Plant selective uptake of halogenated flame retardants at an e-waste recycling site in southern China

Environmental Pollution 214 (2016) 705e712

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Plant selective uptake of halogenated flame retardants at an e-waste recycling site in southern China* Shaorui Wang a, d, Yan Wang b, Chunling Luo a, *, Jun Li a, Hua Yin c, Gan Zhang a a

Guangzhou Institute of Geochemistry, Chinese Academy of Sciences, Guangzhou 510640, China Key Laboratory of Industrial Ecology and Environmental Engineering (MOE), School of Environmental Science and Technology, Dalian University of Technology, Dalian 116024, China c College of Environment and Energy, South China University of Technology, Guangzhou, China d Graduate University of Chinese Academy of Sciences, Beijing 100039, China b

a r t i c l e i n f o

a b s t r a c t

Article history: Received 4 January 2016 Received in revised form 11 April 2016 Accepted 19 April 2016 Available online 2 May 2016

The concentrations and homolog patterns of halogenated flame retardants (HFRs) in vegetables grown at an e-waste contaminated site were investigated. Polybrominated diphenyl ethers (PBDEs) were the dominant HFRs in vegetable tissues, with concentrations ranging from 10.3 to 164 ng g
1 and 1.16 e107 ng g
1 in shoots and roots, respectively, followed by novel brominated flame retardants (NBFRs) and dechlorane plus (DPs). This is an indication that PBDE contamination in vegetables grown around ewaste recycling sites may pose a risk to the local terrestrial ecosystem and residents. In addition, this is the first report on the concentrations and compositions of NBFRs in vegetables around e-waste recycling sites. The HFRs concentrations in vegetables varied greatly with the vegetable species, with the highest concentrations observed in Brassica oleracea var. capitata. Root concentration factors (RCF) decreased with increasing log Kow of HFRs, which indicated that the uptake of HFRs was controlled mainly by log Kow. Dissimilar HFRs profiles in shoots and roots suggested that the uptake and translocation of HFRs by plants were selective, with lower halogenated congeners prone to accumulation in vegetable tissues. Positive relationships between PBDEs and their substitutes were observed in vegetable tissues, suggesting that the replacement of PBDEs by NBFRs has not resulted in an obvious transition in plants within the study area. © 2016 Elsevier Ltd. All rights reserved.

Keywords: Vegetable E-waste Plant uptake PBDEs NBFRs DPs

1. Introduction Driven by profit, the recycling of electronic waste (e-waste) using primitive processes is being carried out extensively in developing countries (Leung et al., 2011; Zhang et al., 2012). Approximately 70% of e-waste generated worldwide is processed in China every year (Fujimori and Takigami, 2014; Robinson, 2009). Although China has already drafted and implemented laws and regulations to control illegal handling of e-waste, ineffective enforcement has facilitated serious environmental pollution to occur (Tong, 2004). Polybrominated diphenyl ethers (PBDEs) and Dechlorane Plus (DPs) are a group of chemicals historically used widely as flame

*

This paper has been recommended for acceptance by Baoshan Xing. * Corresponding author. E-mail address: [email protected] (C. Luo).

http://dx.doi.org/10.1016/j.envpol.2016.04.071 0269-7491/© 2016 Elsevier Ltd. All rights reserved.

retardants in a variety of electronic products (Morf et al., 2005). Primitive e-waste processing, such as open air incineration, acid washing, and manual disassembling, undertaken has resulted in extensive release of these compounds into the surrounding environment (Wong et al., 2007). For instance, high concentrations of PBDEs have been observed in soil (2720e4250 ng/g) (Leung et al., 2007), air (21.5 ng/m3) (Deng et al., 2007), sediment (6000e30 000 ng/g), and biota samples (3100 ng/g lipid, processing workers) (Bi et al., 2007) around e-waste dismantling sites. Due to the growing recognition of their adverse environmental and ecological effects, many PBDE formulations have come under increasing regulatory control. Following the phase-out of PBDEs, novel brominated flame retardants (NBFRs) which commonly consist of 1,2-bis(2,4,6-tribromophenoxy) ethane (TBE), 2ethylhexyl-2,3,4,5-tetrabromobenzoate (TBB), bis(2-ethylhexyl)3,4,5,6-tetrabromo-phthalate (TBPH), hexabromobenzene (HBB), pentabromoethylbenzene (PBEB) and decabromodiphenylethane (DBDPE) have been marketed (Tian et al., 2012). Recently, more

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information related to the environmental occurrence of NBFRs, particularly regarding their fate, toxicological profile, and transport characteristics, has been obtained (de Wit et al., 2010; Ismail et al., 2009; Shi et al., 2009). However, limited publications are available on the distribution pattern of old and emerging flame retardants in vegetation from e-waste recycling sites, in particular for vegetables consumed by local residents. The uptake of persistent organic pollutants (POPs) from environmental matrices into plants has attracted considerable research interest, because it plays an important role in trapping and transferring POPs to terrestrial ecosystems, with a corresponding ecological risk (Luo et al., 2015). Soil-air-leaf and soil-root pathways are the two widely accepted routes for organic chemical uptake by plants, which have generally been described by the transpiration stream concentration factor and octanol-air or octanol-water partitioning (log Koa or log Kow) (Limmer and Burken, 2014; Tian et al., 2012). However, the translocation of some hydrophilic compounds in plants reveals the limited ability of chemical physicochemical properties, such as Kow, in accurate descriptions of the translocation of organic contaminants, because their log Kow values do not fall within an intermediate hydrophobicity range (Dettenmaier et al., 2008; Limmer and Burken, 2014). In addition, environmental conditions, the plant species, and plant physiology have been reported as factors controlling plant uptake of POPs (Wang et al., 2014b). Assessing accumulation of POPs in plants solely by gathering exhaustive experimental data such as using pot experiments, while reliable, is overly resource intensive and unsustainable, particularly when considering the diversity of plant varieties and the number of chemicals being generated in abundance. In contrast, plant uptake of POPs from contaminated sites in the presence of multiple contaminants, is a pressing area for further investigation. The present study was conducted in an intensive e-waste recycling region, Guiyu, which is one of the most notorious e-waste recycling areas in China. Active aqua- and agricultural operations can still be observed amid recycling activities, in rivers and farmlands surrounding the area. The distribution and composition of HFRs in rhizosphere and non-rhizosphere soils of farmland in this region were investigated in our previous study. However, limited investigations have been undertaken on the accumulation of POPs in vegetation affected by e-waste recycling activities. Thus, this study was designed to (a) determine the in-situ distribution and composition of HFRs in vegetables grown at the e-waste recycling site, (b) elucidate the potential relationship between the physicochemical properties of HFRs and accumulation in vegetation, and provide greater insight into the potential effects of e-waste recycling on terrestrial ecosystems. 2. Materials and methods 2.1. Sampling site As shown in Fig. 1, all of the sampling sites were adjacent to an ewaste dismantling site in Guiyu town [23 30 N, 116 030 E], eastern Guangdong Province, South China. The agrotype in this area is red earth, the average annual rainfall and average annual temperature are approximately 1721 mm and 21.5  C, respectively (Yu et al., 2006). The samples were collected in December 2012. In total, 14 types of vegetables, including cabbage lettuce (Lactuca sativa L. var. capitata L, P1), Chinese cabbage (Brassica pekinensis, P2), celery (Apium graveolens, P3), Chinese kale (Brassica alboglabra L. H. Bailey, P4), broccoli (Brassica oleracea L. var. botrytis L, P5), shallot (Allium fistulosum, P6), cabbage (Brassica oleracea var. capitata, P7), radish (Raphanus sativus L, P8), taro (Colocasia esculenta (L.) Schoot, P9), crown daisy (Chrysanthemum coronarium L., P10), pakchoi (Brassica campestris L. ssp., P11), snow peas (Pisum sativum, P12), sweet

Fig. 1. Sampling sites.

potato (Ipomoea batatas (L.) Lam., P13), and lettuce (Lactuca sativa, P14) were sampled. In addition, the corresponding rhizosphere soils were also collected, and the detail descriptions can be found in our previous study (Wang et al., 2016). Each sample was composed of at least three subsamples collected from the same type of vegetable around the sampling site. All samples were wrapped in aluminium foil, placed in polythene zip-lock bags, and transported to the lab immediately. 2.2. Chemical analysis All plant samples were washed with tap water and rinsed with deionized water. Each individual plant sample was divided into shoot (aboveground parts) and root subsamples. The samples were freeze-dried and ground into fine powder. Subsequently, approximately 5 g plant samples homogenized with 3 g anhydrous sodium sulfate, spiked with relevant recovery standards (PCB 30, PCB 198, and PCB 209), were soxhlet extracted using hexane/acetone (3:1, V/ V) for 72 h. The fractionated plants were concentrated to ~0.5 mL after solvent-exchange to hexane. The plant extracts were washed with sulfuric acid and then cleaned up using a multi-layer column containing neutral alumina (3% deactivated), neutral silica gel (3% deactivated), 50% (w/w) sulfuric acid-silica gel, and anhydrous Na2SO4, from bottom to top, using an eluent of 20 ml hexane/DCM (1:1, V/V). After evaporating to approx. 50 ml, 13C-PCB 141 was added as the internal standard before instrumental analysis. 2.3. Instrumental analysis GC-ENCI-MS (Agilent GC7890 coupled with 5975C MSD) applied with a CP-Sil 13 CB column (15 m  25 mm i.d.  0.25 mm film thickness) was used to analyse BDE 209. Eight PBDEs (BDE 28, 47, 99, 100, 154, 153, 183, and 209), two DPs (syn-DP and anti-DP), and six NBFRs (TBE, TBB, TBPH, HBB, PBEB, and DBDPE) were analysed separately using a DB5-MS capillary column (30 m  0.25 mm i.d.  0.25 mm film thickness). Analytical details have been described previously (Wang et al., 2011). 2.4. QA/QC A procedural blank, a spiked blank containing all chemicals, and

S. Wang et al. / Environmental Pollution 214 (2016) 705e712

a duplicated sample were run simultaneously with each batch of 10 samples to assess potential sample contamination and the repeatability of the analysis. No target compounds were detected in the laboratory blanks. The surrogate recoveries for polychlorinated biphenyl (PCB 30), PCB 198, and PCB 209 in all samples were 56 ± 8%, 80 ± 14%, and 78 ± 14%, respectively. The results of this study were corrected based on the surrogate recoveries. 2.5. Statistical analysis All statistical calculations, such as Pearson's correlation analysis (p-value < 0.05), were performed using SPSS ver.17.0. 3. Results and discussion 3.1. Accumulation of HFRs in vegetables The total concentration of eight PBDE congeners (SPBDEs) in shoots averaged 37.5 ng g
1, ranging from 10.3 to 164 ng g
1, while SPBDEs in roots averaged 21.2 ng g
1, ranging from 1.16 to 107 ng g
1 (Fig. 2). The highest shoot and root PBDE concentrations were both observed in cabbage. These values are close to those found in eucalyptus (30.6e154 ng g
1), but lower than those in pine needles (15.1e236 ng g
1) grown at the e-waste contaminated site (Tian et al., 2012). However, they are much higher than those reported in plants (13.9e15.1 ng g
1) (Wang et al., 2011) and vegetables (0.88e5.69 ng g
1 in shoot, 0.97e13.0 ng g
1 in root) (Wang et al., 2014b) grown on agricultural soil around another e-waste dismantling site. Such elevated values can be attributed to several factors, including the variability in e-waste and the characteristics of the region. Root concentrations of PBDEs in radish, taro and lettuce were much lower than those in other plant species, probably due to a reduction in absorbed PBDEs by the relatively larger root volume and the lower root-specific surface of these species. BDEs 28 and 47 were the most abundant congeners in shoots, while BDE 209 was the most abundant congener in roots. The concentrations of BDE 209 were in the ranges of 1.75e143 ng g
1 (mean 17.8 ng g
1) and 0.72e88.0 ng g
1 (mean 15.7 ng g
1) in shoots and roots, respectively. With respect to NBFRs, the concentrations in shoots and roots ranged from 8.41 to 69.5 and 7.08e82.0 ng g
1, with averages of 28.8 and 30.0 ng g
1, respectively (Fig. 2). Among the NBFR congeners, the highest abundance was observed for DBDPE in the range of 0.66e17.0 ng g
1 (mean 4.23 ng g
1) and 0.69e18.4 ng g
1 (mean 4.68 ng g
1) in shoots and roots respectively, followed by HBB and TBB. The only publication on NBFR distribution in plant tissues reported higher concentrations of DBDPE in pine needles (11.2e42.3 ng g
1) and eucalyptus leaves (9.14e35.6 ng g
1), in another intensive e-waste recycling area in South China (Tian et al.,

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2012). In contrast, TBPH was found at the lowest concentrations with ranges of 0.35e1.74 ng g
1 (mean 0.70 ng g
1) and 0.03e6.71 ng g
1 (mean 3.09 ng g
1) in shoots and roots, respectively. To the best of our knowledge, this is the first report of concentrations and compositions of NBFRs in vegetables around an ewaste recycling site. DPs concentrations in shoots and roots were 0.34e1.22 ng g
1 and 0.08e16.98 ng g
1, with average concentrations of 0.78 and 1.60 ng g
1, respectively (Fig. 2). The highest DPs concentrations in shoots and roots were observed in cabbage and radish, respectively. Concentrations measured in this study were lower than those found in eucalyptus foliage (0.45e16.7 ng g
1) and pine needles (0.51e51.9 ng g
1) at another e-waste site, but close to those measured in plant samples from the reference site (0.09e2.46 ng g
1) (Chen et al., 2011), which indicated that DPs were not the dominant contaminant at this e-waste recycling site. This was also confirmed by the relatively low concentrations of DPs in the corresponding soils described in our previous study (Wang et al., 2016). Previous studies (Tian et al., 2012, 2011) reported that concentrations of DBDPE were lower than those of BDE 209 in pine needle and air samples around e-waste contaminated sites. However, in the current study, DBDPE concentrations in shoots were higher than those of BDE 209 in most detected samples. In contrast, no consistent trend was found between DBDPE and BDE 209 in roots. These results may be related to the temporal variations in HFR usage and emission. 3.2. Homologue pattern of HFRs in vegetables Homologue patterns of PBDEs and NBFRs in vegetables are shown in Fig. 3. Lower brominated PBDEs, such as BDEs 28 and 47, showed higher proportions in shoots than in roots. The sum of BDEs 28 and 47 accounted for more than 50% of total PBDEs in shoots, while they accounted for 24.8% in roots. A relatively low proportion of BDE 209 (mean ¼ 33%) was found in shoots, while a predominance of BDE 209 in roots was found in most samples, with a mean value of 60.9%. However, the proportions of lower brominated PBDEs (BDEs 28 and 47) in vegetable roots were much higher than those in the corresponding rhizosphere soils, as shown in our previous study (Wang et al., 2016). In addition, our previous result showed that lower brominated PBDEs were acropetally translocated preferentially from roots to shoots, in comparison with higher brominated PBDEs, after growing on e-waste contaminated soils for 60 days (Wang et al., 2015a). Hence, the lower brominated PBDEs (BDEs 28 and 47) presented here were potentially taken up by plant roots and then translocated to shoots, while higher brominated PBDEs (BDE 209) did not easily transpose within vegetable tissue. This finding agreed well with a previous study,

Fig. 2. Concentrations of HFRs in different vegetables.

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Fig. 3. Homologue compositions of HFRs in plant roots and shoots.

which found that lower brominated PBDEs such as BDEs 47, 66, and 99 were present in higher proportions in roots than in soils, while higher brominated PBDEs (with BDE 209 more apparent) were present in lower proportions in plant roots than in soils (Huang et al., 2011). In addition, air-leaf exchange of PBDEs would also contribute part of PBDEs, particularly lower brominated PBDEs, to the accumulation in shoots for field growing (Wang et al., 2015b). Hence, to some extent, the shoot PBDEs would be composed of PBDEs translocated from roots and deposited from atmosphere. For NBFRs, the proportion of DBDPE was higher than those of other compounds in shoot and root samples (except Chinese cabbage and shallot), with mean values of 52.7% and 38.2%, respectively. Higher proportions of TBPH and TBB were found in roots than in shoots. Meanwhile, TBE, TBB, and TBPH were found to be concentrated selectively in roots in comparison, with concentrations in the corresponding rhizospheric soil reported previously (Wang et al., 2016). It is clear that lower brominated flame retardants were prone to uptake by plant roots. In addition, profiles of PBDEs and NBFRs in cabbage varied greatly compared with other vegetation species, which could be attributed to the specific vegetation cultivar. For DPs, the fractions of anti-DP and syn-DP in total DPs were generally used when discussing the environmental transport and fate of these two structural isomers. In this study, the values of fanti (ratio of anti-DP to total DPs) ranged from 0.48 to 0.67 (mean ¼ 0.57) in shoots and 0.46 to 0.75 (mean ¼ 0.61) in roots (Table S1), lower than the values in a commercial DPs product (0.75e0.8) (Qiu et al., 2007), but higher than those reported in rhizosphere soils (ranging from 0.47 to 0.61, with an average of 0.53) (Wang et al., 2016). This was an indication that DPs in the study area may not originate from raw commercial DPs products,

and anti-DP and syn-DP underwent different environmental processes. In addition, anti-DP accumulated selectively in roots and shoots. Given the similar physicochemical properties of HFRs congeners, such as BDEs 99/100 and BDEs 153/154, comparison of these congeners in shoots and roots provides an opportunity to explore how bioprocessing affects the isomer distributions in vegetable tissues. As shown in Table S1, results revealed that BDEs 99/100 and 153/154 ratios in shoots were higher than those in roots, with mean values of 6.24 and 1.66 in shoots and 5.39 and 0.96 in roots, respectively. These results indicate that BDEs 99 and 153 were concentrated in shoots preferentially over their structural isomers. The probable explanations are as follows: first, BDEs 99/153 may be more prone to translocation from roots to shoots compared with BDEs 100/154 (Limmer and Burken, 2014). The octanol-water coefficient (log Kow) was used to evaluate the potential capacity of transposition of POPs within plant tissue, while chemicals with lower Kow were considered to be transferred within plant tissue; among these structural isomers, lower Kow values were observed in BDEs 99 (log Kow ¼ 7.12) and 153 (log Kow ¼ 7.48). One study reported that higher levels of BDE 99 were accumulated in zucchini compared with BDE 100 after 70 days of growth (Mueller et al., 2006), and BDE 99 accumulation in tobacco tissue was twofold greater than that of BDE 100 after 6 months of growth (Vrkoslavova et al., 2010). Meanwhile, higher abundance of BDE 153 was observed in plant samples in comparison with BDE 154 (Jin et al., 2008). Second, evaporation of these structural isomers from soil to air varied due to their different physiochemical properties, which may also alter the direct absorption rate from air by leaves. Numerous studies have demonstrated that concentrations of BDEs 99 and 153 in air and dust were higher than those of BDEs 100 and

S. Wang et al. / Environmental Pollution 214 (2016) 705e712

154, respectively (Deng et al., 2007; Zhang et al., 2009). Although studies have demonstrated that weathered POPs were taken up by plant roots in only limited quantities, the present data show that in situ POPs bioprocesses exist and are controlled by the physiochemical properties of the contaminated site. In addition, the pairwise occurrence of TBB and TBPH in commercial products provides an insight into their environmental fate under biological processes. Higher values of TBB/TBPH were found in shoots, with an average value of 3.67, while the average value in roots was 1.36. This discrepancy may be linked to their different usages and environmental fates. Different alternative formulations of TBB and TBPH were contained in Firemaster 550 (35% TBB, 15% TBPH) (Ma et al., 2012a) and Firemaster BZ-54 (70% TBB, 30% TBPH) (Ma et al., 2012b), and the complex usage profiles of these products altered their ratio in environmental matrices. TBPH (log Kow ¼ 10.1) was considered to be more persistent and accumulative than was TBB (log Kow ¼ 8.7) in the environment due to the higher octanolwater coefficient, which might influence plant uptake of these contaminants.

3.3. Root concentration factor (RCF) and log Kow To further demonstrate congener-specific uptake of HFRs by plant roots, the ratios of HFRs concentrations in roots to those in

709

soils were calculated and compared with log Kow values for HFRs. As expected, enrichment of HFRs was observed in rhizosphere soils, which were closely associated with plant uptake of HFRs. Hence, the RCF was calculated as the ratio of the concentration in roots to the concentration in rhizospheric soil (CR/CRS). The concentrations in rhizosphere soils were discussed in our previous study (Wang et al., 2016). In general, CR/CRS ratios varied greatly among vegetable varieties, with higher CR/CRS values observed in celery, cabbage, and sweet potato for HFRs congeners. This discrepancy may be attributed to the different rhizosphere effects associated with specific vegetable species on the distribution of chemicals in soils. In addition, the differentiation of abundance and diversity of rhizospheric microbes and root exudates trigged by different vegetable species could also be the reason (Wang et al., 2014b). Divergent conclusions were observed in previous studies conducted on rhizosphere POPs. For example, PCBs concentrations decreased with the distance to the root surface, while PAHs were reported to gather within the rhizosphere (Javorska et al., 2009; Liste and Alexander, 2000). Hence, bioavailable HFRs triggered by plant cultivation may be a pivotal controlling factor. Selective uptake of bioavailable HFRs by root, depending on the Kow of HFRs, could also be a factor. As shown in Fig. 4, CR/CRS values decreased with increasing Kow of HFRs congeners. This finding corresponded well with previous studies on higher brominated PBDEs, which

Fig. 4. Relationships between RCF and Kow of PBDEs and NBFRs.

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-1.0

Shoot

-1.5

1

Ln BDE183

-2.0

Ln BDE183

Root

2

-2.5 -3.0 -3.5

0 -1 -2

-4.0

-3

-4.5

-4

-5.0 -1.0

-5 -.5

0.0

.5

1.0

1.5

2.0

2.5

-1

0

1

Ln TBE

1.8

3

4

2

Shoot

1.6

2

Ln TBE

Root 1

Ln penta-BDE

Ln penta-BDE

1.4 1.2 1.0 .8 .6

0

-1

-2

.4 -3 .2 0.0

-4 -.5

0.0

.5

1.0

1.5

2.0

2.5

3.0

.5

3.5

1.0

Ln TBB/TBPH

1.5

2.0

2.5

3.0

3.5

Ln TBB/TBPH

4.5

3.5

Shoot

4.0

Root 3.0

Ln DBDPE

Ln DBDPE

3.5

3.0

2.5

2.5

2.0

2.0 1.5 1.5

1.0

1.0 0

1

2

3

Ln BDE209

4

5

6

-1

0

1

2

Ln BDE209

Fig. 5. Pairwise correlations of BDE183 vs. TBE, penta-BDEs vs. TBPH and TBB, and BDE209 vs. DBDPE.

3

4

5

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were found in higher concentrations in soils in comparison with lower brominated PBDEs (Huang et al., 2011; Wang et al., 2014a). It also has been demonstrated that root uptake of xenobiotics could be illustrated using a bell-shaped curve, while uptake and translocation within plant tissues weakened when Kow > 3 (Dettenmaier et al., 2008) (see Fig. 4). In addition, the linear fitting curve showed that PBDEs uptake by plant roots was more strongly dependent on log Kow than that of NBFRs (p ¼ 0.045 for PBDEs; p ¼ 0.157 for NBFRs), probably due to the potential differentiation of bioavailability between PBDEs and NBFRs in soil. The bioavailability of weathered organic compounds is generally thought to decline with residence time in the environment (Alexander, 2000). This trend of decreased availability with aging has been observed for PCBs, PAHs, and PBDEs (Carroll and Harkness, 1995; Hatzinger and Alexander, 1995). For instance, previous studies reported that aging of PBDEs may significantly diminish their bioavailability in soil, with a reduction ranging from 22 to 84% compared with freshly spiked soil (Liang et al., 2010). Thus, in the current study, the relatively long residence time of old flame retardants (PBDEs) could lead to strong absorption in soil organic matter, resulting in a reduction in their bioavailability. Subsequently, the effect of root excretion on desorption of these absorbed PBDEs may be stronger for lower brominated PBDEs (lower log Kow) in comparison with higher brominated PBDEs (higher log Kow). In contrast, NBFRs were not found to adhere tightly to soil organic carbon due to their relatively short service time (Wang et al., 2016). This means the bioavailability of NBFRs in the study region was higher than that of PBDEs, which was also found in the mean RCF values. Hence, it can be speculated that root uptake of NBFRs does not depend solely on log Kow but is also driven by their environmental abundance. Similar results have been demonstrated previously, showing that rhizosphere effects on chemical distribution patterns are more apparent in aged contaminated sites than newly contaminated areas (Wang et al., 2014b). 3.4. Substitutive characteristics between PBDEs and NBFRs in vegetables The discontinued and current flame retardants analysed in this survey provide a unique opportunity to identify how market shifts may have affected environmental concentrations and distribution of these chemicals within plant tissues, especially the e-waste disposal manners didn't change a lot in the present study area over the past decades. For instance, DBDPE was introduced to the market as a replacement for BDE 209 in anticipation of its eventual withdrawal (Covaci et al., 2011). Hypothetically, the concentrations of these two compounds should be negatively correlated, which means the concentration of BDE 209 would decrease with the increasing concentration of DBDPE in environmental matrices. However, it is the opposite of what was observed here. Significantly positive relationships between DBDPE and BDE 209 were observed in shoots (r ¼ 0.736, p ¼ 0.003), while no obvious relationship between DBDPE and BDE 209 was seen in roots (r ¼ 0.338, p ¼ 0.237) (Fig. 5). These results could be linked to the substantial residence time of BDE 209 in soil and the ongoing input of DBDPE in environment media, which resulted in the contemporary uptake of BDE209 and DBDPE by plant. As a replacement for BDE 183, TBE was significantly positively correlated with BDE 183 in roots (r ¼ 0.904, p ¼ 0.005), and no obvious correlation between TBE and BDE 183 in shoots was observed (r ¼
0.108, p ¼ 0.71) (Fig. 5). These differences could be attributed to the potential atmospheric deposition of these chemicals onto vegetable leaves, resulting in differentiation of accumulation in shoots. Similar positive correlations between TBE and BDE

711

183 were reported in a previous study, which focused on analysis of air and precipitation samples around the Great Lakes area, North America (Ma et al., 2013). Given that commercial penta-BDEs have been replaced by TBPH and TBB (Firemaster 550) in the market, it is necessary to look at the relationship between these compounds. A positive correlation between TBPH plus TBB and penta-BDEs (sum of BDE99 and BDE100) was observed in roots (p ¼ 0.04) (Fig. 5), which indicated that the replacement of commercial penta-BDEs mixtures by Firemaster 550 is not yet evident in this region. However, there was no visual relationship between TBPH/TBB and penta-BDEs in shoots; differences in physicochemical properties and sources controlling the environmental fate of different chemicals should be considered as likely causes, as discussed in section 3.2. Other factors that differ widely and potentially contribute to the variability and uncertainty in the uptake of organic chemicals by plants, such as the specific plant species, should also be taken into consideration. Generally, alternative characterizations between PBDEs and NBFRs are not yet evident in vegetable tissues, which lead to co-occurrence of PBDEs and NBFRs in e-waste presently. 4. Conclusions A relatively high abundance of HFRs was observed in vegetables. Lower brominated flame retardants, such as BDEs 28 and 47, preferentially accumulated in roots and then acropetally translocated to shoots, indicating a potential ecological risk in farmland around the e-waste recycling site. Relationships between RCF and log Kow indicated that selected bioaccumulations of HFRs in vegetation roots existed at the e-waste contaminated site. In addition, positive correlations were found between PBDEs and their replacements, which indicated that the replacement of commercial deca-BDE by DBDPE, octa-BDE by TBE, and penta-BDEs by TBB/TBPH is not yet evident in the research area. This study also furthered the understanding of root uptake of old and emerging flame retardants in the soil-vegetation system. Further research should focus on ecological risk assessment of HFRs. Acknowledgments This work was supported by the Joint Funds of the National Natural Science Foundation of China and the Natural Science Foundation of Guangdong Province, China (Nos. U1133004 and U1501234), and the National Natural Science Foundation of China (Nos. 41322008 and 21307133). Appendix A. Supplementary data Supplementary data related to this article can be found at http:// dx.doi.org/10.1016/j.envpol.2016.04.071. References Alexander, M., 2000. Aging, bioavailability, and overestimation of risk from environmental pollutants. Environ. Sci. Technol. 34, 4259e4265. Bi, X., Thomas, G.O., Jones, K.C., Qu, W., Sheng, G., Martin, F.L., Fu, J., 2007. Exposure of electronics dismantling workers to polybrominated diphenyl ethers, polychlorinated biphenyls, and organochlorine pesticides in South China. Environ. Sci. Technol. 41, 5647e5653. Carroll, K.M., Harkness, M.R., 1995. Application of permeant/polymer diffusional model to the desorption of polychlorinated biphenyls from Hudson River sediments. Reply to comments. Environ. Sci. Technol. 29, 285e285. Chen, S.-J., Tian, M., Wang, J., Shi, T., Luo, Y., Luo, X.-J., Mai, B.-X., 2011. Dechlorane Plus (DP) in air and plants at an electronic waste (e-waste) site in South China. Environ. Pollut. 159, 1290e1296. Covaci, A., Harrad, S., Abdallah, M.A.E., Ali, N., Law, R.J., Herzke, D., de Wit, C.A., 2011. Novel brominated flame retardants: a review of their analysis, environmental fate and behaviour. Environ. Int. 37, 532e556.

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