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Persistent organic pollutants (POPs) in oriental magpie-robins from e-waste, urban, and rural sites: Site-specific biomagnification of POPs
Ecotoxicology and Environmental Safety 186 (2019) 109758
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Persistent organic pollutants (POPs) in oriental magpie-robins from e-waste, urban, and rural sites: Site-specific biomagnification of POPs
T
Ling Moa,b, Xiaobo Zhengb,d,∗, Chunyou Zhub, Yuxin Sunc,∗∗, Lehuan Yue, Xiaojun Luob, Bixian Maib a
Hainan Research Academy of Environmental Sciences, Haikou, 510100, China Guangdong Provincial Key Laboratory of Environmental Protection and Resources Utilization and State Key Laboratory of Organic Geochemistry, Guangzhou Institute of Geochemistry, Chinese Academy of Sciences, Guangzhou, 510640, China c Key Laboratory of Tropical Marine Bio-resources and Ecology, Guangdong Provincial Key Laboratory of Applied Marine Biology, South China Sea Institute of Oceanology, Chinese Academy of Sciences, Guangzhou, 510301, China d College of Resources and Environment, South China Agricultural University, Guangzhou, 510642, China e School of Biology and Food Engineering, Guangdong University of Education, Guangzhou, 510303, China b
A R T I C LE I N FO
A B S T R A C T
Keywords: Persistent organic pollutants Birds E-waste site Biomagnification
Plenty of banned and emerging persistent organic pollutants (POPs), including dichlorodiphenyltrichloroethane and its metabolites (DDTs), polychlorinated biphenyls (PCBs), polybrominated diphenyl ethers (PBDEs), dechlorane plus (DP), and decabromodiphenyl ethane (DBDPE), were measured in oriental magpie-robins from an e-waste recycling site, an urban site (Guangzhou City), and a rural site in South China. Median concentrations of DDTs, PCBs, PBDEs, DP, and DBDPE ranged from 1,000–1,313, 800-59,368, 244-5,740, 24.1–127, and 14.7–36.0 ng/g lipid weight, respectively. Birds from the e-waste site had significantly higher concentrations of PCBs and PBDEs than those from urban and rural sites (p < 0.05), implying contamination of PCBs and PBDEs brought by e-waste recycling activities. DDTs were the predominant POPs in birds from urban and rural sites. The values of δ15N were significantly and positively correlated with concentrations of p,p′-DDE and low-halogenated chemicals in samples from the e-waste site (p < 0.05), indicating the trophic magnification of these chemicals in birds. However, concentrations of most POPs were not significantly correlated with the δ15N values in birds from urban and rural sites. PCBs and PBDEs in birds from urban and rural sites were not likely from local sources, and the biomagnification of POPs in different sites needed to be further investigated with caution.
1. Introduction Persistent organic pollutants (POPs) are persistent, bioaccumulative, and toxic chemicals. Many pesticides, such as dichlorodiphenyltrichloroethane (DDTs), and plastic additives, such as polychlorinated biphenyls (PCBs), and polybrominated diphenyl ethers (PBDEs) have been banned or restricted by the Stockholm Convention in the last few decades (UNEP, 2009; Stockholm, 2017). The abandon of PBDEs boosted the production and usage of emerging flame retardants (FRs), such as dechlorane plus (DP) and decabromodiphenyl ethane (DBDPE) (Covaci et al., 2011; Sverko et al., 2011). These emerging FRs have been ubiquitously detected in environmental samples (Covaci et al., 2011; Xian et al., 2011) and were considered as POPs-like chemicals, which posed ecological risks to the environment (Covaci et al.,
2011; Sverko et al., 2011; Xian et al., 2011). Meanwhile, the restricted chemicals, such as DDTs and PCBs, were consistent and frequently detected in organisms (Eens et al., 2013; Sun et al., 2014; Zheng et al., 2015), which still warrants attention. Birds have been widely used as bio-sentinels of environmental contaminants worldwide (Chen and Hale, 2010; Eens et al., 2013). Birds are sensitive to environmental changes, because birds have dietary diversity and occupy a top position in food webs. Blood concentrations of Hg and POPs negatively impacted long-term breeding probability, hatching and fledging probabilities of birds (Goutte et al., 2014). Numerous studies have focused on contamination of POPs in birds, in order to assess the occurrence and ecological risks of local contamination (Lam et al., 2008; Luo et al., 2009). The profiles and bioaccumulation of POPs in birds were highly variable in literature
∗
Corresponding author. Guangdong Provincial Key Laboratory of Environmental Protection and Resources Utilization and State Key Laboratory of Organic Geochemistry, Guangzhou Institute of Geochemistry, Chinese Academy of Sciences, Guangzhou, 510640, China. ∗∗ Corresponding author. E-mail addresses: [email protected] (X. Zheng), [email protected] (Y. Sun). https://doi.org/10.1016/j.ecoenv.2019.109758 Received 2 August 2019; Received in revised form 23 September 2019; Accepted 2 October 2019 0147-6513/ © 2019 Elsevier Inc. All rights reserved.
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2.2. Sample preparation and extraction
(Jaspers et al., 2006; Luo et al., 2009). Different biomagnification factors (BMF) were reported in predatory food chains (Voorspoels et al., 2007; Yu et al., 2013). In the study of Yu et al. (2013), a list of POPs, including PCBs, PBDEs, DP, and hexabromocyclododecane (HBCD) were biomagnified in terrestrial food chains. High contributions of lower brominated congeners were observed in eagle owl (Bubo bubo) and little owl (Athene noctua) while highly brominated congeners were more abundant in common kestrel (Falco tinnunculus) (Yu et al., 2013). The BMF values were generally higher in the rat-owl food chain than those in the sparrow-kestrel food chain (Yu et al., 2013). Tropical levels and in vivo metabolism were possible factors mediating the concentrations and profiles of POPs in birds (Voorspoels et al., 2007; Yu et al., 2013). In a previous study, insectivorous birds had generally higher concentrations of DDTs, PCBs, and PBDEs than those of granivorous birds (Mo et al., 2018). The higher trophic levels in insectivorous birds and the variable dietary sources in birds were suggested as possible reasons (Mo et al., 2018). No significant covariations were observed between POPs and δ15N in Scopoli's shearwater (Calonectris diomedea) from Mediterranean (Costantini et al., 2017). Variable levels of POPs in Scopoli's shearwater was attributed to foraging area rather than prey type (Costantini et al., 2017). Moreover, compositions of POPs varied in the same bird species from different sampling sites, which suggested that dietary sources also played a significant role in biomagnification of POPs in birds (Sun et al., 2012; Yu et al., 2014). In literature, birds were collected from different sampling sites, including heavy polluted sites like e-waste recycling sites (Luo et al., 2009; Mo et al., 2018), developed areas like cities (Sun et al., 2012), and rural areas like villages and forests (Dauwe et al., 2009; Lam et al., 2008). We assumed that the feeding behavior and dietary sources are different for even the same bird species in different sampling sites, which results in the different bioaccumulation profiles of POPs in birds. In addition, it is unclear if biomagnification of POPs is still consistent in the same bird species exposed to diverse sources of POPs, which is of vital importance in comparisons between literature and the ecological risk assessment of POPs. Due to the small territories and foraging areas of terrestrial passerine birds, passerine bird species are especially suited to monitor local contamination for POPs (Dauwe et al., 2009; Van den Steen et al., 2009). Oriental magpie-robin (Copsychus saularis, OMR) is a common terrestrial bird species in South China. Occurrence of several brominated flame retardants (BFRs) in OMRs from e-waste recycling sites has been reported in a previous study (Sun et al., 2012). In the present study, 32 OMRs from e-waste, urban, and rural sites from Guangdong Province, South China, were collected and analyzed for a wide suite of POPs, including DDTs, PCBs, PBDEs, and emerging flame retardants. The objectives of this study were to know profiles of POPs in OMRs from different sites, and to investigate if the biomagnification of POPs in OMRs differed locally.
The method used for sample extraction was described previously (Sun et al., 2012). Briefly, about 5 g wet weight of muscle tissue was freeze-dried, grounded into fine powder, and mixed with anhydrous sodium sulfate. Samples were spiked with mixture of surrogate standards (40 ng of BDEs 77, 181, and 205, and CBs 30, 65, and 204, 100 ng of 13C12-BDE 209) before Soxhlet extraction with 200 mL acetone/ hexane (v/v = 1:1) for 48 h. The extract was concentrated to 10 mL by a rotary evaporator. An aliquot was moved for gravimetric determination of lipid content in samples. The remaining extraction was purified by a gel permeation chromatography column packed with 40 g SX-3 BioBeads (Bio-Rad Laboratories, Inc. California, USA) to remove proteins and lipids. Eluate from 90 to 280 mL of dichloromethane/hexane (v/ v = 1:1) was collected and concentrated to 1 mL, then cleaned by a multilayer column packed with 8 cm neutral silica, 8 cm acidified silica, and 2 cm anhydrous sodium sulfate from bottom to top. Target chemicals were eluted with 30 mL hexane/dichloromethane (v/v = 1:1). The eluate was further concentrated to near dryness and reconstituted in 200 μL of isooctane. Known amounts (40 ng) of internal standards (BDEs 118 and 128, 4-F-BDE 67, 3-F-BDE 153, 13C12-PCB 141, CBs 24, 82, and 198) were spiked into samples before instrumental analysis. 2.3. Instrumental analysis Concentrations of PCBs (CBs 28/31, 52, 60, 66, 74, 99, 101, 105, 115/87, 118, 123, 128, 130, 137, 138, 146, 149/139, 153, 156, 157, 158, 164/163, 169, 171, 172, 175, 180, 183, 187, 190, 191, 194, 195, 203, 205, 206, and 209), DDTs (p,p′-DDT and o,p′-DDT) and metabolites of DDTs (p,p′-DDD, p,p′-DDE, p,p′-DDM, p,p′-DDMU, o,p′-DDE, and o,p′-DDD) were measured with an Agilent 7890 gas chromatography (GC) equipped with an Agilent 5975 mass spectrometer (MS) in the selective ion-monitoring (SIM) mode. Separation of PCBs and DDTs was performed by a DB-5MS capillary column (60 m × 0.25 mm × 0.25 μm, J&W Scientific, USA). BDEs 28, 47, 66, 100, 99, 85, 154, 153, and 183, and anti- and syn-DP were analyzed by an Agilent 6890 GC connected with an Agilent 5975 MS using electron capture negative ionization (ECNI) in the SIM mode. A DB-XLB column (30 m × 0.25 mm × 0.25 μm, J&W Scientific, USA) was used for separation. BDEs 202, 197, 203, 196, 208, 207, 206, and 209, and DBDPE were quantified by a Shimadzu model 2010 GC coupled with a model QP 2010 MS (Shimadzu, Japan) and separated by a DB-5HT column (15 m × 0.25 mm × 0.10 μm, J&W Scientific, USA). Details on the GC conditions and monitored ions can be found elsewhere (Luo et al., 2009). 2.4. Quality assurance and quality control
2. Materials and methods
One procedural blank was performed in each batch of sample analysis. Trace amounts of BDE 153 were detected in the procedural blanks (n = 3) and subtracted from the sample concentrations. Recoveries of target chemicals were evaluated by spiking mixtures of PCBs, PBDEs, and DBDPE in matrices and solutions, which were analyzed the same with other samples. The average recoveries of target chemicals in the spiked blanks (n = 3) and matrices (n = 3) ranged from 98% to 116% and 70%–130%, respectively. The relative standard deviations (RSD) of all target compounds in the spiked blanks and matrices were less than 18%. The average recoveries of surrogate standards in all samples (n = 32) ranged between 89 ± 12% to 108 ± 16%. Concentrations of POPs were not corrected by surrogate recoveries. For BDE 153, method detection limit (MDL) was defined as three times the standard deviation of the procedural blanks. For undetected compounds in procedural blanks, MDLs were set as a signal of five times the noise level. MDLs for DDTs, PCBs, PBDEs, and DP ranged from 0.0073 to 0.22 ng/g lw (lipid weight). MDL for DBDPE was 0.56 ng/g lw.
2.1. Sample collection Thirty-two oriental magpie-robins (OMRs) were collected in March and November 2011 from three sampling sites in Guangdong Province, South China. The e-waste site is located in the rural area of Qingyuan (Fig. 1), where about 700,000 t e-wastes were processed each year within an area of 330 km2 using primitive techniques such as manual disassembly, acid dipping and open incineration. The urban site is situated in Guangzhou, a highly industrialized megacity. The rural site is located in an agricultural region of Zhaoqing City, with no e-waste recycling or industrial activities. The details of avian sampling method were described in Zhang et al. (2011a). Birds were immediately transported to the laboratory and euthanized with N2. Pectoral muscles were excised from each bird and stored at −20 °C until chemical analysis. 2
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Fig. 1. Map of sampling sites.
2.5. Statistical analysis
Table 1 Mean, median, and range concentrations of POPs (ng/g lw for all chemicals) in oriental magpie-robins from the e-waste, urban and rural sites, South China.
All concentration data were presented on a lipid weight basis. Statistical analysis was performed with SPSS 16.0 (SPSS Inc., Illinois, USA). The level of significance was set at p < 0.05. The raw concentration data and log-transformed data of POPs were tested to know if the data were normally distributed. The log-transformed concentrations of total DDTs, PCBs, and PBDEs were normal distributed, and one-way ANOVA was used to assess differences in concentrations of total DDTs, PCBs, and PBDEs among the three sampling sites. Spearman correlation analysis with the Least Significant Difference (LSD) test was used to assess correlations between individual POPs in birds.
N Lipid (%) ΣPCBsb ΣDDTsc ΣPBDEsd DBDPE ΣDPsf
3. Results and discussion
fanti
3.1. Concentrations of POPs
Anti-Cl11-DP
Concentrations of POPs in OMR samples from the e-waste, urban, and rural sites are summarized in Table 1. Median concentrations of ΣDDTs had a decreasing order of rural (1,313 ng/g lw) > urban (1,075 ng/g lw) > e-waste site (1,000 ng/g lw) (Table 1). However, no significant differences in concentrations of ΣDDTs were observed among the three sampling sites (p > 0.05). Sum PCB concentrations ranged from 446 ng/g lw at the urban site to 248,097 ng/g lw at the ewaste site. Levels of ΣPCBs in birds from the e-waste site were significantly higher than those from the urban and rural sites (p < 0.01), but concentrations of ΣPCBs did not differ significantly between the urban and rural sites (p > 0.05). The geographical distribution of concentrations of ΣPBDEs decreased in the order of e-waste site (5,740 ng/g lw) > urban (843 ng/g lw) > rural (244 ng/g lw) (Table 1). Birds from the urban site had significantly higher
Syn-Cl11-DP
a
Mean/Median Range Mean/Median Range Mean/Median Range Mean/Median Range Mean/Median Range Mean/Median Range Mean/Median Range Mean/Median Range
E-waste site
Urban site
Rural site
17 2.97 ± 0.25a 78,315/59,368 6,087–248,097 1,768/1,000 239-7,910 6,221/5,740 872-15,341 36.2/26.0 nd e −149 254/127 39.0–928 0.79/0.78 0.73–0.90 4.48/3.10 nd-13.0 1.11/nd nd-6.90
5 2.92 ± 0.60 873/800 446-1,518 2,487/1,075 224-7,667 1194/843 293-2,550 40.3/36.0 13–92 98.0/98.0 54.0–134 0.70/0.68 0.67–0.76 0.57/0.42 0.14–1.20 0.09/nd nd-0.34
10 2.81 ± 0.19 973/1,078 459-1,313 152,2/1,313 406-2,710 263/244 130–540 15.5/14.7 5.3–27.2 33.6/24.1 8.40–90.1 0.74/0.75 0.65–0.78 0.33/0.26 nd-1.40 0.05/nd nd-0.26
Mean ± SE. Sum of CBs 28/31, 52, 60, 66, 74, 99, 101, 105, 115/87, 118, 123, 128, 130, 137, 138, 146, 149/139, 153, 156, 157, 158, 164/163, 169, 171, 172, 175, 180, 183, 187, 190, 191, 194, 195, 203, 205, 206 and 209. c Sum of p,p′-DDT, o,p′-DDT, p,p′-DDD, p,p′-DDE, p,p′-DDM, p,p′-DDMU, o,p′DDE and o,p′-DDD. d Sum of BDEs 28, 47, 66, 100, 99, 85, 154, 153, 183, 202, 197, 203, 196, 208, 207, 206 and 209. e Not detected. f Sum of anti-DP and syn-DP. b
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concentrations of ΣPBDEs than those from the rural site (p < 0.01). DBDPE was detected in all the birds except one sample at the ewaste site with concentrations ranging from non detectable (nd) to 149 ng/g lw (Table 1). Levels of DBDPE in birds from the rural sites were significantly lower than those from the e-waste (p < 0.05) and urban sites (p < 0.05). DP (anti-DP and syn-DP) was detected in all the birds with concentrations ranging from 8.4 to 928 ng/g lw. Similar to DBDPE, levels of ΣDPs in birds from the rural sites were significantly lower than those from the e-waste (p < 0.01) and urban sites (p < 0.01). Concentrations of PCBs and PBDEs in birds from the e-waste site were generally higher than those from urban and rural sites, which highlighted the pollution of organic contaminants in e-waste recycling activities. Extremely higher concentrations of ΣPCBs and ΣPBDEs were also observed in birds, fish, soil, plant, and air from the same e-waste sampling site (Chen et al., 2014; Luo et al., 2009; Zhang et al., 2011b, 2011c; Zhang et al., 2012). Moreover, higher concentrations of PCBs and PBDEs were often found at other e-waste dismantling sites in China (Leung et al., 2011) and Vietnam (Tue et al., 2013). Concentrations of PBDEs and DBDPE were similar in OMRs collected in 2009 (Sun et al., 2012) and in 2011 (the current study) from the same sampling site. This indicates that primitive e-waste dismantling activities were still significant emission sources of PBDEs and emerging FRs in the study area. Meanwhile, birds from urban site had significantly higher levels of FRs than those in birds from rural sites. The elevated pollution status of FRs in birds from urban site was attributed to the large quantity of commercial products in cities. DDT concentrations were similar in birds from different sampling sites, implying the similar retrospective pollution of DDTs in these regions.
94.7 ± 2.75%, and 94.5 ± 1.20% to total DDTs in birds from e-waste, urban, and rural sites, respectively (Fig. S1, Supplementary Materials). The results confirmed that there was no recent input of DDTs in the sampling regions. The predominant PCB congeners were CBs 138 (contributions: 10.4–17.6%), 153 (12.6–24.2%), and 180 (5.95–8.00%) in birds from all sampling sites (Fig. 3). PBDE congener patterns exhibited complex features (Fig. 4). BDEs 99, 153, and 209 were the main congeners of PBDEs. BDE 153 (23.8%) dominated in PBDEs in birds from e-waste site, followed by BDEs 183 (17.0%) and 99 (13.8%). BDEs 209 (18.6%), 153 (17.3%), and 207 (10.6%) were the most abundant PBDE congeners in birds from the urban site. BDEs 153 (19.4%), 209 (13.9%), and 47 (11.8%) were main PBDE congeners in birds from the rural site. BDEs 99 and 183 took significant fractions in PBDEs in birds from e-waste site. The e-waste dismantling of obsolete electronic products could introduce large quantities of Penta-BDE and Octa-BDE mixtures into environment, which contained abundant BDEs 99 and 153, respectively. In urban and rural sites, Deca-BDE mixtures were more likely used in commercial products, as Penta-BDE and Octa-BDE mixtures were banned since 2009 (UNEP, 2009). The fanti values (ratios of concentrations of anti-DP divided by sum concentrations of anti-DP and syn-DP) were 0.79 ± 0.06, 0.70 ± 0.04, and 0.74 ± 0.04 in birds from e-waste, urban, and rural sites, respectively. The fanti values in birds from e-waste site were significantly higher than those from urban and rural sites (p < 0.01), which suggest site-specific bioaccumulation of DP isomers in the orientated magpie-robins. Overall, local sources of POPs seemed to significantly influence the profiles of POPs in birds. 3.3. Influence of trophic levels on bioaccumulation of POPs Stable nitrogen isotope ratio could provide independent measurement of trophic level in wildlife (Jardine et al., 2006). The δ15N values ranged from 4.06‰ to 10.7‰, 4.40–7.39‰, and 4.66–11.8‰ in OMRs from e-waste, urban, and rural sites, respectively, indicating the large variability in food items of oriental magpie-robins. In order to access the influence of tropic level on the contaminant levels, we performed correlation analysis between δ15N values and concentrations of the main POPs (all PBDE congeners, seven indicator PCBs, p,p′-DDE, DP, and DBDPE) in birds from different sampling sites (Tables S1–S3, Supplementary Materials). The δ15N values were significantly correlated with concentrations of most chemicals except CBs 52 and 101, and some BFRs with high octanol-water partition coefficient (Kow), including BDEs 196, 206, 207, 208, and 209, and DBDPE in OMRs from the e-waste site. The results indicate the biomagnification of most contaminants except the highly lipophilic BFRs in OMRs. In urban site, the δ15N values were only significantly correlated with the concentrations of BDEs 47, 99, 100, 196, and 203 in birds (p < 0.05). In rural site, the δ15N values were significantly correlated with the concentrations of BDEs 197 and 207, CBs 28, 52, 101, and 118 in birds (p < 0.05). Tropic level was not the main factor which determined the concentrations of POPs in urban and rural sites. High-brominated PBDEs and DBDPE have relatively high molecular weight, which could restrict the bioavailability of these chemicals in bird guts. However, the hexa- and hepta-BDEs, p,p′-DDE, and CBs 138, 153, and 180 were also not biomagnified in samples from urban and rural sites. BDEs 153, 154, and 183 have been proven to be the most bioaccumulative PBDE congeners in terrestrial food chains (Voorspoels et al., 2007; Yu et al., 2011, 2013). The possible reason might be that levels of hexa- and hepta-BDEs and PCBs were relatively low in dietary sources of birds from urban and rural sites. OMR samples were collected in two seasons (March and November) in the present study. OMRs are opportunistic predators of plants, fruits, insects, and other invertebrates. Diet compositions of birds were always different in different seasons (US EPA, 1993). So it is difficult to figure out the diet items for OMRs and bioavailability of POPs in diet items. OMRs in cities may also ingest more human-related diets, such as discarded human food and other garbage, than rural sites. It is also possible that biomagnification profile
3.2. Compositions of POPs Distinct composition patterns of POPs were found among the sampling sites (Fig. 2). PCBs (85.7%) were the predominant contaminants in birds at the e-waste site, followed by PBDEs (9.52%), DDTs (2.93%), DP (0.51%), and DBDPE (0.12%), but the predominant pollutants were DDTs in samples from the urban (42.1) and rural (52.1%) sites. Contributions of PCBs to POPs in birds from the e-waste site (85.7%) were significantly higher than those from the urban (26.1%) and rural (35.9%) sites. The high abundance of PCBs in birds was inevitably derived from the local primitive recycling of e-wastes. Birds from the urban site had higher proportions of halogenated flame retardants (PBDEs, DBDPE, and DPs) compared to those from the e-waste and rural sites. The great usage amount of commercial products in Guangzhou City could be the reason for the higher abundance of halogenated FRs. Compositions of DDTs and PCBs were similar in birds. DDTs were dominated by p,p′-DDE, which contributed 91.5 ± 1.19%,
Fig. 2. Contamination profiles of POPs in OMRs from the e-waste, urban and rural sites, South China. 4
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Fig. 3. PCB homologue profiles in OMRs from different sampling sites.
Fig. 4. PBDE congener profiles in OMRs from different sampling sites.
et al. (2015). The results indicate that the biomagnification of POPs in OMRs were highly variable, which might be affected by the pollution status of POPs in the dietary sources and dietary compositions in the habitats of OMRs. The biomagnification potential of POPs needs to be interpreted with caution in terrestrial avian food chains. Concentrations of most BFRs were significantly and positively correlated in samples of three bird species from the e-waste and rural site (Sun et al., 2012), which was inconsistent with the results in the present study. In OMRs from the e-waste site, two clusters of chemicals were identified (Tables S1–S3, Supplementary Materials). The first cluster included tetra-to octa-BDEs, PCBs, and p,p′-DDE. These chemicals can
of POPs in birds was determined by hepatic metabolism or excretion processes (Van den Steen et al., 2007), in addition to bioavailability of POPs in bird diets from these sites. In order to explore the biomagnification patterns of DP isomers, the correlations between fanti values and δ15N values were also examined. No significant relationship was observed in data from the e-waste, urban, and rural sites, separately, which was different with the results in previous studies (Chen et al., 2013; Mo et al., 2013; Peng et al., 2015). The carnivorous and piscivorous birds were investigated in Chen et al. (2013) and Mo et al. (2013), respectively. Three insectivorous birds and four omnivorous birds were collected in the study of Peng
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be considered as biomagnified POPs, as concentrations of them were significantly correlated with δ15N values. The other cluster of chemicals were non-biomagnified POPs, whose concentrations were not correlated with δ15N values. In OMRs from the urban site, concentrations of biomagnified POPs, including BDEs 47, 99, 100, 196, and 203 were significantly correlated, while concentrations of non-biomagnified POPs, including most hexa-to deca-BDEs, CBs 138, 153, and 180, and p,p′-DDE were significantly correlated (p < 0.05). The correlations were more complex in the rural site. Three clusters were observed: the first cluster included BDEs 47 and 100, CBs 138 and 153; the second cluster included BDEs 183, 202, 197, and 203; the third cluster included BDE 209 and CBs 28, 52, 101, 118, and 138. The three clusters had different log Kow or log octanol-air partition coefficient (Koa) except BDE 209. Chemicals in three clusters had log Kow between 6.57 -8.01, 8.38-8.99, and 5.62-6.87, or log KOA between 10.1-10.82, 12.52-13.38, and 8.29-10.51, respectively. POPs in rural site were likely from the transport of contaminants from other areas. Chemicals with different log KOA had different long-range transport capacities, which would result in the similar bioaccumulation profiles of POPs with similar log KOA values in birds.
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Brominated flame retardants and organochlorines in the European environment using great tit eggs as a biomonitoring tool. Environ. Int. 148, 648–653. Van den Steen, E., Pinxten, R., Jaspers, V.L.B., Covaci, A., Barba, E., Carere, C., Cichoń, M., Dubiec, A., Eeva, Tapio, Heeb, P., Kempenaers, B., Lifjeld, J.T., Lubjuhn, T., Mänd, R., Massa, B., Nilsson, J.Å., Norte, A., 2009. Brominated flame retardants and organochlorines in the European environmentusing great tit eggs as a biomonitoring tool. Environ. Int. 35, 310–317. Voorspoels, S., Covaci, A., Jaspers, V.L.B., Neels, H., Schepens, P., 2007. Biomagnification of PBDEs in three small terrestrial food chains. Environ. Sci. Technol. 41, 411–416. Xian, Q., Siddique, S., Li, T., Feng, Y.l., Takser, L., Zhu, J., 2011. Sources and environmental behavior of dechlorane plus - a review. Environ. Int. 37, 1273–1284. Yu, L.H., Luo, X.J., Wu, J.P., Liu, L.Y., Song, J., Sun, Q.H., Zhang, X.L., Chen, D., Mai, B.X., 2011. Biomagnification of higher brominated PBDE congeners in an urban terrestrial food web in North China based on field observation of prey deliveries. Environ. Sci. Technol. 45, 5125–5131. Yu, L.H., Luo, X.J., Zheng, X.B., Zeng, Y.H., Chen, D., Wu, J.P., Mai, B.X., 2013. Occurrence and biomagnification of organohalogen pollutants in two terrestrial predatory food chains. Chemosphere 93, 506–511. Yu, L.H., Luo, X.J., Liu, H.Y., Zeng, Y.H., Zheng, X.B., Wu, J.P., Yu, Y.J., Mai, B.X., 2014. Organohalogen contamination in passerine birds from three metropolises in China: geographical variation and its implication for anthropogenic effects on urban
4. Conclusions Occurrence and profiles of DDTs, PCBs, PBDEs, DP, and DBDPE were assessed in OMRs from e-waste, urban, and rural sites. The elevated concentrations of PCBs and PBDEs in birds highlighted the heavy contamination of POPs in e-waste sites. In birds from the e-waste site, trophic biomagnification were observed for POPs except for high-brominated chemicals, which could be attributed to the low bioavailability of highly lipophilic chemicals. In contrast, most of POPs were not biomagnified in OMRs from the urban and rural sites. The results indicate that the biomagnificantion of POPs in OMRs was not consistent in different sites, which could be affected by bioavailability of POPs in diverse diet sources of birds in local environment. Acknowledgements This study was financially supported by the National Natural Science Foundation of China (Nos. 41603085, 41877361, 41573084 and 41931290), Talent Support Project of Guangdong Province, China (No. 201629019), Guangdong Foundation for Program of Science and Technology Research (Nos. 2017B030314052 and 2017B030314057), Pearl River S&T Nova Program of Guangzhou (Nos. 201806010079 and 201806010185), and Guangzhou Science and Technology Program (No. 201707020033). Appendix A. Supplementary data Supplementary data to this article can be found online at https:// doi.org/10.1016/j.ecoenv.2019.109758. References Chen, D., Hale, R.C., 2010. A global review of polybrominated diphenyl ether flame retardant contamination in birds. Environ. Int. 36, 800–811. Chen, D., Wang, Y., Yu, L., Luo, X., Mai, B., Li, S., 2013. Dechlorane Plus flame retardant in terrestrial raptors from northern China. Environ. Pollut. 176, 80–86. Chen, S.J., Tian, M., Zheng, J., Zhu, Z.C., Luo, Y., Luo, X.J., Mai, B.X., 2014. Elevated levels of polychlorinated biphenyls in plants, air, and soils at an E-waste site in southern China and enantioselective biotransformation of chiral PCBs in plants. Environ. Sci. Technol. 48, 3847–3855. Costantini, L., Sebastiano, M., Müller, M.S., Eulaers, I., Ambus, P., Malarvannan, G., Covaci, A., Massa, B., Dell'Omo, G., 2017. Individual variation of persistent organic pollutants in relation to stable isotope ratios, sex, reproductive phase and oxidative status in Scopoli's shearwaters (Calonectris diomedea) from the Southern Mediterranean. Sci. Total Environ. 598, 179–187. Covaci, A., Harrad, S., Abdallah, M.A., 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, 532–556.
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biphenyls and organochlorine pesticides in birds from a contaminated region in South China: association with trophic level, tissue distribution and risk assessment. Environ. Sci. Pollut. Res. 18, 556–565. Zhang, K., Schnoor, J.L., Zeng, E.Y., 2012. E-waste recycling: where does it go from here? Environ. Sci. Technol. 46, 10861–10867. Zheng, X.B., Luo, X.J., Zeng, Y.H., Wu, J.P., Mai, B.X., 2015. Chiral polychlorinated biphenyls (PCBs) in bioaccumulation, maternal transfer, and embryo development of chicken. Environ. Sci. Technol. 49, 785–791.
environments. Environ. Pollut. 188, 118–123. Zhang, Q., Han, R.C., Zou, F.S., 2011a. Effects of artificial afforestation and successional stage on a low land forest bird community in southern China. For. Ecol. Manag. 261, 1738–1749. Zhang, X.L., Luo, X.J., Liu, H.Y., Yu, L.H., Chen, S.J., Mai, B.X., 2011b. Bioaccumulation of several brominated flame retardants and dechlorane plus in waterbirds from an ewaste recycling region in South China: associated with trophic level and diet sources. Environ. Sci. Technol. 45, 400–405. Zhang, X.L., Luo, X.J., Liu, J., Luo, Y., Chen, S.J., Mai, B.X., 2011c. Polychlorinated
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Persistent organic pollutants (POPs) in oriental magpie-robins from e-waste, urban, and rural sites: Site-specific biomagnification of POPs
T
Ling Moa,b, Xiaobo Zhengb,d,∗, Chunyou Zhub, Yuxin Sunc,∗∗, Lehuan Yue, Xiaojun Luob, Bixian Maib a
Hainan Research Academy of Environmental Sciences, Haikou, 510100, China Guangdong Provincial Key Laboratory of Environmental Protection and Resources Utilization and State Key Laboratory of Organic Geochemistry, Guangzhou Institute of Geochemistry, Chinese Academy of Sciences, Guangzhou, 510640, China c Key Laboratory of Tropical Marine Bio-resources and Ecology, Guangdong Provincial Key Laboratory of Applied Marine Biology, South China Sea Institute of Oceanology, Chinese Academy of Sciences, Guangzhou, 510301, China d College of Resources and Environment, South China Agricultural University, Guangzhou, 510642, China e School of Biology and Food Engineering, Guangdong University of Education, Guangzhou, 510303, China b
A R T I C LE I N FO
A B S T R A C T
Keywords: Persistent organic pollutants Birds E-waste site Biomagnification
Plenty of banned and emerging persistent organic pollutants (POPs), including dichlorodiphenyltrichloroethane and its metabolites (DDTs), polychlorinated biphenyls (PCBs), polybrominated diphenyl ethers (PBDEs), dechlorane plus (DP), and decabromodiphenyl ethane (DBDPE), were measured in oriental magpie-robins from an e-waste recycling site, an urban site (Guangzhou City), and a rural site in South China. Median concentrations of DDTs, PCBs, PBDEs, DP, and DBDPE ranged from 1,000–1,313, 800-59,368, 244-5,740, 24.1–127, and 14.7–36.0 ng/g lipid weight, respectively. Birds from the e-waste site had significantly higher concentrations of PCBs and PBDEs than those from urban and rural sites (p < 0.05), implying contamination of PCBs and PBDEs brought by e-waste recycling activities. DDTs were the predominant POPs in birds from urban and rural sites. The values of δ15N were significantly and positively correlated with concentrations of p,p′-DDE and low-halogenated chemicals in samples from the e-waste site (p < 0.05), indicating the trophic magnification of these chemicals in birds. However, concentrations of most POPs were not significantly correlated with the δ15N values in birds from urban and rural sites. PCBs and PBDEs in birds from urban and rural sites were not likely from local sources, and the biomagnification of POPs in different sites needed to be further investigated with caution.
1. Introduction Persistent organic pollutants (POPs) are persistent, bioaccumulative, and toxic chemicals. Many pesticides, such as dichlorodiphenyltrichloroethane (DDTs), and plastic additives, such as polychlorinated biphenyls (PCBs), and polybrominated diphenyl ethers (PBDEs) have been banned or restricted by the Stockholm Convention in the last few decades (UNEP, 2009; Stockholm, 2017). The abandon of PBDEs boosted the production and usage of emerging flame retardants (FRs), such as dechlorane plus (DP) and decabromodiphenyl ethane (DBDPE) (Covaci et al., 2011; Sverko et al., 2011). These emerging FRs have been ubiquitously detected in environmental samples (Covaci et al., 2011; Xian et al., 2011) and were considered as POPs-like chemicals, which posed ecological risks to the environment (Covaci et al.,
2011; Sverko et al., 2011; Xian et al., 2011). Meanwhile, the restricted chemicals, such as DDTs and PCBs, were consistent and frequently detected in organisms (Eens et al., 2013; Sun et al., 2014; Zheng et al., 2015), which still warrants attention. Birds have been widely used as bio-sentinels of environmental contaminants worldwide (Chen and Hale, 2010; Eens et al., 2013). Birds are sensitive to environmental changes, because birds have dietary diversity and occupy a top position in food webs. Blood concentrations of Hg and POPs negatively impacted long-term breeding probability, hatching and fledging probabilities of birds (Goutte et al., 2014). Numerous studies have focused on contamination of POPs in birds, in order to assess the occurrence and ecological risks of local contamination (Lam et al., 2008; Luo et al., 2009). The profiles and bioaccumulation of POPs in birds were highly variable in literature
∗
Corresponding author. Guangdong Provincial Key Laboratory of Environmental Protection and Resources Utilization and State Key Laboratory of Organic Geochemistry, Guangzhou Institute of Geochemistry, Chinese Academy of Sciences, Guangzhou, 510640, China. ∗∗ Corresponding author. E-mail addresses: [email protected] (X. Zheng), [email protected] (Y. Sun). https://doi.org/10.1016/j.ecoenv.2019.109758 Received 2 August 2019; Received in revised form 23 September 2019; Accepted 2 October 2019 0147-6513/ © 2019 Elsevier Inc. All rights reserved.
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2.2. Sample preparation and extraction
(Jaspers et al., 2006; Luo et al., 2009). Different biomagnification factors (BMF) were reported in predatory food chains (Voorspoels et al., 2007; Yu et al., 2013). In the study of Yu et al. (2013), a list of POPs, including PCBs, PBDEs, DP, and hexabromocyclododecane (HBCD) were biomagnified in terrestrial food chains. High contributions of lower brominated congeners were observed in eagle owl (Bubo bubo) and little owl (Athene noctua) while highly brominated congeners were more abundant in common kestrel (Falco tinnunculus) (Yu et al., 2013). The BMF values were generally higher in the rat-owl food chain than those in the sparrow-kestrel food chain (Yu et al., 2013). Tropical levels and in vivo metabolism were possible factors mediating the concentrations and profiles of POPs in birds (Voorspoels et al., 2007; Yu et al., 2013). In a previous study, insectivorous birds had generally higher concentrations of DDTs, PCBs, and PBDEs than those of granivorous birds (Mo et al., 2018). The higher trophic levels in insectivorous birds and the variable dietary sources in birds were suggested as possible reasons (Mo et al., 2018). No significant covariations were observed between POPs and δ15N in Scopoli's shearwater (Calonectris diomedea) from Mediterranean (Costantini et al., 2017). Variable levels of POPs in Scopoli's shearwater was attributed to foraging area rather than prey type (Costantini et al., 2017). Moreover, compositions of POPs varied in the same bird species from different sampling sites, which suggested that dietary sources also played a significant role in biomagnification of POPs in birds (Sun et al., 2012; Yu et al., 2014). In literature, birds were collected from different sampling sites, including heavy polluted sites like e-waste recycling sites (Luo et al., 2009; Mo et al., 2018), developed areas like cities (Sun et al., 2012), and rural areas like villages and forests (Dauwe et al., 2009; Lam et al., 2008). We assumed that the feeding behavior and dietary sources are different for even the same bird species in different sampling sites, which results in the different bioaccumulation profiles of POPs in birds. In addition, it is unclear if biomagnification of POPs is still consistent in the same bird species exposed to diverse sources of POPs, which is of vital importance in comparisons between literature and the ecological risk assessment of POPs. Due to the small territories and foraging areas of terrestrial passerine birds, passerine bird species are especially suited to monitor local contamination for POPs (Dauwe et al., 2009; Van den Steen et al., 2009). Oriental magpie-robin (Copsychus saularis, OMR) is a common terrestrial bird species in South China. Occurrence of several brominated flame retardants (BFRs) in OMRs from e-waste recycling sites has been reported in a previous study (Sun et al., 2012). In the present study, 32 OMRs from e-waste, urban, and rural sites from Guangdong Province, South China, were collected and analyzed for a wide suite of POPs, including DDTs, PCBs, PBDEs, and emerging flame retardants. The objectives of this study were to know profiles of POPs in OMRs from different sites, and to investigate if the biomagnification of POPs in OMRs differed locally.
The method used for sample extraction was described previously (Sun et al., 2012). Briefly, about 5 g wet weight of muscle tissue was freeze-dried, grounded into fine powder, and mixed with anhydrous sodium sulfate. Samples were spiked with mixture of surrogate standards (40 ng of BDEs 77, 181, and 205, and CBs 30, 65, and 204, 100 ng of 13C12-BDE 209) before Soxhlet extraction with 200 mL acetone/ hexane (v/v = 1:1) for 48 h. The extract was concentrated to 10 mL by a rotary evaporator. An aliquot was moved for gravimetric determination of lipid content in samples. The remaining extraction was purified by a gel permeation chromatography column packed with 40 g SX-3 BioBeads (Bio-Rad Laboratories, Inc. California, USA) to remove proteins and lipids. Eluate from 90 to 280 mL of dichloromethane/hexane (v/ v = 1:1) was collected and concentrated to 1 mL, then cleaned by a multilayer column packed with 8 cm neutral silica, 8 cm acidified silica, and 2 cm anhydrous sodium sulfate from bottom to top. Target chemicals were eluted with 30 mL hexane/dichloromethane (v/v = 1:1). The eluate was further concentrated to near dryness and reconstituted in 200 μL of isooctane. Known amounts (40 ng) of internal standards (BDEs 118 and 128, 4-F-BDE 67, 3-F-BDE 153, 13C12-PCB 141, CBs 24, 82, and 198) were spiked into samples before instrumental analysis. 2.3. Instrumental analysis Concentrations of PCBs (CBs 28/31, 52, 60, 66, 74, 99, 101, 105, 115/87, 118, 123, 128, 130, 137, 138, 146, 149/139, 153, 156, 157, 158, 164/163, 169, 171, 172, 175, 180, 183, 187, 190, 191, 194, 195, 203, 205, 206, and 209), DDTs (p,p′-DDT and o,p′-DDT) and metabolites of DDTs (p,p′-DDD, p,p′-DDE, p,p′-DDM, p,p′-DDMU, o,p′-DDE, and o,p′-DDD) were measured with an Agilent 7890 gas chromatography (GC) equipped with an Agilent 5975 mass spectrometer (MS) in the selective ion-monitoring (SIM) mode. Separation of PCBs and DDTs was performed by a DB-5MS capillary column (60 m × 0.25 mm × 0.25 μm, J&W Scientific, USA). BDEs 28, 47, 66, 100, 99, 85, 154, 153, and 183, and anti- and syn-DP were analyzed by an Agilent 6890 GC connected with an Agilent 5975 MS using electron capture negative ionization (ECNI) in the SIM mode. A DB-XLB column (30 m × 0.25 mm × 0.25 μm, J&W Scientific, USA) was used for separation. BDEs 202, 197, 203, 196, 208, 207, 206, and 209, and DBDPE were quantified by a Shimadzu model 2010 GC coupled with a model QP 2010 MS (Shimadzu, Japan) and separated by a DB-5HT column (15 m × 0.25 mm × 0.10 μm, J&W Scientific, USA). Details on the GC conditions and monitored ions can be found elsewhere (Luo et al., 2009). 2.4. Quality assurance and quality control
2. Materials and methods
One procedural blank was performed in each batch of sample analysis. Trace amounts of BDE 153 were detected in the procedural blanks (n = 3) and subtracted from the sample concentrations. Recoveries of target chemicals were evaluated by spiking mixtures of PCBs, PBDEs, and DBDPE in matrices and solutions, which were analyzed the same with other samples. The average recoveries of target chemicals in the spiked blanks (n = 3) and matrices (n = 3) ranged from 98% to 116% and 70%–130%, respectively. The relative standard deviations (RSD) of all target compounds in the spiked blanks and matrices were less than 18%. The average recoveries of surrogate standards in all samples (n = 32) ranged between 89 ± 12% to 108 ± 16%. Concentrations of POPs were not corrected by surrogate recoveries. For BDE 153, method detection limit (MDL) was defined as three times the standard deviation of the procedural blanks. For undetected compounds in procedural blanks, MDLs were set as a signal of five times the noise level. MDLs for DDTs, PCBs, PBDEs, and DP ranged from 0.0073 to 0.22 ng/g lw (lipid weight). MDL for DBDPE was 0.56 ng/g lw.
2.1. Sample collection Thirty-two oriental magpie-robins (OMRs) were collected in March and November 2011 from three sampling sites in Guangdong Province, South China. The e-waste site is located in the rural area of Qingyuan (Fig. 1), where about 700,000 t e-wastes were processed each year within an area of 330 km2 using primitive techniques such as manual disassembly, acid dipping and open incineration. The urban site is situated in Guangzhou, a highly industrialized megacity. The rural site is located in an agricultural region of Zhaoqing City, with no e-waste recycling or industrial activities. The details of avian sampling method were described in Zhang et al. (2011a). Birds were immediately transported to the laboratory and euthanized with N2. Pectoral muscles were excised from each bird and stored at −20 °C until chemical analysis. 2
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Fig. 1. Map of sampling sites.
2.5. Statistical analysis
Table 1 Mean, median, and range concentrations of POPs (ng/g lw for all chemicals) in oriental magpie-robins from the e-waste, urban and rural sites, South China.
All concentration data were presented on a lipid weight basis. Statistical analysis was performed with SPSS 16.0 (SPSS Inc., Illinois, USA). The level of significance was set at p < 0.05. The raw concentration data and log-transformed data of POPs were tested to know if the data were normally distributed. The log-transformed concentrations of total DDTs, PCBs, and PBDEs were normal distributed, and one-way ANOVA was used to assess differences in concentrations of total DDTs, PCBs, and PBDEs among the three sampling sites. Spearman correlation analysis with the Least Significant Difference (LSD) test was used to assess correlations between individual POPs in birds.
N Lipid (%) ΣPCBsb ΣDDTsc ΣPBDEsd DBDPE ΣDPsf
3. Results and discussion
fanti
3.1. Concentrations of POPs
Anti-Cl11-DP
Concentrations of POPs in OMR samples from the e-waste, urban, and rural sites are summarized in Table 1. Median concentrations of ΣDDTs had a decreasing order of rural (1,313 ng/g lw) > urban (1,075 ng/g lw) > e-waste site (1,000 ng/g lw) (Table 1). However, no significant differences in concentrations of ΣDDTs were observed among the three sampling sites (p > 0.05). Sum PCB concentrations ranged from 446 ng/g lw at the urban site to 248,097 ng/g lw at the ewaste site. Levels of ΣPCBs in birds from the e-waste site were significantly higher than those from the urban and rural sites (p < 0.01), but concentrations of ΣPCBs did not differ significantly between the urban and rural sites (p > 0.05). The geographical distribution of concentrations of ΣPBDEs decreased in the order of e-waste site (5,740 ng/g lw) > urban (843 ng/g lw) > rural (244 ng/g lw) (Table 1). Birds from the urban site had significantly higher
Syn-Cl11-DP
a
Mean/Median Range Mean/Median Range Mean/Median Range Mean/Median Range Mean/Median Range Mean/Median Range Mean/Median Range Mean/Median Range
E-waste site
Urban site
Rural site
17 2.97 ± 0.25a 78,315/59,368 6,087–248,097 1,768/1,000 239-7,910 6,221/5,740 872-15,341 36.2/26.0 nd e −149 254/127 39.0–928 0.79/0.78 0.73–0.90 4.48/3.10 nd-13.0 1.11/nd nd-6.90
5 2.92 ± 0.60 873/800 446-1,518 2,487/1,075 224-7,667 1194/843 293-2,550 40.3/36.0 13–92 98.0/98.0 54.0–134 0.70/0.68 0.67–0.76 0.57/0.42 0.14–1.20 0.09/nd nd-0.34
10 2.81 ± 0.19 973/1,078 459-1,313 152,2/1,313 406-2,710 263/244 130–540 15.5/14.7 5.3–27.2 33.6/24.1 8.40–90.1 0.74/0.75 0.65–0.78 0.33/0.26 nd-1.40 0.05/nd nd-0.26
Mean ± SE. Sum of CBs 28/31, 52, 60, 66, 74, 99, 101, 105, 115/87, 118, 123, 128, 130, 137, 138, 146, 149/139, 153, 156, 157, 158, 164/163, 169, 171, 172, 175, 180, 183, 187, 190, 191, 194, 195, 203, 205, 206 and 209. c Sum of p,p′-DDT, o,p′-DDT, p,p′-DDD, p,p′-DDE, p,p′-DDM, p,p′-DDMU, o,p′DDE and o,p′-DDD. d Sum of BDEs 28, 47, 66, 100, 99, 85, 154, 153, 183, 202, 197, 203, 196, 208, 207, 206 and 209. e Not detected. f Sum of anti-DP and syn-DP. b
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concentrations of ΣPBDEs than those from the rural site (p < 0.01). DBDPE was detected in all the birds except one sample at the ewaste site with concentrations ranging from non detectable (nd) to 149 ng/g lw (Table 1). Levels of DBDPE in birds from the rural sites were significantly lower than those from the e-waste (p < 0.05) and urban sites (p < 0.05). DP (anti-DP and syn-DP) was detected in all the birds with concentrations ranging from 8.4 to 928 ng/g lw. Similar to DBDPE, levels of ΣDPs in birds from the rural sites were significantly lower than those from the e-waste (p < 0.01) and urban sites (p < 0.01). Concentrations of PCBs and PBDEs in birds from the e-waste site were generally higher than those from urban and rural sites, which highlighted the pollution of organic contaminants in e-waste recycling activities. Extremely higher concentrations of ΣPCBs and ΣPBDEs were also observed in birds, fish, soil, plant, and air from the same e-waste sampling site (Chen et al., 2014; Luo et al., 2009; Zhang et al., 2011b, 2011c; Zhang et al., 2012). Moreover, higher concentrations of PCBs and PBDEs were often found at other e-waste dismantling sites in China (Leung et al., 2011) and Vietnam (Tue et al., 2013). Concentrations of PBDEs and DBDPE were similar in OMRs collected in 2009 (Sun et al., 2012) and in 2011 (the current study) from the same sampling site. This indicates that primitive e-waste dismantling activities were still significant emission sources of PBDEs and emerging FRs in the study area. Meanwhile, birds from urban site had significantly higher levels of FRs than those in birds from rural sites. The elevated pollution status of FRs in birds from urban site was attributed to the large quantity of commercial products in cities. DDT concentrations were similar in birds from different sampling sites, implying the similar retrospective pollution of DDTs in these regions.
94.7 ± 2.75%, and 94.5 ± 1.20% to total DDTs in birds from e-waste, urban, and rural sites, respectively (Fig. S1, Supplementary Materials). The results confirmed that there was no recent input of DDTs in the sampling regions. The predominant PCB congeners were CBs 138 (contributions: 10.4–17.6%), 153 (12.6–24.2%), and 180 (5.95–8.00%) in birds from all sampling sites (Fig. 3). PBDE congener patterns exhibited complex features (Fig. 4). BDEs 99, 153, and 209 were the main congeners of PBDEs. BDE 153 (23.8%) dominated in PBDEs in birds from e-waste site, followed by BDEs 183 (17.0%) and 99 (13.8%). BDEs 209 (18.6%), 153 (17.3%), and 207 (10.6%) were the most abundant PBDE congeners in birds from the urban site. BDEs 153 (19.4%), 209 (13.9%), and 47 (11.8%) were main PBDE congeners in birds from the rural site. BDEs 99 and 183 took significant fractions in PBDEs in birds from e-waste site. The e-waste dismantling of obsolete electronic products could introduce large quantities of Penta-BDE and Octa-BDE mixtures into environment, which contained abundant BDEs 99 and 153, respectively. In urban and rural sites, Deca-BDE mixtures were more likely used in commercial products, as Penta-BDE and Octa-BDE mixtures were banned since 2009 (UNEP, 2009). The fanti values (ratios of concentrations of anti-DP divided by sum concentrations of anti-DP and syn-DP) were 0.79 ± 0.06, 0.70 ± 0.04, and 0.74 ± 0.04 in birds from e-waste, urban, and rural sites, respectively. The fanti values in birds from e-waste site were significantly higher than those from urban and rural sites (p < 0.01), which suggest site-specific bioaccumulation of DP isomers in the orientated magpie-robins. Overall, local sources of POPs seemed to significantly influence the profiles of POPs in birds. 3.3. Influence of trophic levels on bioaccumulation of POPs Stable nitrogen isotope ratio could provide independent measurement of trophic level in wildlife (Jardine et al., 2006). The δ15N values ranged from 4.06‰ to 10.7‰, 4.40–7.39‰, and 4.66–11.8‰ in OMRs from e-waste, urban, and rural sites, respectively, indicating the large variability in food items of oriental magpie-robins. In order to access the influence of tropic level on the contaminant levels, we performed correlation analysis between δ15N values and concentrations of the main POPs (all PBDE congeners, seven indicator PCBs, p,p′-DDE, DP, and DBDPE) in birds from different sampling sites (Tables S1–S3, Supplementary Materials). The δ15N values were significantly correlated with concentrations of most chemicals except CBs 52 and 101, and some BFRs with high octanol-water partition coefficient (Kow), including BDEs 196, 206, 207, 208, and 209, and DBDPE in OMRs from the e-waste site. The results indicate the biomagnification of most contaminants except the highly lipophilic BFRs in OMRs. In urban site, the δ15N values were only significantly correlated with the concentrations of BDEs 47, 99, 100, 196, and 203 in birds (p < 0.05). In rural site, the δ15N values were significantly correlated with the concentrations of BDEs 197 and 207, CBs 28, 52, 101, and 118 in birds (p < 0.05). Tropic level was not the main factor which determined the concentrations of POPs in urban and rural sites. High-brominated PBDEs and DBDPE have relatively high molecular weight, which could restrict the bioavailability of these chemicals in bird guts. However, the hexa- and hepta-BDEs, p,p′-DDE, and CBs 138, 153, and 180 were also not biomagnified in samples from urban and rural sites. BDEs 153, 154, and 183 have been proven to be the most bioaccumulative PBDE congeners in terrestrial food chains (Voorspoels et al., 2007; Yu et al., 2011, 2013). The possible reason might be that levels of hexa- and hepta-BDEs and PCBs were relatively low in dietary sources of birds from urban and rural sites. OMR samples were collected in two seasons (March and November) in the present study. OMRs are opportunistic predators of plants, fruits, insects, and other invertebrates. Diet compositions of birds were always different in different seasons (US EPA, 1993). So it is difficult to figure out the diet items for OMRs and bioavailability of POPs in diet items. OMRs in cities may also ingest more human-related diets, such as discarded human food and other garbage, than rural sites. It is also possible that biomagnification profile
3.2. Compositions of POPs Distinct composition patterns of POPs were found among the sampling sites (Fig. 2). PCBs (85.7%) were the predominant contaminants in birds at the e-waste site, followed by PBDEs (9.52%), DDTs (2.93%), DP (0.51%), and DBDPE (0.12%), but the predominant pollutants were DDTs in samples from the urban (42.1) and rural (52.1%) sites. Contributions of PCBs to POPs in birds from the e-waste site (85.7%) were significantly higher than those from the urban (26.1%) and rural (35.9%) sites. The high abundance of PCBs in birds was inevitably derived from the local primitive recycling of e-wastes. Birds from the urban site had higher proportions of halogenated flame retardants (PBDEs, DBDPE, and DPs) compared to those from the e-waste and rural sites. The great usage amount of commercial products in Guangzhou City could be the reason for the higher abundance of halogenated FRs. Compositions of DDTs and PCBs were similar in birds. DDTs were dominated by p,p′-DDE, which contributed 91.5 ± 1.19%,
Fig. 2. Contamination profiles of POPs in OMRs from the e-waste, urban and rural sites, South China. 4
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Fig. 3. PCB homologue profiles in OMRs from different sampling sites.
Fig. 4. PBDE congener profiles in OMRs from different sampling sites.
et al. (2015). The results indicate that the biomagnification of POPs in OMRs were highly variable, which might be affected by the pollution status of POPs in the dietary sources and dietary compositions in the habitats of OMRs. The biomagnification potential of POPs needs to be interpreted with caution in terrestrial avian food chains. Concentrations of most BFRs were significantly and positively correlated in samples of three bird species from the e-waste and rural site (Sun et al., 2012), which was inconsistent with the results in the present study. In OMRs from the e-waste site, two clusters of chemicals were identified (Tables S1–S3, Supplementary Materials). The first cluster included tetra-to octa-BDEs, PCBs, and p,p′-DDE. These chemicals can
of POPs in birds was determined by hepatic metabolism or excretion processes (Van den Steen et al., 2007), in addition to bioavailability of POPs in bird diets from these sites. In order to explore the biomagnification patterns of DP isomers, the correlations between fanti values and δ15N values were also examined. No significant relationship was observed in data from the e-waste, urban, and rural sites, separately, which was different with the results in previous studies (Chen et al., 2013; Mo et al., 2013; Peng et al., 2015). The carnivorous and piscivorous birds were investigated in Chen et al. (2013) and Mo et al. (2013), respectively. Three insectivorous birds and four omnivorous birds were collected in the study of Peng
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be considered as biomagnified POPs, as concentrations of them were significantly correlated with δ15N values. The other cluster of chemicals were non-biomagnified POPs, whose concentrations were not correlated with δ15N values. In OMRs from the urban site, concentrations of biomagnified POPs, including BDEs 47, 99, 100, 196, and 203 were significantly correlated, while concentrations of non-biomagnified POPs, including most hexa-to deca-BDEs, CBs 138, 153, and 180, and p,p′-DDE were significantly correlated (p < 0.05). The correlations were more complex in the rural site. Three clusters were observed: the first cluster included BDEs 47 and 100, CBs 138 and 153; the second cluster included BDEs 183, 202, 197, and 203; the third cluster included BDE 209 and CBs 28, 52, 101, 118, and 138. The three clusters had different log Kow or log octanol-air partition coefficient (Koa) except BDE 209. Chemicals in three clusters had log Kow between 6.57 -8.01, 8.38-8.99, and 5.62-6.87, or log KOA between 10.1-10.82, 12.52-13.38, and 8.29-10.51, respectively. POPs in rural site were likely from the transport of contaminants from other areas. Chemicals with different log KOA had different long-range transport capacities, which would result in the similar bioaccumulation profiles of POPs with similar log KOA values in birds.
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4. Conclusions Occurrence and profiles of DDTs, PCBs, PBDEs, DP, and DBDPE were assessed in OMRs from e-waste, urban, and rural sites. The elevated concentrations of PCBs and PBDEs in birds highlighted the heavy contamination of POPs in e-waste sites. In birds from the e-waste site, trophic biomagnification were observed for POPs except for high-brominated chemicals, which could be attributed to the low bioavailability of highly lipophilic chemicals. In contrast, most of POPs were not biomagnified in OMRs from the urban and rural sites. The results indicate that the biomagnificantion of POPs in OMRs was not consistent in different sites, which could be affected by bioavailability of POPs in diverse diet sources of birds in local environment. Acknowledgements This study was financially supported by the National Natural Science Foundation of China (Nos. 41603085, 41877361, 41573084 and 41931290), Talent Support Project of Guangdong Province, China (No. 201629019), Guangdong Foundation for Program of Science and Technology Research (Nos. 2017B030314052 and 2017B030314057), Pearl River S&T Nova Program of Guangzhou (Nos. 201806010079 and 201806010185), and Guangzhou Science and Technology Program (No. 201707020033). Appendix A. Supplementary data Supplementary data to this article can be found online at https:// doi.org/10.1016/j.ecoenv.2019.109758. References Chen, D., Hale, R.C., 2010. A global review of polybrominated diphenyl ether flame retardant contamination in birds. Environ. Int. 36, 800–811. Chen, D., Wang, Y., Yu, L., Luo, X., Mai, B., Li, S., 2013. Dechlorane Plus flame retardant in terrestrial raptors from northern China. Environ. Pollut. 176, 80–86. Chen, S.J., Tian, M., Zheng, J., Zhu, Z.C., Luo, Y., Luo, X.J., Mai, B.X., 2014. Elevated levels of polychlorinated biphenyls in plants, air, and soils at an E-waste site in southern China and enantioselective biotransformation of chiral PCBs in plants. Environ. Sci. Technol. 48, 3847–3855. Costantini, L., Sebastiano, M., Müller, M.S., Eulaers, I., Ambus, P., Malarvannan, G., Covaci, A., Massa, B., Dell'Omo, G., 2017. Individual variation of persistent organic pollutants in relation to stable isotope ratios, sex, reproductive phase and oxidative status in Scopoli's shearwaters (Calonectris diomedea) from the Southern Mediterranean. Sci. Total Environ. 598, 179–187. Covaci, A., Harrad, S., Abdallah, M.A., 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, 532–556.
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