Trophic Magnification of Poly- and Perfluorinated Compounds in a

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Trophic Magnification of Poly- and Perfluorinated Compounds in a Subtropical Food Web Eva I. H. Loi,†,‡ Leo W. Y. Yeung,†,‡,|| Sachi Taniyasu,‡ Paul K. S. Lam,*,† Kurunthachalam Kannan,§ and Nobuyoshi Yamashita*,‡ †

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State Key Laboratory in Marine Pollution, Department of Biology and Chemistry, City University of Hong Kong, Tat Chee Avenue, Kowloon, Hong Kong SAR, China ‡ National Institute of Advanced Industrial Science and Technology (AIST), 16-1 Onogawa, Tsukuba, Ibaraki, Japan § Wadsworth Center, New York State Department of Health and Department of Environmental Health Sciences, State University of New York at Albany, Empire State Plaza, PO Box 509, Albany, New York 12201-0509, United States Department of Chemistry, University of Toronto, 80 St George Street, Toronto, M5S 3H6, Canada

bS Supporting Information ABSTRACT: Perfluorinated compounds (PFCs) are known to biomagnify in temperate and Arctic food webs, but little is known about their behavior in subtropical systems. The environmental distribution and biomagnification of PFCs, extractable organic fluorine (EOF), and total fluorine were investigated in a subtropical food web. Surface water, sediment, phytoplankton, zooplankton, gastropods, worms, shrimps, fishes, and waterbirds collected in the Mai Po Marshes Nature Reserve in Hong Kong were analyzed. Trophic magnification was observed for perfluorooctanesulfonate (PFOS), perfluorodecanoate (PFDA), perfluoroundecanoate (PFUnDA), and perfluorododecanoate (PFDoDA) in this food web. Risk assessment results for PFOS, PFDA, and perfluorooctanoate (PFOA) suggest that current PFC concentrations in waterbird livers are unlikely to pose adverse biological effects to waterbirds. All hazard ratio (HR) values reported for PFOS and PFOA are less than one, which suggests that the detected levels will not cause any immediate health effects to the Hong Kong population through the consumption of shrimps and fishes. However, only 10
12% of the EOF in the shrimp samples was comprised of known PFCs, indicating the need for further investigation to identify unknown fluorinated compounds in wildlife.

’ INTRODUCTION Concern over poly- and perfluorinated compounds (PFCs), a group of anthropogenic organofluorine (OF) chemicals, has been growing since the 1990s because of their toxicities, environmental persistence, and bioaccumulation in wildlife and humans.1,2 Perfluorooctanesulfonate (PFOS) and its salts (e.g., perfluorooctanesulfonyl fluoride (PFOSF)), are currently classified as Persistent Organic Pollutants (POPs) under the Stockholm Convention [http://chm.pops.int/Programmes/NewPOPs/Publications/tabid/ 695/language/en-US/Default.aspx]. The United States (U.S.), European Union (EU), Canada, and Japan (under the Rule of Regulation and Manufacture of Chemical Substances) have taken corresponding measures and actions to regulate PFOS and related chemicals.3,4 Field studies have reported biomagnification of PFCs in aquatic food webs, especially for PFOS and some long-chain perfluorocarboxylates (PFCAs), in Arctic and temperate regions.5
7 Earlier studies reported that bioaccumulation patterns of PFCs vary r 2011 American Chemical Society

depending on salinity levels and trophic status.8 Globally, subtropical regions comprise approximately 1.6  107 hectares.9 However, there is limited information on PFC bioaccumulation in subtropical areas. The Mai Po Marshes Nature Reserve (MPMNR), Hong Kong, a Ramsar Wetland of International Importance with an area of 1500 ha, was the chosen study site (Figure S1). MPMNR includes diverse nursery, foraging, and roosting habitat (e.g., tidal shrimp ponds) for a wide variety of biota and both resident and migratory birds, including 27 globally threatened species. Despite efforts to conserve the nature reserve, water quality in coastal areas of Hong Kong is deteriorating due to the discharge of pollutants by adjacent rivers, especially those draining into the Pearl River Delta, which is polluted by a variety of sources Received: February 7, 2011 Accepted: May 24, 2011 Revised: May 5, 2011 Published: June 06, 2011 5506

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Environmental Science & Technology including shipping activity, industrial waste and domestic wastewater discharge, and agricultural runoff.10 Recent studies have reported the occurrence of heavy metals, polycyclic aromatic hydrocarbons (PAHs), and polychlorinated biphenyls (PCBs) in MPMNR,10 and also PFCs in Hong Kong coastal waters, sediments, marine mammals, and waterbirds.11
13 It is currently impossible to identify and quantify all OFs in environmental samples due to the lack of suitable authentic standards and methods, and therefore a mass balance of fluorine approach was applied in the present study to provide a better understanding of the presence, fate, and transfer of OF contaminants in the environment. By measuring total fluorine (TF), extractable organic fluorine (EOF), and known PFCs in the samples, the extent of environmental contamination in an aquatic food web by known and unknown fluorochemicals can be evaluated. The objectives of this study are as follows: (i) to determine PFC concentrations in water, sediment, and biota at various trophic levels (TLs) (i.e., phytoplankton, zooplankton, gastropod, worm, shrimp, fish, and waterbird liver) from a tidal shrimp pond within the MPMNR; (ii) to evaluate the trophic transfer and potential biomagnification of PFCs in this food web; (iii) to evaluate the health risks of PFCs to humans associated with fish and shrimp consumption, and waterbirds based on liver concentrations and toxicity thresholds; and (iv) to carry out a mass balance analysis of fluorine in the food web samples.

’ MATERIALS AND METHODS Sample Collection, Storage, and Handling. Surface water (n = 12), sediment (n = 6), phytoplankton in general [pooled samples (p) = 3], zooplankton [mainly amphipods and copepods (p = 2)], gastropods (p = 3), worms (p = 10 of 3 families: Capitellidae, p = 5; Nephtyida, p = 3; Sabellidae, p = 2), shrimps [p = 4 of 2 species: black tiger prawn (Penaeus monodon), p = 2; sand prawn (Metapenaeus ensis), p = 2], fish [n = 21 of five species: grey mullet (Mugil cephalus), n = 5; ladyfish (Elops saurus), n = 6; Mozambique tilapia (Oreochromis mossambicus), n = 5; small snakehead (Channa asiatica), n = 3; flag-tailed glass perchlet (Ambassis miops), p = 2 with each pool consisting of 27 individuals] were collected from a tidal shrimp pond located in the MPMNR (Figure S1 in the Supporting Information (SI)) in four sampling times from November 2008 to March 2010. Samples collected at each sampling time were analyzed independently. Surface water and sediment samples were sampled concurrently with the biota samples. Liver samples of grey heron (Ardea cinerea) (n = 3), and Chinese pond heron (Ardeola bacchus) (n = 3) were collected from MPMNR in 2003 by the Agricultural, Fisheries and Conservation Department of Hong Kong. Sample details are given in Table S1. All samples were stored at
20 °C prior to extraction. Reagents, Extraction, and Analyses. Details regarding chemicals and reagents, extraction methods, and instrumental analyses are provided in the Supporting Information. Briefly, unfiltered water samples were extracted using OASIS WAX-SPE cartridges following published methods.14,15 Sediment samples were extracted with 100 mM NaOH in methanol, followed by purification with an ENVI-Carb and OASIS WAX-SPE method. Biota samples were extracted using an ion-pair method,16 followed by purification with ENVI-Carb and OASIS WAX-SPE.14,15 Separation and determination of analytes was performed using HPLC-MS/MS (electrospray ionization in negative mode). An external calibration curve was used for quantification. TF and EOF were determined using modified combustion ion chromatography (CIC-F), by the combination of an automated combustion unit (AQF-100 type AIST; Dia Instruments

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Co., Ltd.) and an ion chromatography system (ICS-3000; Dionex Corp., Sunnyvale, CA). Quality Assurance and Quality Control (QA/QC). Detailed QA/QC measures for the PFC analysis, including limits of quantification (LOQs), calibration curves, field and procedural blanks, and procedural and matrix recoveries, are given in the SI. Matrix recoveries ranged from 75 to 124% for water, 77 to 127% for sediment, 71 to 111% for fish liver, 65 to 103% for fish tissue, 72 to 105% for shrimp, 74 to 105% for worms, and 73 to 111% for the soft tissues of gastropods. Surrogate standard recoveries ranged from 54 to 93% for phytoplankton samples (Table S2, Figure S3). Matrix recovery tests were conducted in duplicate, and the relative standard deviations (RSDs) were less than 20%. PFC concentrations in samples were not corrected for recoveries. Analyses of TF and EOF were conducted in duplicate and the RSDs of all the duplicate analyses were 1 indicates that the contaminant biomagnifies.17 BAFs and BSAFs were also calculated for phytoplankton and worm samples, respectively, to estimate the partitioning behavior of PFCs between biota and abiota. This calculation was based on the assumption that water and sediment are the dominant exposure pathways for phytoplankton and worms, respectively, using the following equations: BAF ¼ ½PFC concentration in phytoplankton ðwwÞ= PFC concentration in water BSAF ¼ ½PFC concentration in worm ðwwÞ= PFC concentration in sediment ðdry weight, dwÞ Statistical Analysis. Because all the PFC concentrations measured in individual species failed the normality test both 5507

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Figure 1. PFC concentrations in (a) abiotic samples (upper right) and (b) food web samples collected from the Mai Po Marshes Nature Reserve, Hong Kong (lower left). [Absence of bars indicates concentrations below LOQ. LOQs for water (ng/L): N-EtFOSAA (10%) > PFTeDA (7%); gastropods, 7:3 FTCA (40%) > PFOS (37%) > PFTeDA (12%); zooplankton, PFOS (57%) > PFUnDA (7%) > N-EtFOSAA ∼ PFDoDA ∼ PFHpA (6%); phytoplankton, PFNA (30%) > PFOA (27%) > PFUnDA ∼ PFOS (13%). Different composition profiles were found among the different animal groups, e.g., waterbird liver vs fish vs shrimp vs worm, while relatively similar composition profiles were observed within animal groups (Figure S5). Food Web Biomagnification. Various accumulation factors (i.e., TMF, BAF, and BSAF) have been developed for understanding partitioning, food chain transfer, and biomagnification of toxicants (Figure 2). In this study, BAFs and BSAFs were determined for the estimation of PFC uptake by biota from water and sediment. BAF represents chemical uptake from multiple exposure pathways including water and food. Because the exact composition of their diets is not known, BAFs for organisms at the higher TLs were not determined. BAFs for phytoplankton and BSAFs for worms were calculated for the nine commonly detected PFCs in both abiotic and biotic samples (Figure 2; Table S7). The greatest BAF for phytoplankton was found to be for PFUnDA (4510), followed by PFNA (1650), and PFDA (765), while relatively lower BAFs were found for PFOA (292), N-EtFOSAA (180), PFOS (169), and PFHxS (58). This finding is in line with the conclusions drawn by a previous study that PFCAs with 11
12 fluorinated carbons.34 BSAFs are useful in understanding partitioning of PFCs from sediment to biota, especially for benthic organisms. The highest BSAF in worms was found for PFTeDA (range: 3.1
46); BSAF values decreased in the following order: PFOS (1.7
24) > PFDoDA (2.0
15) > PFDA (3.2
8.3) > N-EtFOSAA (1.9
8.1) > PFUnDA (2.3
6.4). A large variation in BSAF values was found among the three worm families analyzed. The highest BSAF was found for Capitellidae, followed by Sabellidae, and the lowest value was found for Nereidae; these results are in line with the magnitude of sediment-feeding activity of each family. The BSAFs of PFOS (comparison was made on a ww basis) in the present study were of the same order of magnitude as those determined in a study conducted in a brackish estuary in Western Scheldt, The Netherlands.35 However, the values for C8
C12 PFCs estimated in Lumbriculus variegates from a laboratory study,24 ranged between 0 to 2, which are much lower than those determined in the present study. This difference is likely due to the great variations between field and laboratory exposure conditions. 5509

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Figure 2. Food web trophic magnification factors (TMFs), bioaccumulation factors (BAFs), and biota-sediment accumulation factors (BSAFs) of PFCs in biota from the Mai Po Marshes Nature Reserve, Hong Kong.

The trophic status of the food web organisms analyzed, determined using the stable-nitrogen isotope, was phytoplankton (TL = 0.7) f zooplankton (TL = 2.0) f gastropod (TL = 2.6) f flagtailed glass perchlet (TL = 1.9) f worm (TL = 3.2) f Mozambique tilapia (TL = 3.4), grey mullet (TL = 4.3), ladyfish (TL = 5.0) f shrimp (TL = 4.8) f small snakehead (TL = 5.5) (Table S6). δ13C values are commonly used to identify the food sources of organisms, with the carbon isotope ratio generally indicating 1% enrichment with each increasing TL.36 The range of δ13C was from
28.1% for gray mullet and Mozambique tilapia to
22.9% for gastropod. The δ15N and δ13C provided distinctive groupings among the various species across different TLs (Figure S4), implying that the animal species sampled had δ13C signatures that corresponded well with their feeding behaviors in the present food web. Indeed, the δ13C isotope signatures (i.e., less than 1% difference) revealed a closer relationship between sediment and Capitellidae, suggesting that sediment is a potential carbon source to Capitellidae. However, different PFC contributions and patterns were observed in the sediment and Capitellidae composition profiles, suggesting that food sources are only one factor determining PFC exposure levels. Because biomagnifications in higher trophic organisms is a complex process and is influenced by variables and complex diets, the extrapolation of BAF and BSAF data for plant and invertebrate is difficult for higher TLs due to the biological differences between low and higher trophic biota. Therefore, TMF values are extremely useful for evaluating bioaccumulation potentials in high trophic organisms. Linear regression was used to evaluate associations between TLs and PFC concentrations in tissues (Figure S6; Table S8). Among the nine analyzed PFCs, four (PFOS, PFDA, PFUnDA, and PFDoDA) showed significant (p < 0.05) associations with TLs. The TMF values of these compounds were all greater than 1 (TMF = 1.30 for PFOS, 1.50 for PFDA, 1.74 for PFUnDA, and 1.38 for PFDoDA). These results are in agreement with those of other food web studies, showing that PFOS and some long-chain PFCAs (>C8) biomagnify in the food web.5,7,25,34 No significant trend was observed for PFOA (p = 0.83), PFNA (p = 0.89), PFTeDA (p = 0.36), N-EtFOSAA (p = 0.46), or 7:3 FTCA (p = 0.10). Although the highest TMF value was reported for PFOS in earlier studies,7,25,37 PFUnDA showed the greatest TMF value in the present study, followed by PFDA.

Moreover, there were differences in accumulation pattern and magnitude between our study and previous studies based on TMF values using whole-body concentrations in the sampled organisms.25,29,37 For instance, the highest TMF value was PFOS for the Arctic study and PFOA for the temperate study, while PFUnDA was dominant in the present study. The accumulation patterns of other PFCs were also different. For example, TMF values of PFUnDA for the Arctic were 2.7- to 4.6-fold higher, while a 1.3-fold higher value was found in the temperate study when compared to our values. Relatively lower TMF values were found in the present study. This variation might be due to several reasons. First, regional differences: most of the previous studies were conducted in the Arctic and temperate regions.5,7,25,28
30 Regional differences in environmental conditions such as water chemistry and temperature might alter the physicochemical properties of PFCs and also the physiology of organisms including uptake and elimination, distribution, storage, biotransformation, and excretion. A recent study suggested that there are spatial differences in the extent of PFOS biomagnification in the eastern and western Canadian Arctic food webs.30 Second, earlier studies on biomagnification were conducted in marine7,28
30 and freshwater5,25,38 ecosystems, whereas shrimp ponds are generally considered to be brackish with salinity ranging from 5 to 16%. Furthermore, comparatively high TMF values observed in previous studies are likely due to the relatively broader range of TLs in the Arctic and temperate food webs. For example, marine mammals such as bottlenose dolphin, beluga whale, and ringed seal were the top predators in these food webs,29,37 while the top predator in the present food web is an omnivorous fish. All of these factors can contribute to variation in TMF values. To our knowledge, this is the first report to examine the trophic transfer of PFCs in a subtropical brackish food web, and our results suggest that bioaccumulation and biomagnification of PFCs differed from those reported in previous studies of the Arctic and temperate food web. Risk Assessment of PFC Exposure. Although livers of waterbirds (2003) and fish samples (2008) were collected at different times, relatively similar composition profiles of PFCs (i.e., same dominant PFC with similar composition pattern) were found in 5510

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Figure 3. (a) Total fluorine (TF), extractable organic fluorine (EOF), and known PFC concentrations in biota samples from Mai Po Marshes Nature Reserve, Hong Kong. (b) Contribution of known PFCs, EOF to TF (%) in Mai Po samples. (c) Contribution of known PFCs to EOF (%) in biota samples.

both animal groups (Figure S5). Grey mullet and Mozambique tilapia are two important prey fish species of Chinese pond heron and grey heron,11,39 and our results support the diet as a major exposure pathway of PFCs to waterbirds. A recent study reported a lowest observable adverse effect concentration (LOAEC) for PFOS of 600 ng/g ww in mallard (Anas platyrhynchos) and northern bobwhite quail (Colinus virginianus).40 A recent chicken exposure found that total concentrations of PFOS, PFDA, and PFOA of up to 4900 ng/mL in blood plasma did not cause any significant changes in body index, clinical biochemistry, or histopathology.40 In the present study, the hepatic concentrations of PFOS and the sum of PFOS/PFOA/PFDA concentrations are lower than the reported value causing adverse health effects in birds. Thus, current PFOS concentrations alone with other PFCAs in livers of waterbirds are unlikely to pose any adverse biological effects, though interspecies differences among birds should be considered. Human health risk through shrimp and fish consumption was also evaluated by estimating HRs.26 Average EDI and HR values are summarized in Table S9. All the HRs derived from best- and worstcase scenarios based on PFOS and PFOA concentrations were less than unity. These results suggest that current concentrations of PFCs in shrimps and fishes are unlikely to cause immediate harm to Hong Kong consumers. Although fish and shrimp (constituted to only around 6% of the total daily consumption) are not a major constituent of the diet of Hong Kong people, this is the first study focusing on PFCs in food in Hong Kong. Therefore, the measurement of other foodstuffs is necessary to allow more comprehensive public health risk assessment. Apart from this, recent studies demonstrated the occurrence of unknown OFs other than PFCs in rats, dolphins and humans.13,41,42 Therefore, there might be health risks when other unknown OFs are also considered. To conduct a more comprehensive risk assessment, it is important to understand the degree of OF contamination and the contribution of the known PFCs to the EOFs in the samples.

Mass Balance Analysis of Fluorines in Mai Po Samples. Because EOF concentrations in fish tissues were below LOQs ( 0.5
3.7% in worm samples > 0.4% in soft tissue of gastropod; Figure 3c). These results suggest that organisms in Mai Po are exposed to a wide range of OFs other than PFCs. Moreover, variation of the contributions among organisms was observed and this might be related to species-specific differences in uptake and elimination metabolism or bioaccumulation or feeding habits. Another suggestion is that there are differences in the sources and pathways of OF in the food web to different organisms. The present study suggests the presence of other forms of OFs in addition to known PFCs in wildlife. These unidentified OFs might be intermediates or metabolites of PFCs such as PFOS precursors which might undergo biotransformation.13 Moreover, there are around 30 OF compounds of natural origin43 and over one million OF compounds have been manufactured by industries.44 Natural defluorination was found to occur for mono- and difluoro methyl groups;45 however, many agrochemicals and pharmaceuticals contain trifluoro methyl groups and fluoropolymers are resistant to defluorination in the environment and have limited biodegradability. Since manufactured OFs have been widely used for different applications including pharmaceuticals, insecticides, pesticides, fluoropolymer fabrics, surfactants, refrigerants, aerosol propellants, nonstick 5511

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Environmental Science & Technology surfaces for cookware, and chemical-resistant tubing, some of the unidentified OFs might come from other sources that accumulated in the food web.46 A recent study reported the detection of a new class of fluorinated surfactants in human blood sera.47 Parts of the unidentified OFs might also be coming from these newly found PFCs, as a similar extraction method was used. The presence of large proportion of unknown OFs highlights the potential for concern about these persistent OFs, and demonstrates the need for risk assessment in relation to their environmental effects. The HRs estimated in the present study suggest that there is no immediate risk due to consumption of PFC-contaminated fishes and shrimp; however, these HRs are derived from 10 to 12% of the EOFs for shrimp. Further investigation for the purpose of identifying these unknown fractions should be performed to allow for a better understanding of the sources and the exposure pathways of both known and unknown OF, which is critical for a comprehensive risk assessment of these compounds to wildlife and human populations.

’ ASSOCIATED CONTENT

bS

Supporting Information. Details of the sample information and location, chemicals and reagents used, the experimental procedures employed, QA/QCs, individual PFC concentrations, results of stable isotope analysis, and data of the accumulation constants and HRs. This material is available free of charge via the Internet at http://pubs.acs.org.

’ AUTHOR INFORMATION Corresponding Authors

*Tel: þ852-2788-7681; fax: þ852-2788-7406; e-mail: bhpksl@ cityu.edu.hk (P.K.S.L.); Tel: þ81-29-861-8335; fax: þ81-29861-8335; e-mail: [email protected] (N.Y.).

’ ACKNOWLEDGMENT The work described in this paper was supported by a grant from the Research Grants Councils (CityU160408) of the Hong Kong Special Administrative Region, China. This work was undertaken during the tenure of a City University Postgraduate Studentship to E.IHL. We gratefully acknowledge sampling help from WWF, Hong Kong, for this study. We thank Yamazaki Eriko (Hosei University, Japan) for the help of parts of CIC-F analysis. We sincerely thank Dr. Margaret Murphy (City University of Hong Kong) for critical suggestions on this paper. ’ REFERENCES (1) Giesy, J. P.; Kannan, K. Global distribution of perfluorooctane sulfonate in wildlife. Environ. Sci. Technol. 2001, 35, 1339–1342. (2) Giesy, J. P.; Kannan, K. Perfluorochemical surfactants in the environment. Environ. Sci. Technol. 2002, 36, 146A–152A. (3) EU. Directive 2006/122/ECOF of the European Parliament and of the Council of 12 December 2006. In Official Journal of the European Union, 2006. (4) OECD. Risk management: Recommendations from an OECD workshop on perfluorocarboxylic acids (PFCAs) and precursors; Paris, 2007. (5) Kannan, K.; Tao, L.; Sinclair, E.; Pastva, S. D.; Jude, D. J.; Giesy, J. P. Perfluorinated compounds in aquatic organisms at various trophic levels in a Great Lakes food chain. Arch. Environ. Contam. Toxicol. 2005, 48, 559–566.

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