Hydroxylated and methoxylated polybrominated diphenyl ethers in a marine food web of Chinese Bohai Sea and their human dietary exposure

Environmental Pollution 233 (2018) 604e611

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Hydroxylated and methoxylated polybrominated diphenyl ethers in a marine food web of Chinese Bohai Sea and their human dietary exposure* Yanwei Liu a, b, Jiyan Liu a, b, *, Miao Yu a, b, Qunfang Zhou a, b, Guibin Jiang a, b a

State Key Laboratory of Environmental Chemistry and Ecotoxicology, Research Center for Eco-Environmental Sciences, Chinese Academy of Sciences, Beijing 100085, China College of Resources and Environment, University of Chinese Academy of Sciences, Beijing 100049, China

b

a r t i c l e i n f o

a b s t r a c t

Article history: Received 19 June 2017 Received in revised form 3 October 2017 Accepted 26 October 2017

Hydroxylated (OH-) and methoxylated (MeO-) polybrominated diphenyl ethers (PBDEs) have been identified ubiquitous in wildlife and environment. However, understanding on their trophic accumulation and human exposure was hitherto limited. In this study, the occurrences and trophic behaviors were demonstrated for OH- and MeO-PBDEs using the biota samples collected from Dalian, a coastal city near P Chinese Bohai Sea. OH-PBDEs exhibited a wider concentration range (
Keywords: OH-PBDEs MeO-PBDEs Marine organisms Trophic behavior Dietary intake

1. Introduction Artificially synthesized polybrominated diphenyl ethers (PBDEs) have been widely applied as additive brominated flame retardants (BFRs) in consumer products since 1970s, leading to extensive release into the environment. Due to the characteristics of persistence, bioaccumulation, long-distance transportation and adverse health effects, penta-BDEs and octa-BDEs have been listed as persistent organic pollutants (POPs) in the Stockholm Convention in 2009. As the analogues of PBDEs, hydroxylated (OH-) and methoxylated (MeO-) PBDEs have also received public attentions. Special concerns have been given to the deleterious health effects and toxicity mechanisms of OH-PBDEs and MeO-PBDEs.

*

This paper has been recommended for acceptance by Maria Cristina Fossi. * Corresponding author. State Key Laboratory of Environmental Chemistry and Ecotoxicology, Research Center for Eco-Environmental Sciences, Chinese Academy of Sciences, Beijing 100085, China. E-mail address: [email protected] (J. Liu). https://doi.org/10.1016/j.envpol.2017.10.105 0269-7491/© 2017 Elsevier Ltd. All rights reserved.

In vivo and in vitro studies have determined that OH-PBDEs were more potent than PBDEs and MeO-PBDEs on some toxicological effects (Wiseman et al., 2011; Kojima et al., 2009; Su et al., 2012). Due to the structural resemblance to thyroid hormones, OH-PBDEs showed high affinities to the thyroid hormone transporter and receptor, disrupting the thyroid hormone homeostasis (Wiseman et al., 2011). Besides, OH-PBDEs can cause steroidogenesis disturbance, endocrine-disrupting effects, developmental toxicity, dioxin-like activity, genotoxicity and neurotoxicity (Kojima et al., 2009; Legradi et al., 2017; Peng et al., 2016; Dingemans et al., 2008). It was considered that some of the serious adverse effects of PBDEs were caused by their hydroxylated metabolites (Wiseman et al., 2011; Kojima et al., 2009; Su et al., 2012). Comparatively, the adverse effects reported for MeO-PBDEs were rare. Dioxin-like activity and endocrine-disrupting effects were also identified for several MeO-PBDE congeners (Kojima et al., 2009; Su et al., 2012). As far as we know, OH-PBDEs and MeO-PBDEs have no anthropogenic source and are considered as the transformation products of PBDEs. Biotransformation from PBDEs to MeO-PBDEs

Y. Liu et al. / Environmental Pollution 233 (2018) 604e611

was identified in pumpkin (Yu et al., 2013; Sun et al., 2013c) and maize (Xu et al., 2016). OH-PBDEs were identified as PBDE metabolites in human hepatocytes, rats, mice and fish, with transformation ratios less than 1% (Wiseman et al., 2011; Stapleton et al., 2009). Those biotransformation processes were thought to be catalyzed by cytochrome P450 monooxygenase (CYP) enzymes. On the other hand, OH-PBDEs were able to be generated through oxidation of PBDEs in abiotic environment (Ueno et al., 2008). It was also verified that OH-PBDEs and MeO-PBDEs have natural origins. OH-PBDEs in marine sponge Dysidea herbacea were proved to be naturally produced by the symbiotic filamentous cyanobacterium Oscillatoria spongeliae (Unson et al., 1994). 6-MeO-BDE-47 and 20 -MeO-BDE-68 were demonstrated as natural products by radiocarbon analysis in a North Atlantic True's beaked whale (Teuten et al., 2005). Interconversion between OH-PBDEs and MeO-PBDEs found in Japanese Medaka, marine sediment, pumpkins and soybeans implied another environmental source (Zhang et al., 2012; Wan et al., 2010; Sun et al., 2014; Pan et al., 2016). Because of the natural origin in marine environment, OH-PBDEs and MeO-PBDEs were generally at high concentrations in the primary producers and low-rank invertebrates, such as algae, marine sponges, and ascidians (Sionov et al., 2005; Fu et al., 1995; Schumacher and Davidson, 1995; Haraguchi et al., 2010). According to the available data, OH-PBDEs and MeO-PBDEs could be transferred through the food chain to fish, marine mammals and seabirds. However, their trophic transfer behaviors were not accurately evaluated since the primary producers and the low trophic level invertebrates were not concerned enough in the limited numbers of articles (Zhang et al., 2010a, 2012; Kelly et al., 2008; Dahlgren et al., 2016). OH-PBDEs and MeO-PBDEs existed in the seafood would be finally accumulated in human beings, and have been identified in human blood and breast milk samples (Eguchi et al., 2012; Chen et al., 2013; Lacorte and Ikonomou, 2009; Fujii et al., 2014; Wang et al., 2016), with higher concentrations in coastal residents' serum than inland e-waste recycling workers' (Eguchi et al., 2012). It has been found that environmental pollution and human exposure to OH-PBDEs and MeO-PBDEs around coastal areas were mainly attributed to the processing and consumption of tons of seafoods (Sun et al., 2013a, 2013b). Wang et al. (2011) found that marine fish contributed to higher dietary intakes of OH-PBDEs and MeO-PBDEs than freshwater fish (Wang et al., 2011). However, there is no scientific estimation on the dietary intakes and the human health risks of OH-PBDEs and MeO-PBDEs via various seafood consumption for coastal residents. In this work, the frequently detected OH-PBDEs, MeO-PBDEs and PBDEs in the marine environment of Bohai Sea (Zhang et al., 2010a, 2012; Kelly et al., 2008; Sun et al., 2013a) were analyzed in marine algae, invertebrates and fish species. Our objectives were to i) characterize their distribution patterns in different marine organisms collected from Bohai Sea, ii) investigate their trophic transfer behaviors, and iii) estimate human dietary intakes of these compounds via seafood consumption. The contributions of the primary producers and low trophic level invertebrates to these compounds' fates were particular focused and evaluated in the selected food web. 2. Materials and methods

605

and 3-MeO-BDE47; 10 mg/mL for 20 -MeO-BDE-68, 6-MeO-BDE-47, 40 -MeO-BDE-49, 4-MeO-BDE-42, 60 -MeO-BDE-99, 50 -MeO-BDE-99 and 6-MeO-BDE-85) and seven PBDE standards (50 mg/mL for BDE28, BDE-47, BDE-66, BDE-99, BDE-85, BDE-154, BDE-153). BDE-75 (50 mg/mL) and 13C-6-OH-BDE-47 (50 mg/mL) were selected as surrogated standards for PBDEs, MeO-PBDEs and OH-PBDEs. All standards were purchased from AccuStandard (New Haven, CT, USA) and Wellington (Guelph, ON, Canada). Acetonitrile (ACN), methyl tert-butyl ether (MTBE) and 2propanol were of HPLC grade. Acetone, hexane (HX) and dichloromethane (DCM) were of pesticide grade. All solvents were purchased from J. T. Baker (Phillipsburg, NJ, USA). Milli-Q water (18.3 MU cm) was generated by a Milli-Q system (Millipore, Billerica, MA). Silica gel (100e200 mesh size) was purchased from Merck (Darmstadt, Germany). Analytical reagent grade anhydrous sodium sulfate was purchased from Sinopharm Chemical Reagent, Inc. (Beijing, China). Silica gel and anhydrous sodium sulfate were heated at 140  C for 7 h and 660  C for 6 h before use, respectively. 2.2. Sample collection and preparation Marine biological samples of Bohai Sea were collected from costal area of Dalian in 2012. A total of 20 marine species were involved, including five species of marine fish, ten species of invertebrates and five species of algae. The details on organism species, sample number, trophic levels (TL), water contents (water %), lipid contents (lipid%), and stable isotope ratios were shown in Table S1. Among all the selected seafood types, the marine species of fish, crab, shrimp, cephalopod, bivalve and algae were the seafood most commonly consumed by local residents. The collected samples were immediately transported to laboratory on ice and cleaned by water. Stainless steel scalpel blades were used to get the target tissue, including flesh of fish, soft tissue of invertebrates and the whole algae. Wet tissues of several individual organisms were then freeze-dried and homogenized to form one composite sample. Each composite sample was formed from a certain number of individuals of algae, invertebrates and fish. Finally, samples were stored at 20  C until analysis. All the tools were rinsed by acetone between samples to avoid cross contamination. The sample extraction and purification method adopted in current study showed good recoveries (71e113%) and repeatability (4e12% RSD) in various matrix (water, soil, sediment, plant, mollusk and fish) (Sun et al., 2012). An amount of 2 g biological samples was successively spiked with surrogate standards and 15 mL of HX/ MTBE mixture (1:1, v/v). After ultrasonic extraction for 20 min twice, the extracts were combined and dried under a nitrogen flow, re-dissolved in DCM and mixed with 10 g 44% acidified silica gel (H2SO4: silica gel ¼ 44:66; m/m) to remove lipid. Then the organic phase was loaded on an anhydrous sodium sulfate column to remove water. After rinsing the column, the combined organic phase was concentrated to 2 mL by rotary evaporation. A silica column (5 g, deactivated with 5% water) preconditioned by hexane was used for further cleanup and separation. PBDEs, MeO-PBDEs and OH-PBDEs were successively eluted by 50 mL of 3% DCM in hexane, 60 mL of 20% DCM in hexane and 70 mL of DCM. Finally, the eluents of PBDEs and MeO-PBDEs were combined and concentrated to a final volume of 100 mL in hexane. The eluent of OH-PBDEs was concentrated to 100 mL in acetonitrile.

2.1. Chemicals and reagents 2.3. Instrumental analysis Standards of target compounds included ten OH-PBDE standards (50 mg/mL for 5-OH-BDE-47, 30 -OH-BDE-28 and 3-OH-BDE47; 10 mg/mL for 20 -OH-BDE-68, 6-OH-BDE-85, 4-OH-BDE-42, 40 OH-BDE-49, 6-OH-BDE-47, 50 -OH-BDE-99 and 60 -OH-BDE-99), ten MeO-PBDE standards (50 mg/mL for 5-MeO-BDE47, 30 -MeO-BDE28

Analysis of OH-PBDEs was performed on an Agilent 1290 liquid chromatograph (LC) interfaced with an Agilent 6460 triplequadrupole mass spectrometer (MS/MS) using electrospray ionization (ESI) in the negative ion multiple-reaction monitoring

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(MRM) mode. A C18 column (100 mm  2.1 mm, 2.2 mm particle size, Thermo Fisher Scientific, USA) was chosen for separation. The injection volume, column temperature and flow rate were set at 10 mL, 40  C and 0.38 mL min1, respectively. Mixture of acetonitrile and water was the mobile phase. The ratio of acetonitrile and water was initiated at 50:50, and then switched to 50:30 in 14 min. The column was equilibrated at 50:50 for 4 min between injections. PBDEs and MeO-PBDEs were simultaneously analyzed on an Agilent 7890A gas chromatograph (GC) coupled with an Agilent 7000A triple-quadrupole mass spectrometer (MS/MS). Methane was the reagent gas for the electron-capture negative ionization (ECNI). The DB-5 MS fused silica capillary column (30 m  250 mm i.d.  0.1 mm film thickness) used for separation was obtained from J & W Scientific, Folsom, CA. The carrier gas was helium and set at a constant flow of 1.0 mL min1. The initial oven temperature was 150  C and held for 2 min. Then the temperature increased to 220  C at a rate of 3  C min1 and finally to 260  C at 1  C min1. The post run was set at 300  C and held for 3 min. Selected ion monitoring (SIM) mode was used for the determination of PBDEs and MeO-PBDEs. Details about MS parameters and ion transitions of PBDEs, OH-PBDEs and MeO-PBDEs were presented in our previous studies (Sun et al., 2012, 2013a).

2.4. Calculation of trophic magnification factors Trophic magnification factors (TMFs) were used to assess the biomagnification potential of analytes. Stable isotopes of nitrogen and carbon were determined using a Thermo DELTA V advantage isotope ratio mass spectrometer coupled with a Flash EA1112 HT elemental analyzer (Thermo Fisher, USA). The stable nitrogen isotope ratios of nitrogen (d13C) in marine fish (20.32‰ to 15.92‰) and invertebrates (21.54‰ to 16.44‰) were within the values previously determined in Bohai ecosystem (25.38‰ to 11.08‰) (Wan et al., 2005), implying the same carbon source. The trophic level (TL) of organisms was calculated as formula (1) by the stable nitrogen isotope ratios of nitrogen (d15N) (Fisk et al., 2001).

TL ¼

d15 Nconsumer  d15 Nprimaryconsumer 3:8

þ 2:0

(1)

Where the filter feeder Chlamys farreri was considered as primary consumer with the trophic level 2.0, and the trophic enrichment factor of stable nitrogen isotope ratios (d15N) is 3.8 (Hop et al., 2002). Based on the regression equation (2) between the lipidnormalized analyte concentrations (C) and trophic levels, TMF values were calculated as formula (3):

log C ¼ a  TL þ k

(2)

TMF ¼ 10a

(3)

Based on the 0.05 significance level, the analyte was considered having the potential of biomagnification when its TMF > 1 and biodilution when its TMF < 1. During TMF calculation, data below detection limits is substituted with values derived from Regression on Order Statistics (ROS) to avoid biased results.

2.5. Calculation of dietary intakes via seafoods The average daily intake (ADI) of OH-PBDEs and MeO-PBDEs via seafood consumption was calculated as below:

ADI ¼

Cseafood  Daily consumption Body weight

(4)

Where Cseafood represents the average analyte's concentration (wet weight) of each seafood type. The dominant six seafood types for coastal residents were used for ADI calculation, that is fish, crab, shrimp, cephalopod, bivalve and algae. The daily consumption of seafood through dietary intake was estimated based on the survey from Chinese coastal city, Zhoushan, and human body weight was set at 60 kg (Jiang et al., 2007). The daily consumption of fish, crab, shrimp, cephalopod, bivalve and algae was 105 g, 17.3 g, 54.1 g, 3.37 g, 76.5 g and 0.2 g, respectively. 2.6. Quality assurance and quality control Identification of target compounds was conducted by comparing the retention time and the relative abundance of qualitative ions with corresponding standards. All reported concentrations were corrected by recoveries of surrogate standards which were 88 ± 22% and 100 ± 14% for 13C-6-OH-BDE-47 and BDE-75. One procedural blank was conducted in each batch of five samples. Solvent blanks were injected during instrumental analysis. No target compounds or carryover effect were observed. The method detection limit (MDL) and method quantification limit (MQL) were defined as the concentration that caused a signal-to-noise ratio (S/ N) of 3 and 10, respectively. MDLs and MQLs of each compound in different types of biotic samples were presented in Table S2. 3. Results and discussion 3.1. Concentrations of OH-PBDEs and MeO-PBDEs in marine biota To understand the contamination levels of the Bohai Sea marine organisms, the total concentrations of OH- and MeO-PBDEs were compared with the reported data. Since algal concentrations reported in literature were usually based on wet weight and the concentrations of marine animals were always on a lipid weight basis, the concentrations in algae and marine animals presented in Table 1 were based on wet weight (ww) and lipid weight (lw), respectively. The maximum concentrations of OH-PBDEs were found in red alga Mazaella japonica (5 ng/g ww). Algal concentraP P tions of OH-PBDEs and MeO-PBDEs in Bohai Sea were comparable or lower than those in the Baltic Sea and Philippine Waters €rn et al., (Haraguchi et al., 2010; Dahlgren et al., 2016; Malmva P 2008). The concentrations in algae were in the order of OHP MeO-PBDEs (0.01e0.1 ng/g PBDEs (0.09e5 ng/g ww) > P ww) > PBDEs (
Y. Liu et al. / Environmental Pollution 233 (2018) 604e611 Table 1 P Concentrations of OH-/MeO-PBDEs in marine organisms in this study and literature.a P Organism Seafood Types OH-PBDEs Algae (ng/g ww) Symphyocladia latiuscula Mazaella japonica Grateloupia ramosissima Wakame Sea lettuce Ceramium tenuicorne Ceramium tenuicorne Fucus gardneri Green algae Brown algae Red algae

607

P MeO-PBDEs

Sampling Location

Reference

Algae Algae Algae Algae Algae Algae Algae Algae Algae Algae Algae

0.2 5 0.1 0.09 1 9e12 0.2e7 ndb nde2 0.4e101 nde31

0.04 0.1 0.06 0.01 0.02 0.3e0.4 0.01e0.2 nd nde8 0.4e232 0.2e107

Bohai Sea Bohai Sea Bohai Sea Bohai Sea Bohai Sea Baltic Sea Baltic Sea Hudson Bay Philippine Waters Philippine Waters Philippine Waters

This study This study This study This study This study €rn et al., 2008) (Malmva €rn et al., 2008) (Malmva (Kelly et al., 2008) (Haraguchi et al., 2010) (Haraguchi et al., 2010) (Haraguchi et al., 2010)

Polychaete Echinoderm Cephalopod Gastropod Bivalve Bivalve Bivalve Shrimp Crab Crab Bivalve and Gastropod Bivalve Bivalve Bivalve Crab

63 10 6 30 7 5 16 nd 0.3 nd 6 160e3500 nd 2 nd

21 2 5 nd 18 5 10 nd 2 nd 4 160e420 14 16 2

Bohai Sea Bohai Sea Bohai Sea Bohai Sea Bohai Sea Bohai Sea Bohai Sea Bohai Sea Bohai Sea Bohai Sea Bohai Sea Baltic Sea Hudson Bay Liaodong Bay Liaodong Bay

This study This study This study This study This study This study This study This study This study This study (Sun et al., 2013a) €fstrand et al., 2011) (Lo (Kelly et al., 2008) (Zhang et al., 2010a, 2012) (Zhang et al., 2010a, 2012)

Fish Fish Fish Fish Fish Fish Fish Fish Fish Fish Fish Fish Fish Fish Fish

0.3 0.3 0.5 0.4 nd 0.3 0.3 nd 0.8 nm nm nm nm nm nm

2 7 9 17 4 9 126 3e42 nmc nde48 34 6e286 nde2 190e401 353e578

Bohai Sea Bohai Sea Bohai Sea Bohai Sea Bohai Sea Bohai Sea Liaodong Bay Hudson Bay Yangtze River Yangtze River Baltic Proper Bizerte Lagoon Bizerte Lagoon Mediterranean Sea Mediterranean Sea

This study This study This study This study This study This study (Zhang et al., 2010a, 2012) (Kelly et al., 2008) (Zhang et al., 2010b) (Su et al., 2010) (Haglund et al., 2010) (Ameur et al., 2011) (Ameur et al., 2011) (Ameur et al., 2011) (Ameur et al., 2011)

Invertebrates (ng/g lw) Clam worm Sea urchin Octopus Arthritic neptune Yesso scallop Washington clam Ark shell Sand shrimp Gazami crab Asian paddle crab 3 Mollusk species Blue mussel Mytilis edulis 3 Bivalve species Chinese mitten-handed crab Fish muscle (ng/g lw) Conger eel Korean rockfish Javelin goby Japanese flounder Greenling-L Greenling-S 8 Fish species Cod, sculpin, salmon Chinese sturgeon Anchovy Perch Mullet Sea bass Mullet Sea bass a b c

Concentrations in algae and marine animals were based on wet weight (ww) and lipid weight (lw), respectively. Not detectable. Not measured.

comparable to fish collected from Hudson Bay (Kelly et al., 2008), Yangtze River (Su et al., 2010) and the Baltic Proper (Haglund et al., 2010). It was concluded that OH-/MeO-PBDEs in organisms from Bohai Sea were at relatively low or moderate levels in comparison with the observations from other areas. 3.2. Relative contributions to total concentrations in marine biota Fig. 1 illustrated the concentrations and congener profiles of all the detected OH-PBDEs, MeO-PBDEs and PBDEs in marine organisms. Except for 60 -MeO-BDE-99 and 6-MeO-BDE-85, eight MeOPBDEs were detected in the marine organisms. 6-MeO-BDE-47 and 20 -MeO-BDE-68 were the predominant MeO-PBDE congeners, with the detection frequency of 86% and 76%. As for OH-PBDEs, 20 OH-BDE-68 and 6-OH-BDE-47 were most frequently detected, followed by 6-OH-BDE-85 and an unknown OH-PBDE compound. 30 OH-BDE-28 and 40 -OH-BDE-49 were only detected in several samples. The unknown compound showed different retention time but same mass spectrum as that of 6-OH-BDE-85 (Fig. S1), and was

detected in the commercial standard of 6-OH-BDE-85. Therefore, this compound was probably another OH-pentaPBDE isomer. As shown in Fig. 1(d), the relative contributions of OH-PBDEs, MeO-PBDEs and PBDEs varied with biota, which was related with organism species and tissue selection. For fish muscle samples, MeO-PBDE congeners showed percentages from 36% to 72% and the proportions of PBDEs ranged from 26% to 59%. The total amounts of PBDEs and MeO-PBDEs accounted for over 96% of these three compounds' burden in fish muscle, whereas the amount of OHPBDEs was very little. These results indicated that MeO-PBDEs and PBDEs were more accumulative in fish muscle than OHPBDEs, accordant with previous findings in muscle samples of zebrafish and marine fish (Zhang et al., 2012; Kelly et al., 2008; €fstrand et al., 2011; Wen et al., 2015). This phenomenon was Lo attributed to the fact that PBDEs and MeO-PBDEs were more lipophilic, while OH-PBDEs were more water-soluble and more easily excreted than PBDEs and MeO-PBDEs (Wiseman et al., 2011; Zhang et al., 2010b; Wen et al., 2015). It was observed that large-size greenling contained less OH-PBDEs and MeO-PBDEs than the

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Fig. 1. Concentrations and profiles of all the detected (a) MeO-PBDE, (b) OH-PBDE, and (c) PBDE congeners and (d) their total concentrations in different marine organisms (ng/g dw). Semiquantification of the unknown OH-PBDE was based on the calibration curve of 6-OH-BDE-85.

small-size, which might be caused by their different diet habits. Young greenlings mainly feed on shrimp, cephalopod and polychaete, while the adult greenlings live on fish and shrimp (Kwak et al., 2005). In comparison with fish and shrimp, octopus (cephalopod) and clam worm (polychaete) contain considerable OHPBDEs and/or MeO-PBDEs. It was suggested that the profiles of OH-/MeO-PBDEs varied with diet-dependent life stages. Among invertebrates, crustaceans, Washington clam and Yesso scallop showed specific accumulation abilities to PBDEs. It might be attributed to their slow metabolic rates and benthic living environment as sediment is a great reservoir for PBDEs (Zhang et al., 2012; Sun et al., 2013a). For other invertebrates and algae, OHPBDEs were the most abundant compounds (36%e98%). The concentrations of different compounds in algae and several invertebrates were in the order of SOH-PBDEs > SMeOPBDEs > SPBDEs. The high proportions of OH-/MeO-PBDEs in these organisms were due to their natural origins. Because the predominant OH-/MeO-PBDE congeners all contained a hydroxyl or methoxyl group in the ortho position which has been identified as the characteristic of natural produced OH-/MeO-PBDEs. According to all above results, the species-dependent compound profiles were caused by comprehensive reasons including the physicochemical properties and origins of the chemicals, and the diet habit of the organisms. 3.3. Trophic accumulation in the marine food web As a typical aquatic system affected by the estuary, the marine ecosystem in Bohai Sea is frequently applied to investigate trophic behaviors of various compounds. To intuitively represent the trophic distribution patterns of target compounds, the sampled organisms were separated into four trophic groups based on dietary studies (Odum et al., 1955; Harrold and Reed, 1985; Yang, 2001a, 2001b). Photoautotrophic algae are primary producers, whereas

herbivorous bivalve and sea urchin were assigned to primary consumers (Harrold and Reed, 1985). Arthritic neptune, octopus and crustaceans were secondary consumers since these species mainly feed on mollusks, crustaceans and polychaetes (Yang, 2001b). Considering the food items of small fish, crustaceans and octopus (Yang, 2001a), fish species in current study were classified as tertiary consumers. Clam worm was excluded from this grazing food chain, as it is generally classified into the detritus food chain (Odum et al., 1955). The concentrations (dry weight basis) of OH-PBDEs, MeO-PBDEs and PBDEs in different trophic groups were presented in Fig. 2. Besides the species-dependent concentrations discussed above, Fig. 2 revealed that the distribution patterns of these compounds in marine species were related to the trophic positions of the organisms. For OH-PBDE congeners, Fig. 2 shows that their median and mean total concentrations descended in the order of producers > primary consumers > secondary consumers > tertiary consumers. It suggested that OH-PBDEs displayed dilution trends along the food web according to the interspecific relations of feeding and predatism. To further confirm the dilution trends, the trophic magnification factors (TMFs) were introduced, in which lipid-normalized concentrations were used. TMF estimations P showed that log concentrations of OH-PBDEs were negatively correlated with the organism trophic levels (p < 0.01, R2 ¼ 0.385, TMF ¼ 0.23; Table S3), corroborating the dilution trends. Four dominant OH-PBDE congeners all exhibited the similar trophic behaviors (Fig. S2). This result was also accordant with the trophic dilution previously determined in an invertebrate-fish-bird food web for 6-OH-BDE-47 (TMF 0.21) and 20 -OH-BDE-68 (TMF 0.15) (Zhang et al., 2012). Though the use of fish muscle as the sample of tertiary consumers would introduce bias into TMF calculation, the P concentrations of OH-PBDEs and major congeners still decreased with the increase of trophic levels if fish species were excluded (p > 0.05, TMF ¼ 0.34e0.58). Although the negative linear

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consumers. Excluding these bivalve species, PBDE concentrations were in the order of tertiary consumers > secondary consumers > primary consumers > producers, in agreement with the increasing concentrations with trophic levels reported in literature (Zhang et al., 2010a; Kelly et al., 2008). 3.4. Dietary intakes and health risks via seafood consumption

P P P Fig. 2. Concentrations of OH-PBDEs, MeO-PBDEs and PBDEs (ng/g dw) in a) marine organisms and b) different trophic groups.

relationship was not significant, the decreasing trend was in conformity with the conclusion of trophic dilution. As these OH-PBDE congeners were all naturally produced, our findings suggested that the dilution behavior along the food chain/web was probably prevalent for naturally produced OH-PBDEs. As for MeO-PBDEs, tertiary consumers showed the highest accumulation potential, whereas the concentrations in other trophic groups did not differ much (p > 0.05). The special accumulation at high trophic levels was accordant with literature, as MeOPBDEs were proposed to undergo bioaccumulation and biomagnification like PBDEs due to their stability and hydrophobicity (Kelly et al., 2008; Zhang et al., 2010a). Biomagnification was previously determined for 20 -MeO-BDE-68 and 6-MeO-BDE-47 in a Canadian Arctic marine food web (Kelly et al., 2008) and a marine food web from Sydney Harbour, Australia (Weijs et al., 2009). But no statistically significant biomagnification was observed in this study and another study conducted in Bohai Sea (Zhang et al., 2010a). As reported, MeO-PBDEs can be rapidly metabolized to OH-PBDEs via rainbow trout microsomes and some mammals (Chang et al., 2009; Mizukawa et al., 2015), which probably led to the negative skewness of MeO-PBDEs' biomagnification potential. Tissue selection of fish muscle for fish in current study would be another contributor, because tissues with high accumulation capacity (e.g. liver and blubber) were used in the former study (Kelly et al., 2008). Moreover, this trophic distribution pattern also depended on food web components. Different from the limited food web studies regarding OH-PBDEs and MeO-PBDEs (Zhang et al., 2010a, 2012; Kelly et al., 2008; Dahlgren et al., 2016), more algae and invertebrates which were suggested as the natural origins of OH-/MeO-PBDEs were included in current food web. MeOPBDE congeners in fish and marine mammals were also suggested as natural products (Teuten et al., 2005). Thus MeO-PBDEs in tertiary consumers would accumulated from these lower-trophiclevel organisms. Namely, algae and invertebrates contributed to the majority of OH-/MeO-PBDEs in the whole marine ecosystem, and play a crucial role when evaluating the trophic behaviors of OH-/MeO-PBDEs. For PBDEs, the specific accumulation capacity of bivalve made the great concentration variation in primary

Fig. 3 illustrated the dietary intakes of OH-PBDEs, MeO-PBDEs and PBDEs via seafood consumption for residents of Dalian. 6-MeOBDE-47 was the predominant chemical contributing to the dietary intake with an ADI value of 0.4 ng/kg/d, followed by BDE-47 (0.3 ng/ kg/d) and 20 -MeO-BDE-68 (0.2 ng/kg/d). Comparatively, ADIs of individual OH-PBDE congeners (0.02e0.08 ng/kg/d) were relatively low. It was also evident that fish and bivalve were responsible for the majority of dietary exposure to these chemicals for coastal residents. Fish contributed to 70%, 35% and 53% of the dietary intake of MeO-PBDEs, OH-PBDEs and PBDEs, respectively. For OHPBDEs, bivalve accounted for a slightly larger proportion (39%) than fish. The daily intakes via various seafood consumption were comparable for MeO-PBDEs (0.8 ng/kg/d) and PBDEs (0.8 ng/kg/d), both of which were two times higher than the intake of OH-PBDEs (0.4 ng/kg/d). Compared with previous studies, the daily intake of OH-PBDEs and MeO-PBDEs via marine fish consumption in Dalian (MeO-PBDEs: 0.6 ng/kg/d; OH-PBDEs: 0.1 ng/kg/d) was within the range of intakes via fish consumption in Hongkong (MeO-PBDEs: 0.5e4 ng/kg/d; OH-PBDEs: 0.02e0.2 ng/kg/d) (Wang et al., 2011). And MeO-PBDEs showed a higher contribution to the intake than OH-PBDEs via seafood consumption in Dalian, fish consumption in Hongkong (Wang et al., 2011) and 24-diet samples in Japan (Fujii et al., 2014). The resemblance is resulted from the high seafood consumption frequencies and amounts in these coastal areas. And seafood was probably the major dietary source of OH-/MeO-PBDEs for coastal residents. This can also help to explain the higher concentrations of OH-PBDEs and MeO-PBDEs in serum of coastal residents than that of inland e-waste recycling workers (Eguchi et al., 2012). Coastal inhabitants are taking higher risks to the expose to OH-PBDEs and MeO-PBDEs than inland residents as the result of seafood consumption. For the lack of accurate toxicity data on human and the health risk assessment criteria for PBDEs, OH-PBDEs and MeO-PBDEs, it is hard to quantitatively assess the human exposure risk of these chemicals via seafood consumption. However, some toxicology

Fig. 3. Average daily intakes (ADIs) of OH-PBDEs, MeO-PBDEs and PBDEs via seafood consumption in Dalian, China. According to the calculation formula of ADI, the congener concentrations were based on wet weight.

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researches using animals and cell lines are referenced. The PBDE intake via seafood consumption (0.8 ng/kg/d) was six orders of magnitude lower than 1 mg/kg/d, the lowest observed adverse effect level derived from exposure experiments on rodents (Darnerud et al., 2001). But in vivo exposure data on mammals was unavailable for OH-PBDEs and MeO-PBDEs. Exposure studies on zebrafish and chicken has verified OH-PBDEs induced development toxicity at micromolar or nanomolar levels (Legradi et al., 2017; Peng et al., 2016), whereas in vitro studies using cell lines or assays identified that OH-PBDEs caused adverse effects at lower concentrations compared with PBDEs and MeO-PBDEs (Su et al., 2012; Kojima et al., 2009). Besides, OH-PBDEs can be formed from both MeO-PBDEs and PBDEs in biota. Investigation using rainbow trout, chicken, and rat microsomes revealed that OHPBDEs were more easily formed from MeO-PBDEs than PBDEs (Chang et al., 2009). Namely, MeO-PBDEs assimilated in human would further contribute to the risks of OH-PBDEs. Despite the small dietary intakes of OH-PBDEs and MeO-PBDEs, human exposure to these naturally produced chemicals should be paid more attentions. More investigation is required to elucidate the in vivo toxicity of OH-/MeO-PBDEs and provide more reliable risk assessment criteria. 4. Conclusion The present study determined that OH-PBDEs, MeO-PBDEs and PBDEs were at relatively low or moderate levels in marine organisms collected from Bohai Sea compared with other areas. The relative contributions and distribution patterns of OH-PBDEs, MeOPBDEs and PBDEs were different in marine biota, which was attributed to their different origins, physicochemical properties and the diet habits of the organisms. Unlike PBDEs, the majority of OH-/ MeO-PBDEs in the marine ecosystem are naturally produced, and algae and low-rank invertebrates are the primary source. Trophic dilution was determined for naturally produced OH-tetraPBDE and OH-pentaPBDE congeners, and was probably applicable for other natural OH-PBDEs. Though no biomagnification potential was observed for MeO-PBDEs and PBDEs, these compounds preferred to accumulate in tertiary consumers, raising the health and ecological concern over these organohalogen compounds at high trophic levels. Dietary intakes via seafood consumption were evaluated for OHPBDEs and MeO-PBDEs. Fish and bivalve contributed to great exposure risks. Though the dietary intake of OH-PBDEs was less than MeO-PBDEs and PBDEs, the exposure risks of OH-PBDEs could not be ignored. This finding raised the concern over the dietary exposure of these natural halogen organic compounds. Acknowledgment This work was jointly supported by the National Basic Research Program of China (2014CB441105) and National Natural Science Foundation of China (21621064, 21177147) and the Strategic Priority Research Program of the Chinese Academy of Sciences (XDB14010400). Appendix A. Supplementary data Supplementary data related to this article can be found at https://doi.org/10.1016/j.envpol.2017.10.105. References Ameur, W. Ben, Ben Hassine, S., Eljarrat, E., El Megdiche, Y., Trabelsi, S.,  , D., Driss, M.R., 2011. Polybrominated diphenyl ethers and Hammami, B., Barcelo

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