Environ. Sci. Technol. 2009, 43, 312–317
Temporal Trends and Spatial Distribution of Non-polybrominated Diphenyl Ether Flame Retardants in the Eggs of Colonial Populations of Great Lakes Herring Gulls L E W I S T . G A U T H I E R , †,‡ D A V E P O T T E R , § CRAIG E. HEBERT,† AND R O B E R T J . L E T C H E R * ,†,‡ Wildlife and Landscape Science Directorate, Science and Technology Branch, Environment Canada, National Wildlife Research Centre, Carleton University, Ottawa, ON, K1A DH3, Canada, Department of Chemistry, Carleton University, Ottawa, Ontario, K1S 5B6, Canada, and Wellington Laboratories, Research Division, Guelph, ON, N1G 3M5, Canada
Received July 11, 2008. Revised manuscript received September 17, 2008. Accepted September 30, 2008.
The production and use of nonpolybrominated diphenyl ether (non-PBDE), brominated flame retardant (BFR) alternatives have been on the rise, although their assessment in environmental samples is largely understudied. In the present study, several nonPBDE BFRs were found in the egg pools of herring gulls (Larus argentatus) from seven colonies in the five Laurentian Great Lakes (collected in 1982 to 2006). Of the 19 BFRs monitored, hexabromobenzene (HBB), 1,2-bis(2,4,6-tribromophenoxy)ethane (BTBPE), decabromodiphenyl ethane (DBDPE), and R-, β-, γ-, and δ-isomers of 1,2-dibromo-4-(1,2-dibromoethyl)cyclohexane (TBECH) were present in eggs from all the colonies with the highest detection frequencies of 100%, 54%, 9% and 97%, respectively. In 2005 and 2006 eggs, the concentrations of DBDPE were highest at three of the seven colonies (1.3 to 288 ng/g wet weight (ww)) and surpassed decabromodiphenyl ether (BDE-209). HBB (0.10 to 3.92 ng/g ww), BTBPE (1.82 to 0.06 ng/g ww), and ∑-TBECH (0.04 to 3.44 ng/g ww; mainly the β-isomer 52 to 100% of ∑-TBECH) were detected at lower concentrations (and generally ,∑PBDE concentrations). Spatial trends were observed, although temporal trends were not obvious in most cases. Regardless, over the past 25 years non-PBDE BFRs have accumulated variably in female herring gulls and have been transferred during ovogenesis to their eggs, indicating that there has been continual exposure and bioaccumulation of several BFRs in the Great Lakes.
Introduction Brominated flame retardant (BFR) chemicals have been used to reduce the flammability of polymeric matrices utilized in commercial materials for several decades. Polybrominated diphenyl ethers (PBDEs) are the most extensively studied class of additive BFRs in the environment, but continue to * Corresponding author phone: (613) 998-6696; fax (613) 998-0458; e-mail:
[email protected]. † National Wildlife Research Centre, Carleton University. ‡ Department of Chemistry, Carleton University. § Wellington Laboratories. 312
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be increasingly regulated with respect to global production and applications (1). For instance, the production and use of PentaBDE and OctaBDE technical mixtures have been banned or phased-out in response to their ubiquitous environmental presence and potential toxicities associated with certain individual PBDE congeners (e.g., BDE-47 and BDE-99) (2). Recently, a European Court of Justice judgment was made against the European Commission’s decision to exempt DecaBDE (composed of mainly 2,2′,3,3′,4,4′,5,5′,6,6′decabromodiphenyl ether (BDE-209)) (Oct. 2005) from a list of hazardous substances banned in the Restriction of Hazardous Substances (RoHS) Directive, which entered into force in July 2008 (3). There is growing use and demand in the marketplace for non-regulated, additive non-PBDE BFRs (and other non-BFRs) as alternatives. A USEPA BFR alternatives report (4) lists 13 replacements for PentaBDE and OctaBDE mixtures containing additive, non-phenol- and non-acid-type BFRs with similar molecular weight and physical-chemical properties (log Kow, vapor pressure) to the PBDEs. Four of these are based on tetrabromobisphenol A (TBBPA) and include 1,1′-(1-methylethylidene)bis[3,5-dibromo-4-(2,3-dibromopropoxy)benzene (or tetrabromobisphenol-A-bis(2,3-dibromopropyl ether; TBBPA-DBPE), as well as 1,2-bis(2,4,6-tribromophenoxy)ethane (BTBPE) and octabromo-1,3,3-trimethyl-1-phenylindane (OBIND), which are potential PentaBDE and OctaBDE or even DecaBDE replacements. Considerable environmental attention has focused on two non-PBDE BFR alternatives: BTBPE and decabromodiphenyl ethane (DBDPE). Chemtura has announced that OctaBDE technical mixtures will be replaced with BTBPE (5). BTBPE has been detected in a variety of biotic and abiotic media on a global basis (6-10), including bird eggs (11-13). DBDPE is marketed as a replacement and alterative to the presently used DecaBDE commercial mixture. DecaBDE formulations are coming under increased environmental scrutiny (3), in light of recent reports of BDE-209 increasingly being shown to be present in the environment, e.g., Great Lakes sediments and in wildlife tissues and bird eggs including those of Great Lakes herring gulls (14-16). Recent reports of DBDPE generally involve its detection in abiotic samples (9, 17-19), with one exception where DBDPE was measured in tree bark from the United States (16). Isomers of another environmentally novel BFR, 1,2-dibromo-4-(1,2-dibromoethyl)cyclohexane (TBECH), were recently identified in Canadian arctic beluga whale (Delphinapterus leucas) (20). Regular, periodic sampling of tissues from a species from consistent locations is important for optimal biomonitoring of contaminant residues in wildlife and their ecosystems. Regardless of the precise levels of contamination, changes in contaminant levels can be accurately measured and correlated with remedial measures (21). We report on the identification of several previously unknown BFRs and isomers, and the temporal and spatial distribution of identified non-PBDE BFRs in the eggs of herring gulls from the Laurentian Great Lakes of North America.
Experimental Section Sample Information. Herring gull eggs were collected in each of 15 years (1982, 1987, 1992, and 1995-2006) in lateApril to early-May of each year, at seven of the fifteen annually monitored colonies in the Laurentian Great Lakes (Figure 1) (22). For each site, n ) 10 to 13 eggs were subsequently pooled on an equal wet weight (ww) basis, and homogenate pools were stored at -40 °C prior to chemical analysis. There are numerous, long-term studies reinforcing the valid repre10.1021/es801687d CCC: $40.75
2009 American Chemical Society
Published on Web 11/26/2008
FIGURE 1. Seven representative herring gull colonies from the Laurentian Great Lakes: (1) Agawa Rocks, Lake Superior; (2) Gull Island, Lake Michigan; (3) Channel-Shelter Island, Lake Huron; (4) Chantry Island, Lake Huron; (5) Fighting Island, Detroit River; (6) Niagara River, above the falls; (7) Toronto Harbor, Lake Ontario. sentation of pooled egg homogenates as an alternative to using individual eggs. Organic contaminant trend examination and analysis and additional details regarding sampling procedures, storage, and processing can be found elsewhere (21, 22). Standards and Materials. Nineteen non-PBDE BFRs and/ or isomers were monitored (Figure 2) (12). Pentabromoethyl benzene (PBEB), 1,2-bis(2,4,6-tribromophenoxy)ethane (BTBPE), decabromodiphenyl ethane (DBDPE), and hexabromobenzene (HBB) were all obtained from Wellington Laboratories (Guelph, ON, Canada). Those obtained from SigmaAldrich (Mississauga, ON, Canada) were pentabromobenzyl acrylate (PBBA), pentabromobenzyl bromide (PBBB), pentabromophenyl allyl ether (PBPAE), 2,4,6-tribromophenyl allyl ether (TBPAE), and pentabromotoluene (PBT). Non-PBDE
BFRs that were not reported previously in herring gull eggs (12) were monitored: 1,2-Dibromo-4-(1,2-dibromoethyl)cyclohexane isomers (R-, β-, γ-, and δ-TBECH), R- and β-1,2,5,6tetrabromocyclooctane (TBCO), tetrabromo-p-xylene (pTBX), and tetrabromobisphenol-A-bis(2,3-dibromopropyl ether) (TBBPA-DBPE) reference standards were obtained from Wellington Laboratories. Octabromo-1,3,3-trimethyl-1-phenylindane (OBIND) was donated from Dr. Åke Bergman, via Dead Sea Bromine Group (Be’er Sheva, Israel), and tetrabromobisphenol-S-bis(2,3-dibromopropyl ether) (TBBPDBPE) was obtained from Hainan Zhongxin Chemical Co., Ltd. (Shanghai, China). Sample Preparation. Approximately 3 g wet weight (ww) of frozen and thawed egg homogenate were ground with anhydrous sodium sulfate and then extracted with 175 mL of 50:50 dichloromethane:n-hexane (DCM:HEX). The internal standard BDE-30 was spiked to the head of the glass extraction column for quantification of FRs. Prior to cleanup by gelpermeation chromatography (12), a 10% portion of the column extraction eluant was used for gravimetric lipid determination. Final sample cleanup was performed using 6 mL, 0.5 g silica (SiOH) absorbent Bakerbond disposable solid-phase extraction cartridges (VWR International, Mississauga, ON, Canada). The SPE cartridge was prewashed with 6 mL of each DCM and HEX, and the sample extract was eluted with 12 mL of 15:85 DCM:HEX. The final volume of the sample extract was accurately adjusted to 200 µL by determining the equivalent mass of isooctane. GC-MS Analysis. As fully described in Gauthier et al. (2007) (12), the final chemical fractions from the samples were analyzed using an Agilent 5890 gas chromatograph-mass spectrometer working in electron capture negative ionization mode (GC/ECNI-MS). The analytical column was a J & W Scientific 15 m × 0.25 mm × 0.10 µm DB-5 HT fused-silica column (Chromatographic Specialties, Brockville, ON, Canada). The injector was operated in pulsed-splitless mode,
FIGURE 2. Chemical structures of brominated flame retardants currently under investigation: A, 1,2-bis-(2,4,6-tribromophenoxy)ethane (BTBPE); B, pentabromoethylbenzene (PBEB); C, pentabromobenzyl bromide (PBBB); D, decabromodiphenylethane (DBDPE); E, pentabromophenyl allyl ether (PBPAE); F, 2,4,6-tribromophenyl allyl ether (TBPAE); G, pentabromotoluene (PBT); H, hexabromobenzene (HBB); I, pentabromobenzyl acrylate (PBBA); J, tetrabromo-p-xylene (pTBX); K, octabromo-1,3,3-trimethyl-1-phenylindane (OBIND), L/M, rand β-1,2,5,6-tetrabromocyclooctane (r- and β-TBCO); N/O/P/Q, r-, β-, γ-, and δ-1,2-dibromo-4-(1,2-dibromoethyl)cyclohexane (r-, β-, γ-, and δ-TBECH), respectively; R, tetrabromobisphenol-S-bis(2,3-dibromopropyl) ether (TBBP-DBPE); S, tetrabromobisphenol-A-bis (2,3-dibromopropyl) ether (TBBPA-DBPE). Most hydrogen atoms have been omitted for clarity. VOL. 43, NO. 2, 2009 / ENVIRONMENTAL SCIENCE & TECHNOLOGY
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FIGURE 3. Temporal distribution for hexabromobenzene (HBB), 1,2-bis(2,4,6-tribromophenoxy)ethane (BTBPE), and 1,2-dibromo-4-(1,2-dibromoethyl)cyclohexane (sum of r- and β-isomers) at four representative herring gull colonies on the Laurentian Great Lakes (see Supporting Information for other Great Lakes colonies). with the injector held at 240 °C. The GC oven ramping temperature program was as follows: initial 100 °C for 2.0 min, 25 °C/min until 260 °C, 1.5 °C/min until 280 °C, 25 °C/min until 325 °C and held for a final 7.0 min. The GC to MS transfer line was held at 280 °C, ion source temperature was 200 °C, and the quadrupole temperature was 150 °C. Quantification of all BFRs was via selected ion monitoring (SIM) for isotopic 79Br- and 81Br-. Structural confirmation of all current-use BFR under study was accomplished by GC-HRMS. Several ions were monitored for the BFRs using GC-HRMS in the SIM mode, which consisted of the most abundant fragment and the molecular ions (see Supporting Information). In sample screening for the possible presence of TBBP-DBPE, liquid chromatography-atmospheric pressure photoionization-mass spectrometry (LC-APPI-MS) was used (see Supporting Information). Quality Control and Assurance. Method limits of quantification (MLOQ) were based on the criterion that an analyte response must be 10 times the standard deviation of the noise. For an analyte to be detectable but not quantifiable, the analyte response must be at least 3 times the standard deviation of the noise. In general, the MLOQs for BFRs varied depending on the degree of bromination, although were generally between 0.05 and 0.1 ng/g ww, excluding DBDPE for which the MLOQ was about 0.3 ng/g ww. The recovery efficiencies based on the BDE-30 internal standard averaged 90 ( 10% in all samples analyzed. A method blank was included in each sample block (homogenates from seven locations) and did not contain any of the target compounds above MLOQs. To assess precision and accuracy of nonPBDE BFR levels, and especially the quantifiable HBB, BTBPE, DBDPE, and R- and β-TBECH, replicate analyses (n ) 4) were made on standard additons to an in-house (NWRC) reference material (RM) of double-crested cormorant (Phalacrocorax auritus) (DCCO) egg homogenate (12, 14). The exception was for R- and β-TBECH, which were detected in the DCCO egg homogenate RM, and this standard addition replicate (n ) 4) analyses were made using commercial chicken egg homogenate. The results showed that recovery efficiency was the same as BDE-30 and thus was successfully evaluated as an internal standard and surrogate for all GCamenable BFRs. 314
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Results and Discussion Of the 19 BFR compounds and isomers that are presently monitored (Figure 2), HBB, BTBPE, DBDPE, and R- and/or β-TBECH were present in eggs from all the colonies with detection frequencies of 100%, 54%, 9%, and 97%, respectively. Assessment of spatial and temporal trends are limited to these BFRs. Non-PBDE BFRs that were newly screened and identified in gull eggs (12) include TBCO isomers and OBIND. Hexabromobenzene. Levels of HBB in the egg pools ranged from 0.10 to 3.92 ng/g ww for the seven colonies from 1982 to 2006 and were quite similar but variable, and there were no obvious temporal changes over the 25-year time span (Figure 3 and Figure S1, Table S1, Supporting Information). The low and comparable levels of HBB (using 2006 collected eggs as an example (Table 1),
