Perfluoroalkyl Substances in the Riverine and Coastal Water of The

Science of the Total Environment 660 (2019) 297–305

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Science of the Total Environment

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Perﬂuoroalkyl substances in the riverine and coastal water of the Beibu Gulf, South China: Spatiotemporal distribution and source identiﬁcation

Chang-Gui Pan, Ke-Fu Yu ⁎, Ying-Hui Wang ⁎, Wei Zhang, Jun Zhang, Jing Guo

Guangxi Laboratory on the Study of Coral Reefs in the South China Sea, Guangxi University, Nanning 530004, China Coral Reef Research Center of China, Guangxi University, Nanning 530004, China School of Marine Sciences, Guangxi University, Nanning 530004, China

HIGHLIGHTS GRAPHICAL ABSTRACT

• A comprehensive survey of PFASs in the Beibu Gulf, China, is reported. • Total PFASs concentrations ranged from 610 to 4920 pg/L in the Beibu Gulf. • PFPeA and PFBA were the dominant PFASs compound, rather than PFOA and PFOS. • The distribution of PFASs was strongly affected by ocean currents. • PFASs would represent a low risk to the aquatic organisms in the Beibu Gulf.

article info abstract

Article history: Few studies have examined the perfluoroalkyl substances (PFASs) contamination in less-developed coastal re- Received 4 November 2018 gions. In the present study, we collected 19 riverine and 21 coastal surface water samples in the summer and win- Received in revised form 3 January 2019 ter of 2017 to investigate PFASs contamination in the Beibu Gulf, South China. The results show that eleven and Accepted 3 January 2019 twelve target PFASs were detected in the summer and winter, respectively. The total PFASs (ΣPFASs) concentra- Available online 04 January 2019 tions in the water of the Beibu Gulf were in the range of 1609–4727 pg/L and 610–4920 pg/L in summer and win- fl fl fl Editor: Yolanda Picó ter, respectively. Per uoropentanoic acid (PFPeA), per uorobutanoic acid (PFBA) and per uorobutane sulfonate (PFBS) were the predominantly detected PFASs in both seasons with maximum concentrations of 2968 pg/L, Keywords: 1771 pg/L, and 1764 pg/L, respectively. Strong positive correlations between some PFASs were observed Perfluoroalkyl substances (PFASs) (e.g., PFBA and PFBS, PFOS and PFBS, p b 0.05), suggesting these correlated pollutants may share similar sources. Perfluorobutane sulfonate (PFBS) PFASs contamination in the Beibu Gulf was strongly affected by ocean currents, and their concentrations were Beibu Gulf lower than most coastal waters around the world. Risk assessment indicates a low risk associated with target Riverine water PFASs to aquatic organisms in the Beibu Gulf. The results of the present research provided a baseline and good Coastal water overview of the spatial distribution of PFASs along the Beibu Gulf. Risk assessment © 2019 Elsevier B.V. All rights reserved.

⁎ Corresponding authors at: Guangxi Laboratory on the Study of Coral Reefs in the South China Sea, Guangxi University, Nanning 530004, China. E-mail addresses: [email protected], [email protected] (K.-F. Yu), [email protected] (Y.-H. Wang).

1. Introduction area, such as Bohai Sea (Zhao et al., 2017), Hong Kong surface seawater (Kwok et al., 2015), and Tokyo bay (Yamashita et al., 2005). Currently, Perfluoroalkyl substances (PFASs), such as perfluoroalkyl carboxylic there is no information on PFASs contamination in the Beibu Gulf, a acids (PFCAs) and perfluoroalkyl sulfonates (PFSAs), have aroused less-developed region. Also, because of the regulation of a few long- widespread concern. They are comprised of a hydrophobic alkyl chain chain PFASs (e.g., PFOS and PFOSF), their alternatives (e.g., short-chain of variable length (typically C4-C14) and a hydrophilic end group. PFASs) are likely to be more prevalent in the environment. However, PFASs represent a large group of man-made chemicals used in a wide it is unclear regarding the changing trends between short-chain and range of consumer and industrial products, including firefighting long-chain PFASs in the environment. In order to better understand foams, adhesives, aerospace, paper packaging, cookware and electron- the occurrence and sources of PFASs in the Beibu Gulf, it is required to ics, for more than six decades due to their surface-active properties, perform a systematic investigation of PFASs contamination in this area. high chemical and thermal stability (Giesy and Kannan, 2002; The aim of the present study was to investigate the spatiotemporal Lindstrom et al., 2011; Prevedouros et al., 2006). Perfluoroalkyl acids distribution of PFASs in riverine and coastal waters of the Beibu Gulf. Ac- (PFAAs) including PFCAs and PFSAs, are not readily degradable under cordingly, potential sources of PFASs were elucidated. Changing trends nature environmental conditions, whereas many of their precursors between short-chain and long-chain PFASs were also evaluated. In addi- can transform into PFAAs and other intermediates via biotic and/or abi- tion, a preliminary risk assessment was performed to determine the po- otic degradation (Harding-Marjanovic et al., 2015; Li et al., 2019; Mejia- tential risk of PFASs for aquatic organisms in this region. Avendaño et al., 2016; Moe et al., 2012). Particularly, long-chain PFAAs ≥ (PFCAs with carbon chain length C 8 and PFSAs with carbon chain 2. Material and methods length C ≥ 6) have shown strong bioaccumulation and biomagnification in biota samples (Chen et al., 2018; Munoz et al., 2017). Furthermore, 2.1. Chemicals and reagents there is evidence that exposure to perfluorooctane sulfonate (PFOS) can lead to various adverse effects, such as hepatotoxicity, neurotoxicity A total of 18 target PFASs, including 11 PFCAs, 5 PFSAs, and developmental toxicity (Briels et al., 2018; Han et al., 2018; Yuan perfluorooctane sulfonamide (FOSA) and N‑ethylperfluorooctane et al., 2018). Efforts have been made towards phasing out production sulfonamidoacetic acid (EtFOSAA) were investigated in this study. Six of PFOS since 2000. For example, Minnesota Mining and Manufacturing 13 13 13 13 isotope-labeled standards ( C4-PFBA, C2-PFHXA, C4-PFOA, C2- (3 M) Company ceased production of most of PFOS and 18 13 PFDA, O2-PFHXSand C4-PFOS) were used as internal standards fl fl per uorooctanesulfonyl uoride (POSF)-based chemicals in 2000 (ISs) for quantification. Details on the chemicals and reagents are pro- fl (Yeung et al., 2006). In 2009, PFOS and its precursor per uorooctane vided in the text and Table S1 in Supplementary material (SM). sulfonyl fluoride (PFOSF) were added to the annex B of the Stockholm Convention on persistent organic pollutants (POPs), resulting in global 2.2. Sample collection and sample extraction restriction of their production and use (UNEP, 2009). Furthermore, the Stockholm Convention recently recommended PFOA to be listed as a The study area comprised rivers and nearshore waters along the persistent organic pollutant (UNEP, 2015). However, they are still fre- coast of the Beibu Gulf (Fig. 1). We collected duplicate surface water quently detected in the environment (Benskin et al., 2012; Wan et al., samples (0.5 m depth) on the boat using a water sampler at forty river- 2017). ine and coastal sites in the August (summer) and December (winter) in Due to the incomplete removal in conventional wastewater treat- 2017. Samples were collected on sunny or cloudy days (also before sam- ment plants (WWTPs) (Pan et al., 2016), PFASs would be discharged pling campaigns) to avoid the interference of rain. Water quality param- to aquatic environment via WWTP effluents. Consequently, PFASs are eters, including salinity and pH, are provided in Table S2. The collected ubiquitous in waters (Gonzalez-Gaya et al., 2014; Pan et al., 2014a), sed- water samples (1 L) were stored in high density polyethylene (HDPE) iment (Gomez et al., 2011; Pan et al., 2014b), wildlife (Li et al., 2008; Pan containers with narrow mouths and screw tops previously washed et al., 2018) and humans (Yeung et al., 2008; Zhang et al., 2013) with tap water, Milli-Q water, methanol, and water from the specific throughout the world. The biogeochemistry and long-range transport sampling site. The water samples were placed in a cooling box and of PFASs depend largely on their physicochemical properties. Because transported to the laboratory immediately, then filtered using glass of the carboxylic/sulfonic acid groups, PFCAs and PFSAs are highly mo- fiber filters once arriving at the laboratory, stored at 4 °C in darkness bile and less volatile in the aqueous systems compared with legacy per- and extracted within three days. Filtrated water samples were extracted sistent organic pollutants (POPs), such as polychlorinated biphenyls using solid phase extraction method with WAX Cartridges, which have (PCBs) and poly brominated diphenyl ethers (PBDEs) (Kissa, 2001). As been used and validated in our previous paper (Pan et al., 2016). De- a result, marine waters become a final sink or the most important reser- tailed information of water extraction procedure is presented in the SM. voir for PFASs (Taniyasu et al., 2005; Yamashita et al., 2008). PFASs have been proposed as an excellent tracer of global circulation of marine waters due to their persistency and high water solubility (Yamashita et al., 2.3. Instrumental analysis 2008). Generally, PFASs have been detected at levels ranging from hundreds of pg/L to hundreds of ng/L in coastal regions around the world Concentrations of PFASs were determined using an Agilent 1290 depending on the sites and the compounds (Ahrens et al., 2009a, ultra-performance liquid chromatography (UPLC) system interfaced 2010; So et al., 2004; Zhu et al., 2017). with an Agilent 6460 triple quadrupole mass spectrometer (Agilent The Beibu Gulf (northwest of South China Sea), ranges from Leizhou Technologies, Santa Clara, CA) equipped with a Jetstream electrospray Peninsula, Qiongzhou Strait and Hainan Island to Vietnam, and has a ionization (ESI) source in the negative mode. Full details on instrument population of over 20 million people. It has traditionally been playing parameters are provided in the SM. an important role in the economic development of China and Vietnam through providing a highly productive and diverse marine products re- 2.4. Quantification and quality assurance/quality control (QA/QC) source. Several cities in the Beibu Gulf, such as Nanning, Haikou, Zhanjiang, Qinzhou, Fangchenggang and Beihai, have experienced Quantification of the target PFASs was acquired using a dilution of rapid economic growth in the past decades. Also, there are a large num- standards and constant internal standards in pure methanol (internal ber of estuaries that may be subjected to PFASs contamination in the standard method). An eight-point calibration curve (0.1, 0.2, 0.5, 1, 2, Beibu Gulf. However, previous monitoring studies of PFASs in the 5, 10 and 20 ng/mL) was used to calculate PFAS concentrations. Qualifi- coastal waters in the world have mainly focused on the developed cation of the target PFASs was accomplished by comparing the retention C.-G. Pan et al. / Science of the Total Environment 660 (2019) 297–305 299

Fig. 1. Distribution of sampling sites in the Beibu Gulf. time and the signal ratio of the two selected transitions (precursor- than LODs were treated as zero, levels between LODs and LOQs were product ions, if available) with the standards. assigned as half of the respective LOQ value. To examine potential corre- Quality assurance/quality control procedures were strictly followed lations among various PFASs in water samples, we also performed cor- during the whole procedure, including sampling, extraction and instru- relation analyses. Because concentration data did not follow normal mental analysis. Neither fluorinated materials (e.g., Teflon) nor glass- distribution in the Kolmogorov-Smirnov test, we used spearman rank ware were used during the sampling and analysis, to minimize correlation analysis. To characterize the similarity among PFASs or sam- contamination of the samples or to avoid irreversible adsorption of pling sites, heat map-hierarchical cluster analysis (HM-HCA) was con- some PFASs (Moody and Field, 1999). Recovery of spiked sample, limit ducted using the package ComplexHeatmap (Gu et al., 2016). All of detection (LOD), limit of quantification (LOQ), and laboratory blanks statistical analyses were performed with SPSS (Version 22.0, SPSS Incor- were measured. The LOQ and LOD were defined as a signal to noise ratio porate) except for HM-HCA which was performed using the R software. (S/N) of 10 and 3 based on the lowest signal of the transitions, respec- The significance level was set at p = 0.05 using a 95% confidence level. tively. They ranged from 13 to 83 pg/L and 4–25 pg/L, respectively. See Table S3 for details of recoveries, LODs and LOQs of individual 3. Results and discussion PFASs in the water phase. All PFASs in the laboratory blank were less than their corresponding LODs. Blanks and control samples were run 3.1. Occurrence and composition profiles of PFASs in rivers every 8 samples to check any carryover, background contamination, and instrumental drift. There were 11 and 12 out of the 18 targeted PFASs found in riverine water samples (sites: R1-R19) from the Beibu Gulf in the summer and 2.5. Ecological risks assessment winter, respectively. The detailed concentrations and detection frequencies of individual PFASs in both seasons are shown in Fig. 2, The potential ecological risks associated with PFASs were evaluated Tables 1, S4, and S5. The total PFASs concentrations were in the range by comparing the measured environmental concentrations (MECs) of 1609–4583 pg/L with a mean value of 2964 pg/L in the summer and with guideline values for protecting aquatic organisms. Accordingly, 610–4523 pg/L with a mean value of 3278 pg/L in the winter. In the the risk quotient (RQ) was determined as the ratio of MEC to the pre- Fancheng River, in both seasons the concentration of ∑PFASs increased dicted no effect concentration (PNEC), to assess the potential ecological greatly from R1 to R3, suggesting the existence of PFASs sources input in risks of PFASs in aquatic environment. To further illustrate the risk levels this region. However, in the remaining four rivers (Maoling River, Qin of PFASs in the Beibu Gulf, ecological risks were divided into three River, Dafeng River and Nauliu River), there was no obvious changes levels: minimal risk (b0.1), medium risk (0.1–1), and high risk (N1) of ∑PFASs concentrations or compositional profile, which indicates (Yan et al., 2013). the absence of substantial inputs of ∑PFASs in these regions. The PFASs with carbon chain length less or equal to eight (C ≤ 8, PFBA, 2.6. Statistical analysis PFPeA, PFBS, PFHxA, PFHpA, PFHxS, PFOA and PFOS) showed much higher detection frequencies (100%) than those PFASs with carbon All experiments were performed in duplicate. Concentrations of chain length more than eight (C N 8, PFUnDA, PFDS, PFDoDA, PFTrDA PFASs were presented as mean value. While PFASs concentrations less and PFTeDA, 0–36.8%) (Table 1). This can be explained by their large- 300 C.-G. Pan et al. / Science of the Total Environment 660 (2019) 297–305

Fig. 2. Concentrations (ng/L) of individual PFASs in the surface water from rivers (R1-R19) and the coastal area (C1-C21) of the Beibu Gulf, China, during the summer and winter of 2017. Note: R1-R3 are located in Fangcheng River; R4-R6 are located in Maoling River; R7-R9 are located in Qin River; R10-R12 are located in Dafeng River; R13-R19 are located in Nanliu River. scale use and high solubility. Furthermore, PFBA, PFPeA, PFBS and PFOA However, in recent years, more and more studies reported the preva- were the predominant compounds in the riverine water. PFBA had con- lence of short-chain PFASs (Pan et al., 2016; Wei et al., 2018). For exam- centrations in the range of 252–1771 pg/L and 261–1265 pg/L in the ple, Wei et al. (2018) reported that concentrations of short-chain PFASs summer and winter, respectively. The concentrations of PFPeA ranged (e.g., PFPeA and PFBS) were approximately three times higher than from 140 to 1362 pg/L in the summer and from 49 to 1968 pg/L in the those of long-chain PFASs (e.g., PFOS) in surface water collected from winter. For the PFBS, it should be noted that the Nanliu River had high Jiangsu Province (China). This can be partly attributed to the increasing concentrations of PFBS (mean value = 1336 pg/L, Fig. 2) in the winter. production and use of short chain PFASs that were introduced after the This could be attributed to the increasing production and use of PFBS, restricted use of long-chain PFASs. These results indicate that the emis- a substitute for PFOS, in the Nanliu river basin (Kwok et al., 2015). sions of long-chain PFASs gradually decreased whereas short-chain In the present study, the concentrations of short-chain PFASs PFASs became more prevalent in the environment. For example, the (e.g., PFBA, PFPeA and PFBS) were much higher than long-chain PFASs. concentration of PFBS (a short-chain alternative to PFOS) was generally This is contrary to most previous studies performed several years ago one order of magnitude higher than that of PFOS in water samples col- when long chain PFASs (generally PFOA and PFOS) were predominant lected from a wastewater treatment plant in Guangzhou, South China PFASs (Ahrens et al., 2010; Chen et al., 2011; Yamashita et al., 2005). (Pan et al., 2016). C.-G. Pan et al. / Science of the Total Environment 660 (2019) 297–305 301

Table 1 PFASs concentrations (pg/L) and detection frequencies (DF, %) in the surface water from the Beibu Gulf.

PFAS Riverine water Coastal water

Summer Winter Summer Winter

Min Max Mean Median DF Min Max Mean Median DF Min Max Mean Median DF Min Max Mean Median DF

PFBA 252 1771 965 906 100 261 1265 758 790 100 735 1304 937 916 100 343 836 506 489 100 PFPeA 140 1362 510 430 100 49 1968 512 438 100 118 2323 863 803 100 180 2968 658 496 100 PFHxA 68 313 184 188 100 33 434 194 179 100 178 1001 301 272 100 94 319 184 170 100 PFHpA 77 390 231 227 100 62 428 206 182 100 134 350 216 205 100 113 259 156 149 100 PFOA 139 636 353 364 100 132 1046 466 450 100 441 843 544 525 100 230 589 411 380 100 PFNA 113 320 225 222 100 nd a 402 175 168 95 76 334 148 141 100 34 109 66 63 100 PFDA 66 121 87 85 100 28 143 55 47 100 51 252 77 67 100 nd 173 30 29 67 PFUnDA nd 54 14 nd 32 nd 133 14 0 37 nd 51 19 26 52 nd nd nd nd 0 PFBS 66 313 184 188 100 41 1764 583 186 100 147 280 207 212 100 141 557 201 186 100 PFHxS 58 247 108 93 100 nd 151 65 70 79 105 247 156 152 100 nd 180 102 124 81 PFOS nd 181 110 119 89 nd 487 240 225 95 49 281 123 110 100 nd 369 161 152 90 FOSA nd nd nd nd 0 nd 31 10 0 47 nd nd nd nd 0 nd 19 1 0 5 ΣPFASs 1609 4583 2964 3068 100 610 4523 3278 3592 100 2831 4727 3592 3496 100 1937 4920 2475 2239 100

a nd represents not detected.

The profiles of relative concentrations of the detected PFASs in the (Paul et al., 2009; Sanchez-Avila et al., 2010). Further, the discharges surface water in both seasons are displayed in Fig. S1. Although there of wastewater around site C6 might be an additional source. was a similarity of PFASs composition between the two seasons, the Same as the composition profiles of PFASs in the riverine water, contributions of PFBS to the ∑PFASs varied among sampling sites in PFBA and PFPeA were the predominant PFASs with a similar average both seasons. PFBA (15.7–49.7%) and PFPeA (1.5–60.3%) showed the contribution (24%) to the total PFASs, followed by PFOA (16%) in the greatest average contributions to ∑PFASs, followed by other PFASs coastal water. Other PFASs showed much less or no contribution to with shorter chains, such as PFOA, PFBS, PFOS, PFHxA and PFHpA. How- the total PFASs (Fig. S1 and Table 1). ever, long chain PFASs (PFUnDA, PFDoDA, PFTrDA, PFTeDA, FOSA, EtFOSAA and PFDS) showed much less or no contributions to ∑PFASs. 3.3. Source identification for PFASs in the Beibu Gulf Unlike the present investigation, most previous studies demon- strated that PFOA and PFOS were the most dominant PFASs in the wa- In the HM-HCA analysis, PFASs or sampling sites with the similar ters around the world (Eschauzier et al., 2010; Labadie and Chevreuil, sources would group into the same cluster. While PFASs clustered into 2011; Pan et al., 2014a). This might be related to different types of in- two distinct groups in the summer, they clustered into three distinct dustry in this district and the gradual replacement of long-chain PFASs groups in the winter (Fig. 3). Specifically, in the summer, PFHpA, by short-chain PFASs due to their restrictions. PFNA, PFBS, PFHxA, PFHxS, PFOS, PFDA, PFUnDA and PFOA were clustered together and were apart from PFBA and PFPeA (Fig. 3A). In the 3.2. Occurrence and composition profiles of PFASs in the coastal seawater winter, while PFBA, PFOA and PFBS were clustered into the same group, PFHxA, PFHpA, PFNA, PFOS, PFHxS, PFDA, EtFOSAA and FOSA Similar to PFASs contamination in the riverine water, there were 11 were clustered into another group. Both groups were dissimilar to PFASs detected in the coastal seawater from the Beibu Gulf in both sea- PFPeA (Fig. 3B). As compounds in the same group might originate sons. The concentrations of the detected PFASs are shown in Fig. 2, from similar sources (McGregor et al., 2012; Shi et al., 2012), PFASs in Tables 1, S4, and S5. The ΣPFASs concentrations were in the range of surface water of the Beibu Gulf may mainly originate from three differ- 2831–4727 pg/L with a mean value of 3592 pg/L in the summer and ent types of sources, such as effluent discharges from domestic and in- 1937–4920 pg/L with a mean value of 2475 pg/L in the winter. Interest- dustrial WWTPs, PFAS-related manufacturing facilities and vessels ingly, the ΣPFASs concentrations in the coastal water were significantly (e.g., ships and boats) (Bao et al., 2011; Kim et al., 2012; Paul et al., higher in the summer than winter (p b 0.05; Fig. 2 and Table 1), even 2009; Sanchez-Avila et al., 2010). Similar to PFASs clusters, there were slightly higher than those in the riverine water in the summer. This is also several of sampling sites in both seasons. However, sampling sites very likely to be related to the difference in oceanic current between were clustered differently between summer and winter. For example, the summer and winter (Fig. 1). It has been reported that the sources C21, R3, R9 and R19 clustered into the same group in the summer, of PFASs in the marine environment mostly originated from wastewa- whereas R14-R19 clustered into the same group in the winter ters and riverine inputs (Ahrens, 2011; Benskin et al., 2012; Pistocchi (Fig. 3A). Nevertheless, sampling sites close to each other were gener- and Loos, 2009). Also, the ocean current flows from the southwest to ally clustered into the same group and are likely to share similar sources the east in the summer and southeast to west in the winter (Fig. 1). or characteristics. Taken together, it is very likely that PFASs pollution in southwest of In addition to HM-HCA, spearman correlation analysis was further the study area is more serious than the Beibu Gulf. So et al. (2004) conducted to characterize the sources of PFASs. There were significantly also found differences in PFASs distribution patterns between seasons positive correlations between some PFASs (PFBS and PFOS, PFNA and due to a seasonal shift of the ocean currents in the South China Sea. PFDA, PFOA and PFHxA, etc.) (p b 0.05) (Table S6), suggesting these Among all detected target compounds, PFBA, PFPeA, PFBS, PFHxA, compounds may be derived from similar sources, such as effluents of PFHpA, PFOA and PFNA were the most ubiquitous, with detection fre- WWTPs (Schultz et al., 2006) and rain or surface runoff (Kim and quencies of 100%, followed by PFOS, PFHxS, PFUnDA and FOSA. Also, Kannan, 2007). PFBS and PFOS were significantly positively correlated PFPeA showed the highest concentrations (118–2968 pg/L, Table 1) in the winter, which suggests these two pollutants may come from sim- and occurred at site C6, indicating the existence of point sources near ilar sources. Indeed, previous studies have revealed that PFBS was an al- this site. Indeed, site C6 is close to a fishing port that hosts fishing ternative chemical to PFOS (Kwok et al., 2015; Qi et al., 2016). On the ships or boats, which is likely responsible for the high concentration of other hand, the absence of the correlation between PFBS and PFOS in PFPeA at site C6. Likewise, it has been reported that paints and grease the summer could be due to different ocean currents, weather condi- repellence for ship and dock protection, shipping as well as boat main- tions, or discharge patterns between the two seasons. The strong, posi- tenance can lead to the release of PFASs into the water environment tive correlation between PFNA and PFDA in both seasons could be 302 C.-G. Pan et al. / Science of the Total Environment 660 (2019) 297–305

Fig. 3. HM-HCA results of PFASs in water samples during summer (A) and winter (B) from the Beibu Gulf. In Heat map, the blue-red color gradient presents the concentrations (ng/L) of individual PFASs of lowest to highest intensity. (For interpretation of the references to color in this figure legend, the reader is referred to the web version of this article.) partially explained by the degradation of fluorotelomer alcohols (Kwok et al., 2015; Xie et al., 2013). While PFOS and PFOA were the pre- (FTOHs), as FTOHs can yield even- and odd-chain-length PFCAs, includ- dominant PFAS compounds in most area around the world, the concen- ing PFNA and PFDA (Yeung et al., 2006). Although it has been reported tration of PFOS was quite low and short chain PFASs (PFPeA and PFBA) that PFNA and PFOA were positively correlated in snow samples from were the dominant PFASs in the present study. This is very likely due to remote ice caps, Atlantic Ocean and Northern Europe (Ahrens et al., the replacement of long chain PFASs (e.g., PFOS) by short chain PFASs 2009b, 2010; Young et al., 2007), there was no significant correlation (e.g., PFPeA and PFBA). between PFNA and PFOA in the present study. Therefore, it is likely In generally, the PFASs concentrations in coastal waters ranged from that they mainly originated from direct emissions rather than atmo- tens of pg/L to tens of ng/L depending on sampling sites (Cai et al., 2012; spheric deposition. Further, it has been reported that the ratio of Chen et al., 2011; Gomez et al., 2011; Sanchez-Avila et al., 2010; PFHpA to PFOA increased with increasing distance from Taniyasu et al., 2005; Theobald et al., 2011; Wan et al., 2017; nonatmospheric source and a high ratio could be an effective tracer of Yamashita et al., 2005). Same as in the riverine water, PFASs concentra- atmospheric deposition with the ratio ranging from 0.5 to 0.9 in urban tions determined in the coastal waters in the present study were also areas and from 6 to 16 in remote areas (Simcik and Dorweiler, 2005). lower than most other coastal waters in the world. For example, in com- In the present study, values of PFHpA/PFOA were lower than 1 at all parison with concentrations determined here, much higher concentra- sampling stations, indicating PFASs in the Beibu Gulf originated from di- tions of PFASs were reported in Tokyo Bay of Japan, South Korea, rect sources. Bohai Sea and Shandong Peninsula of China (Chen et al., 2011; So et al., 2004; Wan et al., 2017; Yamashita et al., 2005), which were 3.4. Comparison of PFASs concentrations with previous studies known to be developed and heavily polluted areas. In particular, PFOA and PFOS concentrations were about 1–3 orders of magnitude higher Because PFASs have been investigated in riverine and coastal waters in Tokyo Bay and South Korea than the Beibu Gulf (Yamashita et al., worldwide, here we performed a global comparison of PFASs concentra- 2005; So et al., 2004). PFASs concentrations detected in our study tions (Table 2). In general, the PFAS concentrations in the rivers of the were comparable to those from the coast of west Baltic Sea (Theobald Beibu Gulf were 1–3 orders of magnitude lower than those in other riv- et al., 2011), Catalonia and Cantabrian Sea in Spain (Gomez et al., ers (mostly a few ng/L to hundreds ng/L) in the world. This could be as- 2011; Sanchez-Avila et al., 2010) and East to South China Sea (Cai cribed to the less use and lower production of PFASs in the Beibu Gulf, a et al., 2012; Kwok et al., 2015), even slightly higher than those detected developing region that has much less PFASs-related industries com- in the Sulu Sea (Yamashita et al., 2005) and other open ocean waters pared with most of other regions. Indeed, previous studies have illus- (Gonzalez-Gaya et al., 2014) where PFASs concentrations ranged from trated that PFASs concentrations were positively correlated with the tens to hundreds of pg/L. However, it should be noted that Sulu Sea is gross domestic product (GDP), population density and industry type far away from the land compared with our study, which probably C.-G. Pan et al. / Science of the Total Environment 660 (2019) 297–305 303

Table 2 Concentrations (ranges) of individual PFASs in coastal waters (ng/L) around the world.

Coastal regions PFOA PFOS PFBS PFBA PFPeA Reference

Dalian b0.06–2.25 0.17–37.55 Ju et al., 2008 Bohai Sea b1.0–82 b0.2–31 b2.0–2.3 Chen et al., 2011 Bohai Sea b0.05–83.4 b0.04–6.8 b0.12–1.46 b0.24–2.9 b0.16–7.91 Chen et al., 2016 Shandong peninsula 10.49–61.64 4.2–25.4 0.15–2.35 b0.6–4.11 0.49–7.11 Wan et al., 2017 Yellow Sea 7.1–45 2.9–14 0.69–14 Zhu et al., 2017 East to South China Sea 0.0375–1.542 b0.0207–0.0703 0.023–0.941 b0.0203–0.439 Cai et al., 2012 Hong Kong 0.24–16 0.02–12 So et al., 2004 South China Sea 0.0308–1.150 0.0173–1.640 Kwok et al., 2015 South Korea 0.24–320 0.04–730 b0.005–5 So et al., 2004 Tokyo bay 1.8–192 0.338–57.7 Yamashita et al., 2005 Coastal area of Japan b2.5–59 Taniyasu et al., 2003 Coastal area of Bangladesh 3.17–27.8 b0.08–5.10 b0.08–3.67 b0.008–1.82 0.47–8.07 Habibullah-Al-Mamun et al., 2016 NW Mediterranean Sea b0.08–1.86 b0.03–3.93 b0.07–0.24 Sanchez-Avila et al., 2010 German Bight 2.67–7.83 0.69–3.95 3.38–17.7 Ahrens et al., 2009a West Baltic Sea 0.47–1.1 0.33–0.90 Theobald et al., 2011 Beibu Gulf 0.132–1.046 0–0.487 0.041–1.764 0.252–1.771 0.049–2.968 This study

explains the above results. Nevertheless, PFASs concentrations in the distribution of PFASs in the Beibu Gulf was strongly affected by ocean coastal water from the Beibu Gulf were at a relatively low level com- currents and there was a significant seasonal variation of PFASs concen- pared with other coastal regions in the world. trations in the coastal water. Our results demonstrate that the Beibu Gulf was relatively less polluted by PFASs compared with other coastal 3.5. Ecological risks assessment and environmental implications areas worldwide. These results also indicate that targeted PFAAs would not pose risks to aquatic organisms in the Beibu Gulf. Although PFASs are ubiquitously present in the environment, their potential effects remain unclear. Several studies have recommended CRediT authorship contribution statement corresponding values of PFASs concentrations to protect the most sensi- tive aquatic organisms. For example, the recommended PNECs for PFOA Chang-Gui Pan: Conceptualization, Investigation, Writing - original draft. and PFOS were 0.57 mg/L and 0.61 μg/L, respectively (Cao et al., 2013; Qi Ke-Fu Yu: Conceptualization, Writing - review & editing. Ying-Hui et al., 2011). Also, for other PFASs, such as PFPeA, PFHxA, PFNA and Wang: Conceptualization, Writing - review & editing. Wei Zhang: Inves- PFDA, the recommended PNECs were 32 μg/L, 97 μg/L, 100 μg/L and 11 tigation. Jun Zhang: Investigation. Jing Guo: Investigation. μg/L, respectively (Hoke et al., 2012). Additionally, to protect the pelagic aquatic organisms in seawater, a previous study also proposed annual average environmental quality standards for PFBA (1.4 μg/L), PFPeA Acknowledgments (0.6 μg/L), PFHxA (0.2 μg/L), PFOA (20 ng/L) and PFBS (0.6 μg/L) (Valsecchi et al., 2017). The author would like to thank the financial support by the National The concentrations of individual PFASs detected in our study area Natural Science Foundation of China (Nos. 41503108 and 91428203), ranged from tens to hundreds of pg/L, which are far lower than those the Guangxi scientific projects (Nos. AD17129063, AA17204074, recommended PNECs no matter which guideline values were used. Ac- AA17202020, and 2018AA23005), and the Bagui Fellowship from cordingly, all calculated RQ values were far below 1, suggesting that Guangxi Province of China. We would also like to thank five anonymous PFASs in the Beibu Gulf are unlikely to pose adverse effects on aquatic reviewers who have provided many insightful comments. organisms. However, the risks of long-term exposure to low levels (en- vironmentally relevant) of PFASs are still not clear and need to be eluci- Appendix A. Supplementary data dated. 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