Perfluorinated alkyl substances in water, sediment, plankton and fish from Korean rivers and lakes: A nationwide survey

Perfluorinated alkyl substances in water, sediment, plankton and fish from Korean rivers and lakes: A nationwide survey

Per fluorinated alkyl substances in water, sediment, plankton and fish

from Korean rivers and lakes: A nationwide survey

Nguyen-Hoang Lama, Chon-Rae Chob, Jung-Sick Leea, Ho-Young Soha, Byoung-Cheun Leec, Jae-An Leec, Norihisa Tatarozakod, Kazuaki Sasakie, Norimitsu Saitoe, Katsumi Iwabuchie,

a College of Fisheries and Ocean Sciences, Chonnam National University, Yeosu 550-749, Republic of Korea

b Korea Research Institute of Chemical Technology, Daejeon 305-600, Republic of Korea

c

National Institute of Environmental Research, Incheon 404-408, Republic of Korea

d

National Institute for Environmental Studies, Tsukuba, Ibaraki 305-8506, Japan

e

Research Institute for Environmental Sciences and Public Health of Iwate Prefecture, Iwate 020-0852, Japan

f

Wadsworth Center, New York State Department of Health, and School of Public Health, State University of New York at Albany, Empire State Plaza, PO Box 509, Albany, NY 12201-0509, USA

H I G H L I G H T S

• PFOS was found at greatest concentrations in water, sediment, plankton and fish

• High concentrations of long chain PFCAs were found in sediment samples

• Mean ratios of PFASs concentration in fish blood to liver were mostly N2

• PFOS, PFUnA, PFDoA and PFDA accounted for 94–99% of ∑PFASs concentration in fish

• Only PFOS and PFNA were concentrated in plankton samples

a b s t r a c t

a r t i c l e i n f o

Article history:

Received 30 October 2013

Received in revised form 10 January 2014

Accepted 10 January 2014

Available online xxxx

Keywords:

Perfluorooctanesulfonate

Perfluorinated compounds

Korea

Freshwater

Bioconcentration factor

Fish tissues

Water, sediment, plankton, and blood and liver tissues of crucian carp (Carassius auratus) and mandarinfish (Siniperca scherzeri) were collected from six major rivers and lakes in South Korea (including Namhan River, Bukhan River, Nakdong River, Nam River, Yeongsan River and Sangsa Lake) and analyzed for perfluorinated alkyl substances (PFASs) Perfluorooctane sulfonate (PFOS) was consistently detected at the greatest concentrations in all media sur-veyed with the maximum concentration in water of 15 ng L−1and in biota of 234 ng mL−1(fish blood) A general ascending order of PFAS concentration of waterb sediment b plankton b crucian carp tissues b mandarin fish tis-sues was found Except for the Nakdong River and Yeongsan River, the sum PFAS concentrations in water samples were below 10 ng L−1 The PFOS and perfluorooctanoic acid (PFOA) concentrations in water did not exceed levels for acute and/or chronic effects in aquatic organisms High concentrations of long chain perfluorocarboxylates (LCPFCAs) were found in sediment samples PFOS, perfluoroundecanoic acid (PFUnA), perfluorododecanoic acid (PFDoA) and perfluorodecanoic acid (PFDA) accounted for 94–99% of the total PFASs concentration in fish tissues The mean ratios of PFAS concentration betweenfish blood and fish liver were above 2 suggesting higher levels in blood than in liver Significant positive correlations (r N 0.80, p b 0.001) were observed between PFOS concentration

in blood and liver tissues of both crucian carp and mandarinfish This result suggests that blood can be used for non-lethal monitoring of PFOS infish Overall, the rank order of mean bioconcentration factors (BCFs) of PFOS in biota was; phytoplankton (196 L/kg)b zooplankton (3233 L/kg) b crucian carp liver (4567 L/kg) b crucian carp blood (11,167 L/kg)b mandarin liver (24,718 L/kg) b mandarin blood (73,612 L/kg)

© 2014 Elsevier B.V All rights reserved

1 Introduction

The unique properties such as resistance to hydrolysis, photolysis,

bio-degradation and thermal stability, in combination with widespread

application of perfluoroalkyl substances (PFASs), made them global pol-lutants in abiotic and biotic matrices including food stuffs (Picó et al.,

2011), human blood (Kannan et al., 2004; Harada et al., 2010), breast milk (Llorca et al., 2010), wildlife such asfish, birds and marine mam-mals (Giesy and Kannan, 2001), sediment (Nakata et al., 2006), water (Yamashita et al., 2005) and atmosphere (Li et al., 2011) The worldwide distribution of PFASs was reported in urban and remote areas including

Science of the Total Environment xxx (2014) xxx–xxx

⁎ Corresponding author Tel.: +82 616597146; fax: +82 61 654 2975.

E-mail address: hscho@jnu.ac.kr (H.-S Cho).

0048-9697/$ – see front matter © 2014 Elsevier B.V All rights reserved.

http://dx.doi.org/10.1016/j.scitotenv.2014.01.045

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deep oceanic water of up to 5000 m (Yamashita et al., 2005) and in polar

bears from the Arctic Ocean (Giesy and Kannan, 2001)

Due to their persistence and bioaccumulation, some PFASs can

elicit harmful effects in terrestrial and aquatic organisms (Lau et al.,

2004) Perfluorooctane sulfonate (PFOS) also biomagnifies in wildlife

at higher trophic levels in the food chain (Giesy and Kannan, 2001;

Kannan et al., 2005) To humans, the major routes of PFAS exposures

include diet (Tittlemier et al., 2007; Zhang et al., 2010), drinking

water (Takagi et al., 2008; Nolan et al., 2010; Llorca et al., 2012)

and indoor dust (Strynar and Lindstrom, 2008; Björklund et al.,

2009)

Following the discovery of widespread global contamination by

PFOS, the 3 M Company, a major producer of this compound, phased

out its production in the USA from 2001 (Giesy and Kannan, 2001)

Sev-eral other countries have put forward some regulations to ban or limit

the use of PFASs; for example, in industrial and domestic products in

Canada and European Union in 2006 PFOS and, its salts and

perfluorooctane sulfonyl fluoride were listed on Annex B of The

Stockholm Convention on persistent organic pollutants by the Fourth

Conference of Parties in May 2009 (Kannan, 2011)

South Korea is a developed and industrialized country PFASs have

been used extensively in various industries including electronic and

tex-tile industries in South Korea The concentrations of PFASs in surface

water from certain industrial areas in South Korea are the highest

among several Asian countries as well as globally (Rostkowski et al.,

2006; Cho et al., 2010) Previous studies have also reported high

accu-mulation of PFASs in human blood (Kannan et al., 2004; Harada et al.,

2010; Ji et al., 2012), birds (Kannan et al., 2002a; Yoo et al., 2008),

minke whales and common dolphins (Moon et al., 2010), Asian

peri-winkles and rockfish (Naile et al., 2010) and coastal and ocean waters

from Korea (So et al., 2004; Yamashita et al., 2005; Rostkowski et al.,

2006; Naile et al., 2010) Despite this, available studies on PFASs in

Ko-rean freshwater ecosystems such as lakes or rivers are limited Here,

we carried out a systematic study during 2010 to 2012 to determine

the current status and extent of PFAS concentrations in both abiotic

and biotic matrices in six major rivers and lakes in Korea Rivers and

lakes were surveyed along a spatial gradient representing upstream

and downstream locations to identify sources of pollution

Accumula-tion in tissues (blood and liver) of various freshwater aquatic organisms

was investigated

2 Materials and methods

2.1 Chemicals and reagents

MPFAC-MXA, a mixture of 9 surrogate standards containing13C4

-PFOS (sodium perfluoro-1-[1,2,3,4-13C4] octane sulfonate), and13C4

-PFOA (Perfluoro-n-[1,2,3,4-13

C4]) octanoic acid were purchased with PFAC-MXB, a mixture of 17 native perfluorocarboxylate acids (PFCAs)

and perfluoroalkyl sulfonates from Wellington Laboratories (Guelph,

ON, Canada).13C4-PFOS was used as a surrogate for the perfluoroalkyl

sulfonates and13C4-PFOA was used as a surrogate for the PFCAs

PFAC-MXB mixture was used for standard calibration at concentrations

rang-ing from 0.1 to 50 ng/mL High performance liquid chromatography

(HPLC) grade reagents including methanol (Kanto Chemical, Tokyo,

Japan), water (J.T Baker, USA) and ammonium acetate (Junsei, Japan)

were used Milli-Q water was prepared by a Barnstead Nanopure In

fin-ityTMwater purification system (Thermo Scientific, USA)

2.2 Sample collection

Samples of water, sediment, plankton, and blood and liver tissues of

an omnivorousfish species (crucian carp) and a carnivorous fish species

(mandarinfish) were collected from 17 sampling sites in six major

riv-ers and lakes in South Korea including Bukhan, Namhan, Nakdong, Nam,

Yeongsan Rivers and Sangsa Lake (Fig 1) The Nakdong River, Yeongsan

River and Han River are three of four largest river basins in South Korea and play an important role as a water resource for agriculture, industry, recreational and drinking water for millions of people living in metro-politan cities of Seoul, Daegu, Busan and Gwangju The Bukhan and Namhan Rivers are two major tributaries of the Han River The Nakdong River, and its main tributary, Nam River are located in the southeastern region; the Yeongsan River and Sangsa Lake are located in the south-western region and the Namhan and Bukhan Rivers are located in the northeastern region of the Korean peninsula The sampling areas were divided generally into 3 groups as highly industrialized areas (Yeongsan River and Nakdong River), moderately industrialized areas (Namhan River and Nam River) and less industrialized areas (Sangsa Lake and Bukhan River) In order to survey the effects of discharge of waste water treatment plant (WWTP) effluents on PFASs concentration in sur-face water samples, the sampling sites 7 and 13 were from downstream

of industrial waste water treatment plants (I-WWTP) in Daegu metro-politan city (treatment capacity of 520,000 ton/day) and in Haman town (treatment capacity of 3400 ton/day), respectively; the sampling sites 16 and 13 were located downstream of domestic waste water treatment plants (D-WWTP) in Gwangju metropolitan city (treatment capacity of 600,000 ton/day) and in Seungju town (capacity of

2500 ton/day), respectively Because the sampling sites were selected

to represent Korea, and involved various levels of industrialization, the results of this study represent PFAS concentrations in freshwater eco-systems in Korea

One liter clean polypropylene (PP) bottles pre-rinsed with Milli-Q water, methanol and water from a specific sampling site were sunk to col-lect surface waters Surface layer (1–5 cm) of sediment samples was col-lected using a clean, methanol rinsed PP spatula and stored in pre-cleaned

50 mL PP tubes Phytoplankton, micro-zooplankton and meso-zooplankton samples were collected vertically by using NORPAC® plank-ton net with 3 mesh sizes of 20, 60, 200μm, respectively Depending on the depth of water column and topography offishing sites, fish samples were collected by drift gill net, cast net orfish and hook Fresh blood and liver tissues were obtained fromfish Sexes, body weight, body length, hepatosomatic index (HSI) and gonadosomatic index (GSI) of fishes were also determined Water and sediment samples were transported on ice, to the laboratory, and keep at 4 °C until extraction Biota samples were stored in dry ice immediately after collection in the field and kept at −20 °C in the laboratory until extraction

Fig 1 Map showing 17 sampling sites located in six major rivers and lakes from South Korea.

2.3 Sample extraction and analysis

Ten perfluorinated compounds including perfluorohexanoic acid

(PFHxA), perfluoroheptanoic acid (PFHpA), perfluorooctanoic acid

(PFOA), perfluorononanoic acid (PFNA), perfluorodecanoic acid (PFDA),

perfluoroundecanoic acid (PFUnA), perfluorododecanoic acid (PFDoA),

perfluorohexane sulfonate (PFHxS), perfluorooctane sulfonate (PFOS),

and perfluorodecane sulfonate (PFDS) were the target analytes in the

present study

Water samples were notfiltered to avoid the loss of some PFASs and

potential for contamination of target PFASs fromfilter papers during the

filtration procedure Thus, concentrations reported for water samples

represent both dissolved and particulate phase concentrations

Sedi-ment samples were air-dried, crushed with pestle and mortar and

sieved through a 0.25 mm sieve prior to extraction Water samples

were analyzed following the method described byYamashita et al

(2004) Sediment samples were extracted based on the method of

Nakata et al (2006) Biota samples were analyzed by ion-pair extraction

method described elsewhere (Hansen et al., 2001; Giesy and Kannan,

2001; Hart et al., 2008) Concentrations of PFASs were determined by

an Agilent 1100TM HPLC interfaced with Applied Biosystems API

2000TMelectrospray ionization tandem mass spectrometer (ESI-MS/

MS) TenμL aliquot of the extracted sample were injected Flow rate of

the mobile phase was 300μL/min To quantify the target chemicals by

MS/MS, a multiple reaction monitoring (MRM) mode was used

2.4 Quality assurance and quality control

Procedural blanks were prepared to check for possible

contamina-tions arising from the sample preparation procedure Concentracontamina-tions

of target chemicals were subtracted from concentrations found in

blanks, when applicable The regression coefficient (r2) of the

calibra-tion curves for all target analytes, prepared at concentracalibra-tions of 0.1,

0.2, 0.5, 1, 2, 5, 10, 20, and 50 ng/mL was≥0.99 The detection limits

of PFASs in samples ranged from 0.01 to 0.1 ng L−1for water, 0.01 to

0.02 ng g−1dry weight (dw) for sediment, and 0.01 to 0.1 ng g−1wet

weight (ww) or ng mL−1for biota The recovery rates (%) of surrogate

standards spiked into each sample prior to extraction were in the

range of 73.6% to 131% The concentrations of target analytes were not

corrected for surrogate recovery rates

2.5 Statistical analysis

In this study, the parametric method of regression on order statistics

function and the nonparametric method of Kaplan–Meier built in the

statistical software of ProUCL 4.1 (U.S Environmental Protection

Agency) were utilized to treat the data sets with 0%b % non-detected (NDs)b 80% Alternatively, if the %NDs in a data set exceeded 80% or if the number of distinct observation in a data set was smaller than 5, which is the minimum distinct observation size required to run ProUCL 4.1, all NDs were assigned a value of zero (Singh et al., 2006) Spearman's correlation analysis and Student's t-test were also per-formed by using SPSS® (IBM, version 21) to investigate correlations and statistical differences between selected data groups

3 Results and discussion The overall observation of all target analytes in various matrices is presented inTable 1

3.1 PFASs in water Except for the Nakdong River and Yeongsan River, the sum PFAS concentrations in water samples collected in rivers and lakes from Korea were below 10 ng L−1(Fig 2) Among PFASs analyzed, PFOA and PFOS were consistently detected at high concentrations in river and lake water samples (Table 2) The mean percentages of PFOA and PFOS concentrations in total PFASs concentration in water were 24% and 37%, respectively The greatest concentrations of PFOA and PFOS were found in the sampling sites 7 and 16, respectively, which are

locat-ed downstream of industrial and domestic waste water treatment plants (WWTPs) in Daegu and Gwangju metropolitan cities These re-sults suggest that WWTPs are the“point-sources” of aqueous discharges

of PFASs into the aquatic environments The ratios of concentration of PFOS to PFOA were in the range of 0.23 to 39 (mean = 4.15), which is comparable to a general concentration ratio of PFOS to PFOA (mean of N4) in water samples from Korean coastal waters (Naile et al., 2010) Apart from the Nam River, where this ratio ranged from 0.23 to 0.30, the PFOS/PFOA concentration ratio in water samples from other fresh-water sampling sites was generally greater than 1 This result suggests that except for the Nam River where PFOA was the dominant PFAS, PFOS was dominant in water samples from the other sampling areas Higher concentrations of PFOS and PFOA have been reported in sur-face waters from some other regions in South Korea and Asia, than those found in the present study In South Korea, the greatest concentrations

of PFOS and PFOA were found in water samples collected from the heavily industrialized area of Shihwa Lake High concentrations of PFOS and PFOA in water samples from this“hotspot” were reported

byRostkowski et al (2006)(max PFOS = 651 ng L−1; max PFOA = 61.7 ng L−1; n = 21);Naile et al (2010)(max PFOS = 450 ng L−1; max PFOA = 68.6 ng L−1; n = 8) andSo et al (2004)(mean PFOS =

730 ng L−1; mean PFOA = 320 ng L−1; n = 1) Additionally, mean

Table 1

Overview of PFASs analysis results.

Item Water Sediment Plankton Carp blood Carp liver Mandarin blood Mandarin liver

PFUnA 15 (79) 23 (85) 6 (50) 69 (100) 69 (100) 20 (100) 20 (100) PFDoA 12 (63) 27 (100) 7 (58) 69 (100) 67 (97) 20 (100) 15 (75)

PFOS 19 (100) 27 (100) 6 (50) 69 (100) 58 (84) 20 (100) 20 (100)

Average detected 14 (74) 17 (62) 3 (25) 35 (51) 32 (46) 13 (66) 7 (33)

a

Sites 4 and 5 were surveyed in 2010 and others were surveyed in 2012.

b

Collected in sites 4 and 5.

c

Collected in sites 2, 4, 5, 7, 10, 13 and 16.

concentrations of PFOS (67.2 ng L−1) and PFOA (32.5 ng L−1) in

seawa-ter samples (n = 11) from Korean Wesseawa-tern and Southern coast reported

bySo et al (2004)were higher than those found in freshwater in this

study In Japan, mean PFOS concentrations in water samples (n = 14)

collected from Tokyo Bay, Osaka Bay and Ariake Bay (Taniyasu et al.,

2003) were 1.2–6.7 fold greater than the mean PFOS concentration

found in the present investigation.Senthilkumar et al (2007)andLien

et al (2008)also reported higher PFOS and PFOA concentrations in

river water from Kyoto area and the Yodo River basin in Japan than

those found in the present study, but the concentrations were similar

to those reported bySinclair et al (2006)for river and lake waters in

New York (USA),So et al (2007)for waters from the Pearl River,

Guang-zhou and the Yangtze Rivers, Shanghai (China) andLiu et al (2009)for

rain and snow from Dailan (China) More detailed comparisons of PFOS

and PFOA concentration obtained in water samples from the present

study with those reported in previous studies are provided in the

Sup-plementary information

PFHxS, PFNA and PFHxA accounted for 12.3%, 6.93% and 6.79% of

total PFAS concentrations in water samples, respectively

Concentra-tions of these compounds in water samples in the present study were

relatively lower than those reported from the west coast of Korea

(Naile et al., 2010) and from Shihwa Lake (Rostkowski et al., 2006)

but higher than those reported in water samples from Geonggi Bay

(Rostkowski et al., 2006) PFDS was not found in any of water samples,

even in downstream sampling sites of domestic and industrial WWTPs

in the Nakdong River (no 7), Yeongsan River (no.16), Sangsa Lake (no.17) and Nam River (no.13) This is similar with those described in

Naile et al (2010), who reported below method detection limit concen-trations for PFDA in the Yeongsan River estuary, the heavily industrial-ized area of Shihwa Lake and Sinduri Beach The different patterns of concentration of PFASs analyzed in the present study, combined with the comparisons with other previous studies, suggest a site-specific PFAS sources in Korean surface waters Thus, further investigations are needed to identify the sources of PFASs

The US EPA's Great Lakes Initiative (GLI,USEPA, 1995) intends to provide both acute and chronic data for the protection offish, inverte-brates, and other aquatic organisms based on the results of toxicity test-ing with freshwater organisms In this guideline, acute toxicity data from a range of specified taxa was collected to identify a final acute value (FAV) that can protect 95% of test species and the acute criterion

or criteria maximum concentration (CMC) was established as equiva-lent to one-half of the FAV Additionally, within the guideline, the chronic criterion or criteria continuous concentration (CCC) was established to represent a concentration of a chemical such that 95%

of the genera tested have greater chronic values Following this guide-line,Giesy et al (2010)used data from acceptable tests with freshwater organisms from North America including a variety of genera such as waterflea, mussel, spring peeper, planarian, amphipod, rainbow trout, leopard frog, oligochaete, fathead minnow, midge and some sensitive aquatic plants and algae to summarize numerical water quality criteria values for selected PFASs These water quality criteria values were de-termined as 5.1μg PFOS/L and 2.9 mg PFOA/L for CCC and 21 μg PFOS/

L and 25 mg PFOA/L for CMC An evaluation of potential ecological risks to aquatic organisms associated with exposure to PFOS and PFOA was employed by comparing the determined concentration of PFOS and PFOA in water samples in the present study with the water quality criteria values for the protection of aquatic organisms reported byGiesy

et al (2010) The comparison indicates that PFOS concentrations (up to 15.1 ng L−1) and PFOA concentrations (up to 8.34 ng L−1) found in sur-face water samples in the present study were 300–300,000 fold less than the reported CMC and CCC values This result suggests that chronic and acute effects on aquatic organisms exposed to PFOS and PFOA in surface waters from the six major rivers and lakes in Korea were not likely

Furthermore, the reported water concentration of PFOS that is pro-tective of avian wildlife was also determined to be 47 ng L−1byGiesy

et al (2010) This value was calculated as the geometric mean of three avian wildlife values for herring gull, bald eagle and kingfisher, which were 41 ng PFOS/L, 71 ng PFOS/L and 36 ng PFOS/L, respectively In the present study, the highest concentration of PFOS found in water samples was less than this avian wildlife protection value This result

0

10

20

30

40

Bukhan Namhan Nakdong Nam Sangsa Yeongsan

River name

mean

min Q3 median Q1 max

Fig 2 Sum PFASs concentrations in water collected from 6 major rivers and lakes in Korea.

The mean total PFAS concentrations in Bukhan River, Namhan River, Nam River and

Sangsa Lake were below 10 ng/L.

Table 2

Concentration (ng L−1) of PFASs in water showed in min–max (mean).

Site (n) PFHxA PFHpA PFOA PFNA PFDA PFUnA PFDoA PFHxS PFOS PFDS ∑PFASs a

Bukhan (3) 0.11–0.31

(0.18)

0.12–0.27 (0.19)

0.56–1.41 (0.94)

0.29–0.52 (0.38)

0.10–0.21 (0.14)

0.19–0.32 (0.24)

0.10–0.12 (0.11)

ND–0.72 (0.39)

0.83–1.84 (1.27)

ND 2.31–5.71 (3.85) Namhan (4) ND ND–0.45

(0.26)

ND–0.64 (0.20)

ND–0.32 (0.08)

ND–0.11 (0.02)

ND ND 0.50–3.97

(2.03)

0.67–6.25 (3.30)

ND 1.17–10.86 (5.90) Nakdong (3) 0.51–7.94

(3.82)

0.71–3.43 (1.85)

3.56–8.34 (6.50)

0.83–4.49 (2.32)

0.53–4.80 (2.13)

0.28–1.13 (0.59)

0.13–0.33 (0.20)

0.89–1.71 (0.21)

6.27–8.46 (7.36)

ND 14.71–40.63 (26.00) Nam (3) 0.86–1.31

(1.03)

0.45–0.91 (0.68)

3.40–4.65 (3.84)

0.53–0.69 (0.62)

0.19–0.33 (0.26)

0.17–0.21 (0.20)

0.07–0.13 (0.10)

0.23–0.37 (0.32)

0.87–1.06 (0.98)

ND 7.09–9.61 (8.01) Sangsa (3) 0.02–0.18

(0.10)

ND–0.18 (0.06)

0.29–0.63 (0.43)

0.14–0.33 (0.21)

0.05–0.07 (0.06)

0.10–0.13 (0.12)

0.06–0.08 (0.06)

0.03–0.11 (0.07)

0.25–0.99 (0.59)

ND 1.51–1.83 (1.70) Yeongsan (3) 0.93–1.33

(1.11)

0.41–0.79 (0.60)

2.43–4.66 (3.97)

0.54–1.08 (0.85)

0.14–1.10 (0.64)

0.13–0.73 (0.41)

0.10–0.31 (0.21)

0.42–1.63 (1.03)

1.18–15.07 (11.06)

ND 8.47–25.19 (18.68) All sampling sites

(19)

ND–7.94

(0.98)

ND–3.43 (0.59)

ND–8.34 (2.49)

ND–4.49 (0.71)

ND–4.80 (0.52)

ND–1.13 (0.25)

ND–0.33 (0.11)

ND–3.97 (0.90)

ND–15.07 (3.89)

ND 1.17–40.63 (10.44) n: number of analyzed sample; ND: below the method detection limit.

a ∑PFASs refer to sum of ten detectable PFAS in each sampling site.

indicates that the concentrations of PFOS in water samples from all

sam-pling sites in the present study are unlikely to cause potential harmful

effects to avian wildlife

3.2 PFASs in sediment

The distribution of PFASs concentration in sediment samples is

sum-marized inTable 3 Approximately 2/3 of the sediment samples

ana-lyzed in this study contained PFASs above the detection limits Similar

to that in water samples, PFDS was not detected in any of sediment

sam-ples (Table 1) PFOS and PFDoA were found in all analyzed sediment

samples Mean PFOS concentration in sediments was 0.12 ng g−1dw,

which accounted for 32% of the total PFAS concentrations in sediments

The measured PFOS concentrations from sediments in the present study

were lower than those reported previously from Korean western coasts

(Naile et al., 2010; min = 2 ng g−1dw), Roter Main River in Germany

(Becker et al., 2008; mean = 0.21 ng g−1dw), Dailao River system in

China (Bao et al., 2009; mean = 0.21 ng g−1dw), Yangtze River estuary

in China (Pan and You, 2010; mean = 536 ng g−1dw), Tokyo Bay in

Japan (Sakurai et al., 2010; mean = 0.54 ng g−1dw) and San Francisco

Bay in the USA (Higgins et al., 2005; mean = 0.85 ng g−1dw), but

were comparable with those described from Liao River in China

(Yang et al., 2011; mean = 0.15 ng g− 1dw), Taihu Lake in China

(Yang et al., 2011; mean = 0.15 ng g−1dw) and Southern Rivers of

Japan (Nakata et al., 2006; range: 0.09–0.14 ng g− 1dw) PFDoA

(mean = 0.05 ng g− 1dw) was the next predominant PFAS found

in the sediments PFDoA levels in sediments were 13 to 48 fold lower

than those from Uji River (mean = 0.75 ng g−1dw), Tenjin River

(mean = 2.4 ng g−1dw), or in Kamo River (0.94 ng g−1dw), and

Katsura River (1.7 ng g−1dw) in Japan (Senthilkumar et al., 2007),

but were higher than those from Liao River (mean = 0.01 ng g−1dw)

and Taihu Lake (mean = 0.03 ng g−1dw) in China (Yang et al., 2011)

Following PFDoA, PFOA was found as the next dominant PFAS in the

sediments Detailed comparisons of PFOS and PFOA concentration

found in the present study with those reported in previous studies are

provided in the Supplementary information

Similar to PFDoA and PFOA, other long-chain perfluorocarboxylates

(LCPFCAs) including PFNA, PFDA and PFUnA were detected in

sedi-ments with high detection frequency (Table 1) This result is

compara-ble with that in sediment samples from the Liao River and Taihu River,

China (Yang et al., 2011) High percentages of mean concentrations of

these LCPFCAs to total PFASs concentration in sediment samples were

found consistently in all studied rivers and lakes at 71.8%, 50.6%,

63.3%, 85.2%, 79.1% and 79.8% in Bukhan River, Namhan River, Nakdong

River, Nam River, Sangsa Lake and Yeongsan River, respectively This

re-sult suggests that these LCPFCAs are dominant chemicals for sorption

process on freshwater sediment samples in the present study

Partition coefficients of PFASs between sediment and surface water

(Kd), which is estimated by the ratio of the concentration of PFASs in

the sediment (ng g−1dw) to the concentration of PFASs in the overlying

water (ng/L) at the same sampling sites, were used to evaluate PFASs

dis-tribution patterns in the sediment samples The mean Kdvalues are

sum-marized inTable 4 An ascending order of mean Kdfor LCPFCAs of PFOA

(0.04)b PFNA (0.10) b PFDA (0.13) b PFUnA (0.21) b PFDoA (0.72)

was found The positive association between Kdvalue with the number

of perfluorocarbon chain length obtained in the present study is

consis-tent with that described byHiggins and Luthy (2006) It is worth noting

thatHiggins and Luthy (2006) reported that perfluorocarbon chain

length was the dominant structural feature influencing sorption, with

each CF2moiety contributing 0.50–0.60 log units to the measured

fresh-water–sediment distribution coefficients of perfluorinated surfactants

However, PFOS and PFOA had different Kdvalues Mean Kdvalue for

PFOS was higher than that for PFOA in most sampling sites This

differ-ence may be caused by the effect of the sulfonate moiety, which

contrib-uted an additional 0.23 log units to the measured distribution coefficient,

1 dw)

3.3 PFASs in biota

The concentration profiles of PFASs in plankton samples are shown in

Table 5 PFHxA, PFHpA, PFOA, PFHxS, and PFDS were not detected in any

plankton samples Despite the highest detection frequency of PFNA (83%),

the greatest mean PFASs concentration was observed for PFOS (2.08 ng

PFOS/g ww) in plankton samples It is worth to note that the next greatest

mean PFAS concentration was for PFDoA at 0.36 ng g−1ww, which was

approximately 6-fold less than the mean concentration of PFOS The

mean concentrations of remaining PFASs were in the order of PFNA

N PFUnA N PFDA N PFDoA Very few studies have measured PFASs in

plankton The mean concentration of PFOS in zooplankton samples

ana-lyzed in this study was relatively less than that reported from China (Li

et al., 2008; 4.18 ng g−1ww), or from the Barents Sea (Haukås et al.,

2007; mean = 3.85 ng g−1ww) but was higher than that reported from

Western Arctic (Powley et al., 2008; max = 0.2 ng g−1ww) and Eastern

Arctic (Tomy et al., 2004; mean = 1.8 ng g−1ww) PFNA was not detected

in zooplankton samples from the Barents Sea (Haukås et al., 2007)

but was found in a sample from Beijing, China (Li et al., 2008;

0.15 ng g−1ww) Although PFOA was not detected in any plankton

samples in the present study and in zooplankton samples from

Bank Island, Western Arctic (Powley et al., 2008), this chemical was found at relatively high concentration in zooplankton collected from Frobisher Bay (Tomy et al., 2004; mean = 2.6 ng g−1ww), Ba-rents Sea (Haukås et al., 2007; mean = 3.15 ng g− 1ww) and Gaobeidian Lake (Li et al., 2008; mean = 0.05 ng g−1ww)

Concentrations of PFASs in blood and liver of crucian carp and man-darinfish are summarized inTable 6 PFHpA was not detected in all in-vestigatedfish tissues PFOS was consistently found at the highest concentration and accounted for 37%, 57%, 49% and 52% of the total PFASs concentration in crucian carp blood, crucian carp liver, mandarin fish blood and mandarin fish liver, respectively Following PFOS, PFUnA was the next predominant PFAS infish tissues PFOS and PFUnA were also reported as the predominant PFASs found in both liver samples from marine mammals from Korean coastal waters (Moon et al.,

2010) and skipjack tuna collected from offshore waters and some open ocean sites in the Sea of Japan, the East China Sea, the Indian Ocean, and the Western North Pacific Ocean (Hart et al., 2008) In the present study, PFUnA was found in allfish tissues samples The detect-ing frequency of PFOS and PFDoA was 100% in crucian carp and manda-rinfish blood samples and the detecting frequency of PFDA was 100% in crucian carp blood and liver samples The sum concentrations of these 4

Table 4

Mean partition coefficients (K d ) of PFASs between sediment and surface water.

All sampling sites (17) 0.02 – 0.04 0.10 0.13 0.21 0.72 0.03 0.07 – n: number of sampling site.

Table 5

Concentration of PFASs in plankton samples (ng g−1ww) showed in min–max (mean).

Phytoplankton (4) 0.30–0.50 (0.43) ND–0.39 (0.10) ND–0.27 (0.13) ND–0.71 (0.26) ND–0.70 (0.21) 0.30–2.15 (1.12) Micro-zooplankton (4) ND–0.40 (0.20) ND ND–0.44 (0.17) ND–0.96 (0.43) ND–11.07 (2.82) 0.10–12.47 (3.61) Meso-zooplankton (4) ND–0.50 (0.25) ND ND–0.27 (0.10) ND–1.08 (0.39) ND–12.67 (3.21) 0.20–12.98 (3.94) n: number of analyzed sample; ND: below the method detection limit.

a ∑PFASs refer to sum of ten detectable PFAS in each sampling site.

Table 6

Range and mean concentration (ng g−1ww or ng mL−1) of PFASs in fish tissues.

Crucian carp (n = 69) Mandarin fish (n = 20)

BW (g) 76.40 ∼ 973.19 (237.74) 52.58 ∼ 424.60 (134.85)

BL (cm) 12.50 ∼ 32.00 (19.40) 15.20 ∼ 29.40 (19.27)

PFOA ND ∼ 0.89 (0.09) ND ∼ 0.33 (0.03) 0.06 ∼ 0.34 (0.19) 0.09 ∼ 0.33 (0.13) PFNA ND ∼ 13.22 (1.46) ND ∼ 0.86 (0.07) 0.03 ∼ 1.00 (0.21) ND

PFDA 0.44 ∼ 20.58 (5.15) 0.06 ∼ 3.48 (0.75) ND ∼ 28.33 (12.20) 0.38 ∼ 5.78 (1.68) PFUnA 0.88 ∼ 45.16 (7.11) 0.04 ∼ 5.01 (0.80) 9.98 ∼ 52.39 (20.32) 1.93 ∼ 8.04 (4.53) PFDoA 0.11 ∼ 19.18 (3.20) ND ∼ 2.08 (0.43) 3.10 ∼ 13.94 (6.74) 0.92 ∼ 3.17 (1.76)

PFOS 0.18 ∼ 145.23 (13.93) ND ∼ 43.76 (6.15) 3.68 ∼ 233.68 (60.62) 1.61 ∼ 114.99 (19.38) PFDS ND ∼ 0.60 (0.04) ND ∼ 0.58 (0.05) 0.08 ∼ 1.27 (0.44) ND ∼ 0.23 (0.01)

∑PFASs** 1.72 ∼ 236.29 (31.18) 0.15 ∼ 54.64 (8.29) 31.08 ∼ 296.72 (100.72) 6.13 ∼ 131.58 (6.13) BW: body weight; BL: body length; ND: below the method detection limit; n: number of analyzed sample.

a

f/m (n.d.): female/male (not determined).

b ∑PFASs refer to sum of ten detectable PFAS in each individual fish.

dominant PFASs including PFOS, PFUnA, PFDoA and PFDA accounted for

94–99% of the total PFASs concentration in fish (Fig 3)

The concentrations of PFOS infish blood ranged from 0.18 to

145 ng mL−1(mean = 13.9 ng mL−1) in crucian carp and from 3.68

to 234 ng mL−1(mean = 60.6 ng mL−1) in mandarinfish The next 3

abundant PFASs were in the order of, PFUnA (mean = 7.11 ng mL−1)

N PFDA (mean = 5.13 ng mL−1)N PFDoA (mean = 3.2 ng mL−1) in

crucian carp blood and at mean concentration of 20.3 ng mL−1

N 12.2 ng mL−1N 6.74 ng mL−1in mandarinfish blood Mean PFOS

con-centrations infish blood analyzed in this study were relatively lower

than those reported for blood of mullet from Shihwa Lake, Korea (Yoo

et al., 2009); crucian carp and common carp from Gaobeidian Lake,

China (Li et al., 2008); a variety offish collected from Tokyo Bay,

Osaka Bay, Biwa Lake in Japan (Taniyasu et al., 2003); dolphin and

bluefin tuna from Italian coast (Kannan et al., 2002b) but higher than

those in the blood of shad from Shihwa Lake, Korea (Yoo et al., 2009);

and white semiknife carp, tilapia and leather catfish in China (Li et al.,

2008)

The profiles of PFOS concentration in fish liver varied widely The

maximum concentration of PFOS infish liver was 115 ng g−1ww in a

mandarinfish liver sample The mean concentration of PFOS in fish

liver samples and other aquatic animals collected from Korea (Moon

et al., 2010), Japan (Taniyasu et al., 2003) or the USA (Sinclair et al.,

2006) was relatively higher than that found in the present study PFOS

concentrations from skipjack tuna in the oceans (Hart et al., 2008) and

PFDA, PFUnA and PFDoA concentrations infish liver from Korea (Yoo

et al., 2009) were higher than those reported for crucian carp but

lower than those reported for mandarinfish in the present study

PFNA concentration found infish liver tissues in the present study was

lower than that reported for rockfish, shad and mullet from Korea

(Yoo et al., 2009) More detail comparisons of PFOS and PFOA

concen-trations obtained in biota sample from the present study with those

re-ported in previous studies are provided in the Supplementary

information

Significant positive correlations (p b 0.001) between PFAS

concen-trations in blood and corresponding concenconcen-trations in liver were

found for PFOS and PFDA in both crucian carp and mandarinfish

(Figs 4 and 5) Additionally, Spearman's correlation analysis showed

the significant positive correlation between concentrations among

PFOA, PFNA, PFDA, PFUnA, PFDoA, PFDS (p b 0.01) and PFHxS (p

b 0.05) in crucian carp blood and liver However, strong significant

cor-relations (pb 0.01 and r N 0.8) between PFASs concentration in fish

blood and liver were only observed for PFOS, PFUnA, PFDoA in crucian

carp and PFOS in mandarinfish These results suggest that blood can

be used for nonlethal monitoring of PFASs infishes

The ratio of PFAS concentrations infish blood to corresponding

con-centrations infish liver varied widely The ratio of PFOS concentration in

blood to liver varied from 0.71 to 5.17 (mean = 2.31) in crucian carp

and from 0.75 to 12.5 (mean = 4.81) in mandarinfish These

observa-tions suggest a non-equilibrium in PFAS concentraobserva-tions between liver

and blood offish, and indicate an ongoing exposure of fish to PFASs

(Taniyasu et al., 2003) Furthermore, physiological conditions (e.g., re-productive stages) may play a role in the alteration of blood to liver ra-tios in concentrations of PFASs (Kannan, 2011)

A significant negative correlation was observed between HSI and blood to liver ratio of PFOS and PFNA (pb 0.05) in crucian carp The blood to liver concentration ratio of PFOS and PFNA, thus, decreased with increasing HSI in crucian carp A significant positive correlation was found between GSI and blood to liver ratio of PFOS (pb 0.05) in mandarinfish The blood to liver ratio of PFOS, therefore, increased with increasing sexual maturity of mandarinfish, which is represented

by GSI

Some previous studies have reported gender-specific differences in the PFAS concentrations in aquatic animals (Keller et al., 2005; Kannan et al., 2002b) In the present study, there was no significant dif-ference (pN 0.05) in all PFAS concentrations between sexes of fish tis-sues except for PFNA in mandarinfish blood The PFNA concentration

in female mandarinfishes was significantly greater than that in males (pb 0.05)

PFNA was also the only PFAS that has the significant positive corre-lation with crucian carp body weight and body length (pb 0.05) These results suggest different PFAS composition profiles in the sur-veyedfish and chemical compound-specific, fish species-specific and tissue-specific bioaccumulation of PFASs

3.4 Bioconcentration factor (BCF) Mean BCFs of PFASs in biota are shown inTable 7 An increasing level

of mean concentrations of PFOS was found in biota with the increase in

Carp blood

Carp liver

Mandarin blood

Mandarin liver

Fig 3 Patterns showing relative concentrations of individual PFASs

(mean-%-composi-tion) in the surveyed fish tissues PFOS, PFUnA, PFDA and PFDoA were 4 predominant

PFASs in the fish tissues and accounted averagely for 97.47% of total PFASs concentration.

0 20 40

60

PFOS

0 1 2 3 4

PFDA

Blood concentration (ng/ml)

Fig 4 Relationship between PFOS, PFDA concentrations in blood and those in liver in crucian carp (Spearman's correlation, n = 69, r PFOS = 0.953, p PFOS b 0.001; r PFDA = 0.494, p PFDA b 0.001).

0 25 50 75

100 PFOS

0 2 4 6

0 100 200 300 0 20 40

PFDA

Blood concentration (ng/ml)

Fig 5 Relationship between PFOS, PFDA concentrations in blood and those in liver in man-darin fish (Spearman's correlation, n = 20, r PFOS = 0.880, p PFOS b 0.001; r PFDA = 0.675,

p PFDA = 0.001).

trophic level in the food chain The BCF of PFOS (concentration in biota/

concentration in water) was as follows: phytoplankton (196 L/kg)

b zooplankton (3233 L/kg) b crucian carp liver (4567 L/kg) b crucian

carp blood (11,167 L/kg)b mandarin liver (24,718 L/kg) b mandarin

blood (73,612 L/kg) This result was consistent with that reported in

earlier studies which reported the positive correlations of PFOS

concen-trations in biota with the increase in trophic level in the food chain

(Giesy and Kannan, 2001; Martin et al., 2004; Tomy et al., 2004; Li

et al., 2008)

Mean BCFs of all investigated PFASs infish blood were higher than

those infish liver The average BCF of PFOS in fish tissues in this study

was relatively higher than those reported in a variety offishes and

some other aquatic animals in bothfield and laboratory studies (3M,

2003; Moody et al., 2002; Morikawa et al., 2006) Although PFOS

con-centrations in water samples were comparable with PFOA

concentra-tions, the BCFs of PFOA in biota were 18–100 fold less than those of

PFOS Apart from PFOS, only PFNA was concentrated in plankton

sam-ples The BCFs of PFNA in phytoplankton and zooplankton were 1449

(L/kg) and 1312 (L/kg), respectively

4 Conclusions

The results of this study indicate a general ascending order of PFAS

concentration in freshwater aquatic ecosystem comprising water,

sedi-ment, plankton, crucian carp tissues, and mandarinfish tissues PFOS

was consistently detected at the greatest concentrations throughout

the investigated media No potential chronic and/or acute effects on

aquatic organisms due to PFOS and PFOA levels measured in surface

wa-ters from the six major rivers and lakes were expected

The rank order of mean BCF of PFOS in biota was; phytoplankton

b zooplankton b crucian carp liver b crucian carp blood b mandarin

fish liver b mandarin fish blood The data from the present study also

demonstrate that PFOS and LCPFCAs have high BCFs in crucian carp

tis-sues; only PFOS and PFNA were concentrated in plankton samples

Dif-ferent PFAS composition patterns infish tissues suggest species-specific

and tissue-specific bioaccumulation

The profiles of occurrence and spatial distribution of PFASs in various

environmental media suggest the existence of several sources of PFASs

and the continuing input PFASs in Korean rivers and lakes WWTP

dis-charges are a source of PFASs in freshwater ecosystems in South

Korea Further study should focus on identifying the existence and

sta-tus of PFASs sources in South Korean freshwater ecosystems

Conflict of interest

The authors declare no conflict of interest

Acknowledgments

This study was funded by the National Institute of Environmental

Research (NIER) of Korea (NIER/2010/1697 grant and NIER/SP2012/

166 grant)

Appendix A Supplementary data Supplementary data to this article can be found online athttp://dx doi.org/10.1016/j.scitotenv.2014.01.045

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