Article pubs.acs.org/est
Trophic Magnification and Isomer Fractionation of Perfluoroalkyl Substances in the Food Web of Taihu Lake, China Shuhong Fang, Xinwei Chen, Shuyan Zhao, Yifeng Zhang, Weiwei Jiang, Liping Yang, and Lingyan Zhu* College of Environmental Science and Engineering, Tianjin Key Laboratory of Environmental Remediation and Pollution Control, Key Laboratory of Pollution Processes and Environmental Criteria, Ministry of Education, Nankai University, Tianjin 300071, People’s Republic of China S Supporting Information *
ABSTRACT: Biomagnification of perfluoroalkyl substances (PFASs) are well studied in marine food webs, but related information in fresh water ecosystem and knowledge on fractionation of their isomers along the food web are limited. The distribution, bioaccumulation, magnification, and isomer fractionation of PFASs were investigated in a food web of Taihu Lake, China. Perfluorooctanesulfonate (PFOS) and perfluorocarboxylates (PFCAs) with longer carbon chain lengths, such as perfluorodecanoate (PFDA) and perfluoroundecanoate (PFUnA), were predominant in organisms, while perfluorohexanoate (PFHxA) and perfluorooctanoate (∑PFOA) contributed more in the water phase. The consistent profile signature of PFOA isomers in water phase with 3M electrochemical fluorination (ECF) products suggests that ECF production of PFOA still exists in China. Linear proportions of PFOA, PFOS and perfluorooctane sulfonamide (PFOSA) in the biota were in the range of 91.9− 100%, 78.6−95.5%, and 72.2−95.5%, respectively, indicating preferential bioaccumulation of linear isomers in biota. Trophic magnification factors (TMFs) were estimated for PFDA (2.43), perfluorododecanoate (PFDoA) (2.68) and PFOS (3.46) when all biota were included, suggesting that PFOS and long-chained PFCAs are biomagnified in the fresh water food web. The TMF of PFOS isomers descended in the order: n-PFOS (3.86) > 3+5m-PFOS (3.35) > 4m-PFOS (3.32) > 1m-PFOS (2.92) > m2PFOS (2.67) > iso-PFOS (2.59), which is roughly identical to their elution order on a FluoroSep-RP Octyl column, suggesting that hydrophobicity may be an important contributor for isomer discrimination in biota.
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INTRODUCTION Perfluoroalkyl substances (PFASs), including perfluorosulfonates (PFSAs) and perfluorocarboxylates (PFCAs), are widely used in various consumer products, such as refrigerants, agrochemicals, chemical catalysts/reagents, surfactants, and fire-fighting foams, due to their special physicochemical properties.1,2 Since perfluorooctanesulfonate (PFOS) was first detected in biota in 2001,3 PFASs have been identified in wildlife all around the world, such as in fish, birds, mammals, and even in remote Arctic wildlife.4−6 Two primary processes, electrochemical fluorination (ECF) and telomerization, have been used to synthesize PFASs. The ECF method has been used by 3M, one of the largest manufacturers of PFASs in the world, to produce perfluorooctanoate (PFOA) since 1947 and perfluorooctane sulfonyl fluoride (PFOSF, C8F17SO2F)-based products since 1949. The ECF products are composed of complex isomeric mixtures with rather consistent compositions: 70−80% linear and 20−30% branched isomers.7,8 Due to the suspected health effects of PFOS, 3M voluntarily phased out PFOS and its related products in 2000.8 They also ceased production of PFOA by the ECF method as of 2002. Thereafter, the telomerization method, © 2014 American Chemical Society
which was developed by Dupont in the 1970s and produces strictly linear geometry, becomes the predominant method to manufacture PFOA.9 Even though the production of PFOS and its precursors decreased since 2000 as a result of the voluntary phase out by 3M, the manufacturing of PFASs in Asia, especially in China, has increased. It was reported that the production of PFOS was 200−250 t/year during 2008−2011 in China.10 Many laboratory studies11,12 and field investigations5,13−15 demonstrated that PFASs, especially for PFOS and long-chain PFCAs, could be bioaccumulated in various organisms. Some of the recent interest in PFASs is about their magnification in food webs due to their unique chemical and biological stability. Nevertheless, the research about PFAS biomagnification is still limited compared to traditional lipophilic contaminants, such as polychlorinated biphenyls (PCBs) and polybrominated biphenyl ethers (PBDEs). Among the studies regarding PFAS biomagnification,13,14,16 most of them were about marine food webs and Received: Revised: Accepted: Published: 2173
July 15, 2013 January 20, 2014 January 25, 2014 January 26, 2014 dx.doi.org/10.1021/es405018b | Environ. Sci. Technol. 2014, 48, 2173−2182
Environmental Science & Technology
Article
high trophic level organisms (TL > 5), such as seabirds and marine mammals, were included, and inconsistent biomagnification results were observed. A few of them were about PFAS biomagnification in fresh water food webs and all mostly in Lake Ontario. Moreover, most of the studies took PFASs as single compounds without further identification of their isomers. Even though there are some studies about the isomeric bioaccumulations of PFOS and PFOA in organisms and humans,17,18 sparse information is available for the fractionation of the isomers along the food web. Loveless et al.19 found that the body weight of rodents was affected by PFOA and decreased in the following order: 80% linear/20% branched mixture > 100% linear > 100% branched PFOA. Therefore, the risk of a PFAS would be over- or underestimated if it is considered as a single compound without differentiating its isomers. Taihu Lake, located between Jiangsu and Zhejiang provinces, is the second largest freshwater lake in China. It not only provides drinking water for the surrounding population, but also plays an important role in the fishery industry in China. However, recent studies indicate heavy pollution of heavy metals and organic chemicals in Taihu Lake.20,21 PFASs were also detected in Taihu Lake (mean concentration 53.0 ng/L) and relatively high PFAS levels appeared in the Meiliang Area (mean concentration 102 ng/L),21 which is the most northern part of Taihu Lake and by the industrial city, Wuxi. Discharge of effluent from municipal wastewater treatment plants or/and direct discharge of industrial wastewater in the upstream could make contribution to the high level of PFASs in Meiliang area. In May of 2012, a sample campaign took place in Taihu Lake, wherein water and organisms at different trophic levels were sampled. The current study aimed to accomplish the following: (1) investigate the accumulation levels of PFASs and homologue profiles in the various aquatic organisms; (2) to study the isomeric profiles of PFOA, PFOS, and perfluorooctane sulfonamide (PFOSA) in the water and biota samples in Taihu Lake; and (3) to evaluate bioaccumulation and trophic magnification of PFASs and isomeric discrimination in aquatic organisms.
shrimp, and soft parts of the bivalves were freeze-dried at −60 °C for 48 h and stored at −20 °C for further extraction. Reagents, Extraction, and Analyses. Details regarding chemicals and reagents, extraction methods, and instrumental analysis are provided in the SI. Briefly, filtered water was concentrated using Cleanert PEP cartridges (made of polydivinylbenzene on which the surface is functionalized with vinyl prolidone, 500 mg/6 mL, Bonna-Agela Technologies, China). Zooplankton, invertebrates, and fish were extracted with 10 mM NaOH in methanol,22 followed by purification with Pesti-Carb (made of graphitized carbon by a distinct surface modification process, 500 mg/6 mL, BonnaAgela Technologies, China) and PWAX (a weak anion exchange SPE cartridge, 500 mg/6 mL, Bonna-Agela Technologies, China) method. Phytoplankton samples were extracted by DCM and methanol23 and followed by purification with Pesti-Carb and PWAX cartridges. PFASs and the isomers were separated and quantified by UPLC-MS/MS (electrospray ionization in negative mode) with a FluoroSep-RP Octyl column (Table S2 in the SI). Quality Control. A procedure blank was carried out with each batch of 12 samples to monitor for any method contamination. The method detection limits (MDLs) were defined as the concentration with a signal-to-noise ratio of 3 if the specific PFASs were not detected in the blanks. For analytes detected in the blanks, MDLs were defined as the mean blank concentration plus three times the standard deviation of the blank (see SI Table S3). Concentrations lower than MDLs were replaced with MDLs divided by the square root of 2, while those not detected were reported as n.d. (not detected), and zero was assigned for statistical purpose. The matrix spiked recoveries of water (10 ng/L), muscle (10 ng/g, dw), and phytoplankton (5 ng/g, dw) ranged from 93% to 109%, 73− 100%, and 70−103%, respectively (see SI Table S3, the recoveries were calculated relative to the internal standards in both the samples and standards after subtracting the response of the unspiked sample, the recoveries of internal standards were in the range 83−108%), and the concentrations of PFASs in samples were not corrected for recovery. Stable Isotope Determination and Variable Calculation. Stable-nitrogen (δ15N) and stable-carbon (δ13C) isotopes were used to determine the food web structure and trophic positions of the organisms tested in the current study. Details regarding δ15N analysis and calculation for trophic levels (TLs), bioaccumulation factor (BAF), and trophic magnification factors (TMFs) are provided in the SI. Nomenclature for Isomers. The nomenclature for specific PFOS and PFOA isomers (SI Table S2) is adopted from Benskin et al.24 Briefly, linear and perfluoroisopropyl are abbreviated as n- and iso-, respectively. For the other monomethyl branched isomers, m- refers to a perfluoromethyl branch, and the number preceding m- represents the carbon number on which the perfluoromethyl branch resides (e.g., 5-perfluoromethyl-PFOS is 5m-PFOS). The sum of all diperfluoromethyl isomers are abbreviated as m2-. The terms ∑PFOS and ∑PFOA are used when referring to the sum of all isomers. Due to the lack of branched standards of PFOSA, the proportions of the isomers of PFOSA were estimated based on their chromatographic peak areas relative to the total peak areas detected with m/z 499 to 78 transition, as reported by Asher et al.25 Statistical Analysis. All statistical analyses were performed with IBM.SPSS.Statistics.v20. Pearson’s rank correlation
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MATERIALS AND METHODS Sample Collection, Storage, and Handling. The sampling took place in May 2012 at the Meiliang area of Taihu Lake (see Supporting Information, SI, Figure S1) with the assistance of local fisherman. Surface water (n = 5), phytoplankton [pooled samples (p) = 3], zooplankton (p = 3), invertebrates [including Taihu Lake shrimp (n = 30), white shrimp (n = 6), freshwater mussel (n = 3), pearl mussel (n = 3)], fish [including minnow (n = 10), silver carp (n = 3), whitebait (n = 60), crucian (n = 6), lake saury (n = 10), carp (n = 3), mongolian culter (n = 20), mud fish (n = 10), Chinese bitterling (n = 60), and gobies (n = 30)] were collected (see SI Table S1). The samples were brought to the laboratory of the Research Center for Eco-Environmental Science, Chinese Academy of Science (Wuxi, China) immediately for further pretreatment (stored at −20 °C). Pelagic invertebrates (phytoplankton and zooplankton) were classified as plankton while benthic invertebrates, including shrimp and mussel were classified as invertebrates. Latin names, feeding habitat, body length, sample numbers, and water content are presented in SI Table S1. Homogenized plankton, muscle tissue of fish and 2174
dx.doi.org/10.1021/es405018b | Environ. Sci. Technol. 2014, 48, 2173−2182
Environmental Science & Technology
Article
∑PFOA ( 7).28 In addition, it suggests that the production volume of short-chained PFCAs and PFSAs, which are being used as alternatives29 of longer PFASs due to their lower toxicity,30 is increasing since the voluntarily phase out of PFOS and related products by 3M. The concentration of PFOSA, one of the precursors of PFOS, in water was 0.0456 ng/L, lower than that in the Pearl River in Guangzhou (ranging 0.073−0.34 ng/L),31 surface water in South Poland (ranging
