Biomagnification of Higher Brominated PBDE Congeners in an

ARTICLE pubs.acs.org/est

Biomagnification of Higher Brominated PBDE Congeners in an Urban Terrestrial Food Web in North China Based on Field Observation of Prey Deliveries Le-Huan Yu,†,^ Xiao-Jun Luo,*,† Jiang-Ping Wu,† Li-Yu Liu,‡ Jie Song,‡ Quan-Hui Sun,§ Xiu-Lan Zhang,†,^ Da Chen,*,|| and Bi-Xian Mai† †

)

State Key Laboratory of Organic Geochemistry, Guangzhou Institute of Geochemistry, Chinese Academy of Sciences, Guangzhou 510640, China ‡ Key Laboratory for Biodiversity Science and Ecological Engineering, College of Life Sciences, Beijing Normal University, Beijing 100875, China § Beijing Raptor Rescue Center, International Fund for Animal Welfare, Beijing 100875, China Department of Environmental and Aquatic Animal Health, Virginia Institute of Marine Science, The College of William and Mary, Gloucester Point, Virginia 23062, United States ^ Graduate University of Chinese Academy of Sciences, Beijing 100039, China

bS Supporting Information ABSTRACT: As an important group of brominated flame retardants, polybrominated diphenyl ethers (PBDEs) persist in the wildlife food webs. However, the biomagnification of PBDEs has not been adequately studied in the terrestrial food webs. In this study, a terrestrial food web composed of common kestrels, sparrows, rats, grasshoppers, and dragonflies in the urban environment from northern China was obtained. A field prey delivery study, reinforced by δ13C and δ15N analyses, indicates that sparrows are the primary prey items of common kestrels. Concentrations of PBDEs were in the following order: common kestrel > sparrow > rat > grasshopper and dragonfly with BDE-209 as the dominant congener. Biomagnification factors (BMFs) were calculated as the ratio between the lipid normalized concentrations in the predator and prey. The highest BMF (6.9) was determined for BDE-153 in sparrow/common kestrel food chain. Other higher brominated congeners, such as BDE-202, -203, -154, -183, -197, and -209, were also biomagnified in this terrestrial food chain with BMF of 1.3
4.7. BDE-47, -99, and -100 were found to be biodiluted from sparrow to common kestrel (BMFs < 1). Measured BMF values for BDE-153, -47, -99, and -100 were consistent with predicted values from a nonsteady-state model in American kestrels from another study. Retention factors and metabolism of BDE congeners may be confounding factors influencing the measured BMFs in this current study.

’ INTRODUCTION Polybrominated diphenyl ethers (PBDEs) are brominated flame retardants (BFRs) widely used in textiles, polyurethane foams, thermoplastics, and electronic products.1 PBDEs are lipophilic and persistent; therefore, their biomagnification along the food chain can lead to concentration enrichment and health consequences in top predators, such as birds of prey. Due to growing environmental and human health concerns on the adverse effects of PBDEs, increasing regulations and restrictions have been carried out on the industrial use of the two major PBDE commercial formulations: penta- and octa-BDE mixture.2 However, deca-BDE, the largest commercial formulation produced by volume, remains in prevalent use in China even though its primary component, BDE-209, has been documented to debrominate to biologically harmful lower brominated congeners in the environment.3 r 2011 American Chemical Society

A number of studies have reported the biomagnification of PBDEs in aquatic food chains.4,5 The most commonly detected PBDE congeners in aquatic biota were those having three to six bromine substituents, of which BDE-47, -100, -154, and -153 were found to biomagnify in food webs of fish and marine mammals.5,6 The higher brominated PBDE congeners (e.g., octa- to deca-BDE) were more frequently observed in terrestrial biota and usually had an elevated contribution to total PBDE burdens in terrestrial animals.7,8 However, research has rarely been performed to evaluate the biomanficiation potential of Received: January 5, 2011 Accepted: May 13, 2011 Revised: May 1, 2011 Published: May 25, 2011 5125

dx.doi.org/10.1021/es200030z | Environ. Sci. Technol. 2011, 45, 5125–5131

Environmental Science & Technology

Figure 1. Map of sampling sites in Beijing, China.

PBDEs, particularly higher brominated congeners, in terrestrial food webs. To our knowledge, only two relevant studies have been done so far. Voorspoels et al.9 reported the biomagnification factors (BMFs) of PBDEs in three small terrestrial food chains in Belgium. Nonsteady-state BMFs of PBDEs in juvenile American kestrels were also calculated in an administrated study.10 However, none of these studies have evaluated the biomagnification potential of octa- to deca-BDE congeners, primarily because these congeners were not detected or levels were below limit of detection in the prey species and food items. Therefore, the biomagnification potential of higher brominated BDEs remains undetermined. Birds of prey are widely used as bioindicators in monitoring the organohalogenated pollution in the environment.7,11 Prey consumption of the predator is an important factor influencing the level and congener profile of PBDEs in the predator.12 Diet composition for birds varied greatly in different geographical areas, which could lead to large uncertainty in assessing the BMF if actual diet composition is unavailable. In our study, common kestrels and their prey were collected from the urban area of Beijing, China, based on direct observation of prey deliveries. The levels, congener profile, and BMFs of PBDEs were determined. Stable nitrogen- and carbon-isotopes (δ15N and δ13C) were also analyzed to confirm the diet source and trophic level. The objectives of this study were to (a) investigate PBDE contamination in primary prey items of common kestrels and (b) evaluate the biomagnfication potential for PBDEs, particularly higher brominated congeners, in the food webs of kestrels. This study is the first biomagnification report for octa- to decaBDE congeners in terrestrial ecosystem.

’ MATERIALS AND METHODS Sampling. Common kestrels (Falco tinnunculus, N = 23) were obtained from the Beijing Raptor Rescue Center (BRRC, China) between January 2005 and July 2007. Specimens available for analysis were received either dead, died during rehabilitation, or were euthanized at the BRRC due to serious injuries. The birds

ARTICLE

were then stored intact at
20 C until dissected with no signs of decay. Pectoral muscle (approximately 1.5 g in dry weight each) was excised for analysis. The prey animals of common kestrel, including sparrows, rats, and insects, were collected in the locations where common kestrels were found (Figure 1). A total of 40 Eurasian tree sparrows (Passer montanus) from 9 stations and 8 brown rats (Rattus norvegicus) from 3 stations were collected. Several hundred grasshoppers and approximately 80 dragonflies were collected from the same region where sparrows were found. The grasshoppers were then pooled into 5 samples (every 3.5 g in dry weight), while dragonflies were pooled into one sample (dry weight = 3.6 g). Additionally, 6 composite grass samples (5 g in dry weight each) and 8 pooled soil samples (30 g in dry weight each) were collected from the same region as the biota for PBDE analysis. Observation of Food Habits of Common Kestrels. The diet composition of the common kestrel was monitored using three methods: video recording, direct observation of prey delivery, and the examination of the prey remains in nests. Three kestrel nests located in Beijing Olympic Park and Beijing Normal University were selected for video recording in 2007 and 2008 for 112 days. Direct observations were conducted in seven selected nests in Haidian District and Changping District in Beijing City by observers using a 20
50 telescope. Nest observations were conducted between 6:00 a.m. and 7:00 p.m. for 5
12 h per day. The frequency of food delivery and the identity of the food items (if possible) were recorded during a total of 223 observation hours. Prey remains were collected from 12 nests and identified at the Key Laboratory for Biodiversity Science and Ecological Engineering of Beijing Normal University. Sample Preparation. Procedures for PBDE extraction and purification had been provided in detail elsewhere.13 Initially, a homogenized lyophilized biota sample was ground to powder and Soxhlet extracted with acetone/hexane (1:1, v/v) for 48 h. Surrogates (BDE-77, BDE-181, and 13C-BDE-209) for recovery estimation were spiked prior to extraction. An aliquot of the extract was used for lipid determination gravimetrically. The remainder was subjected to gel permeation chromatography (GPC) and eluted with dichloromethane/hexane (1:1, v/v) for lipid removal. The fraction from 90 to 280 mL, containing target compounds, was concentrated for further cleanup on a 2 g silica gel solid phase extraction column (Isolute, Biotage AB, Sweden), which was preactivated under 130 C for 15 h before use. The fraction containing PBDEs was obtained by elution with 6.5 mL of hexane/dichloromethane (60:40, v/v) and redissolved in 200 μL of isooctane. Internal standards (BDE-118 and -128) were spiked before instrumental analysis. The specific procedures of the pretreatment and cleanup for grass and soil samples, chemical information, and instrumental analysis are given in the Supporting Information (SI). QA/QC. Quality assurance and quality control was performed through the analysis of procedural blanks, triplicate spiked blanks, triplicate spiked matrices, and triplicate samples. Procedural blanks were consistently analyzed to each batch of twelve samples, and therefore the mean values were used for subtraction. PBDE levels in blanks were less than 10% of that in the samples. The mean recoveries for tri- to nona-BDEs ranged from 81.4
89.4% (RSDs < 5%) and was 104.3% (RSD = 8.0%) for BDE-209 in triplicate spiked matrices. The RSDs for all analytes including BDE-209 were sparrows > rats > grasshoppers and dragonflies, which is in line with the assumption that the predators have high concentrations of the contaminants. Two previous studies reported the PBDEs levels in muscle of kestrels. Jaspers et al.8 showed that PBDEs in muscle of Belgian kestrels have a median of 62 ng/g lw, which was much lower than those of the present study. Large variations in PBDE levels, covering from 279 to 31700 ng/g lw, among individual common kestrels collected in Beijing between March 2004 and January 2006 were found in our previous study.13 With the mean value of 12300 ( 5540 ng/g lw, it is 1 order of magnitude higher than in the present study (1100 ( 1800 ng/g lw), likely due to the extremely high concentration (31700 ng/g lw) of one kestrel.13 However, the median level (995 ng/g lw) was comparable with that of this study (400 ng/g lw). Presently, little information is available for PBDEs in sparrows and rats. Therefore, it is impossible to compare the levels of sparrows and rats in the present study with other studies. Recently, Van den Steen et al. reported the levels of PBDEs in eggs of blue tit and great tit collected from 14 European countries.11,18 PBDE levels, including BDE-28, -47, -100, -99, -154, -153, and -183, in these blue tit and great tit species ranged from 3.95
114 ng/g lw and from 4.00
136 ng/g lw, respectively, which is 1 order of magnitude lower than the levels in sparrows in the current study (100
2600 ng/g lw). Voorspoels et al.9 found that muscle tissues from two species of rodent in Belgium contain 2.2 and 30 ng/g lw PBDE, lower than those found in our study (70
330 ng/g lw). PBDEs in grass and soil varied from 3.1
7.1 ng/g dw and from 1.8
16 ng/g dw, respectively. Soil PBDE levels were slightly lower than those found in the Pearl River Delta (ranged from 2.4
67 ng/g dw)19 but was 2 orders of magnitude lower than those in soil nearby the e-waste recycling workshops.20 Presently, no study has been performed on the levels of PBDE in grass. Congener Profiles of PBDEs. Higher BDE congeners, especially BDE-209 and nona-BDE congeners, were found to be 5127

dx.doi.org/10.1021/es200030z |Environ. Sci. Technol. 2011, 45, 5125–5131

Environmental Science & Technology

ARTICLE

Table 1. Median Concentration and Range of Individual PBDE Congener in Biota (ng/g lw) and Abiota Samples (pg/g dw)a species

CK (n = 23)

ETS (n = 40)

BR (n = 8)

GH (n = 5b)

DF (n = 1b)

grass (n = 6b)

soil (N = 8b)

lipid(%)c

12.2 ( 3.3

10.4 ( 4.1

20.6 ( 10.2

9.7 ( 0.8

8.8




δ15N(%) c

7.2 ( 1.2

6.8 ( 1.3

6.0 ( 0.6

7.3 ( 0.4

8.5

2.9 ( 2.2





δ13C(%) c


18.4 ( 1.7


18.7 ( 3.3


21.8 ( 0.9


13.2 ( 0.4


20.2


14.9 ( 2.1




BDE-28

nd (nd
1.9)

0.83 (nd
3.0)

0.22 (nd
0.36)

0.25 (0.19
0.35)

nd

32 (22
64)

10 (3.5
85)

BDE-47

1.8 (nd
21)

6.9 (1.6
41)

2.6 (nd
4.4)

0.57 (nd
0.91)

3.4

74 (nd
96)

75 (nd
500)

BDE-99

2.9 (nd
260)

6.8 (1.0
39)

1.2 (0.73
1.6)

0.39 (0.29
0.45)

0.66

14 (13
25)

9.8 (2.0
42)

BDE-100

1.0 (nd
78)

1.8 (0.51
25)

0.56 (0.22
1.0)

0.17 (0.15
0.29)

0.27

47 (33
100)

70 (5.3
280)

BDE-153 BDE-154

53 (1.2
1300) 7.2 (nd
280)

7.7 (2.5
91) 3.3 (nd
47)

5.6 (0.91
12) 0.34 (nd
0.70)

0.50 (0.39
1.2) nd

3.6 0.27

nd 34 (25
52)

4.6 (nd
84) 36 (2.5
260)

BDE-183

17 (1.1
220)

9.0 (2.8
210)

4.9 (0.63
7.4)

0.58 (nd
1.2)

1.9

31 (24
58)

46 (4.2
440)

BDE-196

24 (2.3
670)

16 (3.7
420)

7.1 (2.7
11)

0.42 (nd
2.1)

2.2

nd (nd
83)

21 (nd
80)

BDE-197

15 (2.3
400)

11 (nd
390)

6.0 (2.2
11)

nd (nd
1.1)

1.3

nd

71 (nd
480)

BDE-201

10 (1.6
150)

11 (nd
150)

2.7 (nd
4.5)

0.86 (0.64
2.4)

0.82

nd (nd
12)

72 (7.7
350)

BDE-202

19 (1.1
610)

4.1 (1.2
280)

1.0 (nd
2.0)

nd (nd
1.4)

nd

nd

100 (11
340)

BDE-203

25 (3.3
1100)

8.5 (2.8
160)

4.9 (2.2
8.1)

0.88 (nd
3.9)

1.7

nd

99 (21
320)

BDE-206 BDE-207

27 (15
120) 37 (21
600)

34 (nd
200) 33 (14
290)

27 (11
60) 18 (nd
35)

9.6 (7.8
39) 8.7 (6.7
23)

12 nd

320 (nd
410) 510 (nd
630)

280 (nd
630) 430 (nd
1100)

BDE-208

23 (12
560)

23 (7.7
230)

11 (nd
20)

7.7 (5.8
20)

4.1

740 (nd
860)

780 (120
3100)

BDE-209

97 (29
2800)

68 (nd
1100)

45 (nd
150)

40 (19
270)

21

3400 (1600
5200)

2800 (1500
8600)

ΣPBDEs d

400 (120
8500)

250 (100
2600)

150 (70
330)

66 (51
370)

58

5300 (3200
7100)

5700 (1800
16000)

nd: not detectable. CK: common kestrel; ETS: Eurasian tree sparrow; BR: brown rat; GH: grasshopper; DF: dragonfly. b Pooled samples. c Mean ( SD. d ΣPBDEs: sum of BDE-28, -47, -99, -100, -153, -154, -183, -196, -197, -201, -202, -203, -206, -207, -208, and -209. a

Figure 2. Stable isotope ratio of nitrogen and carbon in biota samples.

abundant in all examined organisms and nonbiological matrices (soil and grass) (Figure 3). The proportions of BDE-209 decreased from more than 60% in soil and grass, to above 50% in the grasshoppers, and further to approximately 30% in the sparrows, the rats and the common kestrels. This decreasing trend may be partly explained by the debromination of BDE-209 in high trophic species such as birds and rats. Significantly higher ratios of nona- to deca-BDE found in the bird and rat samples (mean of 1.0, 1.4, and 1.2 for common kestrels, sparrows, and rats, respectively) than soil and grass samples (mean of 0.40 and 0.53, respectively) supported this explanation. Several laboratory exposure studies have reported metabolic debromination of BDE-209 in birds (European starling)21 and rodents (rat).22 BDE-153 was the second most abundant congener found in the common kestrel, similar to our previous study.13 Such congener pattern has been reported in terrestrial species such

Figure 3. Congener profiles of PBDEs in the sampled species.

as red fox,23 raccoon dog,24 and jungle crow,25 demonstrating bioaccumulation of higher BDE congeners in terrestrial organisms. Dragonflies show relatively high abundance of BDE-47 5128

dx.doi.org/10.1021/es200030z |Environ. Sci. Technol. 2011, 45, 5125–5131

Environmental Science & Technology

ARTICLE

Table 2. Biomagnification Factors (BMFs) of Individual PBDE Congener in Common Kestrel’s Food Chain Under Study BMF congener

a

sparrow/CK b

rat/CK

grasshopper/CK

dragonfly/CK

BDE-28

nd

nd

nd

nd

BDE-47

0.26

0.68

2.7

0.52

BDE-99

0.42

2.4

7.3

4.4

BDE-100

0.55

1.8

5.8

3.6

BDE-153 BDE-154

6.9 2.2

9.5 21

100 nd

15 27

BDE-183

1.9

3.6

30

9.1

BDE-196

1.5

3.4

58

11

BDE-197

1.3

2.4

160

12

BDE-201

0.93

3.7

12

12

BDE-202

4.7

20

nd

nd

BDE-203

2.9

5.0

28

15

BDE-206 BDE-207

0.79 1.1

1.0 2.1

2.8 4.3

2.3 7.0

BDE-208

1.0

2.1

2.9

5.5

BDE-209

1.4

2.1

2.4

4.7

ΣPBDEsc

1.6

2.8

6.0

6.9

a

CK: common kestrel. b nd: not detectable because concentration in prey species were under the method detection limit. c ΣPBDEs: sum of BDE-28, -47, -99, -100, -153, -154, -183, -196, -197, -201, -202, -203, 2-06, -207, -208, and -209.

than other organisms (Figure 3), which can attribute to the distinctive living habitat and feeding habit of dragonflies. The larvae of dragonflies live in water and feed on aquatic species small in size. A predominance of BDE-47 in aquatic-feeding species has been demonstrated in previous studies.5 Biomagnification of PBDEs. Few studies have demonstrated the biomagnification of PBDEs in terrestrial food web.9 Here we examined the BMF values (the ratio of lipid-normalized concentrations between predator and prey) for PBDEs in several common kestrel food chains (Table 2). The BMF values for ∑PBDEs ranged from 1.6
6.9, indicating biomagnification of PBDEs in all examined food chains. However, BMF values for individual congener varied from less than 1 to 160, indicating a diverse mechanism of bioaccumulation and biotransformation for PBDE congeners (Table 2). Since sparrow is the primary food item of the common kestrel, BMF calculated from the sparrow/ common kestrel feeding relationship is more credible than other feeding relationships. In the sparrow
kestrel food chain, BDE153 exhibited the highest biomagnification potential with BMF of 6.9, followed by BDE-202, -203, -154, and -183. Surprisingly, no biomagnification could be found for lower brominated congeners such as BDE-47, -99, and -100 (BMF < 1). The highest BMF for BDE-153 has been reported in both marine and terrestrial food webs. Muir et al. 26 estimated ringed seal/polar bear BMFs for BDE-47, -99, -100, and -153 from different locations in the Arctic. All four congeners were biomagnified, and the highest BMF value (71) was found for BDE153. Additionally, BDE-153 was the only PBDE congener showing biomagnification in the ringed seal/polar bear relation from Svalbard, Norway.27 In terrestrial food webs, Voorspoels et al.9 calculated BMFs for several tri- to hepta-BDE congeners in

two predatory bird food chains (passerine/sparrowhawk and rodent/buzzard) and one mammalian food chain (rodent/fox) from Belgium. All congeners, except BDE-28, showed biomagnification in the two avian food chains with the highest BMF obtained for BDE-153 in rodent/buzzard food chain. In a laboratory exposure study,10 the nonsteady-state BMFs for BDE-47, -99, -100, and -153 were predicted by the bioaccumulation model in juvenile American kestrels. The model-predicted nonsteady-state BMF value (6.9) was close to our measured BMF for BDE-153 when BDE-153 was estimated as a persistent chemical. The high BMF for BDE-153 in our kestrels may be due to their persistent and lipophilic nature that favors bioaccumulation and transference along food chains via food uptake. Another possible explanation for the high abundance of BDE-153 in birds is that BDE-153 is derived from metabolic breakdown of BDE209, but this has not been proven. BDE-202 has the second highest BMF in common kestrels. BDE-202 was not found in any of major PBDE formulations.3 However, it has been identified as a metabolite of BDE-209 in common sole and common carp during the dietary exposure studies28,29 as well as in a field study conducted in a wastewater receiving stream.30 Although no experimental evidence for metabolic breakdown of BDE-209 to BDE-202 in terrestrial birds was found, it was reasonable to deduce that the high BMF of BDE-202 is partly due to the debromination of BDE-209. BDE-47, -100, and -99 were unexpectedly not biomagnified in the examined food chains. As the most abundant PBDE congener in aquatic biota, BDE-47 has been reported to biomagnify in most studied aquatic food webs.5,7 The biodilution of BDE-47, -99, and -100 may be due to the rapid elimination of these congeners in the kestrel. BDE-47 has the lowest retention factor in administrated American kestrel,10 and rapid elimination of € and KlassonBDE-47 in rats has been demonstrated by Orn Wether.31 The BMF values calculated in this current field study were very comparable to the values predicted in the American kestrel lab exposure study, i.e., 0.26 vs 0.25 for BDE-47, 0.42 vs 0.61 for BDE-99, and 0.61 vs 0.70 for BDE-100. BDE-209 was the most abundant congener in all organisms and soil in the present study. Although a number of studies have reported the bioaccumulation of BDE-209 in wild organisms, its biomagnification potential has rarely been investigated. In the bioaccumulation model developed by Kelly et al.32 for the prediction of potentially bioaccumulative, BDE-209 has predicted BMF values of 3 and 8 in marine mammals and terrestrial carnivores, respectively. However, few studies reported the biomagnification of BDE-209 in food chains. Jenssen et al.33 observed biomagnification of BDE-209 from polar cod to harbor seals in North-East Atlantic marine ecosystems with a BMF of 2.2. In the present study, BDE-209 was biomagnified in the common kestrel with BMF from 1.4 to 4.7 (Table 2). In addition to BDE-209, several nona- and octa-BDE congeners such as BDE-196, -197, 202, and -203 were also biomagnified with BMF larger than 1. To our knowledge, this is the first report for the biomagnification of octa- to deca-BDE congeners in terrestrial food chains. Therefore, our results suggest that in the evaluation of deca-BDE contamination, the potential degradation products of BDE-209 should not be neglected, as some of them may be more bioavailable and toxic, and have greater biomagnfication potential than BDE-209 itself. Unfortunately, studies remain very limited in the investigation of environmental behaviors of these potential BDE-209 degradation products. 5129

dx.doi.org/10.1021/es200030z |Environ. Sci. Technol. 2011, 45, 5125–5131

Environmental Science & Technology The BMFs were plotted against the log Kow of the PBDE congeners in Figure S1 in the SI. No significant correlation was found between BMFs and log Kow (p > 0.05). BMFs increased up to approximately log Kow = 8.0 then declined with further increasing log Kow. Similar parabolic relationship was found between log BMF and bromine atom numbers in the study on frogs.34 Also, no significant correlation was shown between TMF and log Kow for PBDEs in a Canadian Arctic marine food web.6 The rise in BMFs less than 8.0 was expected to result from their lipophilicity, while the subsequent drop in BMFs likely reflected reduced bioavailability and more elimination as well as faster metabolic degradation in organisms. Gandhi et al.35 also suggested that biotransformation would result in deviation of the BMF values from the general trend. In summary, higher BDE congeners were found to be biomagnified in an urban terrestrial food web while lower BDE congeners were biodiluted. Thus, the bioaccumulation of PBDEs in the terrestrial ecosystem could be distinguished from those in the aquatic ecosystem. More attention should be given on the bioaccumulation of higher BDE congeners in the terrestrial ecosystem to assess the risk of the technical deca-BDE mixture.

’ ASSOCIATED CONTENT

bS

Supporting Information. Detailed information for chemicals, cleanup procedures for abiotic samples, instrumental analysis, method detection limit (Table S1), and relationship between BMFs and log Kow of PBDEs (Figure S1). This material is available free of charge via the Internet at http://pubs.acs.org.

’ AUTHOR INFORMATION Corresponding Author

*Phone: þ86-20-85290146. Fax: þ86-20-85290706. E-mail: [email protected] (X.-J.L.); [email protected] (D.C.).

’ ACKNOWLEDGMENT This work was funded by the National Science Foundation of China (Nos. 20890112, 21077105, and 40773061), the Chinese Academy of Sciences (No. KZCX2-EW-QN 105), and the National Basic Research Program of China (No. 2009CB4216604). This is contribution No. IS-1342 from GIG, CAS. ’ REFERENCES (1) Environmental Health Criteria 162: Brominated diphenyl ethers; World Health Organization: Geneva, Switzerland, 1994. http://www. inchem.org/documents/ ehc/ehc/ehc162.htm (accessed November 28th 2010). (2) Gauthier, L. T.; Hebert, G. E.; Weseloh, D. V. C.; Letcher, R. J. Current-use flame retardants in the eggs of herring gulls (Larus argentatus) from the Laurentian Great Lakes. Environ. Sci. Technol. 2007, 41, 4561–4567. (3) La Guardia, M. J.; Hale, R. C.; Harvey, E. Detailed polybrominated diphenyl ether (PBDE) congener composition of the widely used penta-, octa-, and deca-PBDE technical flame-retardant mixtures. Environ. Sci. Technol. 2006, 40, 6247–6254. (4) Law, R. J.; Allchin, C. R.; de Boer, J.; Covaci, A.; Herzke, D.; Lepom, P.; Morris, S.; Tronczynski, J.; de Wit, C. A. Levels and trends of brominated flame retardants in the European environment. Chemosphere 2006, 64, 187–208. (5) de Wit, C. A.; Herzke, D.; Vorkamp, K. Brominated flame retardants in the Arctic environment
trends and new candidates. Sci. Total Environ. 2010, 408, 2885–2918.

ARTICLE

(6) Kelly, B. C.; Ikonomou, M. G.; Blair, J. D.; Gobas, F. A. P. C. Bioaccumulation behaviour of polybrominated diphenyl ethers (PBDEs) in a Canadian Arctic marine food web. Sci. Total Environ. 2008, 401, 60–72. (7) Chen, D.; Hale, R. C. A global review of polybrominated diphenyl ether flame retardant contamination in birds. Environ. Int. 2010, 36, 800–811. (8) Jaspers, V. L. B.; Covaci, A.; Voorspoels, S.; Dauwe, T.; Eens, M.; Schepens, P. Brominated flame retardants and organochlorine pollutants in aquatic and terrestrial predatory birds of Belgium: Levels, patterns, tissue distribution and condition factors. Environ. Pollut. 2006, 139, 340–352. (9) Voorspoels, S.; Covaci, A.; Jaspers, V. B.; Neels, H.; Schepens, P. Biomagnification of PBDEs in three small terrestrial food chains. Environ. Sci. Technol. 2007, 41, 411–416. (10) Drouillard, K. G.; Fernie, K. J.; Letcher, R. J.; Shutt, L. J.; Whitehead, M.; Gebink, W.; Bird, D. A. Bioaccumulation and biotransformation of 61 polychlorinated biphenyl and four polybrominated diphenyl ether congeners in juvenile American kestrels (Falco sparverius). Environ. Toxicol. Chem. 2007, 26, 313–324. (11) Van den Steen, E.; Pinxten, R.; Jaspers, V. L. B.; Covaci, A.; Barba, E.; Carere, C.; Cicho n, M.; Dubiec, A.; Eeva, T.; Heeb, P.; Kempenaers, B.; Lifjeld, J. T.; Lubjuhn, T.; M€and, R.; Massa, B.; Nilsson, J. A.; Norte, A. C.; Orell, M.; Podzemny, P.; Sanz, J. J.; Senar, J. C.; Soler, J. J.; Sorace, A.; T€ or€ok, J.; Visser, M. E.; Winkel, W.; Eens, M. Brominated flame retardants and organochlorines in the European environment using great tit eggs as a biomonitoring tool. Environ. Int. 2009, 35, 310–317. (12) 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, 5248–5255. (13) Chen, D.; Mai, B. X.; Song, J.; Sun, Q.; Luo, Y.; Luo, X. J.; Zeng, E. Y.; Hale, R. C. Polybrominated diphenyl ethers in birds of prey from Northern China. Environ. Sci. Technol. 2007, 41, 1828–1833. (14) Jardine, T. D.; Kidd, K. A.; Fisk, A. T. Applications, considerations, and sources of uncertainty when using stable isotope analysis in ecotoxicology. Environ. Sci. Technol. 2006, 40, 7501–7511. (15) Wang, G. A.; Han, J. M.; Zhou, L. P.; Xiong, X. G.; Tan, M.; Wu, Z. H.; Peng, J. Carbon isotope ratios of C4 plants in loess areas of North China. Sci. China, Ser. D: Earth Sci. 2006, 49, 97–102. (16) Wang, G. A.; Han, J. M.; Liu, D. S. The carbon isotope composition of C3 herbaceous plants in loess area of northern China. Sci. China, Ser. D: Earth Sci. 2003, 46, 1069–1076. (17) Kelly, J. F. Stable isotopes of carbon and nitrogen in the study of avian and mammalian trophic ecology. Can. J. Zool. 2000, 78, 1–27. (18) Van den Steen, E.; Pinxten, R.; Covaci, A.; Carere, C.; Eeva, T.; Heeb, P.; Kempenaers, B.; Lifjeld, J. T.; Massa, B.; Norte, A. C.; Orell, M.; Sanz, J. J.; Senar, J. C.; Sorace, A.; Eens, M. The use of blue tit eggs as a biomonitoring tool for organohalogenated pollutants in the European environment. Sci. Total Environ. 2010, 408, 1451–1457. (19) Zou, M. Y.; Ran, Y.; Gong, J.; Mai, B. X.; Zeng, E. Y. Polybrominated diphenyl ethers in watershed soils of the Pearl River Delta, China: Occurrence, inventory, and fate. Environ. Sci. Technol. 2007, 41, 8262–8267. (20) Luo, Y.; Luo, X. J.; Lin, Z.; Chen, S. J.; Liu, J.; Mai, B. X.; Yang, Z. Y. Polybrominated diphenyl ethers in road and farmland soils from an e-waste recycling region in Southern China: Concentrations, source profiles, and potential dispersion and deposition. Sci. Total Environ. 2009, 407, 1105–1113. (21) Van den Steen, E.; Covaci, A.; Jaspers, V. L. B.; Dauwe, T.; Voorspoels, S.; Eens, M.; Pinxten, R. Accumulation, tissue-specific distribution and debromination of decabromodiphenyl ether (BDE 209) in European starlings (Sturnus vulgaris). Environ. Pollut. 2007, 148, 648–653. (22) Huwe, J. K.; Smith, D. J. Accumulation, whole-body depletion, and debromination of decabromodiphenyl ether in male SpragueDawley rats following dietary exposure. Environ. Sci. Technol. 2007, 41, 2371–2377. 5130

dx.doi.org/10.1021/es200030z |Environ. Sci. Technol. 2011, 45, 5125–5131

Environmental Science & Technology

ARTICLE

(23) Voorspoels, S.; Covaci, A.; Lepom, P.; Escutenaire, S.; Schepens, P. Remarkable findings concerning PBDEs in the terrestrial top-predator red fox (Vulpes vulpes). Environ. Sci. Technol. 2006, 40, 2937–2943. (24) Kunisue, T.; Takayanagi, N.; Isobe, T.; Takahashi, S.; Nakatsu, S.; Tsubota, T.; Okumoto, K.; Bushisue, S.; Shindo, K.; Tanabe, S. Regional trend and tissue distribution of brominated flame retardants and persistent organochlorines in raccoon dogs (Nyctereutes procyonoides) from Japan. Environ. Sci. Technol. 2008, 42, 685–691. (25) Kunisue, T.; Higaki, Y.; Isobe, T.; Takahashi, S.; Subramanian, A.; Tanabe, S. Spatial trends of polybrominated diphenyl ethers in avian species: Utilization of stored samples in the Environmental Specimen Bank of Ehime University (es-Bank). Environ. Pollut. 2008, 154, 272–282. (26) Muir, D. C. G.; Backus, S.; Derocher, A. E.; Dietz, R.; Evans, T. J.; Gabrielsen, G. W.; Nagy, J.; Norstrom, R. J.; Sonne, C.; Stirling, I.; Taylor, M. K.; Letcher, R. J. Brominated flame retardants in polar bears (Ursus maritimus) from Alaska, the Canadian Arctic, East Greenland, and Svalbard. Environ. Sci. Technol. 2006, 40, 449–455. (27) Sørmo, E. G.; Salmer, M. P.; Jenssen, B. M.; Hop, H.; B!k, K.; Kovacs, K. M.; Lydersen, C.; Falk-Petersen, S.; Gabrielsen, G. W.; Lie, E.; Skaare, J. U. Biomagnification of polybrominated diphenyl ether and hexabromocyclododecane flame retardants in the polar bear food chain in Svalbard, Norway. Environ. Toxicol. Chem. 2006, 25, 2502–2511. (28) Munschy, C.; Heas-Moisan, K.; Tixier, C.; Olivier, N.; Gastineau, O.; Le Bayon, N.; Buchet, V. Dietary exposure of juvenile common sole (Solea solea L.) to polybrominated diphenyl ethers (PBDEs): Part 1. Bioaccumulation and elimination kinetics of individual congeners and their debrominated metabolites. Environ. Pollut. 2011, 159, 229–237. (29) Stapleton, H. M.; Alaee, M.; Letcher, R. J.; Baker, J. E. Debromination of the flame retardant decabromodiphenyl ether by juvenile carp (Cyprinus carpio) following dietary exposure. Environ. Sci. Technol. 2004, 38, 112–119. (30) La Guardia, M. J.; Hale, R. C.; Harvey, E. Evidence of debromination of decabromodiphenyl ether (BDE-209) in biota from a wastewater receiving stream. Environ. Sci. Technol. 2007, 41, 6663–6670. € U.; Klasson-Wehler, E. Metabolism of 2,20 ,4,40 -tetrabro(31) Orn, modiphenyl ether in rat and mouse. Xenobiotica 1998, 28, 199–211. (32) Kelly, B. C.; Ikonomou, M. G.; Blair, J. D.; Morin, A. E.; Gobas, F. A. P. C. Food web-specific biomagnification of persistent organic pollutants. Science 2007, 317, 236–239. (33) Jenssen, B. M.; Sørmo, E. G.; B!k, K.; Bytingsvik, J.; Gaustad, H.; Ruus, A.; Skaare, J. U. Brominated flame retardants in North-East Atlantic marine ecosystems. Environ. Health Perspect. 2007, 115, 35–41. (34) Wu, J. P.; Luo, X. J.; Zhang, Y.; Chen, S. J.; Mai, B. X.; Guan, Y. T.; Yang, Z. Y. Residues of polybrominated diphenyl ethers in frogs (Rana limnocharis) from a contaminated site, South China: Tissue distribution, biomagnification, and maternal transfer. Environ. Sci. Technol. 2009, 43, 5212–5217. (35) Gandhi, N.; Bhavsar, S. P.; Gewurtz, S. B.; Diamond, M. L.; Evenset, A.; Christensen, G. N.; Gregor, D. Development of a multichemical food web model: Application to PBDEs in Lake Ellasjøen, Bear Island, Norway. Environ. Sci. Technol. 2006, 40, 4714–4721.

5131

dx.doi.org/10.1021/es200030z |Environ. Sci. Technol. 2011, 45, 5125–5131