Trophodynamics of Hexabromocyclododecanes and Several Other

Jun 24, 2010 - Trophodynamics of Hexabromocyclododecanes and Several Other Non-PBDE Brominated Flame Retardants in a Freshwater Food Web. Jiang-Ping W...
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Environ. Sci. Technol. 2010, 44, 5490–5495

Trophodynamics of Hexabromocyclododecanes and Several Other Non-PBDE Brominated Flame Retardants in a Freshwater Food Web J I A N G - P I N G W U , †,‡ Y U N - T A O G U A N , * ,† Y I N G Z H A N G , ‡ X I A O - J U N L U O , * ,‡ HUI ZHI,§ SHE-JUN CHEN,‡ AND BI-XIAN MAI‡ Research Center for Environmental Engineering & Management, Graduate School at Shenzhen, Tsinghua University, Shenzhen 518055, China, State Key Laboratory of Organic Geochemistry, Guangzhou Institute of Geochemistry, Chinese Academy of Sciences, Guangzhou 510640, China, and Guangzhou Institute of Biomedicine and Health, Chinese Academy of Sciences, Guangzhou 510663, China

Received April 22, 2010. Revised manuscript received June 11, 2010. Accepted June 11, 2010.

Several currently used non-polybrominated diphenyl ether (PBDE) brominated flame retardants (BFRs), including hexabromocyclododecanes (HBCDs), 1,2-bis(2,4,6-tribromophenoxy)ethane (BTBPE), decabromodiphenyl ethane (DBDPE), hexabromobenzene (HBB), pentabromoethylbenzene (PBEB), and pentabromotoluene (PBT), are examined in the components of a freshwater food web from an electronic waste recycling site, South China. All these BFRs are detectable in the food web, with average concentrations of 13.9-868, 1.71-518, < 3.8-338, 197-3099, 3.98-25.6, and 1.20-3.60 ng/g lipid wt for HBCDs, BTBPE, DBDPE, HBB, PBEB, and PBT, respectively. Food web magnification is observed for (+)-R-, (-)-R-, (()-R-, and total HBCDs, and HBB, with trophic magnification factors (TMFs) of 2.22, 2.18, 2.19, 1.82, and 1.46, respectively; whereas there is trophic dilution of BTBPE and PBT through the food web. The TMFs for (+)-R-, (-)-R-, and (()-R-HBCDs are comparable to those of PBDEs detected previously in the same food web. Biota samples show a shift from γ- toward R-HBCD compared with the suspended particles, sediment, and HBCD technical mixtures, with a significant increase of R-HBCD on ascending trophic levels. Except for R-HBCD in suspended particles and sediment, all the HBCD enantiomers detected are nonracemic in the environmental matrix. In biota, nonracemic residues of R-HBCD were observed in mud carp and crucian carp; β-HBCD in prawn, mud carp, and crucian carp; and γ-HBCD in water snake, with preferences for (+)-R-, (-)-β-, and (+)-γ-HBCDs.

* Address correspondence to either authors. Phone: +86-75526036702 (Y. T. G.); +86-20-85290146 (X. J. L.). Fax: +86-75526036702 (Y. T. G.); +86-20-85290706 (X. J. L.). E-mail: guanyt@ sz.tsinghua.edu.cn (Y. T. G.); [email protected]. (X. J. L.). † Graduate School at Shenzhen, Tsinghua University. ‡ Guangzhou Institute of Geochemistry, CAS. § Guangzhou Institutes of Biomedicine and Health, CAS. 5490

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Introduction Brominated flame retardants (BFRs) reduce the flammability of a broad range of consumer products (1). Tetrabromobisphenol A (TBBPA), polybrominated diphenyl ethers (PBDEs), and hexabromocyclododecanes (HBCDs) are the three main representative BFRs (1). They are ubiquitous in the environment, and certain types have been proven to be toxic (1). In fact, the lower brominated PBDEs (components of the legacy commercial BFRs pentaBDEs and octaBDEs) have been listed as persistent organic pollutants (POPs) in the recently held United Nations Environmental Program Stockholm Convention (2). DecaBDE commercial formulation is now considering bans or phase-outs in several U.S. states (3). To date, there is no global restriction on the production or use of HBCDs. Furthermore, HBCDs are promoted as alternatives to the discontinued BDE formulations in some applications (4, 5), resulting in the continuously increasing global use of these chemicals. HBCDs are bioaccumulative in both freshwater and marine food webs (4, 6, 7). HBCD diastereoisomeric compositions in the biota are variable and significantly different from that of technical mixtures (8–13). After passing through various compartments of the food web, an increase in R-HBCD is concurrent with a decrease in γ-HBCD, while βand δ-isomers are almost absent. These patterns become more prominent in species at the upper trophic level (TL). Enantioselective bioaccumulation of R- and γ-HBCDs has been observed in several aquatic species (10–13), whereas only one report exists on β-HBCD enantioselectivity in an aquatic biota (10). Selectivity to different HBCD enantiomers may be attributed to in vivo biotransformations or uptake by prey or the surroundings. Except for one report that measured chiral signatures of HBCDs in temporally and spatially consistent water and sediment samples (11), no previous study has yet investigated enantiomers compositions in the surroundings and assessed their influence to the enantiomers profiles of organisms. Considerable attention has been given to two alternatives for BDE technical mixtures: 1,2-bis(2,4,6-tribromophenoxy)ethane (BTBPE) and decabromodiphenyl ethane (DBDPE). BTBPE has been detected in fish and birds (or bird eggs) from North America (14–17), China (18, 19), the Faroe Island (20), and even the Norwegian Arctic (21). DPDPE has also been reported in fish and birds (or bird eggs) from North America (14, 16, 17) and China (18, 22, 23), and in two kinds of pandas from China (24). In addition, several other BFR alternatives, such as hexabromobenzene (HBB), pentabromoethylbenzene (PBEB), and pentabromotoluene (PBT), have been reported in wildlife and humans (15–17, 21, 25). These studies provide corroborative evidence that these unregulated, non-PBDE BFRs have entered and persisted in the environment and accumulated in exposed biota. Very little quantitative data is available on the trophic transfer of these currently used non-PBDE BFRs in food webs, which is a vital criterion for assessing their ecological risks. Trophic magnification factors (TMFs) for HBCDs were only reported in two freshwater food webs, that is, food webs from Lake Ontario (26) and Lake Winnipeg (14), and one marine food web from Eastern Canadian Arctic (12). The TMF of total HBCDs in the Lake Ontario food web was 6.3, which was 3-4 times greater than the values for R- (1.4), β(1.3), and γ-HBCDs (2.2) reported in the Lake Winipeg food web and the value for R-HBCD (2.1) in the Eastern Canadian Arctic food web, whereas a TMF of 0.5 for γ- HBCD was found in the Eastern Canadian Arctic food web. At present, 10.1021/es101300t

 2010 American Chemical Society

Published on Web 06/24/2010

TABLE 1. Concentrations of HBCDs and Other Non-PBDE Brominated Flame Retardants in the Aquatic Species (ng/g lipid), Dissolved Phase of Water (ng/L), and Sediment (ng/g wet wt) from an E-waste Recycling Site, South China Chinese mysterysnail n ) 43, [3]a lipid (%) R-HBCD β-HBCD γ-HBCD ΣHBCDsd BTBPE DBDPE HBB PBEB PBT BDE 47e

prawn n ) 7, [3]

mud carp n ) 12, [8]

cruciancarp n ) 18, [7]

0.59 ( 0.11b 2.39 ( 0.32 2.87 ( 0.41 3.63 ( 0.71 7.73 ( 1.83 267 ( 80.9 649 ( 228 102 ( 32.8 0.24 ( 0.24 10.2 ( 2.74 24.5 ( 9.48 5.42 ( 3.39 5.90 ( 1.25 118 ( 29.3 195 ( 66.9 21.1 ( 8.83 13.9 ( 2.61 395 ( 94.5 868 ( 280 129 ( 44.3 67.1 ( 36.4 44.7 ( 8.04 518 ( 277 323 ( 315 bdl 84.3 ( 84.3 338 ( 171 14.0 ( 14.0 298 ( 51.3 197 ( 53.4 2451 ( 778 680 ( 158 14.3 ( 2.53 6.35 ( 2.52 25.6 ( 11.1 3.98 ( 2.10 3.60 ( 0.90 1.55 ( 0.64 3.24 ( 1.51 1.59 ( 0.45 4270 ( 820 4640 ( 1330 20910 ( 3740 5860 ( 1480

northern snakehead n)6

water snake n)2

1.49 ( 0.31 168 ( 82.4 3.12 ( 1.76 16.6 ( 9.06 187 ( 92.7 1.71 ( 1.11 bdl 1153 ( 470 17.5 ( 5.53 1.20 ( 0.57 25960 ( 4020

1.06 ( 0.15 494 ( 315 8.76 ( 6.22 64.0 ( 42.8 567 ( 364 9.22 ( 9.22 bdl 3099 ( 2809 4.14 ( 4.14 106 ( 103 51870 ( 29940

water n ) 6, [3]

sediment n ) 6, [3]

0.05 ( 0.01 61.4 ( 10.2 bdlc 23.5 ( 1.07 0.01 ( 0.00 84.3 ( 4.22 0.06 ( 0.01 169 ( 12.1 0.02 ( 0.01 4554 ( 608 bdl 1796 ( 770 0.52 ( 0.04 8672 ( 1053 0.06 ( 0.00 132 ( 6.12 0.03 ( 0.01 20.6 ( 2.89 10.7 ( 0.14 44130 ( 717

a Numer of individual samples collected, figures in brackets indicate analyses number of pooled samples when individuals were pooled. b Mean ( SE. c Below the detection limit. d total HBCDs. e Data from ref 30 given for comparison.

only one study focused on the TMFs for different HBCD enantiomers, where TMFs of 2.2, 0.5, and 0.5 were reported for (+)-R-, (+)-γ-, and (-)-γ-HBCDs, respectively, in the Eastern Canadian Arctic marine food web (12). These complex results warrant further research into the trophodynamics of HBCD diastereoisomers and enantiomers in the food web. For other non-PBDE BFRs, a TMF of 2.1 for HBB was found in a freshwater food web in South China (19), and TMFs of 2.7 and 1.0 for DBDPE and BTBPE, respectively, were observed in the Lake Winnipeg food web (14). E-waste recycling sites have been identified as hot spots for BFRs (27). A food web model from an e-waste recycling site in South China has been created and successfully used to characterize trophic transfer of polychlorinated biphenyls (PCBs), PBDEs, and Dechlorane Plus (a chlorinated flame retardant) (28, 29). In this study, we are reporting on the occurrences and trophodynamics of HBCD diastereoisomers and enantiomers, DBDPE, BTBPE, HBB, PBEB, and PBT detected in the same food web. The study aims to assess the food web magnification potentials of these BFRs, and to make a better understanding of the environmental fate and ecological risks of these non-PBDE BFRs.

Exprimental Section Chemicals. Native compounds R-, β-, and γ-HBCDs, HBB, and BDE 118 were purchased from Accustandard (New Haven, CT), while BTBPE, DBDPE, PBT, PBEB, and 18d-labeled R-, β-, γ-HBCD were obtained from Wellington Laboratories (Canada). The 13C labeled BDE 209, 13C labeled PCB 208, and 13 C and labeled R-, β-, and γ-HBCDs were bought from Cambridge Isotope Laboratories, Inc. (USA). Sample Collection. The samples analyzed in this study are the same as those in our previous papers (28–30). A total of 88 wild aquatic biota samples, six water samples, and six superficial sediment samples were simultaneously collected from a natural pond in an e-waste recycling site, South China (23.6021 N, 113.0785 E) in 2006. The aquatic species included two invertebrate species, i.e., Chinese mysterysnail (Cipangopaludina chinensis) (n ) 43) and prawn (Macrobrachium nipponense) (n ) 7), three fish species, i.e., mud carp (Cirrhinus molitorella) (n ) 12), crucian carp (Carassius auratus) (n ) 18), and northern snakehead (Ophicephalus argus) (n ) 6), and one reptile species, i.e., water snake (Enhydris chinensis) (n ) 2). Detailed information on the sampling site and biota samples are provided in the Supporting Information (SI). Sample Extraction, Clean-Up, and Analysis. The same extracts previously prepared for the determination of PBDEs and PCBs (30) were used in this study. BTBPE, DBDPE, HBB,

PBT, and PBEB were analyzed using a Shimadzu model QP2010 gas chromatograph-mass spectrometer working in electron capture negative ionization in a selected ion monitoring (SIM) mode. To confirm these BFRs, the extracts of selected samples were injected into a GC/MS in the fullscan or SIM in electron impact (EI) ionization mode using the same capillary column and chromatographic conditions. HBCD diastereoisomers and enantiomers were analyzed using an Agilent 1200 series liquid chromatography and an Agilent 6410 triple quadrupole mass spectrometer, equipped with an electrospray interface operated in negative ionization mode (LC-ESI-MS/MS). The stable nitrogen isotope composition of the biota has already been determined in our previous study (28). Detailed procedures of sample pretreatment, instrumental analysis, quality assurance and quality control, and the calculation method for TL and TMF are available online in the SI.

Results and Discussion Levels of HBCDs and Other BFRs. Measured concentrations of HBCD diastereoisomers, BTBPE, DBDPE, HBB, PBEB, and PBT in water, sediment, and the aquatic species are summarized in Table 1. HBCDs are detectable in all the sampled biota species, with mean values of 14-870 ng/g lipid wt (Table 1). Total HBCD concentrations (range 11-2370 ng/g lipid wt) in the aquatic species in our study are slightly lower than the reported levels (120-3530 ng/g lipid wt) in aquatic species from another Chinese e-waste recycling area (13), but are much higher than those (12-330 ng/g lipid wt) from the Yangtze River, China (31). This range is up to 2 orders of magnitude higher than that in the fish from the North American Great Lakes (3-80 ng/g lipid wt) and Swiss alpine lakes (up to 36 ng/g lipid wt), and is close to that from HBCD hot spots identified in Europe, for example, from the Tees River and Skerne River in UK, Cinca River in Spain, and the Western Scheldt Estuary in Netherlands (30-10270, 70-1640, and 10-1110 ng/g lipid wt, respectively) (4). Results indicate that the e-waste recycling site is likely to be another HBCD hot spot, in addition to HBCDs or HBCD-retarded material production facilities. HBB, BTBPE, DBDPE, PBEB, and PBT were detected in 93%, 83%, 20%, 47%, and 75% of the sampled organisms, respectively. Of particular interest is the very high concentrations of HBB detected in the sampled species (average of 197-3099 ng/g lipid wt) (Table 1). A previous study reported that HBB has been used as an additive BFR in plastic and electronic goods (32). Study also found that polymeric PBDEs can pyrolyze to yield HBB during a high temperature process VOL. 44, NO. 14, 2010 / ENVIRONMENTAL SCIENCE & TECHNOLOGY

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FIGURE 1. Relationships between lipid-normalized concentrations of the aquatic species from an e-waste recycling site in South China. (up to 290 °C) (33). E-waste contains high burdens of PBDEs, and the e-waste recycling procedure involves high temperature processes, such as heating and burning (27). These imply that other sources of HBB aside from HBB itself in e-waste may partly contribute to the high HBB levels in the aquatic species. Little is known about non-PBDE BFRs in wild aquatic species. The concentrations of PBEB reported here are in the same magnitude with our previously reported values (100 °C (36) may lead to the thermal conversion of γ- to R-HBCD, which may occur when some plastic e-waste parts are burned in the sampling site. Further studies are needed for a better understanding of the processes affecting the composition of HBCDs in the e-waste recycling site environment. The HBCD isomer patterns in aquatic species (Figure 2) imply that R-HBCD has the highest bioavailability among the three HBCD isomers, primarily because it is the most water-soluble. In addition, it seems that the fractions of R-HBCD increase, and the fraction of γ-HBCD concurrently decrease on ascending TL. Previous study suggested that γ-HBCD can be metabolized more quickly than R-HBCD and that γ-HBCD can be biotransformed to the R-isomer in fish (38). This metabolism and biotransformation capacity for HBCD diastereomers may be higher in upper TL species, such as fish and water snake, than in lower TL species, such as aquatic invertebrates (Chinese mysterysnail and prawn),

FIGURE 3. Enantiomeric fractions (EFs) of the HBCD enantiomers in the standard solutions, water, suspended particles, sediment, and aquatic species. All the EFs are corrected by isotope-labeled standards (13C-HBCDs). Error bars are (1 standard error. The EFs of γ-HBCD in dissolved phase of water and Chinese mysterysnail, and β-HBCD in dissolved phase of water, Chinese mysterysnail, northern snakehead, and water snake have not been calculated due to their low detection frequencies in these samples. The asterisk refers the significantly different EFs from those in standard solutions (t test, p < 0.05). Std, standard solutions; Wd, dissolved phase of water; Ws, suspended particles in the water; Sed, sediment; CMS, Chinese mysterysnail; Prn, prawn; MuC, mud carp; CrC, crucian carp; NSh, northern snakehead; WS, water snake. resulting in higher R-HBCD concentrations in the biota of higher TL species. On the other hand, some lower TL species that inhabit the bottom of the water column have direct contact with or ingest suspended particles and sediment, which may lead to an increase in γ-HBCD fractions. The predominance of R-HBCD in upper TL organisms and the dominance of γ-HBCD in benthic filter feeders and zooplankton have also been observed in the Eastern Canadian Arctic marine food web (12). Chiral Signatures of HBCDs. Chiral signature is expressed as enantiomeric fractions (EFs), stated fractionally relative to the (+)-enantiomer (10). Previous studies reported that mobile phase composition, column bleed, and sample matrix effects can contribute to the variability of EFs for HBCDs (12, 39, 40). Thus, the calculated EFs in the present study were corrected according to the method of Marvin et al. (39) (described in detail in the SI). Figure 3 shows the corrected EFs for the three HBCD diastereoisomers in the environmental and biota samples examined. The corrected EF ranges (mean ( SE) in the standard solutions were 0.497 ( 0.003, 0.516 ( 0.002, and 0.504 ( 0.001 for R-, β-, and γ-HBCDs, respectively. Only EFs in the environmental and biota samples that significantly deviate from these ranges (t test, p < 0.05) were considered nonracemic residues of HBCD enantiomers. Except for R-HBCD in suspended particles and sediment, all the enantiomers detected were nonracemic in the environmental matrix (dissolved phase of water, suspended particles, and sediment), implying that enantiomer-selective microbial biotransformation of HBCDs may have occurred in the water column. In biota, nonracemic residues of R-HBCD were observed in mud carp and crucian carp; β-HBCD in prawn, mud carp, and crucian carp; and γ-HBCD in northern snakehead, with preferences for (+)-R-, (-)-β-, and (+)-γHBCDs. This is insufficient evidence of enantioseletive HBCD biotransformation in the food web because this trend can be also attributed to the intake of nonracemic enantiomeric matter from water and sediment. However, the EF values of β-HBCD in prawn (0.343 ( 0.003) differed significantly from that of suspended particles (0.466 ( 0.017) and sediment VOL. 44, NO. 14, 2010 / ENVIRONMENTAL SCIENCE & TECHNOLOGY

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(0.497 ( 0.005), indicating that this species may have a piscine enantioselective metabolism, uptake, or excretion of βHBCD. No clear preference for any of the three enantiomers was found from the limited enantiomer-specific HBCD data (10–13). Mud carp and crucian carp in the present study, bib and whiting from the Western Scheldt Estuary (10), clams from the Eastern Canadian Arctic (12), and crucian carp and loach from an e-waste recycling site in China (13) were clearly enriched in (+)-R-HBCD. On the other hand, sole from the Western Scheldt Estuary (10) and winkle from a Chinese e-waste recycling site (13), and several fish species from lakes in UK (11) were dominated by (-)-R-HBCD. Fish species in this study and bib from the Western Scheldt Estuary (10) showed a preference for (-)-β-HBCD, whereas racemic or nearly racemic residues were observed in several fish species from lakes in UK (11). In the case of γ- HBCD, an enrichment in (+)-enantiomer was generally observed (10, 11), except for the winkle from the e-waste recycling site in China that accumulated the (-)-enantiomer (13). These observations indicate that HBCD enantioslectivity in biota may be speciesspecific and may be a complex combination of environmental and biological processes, such as aerobic and anaerobic microbial transformation in the suspended particles and sediment and biotransformation processes in the food web. Further investigation of the enantiomeric composition of HBCDs in biota and in their habitat are needed for a better understanding of biotransformation and the degradation processes affecting HBCDs. The present findings provide clear evidence that some of the currently used non-PBDE BFRs are biomagnified in the present food web, with TMFs comparable to those of PBDEs. Particular attention should be given to monitoring biota levels and assessing ecological risks of these replacement substances developed by the BFR industry for the recently phased-out BFRs.

Acknowledgments This work was financially supported by the National Basic Research Program of China (No. 2009CB421604), the National Science Foundation of China (Nos. 4087307 and 40632012), China Postdoctoral Science Foundation Funded Project (20100470347), and the Earmarked Fund of the State Key Laboratory of Organic Geochemistry (OGL-200905).

Supporting Information Available Text addressing the aquatic samples and sampling site, stable isotope analysis and trophic level and TMF calculation, extraction, cleanup of and instrumental analysis of BFRs, quality assurance and quality control, Table S1 and Figure S1. This material is available free of charge via the Internet at http://pubs.acs.org.

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