provide insights from broader-scale exposurescenarios.10 Gulls (Larids) specifically have been extensivelyused in research focusing on aquatic ecosystems as the majorityof gull species feed at high trophic levels and have been shownto accumulate FRs. In Canada and the United States, aconsiderable amount of research investigating spatial andtemporal trends of FRs has focused on herring gulls (Larusargentatus) from the Laurentian Great Lakes. Contaminantlevels in Great Lakes herring gull eggs have been closelymonitored since the early 1970s, producing a wealth ofinvaluable data for a large suite of halogenated organics andtrace elements.11−14 Conversely, only two studies on FRs inavian species breeding in the highly industrialized and denselypopulated sections of the St. Lawrence River (downstreamfrom the Great Lakes) have been published. Blue herons eggscollected from colonies near Montreal in 2001−2002 contained

1377.4 ng/g ww and 776.9 ng/g ww ∑PBDEs,15 falling withinthe higher range of PBDE contamination for the Great Lakesand St. Lawrence River Basin. A recent pan-Canadian studyinvestigating FRs in several gull species reported that ∑PBDEsin herring gull eggs (781 ng/g ww) collected in 2008 justdownstream from Montreal (Deslauriers Island) not onlyexceeded levels reported in Great Lakes colonies (134−440 ng/g ww) but were the highest concentrations reported inCanada.16 Thus, both these studies support that the greaterMontreal area is a potentially major “hotspot” with respect toFR contamination in avian species, but the exact sources ofexposure for these birds have never been investigated.Furthermore, a more comprehensive screening of emergingFRs 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 ring-billed gull was selected because of its omnivorous diet, whichencompasses terrestrial prey items as well as aquatic organisms,and because of its important utilization of both urban andnonurban habitats.17 These characteristics make this medium-size gull particularly well suited for investigating bioaccumula-tion of historical (Penta-BDE and Octa-BDE) and emerging,unregulated halogenated FRs that may not otherwisebioaccumulate in species feeding exclusively upon aquaticfood webs.

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 thelargest ring-billed gull colonies (48 000 nesting pairs) in North America.

Environmental Science & Technology Article

dx.doi.org/10.1021/es302099f | Environ. Sci. Technol. 2012, 46, 9735−97449736

■ EXPERIMENTAL SECTION

Study Area and Sample Collection. Fieldwork wasconducted from April through June 2010 on Deslauriers Island(45°42′45″ N, 73°26′25″ W), that is, the site identified byChen and co-workers16 as the most FR-contaminated gullcolony in Canada. Deslauriers Island is a 600 m long islandlocated ∼3.2 km downstream from the tip of Montreal in theSt. Lawrence River (Figure 1). It hosts one of the largest ring-billed gull colonies in Eastern Canada with approximately 48000 breeding pairs (2009 survey; P. Brousseau, EnvironmentCanada; personal communication). It is located amidst amosaic of landscape features, some of which representsignificant point sources of FRs: Montreal’s densely populatedurban core and industrial parks, the largest landfill within theprovince of Quebec (∼30 km from Montreal), and Canada’slargest wastewater treatment plant (primary-treated effluentreleased directly into the St. Lawrence River). The region alsoencompasses a number of low-exposure areas to FRs such asforests, lakes, and agricultural lands on which no sewage sludgeis applied.At the beginning of the incubation period (i.e., mid-April to

early May), ring-billed gull nests containing one or two eggswere randomly selected within the different sections of thecolony and marked with a unique number. This preliminarystep was repeated five times over a three week period so that alarge number of nests (n > 300) with a known clutch initiationdate would be available for the study based on the assumptionthat one egg is laid every second day.18,19 From mid-May tomid-June, i.e., once a sufficient number of preidentified nestshad a complete clutch (3 eggs), randomly selected ring-billedgulls (males and females) were live-captured on their nest whileincubating using a dip net or a nest trap triggered from a

distance by a remote control system. 20 Birds were bloodsampled 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 dailyfieldwork (maximum 10 h). In the laboratory, liver wastransferred to a −20 °C freezer and blood was centrifuged at2500g during 7 min. Resulting plasma was stored at −20 °Cuntil chemical analysis (see next section). Capture and handlingmethods were approved by the Institutional Committee onAnimal Care (CIPA) of the Universite du Quebec a Montrealand comply with the guidelines issued by the Canadian Councilon Animal Care (CCAC).

Chemical Standards and Materials. Plasma (n = 30) andliver samples (n = 28) were screened for 47 PBDE congenersand 23 emerging FRs (Table S1 in Supporting Information).All PBDE congeners, α-HBCD, and 13C- labeled BDE-209 werepurchased from Wellington Laboratories (Guelph, ON,Canada), as well as BTBPE, DBDPE, α- and β-TBECH,tetrabromo-o-chlorotoluene, pentabromoethylbenzene, hexab-romobenzene, tetrabromo-p-xylen, and polybrominated bi-phenyl congeners (BB-101 and -153). Reference standardsfor 2,4,6-tribromophenyl allyl ether, pentabromophenyl allylether, pentabromotoluene, pentabromobenzyl acrylate andpentabromobenzyl bromide were purchased from Sigma-Aldrich (Mississauga, ON, Canada). 13C-Dechlorane Plus(DP) isomers (syn and anti) were purchased from CambridgeIsotope Laboratories (Cambridge, MA). Octabromo-1,3,3-trimethyl-1-phenylindane was kindly donated by Dr. ÅkeBergman (University of Stockholm, Sweden). Chemicalanalyses were performed at the National Wildlife ResearchCentre, Environment Canada (Ottawa, ON, Canada).

Sample Preparation. Extraction and cleanup of plasmaand liver samples were performed as described elsewhere,14,21

Table 1. Concentrations (ng/g wwa) of Current and Historical Use Halogenated FRs in Liver (n = 28) and Plasma (n = 30) ofRing-Billed Gulls Breeding in the St. Lawrence River Downstream from Montreal, QC, Canada

liver plasma

samples >MLOD (%) meanb ± S.E. range samples >MLOD meanb ± S.E. range

lipidslipid content (%) 3.79 ± 0.20 2.02−6.83 0.74 ± 0.02 0.55−1.08

∑20non-PBDEsc,d 100 16.0 ± 3.0 ND-64.0 0 ND

anti-DP 100 6.06 ± 1.64 0.70−38.4 0 NDsyn-DP 93 2.38 ± 0.67 ND-15.2 0 NDtotal-HBCDe 89 5.22 ± 1.02 ND-19.8 0 NDHCDBCO 4 ND-0.02 0 NDOBIND (or OBTMI) 4 ND-0.37 3 ND-0.38EHTBB 11 ND-1.55 0 NDα-TBECH 3 ND-0.23 0 NDβ-TBECH/BDE-15 14 ND-0.30 0 NDBEHTBP 89 2.16 ± 0.59 ND-17.6 0 NDBB-101 18 ND-0.57 0 ND

∑45PBDEsf 100 205 ± 32.0 22.4−682 100 27.0 ± 4.05 3.54−90.3

BDE-209 100 57.2 ± 12.2 2.74−283 100 6.99 ± 1.17 0.70−23.8aConversion 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 hadFR concentrations greater than the MLOQ. c∑20Non-PBDEs: sum of BB-101(2,2′,4,5,5′-pentabromobiphenyl), BTBPE (1,2.-bis(2,4,6-tribromophenoxy)ethane), BEHTBP (bis(2-ethylhexyl)-2,3,4,5-tetrabromophthalate), DBDPE (decabromodiphenyl ethane), DP (DechloranePlus), 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-1-phenyl 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 .eTotal-HBCD: sum of α-, β-, γ-HBCD after thermal isomerization into α-HBCD. f∑45PBDEs: see Table S3 in Supporting Information for acomplete list of screened PBDE congener concentrations in liver and plasma.

Environmental Science & Technology Article

dx.doi.org/10.1021/es302099f | Environ. Sci. Technol. 2012, 46, 9735−97449737

with minor modifications. Briefly, thawed liver (1.5 g) andplasma (1 g) samples were homogenized with diatomaceousearth (DE; J.T. Baker, NJ), spiked with 100 μL of internalstandards (BDE-30, BDE-156, 13C-BDE-209, 13C-syn-DP, and13C-anti-DP), and extracted using Accelerated Solvent Extrac-tion (ASE 200, Dionex, Sunnyvale, CA) with 175 mL of 50:50dichloromethane:n-hexanes (DCM:HEX). For liver samples,10% of the extract was removed for lipid determination bygravimetry, and samples were cleaned up using gel permeationchromatography (GPC; O.I. Analytical, College Station, TX).Final sample cleanup on the remaining GPC fraction wasperformed using disposable solid-phase extraction (SPE) silicagel (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) coupledto a single quadrupole mass spectrometer (MS) (AgilentTechnologies 5890, Palo Alto, CA) operating in the electroncapture negative ionization mode (GC/MS-ECNI). Theanalytical column (15 m × 0.25 mm × 0.10 μm) was afused-silica DB-5 HT capillary column (J & W Scientific,Brockville, ON, Canada). Details on the injection mode, gasflow, and temperature ramping program have been described indetails elsewhere.13,14 Quantification of PBDEs and current-useFRs was achieved using selected ion monitoring (SIM) modefor isotopic bromine anions 79Br- and 81Br-, except for BDE-209 (m/z 487) and 13C-BDE-209 (m/z 495). The molecularion m/z 652 was used for quantifying DP isomers and was alsochromatographically resolved.22 Total-HBCD represents thesum of α-, β-, and γ-HBCD isomers as temperatures above 160°C in the injection port caused the thermal isomerization of allisomers into α-HBCD.Quality Control and Assurance. Procedures included

method blanks (DE) and injection of standard referencematerial (SRM 1947; Lake Michigan fish tissue) for each batchof ten samples (n = 3 batches). Background contamination ofmethod blanks was negligible, and no blank correction wasnecessary except for BDE-170 in liver (ND-4.56 ng/g ww inblanks) and BDE-209 also in liver (0.95−2.62 ng/g ww inblanks). Hence, concentrations in liver samples were blank-corrected for those two congeners. Concentrations of FRs in allsamples were quantified using an internal standard approach,and thus all analyte concentrations were inherently recovery-corrected. Method limits of quantification (MLOQs) andmethod limits of detection (MLODs) were based on replicateanalyses (n = 8) of matrix samples spiked at a concentration of3−5 times the estimated detection limit. MLOQs (defined as aminimum amount of analyte producing a peak with a signal-to-noise ratio (S/N) of 10) and MLODs (defined as S/N = 3) canbe 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 thesamples (plasma or liver) had concentrations above thecompound-specific MLOQ (Tables 1 and S1 in SupportingInformation). When this criterion was respected, samples withFR concentrations below the MLOD were assigned a randomvalue between zero and the compound-specific MLOD, whilesamples with concentrations below the MLOQ were assigned arandom value between the MLOD and the MLOQ. Since nodifferences in FR concentrations were found between malesand females (p = 0.96 and p = 0.65 for plasma and liver,respectively), all individuals were merged into one group. Alldata presented in tables are in ng/g wet weight (ww) as it has

been shown for various tissues that FRs do not necessarycorrelate with extractable lipid content and likely bind, at leastin part, to proteins.23 Nevertheless, lipid-normalized data arepresented in the text and in Supporting Information (Table S2)to facilitate comparisons with other studies.

■ RESULTS AND DISCUSSIONNon-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 detectedcompounds (ranging between 3 and 14% detection) includedEHTBB, HCDBCO, OBIND, β-TBECH, and BB-101. Sumconcentrations of current-use FRs and historical FRs (i.e., BB-101) in liver were approximately one order of magnitude lowerthan PBDEs (∑45PBDEs: 205 ng/g ww; ∑20non-PBDEs: 16.0ng/g ww). Current-use FRs were all below MLODs in plasma,with the exception of OBIND which was detected in one birdonly (0.38 ng/g ww).

BEHTBP and EHTBB. Possibly the most striking finding inthe current-use FR liver data was the unexpectedly highoccurrence of BEHTBP, which was detected in nearly allsamples (89%), as well as its high concentrations (mean: 2.16ng/g ww; max: 17.6 ng/g ww) relative to the other non-PBDEFRs. To our knowledge, this represents the highest detectionfrequency and the highest concentrations of BEHTBP reportedthus 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 forthe banned Penta-BDE. 24 They contain varying proportions ofBEHTBP (15% in FM-550, 30% in FM-BZ54, 100% in DP-45)and EHTBB (35% in FM-550, 70% in FM-BZ54, 0% in DP-45).25,26 Firemaster is mostly used in polyurethane foam whileDP-45 serves as a plasticizer in polyvinylchloride (PVC),neoprene, and electrical coating.27 The higher detectionfrequency and higher concentrations of BEHTBP comparedto EHTBB in ring-billed gull liver samples could therefore beindicative of DP-45 as a local source. Slower photodegradationof BEHTBP compared to EHTBB has also been suggested as afactor explaining its higher concentrations in environmentalsamples.28,29

Since their initial detection in house dust from the Bostonarea in 2006,30 BEHTBP and EHTBB have been found insewage sludge of a few locations in the United States,24,31 aswell as in gas and particle phase air samples collected near theshores of the Great Lakes from 2008 to 2010.25 Theenvironmental fate of these compounds is largely unknown,and reports of BEHTBP and EHTBB in biota are still veryscarce: only three studies documenting their occurrence inwildlife have been published at present. BEHTBP has beenreported in eggs of peregrine falcons from Canada and fromSpain,32 with fairly low detection frequency (33% in Canadaand 8% in Spain). The Norwegian Climate and PollutionAgency recently reported on the occurrence of EHTBB andBEHTBP in birds (eider liver, kittiwake liver, and guillemot’seggs), mammals (ringed seal liver, arctic fox liver, polar bearplasma), and fish (capelin) from Svalbard in the NorwegianArctic.33 Detection frequencies of BEHTBP in bird eggs fromSvalbard (50−70%) were lower than in present ring-billed gulllivers, while EHTBB was detected more frequently (90−100%)in eggs from Svalbard than in ring-billed gull livers. The only

Environmental Science & Technology Article

dx.doi.org/10.1021/es302099f | Environ. Sci. Technol. 2012, 46, 9735−97449738

other report of BEHTBP and EHTBB in wildlife is from marinemammals (blubber of humpback dolphins and finlessporpoises) stranded near Hong Kong.34 Detection frequenciesin that study were also lower (40% for BEHTBP and 12% forEHTBB) than in the liver of Montreal-breeding ring-billedgulls.Average concentrations of BEHTBP in the present ring-

billed gull livers (2.16 ng/g ww or 58.3 ng/g lw) were morethan 25-fold greater in comparison to peregrine falcon eggsfrom Canada (2.10 ng/g lw), and almost 50-fold greatercompared to those from Spain (1.20 ng/g lw).32 EHTBB inring-billed gull livers also surpassed levels reported forperegrine 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 4-fold greater than in Norwegian Arctic species (lowest in ringedseal liver: 0.57 ng/g ww; highest in guillemot’s eggs: 1.80 ng/gww). EHTBB concentrations in ring-billed gulls (ND−1.55 ng/g ww) and Arctic species overlapped (from 0.38 ng/g ww incapelin to 3.46 ng/g ww in polar bear plasma).33 AlthoughBEHTBP in ring-billed gull livers was more than 100-foldhigher than in blubber of stranded Hong Kong dolphins (0.51ng/g lw), concentrations reported in the present study were farlower compared to those determined in porpoises’ blubberfrom the same area (342 ng/g lw)the highest levels found inbiota thus far.34 Similarly, EHTBB was higher in ring-billed gulllivers (ND−1.55 ng/g ww = ND−8.64 ng/g lw) than indolphins’ blubber (<0.04 ng/g lw), but much lower than inporpoises’ blubber (<0.04−70 ng/g lw). These reports ofbioaccumulation in wildlife from North America, Europe, Asia,and the Arctic, along with recent controlled-exposuretoxicology data on the genotoxicity of EHTBB and BEHTBPto fish,26 clearly indicate that these relatively newly detectedFRs should be subjected to greater environmental scrutiny andtoxicity testing.Dechlorane Plus. The highly chlorinated FR Dechlorane-

Plus (comprised of two major structural syn and anti isomers)was particularly ubiquitous in ring-billed gull livers. anti-DP hada 100% detection frequency, and syn-DP was found in nearly allsamples (93%). Dechlorane Plus was initially marketed in the1960s as a replacement product for the banned pesticideDechlorane (i.e., Mirex), and the only known productionfacility of DP in North America (OxyChem) is located inNiagara Falls, NY.22 Dechlorane Plus was first reported inenvironmental samples (ambient air, fish, and sediment) fromthe Great Lakes in 2006.6 Since then, it has quickly emerged asa global contaminant and is now increasingly being detectedworldwide. 7 DP has been determined in a few bird species,including the eggs of herring gulls13,22 and bald eagles35 fromthe Great Lakes, the eggs of glaucous-winged (Larusglaucescens), California (Larus californicus), ring-billed orherring gulls from breeding sites across Canada,16 storks fromSpain,36 peregrine falcons from Canada and Spain,37 andaquatic birds from China.38

Mean levels of hepatic ∑DP in the present study (8.44 ng/gww or 230 ng/g lw) were comparable to those in eggs of othergull species from across Canada (0.2 to 15.0 ng/g ww).13,16,22

DP concentrations in the liver of six aquatic bird species fromChina overlapped with those of the present study and reachedlevels ∼2 fold higher. They were lowest in liver of ruddy-breasted crake (29.0 ng/g lw) and highest in slaty-breasted rail’sliver (600 ng/g lw).38 As was reported in herring gull eggs fromthe Great Lakes,22 fractional abundance of the anti-DP isomer(72%) in this study reflected proportions found in the

commercial product and indicated that no stereoselectiveenrichment is occurring in ring-billed gulls breeding inMontreal area.Published data on DP in avian species are still too scarce and

heterogeneous (i.e., different tissues and species sampled) todraw robust conclusions about global spatial trends, but limitedcomparisons between European and North American studiessuggest that North American birds generally exhibit greater DPbody burdens than European birds. DP in eggs from Spanishstorks (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 liversfrom the present study; comparisons between those storks’ eggsand 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 Canadianperegrines (36.4 ng/g lw)37 and ∼80 times lower than ring-billed gull liver. In contrast, differences between our ring-billedgulls and Canadian peregrines were only 4-fold (peregrine >ring-billed gull). Apart from the discrepancies due to thedifferent tissues sampled (i.e., eggs vs liver), it is possible thatdifferences in dietary habits among the species sampled wouldpartly explain the higher DP burden of Canadian birds, butGuerra et al.37 suggested that greater historical use of DP inNorth America and relative proximity of Canadian study sitesto the DP production facility in Niagara Falls could be drivingsuch trends. Information on the potential toxicity of DP is veryscarce and critically needed. Available data on mammaliantoxicity (i.e., Wistar rats and rabbits) originate from themanufacturer’s HPV (high production volume) test challengereport to the EPA39 and from an OxyChem-sponsored study.40

Both these reports concluded that the toxicity of DP wasminimal (except for a dose-related decrease in liver and ovaryweights in female rabbits in the challenge report). Only onestudy investigating avian toxicity has been published thus far.41

DP was not cytotoxic up to a maximum concentration of 3 μMin chicken embryonic hepatocytes, and no effect on pippingsuccess was observed up to the highest nominal dose group of500 ng/g egg. There are, however, no published data onpotential 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 forthis compound.

Total-HBCD. Total-HBCD was the second most frequentlydetected (89%) current-use FR in ring-billed gull livers (equalwith BEHTBP). HBCD has been used internationally as anadditive FR in polystyrene foam, upholstery textiles, andelectrical equipment for over 30 years.42 As PBDEs weregradually withdrawn from the global market, production anduse of HBCD kept increasing worldwide (in North Americaparticularly),43 and HBCD is now considered a high productionvolume by the EPA.44 Despite evidence of bioaccumulation,long-range atmospheric transport, and toxicity, it historicallyreceived much less attention than PBDEs and until now eludedinternational restrictions. However, at the seventh meeting ofthe 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 theinternational market.45 Canada’s Risk Management Plan forHBCD (released jointly with the Final Risk Assessment forHBCD on November 12, 2011) concluded that this compoundmeets the criteria for virtual elimination from the environmentand proposed the prohibition of manufacture, use, sale, offer for

Environmental Science & Technology Article

dx.doi.org/10.1021/es302099f | Environ. Sci. Technol. 2012, 46, 9735−97449739

sale, import, and export of HBCD and products containingHBCD by 2013.46

HBCD has been found in several bird species worldwide.47

Total-HBCD in the current study (5.22 ng/g ww or 145 ng/glw in liver) fell within the lower range of concentrationsreported previously for ring-billed gulls of this colony and forother gull species worldwide. For instance, total-HBCD (sumof α and β) in eggs of California, glaucous-winged, herring gullsfrom sites across Canada ranged from 0.5 to 12 ng/g ww andaveraged 11.8 ng/g ww in eggs of ring-billed gulls.16 Eggs ofgreat black-backed gulls (Larus marinus) from Norwaycontained 8.01−15.96 ng/g ww HBCD,48 while glaucousgulls (Larus hyperboreus) from the Norwegian arctic exhibitedslightly higher concentrations (19.8 ng/g ww in egg yolk; 1.73−2.07 ng/g ww in male and female plasma, respectively).49 Thehighest levels were found in dead and dying glaucous gulls ofthe Norwegian Arctic.50 Median concentrations in theseglaucous gull livers (1100 ng/g lw) were almost 10-fold greaterthan in ring-billed gull livers. Our results indicate that HBCD isfound in yet another avian species, supporting the need forstricter international and national regulations on productionand use of this compound.OBIND. OBIND was detected in one ring-billed gull only.

This compound used to be manufactured by Dead Sea BromineGroup (DSBG, now part of ICL-IP) and commercialized aspart of FR-1808, an additive FR that contains hepta- andoctabromo-1,3,3-trimethyl-1-phenylindanes. Main uses in-cluded styrenics and engineering thermoplastics.51 OBINDhas been previously detected (but not quantified) in GreatLakes herring gulls eggs14 but was not detectable in Chen etal.’s16 recent pan-Canadian study. Falcon eggs from Canada32

contained levels (8.9 ng/g lw) that were comparable to those inring-billed gull livers from the present study (ND−0.37 ng/gww or ND−11.9 ng/g lw). Lower levels of OBIND (10.1 pg/gww) were found in one stork egg from Spain.52 According toDSBG’s Web site,51 ICL-IP has discontinued production andsales of FR-1808.HCDBCO. HCDBCO was detected (<MLOQ) in the liver

of one ring-billed gull. Information on this compound isparticularly scarce. Unlike other halogenated FRs which havebeen monitored in the environment so far, HCDBCO containsboth bromine and chlorine atoms.53 Only one usage (styrenicpolymers) was listed by Covaci et al.1 The only other published

report of HCDBCO in biota is in falcons from Canada. 32

Concentrations in falcon eggs (19.0 ng/g lw) were higher thanin ring-billed gull liver (ND−0.02 ng/g ww or ND−0.28 ng/glw). HCDBCO was screened for, but not detected, in marinemammals from China34 and fish from the Great Lakes.54 As forEHTBB and BEHTBP, closer biomonitoring and additionaltoxicity testing of this unregulated FR is necessary inforthcoming research. A recent study reported on no adverseeffect of HCDBCO on the viability of chicken embryonichepatocytes (CEH) and on the pipping success of chickenembryos, but activity of cytochromes P450 (CYP) in CEH wasaffected (↑CYP2H1, ↑CYP3A37, ↓CYP1A4/5), and trans-thyretin (a blood carrier protein) was down-regulated inembryonic liver.55

BB-101. BB-101 is a discontinued FR which was sold in theUnited States in the early 1970s as part of FM BP-6. FiremasterBP-6 was unintentionally mixed into cattle feed in Michigan in1973, resulting in state-wide contamination of the food chain,subsequent ban of hexabromobiphenyls and gradual replace-ment of BBs with PBDEs.56 BBs are no longer produced orused in commercial quantities in the United States,57 but theyare still being detected in environmental samples worldwide.Liver concentrations of BB-101 (ND−0.57 ng/g ww) in thepresent study were lower than those reported for osprey’s eggsfrom Seattle (ND−3.06 ng/g ww) and from the ColumbiaRiver, WA (0.07−0.99 ng/g ww)58 but slightly higher thanthose in glaucous gull’s eggs (ND−0.38 ng/g ww) from theNorwegian Arctic.49

PBDEs. PBDEs were detected in liver and plasma of allindividuals (Table 1). ∑45PBDEs were approximately oneorder of magnitude lower in plasma than in liver. Mean∑45PBDEs in ring-billed gull liver (205 ng/g ww or 5896 ng/glw) was comparable to mean ∑PBDEs in ring-billed gull’s eggsalso collected from that same colony in 2008 (225 ng/g ww)but lower than in herring gull’s eggs collected from this colonyin 2008 (781 ng/g ww).16 Concentrations were at the midrangeof those reported for Great Lakes herring gull eggs (range:134−440 ng/g ww) in Chen et al.’s16 study but 132-fold greaterthan ∑PBDEs in ivory gull eggs from the Canadian Arctic(44.5 ng/lw).59

Liver concentrations in our study were nearly identical tothose in sparrowhawk liver from China (5550 ng/g lw)60 and inCaspian tern livers from San Francisco Bay (220 ng/g ww).61

Figure 2. Relative contribution (percentages) of major PBDE congeners to ∑45PBDEs in liver (n = 28) and plasma (n = 30) of ring-billed gullsbreeding in the St. Lawrence River downstream from Montreal, QC, Canada.

Environmental Science & Technology Article

dx.doi.org/10.1021/es302099f | Environ. Sci. Technol. 2012, 46, 9735−97449740

In glaucous gulls from the Norwegian Arctic, levels reached 522ng/g ww in liver (∼2.5 fold greater) and 51.5 ng/g ww inplasma (∼2 fold greater).62 Scandinavian herring gull livers had∑PBDEs up to 40 times lower than present ring-billed gulllivers; levels ranged from 135 to 985 ng/g lw in Norway63 and7.5 ng/g ww in Sweden.64 Median ∑PBDEs in various birdspecies from Belgium were 100-fold (58 ng/g lw in kestrelliver) to 0.5-fold lower (3100 ng/g lw in sparrowhawk liver)65

than in the present study. These results are consistent with theglobal trends highlighted in Chen et al. review of worldwideavian data,10 i.e., North American birds tend to exhibit higherPBDE burdens regardless of species, possibly because of greaterhistorical production and use of Penta-BDE on this continent.Congener Patterns: The Case of BDE-209. Most

remarkable in our PBDE data set was the particularly highdetection frequency of BDE-209 in ring-billed gull liver and itshigh concentrations (Table 1) as well as its high relativecontribution to ∑45PBDEs in both liver and plasma samples(Figure 2). BDE-209 is the most abundant congener in Deca-BDE commercial mixture (composed of ∼98% BDE-209), theonly PBDE technical product that theoretically remains on theinternational market. Use of Deca-BDE in electronic equipmenthas been restricted in the European Union since 20083 and thetwo main producers/traders of Deca-BDE in the United Statesagreed to a voluntary phase out by 2013.5 In Canada,restrictions on the use of Deca-BDE are also expected to takeplace by the end of 2013.66,67 However, there is so far nointernationally binding regulatory framework aiming at thecontrol of the production, export, and use of Deca-BDE on theglobal market.BDE-209 concentrations were approximately one order of

magnitude lower in plasma than in liver. BDE-209 accountedfor roughly 25% of ∑45PBDEs in liver, exceeding the relativecontributions of both BDE-47 (17%) and BDE-99 (19%). Aslightly different distribution was found in plasma samples,where the relative contribution of BDE-209 (26%) wascomparable to that of BDE-99 (24%) and BDE-47 (23%).Also worth noticing was the presence of several known orsuggested sequential debromination products of BDE-209 (e.g.,BDE-202, -201, -197, -203, -196, -208, and -207) in both liverand plasma (Figure 2), further supporting the hypothesis thatthis fully brominated compound may undergo sequentialdebromination in organisms and/or in abiotic media.68−70

Overall, this congener profile differed from what has beentypically reported for other predominantly fish-eating Larids; inthose studies, BDE-47 and BDE-99 are consistently the mostabundant congeners. This pattern has been partly explained bythe high molecular weight and octanol−water partitioncoefficient (log Kow: 9.98) of BDE-209, which confers highhydrophobicity, low bioavailability, and low bioaccumulationpotential in aquatic species.Mean BDE-209 in ring-billed gull liver (57.2 ng/g ww or

1654 ng/g lw) was nearly identical to mean BDE-209 in ring-billed gull’s eggs (59.4 ng/g ww) collected from that samecolony in 2008, approximately 2- to 16-fold greater than inherring gull’s eggs from Great Lakes colonies (3.6−35 ng/gww) and 4- to 44-fold greater than in eggs of other gull speciesfrom most other colonies across Canada (1.3−14.4 ng/gww).16 Two sampling sites with high BDE-209 concentrationsstood out in that pan-Canadian study:16 California gull eggsfrom Dalemead Reservoir in Alberta (111 ng/g ww) andherring gull eggs from Deslauriers Island (201 ng/g ww) (samecolony as used in the present study). The relative contribution

of BDE-209 to ∑PBDEs ranged from 1% (herring gull eggsfrom Turkey Island, Ontario) to 17% (herring gull eggs fromBellechasse Island in Quebec), with again those same twooutlying colonies: 56% in eggs of California gulls fromDalemead Reservoir, Alberta, and 26% in herring gull eggsfrom Deslauriers Island.16

BDE-209 was 40-fold lower in the liver of herring gulls fromNorway (40.8 ng/g lw in adults) than in the present ring-billedgulls and represented only 9% of ∑PBDEs.63 BDE-209 wasnonquantifiable in Ivory gull eggs from the Canadian Arctic59

and virtually nondetectable in egg yolk and plasma of glaucousgulls from the Norwegian Arctic.49 A different study reportedlow levels (2.8 ng/g ww in liver samples), but it reported aslightly higher relative percentage of BDE-209 (18% of∑PBDEs) in glaucous gulls from that same population.71

It is probable that ring-billed gulls’ congener profiles (i.e.,high proportion of BDE-209) reflected the importance of localanthropogenic foraging sites for this particular colony. Forinstance, a positive correlation between human density andproportions of BDE-209 concentrations has been reported inperegrine falcons from California72 and from the northeasternUnited States.73 In China, unusually high levels of BDE-209have also been found in aquatic species foraging near e-wasterecycling sites38 and in various terrestrial raptors impacted byurban areas.60

BDE-209 concentrations in the present study stand outcompared to other bird species in which high levels of BDE-209have been reported. Mean BDE-209 concentrations in ring-billed gulls liver (57.2 ng/g ww or 1654 ng/g lw) were 16-foldhigher than in storks from Madrid (3.5 ng/g ww in eggs)74 and19- to 32-fold higher than in various raptors from Belgium(52−85 ng/g lw in liver).65 In fact, mean BDE-209 in ring-billed gull liver even surpassed the levels found in some of themost contaminated apex bird predators such as peregrinefalcons from California (990.9 ng/g lw in eggs of urbanperegrines)72 or from Spain (620 ng/g lw in eggs).32 Besideherring gull eggs from Deslauriers Island, which also containedremarkable BDE-209 concentrations (201 ng/g ww or 2680ng/g lw),16 only kestrels from the Beijing area in Chinaexhibited greater BDE-209 concentrations (2870 ng/g lw inliver) at the time of literature review.60 These results arepreoccupying, as evidence of BDE-209’s toxicity is rapidlygrowing and includes adverse effects on hepatic functions aswell as on the hypothalamo-pituitary-thyroid (HPT) axis,75 onspermatogenesis76 and on neurological functions.77

Further investigation is needed to elucidate the exact sourcesof this high BDE-209 exposure in Montreal-breeding ring-billedgulls. While the above-cited research on predatory birds in theUnited States, Europe, and China strongly suggest terrestrialsources of anthropogenic origins for BDE-209, it is difficult atthis point to rule out the possibility of contaminant uptake fromthe St. Lawrence River food webs. Sampling conducted byEnvironment Canada in 2005−2006 revealed that BDE-209concentrations in the City’s municipal effluent (1000 ng/g insuspended particulate matter) were more than 150-fold greaterthan just upstream from the dispersion plume (6 ng/g).78 Mean∑PBDEs in water sampled ∼20 km downstream fromMontreal (Lavaltrie: 1350 pg/L) surpassed concentrationsreported for the Great Lakes, reaching levels consideredthreatening to piscivorous wildlife, and contained a highproportion of BDE-209 (BDE-209: 48%, BDE-47 and BDE-99:20%).79 To understand how dietary sources and habitat-useinfluence the contaminant burden of Deslaurier Island ring-

Environmental Science & Technology Article

dx.doi.org/10.1021/es302099f | Environ. Sci. Technol. 2012, 46, 9735−97449741

billed gulls, our ongoing work involves a novel approachfounded on the tracking of individual birds using GPS-basedbiotelemetry and stable isotopes of carbon and nitrogen. Thiswill allow better understanding feeding ecology and foraginghabitat utilization of this species, and it may represent apowerful new tool for ecotoxicological research to explainoccasionally large intraspecific variations in contaminantconcentrations and profiles in birds. Current study uncoveredseveral novel current-use FRs and confirmed the presence ofunusually high levels of BDE-209 in a midtrophic avian species,which highlights preoccupying gaps in current and upcomingFRs regulations. While attention is still focused on Deca-BDE,various unregulated replacement products are presently enter-ing the global market to comply with fire regulations whichhave remained unchanged despite growing concerns over thereal benefits of halogenated FRs.80 This significant lag betweenthe implementation of regulations and the speed at which newFRs are commercialized (and subsequently found in environ-mental media) is increasingly problematic.

■ ASSOCIATED CONTENT*S Supporting InformationTables S1, S2, and S3. This material is available free of chargevia the Internet at http://pubs.acs.org.

■ AUTHOR INFORMATIONCorresponding Author*Mailing address: Departement des sciences biologiques,Universite du Quebec a Montreal, C.P. 8888, SuccursaleCentre-ville, Montreal, Quebec, H3C 3P8, Canada; phone:+514-987-3000 ext. 1070; fax: +514-987-4647; e-mail:verreault.jonathan@uqam.ca.NotesThe authors declare no competing financial interest.

■ ACKNOWLEDGMENTSFunding for this project was provided primarily by the NationalScience and Engineering Research Council of Canada(NSERC) Discovery Grant (to J.V.), the Canada ResearchChair in Comparative Avian Toxicology (to J.V.) as well asfinancial support of Environment Canada (Grants & Con-tribution program) (to J.V.). Funding for chemical analysis wasalso via a NSERC Discovery Grant to R.J.L. and fromEnvironment Canada’s Chemicals Management Plan (CMP;to R.J.L.). Chemical analyses were performed in the OrganicContaminants Research Laboratory (OCRL) at the NWRC,Ottawa. Shaogang Chu, Lewis Gauthier and Eric Pelletier aregratefully acknowledged for assistance with the FR determi-nation in the OCRL, with assistance from Vicky Dore. Dr. Jean-Francois Giroux’s behavior ecology lab (Universite du Quebeca Montreal) facilitated field logistics, and we greatly thank allthe volunteers and field assistants who made this researchpossible.

■ REFERENCES(1) Covaci, A.; Harrad, S.; Abdallah, M. A. E.; Ali, N.; Law, R. J.;Herzke, D.; De Wit, C. A. Novel brominated flame retardants: Areview of their analysis, environmental fate and behaviour. Environ. Int.2011, 37 (2), 532−556.(2) UNEP. The 9 new POPS: An introduction to the nine chemicalsadded to the Stockholm Convention by the Conference of the Partiesat its fourth meeting. 2010; http://chm.pops.int/Programmes/New%20POPs/Publications/tabid/695/language/en-US/Default.aspx.

(3) EBFRIP. The RoHS directive and Deca-BDE. Europeanbrominated flame retardant industry panel 2008; http://www.ebfrip.org/main-nav/european-regulatory-centre/rohs-directive-restriction-of-the-use-of-certain-hazardous-substances-in-electrical-and-electronic-equipment/the-rohs-directive-and-deca-bde.(4) EC. Risk management of DecaBDE: Commitment to voluntaryphase-out exports to Canada. Environment Canada: 2011; http://www.ec.gc.ca/toxiques-toxics/default.asp?lang=En&n=F64D6E3B-1&xml=F64D6E3B-0328-4C11-A9E4-790D053E42A1.(5) EPA. DecaBDE phase-out initiative. U.S. Environmental ProtectionAgency: 2009; http://www.epa.gov/oppt/existingchemicals/pubs/actionplans/deccadbe.html.(6) Hoh, E.; Zhu, L.; Hites, R. A. Dechlorane Plus, a chlorinatedflame retardant, in the Great Lakes. Environ. Sci. Technol. 2006, 40 (4),1184−1189.(7) Sverko, E.; Tomy, G. T.; Reiner, E. J.; Li, Y. F.; McCarry, B. E.;Arnot, J. A.; Law, R. J.; Hites, R. A. Dechlorane Plus and relatedcompounds in the environment: A review. Environ. Sci. Technol. 2011,45 (12), 5088−5098.(8) Wu, J. P.; Guan, Y. T.; Zhang, Y.; Luo, X. J.; Zhi, H.; Chen, S. J.;Mai, B. X. Several current-use, non-PBDE brominated flame retardantsare highly bioaccumulative: Evidence from field determinedbioaccumulation factors. Environ. Int. 2011, 37 (1), 210−215.(9) de Wit, C.; Herzke, D.; Vorkamp, K. Brominated flame retardantsin the Arctic environment-trends and new candidates. Sci. TotalEnviron. 2010, 408 (15), 2885−2918.(10) Chen, D.; Hale, R. A global review of polybrominated diphenylether flame retardant contamination in birds. Environ. Int. 2010, 36(7), 800−811.(11) Hebert, C.; Norstrom, R.; Weseloh, D. A quarter century ofenvironmental surveillance: The Canadian Wildlife Service’s GreatLakes herring gull monitoring program. Environ. Rev. 1999, 7 (4),147−166.(12) Weseloh, D. V. C.; Pekarik, C.; De Solla, S. R. Spatial patternsand rankings of contaminant concentrations in herring gull eggs from15 sites in the Great Lakes and connecting channels, 1998−2002.Environ. Monit. Assess. 2006, 113 (1), 265−284.(13) Gauthier, L.; Hebert, C.; Weseloh, D.; Letcher, R. Current-useflame retardants in the eggs of herring gulls (Larus argentatus) fromthe Laurentian Great Lakes. Environ. Sci. Technol. 2007, 41 (13),4561−4567.(14) Gauthier, L.; Potter, D.; Hebert, C.; Letcher, R. Temporaltrends and spatial distribution of non-polybrominated diphenyl etherflame retardants in the eggs of colonial populations of Great Lakesherring gulls. Environ. Sci. Technol. 2009, 43 (2), 312.(15) Champoux, L.; Moisey, J.; Muir, D. Polybrominated diphenylethers, toxaphenes, and other halogenated organic pollutants in greatblue heron eggs. Environ. Toxicol. Chem. 2010, 29 (2), 243−249.(16) Chen, D.; Letcher, R. J.; Burgess, N. M.; Champoux, L.; Elliott,J. E.; Hebert, C.; Martin, P.; Wayland, M.; Weseloh, D. V. C.; Wilson,L. Flame retardants in the eggs of four gull species (Laridae) frombreeding sites spanning Atlantic to Pacific Canada. Environ. Pollut.2012, 168, 1−9.(17) Pollet, I. L.; Shutler, D.; Chardine, J.; Ryder, J. P. Ring-billed gull(Larus delawarensis). In The Birds of North America Online; Poole, A.,Ed.; Cornell Lab of Ornithology: Ithaca, 2012.(18) Nol, E.; Blokpoel, H. Incubation period of ring-billed gulls andthe egg immersion technique. The Wilson Bull. 1983, 95 (2), 283−286.(19) Vermeer, K.; Reynolds, L. M. Organochlorine residues inaquatic birds in the Canadian Prairie Provinces. Can. Field Nat. 1970,84, 117−130.(20) Bustnes, J.; Bakken, V.; Erikstad, K.; Mehlum, F.; Skaare, J.Patterns of incubation and nest site attentiveness in relation toorganochlorine (PCB) contamination in glaucous gulls. J. Appl. Ecol.2001, 38 (4), 791−801.(21) Gauthier, L.; Hebert, C.; Weseloh, D.; Letcher, R. Dramaticchanges in the temporal trends of polybrominated diphenyl ethers(PBDEs) in herring gull eggs from the Laurentian Great Lakes: 1982−2006. Environ. Sci. Technol. 2008, 42 (5), 1524−1530.

Environmental Science & Technology Article

dx.doi.org/10.1021/es302099f | Environ. Sci. Technol. 2012, 46, 9735−97449742

(22) Gauthier, L. T.; Letcher, R. J. Isomers of Dechlorane Plus flameretardant in the eggs of herring gulls (Larus argentatus) from theLaurentian Great Lakes of North America: Temporal changes andspatial distribution. Chemosphere 2009, 75 (1), 115−120.(23) Verreault, J.; Shahmiri, S.; Gabrielsen, G.; Letcher, R.Organohalogen and metabolically-derived contaminants and associa-tions with whole body constituents in Norwegian Arctic glaucous gulls.Environ. Int. 2007, 33 (6), 823−830.(24) Klosterhaus, S.; Konstantinov, A.; Stapleton, H. Characterizationof the brominated chemicals in a PentaBDE replacement mixture andtheir detection in biosolids collected from two San Francisco Bay areawaste water treatment plants. San Fransisco Estuary Institute:2008;http://www.sfei.org/sites/default/files/08BFR_Poster_klosterhaus_shrunk.pdf (May 15th, 2010).(25) Ma, Y.; Venier, M.; Hites, R. A. 2-Ethylhexyl Tetrabromo-benzoate and bis (2-ethylhexyl) tetrabromophthalate flame retardantsin the Great Lakes atmosphere. Environ. Sci. Technol. 2012, 46 (1),204−208.(26) Bearr, J. S.; Stapleton, H. M.; Mitchelmore, C. L. Accumulationand DNA damage in fathead minnows (Pimephales promelas)exposed to 2 brominated flame-retardant mixtures, Firemaster 550and Firemaster BZ-54. Environ. Toxicol. Chem. 2010, 29 (3), 722−729.(27) Chemtura Product Overview: DP-45 TM. 2011;http://www.c h e m t u r a . c o m / b u / v / i n d e x . j s p ? v g n e x t o i d =8829695a71ea6110VgnVCM10000053d7010aRCRD&vgnextchann e l =df5e8d843400c110VgnVCM10000053d7010aRCRD&vgnextfmt=default.(28) Davis, E. F.; Stapleton, H. M. Photodegradation pathways ofnonabrominated diphenyl ethers, 2-ethylhexyltetrabromobenzoate anddi (2-ethylhexyl) tetrabromophthalate: Identifying potential markers ofphotodegradation. Environ. Sci. Technol. 2009, 43 (15), 5739−5746.(29) La Guardia, M. J.; Hale, R. C.; Harvey, E.; Matteson Mainor, T.;Ciparis, S. In Situ accumulation of HBCD, PBDEs, and severalalternative flame-retardants in the bivalve (Corbicula f luminea) andgastropod (Elimia proxima). Environ. Sci. Technol. 2012, 46 (11),5798−5805.(30) Stapleton, H.; Allen, J.; Kelly, S.; Konstantinov, A.; Klosterhaus,S.; Watkins, D.; McClean, M.; Webster, T. Alternate and newbrominated flame retardants detected in US house dust. Environ. Sci.Technol. 2008, 42 (18), 6910−6916.(31) Davis, E. F.; Klosterhaus, S. L.; Stapleton, H. M. Measurementof flame retardants and triclosan in municipal sewage sludge andbiosolids. Environ. Int. 2012, 40 (April), 1−7.(32) Guerra, P.; Alaee, M.; Jimenez, B.; Pacepavicius, G.; Marvin, C.;MacInnis, G.; Eljarrat, E.; Barcelo, D.; Champoux, L.; Fernie, K.Emerging and historical brominated flame retardants in peregrinefalcon (Falco peregrinus) eggs from Canada and Spain. Environ. Int.2012, 40 (April), 179−186.(33) Sagerup, K.; Herzke, D.; Harju, M.; Evenset, A.; Christensen, G.N.; Routti, H.; Fuglei, E.; Aars, J.; Strøm, H.; Gabrielsen, G. W. Newbrominated flame retardants in Arctic biota; Climate and PollutionAgency, Norwegian Ministry of Environment: 2010.(34) Lam, J. C. W.; Lau, R. K. F.; Murphy, M. B.; Lam, P. K. S.Temporal trends of hexabromocyclododecanes (HBCDs) andpolybrominated diphenyl ethers (PBDEs) and detection of twonovel flame retardants in marine mammals from Hong Kong, SouthChina. Environ. Sci. Technol. 2009, 43 (18), 6944−6949.(35) Venier, M.; Wierda, M.; Bowerman, W. W.; Hites, R. A. Flameretardants and organochlorine pollutants in bald eagle plasma from theGreat Lakes region. Chemosphere 2010, 80 (10), 1234−1240.(36) Munoz-Arnanz, J.; Saez, M.; Hiraldo, F.; Baos, R.; Pacepavicius,G.; Alaee, M.; Jimenez, B. Dechlorane plus and possible degradationproducts in white stork eggs from Spain. Environ. Int. 2011, 37 (7),1164−1168.(37) Guerra, P.; Fernie, K.; Jimenez, B.; Pacepavicius, G.; Shen, L.;Reiner, E.; Eljarrat, E.; Barcelo, D.; Alaee, M. Dechlorane Plus andrelated compounds in Peregrine Falcon (Falco peregrinus) eggs fromCanada and Spain. Environ. Sci. Technol. 2011, 45 (4), 1284−1290.

(38) Zhang, X. L.; Luo, X. J.; Liu, H. Y.; Yu, L. H.; Chen, S. J.; Mai, B.X. Bioaccumulation of several brominated flame retardants anddechlorane plus in waterbirds from an e-waste recycling region inSouth China: associated with trophic level and diet sources. Environ.Sci. Technol. 2011, 45 (2), 400−405.(39) EPA. Robust Summaries & Test Plans: Dechlorane Plus. U.S.Environmental Protection Agency: 2008; http://www.epa.gov/chemrtk/pubs/summaries/dechlorp/c15635tc.htm.(40) Brock, W. J.; Schroeder, R. E.; McKnight, C. A.; VanSteenhouse,J. L.; Nyberg, J. M. Oral repeat dose and reproductive toxicity of thechlorinated flame retardant Dechlorane Plus. Int. J. Toxicol. 2010, 29(6), 582−593.(41) Crump, D.; Chiu, S.; Gauthier, L. T.; Hickey, N. J.; Letcher, R.J.; Kennedy, S. W. The effects of Dechlorane Plus on toxicity andmRNA expression in chicken embryos: A comparison of in vitro and inovo approaches. Comp. Biochem. Physiol., Part C: Toxicol. Pharmacol.2011, 154 (2), 129−134.(42) de Wit, C. A. An overview of brominated flame retardants in theenvironment. Chemosphere 2002, 46 (5), 583−624.(43) Chen, D.; Luellen, D.; La Guardia, M. J.; Harvey, E.; Mainor, T.M.; Hale, R. C. Do temporal and geographical patterns of HBCD andPBDE flame retardants in US fish reflect evolving industrial usage?Environ. Sci. Technol. 2011, 45 (19), 8254−8261.(44) EPA. Initial Risk-Based Prioritization of High Production VolumeChemicals: Hexabromocyclododecane (HBCD). 2008; http://www.epa.gov/hpvis/rbp/HBCD.3194556.Web.RBP.31308.pdf.(45) UNEP. Press release: UN experts target toxic flame retardantHBCD for control under global chemicals treaty. 2011; http://new.unep.org/Documents .Mul t i l ingua l/Defau l t . a sp?DocumentID=2656&ArticleID=8906&l=en&t=long.(46) EC. Proposed Risk Management Approach for Hexabromocyclo-dodecane (HBCD). 2011; http://www.ec.gc.ca/ese-ees/default.asp?lang=En&n=5F5A32FB-1.(47) Covaci, A.; Gerecke, A. C.; Robin, J.; Voorspoels, S.; Kohler, M.;Heeb, N. V.; Leslie, H.; Allchin, C. R.; de Boer, J. Hexabromocyclo-dodecanes (HBCDs) in the environment and humans: a review.Environ. Sci. Technol. 2006, 40 (12), 3679−3688.(48) Haukas, M.; Hylland, K.; Berge, J. A.; Nygard, T.; Mariussen, E.Spatial diastereomer patterns of hexabromocyclododecane (HBCD) ina Norwegian fjord. Sci. Total Environ. 2009, 407 (22), 5907−5913.(49) Verreault, J.; Gebbink, W.; Gauthier, L.; Gabrielsen, G.; Letcher,R. Brominated flame retardants in glaucous gulls from the NorwegianArctic: more than just an issue of polybrominated diphenyl ethers.Environ. Sci. Technol. 2007, 41 (14), 4925−4931.(50) Sagerup, K.; Helgason, L. B.; Polder, A.; Strom, H.; Josefsen, T.D.; Skare, J. U.; Gabrielsen, G. W. Persistent organic pollutants andmercury in dead and dying glaucous gulls (Larus hyperboreus) atBjørnøya (Svalbard). Sci. Total Environ. 2009, 407 (23), 6009−6016.(51) DSBG. New FR Systems For Styrenic Plastics. 2012;http://www.d s b g . c o m / b r o m e / b r o m e . n s f / v i e w V i r t u a l L i b r a r y /A73F587C44411314C22565F3003FDA52?OpenDocument.(52) Munoz-Arnanz, J.; Saez, M.; Pacepavicius, G.; Jimenez, B.;Alaee, M. Emerging brominated flame retardants in white storks(Ciconia ciconia) colonies from Spain. Proccedings of BFR Conference,2010, Kyotoa, Japan.(53) Watanabe, K.; Senthilkumar, K.; Masunaga, S.; Takasuga, T.;Iseki, N.; Morita, M. Brominated organic contaminants in the liver andegg of the common cormorants (Phalacrocorax carbo) from Japan.Environ. Sci. Technol. 2004, 38 (15), 4071−4077.(54) Zhou, S. N.; Reiner, E. J.; Marvin, C.; Kolic, T.; Riddell, N.;Helm, P.; Dorman, F.; Misselwitz, M.; Brindle, I. D. Liquidchromatography-atmospheric pressure photoionization tandem massspectrometry for analysis of 36 halogenated flame retardants in fish. J.Chromatogr. A 2010, 1217 (5), 633−641.(55) Egloff, C.; Crump, D.; Chiu, S.; Manning, G.; McLaren, K. K.;Cassone, C. G.; Letcher, R. J.; Gauthier, L. T.; Kennedy, S. W. In vitroand in ovo effects of four brominated flame retardants on toxicity andhepatic mRNA expression in chicken embryos. Toxicol. Lett. 2011, 207(1), 25−33.

Environmental Science & Technology Article

dx.doi.org/10.1021/es302099f | Environ. Sci. Technol. 2012, 46, 9735−97449743

(56) Alaee, M.; Arias, P.; Sjodin, A.; Bergman, Å. An overview ofcommercially used brominated flame retardants, their applications,their use patterns in different countries/regions and possible modes ofrelease. Environ. Int. 2003, 29 (6), 683−689.(57) HHS. Polybrominated Biphenyls. U.S. Department of Health andHuman Services, National Toxicology Program, 12th Report onCarcinogens, 2011; May 2nd, 2012; pp 347−349.(58) Henny, C. J.; Kaiser, J. L.; Grove, R. A.; Johnson, B. L.; Letcher,R. J. Polybrominated diphenyl ether flame retardants in eggs mayreduce reproductive success of ospreys in Oregon and Washington,USA. Ecotoxicology 2009, 18 (7), 802−813.(59) Braune, B. M.; Mallory, M. L.; Grant Gilchrist, H.; Letcher, R. J.;Drouillard, K. G. Levels and trends of organochlorines and brominatedflame retardants in Ivory Gull eggs from the Canadian Arctic, 1976 to2004. Sci. Total Environ. 2007, 378 (3), 403−417.(60) Chen, D.; Mai, B.; Song, J.; Sun, Q.; Luo, Y.; Luo, X.; Zeng, E.Y.; Hale, R. C. Polybrominated diphenyl ethers in birds of prey fromNorthern China. Environ. Sci. Technol. 2007, 41 (6), 1828−1833.(61) Herring, G.; Ackerman, J. T.; Eagles-Smith, C. A.; Adelsbach, T.L.; Melancon, M. J.; Stebbins, K. R.; Hoffman, D. J. Organochlorineand PBDE concentrations in relation to cytochrome P450 activity inlivers of Forster’s Terns (Sterna forsteri) and Caspian Terns(Hydroprogne caspia), in San Francisco Bay, California. Arch. Environ.Contam. Toxicol. 2010, 58 (3), 863−873.(62) Verreault, J.; Bech, C.; Letcher, R.; Ropstad, E.; Dahl, E.;Gabrielsen, G. Organohalogen contamination in breeding glaucousgulls from the Norwegian Arctic: Associations with basal metabolismand circulating thyroid hormones. Environ. Pollut. 2007, 145 (1), 138−145.(63) Sørmo, E.; Lie, E.; Ruus, A.; Gaustad, H.; Skaare, J.; Jenssen, B.Trophic level determines levels of brominated flame-retardants incoastal herring gulls. Ecotoxicol. Environ. Saf. 2011, 74 (7), 2091−2098.(64) Carlsson, P.; Herzke, D.; Wedborg, M.; Gabrielsen, G. W.Environmental pollutants in the Swedish marine ecosystem, withspecial emphasis on polybrominated diphenyl ethers (PBDE).Chemosphere 2011, 82 (9), 1286−1292.(65) Jaspers, V.; Covaci, A.; Voorspoels, S.; Dauwe, T.; Eens, M.;Schepens, P. Brominated flame retardants and organochlorinepollutants in aquatic and terrestrial predatory birds of Belgium: levels,patterns, tissue distribution and condition factors. Environ. Pollut.2006, 139 (2), 340−352.(66) EC. Risk management strategy for polybrominated diphenylethers (PBDEs). Environment Canada, Chemicals Sectors Directorate,Environmental Stewardship Branch : 2010; http://www.healthyenvironmentforkids.ca/sites/healthyenvironmentforkids.ca/files/RiskManagementStrategyForPBDEsAugust2010.pdf.(67) Government of Canada. Publication of results of investigations andrecommendations for a substance - Decabromodiphenyl Ether; CanadaGazette; 2012; Volume 146, (6).(68) Noyes, P. D.; Hinton, D. E.; Stapleton, H. M. Accumulation anddebromination of Decabromodiphenyl Ether (BDE-209) in juvenileFathead Minnows (Pimephales promelas) induces thyroid disruptionand liver alterations. Toxicol. Sci. 2011, 122 (2), 265−274.(69) Gandhi, N.; Bhavsar, S. P.; Gewurtz, S. B.; Tomy, G. T. Canbiotransformation of BDE-209 in lake trout cause bioaccumulation ofmore toxic, lower-brominated PBDEs (BDE-47,-99) over the longterm? Environ. Int. 2011, 37 (1), 170−177.(70) Van den Steen, E.; Covaci, A.; Jaspers, V.; Dauwe, T.;Voorspoels, S.; Eens, M.; Pinxten, R. Accumulation, tissue-specificdistribution and debromination of decabromodiphenyl ether (BDE209) in European starlings (Sturnus vulgaris). Environ. Pollut. 2007,148 (2), 648−653.(71) Sagerup, K.; Savinov, V.; Savinova, T.; Kuklin, V.; Muir, D. C.G.; Gabrielsen, G. W. Persistent organic pollutants, heavy metals andparasites in the glaucous gull (Larus hyperboreus) on Spitsbergen.Environ. Pollut. 2009, 157 (8−9), 2282−2290.(72) Newsome, S. D.; Park, J. S.; Henry, B. W.; Holden, A.; Fogel, M.L.; Linthicum, J.; Chu, V.; Hooper, K. Polybrominated diphenyl ether(PBDE) levels in peregrine falcon (Falco peregrinus) eggs from

California correlate with diet and human population density. Environ.Sci. Technol. 2010, 44 (13), 5248−5255.(73) Chen, D.; La Guardia, M. J.; Harvey, E.; Amaral, M.; Wohlfort,K.; Hale, R. C. Polybrominated diphenyl ethers in peregrine falcon(Falco peregrinus) eggs from the northeastern US. Environ. Sci. Technol.2008, 42 (20), 7594−7600.(74) Munoz-Arnanz, J.; Saez, M.; Aguirre, J. I.; Hiraldo, F.; Baos, R.;Pacepavicius, G.; Alaee, M.; Jimenez, B. Predominance of BDE-209and other higher brominated diphenyl ethers in eggs of white stork(Ciconia ciconia) colonies from Spain. Environ. Int. 2011, 37 (3), 572−576.(75) Lee, E.; Kim, T. H.; Choi, J. S.; Nabanata, P.; Kim, N. Y.; Ahn,M. Y.; Jung, K. K.; Kang, I. H.; Kim, T. S.; Kwack, S. J. Evaluation ofliver and thyroid toxicity in Sprague-Dawley rats after exposure topolybrominated diphenyl ether BDE-209. J. Toxicol. Sci. 2010, 35 (4),535−545.(76) Li, W.; Zhu, L.; Zha, J.; Wang, Z. Effects of decabromodiphenylether (BDE-209) on mRNA transcription of thyroid hormonepathway and spermatogenesis associated genes in Chinese rareminnow (Gobiocypris rarus). Environ. Toxicol. 2011, DOI: 10.1002/tox.20767.(77) Costa, L. G.; Giordano, G. Is decabromodiphenyl ether (BDE-209) a developmental neurotoxicant? Neurotoxicology 2011, 32 (1), 9−24.(78) EC. Tracking Polybrominated Diphenyl Ethers (PBDE): NewChemical Contaminants in the Environment. Environment Canada:2010; http://www.ec.gc.ca/stl/default.asp?lang=En&n=7BBC611F-1.(79) Berryman, D.; Beaudoin, J.; Cloutier, S.; Laliberte, D.; Messier,F.; Tremblay, H.; Moissa, A. D. Les polybromodiphenylethers (PBDE)dans quelques cours d’eau du Quebec meridional et dans l’eau deconsommation produite a deux stations de traitement d’eau potable.Ministere du Developpement durable, de l’Environnement et des Parcs,Quebec, Direction du suivi de l’etat de l’environnement; 2009; 18 pages.(80) Shaw, S. D.; Blum, A.; Weber, R.; Kannan, K.; Rich, D.; Lucas,D.; Koshland, C. P.; Dobraca, D.; Hanson, S.; Birnbaum, L. S.Halogenated flame retardants: do the fire safety benefits justify therisks? Rev. Environ. Health 2010, 25 (4), 261−305.

Environmental Science & Technology Article

dx.doi.org/10.1021/es302099f | Environ. Sci. Technol. 2012, 46, 9735−97449744