Polybrominated diphenyl ethers and alternative halogenated flame retardants in mollusks from the Chinese Bohai Sea: Levels and interspecific differences

Marine Pollution Bulletin 142 (2019) 551–558

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Polybrominated diphenyl ethers and alternative halogenated flame retardants in mollusks from the Chinese Bohai Sea: Levels and interspecific differences ⁎

Lingfang Fua, , Jie Peia, Yuyu Zhanga, Xiaogu Chengb, Shenxing Longa, Lixi Zenga,

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a

School of Environment, Guangzhou Key Laboratory of Environmental Exposure and Health, Guangdong Key Laboratory of Environmental Pollution and Health, Jinan University, Guangzhou 510632, China b Guangzhou Research Institute of Environmental Protection, Guangzhou 510620, China

A R T I C LE I N FO

A B S T R A C T

Keywords: Halogenated flame retardant Mollusk Bohai Sea Interspecific difference Influence factor

Polybrominated diphenyl ethers (PBDEs) and alternative halogenated flame retardants (AHFRs) were measured in eleven mollusk species collected from the Chinese Bohai Sea. PBDEs and AHFRs were detected in all species, and their average total concentrations were in the range of 22.5–355 and 10.0–84.3 ng/g lipid weight, respectively. Decabromodiphenyl ether (BDE-209) and decabromodiphenylethane (DBDPE) were the dominant halogenated flame retardants (HFRs), contributing 22.5% to 73.6% and 3.1% to 38.3% of the total HFRs, respectively. The levels of PBDEs and AHFRs were moderate to high from a global perspective. Interspecific differences in the accumulation of PBDEs and AHFRs were characterized by heat map and cluster analysis. Composition profile differences were also observed, with higher proportions of AHFRs in gastropods than in bivalves. These species-specific differences in concentrations and profiles in mollusks were attributed to different species traits, including feeding habit, trophic level, and metabolic potential.

Halogenated flame retardants (HFRs) are applied in various household and industrial products for fire safety purposes (Iqbal et al., 2017). Although penta-, octa-, and deca-BDEs among classic polybrominated diphenyl ethers (PBDEs) have been successively banned in technical mixtures during different periods, concerns regarding PBDEs persist due to their release from many in-use products (Tian et al., 2015). Alternative halogenated flame retardants (AHFRs) are widely used as replacements for PBDEs and have been detected in environmental matrices including dust, soil, water, sediment and wildlife (Cao et al., 2014; Iqbal et al., 2017; Li et al., 2017; Wang et al., 2015a; Zhu et al., 2018); AHFRs include dechloranes, pentabromoethylbenzene (PBEB), hexabromobenzene (HBB), hexachlorocyclopentadienyl-dibromocyclooctane (HCDBCO), 1,2-bis(2,4,6-tribromophenoxy)ethane (BTBPE), bis(2-ethylhexyl)-tetrabromophthalate (TBPH), and decabromodiphenylethane (DBDPE). Relatively high levels of HFRs have been reported in many regions, especially in some highly industrialized areas, such as the Bohai Economic Rim (Li et al., 2017; Wang et al., 2017b). As one of the most prosperous regions as well as an important fishery in China, the Bohai Economic Rim has become a research hotspot for potential environmental deterioration (Meng et al., 2015a;

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Zheng et al., 2016). Over the past few decades, large amounts of pollutants, including HFRs, have been manufactured and used in this region (Li et al., 2016). These compounds can be discharged into oceans through river input, atmospheric deposition, and human activities (Liu et al., 2014; Sun et al., 2018; Wang et al., 2015b; Zhen et al., 2016). Relatively high concentrations of PBDEs and AHFRs have been found in seawater and sediment near a coastal area of the Bohai Sea (Pan et al., 2011; Pan et al., 2010; Wang et al., 2017a; Wang et al., 2017b). Most HFRs with a high octanol-water partition coefficient (Kow) have strong hydrophobic and lipophilic properties and can accumulate in aquatic animals through bioconcentration and dietary uptake (Morris et al., 2018; Van Ael et al., 2013). For example, previous studies have shown the high accumulation ability of PBDEs and Dechlorane Plus (DP, including syn- and anti-DP) in various marine organisms, including phytoplankton and invertebrates, from the coastal area of the Bohai Sea (Jia et al., 2011; Peng et al., 2014; Shao et al., 2016; Tian et al., 2010; Zhang et al., 2010; Zheng et al., 2016). Although numerous studies have kept a watchful eye on the bioaccumulation of PBDEs and DP in ocean organisms in this region, data for AHFRs are relatively scarce (Jia et al., 2011; Peng et al., 2014). Mollusks, especially gastropods and bivalves, are well known as

Corresponding authors. E-mail addresses: [email protected] (L. Fu), [email protected] (L. Zeng).

https://doi.org/10.1016/j.marpolbul.2019.03.056 Received 8 September 2018; Received in revised form 20 March 2019; Accepted 28 March 2019 Available online 10 April 2019 0025-326X/ © 2019 Elsevier Ltd. All rights reserved.

Marine Pollution Bulletin 142 (2019) 551–558

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from the samples are presented in the Supplementary Data. A Shimadzu gas chromatograph interfaced with a mass spectrometer (GCMS-QP 2010 Ultra) was used to analyse all the targets, and the mass spectrometer was operated in electron-capture negative ionization (ECNI) mode. A DB-5HT column (15 m × 0.25 mm i.d. with 0.1 μm film thickness) was chosen to achieve chromatographic separation of the target compounds. The ion source, quadrupole, and transfer line temperatures were set at 250, 150, and 280 °C, respectively. The column temperature was initiated at 110 °C (held for 5 min), then increased to 200 °C at 40 °C/min (held for 4 min), ramped to 260 °C at 10 °C/min (held for 1 min), and finally ramped to 310 °C at 15 °C/min (held for 15 min). Splitless mode was used to automatically inject samples (1 μL each). The carrier gas was ultrahigh purity helium at a flow rate of 1.5 mL/min. Stable isotope analysis for δ13C and δ15N in mollusks was based on a previous study (Meng et al., 2015a), and TLs were calculated based on the measured δ15N value. The detailed analysis processes for stable isotopes and equations for calculating δ13C, δ15N, and TL are described in the Supplementary Data. Quality assurance and quality control followed previously established methods (Fu et al., 2017; Zhu et al., 2012). A procedural blank, a spiked blank, and a matrix spike were included in every batch of 12 field samples. All target components in the blank samples and field blank samples were undetectable or below the method quantity limit (MQL). The relative recoveries of the target compounds in the spiked samples were 74–118%. The average recoveries of BDE-51, BDE-115, and F-BDE-208 were 85 ± 6%, 83 ± 14%, and 90 ± 11% in all spiked samples and 87 ± 12%, 84 ± 16%, and 81 ± 20% in the field samples, respectively. Duplicate samples were also analysed to ensure good reproducibility, with a relative standard deviation (RSD) value < 20%. The MQL was defined as ten times the signal of the standard compound, ranging from 0.003 (PBEB) to 0.31 ng/g (DBDPE). Details on the recoveries and MQLs of the target analytes are presented in Table S2. Statistical analyses were performed with IBM SPSS 22.0 (SPSS Inc., Illinois, USA) and Sigmaplot v.11 (Systat software Inc., Point Richmond, USA). All concentration data were reported on a lipid weight (lw) basis if not otherwise specified. The statistical level of significance was considered acceptable at p < 0.05. Analyte concentrations under the MQLs were replaced by one-half of the MQL in statistical analysis. Heat mapping and cluster analysis were performed using Heml Software (Heatmap Illustrator, Version 1.0). One-way analysis of variance (ANOVA) was used to determine significant differences, and Tukey's post hoc comparison was performed if necessary. Only individual target analytes with a detected frequency over 50% were used for further analysis to ensure reliable results. The concentrations of HFRs in 11 mollusk species from the Chinese Bohai Sea are summarized in Table 1 and Table S4, and the composition profiles of the detected targets are presented in Fig. 1. Both ∑PBDE (sum of BDE-47, 100, 99, 154, 153 and 209) and ∑AHFR (sum of DP, PBEB, HBB, TBPH and DBDPE) were detectable in the 91 composite samples, with ranges from 22.5 to 355 ng/g lw (mean of 55.0 ng/g lw) and 10.0 to 84.3 ng/g lw (mean of 34.7 ng/g lw), respectively, indicating universal HFR contamination in the coast of the Chinese Bohai Sea. BDE209 (10.2–284 ng/g lw) and DBDPE (4.73–63.8 ng/g lw) were the dominant contaminants of HFRs and were detectable in 94.5% and 75.8% of the samples, with contributions ranging from 22.5% to 73.6% and 3.1% to 38.3%, respectively (Fig. 1). Similar results were also found for mud snail and veined rapa whelk collected from Bohai Bay (Tian et al., 2010) and almost all invertebrate species collected from the Pearl River (Sun et al., 2018). The variations in the contributions of BDE-209 and DBDPE implied accumulation differences among species. In the study presented here, as the AHFR contaminant with the secondhighest concentration, TBPH was detected in all mollusk species with an average concentration of 5.59 ng/g lw. It is widely considered that the bioaccumulation potential of compounds tends to increase with log

bioindicators that have successfully been used to elucidate the occurrence of persistent organic pollutant contamination in marine ecosystems due to their sessile lifestyle, low trophic level (TL) and filter feeding habit (Wang et al., 2008). Interspecific differences in the levels and composition profiles of various persistent contaminants in mollusks have been observed in previous studies (Dauwe et al., 2009; Eulaers et al., 2013; Meng et al., 2015a; Morris et al., 2018; Zhang et al., 2013; Zheng et al., 2016). Feeding habit has also been highlighted as an important factor in determining PBDE profiles in different species (Nie et al., 2015; Zeng et al., 2016). Trophic position is the main influential factor on the concentration of PBDEs in mollusks (Meng et al., 2015a; Wang et al., 2008; Zheng et al., 2016). A previous report showed that mollusks have different abilities to metabolite PBDEs (Tian et al., 2015). Despite the above observations, little is known about the species-specific bioaccumulation of AHFRs and corresponding potential influence factors among mollusk species. These studies also show that feeding habit, trophic transfer, and metabolic ability are considered key factors influencing the accumulation of pollutants. Understanding the interspecific differences among mollusks exposed to HFRs as well as their potential interaction factors may allow for a more precise assessment of contaminant status. The concentrations of HFRs in 91 samples of eleven mollusk species collected from coastal areas along the Bohai Sea were detected, and the corresponding carbon and nitrogen stable isotope ratios (δ13C and δ15N) were simultaneously measured. The aim of this paper was to determine the levels of PBDEs and AHFRs in eleven mollusk species. We also focused on interspecific differences in the accumulation concentration and profile of PBDEs and AHFRs among mollusk species and attempted to account for these variations through feeding habit, trophic position, and metabolic ability. The sampling areas include nine cities belonging to four provinces along the Bohai Economic Rim, including Weihai, Yantai, Penglai, Tianjin, Shouguang, Qinhuangdao, Huludao, Yingkou, and Dalian (Fig. S1). The Bohai Sea is surrounded by the Liaodong Peninsula, Shandong Peninsula, and North China Plain and is located in eastern China. These coastal regions include highly industrialized cities with frequent human activity and booming industrial development. The Bohai Sea receives a large amount of water that may contain masses of pollutants from over 40 rivers (Meng et al., 2015b). As a semi-enclosed inner shelf sea with slow changes in water, the polluted Bohai Sea is not easily self-cleaned once contaminated. Eleven mollusk samples, including Rapana venosa (Rap), Neverita didyma (Nev), Mactra veneriformis (Mac), Meretix meretrix (Mer), Mya arenaria (Mya), Crassostrea talienwhanensis (Ost), Amusium veneriformis (Amu), Cyclina sinensis (Cyc), Chlamys farreri (Chl), Scapharca subcrenata (Sca), and Mytilus edulis (Myt) were selected and collected from nine coastal cities along the Bohai Sea in 2012. Detailed information on the samples is presented in Supporting Data Table S2. After being depurated for approximately 12 h in filtered water, the mollusk samples were carried in ice boxes and transported quickly to the laboratory and successively cleaned with tap water and ultrapure water. The soft-body tissue and shell of samples were separated by stainless-steel scalpel rinsed with ultrapure water. Approximately 100 to 500 g of wet soft tissue from the same sampling site was used to form a composite sample of each species. The samples were homogenized by a blender and then freeze-dried. Before analysis, the samples were frozen at −20 °C. Sample preparation and instrumental analysis for 7 PBDEs (BDE-47, 100, 99, 154, 153, 183, and 209), 11 HFRs (DP, Dechlorane 602 (Dec602), Dechlorane 603 (Dec603), Dechlorane 604 (Dec604), PBEB, HBB, HCDBCO, TBPH, BTBPE, and DBDPE) were based on previously established procedures (Liu et al., 2014; Luo et al., 2014), with minor modifications. Briefly, approximately 1–2 g of each sample was weighed and then Soxhlet-extracted for 48 h. The extracts were preliminarily purified with concentrated sulfuric acid to remove lipids and other interferences and then further cleaned through a multilayer packed column. Details on the extraction and purification of targets 552

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Table 1 Mean concentrations (ng/g lipid weight) of PBDEs and AHFRs with high detected frequency (< 50%) in eleven mollusk species from the Bohai coastal area in China. Abbreviation

N

BDE-47

BDE-100

BDE-99

BDE-154

BDE-153

BDE-209

∑PBDEb

DP

PBEB

HBB

TBPH

DBDPE

∑AHFRc

Rap Nev Mac Mer Mya Ost Amu Cyc Chl Sca Myt Mean Median Min Max Detected frequency (%)

18 7 5 11 2 7 8 8 9 9 7

5.74 2.04 1.50 2.74 0.87 3.59 1.52 6.89 6.77 3.93 4.60 3.65 3.59 0.87 6.89 100

6.51 4.56 1.22 0.83 0.95 12.51 4.30 2.44 53.2 23.3 5.99 10.52 4.56 0.83 53.2 98.9

6.46a 3.92 2.23 1.70 0.90 4.85 3.64 5.98 6.11 2.29 4.40 3.86 3.92 0.90 6.46 90.1

1.20 0.74 0.90 0.51 0.54 2.44 1.15 2.24 2.41 0.39 0.54 1.19 0.90 0.39 2.44 69.2

1.26 1.50 0.67 0.66 0.57 0.84 0.93 1.34 2.28 0.56 0.50 1.01 0.84 0.50 2.28 57.1

21.1 14.9 66.3 60.1 18.7 101 15.6 36.1 284 47.1 10.5 61.5 36.1 10.5 284 94.5

42.3 27.7 72.8 66.5 22.5 126 27.1 55.0 355 77.5 26.5 81.7 55.0 22.5 355 100

4.68 3.86 3.22 1.97 2.27 3.94 2.52 3.89 4.45 2.60 1.72 3.19 3.22 1.72 4.68 68.1

2.77 4.87 0.56 0.42 0.38 0.48 0.89 2.56 4.94 1.15 0.80 1.80 0.89 0.38 4.94 100

2.59 2.34 3.16 2.12 0.27 2.00 1.37 6.97 2.94 2.01 1.69 2.50 2.12 0.27 6.97 98.9

4.93 3.64 4.58 4.32 2.37 14.0 2.85 12.9 6.74 1.98 2.49 5.53 4.32 1.98 14.0 100

35.5 23.8 6.33 8.06 4.73 63.8 9.00 42.6 12.2 20.2 12.6 21.7 12.6 4.73 63.8 75.8

50.5 38.5 17.9 16.9 10.0 84.3 16.2 68.9 31.2 27.9 19.3 34.7 27.9 10.0 84.3 100

a b c

The maximum and minimum values are shown in bold. Sum of BDE-47, 100, 99, 154, 153, and 209 concentration. Sum of DP, PBEB, HBB, TBPH, and DBDPE concentration.

(Table 1). The investigated contaminants, including BDE-183 (20.9%), Dec602 (48.4%), Dec603 (17.5%), Dec604 (16.5%), HCDBCO (28.6%), and BTBPE (17.6%), were detected at low frequencies (detection frequency < 50%) and concentrations (Table S4), which could be attributed to their relatively small production and application in this study region (Zhu et al., 2014). The low detection frequency of BTBPE was similar to that of its market substitute, BDE-208, which is consistent with those found in mussels (Mytilus spp.) along the California coast (Dodder et al., 2014). Compared to Dec603 and Dec604, a higher detection frequency and level of Dec602 were found in mollusk samples; this trend is similar to that in a previous report (Jia et al., 2011). These results suggest that there is a certain degree of HFR contamination in the Bohai Sea. One possible reason is that the seawater in the Bohai Sea is restricted to limited exchange due to its semi-enclosed topographic characteristics, which reduces the dilution of pollutants (Meng et al., 2015a). For most HFRs, especially PBDEs, the highest concentrations were found in Chl (Table 1). In addition, relatively high concentrations of HFRs were also found in Ost (126 ng/g lw for ∑PBDE and 80.3 ng/g lw

Kow value in the span of 5–7 but shows a decreasing trend with increasing log Kow value when log Kow exceeds 7. Compared with other targets in the present study, BDE-209, DBDPE, and TBPH have a relatively large molecular mass (949.2, 971.2, and 706.1) and high log Kow (9.87, 11.1, and 9.34); these properties can influence bioaccumulation because of low bioavailability (Wu et al., 2008). Previous reports have shown that DBDPE and TBPH were the predominant HFR compounds found in atmospheric gaseous and particulate samples from Tianjin (Li et al., 2017) and BDE-209 was the most dominant PBDE congener found in seawater from the same region (Wang et al., 2017b). These results indicate that relatively high concentrations of these compounds exist in the environment around the Bohai Sea. Thus, the higher concentrations of BDE-209, DBDPE, and TBPH in the mollusk samples may be attributed to the dynamic input of these pollutants. BDE-100 was found in 98.9% of the samples at concentrations ranging from 0.83 to 58.2 ng/g lw and showed a large variation in the proportion of the total contaminant load (1.0%–22.1%). Among the HFRs with high detection frequency (> 50%), BDE-47, BDE-99, BDE-154, BDE-153, DP, PBEB, and HBB presented relatively low concentrations (0.39–3.65 ng/g lw) and low proportions of the total contaminant load (0.4%–10%)

Fig. 1. Profiles of PBDEs and AHFRs in mollusk species collected from the Bohai Sea coastal area in China. 553

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for ∑AHFR). Previous studies have found that Myt and Ost collected from the same regions had relatively high capacities to accumulate PBDEs (excluding BDE-209, which was not detected or less than the limit of detection), but concentrations of HFRs in Myt were notably lower than those in Ost in this study, which may be due to the difference in accumulation of BDE-209 in Myt (10.5 ng/g lw, accounting for 23.0% of all HFRs) and in Chl (101 ng/g lw, accounting for 73.6% of all HFRs) in this area. The concentrations and proportions of BDE-209 in Chl and Ost were higher than those in other species, while Rap, Cyc and Ost showed a relatively high accumulation capacity for DBDPE and TBPH (Table 1 and Fig. 1). These results indicated that there were selective accumulation differences for these highly hydrophobic compounds among mollusk species. A variable enrichment potential of heavy metals has also been found in various mollusks. For example, Ost can accumulate more Cu and Zn, but Rap has a significantly higher accumulation potential for Cd and Hg than other species (Liang et al., 2004; Liang et al., 2003; Wang et al., 2005). Mya was shown to be more suitable than other species to indicate contamination by butyltin compounds in mollusks (Zhang et al., 2013). Therefore, in addition to the source and physicochemical properties of pollutants, the selective accumulation of specific contaminants may also affect the occurrence of contaminants in different mollusk species, which may be related to their species traits (Liu et al., 2016; Meng et al., 2015a). Available data for HFR concentrations in mollusks worldwide are summarized in Table S5. A boxplot is used to compare the concentrations of PBDEs in mollusk species worldwide with those in the present study (Fig. 2). The levels of ∑PBDE (22.5–355 ng/g lw, 1.92–42.7 ng/g dw) detected in the present study are higher than those from the Pearl River Estuary of China in 2013 (2.5–38 ng/g lw) (Sun et al., 2015a) and most aquatoria in Europe (ND–52.7 ng/g lw) (Aznar-Alemany et al., 2018; Aznar-Alemany et al., 2016; Munschy et al., 2015; Piersanti et al., 2015; Trabalon et al., 2017; Villaverde-de-Saa et al., 2013), comparable to those from the Dongjiang River in China (120 and 146 ng/g lw) (Sun et al., 2018), the catchment of Singapore (48.4 ng/g lw) (Wang and Kelly, 2018), Lake Winnipeg of Canada (127 ng/g lw) (Law et al., 2006), the California coast in America (13.1 ng/g dw) (Dodder et al., 2014), and some Asian coastal areas (0.46–440 ng/g lw) (Isobe et al., 2012), but only lower than those reported for the Pearl River in 2014 (890 ng/g lw) (Sun et al., 2018)and the Yadkin River in America (47,200 and 64,900 ng/g lw) (La Guardia et al., 2012). The comparative results suggest that the PBDE pollution in mollusks collected from the Bohai Sea is at a middle-upper level from a global perspective. Data on mollusk contamination by some AHFRs remains very scarce

on a worldwide level, so only DP, HBB, BTBPE, and DBDPE results were compared worldwide (Table S5 and Fig. 1). In general, the DP, HBB, BTBPE, and DBDPE levels detected in mollusks in the current study were also at moderate or high levels compared to those in other studies (Fig. 1). The concentrations of DP and DBDPE (1.72–4.68 ng/g lw and 4.73–63.8 ng/g lw, respectively) were slightly higher than those in mangrove biota collected from the Pearl River Estuary in 2013 (0.28–2.0 ng/g lw and 0.78–6.9 ng/g lw) (Sun et al., 2015b) but lower than those in mud snail collected from the Pearl River in 2014 (24.6 ng/ g lw and 97.4 ng/g lw) (Sun et al., 2018). This may be attributed to interspecific differences and/or the increasing usage of AHFRs in the Pearl River area, which is also located in an economically developed region. The concentrations of DP in this study were higher than those in other regions, except Greece (21.5 ng/g lw) (Aznar-Alemany et al., 2018), (Table S5). Similarly, the DBDPE concentrations (4.73–63.8 ng/ g lw, 0.07–1.92 ng/g ww) in this study were comparable to and lower than those detected in mollusks from the Dongjiang River and Lake Taihua in China (15.1 and 111 ng/g lw, respectively; 0.28–9.31 ng/g ww) (Sun et al., 2018; Zheng et al., 2018), respectively and were generally much higher than those found in European and North American countries (Table S5). The levels of HBB in this study were considerably higher than those found in mollusks from Singapore, France, Albania, Italy, Norway, Spain, and the United Kingdom (AznarAlemany et al., 2018; Munschy et al., 2015; Trabalon et al., 2017; Wang and Kelly, 2018). The concentrations of BTBPE in mollusks (ND–1.14 ng/g lw, ND–0.04 ng/g ww) were consistent with those reported in three mollusk species from the Dongjiang River in China (0.09 and 0.79 ng/g lw) (Sun et al., 2018), mussels from Canada (1.29 ng/g lw) (Law et al., 2006), and oysters from three regions of France (0.002–0.015 ng/g ww) (Munschy et al., 2015), but lower than those in snail from Lake Taihua in China (0.78 ng/g ww) (Zheng et al., 2018) and approximately two orders of magnitude less than those in gastropods and bivalves from the Yadkin River in America (303 and 153 ng/g lw) (La Guardia et al., 2012). The relatively high exposure of these HFRs in mollusks from the Bohai Sea suggests that this region has been polluted to a certain degree, which may be attributed to the prosperous commercial activities over the past several decades and semi-enclosed terrain in the Bohai Economic Rim (Zhu et al., 2012). Among the other AHFRs, the concentrations of TBPH (1.98–14.0 ng/g lw, 0.04–0.43 ng/g ww) were one to two orders of magnitude less than those from the Yadkin River in America (380 and 1370 ng/g lw), where there is a textile manufacturing outfall (La Guardia et al., 2012), but comparable to those from Lake Taihua in China (0.05–0.51 ng/g ww) (Zheng et al., 2018). The concentration of PBEB in mussels (0.9–2.9 ng/g lw) from Lake Maggiore in Italy was comparable with those found in our study (0.38–4.94 ng/g lw) (Poma et al., 2014), but PBEB was not detected in many European countries (Aznar-Alemany et al., 2018). The relatively low concentrations (0.26–0.66, ND–0.60, and ND–0.93 ng/g lw) of DP-related compounds (Dec602, Dec603, and Dec604, respectively) were comparable to those found in oysters from the same region in 2008 (Jia et al., 2011). This similarity may be because these compounds were not manufactured in China (Wang et al., 2016). Other biota were used to compare the levels of HCDBCO due to lack of related data in mollusks. The concentration of HCDBCO ranged from ND to 0.03 ng/g ww, which was similar to those found in ring-billed gulls (ND–0.02 ng/g ww) from the St. Lawrence River in Canada (Gentes et al., 2012). Although the concentrations of HFRs were compared in this study, differences in the transformation and transfer of these pollutants in biota, affected by biological factors and ecological factors, can influence the accuracy of the inferred aquatic environment contamination status (Mizukawa et al., 2013; Roberts et al., 2011). Cluster analysis based on the concentrations of selected target contaminants (detection frequency > 50%) in samples was performed by hierarchical clustering to identify similar and different accumulation patterns of HFRs in the eleven mollusk species (Fig. 3). Two well-

Fig. 2. Comparison of PBDEs and AHFRs concentrations in mollusks worldwide, the mean/median data was used and based on Table S5. Center line was median; box plot edges present the 25th and 75th percentiles; whiskers defined as range of data values. 554

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Fig. 3. Cluster analysis of HFRs in mollusks by heat mapping. The color intensity in each panel shows the concentration of HFRs in specie, referring to the color key at right.

Fig. 4. Ratio of BDE-99/BDE-100 and BDE-99/BDE-47 in mollusks among three groups. The red line represents mean value of median ratio for three groups. Outliers shown (·). Asterisks indicate significant differences among the three groups (Tukey's tests *: p < 0.05). (For interpretation of the references to color in this figure legend, the reader is referred to the web version of this article.)

Fig. 5. The relationship of ∑PBDE and ∑AHFR with TLs in mollusks of group two.

mollusks. Significant interspecies differences in the accumulation of PBDEs, polychlorinated biphenyls, and organochlorine pesticides were also observed in the eggs of three insectivorous bird species in a previous report (Dauwe et al., 2009). Species-specific differences in the profiles of PBDEs and AHFRs were also found among the investigated mollusk species (Fig. 1). Group one had a slight predominance of AHFRs, and the two mollusk species were generally presented similar compositions. DBDPE was the dominant contaminant in Rap and Nev (38.3% and 36.0%), which had higher concentrations than other species. Other AHFRs in group one had similar proportions, and the contributions of DP (5.04% and 5.82%),

differentiated clusters were observed in mollusk species: Cluster 1 can be divided into two subgroups. The first subgroup (group one) included Rap and Nev, which belong to gastropods. Veneroida (Mer, Mac, Cyc, Ost), Pterioida (Amu), and Myoida (Mya) were aggregated in the second subgroup (group two). Cluster 2 (group three) was characterized by a relatively large difference in bioaccumulation pattern from that of other species and included Chl, Sca, and Myt, belonging to Pterioida, Arcoida and Mytioida, respectively. One-way ANOVA also showed that the log-transformed concentrations of ∑PBDE and ∑AHFR differed significantly among all species (F = 3.39, 2.65, p < 0.01). These results indicated interspecies differences in the accumulation of HFRs among

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dilution of persistent semivolatile compounds (PCBs, HCHs, DDTs, TBBPA, and SCCP) has also been found in other invertebrates and fish (Liu et al., 2016; Wang et al., 2008; Yuan et al., 2012). If the ΣPBDE and ΣAHFR concentrations of the three groups were all used to analyse the correlation with TL, the results would no longer be significant (p > 0.05). Hence, it is highly possible that the accumulation of HFRs in group two was primarily affected by trophic transfer; correspondingly, TL as a dominant variable can partially explain the concentration variation in HFRs in group two. Significant negative correlations (R = 0.33, 0.36 and 0.33, p < 0.05) between the log-transformed concentrations of BDE-153, BDE-154 and DBDPE and TLs were also found in group two (Fig. S2). Negative but not significant (p > 0.5) relationships were found between other investigated target chemicals and TLs. The limited trophic range of mollusk species may explain the lack of significant relationships for most individual HFRs with trophic position. Sufficient species, including top predators and producers, are needed to further assess biomagnification or dilution. In conclusion, interspecies differences in the accumulation of HFRs in mollusks are affected by a number of factors, including the structure of the food chain, size of the organism, source, and metabolism, and additional influence factors need to be considered (Mizukawa et al., 2013; Roberts et al., 2011). The present study focused on studying the exposure levels of HFRs in different mollusk species from the Bohai Sea and discussing interspecies differences in the bioaccumulation of HFRs. Compared with worldwide data from previous reports performed on mollusks, middleupper levels of HFRs were found in this study. Significant differences in the concentration and composition profiles of HFRs among mollusk species suggested that the accumulation of HFRs exhibited speciesspecific differences. Gastropods showed a relatively high accumulation capability for AHFRs. Although interspecies differences are the result of multifactor interactions, dietary habit, TL and biotransformation ability as the dominant influencing factors can be used to explain the variation in interspecific accumulation upon exposure to PBDEs and AHFRs. However, it could be concluded that HFR accumulation in mollusks is a complicated process and that more influence factors need to be taken into account.

TBPH (5.31% and 5.50%), PBEB (2.99% and 7.36%), and HBB (2.79% and 3.53%) to the total concentration of HFRs in group one were also generally higher than the corresponding proportions in groups two and three. PBDEs were predominant in the last two groups, with proportions ranging from 44.4%–80.3% in group two and 57.9%–91.9% in group three. The proportion of DBDPE increased with species from left to right in group two (Mac, Mer, Mya, Ost, Amu, and Cyc) and group three (Chl, Sca, and Myt), and an opposite trend was found for BDE-209. Notably, relatively high proportions of BDE-100 were found in group three, accounting for 13.1% to 22.1% of total HFRs, which may be related to weak metabolic capability (Roberts et al., 2011; Zhu et al., 2012). Overall, these results indicated significant interspecific differences in the accumulation of HFRs. Further work will focus on the potential impact factors of these differences. As mentioned previously, three different HFR composition profiles were found in the eleven mollusk species. The reasons for these speciesspecific profiles are attempted to be explained by dietary habit, biological metabolism and TL in this study. The value of δ13C in mollusks is consistent with the origin of their dietary carbon and can be applied to identify their dietary source, as described in previous reports (Zhang et al., 2017). In the present study, δ13C ranged from −21.1 to −18.9‰ (Table S3). Significantly lower δ13C depletion was found in gastropods than in bivalves (F = 5.15, p < 0.05), which indicated that there were different feeding sources for gastropods and bivalves. In addition, the feeding strategies of gastropods and bivalves are different. Most predatory gastropods feed on periphyta or feed by detritus grazing or shredding, but most bivalves are filter-feeders (La Guardia et al., 2012). In addition to dietary sources, bioconcentration from sediment and water could be another source pathway of HFRs in mollusks; however, similar water and sediment accumulation factors of HFRs were found in bivalves and gastropods (La Guardia et al., 2012). The source analysis of HFRs suggests that the differences in the concentrations and compositions of HFRs observed in this region between gastropods and bivalves are likely explained by the organisms' dietary habits. BDE-47 and BDE-100 have been found to be resistant to metabolism, and DE-99 can be rapidly metabolized to BDE-47; thus, the ratios BDE99/BDE-47 and BDE-99/BDE-100 can be used to estimate the metabolic potential of organisms (Roberts et al., 2011; Zhu et al., 2012). Speciesspecific differences in the ratios of BDE-99/BDE-47 and BDE-99/BDE100 were observed among the three groups (Fig. 4). Compared with the other two groups, the measured BDE-99/BDE-47 ratios in group three were slightly lower, although the difference was not significant (p > 0.05), indicating that group three has slightly better metabolic transformation of BDE-99 (Fig. 4a). In addition to BDE-47, BDE-49, the metabolite of BDE-99, was also found in three fish species (Roberts et al., 2011). If this metabolic pathway also exists in mollusks, this could be the reason for the lack of a significant difference in the ratio of BDE-99/BDE-47 among the three groups. The average BDE-99/BDE100 ratios of the three groups ranged from 0.8 to 2.2, which are lower than the ratios for DE-71 (3.7) and Bromkal 70-5DE (5.7), which are technical penta-PBDE mixtures (La Guardia et al., 2006). The ratios of BDE-99/BDE-100 in group three were remarkably lower than those in group two (Fig. 4b), suggesting that the bioaccumulation or bioconcentration capacity of BDE-100 or elimination rate of BDE-99 in group three were higher than those in group two (Roberts et al., 2011). Therefore, in addition to source dependence, selective uptake/metabolism is suggested to be the most likely responsible factor for the congener profile of HFRs in Chl, Sca and Myt. The ratio of nitrogen isotopes is usually used to measure TL, which can indicate the trophic positions of marine species (Zhang et al., 2017). The ranges of δ15N and TLs were 6.88–9.28‰ and 2.68–3.30, respectively (Table S3). Significant negative correlations were found between the log-transformed concentrations of ΣPBDE and ΣAHFR and TLs in group two (R = 0.50, p < 0.01; R = 0.32, p < 0.05) (Fig. 5), which indicated ΣPBDE and ΣAHFR underwent trophic dilution in these mollusks (mainly consisting of Veneroida) in this region. The trophic

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