Bioaccumulation and trophic transfer of perfluorinated compounds in a eutrophic freshwater food web

Bioaccumulation and trophic transfer of perfluorinated compounds in a eutrophic freshwater food web

Environmental Pollution 184 (2014) 254e261 Contents lists available at ScienceDirect Environmental Pollution journal homepage: www.elsevier.com/loca...

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Environmental Pollution 184 (2014) 254e261

Contents lists available at ScienceDirect

Environmental Pollution journal homepage: www.elsevier.com/locate/envpol

Bioaccumulation and trophic transfer of perfluorinated compounds in a eutrophic freshwater food web Jian Xu a, b, Chang-Sheng Guo a, b, Yuan Zhang a, b, *, Wei Meng a, b a b

State Key Laboratory of Environmental Criteria and Risk Assessment, Chinese Research Academy of Environmental Sciences, Beijing 100012, China Laboratory of Riverine Ecological Conservation and Technology, Chinese Research Academy of Environmental Sciences, Beijing 100012, China

a r t i c l e i n f o

a b s t r a c t

Article history: Received 2 June 2013 Received in revised form 4 September 2013 Accepted 5 September 2013

In this study, the bioaccumulation of perfluorinated compounds from a food web in Taihu Lake in China was investigated. The organisms included egret bird species, carnivorous fish, omnivorous fish, herbivorous fish, zooplankton, phytoplankton, zoobenthos and white shrimp. Isotope analysis by d13C and d15N indicated that the carnivorous fish and egret were the top predators in the studied web, occupying trophic levels intermediate between 3.66 and 4.61, while plankton was at the lowest trophic level. Perfluorinated carboxylates (PFCAs) with 9e12 carbons were significantly biomagnified, with trophic magnification factors (TMFs) ranging from 2.1 to 3.7. The TMF of perfluorooctane sulfonate (PFOS) (2.9) was generally comparable to or lower than those of the PFCAs in the same food web. All hazard ratio (HR) values reported for PFOS and perfluorooctanoate (PFOA) were less than unity, suggesting that the detected levels would not cause any immediate health effects to the people in Taihu Lake region through the consumption of shrimps and fish. Ó 2013 Elsevier Ltd. All rights reserved.

Keywords: Bioaccumulation Trophic transfer Perfluorinated compounds Food web

1. Introduction Perfluorinated compounds (PFCs) including perfluorinated carboxylates (PFCAs) and perfluorinated sulfonates (PFSAs) and their precursors, a group of anthropogenic organofluorine chemicals, have been manufactured for more than 50 years and are widely used in industry, particularly in the manufacture of electronic and textile products (Giesy and Kannan, 2002; Prevedouros et al., 2005). They are environmentally recalcitrant and have a bioaccumulation potential similar to other persistent organic pollutants (POPs). Recent reports have revealed that PFCs have toxicological properties such as neonatal mortality and carcinogenicity (Guruge et al., 2006; Kumar, 2005). Based on a rat reproduction experiment, USEPA speculated that current maternal PFOA concentrations might cause adverse effects in human offspring (Martin et al., 2004; USEPA, 2003). Perfluorooctane sulfonate (PFOS) and its salts have been listed as POPs under the Stockholm Convention. PFCs contain a carbonefluorine covalent bond that makes them resistant to metabolism and degradation in the environment. This leads to high trophic magnification factors (TMFs) and the potential for accumulation in various species in the food web (Martin et al.,

* Corresponding author. E-mail address: [email protected] (Y. Zhang). 0269-7491/$ e see front matter Ó 2013 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.envpol.2013.09.011

2004; Tomy et al., 2004). PFCAs and PFSAs have been detected in blood and tissues of humans and wildlife globally, even in the remote regions such as the Arctic (Domingo, 2012; Kelly et al., 2009). Recent studies indicated that exposure to PFOS and FPCAs may arise directly from emission and exposure to PFOS itself, or indirectly via the environmental release and degradation of PFOS-precursors (Asher et al., 2012; Ellis et al., 2004; Müller et al., 2011; Peng et al., 2013). Many field studies have reported biomagnification of PFCs in aquatic food webs, especially for PFOS and PFCAs with eight to twelve carbons (Houde et al., 2006; Kelly et al., 2009; Loi et al., 2011; Martin et al., 2004; Müller et al., 2011; Powley et al., 2008; Tomy et al., 2004, 2009). Most of these studies, however, are mainly focusing on marine or brackish food webs (Kelly et al., 2009; Loi et al., 2011; Powley et al., 2008; Tomy et al., 2004, 2009), with the varying bioaccumulation patterns of PFCs depending on salinity levels and trophic status (Loi et al., 2011). Only few studies investigated the PFCs bioaccumulation in the freshwater food web, for example, in the Lake Ontario (Martin et al., 2004), not to mention the highly eutrophic freshwater lakes. Nowadays the eutrophication of inner lakes is a common problem worldwide, from Lake Okeechobee in the United States to Lake Victoria in Africa and Japan’s largest lakes, Biwa and Kasumigaura (Stone, 2011). However, little information is available on the bioaccumulation and trophic magnification of POPs in the eutrophic freshwater food webs. Taihu Lake, with an area of 2250 square kilometers and an average depth of 1.9 m, is the second largest lake in China, which

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serves as drinking water resources, irrigation water, aquaculture farm as well as recreational attractions. From the late 1980s, water and soil pollution from industry, agriculture, and urban wastes has been increasing significantly in the Taihu Lake region (Ke et al., 2009; Yang et al., 2008). The worsening blooming of toxic algae in Taihu Lake occurred since 1987, and culminated in a massive bloom in 2006 and 2007. As one of the notorious highly eutrophic lakes in China, the environmental pollution of the lake has drawn much concern. Recent studies have reported the occurrence of organic contaminants, such as polycyclic aromatic hydrocarbon (PAHs), polychlorinated biphenyls (PCBs), organochlorine pesticides (OCPs) and polybrominated diphenyl ethers (PBDEs) in the water, sediments, benthic organisms and fish in the lake (Feng et al., 2003; Ke et al., 2009; Liu et al., 2009; Wang et al., 2011, 2012a; Yu et al., 2012). However, the bioaccumulation of POPs, such as PFCs in the food web of Taihu Lake, associated with longterm exposure scenario in humans and wildlife is still a critical data-gap. The objectives of this study are as follows: (1) to determine the concentrations and composition profiles of PFCs in water, sediment and biota at different trophic levels in Taihu Lake; (2) to investigate the bioaccumulation and biomagnification potential of target compounds in this eutrophic freshwater food web, with comparison to other food webs; and (3) to evaluate the contribution and hazard of fish and shrimp consumption to the total PFCs exposure in humans.

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using a 6410A mass spectrometer (Agilent, Palo Alto, CA) after chromatographic separation with an Agilent 1200 LC equipped with a ZORBAX Eclipse C18 column. 2.2.2. Quality assurance and quality control (QA/QC) To achieve lower detection limits, all of the accessible polytetrafluoroethene (PTFE) and fluoropolymer materials were removed from the instruments and apparatus to minimize background signal caused by contamination. All of the target chemicals were spiked into the test samples, and the samples were extracted and analyzed following the analytical procedures. The recoveries were evaluated by subtracting the background levels from the detected concentrations. Procedural blanks were consistently analyzed to each batch of ten samples. Matrix recoveries ranged from 61 to 118% for water, 69 to 128% for sediment, 76 to 123% for shrimp, 72 to 121% for fish tissue, 59 to 113% for plankton, 87 to 117% for zoobenthos, 62 to 115% in muscle of birds, respectively. Matrix recovery tests were conducted in triplicate, and the relative standard deviations (RSDs) were less than 18%. The details of limits of quantification (LOQ) and calibration curve are given in the Supporting Information. 2.2.3. Stable isotope analysis Determination of carbon and nitrogen stable isotope ratios (d13C and d15N) were conducted for all species studied to investigate the diet relationship in this food web. Detailed information is provided in the Electronic Supplementary Information.

2. Sampling and chemical analyses 2.1. Sample collection Surface water (n ¼ 30), surficial sediment (n ¼ 30), phytoplankton (mainly include Chlorophyta, Bacillariophyta and Cyanophyta), zooplankton (mainly include Copepoda, Cladocera, and Rotifers), two zoobenthos species (Bellamya sp. (snail) (n ¼ 9) and Corbiculidae (bivalve) (n ¼ 8)), white shrimp (Exopalaemon modestus Heller) (n ¼ 18), fish samples of nine different species, i.e. Hypophthalmichthys molitrix (n ¼ 10), Protosalanx hyalocranius (n ¼ 6), Hemiculter leucisculus (n ¼ 7), Aristichthys nobilis (n ¼ 4), Hyporhamphus intermedius (n ¼ 6), Pelteobagrus fulvidraco (n ¼ 4), Erythroculter ilishaefor (n ¼ 8), Cyprinus carpio (n ¼ 7), Coilia ectenes (n ¼ 22), and two egret bird species (Egrets and Night Herons) as prey animals were collected from Taihu Lake in May 2010. Detailed information on the sampling site and the corresponding samples is given in the Electronic Supplementary Information (Fig. S1, Table S1eS3). 2.2. Chemical analyses 2.2.1. Sample extraction, clean-up and instrumental analysis Details regarding chemicals and reagents, extraction methods, and instrumental analyses are provided in the Supporting Information. Briefly, water samples were extracted with Oasis WAX cartridges (Taniyasu et al., 2005, 2008). Sediment samples were firstly sonicated with methanol, and the extract was rotary evaporated and further diluted by deionized water, and subjected to clean up with an Oasis WAX-solid phase extraction (SPE) method. The homogenized tissue of biota samples was alkaline digested (Kelly et al., 2009; Shi et al., 2010; Taniyasu et al., 2005), and the concentrated extract was reconstituted in 200 mL water and cleaned up with a preconditioned Oasis WAX cartridge. Separation and determination of PFCs was performed using high performance liquid chromatography-tandem mass spectrometry (HPLC-MS/MS) (electrospray ionization in negative mode). Analytes were quantified by an internal method. PFCs were detected

2.2.4. Trophic levels (TL), TMF and bioaccumulation factors (BAFs) calculation The TMF provides information on the average change in contaminant concentration per relative TL and is calculated using the natural logarithm of the concentration of individual organisms versus their TL (Fisk et al., 2001; Tomy et al., 2004). The calculation is based on the relationship between TL and PFC concentration:

ln concentrationðwet weight; wwÞ ¼ a þ ðb  TLÞ

(1)

TLs were determined using equations slightly modified from Fisk et al. (2001). TL was calculated for each individual sample of zooplankton and fish using the following equation:

.  15 15 3:8 TLconsumer ¼ 2 þ d Nconsumer  d Nzooplankton

(2)

where d15Nzooplankton equals 11.3, and 3.8 is the enrichment factor constant. Captive-rearing studies on birds suggest that a diet-tissue isotopic fractionation factor of þ2.4& is appropriate for these taxa (Tomy et al., 2004). Following the derivation outlined in Tomy et al. (2004) and Fisk et al. (2001), we used the equation:

h  . i 15 15 TLconsumer ¼ 3 þ d Nconsumer  d Nzooplankton þ 2:4 3:8 (3) The slope b of Eq. (1) was used to calculate TMF using:

TMF ¼ eb

(4)

Statistical significance of the regression Eq. (4) was defined at p < 0.05. Bioaccumulation factors (BAFs) are used to investigate the accumulation of PFCs in organisms, which represents chemical uptake from multiple exposure pathways including water and food. BAF is defined as the ratio of the concentrations of PFCs in tissues

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(ng/kg, ww) and the concentrations in the dissolved phase of water (ng/L), using the following equations:

BAF ¼ PFC conc: in aquatic speciesðwwÞ=PFC conc: in water (5) 3. Results and discussion 3.1. Trophic positions of organisms in the freshwater food web of Taihu Lake There was a wide range of d15N in this part of the freshwater food web (7.7e21.2&; Table S4). The mean d15N values can be grouped as zooplankton and zoobenthos (Bellamya sp. and Corbiculidae) (11e12&), herbivorous fish (14e16&), omnivorous fish (17e18&), and carnivorous fish and egrets (19e21&). The trophic structure of this freshwater food web is calculated based on ranges in d15N values converted to TL (Eqs. (2) and (3)). With the trophic level of 2.0 set for zooplankton which were assumed as the primary consumers because of their herbivorous feeding on primary producers (phytoplankton) (Post, 2002), the trophic positions calculated for the organisms sampled in this study ranged from 1.1 to 4.6 (Table S4). Zooplankton and zoobenthos represented the second trophic level (mean TL of 2e2.5), whereas the herbivorous fish and omnivorous fish were intermediate between the second and third (mean TL of 2.9e3.7). Carnivorous fish and egrets represented between the third and fourth trophic level (mean TL of 3.7e4.6). White shrimp showed comparatively higher d15N values than other individuals of the fish species (Table S4), possibly due to their occasional scavenging for organisms of upper trophic levels (Shi and Yan, 1995). 3.2. PFCs in water and sediment An overview of PFCAs and PFOS concentrations in both water and sediment in Taihu Lake can be found in Fig. S2. Of the 12 PFCs analyzed in this study only PFCAs with six to nine carbons and PFOS were regularly detected in water. High concentrations of PFOA (28.1  16 ng/L), PFHxA (11.2  6.4 ng/L), PFNA (3.0  1.5 ng/L), and PFOS (3.5  2.6 ng/L) were observed, indicating the predominance of short-chain PFCs in water samples. In the sediments, PFOA, PFNA, PFDA, PFUnDA, PFDoA and PFOS were commonly detected, and PFOS was the dominant PFC (0.92  1.4 ng/g dw), followed by PFUnDA (0.43  0.29 ng/g dw) and PFNA (0.24  0.04 ng/g dw). It is noticeable that the long-chain PFCAs (C11, C12) were only detectable in sediments, confirming their high affinity for particles and potential accumulation in the sediment (Fig. S2) (Ahrens et al., 2009; Higgins et al., 2007). The spatial distribution of PFCs showed that the highest PFOA concentration in water was in S2 from Zhushan Bay (73.8 ng/L), followed by S20 in Gonghu Bay (50.9 ng/L), whereas the lowest was from S9, S11, and S25. The predominant PFCs in sediments were PFOS and PFUnDA, the sum of which was more than 50% of the total PFCs for most sites. The sediments from Zhushan Bay and Gonghu Bay also presented higher total PFCs concentrations (S2 for 8.2 ng/g dw and S20 for 5.6 ng/g dw, respectively) compared to those from west and south coast of Taihu Lake, and the lowest value was found in the lake center. This regional difference was likely related to the use and emission of PFCs around the lake (Yang et al., 2011). PFCs concentrations in inner bays (S1, S2, S18, S19 and S20) were generally higher than those in outer bays (S5, S15, S16 and S22), illustrating a descending trend along the flow directions. The north part of Taihu Lake was surrounded by Changzhou City, Wuxi City and Suzhou City, the several highly developed cities in China. Much

Fig. 1. Concentrations and compositional patterns of PFCs detected in food web samples collected from Taihu Lake (Absence of bars indicates concentrations below LOQ).

more anthropogenic inputs can be expected, since wastes generated in these cities may be discharged into Taihu Lake through several canals, resulting in the highly pollution of Zhushan Bay, Meiliang Bay and Gonghu Bay (Fig. S1). The much higher PFCs levels in north part of Taihu Lake was consistent with previous research on other organic pollutants such as PAHs, OCPs and PBDEs (Liu et al., 2009; Wang et al., 2012b; Zhang et al., 2012a, 2012b), where north part was more influenced by human activities. 3.3. PFC concentrations and composition in biota PFC concentrations detected in different organisms from Taihu Lake are illustrated in Fig. 1 and Table S4. PFCs were generally detected (>LOQ) in more than 60% of phytoplankton, zooplankton, fish, white shrimp and egret samples analyzed. PFCAs (C8eC12) and PFOS were detected in all of the biological samples. PFBA and PFPA were not detected, while PFHpA and PFTrA were less frequently detected (<50%). PFHxS was only detected in P. fulvidraco, C. carpio and egret. Organic pollutant levels in biota may be affected by diet choice and metabolic capability of animals (Tomy et al., 2004), which may explain the significant difference of PFCs levels among various aquatic animals. PFOS was the dominant PFC ranging from 0.7 to 20.9 ng/g ww in the aquatic biota samples of Taihu Lake, which accounted for 17.8e 47.7% of the total PFCs (Table S4 and Fig. 2). Interestingly, the proportion of PFOS to the total PFC concentrations in lower TLs such as zooplankton, zoobenthos and herbivorous fish (28.3%e42.6%) were comparable to the levels in higher trophic organisms, e.g., carnivorous fish species and prey bird species (38.9%e47.3%), which was in contrast to previous reports that the PFOS proportions were enriched from lower to higher trophic organisms (Loi et al., 2011; Powley et al., 2008). Concentrations of PFOS in fish were higher (11.07  4.09 ng/g ww) than those in shrimp (2.26  1.12 ng/g ww), phytoplankton (1.25  1.38) and zooplankton (0.94  1.84 ng/g ww). The PFOS levels in Taihu fish were lower than the reported values in the fillets of common carp in the Mississippi River (11e 90 ng/g ww) (Ye et al., 2008), much lower than that in the fish collected from Lake Ontario, Canada (mean concentration of 46e 450 ng/g ww) [5](Martin et al., 2004), but higher than the levels in

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Fig. 2. Profiles of PFCs in organisms from the food web of Taihu Lake.

whole-body homogenates of fish from the Mai Po Marshes Nature Reserve of Hong Kong (2.70e8.20 ng/g ww) (Loi et al., 2011)and Sarasota Bay in Florida, USA (3.1e8.8 ng/g ww) (Houde et al., 2006), and comparable to the levels in several species of fish from Baiyangdian Lake in China (0.51e13.7 ng/g ww) (Shi et al., 2012). In the aquatic biota samples of the Taihu Lake food web, PFUnDA (C11, 0.20e9.41 ng/g ww) was the predominant PFCA which contributed 5.9e25.2% to the total PFCs, followed by PFDA (C10, 0.06e10.3 ng/g ww) which accounted for 1.1e27.3% of the total PFCs (Fig. 2). This is consistent with studies of oceanic fish from Asian coastal waters and freshwater fish from Chinese lakes (Hart et al., 2008; Shi et al., 2012) where C10 and C11 were predominant. Organisms at lower TLs such as plankton and zoobenthos contained PFUnDA (C11, 0.44  0.12 ng/g ww) and PFDoA (C12, 0.35  0.03 ng/g ww), which was similar to the report from Mai Po Marshes Nature Reserve of Hong Kong (Loi et al., 2011), but in contrast to previous reports that PFOA (C8) and PFNA (C9) were the two predominant PFCAs in zooplankton (Houde et al., 2006; Martin et al., 2004; Tomy et al., 2004, 2009). For PFCAs in the present study, PFOA (C8) and PFNA (C9) were either less detected in most biota samples or presented at lower levels than other PFCAs (C10eC12). This observation is similar to that reported for samples from the Charleston Harbor (Houde et al., 2006). In contrast to the observations that PFHxS was above detection limits only in zooplankton and phytoplankton (Loi et al., 2011), in this study PFHxS was found in carnivorous fish and egrets, which is possibly due to their occasional scavenging for unknown organisms in the eutrophic Lake (Liu, 2008). Egret and P. fulvidraco situated at the higher end of the food web had high levels of PFDA, PFUnDA and PFOS, respectively. The different profiles of contamination between locations indicated that PFC inputs varied with geographical regions around the world. 3.4. Food web biomagnification BAFs of PFCs in the aquatic species from the food web of Taihu Lake are presented in Fig. 3. Compared to the several other PFCs in fish, the logBAF values of PFOA were the lowest between 0.99 and 1.82 in this study, which is lower than the fish from Baiyangdian Lake (1.77e2.78) (Shi et al., 2012) and from Charleston (2.17) (Houde et al., 2006). The logBAF of PFOA for zooplankton and phytoplankton were 1.47 and 1.94, which is comparable to 1.91 and 2.43 for zooplanktons from Charleston (Houde et al., 2006) and Mai Po Marshes Nature Reserve (Loi et al., 2011), respectively. The logBAF values for PFOS in fish ranged from 2.95 to 3.71, consistent

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Fig. 3. Bioaccumulation factor (BAF) of PFCs in the aquatic species from the food web of Taihu Lake.

with the values in Lake Trout from the Great Lakes (Furdui et al., 2007) and Baiyangdian Lake (Shi et al., 2012). The greatest logBAF for aquatic species from the food web was found for PFDoDA (median: 3.71, range: 2.89e4.06), followed by PFUnDA (median: 3.63, range: 2.50e4.17), and PFOS (median: 3.27, range: 2.23e3.77), while relatively lower logBAF values were found for PFOA (median: 1.37, range: 0.75e1.82), PFNA (median: 2.67, range: 1.69e2.97), and PFDA (median: 3.13, range: 1.48e3.75). The lowest logBAF value was found in zooplankton and zoobenthos in this food web. This conclusion is in agreement with the results by previous studies that PFCAs with <7 fluorinated carbons are not considered bioaccumulative, and bioaccumulative potential is limited by molecular sizes for PFCAs with >11e12 fluorinated carbons (Conder et al., 2008; Loi et al., 2011). The higher accumulation potential for longchain PFCAs and PFOS in aquatic organisms was also verified by Martin et al. (Martin et al., 2004) The difference of logBAFs reflected different capacities of biota to bioaccumulate and metabolize PFCs in different species. Stable isotope analysis was employed to characterize the diet preference and trophic levels of organisms. The d15N is used to infer the position of organisms in food chains because the d15N values would enrich by 2e5& per TL, and d13C values are commonly used to identify the food sources of organisms, with the carbon isotope ratio generally indicating 1& enrichment with each increasing TL (Hobson and Welch, 1992; Loi et al., 2011). In the food web of Taihu Lake, zooplankton had the highest d13C value of 20.5  0.65&, followed by zoobenthos with the d13C value of 21.8  0.78& (Fig. S3). These values were similar to the d13C content in the sediment (22.5  2.1&), suggesting that sediment was a potential carbon source to zoobenthos (Loi et al., 2011). The d15N difference (D15N) between zooplankton (11.36  1.2&) and herbivorous fish (14.96  0.4&) was 3.4&, which fell in the assumed D15N range of 3.4e3.8& (Ben-David et al., 2001; Hobson and Welch, 1992), suggesting that herbivorous fish was feeding on a nitrogen rich diet in the eutrophic lake (Ben-David et al., 2001; Hobson and Welch, 1992; Müller et al., 2011). Distinctive groupings of d15N and d13C among different species across different TLs (Table S4, Fig. S3) implied that the biota species had d13C signatures that corresponded well with their feeding behaviors (Loi et al., 2011). Compared with the relatively narrow range of d13C and d15N values in the sediment and zoobenthos, a wider range of d13C (20.5& to 25.5&) and d15N values (11.3&e21.2&) were found in the zooplankton and fish species/bird species, suggesting that these egrets and carnivorous fish in the water environment of Taihu Lake

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Fig. 4. Regressions between trophic levels and the logPFC concentrations (ng/g ww) in the aquatic species from the food web of Taihu Lake. Data points are arithmetic means and error bars represent range of 1 SD. Linear regression of the logarithm data with TMF values >1 reveals biomagnification in the food web. A TMF equal to 1.0 indicates no significant association of PFC concentrations with TL.

had more diverse food sources (Liu, 2008). Wet weight concentrations of PFCs (ng/g ww) increased significantly (p < 0.05) with increasing trophic levels (Fig. 1, Table S4). The PFC composition profiles were obviously different in the sediment and zoobenthos samples, suggesting that food sources were only one factor determining PFC exposure levels. TMF is generally used to evaluate the bioaccumulation potentials of persistent pollutants in biological samples. The bioaccumulation potential of PFCs, evaluated by TMFs, was mathematically defined

as the slope of the regression model obtained from a plot of contaminant concentrations in organisms versus trophic levels (Conder et al., 2008). The regressions between trophic levels and the wet weight concentrations of PFC in the aquatic species are presented in Fig. 4. Among the analyzed PFCs, PFOS, PFNA, PFDA, PFUnDA and PFDoDA showed significant (p < 0.05) correlations with TLs. The TMF values of these compounds were all greater than 1 (TMF ¼ 2.9 for PFOS, 2.1 for PFNA, 3.7 for PFDA, 3.1 for PFUnDA, and 2.4 for PFDoDA), indicating their biomagnification in the present

J. Xu et al. / Environmental Pollution 184 (2014) 254e261 Table 1 Trophic magnification factors (TMFs) of PFCs around the world. PFCs

Food Food Food Food Food Food Food Food web 8 web 1a web 2b web 3c web 4d web 5e web 6f web 7g (this study)h

PFOS PFOA PFNA PFDA PFUnDA PFDoDA PFTrA PFTeA

6.3 2.1 3.8 6.3 13.7 nd nd nd

11 1.93 4.23 4.18 4.79 2.96 nd 1.97

5.88 0.58 1 3.67 4.71 1 2.45 1

1.8 6.3 2.4 2.2 2.3 0.6 nd nd

6.3 nd nd nd nd nd nd nd

3.1 nd nd nd nd nd nd nd

1.30 nd nd 1.50 1.74 1.38 nd nd

2.9 nd 2.1 3.7 3.1 2.4 nd nd

a A marine food web from the western Canadian Arctic, which consisted of pelagic amphipod, Arctic copepod, fish and marine mammals (Tomy et al., 2009). b A Canadian Arctic marine food web, which consisted of macroalgae, bivalve, fish, seabird and marine mammals (Kelly et al., 2009). c A food web from Lake Ontario in Canada, which consisted of fish and mammals (Martin et al., 2004). d A food web of Charleston Harbor in USA, which consisted of zooplankton, fish, and bottlenose dolphin (Houde et al., 2006). e A food web of Sarasota Bay in USA, which consisted of zooplankton, fish, and dolphin (Houde et al., 2006). f An Eastern Arctic Marine Food Web, which consisted of zooplankton, bivalve, redfish, seabird, and marine mammal (Tomy et al., 2004). g A subtropical food web in the Mai Po Marshes Nature Reserve in Hong Kong, which consisted of zooplankton, worms, shrimps and fish (Loi et al., 2011). h This study; nd: not detectable.

food web. No significant trend was observed for PFOA (p ¼ 0.14) and PFTrA (p ¼ 0.13) in this study, which was in contrast to the previous reports that PFOA was biomagnified in the marine food web from the western Canadian Arctic (TMF ¼ 1.93) (Kelly et al., 2009) and a food web of Charleston Harbor in USA (TMF ¼ 6.3) (Houde et al., 2006), with PFOA having a significant TMF value (p < 0.01). In the Taihu food web the highest TMF value was for PFDA (TMF ¼ 3.7), followed by PFUnDA (TMF ¼ 3.1). This result was different from earlier studies that PFOS was reported with the greatest TMF value in many food webs (Table 1). For instance, the TMF values for PFOS were 3.1 in an eastern Arctic (Baffin Island) marine food web (Tomy et al., 2004), 6.3 in the marine food web from the western Canadian Arctic (Tomy et al., 2009) and Sarasota Bay food web (Houde et al., 2006), and 5.88 in a piscivorous food web from Lake Ontario (Martin et al., 2004). However, a TMF value of 2.9 for PFOS in this study was higher than the values of 1.8 from Charleston Harbor in USA (Houde et al., 2006) and 1.3 from Mai Po Marshes Nature Reserve in Hong Kong (Loi et al., 2011), respectively. The discrepancy of the TMF values in different food webs might be ascribed to the different PFC levels in the organisms, the different environmental conditions (e.g., the water temperature and water chemistry), metabolism from precursors and the different food web compositions. Taihu Lake is a highly eutrophic lake, with high frequency of algae blooming since the late 1970s (Chen et al., 2012; Yang et al., 2008). The contaminants inputs from surrounding industry, agriculture, and urban wastes make the PFC levels in the samples higher than those from Charleston Harbor, USA and Mai Po Marshes Nature Reserve in Hong Kong (Chen et al., 2012; Feng et al., 2003; Liu et al., 2009; Yang et al., 2011). Besides, Taihu Lake locates in the north subtropical region, where the water temperature is higher than other areas such as Lake Ontario (Canada Arctic) and Sarasota Bay (remote Arctic area) (Houde et al., 2006; Martin et al., 2004). The higher water temperature might enhance the organisms’ uptake and elimination capacity for certain PFCs (Houde et al., 2008), giving rise to the different TMFs for these PFCs in food webs. Additionally, organisms in this eutrophic lake might have the stronger metabolic capacity for PFCs, compared to those from Lake Ontario and Mai Po Marshes Nature Reserve food webs. Indirect evidence suggested that the species in the middle trophic position of Taihu food web, such as the herbivorous and omnivorous fish, might have strong

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absorption capacity for certain PFCs (Yu et al., 2012), resulting in the higher TMF values. Compared with the Canadian Arctic marine and Sarasota Bay, the lower TMFs from this study were possibly due to the PFCs occurrence in the relatively broader range of TLs. For example, marine mammals such as bottlenose dolphin, beluga whale, and ringed seal were the top predators in these food webs (Houde et al., 2006; Tomy et al., 2009), while the top predator in the present food web was an omnivorous fish and egrets. In addition, the indirect source of PFOS in biota has been detected by the enrichment of PFOS enantiomers in food web in Ontario Lake (Asher et al., 2012), and the occurrence of fluorotelomer alcohols in sediments may also contribute to the potential bioaccumulation of PFCAs to biota samples (Peng et al., 2013). All of these factors can contribute to the variation of TMF values. To the best of our knowledge, this is the first report to examine the trophic transfer of PFCs in a subtropical freshwater food web, and our results suggest that bioaccumulation and biomagnification of PFCs differed from those reported in previous studies of different food webs. Assessment of whether these PFCs would be a significant source of human exposure is further required. 3.5. Assessment of consumer risks from the intake of PFCs residues Fish consumption has been suggested as the major source of human dietary PFOS exposure (Berger et al., 2009; Ericson et al., 2008). To assess potential impacts on human health associated with the consumption of contaminated fish, a risk assessment based upon a defined estimated daily intake (EDI) is proposed:

EDIðng=kg=dÞ ¼ fish consumptionðg=kg=d; ww basisÞ  PFC concentrationðng=g wwÞ The hazard ratio (HR) is calculated by Loi et al. (2011)

HR ¼ EDI=RfD or TDI

(6)

where RfD is the Reference Dose, and TDI is the Tolerable Daily Intake. The average body weight of people in Taihu Lake region is 63.1 kg (Xiang et al., 2012). The RfD values derived for PFOS and PFOA were 0.025 and 0.333 mg/kg/d, respectively based on a rat chronic carcinogenicity study (Loi et al., 2011; Thayer and Houlihan, 2002), and the TDI values were established by the Scientific Panel on Contaminants in the Food Chain (EFSA, 2008) (Benford et al., 2008). Although there are no internationally agreed TDIs for PFOS and PFOA, because difficulties in setting a non-provisional TDI are some non-allegeable species-dependent differences in the toxicokinetics of PFOS and PFOA, especially between humans and laboratory animals, some suggested values are available that have been proposed by several national or international organizations (Schuetze et al., 2010). In this study, TDIs were derived from a subchronic study in Cynomolgus monkeys for PFOS and in male rats for PFOA by the European Food Safety Authority (EFSA) to enable a provisional risk assessment recommendation for these residues (Benford et al., 2008). Average EDI and HR values are summarized in Table S5. These results suggest that current concentrations of PFCs in shrimps and fishes are unlikely to cause immediate harm to consumers in the Taihu Lake region. As fish and shrimps are not a major constituent of the people diet in the Taihu Lake region (Xiang et al., 2012), the measurement of other foodstuffs (such as eggs, vegetables, fruits, milk, meat and so on), therefore, is necessary to allow more comprehensive public health risk assessment. The consumers should be advised against an excessive consumption of fish caught from surface waters with high levels of PFCs.

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4. Conclusions In this study the occurrence and bioaccumulation of PFCs in a food web from Taihu Lake was investigated. Monitoring results show that among the 12 analyzed PFCs, PFCAs (C8eC12) and PFOS were detected in all biological samples. In water only PFCAs with six to nine carbons and PFOS were regularly detected, while in sediment PFOS was the dominant PFC, and the long-chain PFCAs (C11, C12) were only detectable in sediments. PFCAs with nine to twelve carbons were significantly biomagnified, with TMF values ranging from 2.1 to 3.7, and the trophic magnification potential of PFOS (TMF ¼ 2.9) was generally comparable to or lower than those of the PFCAs in the same food web. The HR values of PFOS and PFOA were less than unity, suggesting that current concentrations of PFCs in shrimps and fishes are unlikely to cause immediate harm to consumers in the Taihu Lake region. However, the occurrence of suspected carcinogens such as PFOS in food for human consumption should not be tolerable even at low levels. Acknowledgments This work was financially supported by China’s National Basic Research Program: ‘‘Water environmental quality evolution and water quality criteria in lakes’’ (2008CB418201). Appendix A. Supplementary data Supplementary data related to this article can be found at http:// dx.doi.org/10.1016/j.envpol.2013.09.011. 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, 6969e6975. Asher, B.J., Wang, Y., De Silva, A.O., Backus, S., Muir, D.C.G., Wong, C.S., Martin, J.W., 2012. Enantiospecific perfluorooctane sulfonate (PFOS) analysis reveals evidence for the source contribution of PFOS-precursors to the Lake Ontario foodweb. Environ. Sci. Technol. 46, 7653e7660. Ben-David, M., Shochat, E., Adams, L.G., 2001. Utility of stable isotope analysis in studying foraging ecology of herbivores: examples from moose and caribou. Alces 37, 421e434. Benford, D., de Boer, J., Carere, A., di Domenico, A., Johansson, N., Schrenk, D., Schoeters, G., de Voogt, P., Dellatte, E., 2008. Opinion of the scientific panel on contaminants in the food chain on perfluorooctane sulfonate (PFOS), perfluorooctanoic acid (PFOA) and their salts. EFSA J., 1e131. Berger, U., Glynn, A., Holmström, K.E., Berglund, M., Ankarberg, E.H., Törnkvist, A., 2009. Fish consumption as a source of human exposure to perfluorinated alkyl substances in Sweden e Analysis of edible fish from Lake Vättern and the Baltic Sea. Chemosphere 76, 799e804. Chen, W., Jia, Y., Li, E., Zhao, S., Zhou, Q., Liu, L., Song, L., 2012. Soil-based treatments of mechanically collected cyanobacterial blooms from Lake Taihu: efficiencies and potential risks. Environ. Sci. Technol. 46, 13370e13376. Conder, J.M., Hoke, R.A., Wolf, W.d., Russell, M.H., Buck, R.C., 2008. Are PFCAs bioaccumulative? A critical review and comparison with regulatory criteria and persistent lipophilic compounds. Environ. Sci. Technol. 42, 995e1003. Domingo, J.L., 2012. Health risks of dietary exposure to perfluorinated compounds. Environ. Int. 40, 187e195. Ellis, D.A., Martin, J.W., De Silva, A.O., Mabury, S.A., Hurley, M.D., Sulbaek Andersen, M.P., Wallington, T.J., 2004. Degradation of fluorotelomer alcohols: a likely atmospheric source of perfluorinated carboxylic acids. Environ. Sci. Technol. 38, 3316e3321. Ericson, I., Martí-Cid, R., Nadal, M., Van Bavel, B., Lindström, G., Domingo, J.L., 2008. Human exposure to perfluorinated chemicals through the Diet: Intake of perfluorinated compounds in foods from the Catalan (Spain) market. J. Agric. Food Chem. 56, 1787e1794. Feng, K., Yu, B.Y., Ge, D.M., Wong, M.H., Wang, X.C., Cao, Z.H., 2003. Organo-chlorine pesticide (DDT and HCH) residues in the Taihu Lake Region and its movement in soilewater system: I. Field survey of DDT and HCH residues in ecosystem of the region. Chemosphere 50, 683e687. Fisk, A.T., Hobson, K.A., Norstrom, R.J., 2001. Influence of chemical and biological factors on trophic transfer of persistent organic pollutants in the northwater polynya marine food web. Environ. Sci. Technol. 35, 732e738.

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