Brominated Flame Retardants in Glaucous Gulls from the Norwegian Arctic: More Than Just an Issue of Polybrominated Diphenyl Ethers JONATHAN VERREAULT, † WOUTER A. GEBBINK, ‡ LEWIS T. GAUTHIER, ‡ GEIR W. GABRIELSEN, † AND ROBERT J. LETCHER ‡, * Norwegian Polar Institute, Tromsø, NO-9296, Norway, and Science and Technology Branch, National Wildlife Research Centre, Environment Canada, Carleton University, Ottawa, Ontario K1A 0H3, Canada Several, unregulated, current-use brominated flame retardants (BFRs), including hexabromobenzene (HBB), 1,2- bis(2,4,6-tribromophenoxy)ethane (BTBPE), pentabromo- ethylbenzene (PBEB), pentabromotoluene (PBT), and hexabromocyclododecane (as total-(R)-HBCD), were examined in egg yolk and plasma of male and female glaucous gulls (Larus hyperboreus) from the Norwegian Arctic. Also examined were BDE209 and 38 tri- to nona- BDE congeners and brominated biphenyl (BB) 101. The HBB, BTBPE, PBEB, and PBT had high detection frequencies and variability in male and female plasma and egg yolk samples, and their concentrations ranged from nondetectable (<0.02-0.27 ng/g wet wt) to 2.64 ng/g wet wt. The detection frequencies and range of concentrations of non- BDE BFRs were generally highest in plasma of males relative to females. Total-(R)-HBCD concentrations were highest among the non-PBDE BFRs (up to 6.12 and 63.9 ng/g wet wt in plasma and egg yolk, respectively). Next highest was HBB with concentrations within a range comparable to the minor PBDEs monitored (e.g., BDE28, 116 and 155). Sum (Σ) 38 PBDE concentrations ranged from 2.49 to 54.5 ng/g wet wt in plasma and 81.2 to 321 ng/g wet wt in egg yolk. The BDE209 was virtually nondetectable, whereas six octa-BDEs (i.e., BDE196, 197, 201, 202, 203, and 205), as well as three nona-BDEs (i.e., BDE206, 207, and 208, and potential BDE209 debromination products) were found sporadically in plasma and egg yolk. The results from this study suggest that in addition to PBDEs, several current- use, non-BDE BFRs undergo long-range atmospheric transport and bioaccumulate at low levels in and are maternally transferred (to eggs) in glaucous gulls from the Norwegian Arctic. Introduction The growing database on brominated flame retardants (BFRs), and primarily polybrominated diphenyl ethers (PB- DEs), in tissues of wildlife demonstrates the ubiquitous environmental occurrence of these widely used consumer and industrial product additives (1, 2). A number of surveys also have reported BFR classes of major environmental concern in several species inhabiting non-urbanized and remote regions, including the high Arctic (3). Specific focus on BFRs in the Arctic has been on PBDEs, hexabromocy- clododecane (HBCD) isomers, and polybrominated biphenyls (PBBs). Generally, top predator birds and mammals residing permanently or seasonally in the Arctic have been reported to accumulate higher levels of PBDEs, HBCD (notably the R-HBCD isomer), and to much lesser extent PBBs, com- paratively to other organisms occupying lower trophic levels in the Arctic food web (3). Over the past few years, one top predator-scavenger seabird in the Norwegian Arctic, the glaucous gull (Larus hyperboreus), has received particular attention with respect to monitoring of new and emerging contaminants, including the bromine-based chemicals of current production and usage (4-6). Concentrations of major PBDEs (including BDE209), total-(R)-HBCD, and BB101 in glaucous gull plasma and egg samples are thus far reported to be among the highest of any arctic seabird species (3). Also reported in glaucous gulls from the Norwegian Arctic is the CYP enzyme-mediated biotransformation products of PBDEs, the hydroxylated (OH) PBDEs, and/or structurally similar and naturally occurring PBDEs such as the meth- oxylated (MeO)- and certain OH-PBDE congeners (6). Current knowledge on the toxicological potential of bioaccumulative BFRs (mainly PBDEs) has raised particular health concerns for chronically exposed avian species occupying high trophic positions in the marine/terrestrial food webs (7-11). In recent years, the scientific community of the European Union (EU) has put considerable effort in conducting environmental risk assessments on potentially persistent, bioaccumulative and toxic BFRs. As a result, the penta- and octa-BDE technical formulations are now subject to bans or restrictions by governmental agencies in most of the EU countries as of August 2004, whereas in Europe there is no use regulation in place for the high production volume deca- BDE (composed mainly of BDE209) (12). Similarly, no global restriction is as yet suggested for the HBCD mixture (mainly R-, -, and γ-HBCD isomers), where the R-HBCD isomer continues to be shown to be the most favorably accumulated isomer in the tissue of wildlife and humans (13). Thus, in response to increasing international regulations by govern- ments and agencies on certain BFR formulations, alternative, additive flame-retardants for achieving commercial product fire safety standards are being developed and used by members of the BFR industry. Recently, two unregulated, non-BDE BFRs were identified in environmental samples of North America and Europe. Specifically, 1,2-bis(2,4,6-tri- bromophenoxy)ethane (BTBPE) and pentabromoethylben- zene (PBEB) were detected in ambient air at various sites in the United States (14). The occurrence of BTBPE also was confirmed in some aquatic species, sediment, and water samples of Lake Winnipeg (Canada) (15), tree bark in the United States and Canada (16), and eggs of herring gulls (Larus argentatus) from the Laurentian Great Lakes of North America (17) and northern fulmars (Fulmarus glacialis) from the Faroe Islands (18). These studies provide corroborative evidence that BTBPE, a replacement product additive in polymeric products for the octa-BDE mixture (14), enters and persists in the environment and accumulates in tissues of exposed organisms. As many other bromine-based alter- natives to the PBDE mixtures are in current production and commercial usage, this will likely result in their more frequent * Corresponding author phone: (613) 998-6696; fax: (613) 998- 0458; e-mail: robert.letcher@ec.gc.ca. † Norwegian Polar Institute. ‡ National Wildlife Research Centre. Environ. Sci. Technol. 2007, 41, 4925-4931 10.1021/es070522f CCC: $37.00  2007 American Chemical Society VOL. 41, NO. 14, 2007 / ENVIRONMENTAL SCIENCE & TECHNOLOGY 9 4925 Published on Web 06/14/2007 Downloaded by NORWAY CONSORTIA on August 10, 2009 Published on June 14, 2007 on http://pubs.acs.org | doi: 10.1021/es070522f