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Occurrence and distribution of perfluoroalkyl substances in surface riverine and coastal sediments from the Beibu Gulf, south China
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Occurrence and distribution of perfluoroalkyl substances in surface riverine and coastal sediments from the Beibu Gulf, south China Chang-Gui Pana,b, Ying-Hui Wanga,b,∗, Ke-Fu Yua,b, Wei Zhanga,b, Jun Zhanga,b, Jing Guoa,b a b
Guangxi Laboratory on the Study of Coral Reefs in the South China Sea, Guangxi University, Nanning, 530004, China School of Marine Sciences, Guangxi University, Nanning, 530004, China
ARTICLE INFO
ABSTRACT
Keywords: PFASs Sediment Beibu gulf Source identification Risk
There is limited understanding on the occurrence of PFASs in coastal sediment, especially in less-developed coastal areas. Here, we collected surface sediment samples from the Beibu Gulf to investigate the occurrence, spatial distribution and environmental risks of 18 PFASs. The concentrations of the total PFASs (ΣPFASs) ranged from 56.2 to 586.3 pg/g dry weight (dw), with a mean value of 172.5 pg/g dw. ΣPFASs concentrations were significantly lower in riverine than in coastal sediments. Additionally, there was a decreasing trend in ΣPFASs concentrations from the west (Fangchenggang) to the east (Beihai) of the Beibu Gulf. Perfluorooctanoic acid (PFOA) and perfluorooctane sulfonate (PFOS) were the predominant PFASs, with their concentrations in the range of 4.8–249.0 pg/g dw and not detected (n.d)-224.8 pg/g dw, respectively. On a global scale, PFOS and PFOA concentrations were at low levels in the sediment of the Beibu Gulf, and they posed negligible environmental risks.
Perfluoroalkyl substances (PFASs) are synthetic chemicals that contain a fluorinated carbon backbone and a charged functional group. Due to the thermal stability, surfactant and hydro-oleophobicity properties, PFASs have been widely used in a range of applications, including aerospace, food package, firefighting foams, electronics, semiconductors, and textile, etc (Prevedouros et al., 2006). PFASs can not be effectively removed by conventional sewage treatment plants (Pan et al., 2016), Eventually, PFASs are ubiquitously present in water (Pan et al., 2019; Liu et al., 2019), sediment (Zhao et al., 2015; Chen et al., 2019), biota (Bangma et al., 2019; Munoz et al., 2019), and humans (Kim et al., 2019). Perfluorooctanoic acid (PFOA) and perfluorooctane sulfonate (PFOS) are two representatives of PFASs. Both chemicals are very persistent in the environment, and they have been demonstrated to bioaccumulate and biomagnify through aquatic food chains/webs (Pan et al., 2014c; Simmonet-Laprade et al., 2019). Several studies have demonstrated that PFOA and PFOS can induce developmental, hepatic and immunological toxicity to animals under laboratory conditions (Nordén et al., 2016; Lai et al., 2017; Liu and Gin, 2018). Consequently, the production and use of these two chemicals are regulated or under consideration worldwide. Previous studies have paid much more attention to PFASs occurrence in water and biota samples than sediments (Boiteux et al., 2017; Newsted et al., 2017), even though sediment has been considered to be the ultimate reservoir as well as a secondary source for PFASs ∗
(Prevedouros et al., 2006). However, sediment is able to significantly affect the environmental chemistry and ecotoxicity of PFASs, because PFASs can be desorbed from sediment and thereby being released back to the water phase (Martin et al., 2004; Prevedouros et al., 2006). In addition, riverine input and atmospheric deposition can contribute to the transportation of PFASs into marine environments (Stock et al., 2007; Pan et al., 2014b), which could lead to adsorption of PFASs onto the sediment. However, partition of PFASs onto sediment is a very complex process, which is influenced by both physicochemical characteristics of PFASs and sediment properties (You et al., 2010; Zhao et al., 2012). Previous studies in sediments have mainly focused on developed coastal regions that have high PFASs concentrations in the water, including Bohai Sea of China (Zhu et al., 2014), Yangtze River Estuary of China (Pan and You, 2010), Pearl River Estuary of China (Gao et al., 2015), German Bight (Zhao et al., 2015), and Tokyo Bay of Japan (Ahrens et al., 2009; Zushi et al., 2010), with concentrations up to several hundred ng/g dry weight (dw). However, there is limited understanding on the fate of PFASs in less-developed coastal regions. The Beibu Gulf is located at the northwest of the South China Sea, which receives discharges from many rivers. During the past decades, the land use in this region has experienced the conversion from agricultural land to industrial and urban land. In turn, the industrialization and urbanization would lead to various pollutants in the Beibu Gulf. Furthermore, urban and industrial areas have been recognized as major
Corresponding author. Guangxi Laboratory on the Study of Coral Reefs in the South China Sea, Guangxi University, Nanning, 530004, China. E-mail address: [email protected] (Y.-H. Wang).
https://doi.org/10.1016/j.marpolbul.2019.110706 Received 30 July 2019; Received in revised form 22 October 2019; Accepted 31 October 2019 Available online 18 November 2019 0025-326X/ © 2019 Elsevier Ltd. All rights reserved.
Please cite this article as: Chang-Gui Pan, et al., Marine Pollution Bulletin, https://doi.org/10.1016/j.marpolbul.2019.110706
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Fig. 1. Map showing the sampling sites in the Beibu Gulf, South China.
sources of PFASs (Pan et al., 2014a). However, previous studies in this region mainly focused on the contamination of nutrients (Wang et al., 2014), heavy metals (Xia et al., 2011), legacy POPs (Zhang et al., 2014; Li et al., 2015) and antibiotics (Zheng et al., 2012). The contamination status of PFASs in the sediment of Beibu Gulf is still unknown. The objectives of this study were i) to investigate the levels and spatial distributions of PFASs in the sediments of the Beibu Gulf, ii) to identify potential PFASs sources in the Beibu Gulf, and iii) to assess the potential environmental risks associated with predominant PFASs. Eighteen PFASs were selected as target compounds in this study (Table S1). Detailed information on standards and reagents are provided in the supporting information (SI, Text S1 and Table S1). We used a grab sampler to collect surficial sediment samples from 35 sampling sites in the Beibu Gulf of South China in 2017 (Fig. 1). Detailed information on the sampling sites is described in Fig. 1 and Table S2. Wet sediments were freeze-dried, homogenized and sieved with a 40-mesh screen, packed in PE bags, and stored at −18 °C until extraction. Sample extraction was conducted following our previous methods (Pan et al., 2014a). Briefly, the sediment samples were extracted with an ion-pair extraction method as detailed in the Text S2. The concentrations of PFASs were determined by an ultrahigh performance liquid chromatography-tandem mass spectrometry (UPLCMS/MS, Agilent 1290/6460) equipped with an electrospray ionization source using multiple reaction monitoring mode in the negative ionization mode. The separation of target compounds was performed on a reverse-phase column (Eclipse plus C18, 2.1 mm i.d. × 50 mm length, 1.8 μm). Detailed information on instrument method is provided in the SI (Text S3). Duplicate samples collected from each sampling site were used for PFAS extraction. All fluorinated materials and glassware were not used to avoid potential PFAS contamination and adsorption. Procedural blanks and spiked samples were included to examine the background contamination and recovery of PFASs. The limit of detection (LOD) and limit of quantification (LOQ) were calculated based on three and ten
times of the signal to noise ratio, respectively. All PFASs in laboratory blanks were below their corresponding LODs. The LOQs for the target compounds ranged from 4 to 33 pg/g. The recovery of each PFAS ranged from 78% to 146%. A 5 ng/mL of standard mixture solution was run for every eight samples to check the instrumental drift. Quantification of the PFASs was based on the internal standard method. A series of standard solutions ranging from 0.1 to 10 ng/mL (0.1, 0.2, 0.5, 1, 2, 5, and 10 ng/mL) were prepared to calculate target PFAS concentrations. The detailed recoveries, LOD and LOQ of each PFAS in the sediment are given in Table S3. PFASs concentrations were reported on a dry weight (dw) basis. ΣPFASs represents the sum of all the 18 target PFAS. Concentrations below LODs were reported as 0, and those between LODs and LOQs were reported as half of the corresponding LOQs. Normality and homogeneity of variance were tested using Shapiro-Wilk test and levene's test, respectively. Accordingly, independent t-test was used to evaluate the significance of difference in PFASs concentrations between riverine and coastal sediments. Spearman rank correlation analysis was performed to evaluate the relations between PFASs. The above statistical analyses were performed using SPSS (Version 22.0, SPSS Incorporate). Additionally, to characterize the similarities of PFASs and sampling sites, a principal component analysis (PCA) was performed using Canoco 5.0. The significance level was set at p = 0.05. Concentrations of PFASs in surface sediments from the Beibu Gulf are shown in Table 1 and Fig. 2. Concentrations of ∑PFASs ranged from 56.2 to 586.3 pg/g dw, with a mean and median value of 172.5 pg/g dw and 155.6 pg/g dw, respectively. The maximum ∑PFASs concentration was observed at site C7, which might be related to the PFAS source in an adjacent port, as demonstrated previously that some materials (paint and grease repellence) related to dock protection, ship maintenance and maritime navigation were able to elevate the PFASs levels in the surrounding area (Paul et al., 2009). Interestingly, ∑PFASs concentrations were significantly higher in coastal sediments than in riverine sediments (p < 0.05) (Table 1 and Fig. 2). This might be due to the 2
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Table 1 Concentrations (pg/g dw) and detection frequencies (df, %) of PFASs in the sediments from the Beibu Gulf. Riverine sediment
PFOA PFNA PFDA PFUnDA PFDoDA PFTrDA PFOS EtFOSAA FOSA ΣPFASs
Coastal sediment
Min
Max
Mean
Median
df (%)
Min
Max
Mean
Median
df (%)
4.8 n.d 10.3 n.d n.d n.d n.d n.d n.d 56.2
37.2 16.5 66.3 28.3 19.3 27.6 59.7 35.3 n.d 189.4
17.4 2.4 20.5 16.8 10.1 17.8 24.1 10.6 n.d 115.8
15.7 n.d 14.2 18.1 11.4 19.5 14.2 n.d n.d 112.1
100 14.3 100 92.9 85.7 92.9 100 42.9 0 100
6.6 n.d n.d 10.8 n.d 16.4 n.d n.d n.d 77.4
249.0 55.6 35.6 62.3 18.1 34.0 224.9 n.d n.d 586.3
61.5 18.4 16.4 23.6 9.9 20.6 56.5 21.2 27.7 211.0
42.1 17.7 14.8 19.4 10.7 20.2 51.1 1.6 2.6 177.5
100 81 95.2 100 85.7 100 81.0 9.5 9.5 100
n.d: not detected.
transportation of PFASs from southwest through oceanic currents and subsequently adsorbed onto the sediment particles (Fig. 1). In support of this speculation, sediment samples collected from the west (Fangchenggang) had higher concentrations of ∑PFASs compared to those from the east (Qinzhou and Beihai) of the Beibu Gulf, with their mean concentrations following the trend: Fangchenggang > Qinzhou > Beihai (Fig. 3). PFOA was the predominant PFAS with the concentration in the range of 4.8–249.0 pg/g dw and a mean level of 43.6 pg/g dw, followed by PFOS with corresponding values of not detected (n.d) −224.8 pg/g dw and 43.2 pg/g dw, respectively. In line with our results, PFOA and PFOS were the predominant PFASs in sediments from most other regions worldwide (Bao et al., 2010; Yeung et al., 2013; Pan et al., 2014a; Zhao et al., 2014; Liu et al., 2019). Nine out of 18 PFASs were detected, including C8–C13–PFCAs, C8–PFSAs, FOSA and EtFOSAA. The detection frequencies of these PFASs were as follows: PFOA (100%), followed by PFDA, PFUnDA and PFTrDA (97%), PFDoDA (86%), PFOS (71%), PFNA (54%), EtFOSAA (23%) and only 6% for FOSA. These frequently detected PFASs are long-chain PFASs with carbon chain length ≥8, whereas PFASs with carbon chain length < 8 were not detected in any samples and excluded from further data analysis. Therefore, it seems that long-chain PFASs are more likely to partition onto the sediment compared to short-chain PFASs (Yeung et al., 2013; Pan et al., 2014a). Several previous studies also reported low detection rates and concentrations of PFASs in sediment samples (Thompson et al., 2011; Long et al., 2013). For example, only PFOS, FOSA, and PFBA were detected with low detection rates (2–17%) and low concentrations in sediments collected from Puget Sound, WA (USA) (Long et al., 2013). The composition profiles of relative contributions of individual PFASs to the ∑PFASs are displayed in Fig. S1. PFOA made the greatest contribution to ∑PFAS in the sediments, with an average contribution of 22.3%. Other major PFASs were PFOS (21.1%), PFTrDA (14.2%), and
PFUnDA (13.5%) on a mean basis. Overall, the C8–C14 PFASs contributed 100% to the ΣPFASs, whereas C4–C7 PFASs made no contribution to the ∑PFASs. This suggests that physicochemical properties of the compound strongly influenced the distribution of PFASs in the sediment, likely due to the lower water solubility of long-chain PFASs relative to short-chain PFASs. Likewise, an earlier study reported that perfluorocarbon chain length was the most important factor that can influence the partition of PFASs onto sediment (Pan et al., 2014a). The results obtained here are consistent with findings reported in the majority of previous studies (Bao et al., 2010; Pan et al., 2014b). For example, PFOS and PFOA showed the highest contribution to target ∑PFASs in surface sediment samples from Haihe River and Dongjiang River in China as well as Bay of Bengal coast (Pan et al., 2014a; Zhao et al., 2014; Habibullah-Al-Mamun et al., 2016). It has been demonstrated that correlation analysis can be used to trace the potential sources of PFASs (Ahrens et al., 2009). Here PFOA was significantly positively correlated with PFNA and PFOS, and PFOS was significantly positively correlated with PFNA, PFDA, FOSA and PFTrDA (Table 2). This indicates that these chemicals may share similar source and transport routes (Gao et al., 2014). Further, as PFDA and PFUnDA could be generated via oxidation of PFASs precursors in the environment (Young et al., 2007), here the frequent detection of PFDA and PFUnDA may imply that atmospheric oxidation of PFASs precursors was a source of PFASs in our study area. The PFOS/PFOA ratio has been used to identify source regions in some studies, as higher PFOS/PFOA ratios were often found in locations closer to PFAS sources (So et al., 2004; Gao et al., 2014). Here the PFOS/PFOA ratios were < 1 at the majority of samples from the Beibu Gulf, suggesting that most sampling sites are not close to PFASs sources. The PCA was further applied to identify PFAS sources and characterize similarities among sampling sites. As shown in Fig. 4, PC 1 and PC 2 explained 45% and 20.5% of the total variation, respectively. Generally, samples from the coastal area clustered to the left part of the PCA diagram and had higher concentrations of PFDA, PFOS, FOSA, PFUnDA, PFOA, PFNA and PFDoDA, whereas samples from riverine area clustered to the right part and had higher concentrations of EtFOSAA and PFTrDA. These results suggest that there was a clear difference in PFAS concentrations between the riverine and coastal area. These results also suggest a different pattern of PFASs sources. Generally, PFOS and PFOA were the most frequently detected PFASs with the highest concentrations in the sediments worldwide, and the concentration of PFOS was usually higher than PFOA (Table S4). Likewise, PFOS and PFOA were the predominant PFASs in the present study. In comparison with findings reported previously in different regions worldwide (Table S4), PFOS and PFOA contamination in the Beibu Gulf was relatively low on a global perspective. PFOS concentrations in the sediment of the Beibu Gulf are similar to those detected in the Pearl River estuary (China; < LOD-0.32 ng/g) and Ariake Sea (Japan; 0.09–0.14 ng/g) (Nakata et al., 2006; Gao et al., 2015), but
Fig. 2. Concentrations of PFASs in sediments from the Beibu Gulf. 3
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Fig. 3. Boxplot of PFOA, PFOS, PFUnDA and ΣPFASs in sediments from the Beibu Gulf. Note: FCG, QZ and BH represent Fangchenggang, Qinzhou and Beihai. The solid line and short dashed line in the box denote median and mean concentration value of corresponding PFAS, respectively.
approximately one order of magnitude lower than those reported in German Bight (Germany; 0.02–5.36 ng/g) (Zhao et al., 2015), Bangladeshi coastal area (0.30–3.56 ng/g) (Habibullah-Al-Mamun et al., 2016) and Sydney Harbor (Australia; 0.80–6.20 ng/g) (Thompson et al., 2011). Nevertheless, much lower PFOS levels have been reported in Laizhou Bay (China; < 0.03–0.06 ng/g) (Zhao et al., 2013). Regarding PFOA, while comparable levels have been found in the Savannah River Estuary (USA; n.d-0.2 ng/g) (Kumar et al., 2009), German Bight (Germany; 0.007–0.43 ng/g) (Zhao et al., 2015) and Sydney Harbor (Australia 0–0.16 ng/g) (Thompson et al., 2011), higher PFOA levels have been reported in the Ariake Sea (Japan; 0.84–1.1 ng/g) (Nakata et al., 2006), Laizhou Bay (China; 0.07–1.8 ng/g) (Zhao et al., 2013) and Charleston Estuary (USA; 0.02–2.52 ng/g) (White et al., 2015). The relatively low concentrations of PFASs in Beibu Gulf are likely due to the low GDP and less PFASs-related industrial facilities in this region. Indeed, a previous study reported a positive correlation between coastal contamination of PFASs and socio-economic situations of the coastal areas (Kwok et al., 2015). PFOS and PFOA can induce various toxic effects on different trophic levels of organisms depending on their concentrations (Beach et al., 2006; Giesy et al., 2010; Zushi et al., 2012). Moreover, sediment has been recognized as a sink and reservoir of PFASs (Prevedouros et al.,
2006). Therefore, it is essential to understand the environmental risks of sediment-associated PFOS and PFOA to aquatic systems. We used risk quotient (RQ) to assess the environmental risks of PFASs in the sediments of the Beibu Gulf. The RQ of each PFAS was calculated by dividing the measured environmental concentration (MEC) by the predicted no-effect concentration (PNEC). An RQ value < 1 indicates no risk and an RQ ≥ 1 represents potential risk. The PNEC used for riverine sediment PFOS and PFOA were 4.9 ng/g and 86 ng/g, respectively, while the PNECs for marine sediment were ten times lower than the corresponding PNECs for riverine sediment (Zhao et al., 2013). The results show that all RQ values were much lower than one, suggesting negligible environmental risks associated with PFOS and PFOA in the sediments from the Beibu Gulf. In contrast, a previous study reported that PFOS and PFOA in sediments from Laizhou Bay can pose low risks to benthic invertebrates (Zhao et al., 2013). Furthermore, it is noteworthy that even low concentrations of PFASs in environment could lead to higher levels of PFASs in biota due to their persistent and bioaccumulative characteristics. Therefore, further study is required to assess the environmental risks and exposure risks of PFAS mixture. PFOA and PFOS were the two predominant PFASs in the sediment of the Beibu Gulf, but they would not pose environmental risks. Longchain PFASs were more frequently detected than short-chain PFASs,
Table 2 Spearman correlation coefficients (two-tailed) for individual PFASs concentrations in surface waters of the Beibu Gulf. PFOA PFNA PFOS PFDA EtFOSAA PFUnDA FOSA PFDoDA PFTrDA a b
PFNA
PFOS
PFDA
EtFOSAA
PFUnDA
FOSA
PFDoDA
0.430b 0.428a −0.312 0.467b 0.356a −0.172 0.114
0.435b −0.05 0.304 0.407a −0.099 0.395a
−0.168 0.449b 0.353a 0.102 0.198
0.013 0.109 −0.028 0.295
0.389a 0.358a 0.515b
−0.174 0.352
0.210
b
0.741 0.462b 0.325 −0.457b 0.343 0.290 −0.164 0.042
Correlation is significant at the 0.05 level. Correlation is significant at the 0.01 level. 4
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urban river sediments from Guangzhou and Shanghai of China. Chemosphere 80 (2), 123–130. Beach, S.A., Newsted, J.L., Coady, K., Giesy, J.P., 2006. Ecotoxicological evaluation of perfluorooctanesulfonate (PFOS). Rev. Environ. Contam. Toxicol. 186, 133–174. Boiteux, V., Dauchy, X., Bach, C., Colin, A., Hemard, J., Sagres, V., Rosin, C., Munoz, J.F., 2017. Concentrations and patterns of perfluoroalkyl and polyfluoroalkyl substances in a river and three drinking water treatment plants near and far from a major production source. Science of the Total Environment 583, 393–400. Chen, L., Tsui, M.M., Lam, J.C., Wang, Q., Hu, C., Wai, O.W., Zhou, B., Lam, P.K., 2019. Contamination by perfluoroalkyl substances and microbial community structure in Pearl River Delta sediments. Environ. Pollut. 245, 218–225. Gao, Y., Fu, J., Meng, M., Wang, Y., Chen, B., Jiang, G., 2015. Spatial distribution and fate of perfluoroalkyl substances in sediments from the Pearl River Estuary, South China. Mar. Pollut. Bull. 96 (1–2), 226–234. Gao, Y., Fu, J., Zeng, L., Li, A., Li, H., Zhu, N., Liu, R.Z., Liu, A.F., Wang, Y.W., Jiang, G., 2014. Occurrence and fate of perfluoroalkyl substances in marine sediments from the Chinese Bohai Sea, Yellow Sea, and east China Sea. Environ. Pollut. 194, 60–68. Giesy, J.P., Naile, J.E., Khim, J.S., Jones, P.D., Newsted, J.L., 2010. Aquatic toxicology of perfluorinated chemicals. Rev. Environ. Contam. Toxicol. 202, 1–52. Habibullah-Al-Mamun, M., Ahmed, M.K., Raknuzzaman, M., Islam, M.S., Negishi, J., Nakamichi, S., Sekine, M., Tokumura, M., Masunaga, S., 2016. Occurrence and distribution of perfluoroalkyl acids (PFAAs) in surface water and sediment of a tropical coastal area (Bay of Bengal coast, Bangladesh). Sci. Total Environ. 571, 1089–1104. Kim, D.H., Lee, J.H., Oh, J.E., 2019. Assessment of individual-based perfluoroalkly substances exposure by multiple human exposure sources. J. Hazard Mater. 365, 26–33. Kumar, K.S., Zushi, Y., Masunaga, S., Gilligan, M., Pride, C., Sajwan, K.S., 2009. Perfluorinated organic contaminants in sediment and aquatic wildlife, including sharks, from Georgia, USA. Mar. Pollut. Bull. 58 (4), 621–629. Kwok, K.Y., Wang, X.H., Ya, M., Li, Y., Zhang, X.H., Yamashita, N., Lam, J.C., Lam, P.K., 2015. Occurrence and distribution of conventional and new classes of per-and polyfluoroalkyl substances (PFASs) in the South China Sea. J. Hazard Mater. 285, 389–397. Lai, K.P., Li, J.W., Cheung, A., Li, R., Billah, M.B., Chan, T.F., Wong, C.K.C., 2017. Transcriptome sequencing reveals prenatal PFOS exposure on liver disorders. Environ. Pollut. 223, 416–425. Li, P., Xue, R., Wang, Y., Zhang, R., Zhang, G., 2015. Influence of anthropogenic activities on PAHs in sediments in a significant gulf of low-latitude developing regions, the Beibu Gulf, South China Sea: distribution, sources, inventory and probability risk. Mar. Pollut. Bull. 90 (1–2), 218–226. Liu, C., Gin, K.Y.H., 2018. Immunotoxicity in green mussels under perfluoroalkyl substance (PFAS) exposure: Reversible response and response model development. Environ. Toxicol. Chem. 37 (4), 1138–1145. Liu, Y., Zhang, Y., Li, J., Wu, N., Li, W., Niu, Z., 2019. Distribution, partitioning behavior and positive matrix factorization-based source analysis of legacy and emerging polyfluorinated alkyl substances in the dissolved phase, surface sediment and suspended particulate matter around coastal areas of Bohai Bay, China. Environ. Pollut. 246, 34–44. Long, E.R., Dutch, M., Weakland, S., Chandramouli, B., Benskin, J.P., 2013. Quantification of pharmaceuticals, personal care products, and perfluoroalkyl substances in the marine sediments of Puget Sound, Washington, USA. Environ. Toxicol. Chem. 32 (8), 1701–1710. Martin, J.W., Whittle, D.M., Muir, D.C.G., Mabury, S.A., 2004. Perfluoroalkyl contaminants in a food web from Lake Ontario. Environ. Sci. Technol. 38 (20), 5379–5385. Munoz, G., Budzinski, H., Babut, M., Lobry, J., Selleslagh, J., Tapie, N., Labadie, P., 2019. Temporal variations of perfluoroalkyl substances partitioning between surface water, suspended sediment, and biota in a macrotidal estuary. Chemosphere 233, 319–326. Nakata, H., Kannan, K., Nasu, T., Cho, H.-S., Sinclair, E., Takemura, A., 2006. Perfluorinated contaminants in sediments and aquatic organisms collected from shallow water and tidal flat areas of the Ariake Sea, Japan: environmental fate of perfluorooctane sulfonate in aquatic ecosystems. Environ. Sci. Technol. 40 (16), 4916–4921. Newsted, J.L., Holem, R., Hohenstein, G., Lange, C., Ellefson, M., Reagen, W., Wolf, S., 2017. Spatial and temporal trends of poly-and perfluoroalkyl substances in fish fillets and water collected from pool 2 of the Upper Mississippi River. Environ. Toxicol. Chem. 36 (11), 3138–3147. Nordén, M., Berger, U., Engwall, M., 2016. Developmental toxicity of PFOS and PFOA in great cormorant (Phalacrocorax carbo sinensis), herring gull (Larus argentatus) and chicken (Gallus gallus domesticus). Environ. Sci. Pollut. Control Ser. 23 (11), 10855–10862. Pan, C.G., Liu, Y.S., Ying, G.G., 2016. Perfluoroalkyl substances (PFASs) in wastewater treatment plants and drinking water treatment plants: Removal efficiency and exposure risk. Water Res. 106, 562–570. Pan, C.G., Ying, G.G., Liu, Y.S., Zhang, Q.Q., Chen, Z.F., Peng, F.J., Huang, G.Y., 2014a. Contamination profiles of perfluoroalkyl substances in five typical rivers of the Pearl River Delta region, South China. Chemosphere 114, 16–25. Pan, C.G., Ying, G.G., Zhao, J.L., Liu, Y.S., Jiang, Y.X., Zhang, Q.Q., 2014b. Spatiotemporal distribution and mass loadings of perfluoroalkyl substances in the Yangtze River of China. Sci. Total Environ. 493, 580–587. Pan, C.G., Yu, K.F., Wang, Y.H., Zhang, W., Zhang, J., Guo, J., 2019. Perfluoroalkyl substances in the riverine and coastal water of the Beibu Gulf, South China: Spatiotemporal distribution and source identification. Sci. Total Environ. 660, 297–305. Pan, C.G., Zhao, J.L., Liu, Y.S., Zhang, Q.Q., Chen, Z.F., Lai, H.J., Peng, F.J., Liu, S.S., Ying, G.G., 2014c. Bioaccumulation and risk assessment of per- and polyfluoroalkyl substances in wild freshwater fish from rivers in the Pearl River Delta region, South
Fig. 4. Principal component loadings for PFASs and sampling sites in sediment samples from the Beibu Gulf. Red circle and blue square represent riverine and coastal sampling sites, respectively. (For interpretation of the references to colour in this figure legend, the reader is referred to the Web version of this article.)
suggesting that long-chain PFASs have a stronger affinity to the sediment compared to the short-chain PFASs. The ΣPFASs concentrations were significantly higher in coastal than in riverine sediments. Additionally, there was a clear decreasing trend in ΣPFASs concentration from the west (Fangchenggang) to the east (Beihai) of the Beibu Gulf. Overall, PFASs concentrations in the sediment of the Beibu Gulf were lower than most other regions worldwide. Declaration of competing interest The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper. Acknowledgments The authors would like to thank the financial support by the National Natural Science Foundation of China (Nos. 41673105 and 91428203), Guangxi Innovation-driven Development Projects (GuikeAA18242031), Natural Science Foundation of Guangxi (2018GXNSFAA050144). Appendix A. Supplementary data Supplementary data to this article can be found online at https:// doi.org/10.1016/j.marpolbul.2019.110706. References Ahrens, L., Yamashita, N., Yeung, L.W.Y., Taniyasu, S., Horii, Y., Lam, P.K.S., Ebinghaus, R., 2009. Partitioning behavior of per- and polyfluoroalkyl compounds between pore water and sediment in two sediment cores from Tokyo Bay, Japan. Environ. Sci. Technol. 43 (18), 6969–6975. Bangma, J.T., Ragland, J.M., Rainwater, T.R., Bowden, J.A., Gibbons, J.W., Reiner, J.L., 2019. Perfluoroalkyl substances in diamondback terrapins (Malaclemys terrapin) in coastal South Carolina. Chemosphere 215, 305–312. Bao, J., Liu, W., Liu, L., Jin, Y., Ran, X., Zhang, Z., 2010. Perfluorinated compounds in
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C.-G. Pan, et al. China. Ecotoxicol. Environ. Saf. 107, 192–199. Pan, G., You, C., 2010. Sediment-water distribution of perfluorooctane sulfonate (PFOS) in Yangtze River estuary. Environ. Pollut. 158 (5), 1363–1367. Paul, A.G., Jones, K.C., Sweetman, A.J., 2009. A first global production, emission, and environmental inventory for perfluorooctane sulfonate. Environ. Sci. Technol. 43 (2), 386–392. Prevedouros, K., Cousins, I.T., Buck, R.C., Korzeniowski, S.H., 2006. Sources, fate and transport of perfluorocarboxylates. Environ. Sci. Technol. 40 (1), 32–44. Simmonet-Laprade, C., Budzinski, H., Babut, M., Le Menach, K., Munoz, G., Lauzent, M., Ferrari, B., Labadie, P., 2019. Investigation of the spatial variability of poly-and perfluoroalkyl substance trophic magnification in selected riverine ecosystems. Sci. Total Environ. 686, 393–401. So, M.K., Taniyasu, S., Yamashita, N., Giesy, J.P., Zheng, J., Fang, Z., Im, S.H., Lam, P.K.S., 2004. Perfluorinated compounds in coastal waters of Hong Kong, South China, and Korea. Environ. Sci. Technol. 38 (15), 4056–4063. Stock, N.L., Furdui, V.I., Muir, D.C., Mabury, S.A., 2007. Perfluoroalkyl contaminants in the Canadian Arctic: evidence of atmospheric transport and local contamination. Environ. Sci. Technol. 41 (10), 3529–3536. Thompson, J., Roach, A., Eaglesham, G., Bartkow, M.E., Edge, K., Mueller, J.F., 2011. Perfluorinated alkyl acids in water, sediment and wildlife from Sydney Harbour and surroundings. Mar. Pollut. Bull. 62 (12), 2869–2875. Wang, Y., Zhang, W., Lin, Y., Cao, W., Zheng, L., Yang, J., 2014. Phosphorus, nitrogen and chlorophyll-a are significant factors controlling ciliate communities in summer in the Northern Beibu Gulf, South China Sea. PLoS One 9 (7). White, N.D., Balthis, L., Kannan, K., De Silva, A.O., Wu, Q., French, K.M., Daugomah, J., Spencer, C., Fair, P.A., 2015. Elevated levels of perfluoroalkyl substances in estuarine sediments of Charleston, SC. Sci. Total Environ. 521, 79–89. Xia, P., Meng, X., Yin, P., Cao, Z., Wang, X., 2011. Eighty-year sedimentary record of heavy metal inputs in the intertidal sediments from the Nanliu River estuary, Beibu Gulf of South China Sea. Environ. Pollut. 159 (1), 92–99. Yeung, L.W.Y., De Silva, A.O., Loi, E.I.H., Marvin, C.H., Taniyasu, S., Yamashita, N., Mabury, S.A., Muir, D.C.G., Lam, P.K.S., 2013. Perfluoroalkyl substances and extractable organic fluorine in surface sediments and cores from Lake Ontario. Environ.
Int. 59, 389–397. You, C., Jia, C., Pan, G., 2010. Effect of salinity and sediment characteristics on the sorption and desorption of perfluorooctane sulfonate at sediment-water interface. Environ. Pollut. 158 (5), 1343–1347. Young, C.J., Furdui, V.I., Franklin, J., Koerner, R.M., Muir, D.C.G., Mabury, S.A., 2007. Perfluorinated acids in arctic snow: new evidence for atmospheric formation. Environ. Sci. Technol. 41 (10), 3455–3461. Zhang, J., Li, Y., Wang, Y., Zhang, Y., Zhang, D., Zhang, R., Li, J., Zhang, G., 2014. Spatial distribution and ecological risk of polychlorinated biphenyls in sediments from Qinzhou Bay, Beibu Gulf of South China. Mar. Pollut. Bull. 80 (1–2), 338–343. Zhao, L., Zhu, L., Yang, L., Liu, Z., Zhang, Y., 2012. Distribution and desorption of perfluorinated compounds in fractionated sediments. Chemosphere 88 (11), 1390–1397. Zhao, X., Xia, X., Zhang, S., Wu, Q., Wang, X., 2014. Spatial and vertical variations of perfluoroalkyl substances in sediments of the Haihe River, China. J. Environ. Sci. 26 (8), 1557–1566. Zhao, Z., Tang, J., Xie, Z., Chen, Y., Pan, X., Zhong, G., Sturm, R., Zhang, G., Ebinghaus, R., 2013. Perfluoroalkyl acids (PFAAs) in riverine and coastal sediments of Laizhou Bay, North China. Sci. Total Environ. 447, 415–423. Zhao, Z., Xie, Z., Tang, J., Zhang, G., Ebinghaus, R., 2015. Spatial distribution of perfluoroalkyl acids in surface sediments of the German Bight, North Sea. Sci. Total Environ. 511, 145–152. Zheng, Q., Zhang, R., Wang, Y., Pan, X., Tang, J., Zhang, G., 2012. Occurrence and distribution of antibiotics in the Beibu Gulf, China: impacts of river discharge and aquaculture activities. Mar. Environ. Res. 78, 26–33. Zhu, Z., Wang, T., Wang, P., Lu, Y., Giesy, J.P., 2014. Perfluoroalkyl and polyfluoroalkyl substances in sediments from South Bohai coastal watersheds, China. Mar. Pollut. Bull. 85 (2), 619–627. Zushi, Y., Hogarh, J.N., Masunaga, S., 2012. Progress and perspective of perfluorinated compound risk assessment and management in various countries and institutes. Clean Technol. Environ. Policy 14 (1), 9–20. Zushi, Y., Tamada, M., Kanai, Y., Masunaga, S., 2010. Time trends of perfluorinated compounds from the sediment core of Tokyo Bay, Japan (1950s-2004). Environ. Pollut. 158 (3), 756–763.
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Baseline
Occurrence and distribution of perfluoroalkyl substances in surface riverine and coastal sediments from the Beibu Gulf, south China Chang-Gui Pana,b, Ying-Hui Wanga,b,∗, Ke-Fu Yua,b, Wei Zhanga,b, Jun Zhanga,b, Jing Guoa,b a b
Guangxi Laboratory on the Study of Coral Reefs in the South China Sea, Guangxi University, Nanning, 530004, China School of Marine Sciences, Guangxi University, Nanning, 530004, China
ARTICLE INFO
ABSTRACT
Keywords: PFASs Sediment Beibu gulf Source identification Risk
There is limited understanding on the occurrence of PFASs in coastal sediment, especially in less-developed coastal areas. Here, we collected surface sediment samples from the Beibu Gulf to investigate the occurrence, spatial distribution and environmental risks of 18 PFASs. The concentrations of the total PFASs (ΣPFASs) ranged from 56.2 to 586.3 pg/g dry weight (dw), with a mean value of 172.5 pg/g dw. ΣPFASs concentrations were significantly lower in riverine than in coastal sediments. Additionally, there was a decreasing trend in ΣPFASs concentrations from the west (Fangchenggang) to the east (Beihai) of the Beibu Gulf. Perfluorooctanoic acid (PFOA) and perfluorooctane sulfonate (PFOS) were the predominant PFASs, with their concentrations in the range of 4.8–249.0 pg/g dw and not detected (n.d)-224.8 pg/g dw, respectively. On a global scale, PFOS and PFOA concentrations were at low levels in the sediment of the Beibu Gulf, and they posed negligible environmental risks.
Perfluoroalkyl substances (PFASs) are synthetic chemicals that contain a fluorinated carbon backbone and a charged functional group. Due to the thermal stability, surfactant and hydro-oleophobicity properties, PFASs have been widely used in a range of applications, including aerospace, food package, firefighting foams, electronics, semiconductors, and textile, etc (Prevedouros et al., 2006). PFASs can not be effectively removed by conventional sewage treatment plants (Pan et al., 2016), Eventually, PFASs are ubiquitously present in water (Pan et al., 2019; Liu et al., 2019), sediment (Zhao et al., 2015; Chen et al., 2019), biota (Bangma et al., 2019; Munoz et al., 2019), and humans (Kim et al., 2019). Perfluorooctanoic acid (PFOA) and perfluorooctane sulfonate (PFOS) are two representatives of PFASs. Both chemicals are very persistent in the environment, and they have been demonstrated to bioaccumulate and biomagnify through aquatic food chains/webs (Pan et al., 2014c; Simmonet-Laprade et al., 2019). Several studies have demonstrated that PFOA and PFOS can induce developmental, hepatic and immunological toxicity to animals under laboratory conditions (Nordén et al., 2016; Lai et al., 2017; Liu and Gin, 2018). Consequently, the production and use of these two chemicals are regulated or under consideration worldwide. Previous studies have paid much more attention to PFASs occurrence in water and biota samples than sediments (Boiteux et al., 2017; Newsted et al., 2017), even though sediment has been considered to be the ultimate reservoir as well as a secondary source for PFASs ∗
(Prevedouros et al., 2006). However, sediment is able to significantly affect the environmental chemistry and ecotoxicity of PFASs, because PFASs can be desorbed from sediment and thereby being released back to the water phase (Martin et al., 2004; Prevedouros et al., 2006). In addition, riverine input and atmospheric deposition can contribute to the transportation of PFASs into marine environments (Stock et al., 2007; Pan et al., 2014b), which could lead to adsorption of PFASs onto the sediment. However, partition of PFASs onto sediment is a very complex process, which is influenced by both physicochemical characteristics of PFASs and sediment properties (You et al., 2010; Zhao et al., 2012). Previous studies in sediments have mainly focused on developed coastal regions that have high PFASs concentrations in the water, including Bohai Sea of China (Zhu et al., 2014), Yangtze River Estuary of China (Pan and You, 2010), Pearl River Estuary of China (Gao et al., 2015), German Bight (Zhao et al., 2015), and Tokyo Bay of Japan (Ahrens et al., 2009; Zushi et al., 2010), with concentrations up to several hundred ng/g dry weight (dw). However, there is limited understanding on the fate of PFASs in less-developed coastal regions. The Beibu Gulf is located at the northwest of the South China Sea, which receives discharges from many rivers. During the past decades, the land use in this region has experienced the conversion from agricultural land to industrial and urban land. In turn, the industrialization and urbanization would lead to various pollutants in the Beibu Gulf. Furthermore, urban and industrial areas have been recognized as major
Corresponding author. Guangxi Laboratory on the Study of Coral Reefs in the South China Sea, Guangxi University, Nanning, 530004, China. E-mail address: [email protected] (Y.-H. Wang).
https://doi.org/10.1016/j.marpolbul.2019.110706 Received 30 July 2019; Received in revised form 22 October 2019; Accepted 31 October 2019 Available online 18 November 2019 0025-326X/ © 2019 Elsevier Ltd. All rights reserved.
Please cite this article as: Chang-Gui Pan, et al., Marine Pollution Bulletin, https://doi.org/10.1016/j.marpolbul.2019.110706
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Fig. 1. Map showing the sampling sites in the Beibu Gulf, South China.
sources of PFASs (Pan et al., 2014a). However, previous studies in this region mainly focused on the contamination of nutrients (Wang et al., 2014), heavy metals (Xia et al., 2011), legacy POPs (Zhang et al., 2014; Li et al., 2015) and antibiotics (Zheng et al., 2012). The contamination status of PFASs in the sediment of Beibu Gulf is still unknown. The objectives of this study were i) to investigate the levels and spatial distributions of PFASs in the sediments of the Beibu Gulf, ii) to identify potential PFASs sources in the Beibu Gulf, and iii) to assess the potential environmental risks associated with predominant PFASs. Eighteen PFASs were selected as target compounds in this study (Table S1). Detailed information on standards and reagents are provided in the supporting information (SI, Text S1 and Table S1). We used a grab sampler to collect surficial sediment samples from 35 sampling sites in the Beibu Gulf of South China in 2017 (Fig. 1). Detailed information on the sampling sites is described in Fig. 1 and Table S2. Wet sediments were freeze-dried, homogenized and sieved with a 40-mesh screen, packed in PE bags, and stored at −18 °C until extraction. Sample extraction was conducted following our previous methods (Pan et al., 2014a). Briefly, the sediment samples were extracted with an ion-pair extraction method as detailed in the Text S2. The concentrations of PFASs were determined by an ultrahigh performance liquid chromatography-tandem mass spectrometry (UPLCMS/MS, Agilent 1290/6460) equipped with an electrospray ionization source using multiple reaction monitoring mode in the negative ionization mode. The separation of target compounds was performed on a reverse-phase column (Eclipse plus C18, 2.1 mm i.d. × 50 mm length, 1.8 μm). Detailed information on instrument method is provided in the SI (Text S3). Duplicate samples collected from each sampling site were used for PFAS extraction. All fluorinated materials and glassware were not used to avoid potential PFAS contamination and adsorption. Procedural blanks and spiked samples were included to examine the background contamination and recovery of PFASs. The limit of detection (LOD) and limit of quantification (LOQ) were calculated based on three and ten
times of the signal to noise ratio, respectively. All PFASs in laboratory blanks were below their corresponding LODs. The LOQs for the target compounds ranged from 4 to 33 pg/g. The recovery of each PFAS ranged from 78% to 146%. A 5 ng/mL of standard mixture solution was run for every eight samples to check the instrumental drift. Quantification of the PFASs was based on the internal standard method. A series of standard solutions ranging from 0.1 to 10 ng/mL (0.1, 0.2, 0.5, 1, 2, 5, and 10 ng/mL) were prepared to calculate target PFAS concentrations. The detailed recoveries, LOD and LOQ of each PFAS in the sediment are given in Table S3. PFASs concentrations were reported on a dry weight (dw) basis. ΣPFASs represents the sum of all the 18 target PFAS. Concentrations below LODs were reported as 0, and those between LODs and LOQs were reported as half of the corresponding LOQs. Normality and homogeneity of variance were tested using Shapiro-Wilk test and levene's test, respectively. Accordingly, independent t-test was used to evaluate the significance of difference in PFASs concentrations between riverine and coastal sediments. Spearman rank correlation analysis was performed to evaluate the relations between PFASs. The above statistical analyses were performed using SPSS (Version 22.0, SPSS Incorporate). Additionally, to characterize the similarities of PFASs and sampling sites, a principal component analysis (PCA) was performed using Canoco 5.0. The significance level was set at p = 0.05. Concentrations of PFASs in surface sediments from the Beibu Gulf are shown in Table 1 and Fig. 2. Concentrations of ∑PFASs ranged from 56.2 to 586.3 pg/g dw, with a mean and median value of 172.5 pg/g dw and 155.6 pg/g dw, respectively. The maximum ∑PFASs concentration was observed at site C7, which might be related to the PFAS source in an adjacent port, as demonstrated previously that some materials (paint and grease repellence) related to dock protection, ship maintenance and maritime navigation were able to elevate the PFASs levels in the surrounding area (Paul et al., 2009). Interestingly, ∑PFASs concentrations were significantly higher in coastal sediments than in riverine sediments (p < 0.05) (Table 1 and Fig. 2). This might be due to the 2
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Table 1 Concentrations (pg/g dw) and detection frequencies (df, %) of PFASs in the sediments from the Beibu Gulf. Riverine sediment
PFOA PFNA PFDA PFUnDA PFDoDA PFTrDA PFOS EtFOSAA FOSA ΣPFASs
Coastal sediment
Min
Max
Mean
Median
df (%)
Min
Max
Mean
Median
df (%)
4.8 n.d 10.3 n.d n.d n.d n.d n.d n.d 56.2
37.2 16.5 66.3 28.3 19.3 27.6 59.7 35.3 n.d 189.4
17.4 2.4 20.5 16.8 10.1 17.8 24.1 10.6 n.d 115.8
15.7 n.d 14.2 18.1 11.4 19.5 14.2 n.d n.d 112.1
100 14.3 100 92.9 85.7 92.9 100 42.9 0 100
6.6 n.d n.d 10.8 n.d 16.4 n.d n.d n.d 77.4
249.0 55.6 35.6 62.3 18.1 34.0 224.9 n.d n.d 586.3
61.5 18.4 16.4 23.6 9.9 20.6 56.5 21.2 27.7 211.0
42.1 17.7 14.8 19.4 10.7 20.2 51.1 1.6 2.6 177.5
100 81 95.2 100 85.7 100 81.0 9.5 9.5 100
n.d: not detected.
transportation of PFASs from southwest through oceanic currents and subsequently adsorbed onto the sediment particles (Fig. 1). In support of this speculation, sediment samples collected from the west (Fangchenggang) had higher concentrations of ∑PFASs compared to those from the east (Qinzhou and Beihai) of the Beibu Gulf, with their mean concentrations following the trend: Fangchenggang > Qinzhou > Beihai (Fig. 3). PFOA was the predominant PFAS with the concentration in the range of 4.8–249.0 pg/g dw and a mean level of 43.6 pg/g dw, followed by PFOS with corresponding values of not detected (n.d) −224.8 pg/g dw and 43.2 pg/g dw, respectively. In line with our results, PFOA and PFOS were the predominant PFASs in sediments from most other regions worldwide (Bao et al., 2010; Yeung et al., 2013; Pan et al., 2014a; Zhao et al., 2014; Liu et al., 2019). Nine out of 18 PFASs were detected, including C8–C13–PFCAs, C8–PFSAs, FOSA and EtFOSAA. The detection frequencies of these PFASs were as follows: PFOA (100%), followed by PFDA, PFUnDA and PFTrDA (97%), PFDoDA (86%), PFOS (71%), PFNA (54%), EtFOSAA (23%) and only 6% for FOSA. These frequently detected PFASs are long-chain PFASs with carbon chain length ≥8, whereas PFASs with carbon chain length < 8 were not detected in any samples and excluded from further data analysis. Therefore, it seems that long-chain PFASs are more likely to partition onto the sediment compared to short-chain PFASs (Yeung et al., 2013; Pan et al., 2014a). Several previous studies also reported low detection rates and concentrations of PFASs in sediment samples (Thompson et al., 2011; Long et al., 2013). For example, only PFOS, FOSA, and PFBA were detected with low detection rates (2–17%) and low concentrations in sediments collected from Puget Sound, WA (USA) (Long et al., 2013). The composition profiles of relative contributions of individual PFASs to the ∑PFASs are displayed in Fig. S1. PFOA made the greatest contribution to ∑PFAS in the sediments, with an average contribution of 22.3%. Other major PFASs were PFOS (21.1%), PFTrDA (14.2%), and
PFUnDA (13.5%) on a mean basis. Overall, the C8–C14 PFASs contributed 100% to the ΣPFASs, whereas C4–C7 PFASs made no contribution to the ∑PFASs. This suggests that physicochemical properties of the compound strongly influenced the distribution of PFASs in the sediment, likely due to the lower water solubility of long-chain PFASs relative to short-chain PFASs. Likewise, an earlier study reported that perfluorocarbon chain length was the most important factor that can influence the partition of PFASs onto sediment (Pan et al., 2014a). The results obtained here are consistent with findings reported in the majority of previous studies (Bao et al., 2010; Pan et al., 2014b). For example, PFOS and PFOA showed the highest contribution to target ∑PFASs in surface sediment samples from Haihe River and Dongjiang River in China as well as Bay of Bengal coast (Pan et al., 2014a; Zhao et al., 2014; Habibullah-Al-Mamun et al., 2016). It has been demonstrated that correlation analysis can be used to trace the potential sources of PFASs (Ahrens et al., 2009). Here PFOA was significantly positively correlated with PFNA and PFOS, and PFOS was significantly positively correlated with PFNA, PFDA, FOSA and PFTrDA (Table 2). This indicates that these chemicals may share similar source and transport routes (Gao et al., 2014). Further, as PFDA and PFUnDA could be generated via oxidation of PFASs precursors in the environment (Young et al., 2007), here the frequent detection of PFDA and PFUnDA may imply that atmospheric oxidation of PFASs precursors was a source of PFASs in our study area. The PFOS/PFOA ratio has been used to identify source regions in some studies, as higher PFOS/PFOA ratios were often found in locations closer to PFAS sources (So et al., 2004; Gao et al., 2014). Here the PFOS/PFOA ratios were < 1 at the majority of samples from the Beibu Gulf, suggesting that most sampling sites are not close to PFASs sources. The PCA was further applied to identify PFAS sources and characterize similarities among sampling sites. As shown in Fig. 4, PC 1 and PC 2 explained 45% and 20.5% of the total variation, respectively. Generally, samples from the coastal area clustered to the left part of the PCA diagram and had higher concentrations of PFDA, PFOS, FOSA, PFUnDA, PFOA, PFNA and PFDoDA, whereas samples from riverine area clustered to the right part and had higher concentrations of EtFOSAA and PFTrDA. These results suggest that there was a clear difference in PFAS concentrations between the riverine and coastal area. These results also suggest a different pattern of PFASs sources. Generally, PFOS and PFOA were the most frequently detected PFASs with the highest concentrations in the sediments worldwide, and the concentration of PFOS was usually higher than PFOA (Table S4). Likewise, PFOS and PFOA were the predominant PFASs in the present study. In comparison with findings reported previously in different regions worldwide (Table S4), PFOS and PFOA contamination in the Beibu Gulf was relatively low on a global perspective. PFOS concentrations in the sediment of the Beibu Gulf are similar to those detected in the Pearl River estuary (China; < LOD-0.32 ng/g) and Ariake Sea (Japan; 0.09–0.14 ng/g) (Nakata et al., 2006; Gao et al., 2015), but
Fig. 2. Concentrations of PFASs in sediments from the Beibu Gulf. 3
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Fig. 3. Boxplot of PFOA, PFOS, PFUnDA and ΣPFASs in sediments from the Beibu Gulf. Note: FCG, QZ and BH represent Fangchenggang, Qinzhou and Beihai. The solid line and short dashed line in the box denote median and mean concentration value of corresponding PFAS, respectively.
approximately one order of magnitude lower than those reported in German Bight (Germany; 0.02–5.36 ng/g) (Zhao et al., 2015), Bangladeshi coastal area (0.30–3.56 ng/g) (Habibullah-Al-Mamun et al., 2016) and Sydney Harbor (Australia; 0.80–6.20 ng/g) (Thompson et al., 2011). Nevertheless, much lower PFOS levels have been reported in Laizhou Bay (China; < 0.03–0.06 ng/g) (Zhao et al., 2013). Regarding PFOA, while comparable levels have been found in the Savannah River Estuary (USA; n.d-0.2 ng/g) (Kumar et al., 2009), German Bight (Germany; 0.007–0.43 ng/g) (Zhao et al., 2015) and Sydney Harbor (Australia 0–0.16 ng/g) (Thompson et al., 2011), higher PFOA levels have been reported in the Ariake Sea (Japan; 0.84–1.1 ng/g) (Nakata et al., 2006), Laizhou Bay (China; 0.07–1.8 ng/g) (Zhao et al., 2013) and Charleston Estuary (USA; 0.02–2.52 ng/g) (White et al., 2015). The relatively low concentrations of PFASs in Beibu Gulf are likely due to the low GDP and less PFASs-related industrial facilities in this region. Indeed, a previous study reported a positive correlation between coastal contamination of PFASs and socio-economic situations of the coastal areas (Kwok et al., 2015). PFOS and PFOA can induce various toxic effects on different trophic levels of organisms depending on their concentrations (Beach et al., 2006; Giesy et al., 2010; Zushi et al., 2012). Moreover, sediment has been recognized as a sink and reservoir of PFASs (Prevedouros et al.,
2006). Therefore, it is essential to understand the environmental risks of sediment-associated PFOS and PFOA to aquatic systems. We used risk quotient (RQ) to assess the environmental risks of PFASs in the sediments of the Beibu Gulf. The RQ of each PFAS was calculated by dividing the measured environmental concentration (MEC) by the predicted no-effect concentration (PNEC). An RQ value < 1 indicates no risk and an RQ ≥ 1 represents potential risk. The PNEC used for riverine sediment PFOS and PFOA were 4.9 ng/g and 86 ng/g, respectively, while the PNECs for marine sediment were ten times lower than the corresponding PNECs for riverine sediment (Zhao et al., 2013). The results show that all RQ values were much lower than one, suggesting negligible environmental risks associated with PFOS and PFOA in the sediments from the Beibu Gulf. In contrast, a previous study reported that PFOS and PFOA in sediments from Laizhou Bay can pose low risks to benthic invertebrates (Zhao et al., 2013). Furthermore, it is noteworthy that even low concentrations of PFASs in environment could lead to higher levels of PFASs in biota due to their persistent and bioaccumulative characteristics. Therefore, further study is required to assess the environmental risks and exposure risks of PFAS mixture. PFOA and PFOS were the two predominant PFASs in the sediment of the Beibu Gulf, but they would not pose environmental risks. Longchain PFASs were more frequently detected than short-chain PFASs,
Table 2 Spearman correlation coefficients (two-tailed) for individual PFASs concentrations in surface waters of the Beibu Gulf. PFOA PFNA PFOS PFDA EtFOSAA PFUnDA FOSA PFDoDA PFTrDA a b
PFNA
PFOS
PFDA
EtFOSAA
PFUnDA
FOSA
PFDoDA
0.430b 0.428a −0.312 0.467b 0.356a −0.172 0.114
0.435b −0.05 0.304 0.407a −0.099 0.395a
−0.168 0.449b 0.353a 0.102 0.198
0.013 0.109 −0.028 0.295
0.389a 0.358a 0.515b
−0.174 0.352
0.210
b
0.741 0.462b 0.325 −0.457b 0.343 0.290 −0.164 0.042
Correlation is significant at the 0.05 level. Correlation is significant at the 0.01 level. 4
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urban river sediments from Guangzhou and Shanghai of China. Chemosphere 80 (2), 123–130. Beach, S.A., Newsted, J.L., Coady, K., Giesy, J.P., 2006. Ecotoxicological evaluation of perfluorooctanesulfonate (PFOS). Rev. Environ. Contam. Toxicol. 186, 133–174. Boiteux, V., Dauchy, X., Bach, C., Colin, A., Hemard, J., Sagres, V., Rosin, C., Munoz, J.F., 2017. Concentrations and patterns of perfluoroalkyl and polyfluoroalkyl substances in a river and three drinking water treatment plants near and far from a major production source. Science of the Total Environment 583, 393–400. Chen, L., Tsui, M.M., Lam, J.C., Wang, Q., Hu, C., Wai, O.W., Zhou, B., Lam, P.K., 2019. Contamination by perfluoroalkyl substances and microbial community structure in Pearl River Delta sediments. Environ. Pollut. 245, 218–225. Gao, Y., Fu, J., Meng, M., Wang, Y., Chen, B., Jiang, G., 2015. Spatial distribution and fate of perfluoroalkyl substances in sediments from the Pearl River Estuary, South China. Mar. Pollut. Bull. 96 (1–2), 226–234. Gao, Y., Fu, J., Zeng, L., Li, A., Li, H., Zhu, N., Liu, R.Z., Liu, A.F., Wang, Y.W., Jiang, G., 2014. Occurrence and fate of perfluoroalkyl substances in marine sediments from the Chinese Bohai Sea, Yellow Sea, and east China Sea. Environ. Pollut. 194, 60–68. Giesy, J.P., Naile, J.E., Khim, J.S., Jones, P.D., Newsted, J.L., 2010. Aquatic toxicology of perfluorinated chemicals. Rev. Environ. Contam. Toxicol. 202, 1–52. Habibullah-Al-Mamun, M., Ahmed, M.K., Raknuzzaman, M., Islam, M.S., Negishi, J., Nakamichi, S., Sekine, M., Tokumura, M., Masunaga, S., 2016. Occurrence and distribution of perfluoroalkyl acids (PFAAs) in surface water and sediment of a tropical coastal area (Bay of Bengal coast, Bangladesh). Sci. Total Environ. 571, 1089–1104. Kim, D.H., Lee, J.H., Oh, J.E., 2019. Assessment of individual-based perfluoroalkly substances exposure by multiple human exposure sources. J. Hazard Mater. 365, 26–33. Kumar, K.S., Zushi, Y., Masunaga, S., Gilligan, M., Pride, C., Sajwan, K.S., 2009. Perfluorinated organic contaminants in sediment and aquatic wildlife, including sharks, from Georgia, USA. Mar. Pollut. Bull. 58 (4), 621–629. Kwok, K.Y., Wang, X.H., Ya, M., Li, Y., Zhang, X.H., Yamashita, N., Lam, J.C., Lam, P.K., 2015. Occurrence and distribution of conventional and new classes of per-and polyfluoroalkyl substances (PFASs) in the South China Sea. J. Hazard Mater. 285, 389–397. Lai, K.P., Li, J.W., Cheung, A., Li, R., Billah, M.B., Chan, T.F., Wong, C.K.C., 2017. Transcriptome sequencing reveals prenatal PFOS exposure on liver disorders. Environ. Pollut. 223, 416–425. Li, P., Xue, R., Wang, Y., Zhang, R., Zhang, G., 2015. Influence of anthropogenic activities on PAHs in sediments in a significant gulf of low-latitude developing regions, the Beibu Gulf, South China Sea: distribution, sources, inventory and probability risk. Mar. Pollut. Bull. 90 (1–2), 218–226. Liu, C., Gin, K.Y.H., 2018. Immunotoxicity in green mussels under perfluoroalkyl substance (PFAS) exposure: Reversible response and response model development. Environ. Toxicol. Chem. 37 (4), 1138–1145. Liu, Y., Zhang, Y., Li, J., Wu, N., Li, W., Niu, Z., 2019. Distribution, partitioning behavior and positive matrix factorization-based source analysis of legacy and emerging polyfluorinated alkyl substances in the dissolved phase, surface sediment and suspended particulate matter around coastal areas of Bohai Bay, China. Environ. Pollut. 246, 34–44. Long, E.R., Dutch, M., Weakland, S., Chandramouli, B., Benskin, J.P., 2013. Quantification of pharmaceuticals, personal care products, and perfluoroalkyl substances in the marine sediments of Puget Sound, Washington, USA. Environ. Toxicol. Chem. 32 (8), 1701–1710. Martin, J.W., Whittle, D.M., Muir, D.C.G., Mabury, S.A., 2004. Perfluoroalkyl contaminants in a food web from Lake Ontario. Environ. Sci. Technol. 38 (20), 5379–5385. Munoz, G., Budzinski, H., Babut, M., Lobry, J., Selleslagh, J., Tapie, N., Labadie, P., 2019. Temporal variations of perfluoroalkyl substances partitioning between surface water, suspended sediment, and biota in a macrotidal estuary. Chemosphere 233, 319–326. Nakata, H., Kannan, K., Nasu, T., Cho, H.-S., Sinclair, E., Takemura, A., 2006. Perfluorinated contaminants in sediments and aquatic organisms collected from shallow water and tidal flat areas of the Ariake Sea, Japan: environmental fate of perfluorooctane sulfonate in aquatic ecosystems. Environ. Sci. Technol. 40 (16), 4916–4921. Newsted, J.L., Holem, R., Hohenstein, G., Lange, C., Ellefson, M., Reagen, W., Wolf, S., 2017. Spatial and temporal trends of poly-and perfluoroalkyl substances in fish fillets and water collected from pool 2 of the Upper Mississippi River. Environ. Toxicol. Chem. 36 (11), 3138–3147. Nordén, M., Berger, U., Engwall, M., 2016. Developmental toxicity of PFOS and PFOA in great cormorant (Phalacrocorax carbo sinensis), herring gull (Larus argentatus) and chicken (Gallus gallus domesticus). Environ. Sci. Pollut. Control Ser. 23 (11), 10855–10862. Pan, C.G., Liu, Y.S., Ying, G.G., 2016. Perfluoroalkyl substances (PFASs) in wastewater treatment plants and drinking water treatment plants: Removal efficiency and exposure risk. Water Res. 106, 562–570. Pan, C.G., Ying, G.G., Liu, Y.S., Zhang, Q.Q., Chen, Z.F., Peng, F.J., Huang, G.Y., 2014a. Contamination profiles of perfluoroalkyl substances in five typical rivers of the Pearl River Delta region, South China. Chemosphere 114, 16–25. Pan, C.G., Ying, G.G., Zhao, J.L., Liu, Y.S., Jiang, Y.X., Zhang, Q.Q., 2014b. Spatiotemporal distribution and mass loadings of perfluoroalkyl substances in the Yangtze River of China. Sci. Total Environ. 493, 580–587. Pan, C.G., Yu, K.F., Wang, Y.H., Zhang, W., Zhang, J., Guo, J., 2019. Perfluoroalkyl substances in the riverine and coastal water of the Beibu Gulf, South China: Spatiotemporal distribution and source identification. Sci. Total Environ. 660, 297–305. Pan, C.G., Zhao, J.L., Liu, Y.S., Zhang, Q.Q., Chen, Z.F., Lai, H.J., Peng, F.J., Liu, S.S., Ying, G.G., 2014c. Bioaccumulation and risk assessment of per- and polyfluoroalkyl substances in wild freshwater fish from rivers in the Pearl River Delta region, South
Fig. 4. Principal component loadings for PFASs and sampling sites in sediment samples from the Beibu Gulf. Red circle and blue square represent riverine and coastal sampling sites, respectively. (For interpretation of the references to colour in this figure legend, the reader is referred to the Web version of this article.)
suggesting that long-chain PFASs have a stronger affinity to the sediment compared to the short-chain PFASs. The ΣPFASs concentrations were significantly higher in coastal than in riverine sediments. Additionally, there was a clear decreasing trend in ΣPFASs concentration from the west (Fangchenggang) to the east (Beihai) of the Beibu Gulf. Overall, PFASs concentrations in the sediment of the Beibu Gulf were lower than most other regions worldwide. Declaration of competing interest The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper. Acknowledgments The authors would like to thank the financial support by the National Natural Science Foundation of China (Nos. 41673105 and 91428203), Guangxi Innovation-driven Development Projects (GuikeAA18242031), Natural Science Foundation of Guangxi (2018GXNSFAA050144). Appendix A. Supplementary data Supplementary data to this article can be found online at https:// doi.org/10.1016/j.marpolbul.2019.110706. References Ahrens, L., Yamashita, N., Yeung, L.W.Y., Taniyasu, S., Horii, Y., Lam, P.K.S., Ebinghaus, R., 2009. Partitioning behavior of per- and polyfluoroalkyl compounds between pore water and sediment in two sediment cores from Tokyo Bay, Japan. Environ. Sci. Technol. 43 (18), 6969–6975. Bangma, J.T., Ragland, J.M., Rainwater, T.R., Bowden, J.A., Gibbons, J.W., Reiner, J.L., 2019. Perfluoroalkyl substances in diamondback terrapins (Malaclemys terrapin) in coastal South Carolina. Chemosphere 215, 305–312. Bao, J., Liu, W., Liu, L., Jin, Y., Ran, X., Zhang, Z., 2010. Perfluorinated compounds in
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C.-G. Pan, et al. China. Ecotoxicol. Environ. Saf. 107, 192–199. Pan, G., You, C., 2010. Sediment-water distribution of perfluorooctane sulfonate (PFOS) in Yangtze River estuary. Environ. Pollut. 158 (5), 1363–1367. Paul, A.G., Jones, K.C., Sweetman, A.J., 2009. A first global production, emission, and environmental inventory for perfluorooctane sulfonate. Environ. Sci. Technol. 43 (2), 386–392. Prevedouros, K., Cousins, I.T., Buck, R.C., Korzeniowski, S.H., 2006. Sources, fate and transport of perfluorocarboxylates. Environ. Sci. Technol. 40 (1), 32–44. Simmonet-Laprade, C., Budzinski, H., Babut, M., Le Menach, K., Munoz, G., Lauzent, M., Ferrari, B., Labadie, P., 2019. Investigation of the spatial variability of poly-and perfluoroalkyl substance trophic magnification in selected riverine ecosystems. Sci. Total Environ. 686, 393–401. So, M.K., Taniyasu, S., Yamashita, N., Giesy, J.P., Zheng, J., Fang, Z., Im, S.H., Lam, P.K.S., 2004. Perfluorinated compounds in coastal waters of Hong Kong, South China, and Korea. Environ. Sci. Technol. 38 (15), 4056–4063. Stock, N.L., Furdui, V.I., Muir, D.C., Mabury, S.A., 2007. Perfluoroalkyl contaminants in the Canadian Arctic: evidence of atmospheric transport and local contamination. Environ. Sci. Technol. 41 (10), 3529–3536. Thompson, J., Roach, A., Eaglesham, G., Bartkow, M.E., Edge, K., Mueller, J.F., 2011. Perfluorinated alkyl acids in water, sediment and wildlife from Sydney Harbour and surroundings. Mar. Pollut. Bull. 62 (12), 2869–2875. Wang, Y., Zhang, W., Lin, Y., Cao, W., Zheng, L., Yang, J., 2014. Phosphorus, nitrogen and chlorophyll-a are significant factors controlling ciliate communities in summer in the Northern Beibu Gulf, South China Sea. PLoS One 9 (7). White, N.D., Balthis, L., Kannan, K., De Silva, A.O., Wu, Q., French, K.M., Daugomah, J., Spencer, C., Fair, P.A., 2015. Elevated levels of perfluoroalkyl substances in estuarine sediments of Charleston, SC. Sci. Total Environ. 521, 79–89. Xia, P., Meng, X., Yin, P., Cao, Z., Wang, X., 2011. Eighty-year sedimentary record of heavy metal inputs in the intertidal sediments from the Nanliu River estuary, Beibu Gulf of South China Sea. Environ. Pollut. 159 (1), 92–99. Yeung, L.W.Y., De Silva, A.O., Loi, E.I.H., Marvin, C.H., Taniyasu, S., Yamashita, N., Mabury, S.A., Muir, D.C.G., Lam, P.K.S., 2013. Perfluoroalkyl substances and extractable organic fluorine in surface sediments and cores from Lake Ontario. Environ.
Int. 59, 389–397. You, C., Jia, C., Pan, G., 2010. Effect of salinity and sediment characteristics on the sorption and desorption of perfluorooctane sulfonate at sediment-water interface. Environ. Pollut. 158 (5), 1343–1347. Young, C.J., Furdui, V.I., Franklin, J., Koerner, R.M., Muir, D.C.G., Mabury, S.A., 2007. Perfluorinated acids in arctic snow: new evidence for atmospheric formation. Environ. Sci. Technol. 41 (10), 3455–3461. Zhang, J., Li, Y., Wang, Y., Zhang, Y., Zhang, D., Zhang, R., Li, J., Zhang, G., 2014. Spatial distribution and ecological risk of polychlorinated biphenyls in sediments from Qinzhou Bay, Beibu Gulf of South China. Mar. Pollut. Bull. 80 (1–2), 338–343. Zhao, L., Zhu, L., Yang, L., Liu, Z., Zhang, Y., 2012. Distribution and desorption of perfluorinated compounds in fractionated sediments. Chemosphere 88 (11), 1390–1397. Zhao, X., Xia, X., Zhang, S., Wu, Q., Wang, X., 2014. Spatial and vertical variations of perfluoroalkyl substances in sediments of the Haihe River, China. J. Environ. Sci. 26 (8), 1557–1566. Zhao, Z., Tang, J., Xie, Z., Chen, Y., Pan, X., Zhong, G., Sturm, R., Zhang, G., Ebinghaus, R., 2013. Perfluoroalkyl acids (PFAAs) in riverine and coastal sediments of Laizhou Bay, North China. Sci. Total Environ. 447, 415–423. Zhao, Z., Xie, Z., Tang, J., Zhang, G., Ebinghaus, R., 2015. Spatial distribution of perfluoroalkyl acids in surface sediments of the German Bight, North Sea. Sci. Total Environ. 511, 145–152. Zheng, Q., Zhang, R., Wang, Y., Pan, X., Tang, J., Zhang, G., 2012. Occurrence and distribution of antibiotics in the Beibu Gulf, China: impacts of river discharge and aquaculture activities. Mar. Environ. Res. 78, 26–33. Zhu, Z., Wang, T., Wang, P., Lu, Y., Giesy, J.P., 2014. Perfluoroalkyl and polyfluoroalkyl substances in sediments from South Bohai coastal watersheds, China. Mar. Pollut. Bull. 85 (2), 619–627. Zushi, Y., Hogarh, J.N., Masunaga, S., 2012. Progress and perspective of perfluorinated compound risk assessment and management in various countries and institutes. Clean Technol. Environ. Policy 14 (1), 9–20. Zushi, Y., Tamada, M., Kanai, Y., Masunaga, S., 2010. Time trends of perfluorinated compounds from the sediment core of Tokyo Bay, Japan (1950s-2004). Environ. Pollut. 158 (3), 756–763.
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