Bioaccumulation and biomagnification of emerging

Science of the Total Environment 598 (2017) 814–820

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Science of the Total Environment journal homepage: www.elsevier.com/locate/scitotenv

Bioaccumulation and biomagnification of emerging bisphenol analogues in aquatic organisms from Taihu Lake, China Qiang Wang a,1, Meng Chen a,1, Guoqiang Shan a, Pengyu Chen a, Shuo Cui a, Shujun Yi a, Lingyan Zhu a,b,⁎ a Key Laboratory of Pollution Processes and Environmental Criteria, Ministry of Education, Key Laboratory of Environmental Remediation and Pollution Control, College of Environmental Science and Engineering, Nankai University, Tianjin 300350, China b College of Natural Resources and Environment, Northwest A&F University, Yangling, Shanxi 712100, China

H I G H L I G H T S

G R A P H I C A L

A B S T R A C T

• The bioaccumulation factors (BAFs) of bisphenol analogues in biota from Taihu Lake were investigated. • Positive relationship between log BAFs and log Kow values observed for bisphenol analogues • The measured log BAFs of bisphenol analogues were in line with the values calculated by EPI Suite model. • Biomagnification of BPAF, BPC and BPZ were observed in food web of Taihu Lake.

a r t i c l e

i n f o

Article history: Received 19 March 2017 Received in revised form 21 April 2017 Accepted 21 April 2017 Available online 27 April 2017 Editor: Jay Gan Keywords: Bisphenol analogues Bioaccumulation Biomagnification Trophic magnification factor

a b s t r a c t Due to regulations on bisphenol A (BPA) in many countries, a variety of bisphenol analogues are being widely manufactured and applied. However, there is a big knowledge gap on bioaccumulation and biomagnification of these emerging bisphenols in aquatic organisms. The bioaccumulation and magnification of nine bisphenol analogues in aquatic organisms at different trophic levels collected from Taihu Lake, China, were evaluated. The total concentrations of the nine bisphenols in the lake waters were in the range of 49.7–3480 ng/L (mean, 389 ng/L). BPA, bisphenol AF (BPAF) and bisphenol S (BPS) were the most predominant analogues in the water. The mean natural logarithm bioaccumulation factor (log BAFs) of BPAF, bisphenol C (BPC), bisphenol Z (BPZ) and bisphenol E (BPE) were greater than BPA, and there was a significantly positive correlation between log BAFs of the biphenols and their octanol-water partition coefficients (log Kow). The trophic magnification factors of BPAF, BPC and BPZ were 2.52, 2.69 and 1.71, respectively, suggesting that they had the potential to biomagnify in the food web. The results of this study call for further investigations on risk assessment of these emerging pollutants in the environment. © 2017 Elsevier B.V. All rights reserved.

1. Introduction ⁎ Corresponding author at: Key Laboratory of Pollution Processes and Environmental Criteria, Ministry of Education, Key Laboratory of Environmental Remediation and Pollution Control, College of Environmental Science and Engineering, Nankai University, Tianjin 300350, China. E-mail address: [email protected] (L. Zhu). 1 The first two authors contributed equally to this work.

http://dx.doi.org/10.1016/j.scitotenv.2017.04.167 0048-9697/© 2017 Elsevier B.V. All rights reserved.

Bisphenol analogues are a group of chemicals with two hydroxyphenyl functional groups and include several compounds such as bisphenol A (BPA), bisphenol B (BPB), bisphenol C (BPC), bisphenol E (BPE), bisphenol F (BPF), bisphenol S (BPS), bisphenol Z

Q. Wang et al. / Science of the Total Environment 598 (2017) 814–820

(BPZ), bisphenol AF (BPAF) and bisphenol AP (BPAP) (Basic information of them are listed in Table S1). Since BPA is a typical endocrinedisrupting chemical (EDC), its production and application in many countries are regulated or limited (Klecka et al., 2009; Delfosse et al., 2012). Other bisphenols, such as BPB, BPE, BPF, BPS, BPAF and BPAP are manufactured as possible alternatives of BPA (Choi, 2013). Among them, BPAF, BPF and BPS are the most extensively applied. The reported annual production of BPAF was approximately 10,000–500,000 lb in the USA during 1986–2002 (Zhang et al., 2013). BPS is produced in massive quantities as a precursor of polycarbonate plastics and epoxy resins and the production volume is 1–10 million pounds in the USA (Kitamura et al., 2005; Environmental Protection Agency, 2012). These emerging bisphenol analogues have been widely detected in various environmental matrices such as water, sediment and indoor dust (Liao et al., 2012a; Liao et al., 2012b; Yang et al., 2014a, 2014b). Elevated detection frequencies and concentrations of BPAF, BPF and BPS have been reported in aquatic environment (Jin and Zhu, 2016); for instance, BPF was the most abundant bisphenol analogue in surface water from some sites in Japan, Korea and China (Yamazaki et al., 2015). BPAF was reported at a concentration (0.9–246 ng/L) similar to that of BPA (6.6–74.6 ng/L) in river water and sediments (0.18–2010 ng/g dry weight, dw) from Hangzhou bay in Zhejiang province, China (Yang et al., 2014a, 2014b). Although these alternatives are thought to be stable and less toxic than BPA, many studies documented that they displayed adverse effects such as estrogenicity (Chouhan et al., 2013; Ji et al., 2013; Rochester, 2013), cytotoxicity (Eladak et al., 2015), genotoxicity (Lee et al., 2013), reproductive and neurotoxicities (Rochester and Bolden, 2015; Shi et al., 2015), which were generally similar to or even greater than BPA (Yamaguchi et al., 2015; Zimmerman and Anastas, 2015; Zhang et al., 2016). A recent study suggested that both BPA and BPS were involved in obesity and steatosis processes, but through two different metabolic pathways (Helies-Toussaint et al., 2014). Some studies reported that BPAF, BPB, BPE, BPS and BPF displayed similar anti-androgenic effect as BPA based on human fetal test (Goldinger et al., 2015; Rochester and Bolden, 2015). It is well known that BPA is not significantly bioaccumulative as compared to classical persistent organic pollutants with a bioaccumulation factor (BAF) in fish in the range of 1.7–182 (Heinonen et al., 2002; Corrales et al., 2015). The low BAF of BPA is partially attributed to its low octanol/water partition coefficient (log Kow 3.32–3.40) (Korenman and Gorokhov, 1973; Staples et al., 1998). The calculated log Kow values of BPAF, BPC and BPZ by U.S. Environmental Protection Agency's Estimation Programs Interface (EPI) Suite software (EPIWEB 4.1) are 4.47, 4.74 and 5.48, respectively, which are much higher than BPA (Chen et al., 2016). It is reported that a chemical with a log Kow N 4.02 may have great bioaccumulation potential (Arnot and Gobas, 2006; Costanza et al., 2012). Thus, it is hypothesized that these alternatives of BPA may be accumulated in a greater extent than BPA. However, most of the current studies focused on the occurrence and distribution of these emerging bisphenols in environmental and human samples (Jin and Zhu, 2016; Liao et al., 2012b; Liao et al., 2012c). A few efforts have been made to examine the bioaccumulation and biomagnification potentials of these compounds in a food web (Shi et al., 2016). Our previous study demonstrated that some bisphenol analogues were widely present in the water and sediments of Taihu Lake, which is the third largest fresh water lake in China (Jin and Zhu, 2016). The objectives of this study were to further investigate bioaccumulation and biomagnification of these compounds in the aquatic food web in Taihu Lake. Water samples and aquatic organisms at different trophic levels were collected in Taihu Lake, China (Fang et al., 2014). Nine widely applied bisphenol analogues (including BPA, BPB, BPC, BPE, BPF, BPS, BPZ, BPAF and BPAP) were measured in these samples. The bioaccumulation and biomagnification potentials of these compounds in the fresh water food web were examined. The results would provide solid evidences to understand the environmental risks of these emerging BPA alternatives.

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2. Materials and methods 2.1. Chemicals and reagents The standards of BPA (purity: 99%), BPS (99.7%) and BPAF (98%) were purchased from Tokyo Chemical Industry Co. Ltd. (Tokyo, Japan). 13 C12-BPA was obtained from Toronto Research Chemicals Inc. (Ontario, Canada). The standard solution of BPF (99.9%) was purchased from Dr. Ehrenstorfer GmbH (Germany). The standard solutions of BPAP (99%), BPB (98.4%), BPC (99.9%), BPE (99%) and BPZ (98%) were all purchased from J & K Co. (Beijing, China). Methanol, acetonitrile and hexane (HPLC grade) were obtained from Tianjin Concord Technology Co., Ltd. (Tianjin, China). HC-C18 SPE (500 mg/6 mL) cartridges were obtained from ANPEL scientific instrument Co., Ltd. (Shanghai, China). The stock solutions of nine types of bisphenols and 13C12-BPA were prepared at 1000 mg/L in methanol and stored at −20 °C. A series of working solutions were prepared by diluting the stock solutions with methanol prior to use. Milli-Q water was used throughout the sample treatment process. 2.2. Sample collection and preparation Water samples were collected from Taihu Lake, China, in May 2015. Thirty-one sites (T1–31) in Taihu Lake were selected according to the guidelines of National Environmental Monitoring Program of China (Fig. S1). Previous studies indicated that Meiliang bay was the most polluted area in the lake (Yang et al., 2011; Lu et al., 2011; Wang et al., 2015a, 2015b). Thus, biota samples were collected at Meiliang bay with the assistance of local fisherman. Phytoplankton, zooplankton, invertebrates [including lobster (n = 10), snail (n = 30) and white shrimp (n = 30)], fish [including anchovy (n = 20), carp (n = 8), catfish (n = 10), Chinese bitterling (n = 10), crucian (n = 15), gobies (n = 15), minnows (n = 15), mud fish (n = 10), parva (n = 20), snake fish (n = 10), trash fish (n = 20) and whitebait (n = 30)] were collected. The species names, feeding habitat, sample numbers, water content, δ13C (‰) andδ15N (‰) of the organisms are presented in Support Information (Table S2). All bottles and sampling equipment used during the sampling were rinsed with methanol and Milli-Q water before each sampling in order to minimize contamination. The water samples were stored in polypropylene (PP) bottles at 4 °C for one day, and biota samples were stored at −54 °C until pretreatment. 2.3. Water sample extraction Two liters of water was filtered through a glass fiber filter (142 mm, pore diameter 0.7 mm, Millipore Corp. USA), which was combusted at 450 °C for 5 h before filtration and weighed, to get the dissolved phase. After filtration, the filter was freeze-dried and weighed and the suspended particulate matter (SPM) content remaining on the filter was determined. For the dissolved water phase, 500 mL of the filtered water was spiked with 20 ng of internal standard (13C12-BPA) and then passed through the HC-C18 solid phase extraction cartridge (500 mg/6 mL). Prior to extraction, the cartridge was preconditioned with 10 mL of methanol followed by 10 mL of HPLC grade water. The sample was loaded on the cartridge at approximately 1–2 drop per second. After loading, the cartridge was washed with 10 mL of 5% methanol/water and pumped dry. The target analytes were eluted into a new PP tube with 10 mL of methanol (0.1% ammonia). For the SPM samples, the glass fiber filter was cut into small pieces (0.5 cm × 0.5 cm), and put into a 50 mL PP tube. It was spiked with 20 ng of internal standard (13C12-BPA) and equilibrated for 2 h. Then 20 mL of methanol (HPLC grade) was added. The mixture was slowly vortexed for 5 min, and shaken in an orbital shaker at 250 rpm for 30 min. After that, ultrasonic extraction continued for 30 min, followed by centrifugation at 8000 rpm

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Fig. 1. Compositional profiles of the nine bisphenols in the surface water samples (a) and aquatic organisms (b) in Taihu Lake, China.

for 20 min. The supernatant was transferred into a new 50 mL PP tube. The extraction was performed twice with methanol, and the supernatants of the two extractions were combined. The procedure of SPE extraction was according to the water treatment. The concentration of individual bisphenol analogues in one water sample was the sum of dissolved phase and SPM.

performed two more times, and the supernatants were combined. The extract was diluted to 500 mL with HPLC grade water, which was then followed by SPE extraction as the water samples. The eluent was volatilized to dryness under a gentle nitrogen stream and then reconstituted with 0.5 mL methanol for analysis by ultra-performance liquid chromatography tandem mass-spectrometry (UPLC-MS/MS).

2.4. Aquatic organism pretreatment

2.5. Instrumental analysis

The aquatic organism samples were freeze-dried, and extracted according to the method described elsewhere (Liao et al., 2012c), but with some modifications. One gram of dry sample (fortified with 20 ng of the internal standard 13C12-BPA) was mixed with 1 mL of 1 M ammonium acetate buffer (pH 5.0; 7.71 g of ammonium acetate dissolved in 93.4 mL of Milli-Q water and 6 mL of acetic acid with 600 μL of β-glucuronidase) in a 15 mL PP centrifuge tube, and then slowly vortexed for 5 min. The mixture was incubated at 37 °C for 20 h. Six milliliters of methanol/water (50:50 v/v) was then added to the centrifuge tube, which was slowly vortexed for 5 min, shaken in an orbital shaker at 250 rpm for 30 min and ultrasonically extracted for 30 min. The sample mixture was centrifuged at 6000 rpm for 10 min, and the supernatant was decanted to a clean 15 mL tube. This procedure was

The bisphenols in the samples were measured by ultra-performance liquid chromatography tandem mass-spectrometry (UPLC-MS/MS). The details about the running conditions and optimized parameters of UPLC-MS/MS are provided in Table S3. 2.6. Stable isotope determination Stable-nitrogen (δ15N) is often used to determine trophic level (TL) due to its stable enrichment in food web. The increment of stablecarbon (δ13C) is so small (about 1‰ enrichment with each increasing TL) that it is generally employed to analyze the diet composition and carbon source of the organisms (Fang et al., 2014). Details regarding δ15N and δ13C analysis are provided in the SI (Fig. S2). Theδ13C (‰) in

Q. Wang et al. / Science of the Total Environment 598 (2017) 814–820 Table 1 Calculated physicochemical properties of the bisphenol analogues using EPIWEB 4.1. Analytes

Molecular weight

Log Kow

Log BAF

BPA BPAF BPC BPZ BPE BPF BPS BPB BPAP

228.29 336.23 256.34 268.35 214.26 200.23 250.27 242.32 290.36

3.64 4.47 4.74 5.48 3.19 3.06 1.65 4.13 4.86

1.86 2.62 2.79 3.28 1.77 1.59 0.75 2.39 2.87

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A TMF value between 0 and 1 indicates that the contaminant is not biomagnified, while TMF N 1 indicates that the contaminant biomagnifies in the food chain. 2.8. Statistical analysis Pearson correlation analysis was performed to assess the correlations between the TLs and concentrations of the bisphenols in biota. Statistical analysis was performed using Origin Version 9.0 and SPSS Version 17.0. 3. Results and discussion

the organisms overlapped each other, indicating that some organisms had a common carbon source, and were prey-predator relationships (Fang et al., 2014). 2.7. Data analysis Trophic levels (TLs) were determined based on the results of δ15N using Eq. (1) reported by Fisk et al. (2001). TLs were determined for individual species based on zooplankton, which is assumed to occupy TL of 2, according to the following relationship: TLconsumer ¼ 2 þ δ15 Nconsumer −δ15 Nzooplankton =3:8

ð1Þ

The bioaccumulation factor (BAF) is defined mathematically as the concentration of a chemical in an organism (wet weight basis) divided by its concentration in water, was calculated according to the following equation: BAF ¼ Cbiota =Cwater

ð2Þ

Cbiota: bisphenol (BP) concentration in biota, ng/kg wet weight; Cwater: BP concentration in water, ng/L. The trophic magnification factors (TMFs) were calculated based on the relationship between TLs and the concentrations of individual compounds according to a method reported in previous studies (Martin et al., 2004; Tomy et al., 2004). lnCbiota ¼ a þ ðb TLÞ

ð3Þ

Using the slope b of Eq. (3), a TMF was calculated as follows: TMF ¼ eb

ð4Þ

Fig. 2. Box diagram of the log BAFs of the most detected seven bisphenols in the aquatic organisms collected from Meiliang Bay of Taihu Lake.

3.1. Occurrence of bisphenol analogues in the surface water of Taihu Lake The target bisphenol analogues (including BPA, BPB, BPC, BPE, BPF, BPS, BPZ, BPAF and BPAP) were measured in the water samples, including the dissolved phase and SPM. The concentrations of the total bisphenols ranged from 49.7 to 3480 ng/L with mean of 389 ng/L (Fig. S3). BPA, BPAF and BPS were identified in all the samples. Other bisphenols (BPC, -F, -Z -E) were detected with frequency of 87.1, 87.1, 83.9 and 58.1%, respectively. BPB and BPAP were not detected in any of the water samples. The mean proportion of each compound in the total bisphenols was 43.3% for BPA, 36.7% for BPAF, 13.2% for BPS, 5.27% for BPZ, 0.71% for BPF, 0.53% for BPC and 0.33% for BPE (see Fig. 1a). The most predominant three compounds, BPA, BPAF and BPS, totally accounted for mean 93.2% of total bisphenols in the water samples. This profile of bisphenol analogues in lake water is consistent with that reported previously by Jin and Zhu (2016). The results suggested that BPA was still the most widely manufactured, but BPAF and BPS were also largely applied in China (Rochester and Bolden, 2015; Delfosse et al., 2012). The BPA concentrations in Taihu lake ranged from 22.9 to 3360 ng/L, which was comparable to those in Jialu River (410–2990 ng/L), Ningbo River (13.6–3337 ng/L) and Jiulongjiang River (0.5–4687 ng/L) in China (Zhang et al., 2011; Zhang et al., 2012; Wang et al., 2015a, 2015b), but much higher than that from Elbe River (17–776 ng/L) in Germany (Heemken et al., 2001), Jarama River (87–126 ng/L) in Spain (Esteban et al., 2014) and Kaveri River (6.6–136 ng/L) in India (Selvaraj et al., 2014). Information on the environmental occurrence of the emerging bisphenols is limited, and only a few studies reported their concentrations in natural waters. Jin and Zhu (2016) reported that the concentrations of BPS and BPAF in Taihu Lake (sampling in September 2013) were 6.0 and 0.28 ng/L, which were much lower than our results: BPS (mean:

Fig. 3. Relationship between the mean log BAFs of the bisphenols and the estimated log Kow by EPI Suite model.

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Fig. 4. Plot of ln C (bisphenol concentrations, ng/g ww) in individual organisms versus their trophic levels. Solid line represents ln-linear regression of concentration-TL relationship over the entire food web.

27.6 ng/L) and BPAF (140 ng/L). One possible reason was that Jin et al. did not measure the compounds in SPM. In this study, the mean contribution of the SPM-bound bisphenols to the total water concentrations was in the range of 2.52–53.6%. Therefore, although SPM was accounted in the total water concentrations, the levels of the bisphenols reported by Jin et al. were still much lower than this study. This may suggest that the release of these compounds to the environment of the studied region is increasing. However, the concentrations of BPS and BPAF were much lower than those from the Pearl River, China (BPS: 135 ng/L), Cooum River, India (BPS: 768 ng/L) (Yamazaki et al., 2015), Hangzhou bay (BPAF: 246 ng/L) in China (Yang et al., 2014a, 2014b). For BPF, its concentration (4.12 ng/L) was lower than those from West River,

Fig. 5. Plot showing relationship between the observed TMFs and log Kow.

China (64 ng/L), Arakawa River, Japan (79 ng/L), and Han River, Korea (633 ng/L) (Yamazaki et al., 2015). These results indicated that the contamination of these emerging bisphenols in the studied region is lower than other areas, but might be in an increasing trend. 3.2. Distribution of bisphenol analogues in the aquatic organisms The concentrations of total bisphenols in the organisms ranged from 1.69 (phytoplankton) to 35.2 ng/g (Parva) wet weight (WW), with a mean concentration 18.5 ng/g WW (Fig. S4). BPA (0.220–14.5 ng/g ww), BPAF (0.179–23.8 ng/g ww) and BPZ (0.175–2.87 ng/g ww) were detected in all of the biota samples. The detection frequency of other bisphenols was in the following order: BPE, 94.1%; BPC, 88.2%; BPF, 82.4%; BPS, 70.6%; BPB, 64.7% and BPAP, 47.1%. The mean proportion of each compound in the total bisphenols was 35.2% for BPA, 25.8% for BPAF, 25.4% for BPC and 9.70% for BPZ, 1.70% for BPE, 1.19% for BPF and 0.34% for BPS (Fig. 1b). As compared to the compositional profile in the water samples, higher detection frequencies and relatively higher contributions of BPAF, BPC and BPZ were observed in the biota samples. The results suggested that BPAF, BPC and BPZ could have higher bioaccumulation potentials than other bisphenols. The bioaccumulation ability of a chemical is related to its properties such as hydrophobicity (log Kow) (Mayer and Reichenberg, 2006; Wen et al., 2012; Mackay et al., 2013). There is very sparse information about measured log Kow values of the emerging bisphenols. Thus, EPI Suite model was used to estimate the log Kow values of the target compounds (Table 1). The estimated log Kow of BPA (3.64) was similar to the measured values (3.32–3.40) (Korenman and Gorokhov, 1973; Staples et al., 1998), suggesting that the estimated values are reasonable. In this study, the target compounds were separated on an ACQUITY UPLC BEH column, which is a hydrophobic reverse phase column. It is possible to predict the hydrophobicity based on their elution order from the column. The bisphenol analogues were eluted in the following order: BPS,


BPF, BPE, BPA, BPAF, BPC, BPZ, with those compounds with greater hydrophobicity eluting later. The elution order of the bisphenols was in agreement with their estimated log Kow values, suggesting that BPAF, BPC and BPZ have greater hydrophobicity than BPA. The natural logarithm of bioaccumulation factors (log BAFs) were calculated for the seven most frequently detected bisphenols, including BPA, BPAF, BPC, BPE, BPF, BPS and BPZ, based on their mean water concentrations in Meiliang bay, and the results are listed in Table S4 and Fig. 2. The mean log BAFs of BPAF, BPC, BPZ and BPE were higher than that of BPA. Fig. 3 illustrates that there was a significantly positive correlation (r = 0.924, p b 0.05) between the mean log BAFs of the bisphenols and their estimated log Kow values. This is in line with a previous study which reported that the log BAFs of 646 chemicals in fish positively correlated with their log Kow (Arnot and Gobas, 2006). These results suggested that hydrophobicity is the principal driving force for bioaccumulation of bisphenol analogues in biota (Wen et al., 2012). 3.3. Trophic magnification of the emerging bisphenols in the aquatic food web

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current investigations on bisphenol analogues, and greatly limit our capacity for assessing their sources, fate regionally or globally, as well as the associated human exposure pathways and risks. Thus, additional field and laboratory-based researches are critically needed in order to comprehensively assess their environmental and ecological risks. Associated contents Operation conditions of UPLC/MS/MS, stable isotope determination, quality assurance and quality control and tables giving the physical and chemical properties parameters of nine bisphenols, information on biological samples of Taihu Lake, the optimized LC-MS/MS parameters, the log BAFs of the bisphenols in the aquatic organisms collected from Taihu Lake, figures illustrating the sampling sites of water samples in Taihu Lake of China, mean (± SD) δ15N (‰) and δ13C (‰) of potential food sources and consumers in Taihu Lake, concentrations of nine bisphenols in the water and aquatic organisms in Taihu Lake. Acknowledgments

Linear regression was used to evaluate the association between the TLs and ln concentrations (ln C) of the seven most frequently detected bisphenol compounds, including BPA, BPAF, BPE, BPC, BPF, BPS and BPZ, in all the aquatic organisms at different TLs. Strong positively linear relationship was observed between the ln C and TLs (p b 0.05) for BPAF, BPC and BPZ, which were also observed to display great bioaccumulation potentials. Such correlations were not observed to BPA, BPE, BPF and BPS. Consistently, a previous study demonstrated that BPA was not biomagnified in a food web in Yangtze River Delta area, China (Gu et al., 2016). Therefore, TMFs were calculated for these three compounds, and they were all N 1 (TMF = 2.52 for BPAF, 2.69 for BPC and 1.71 for BPZ), indicating that BPAF, BPC and BPZ are biomagnified in the aquatic food web of Taihu Lake (Fig. 4). Thus, it is very possible for them to enter human body through consuming food. Many previous studies documented these emerging BPA alternatives displayed numerous toxic effects to wildlife and humans, even greater than BPA (Matsushima et al., 2010; Vandenberg and Catanese, 2014). Therefore, it is very plausible that these emerging BPA alternatives have significant ecological risks, considering that their bioaccumulation capacity and toxicities. Since information about the TMFs of the emerging bisphenols is sparse, they were compared to the TMFs of polychlorinated biphenyls (PCBs) and polybrominated diphenyl ethers (BDEs), which also contain two benzene rings. The TMFs were reported to be in the range 0.26–4.7 for PBDEs and 1.46–6.63 for PCBs in different food webs (Houde et al., 2008; Kelly et al., 2008; Losada et al., 2009; Wu et al., 2009; Yu et al., 2009; Hu et al., 2010). The TMFs of BPAF, BPC and BPZ were similar to those of 4–7 brominated BDE congeners and three chlorinated PCBs, but much lower than higher chlorinated PCBs. Fig. 5 illustrates a curvilinear relationship (r = 0.681, p b 0.05) between the TMFs of organic contaminants (including bisphenols, BDEs, PCBs) versus their log Kow values (Yu et al., 2009; Hu et al., 2010; Walters et al., 2011; Fang et al., 2014; Kobayashi et al., 2015). It indicates that the TMFs of the compounds increased as the log Kow values were b~7, and decreased thereafter (Vidal-Linan et al., 2015). This bell trend was also observed in previous studies (Kelly et al., 2009; Yu et al., 2012). 4. Conclusions The results in this study indicated that some of these BPA alternatives (BPAF, BPC, BPZ) have great potentials to be accumulated in aquatic organisms and then biomagnified along freshwater food chains. Significant positive relationships were found between BAFs of most bisphenol analogues and their log Kow values. The correlation between the TMFs and log Kow suggested that chemical properties of contaminants have profound effects on their trophic transfer in freshwater food chain. However, knowledge gaps remain in many aspects of

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