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Skipjack tuna as a bioindicator of contamination by perfluorinated compounds in the oceans
S CIE N CE OF T H E TOT AL E N V I RO N ME N T 4 0 3 ( 2 00 8 ) 2 1 5–2 21
a v a i l a b l e a t w w w. s c i e n c e d i r e c t . c o m
w w w. e l s e v i e r. c o m / l o c a t e / s c i t o t e n v
Skipjack tuna as a bioindicator of contamination by perfluorinated compounds in the oceans Kimberly Harta , Kurunthachalam Kannana,⁎, Lin Taoa , Shin Takahashib , Shinsuke Tanabeb a Wadsworth Center, New York State Department of Health, and Department of Environmental Health Sciences, School of Public Health, State University of New York, Albany, New York 12201-0509, USA b Center for Marine Environmental Studies (CMES), Ehime University, Matsuyama 790-8577, Japan
AR TIC LE I N FO
ABS TR ACT
Article history:
Perfluorinated chemicals (PFCs) have emerged as global environmental contaminants.
Received 28 April 2008
Studies have reported the widespread occurrence of PFCs in biota from marine coastal
Received in revised form 19 May 2008
waters and in remote polar regions. However, few studies have reported the distribution of
Accepted 20 May 2008
PFCs in biota from offshore waters and open oceans. In this study, concentrations of nine PFCs were determined in the livers of 60 skipjack tuna (Katsuwonus pelamis) collected from
Keywords:
offshore waters and the open ocean along the Pacific Rim, including the Sea of Japan, the
PFOS
East China Sea, the Indian Ocean, and the Western North Pacific Ocean, during 1997–1999. At
Tuna
least one of the nine PFCs was found in every tuna sample analyzed. Overall,
Pacific Ocean
perfluorooctanesulfonate (PFOS) and perfluoroundecanoic acid (PFUnDA) were the
PFOA
predominant compounds found in livers of tuna at concentrations of b 1–58.9 and b1–
Perfluoroundecanoic acid
31.6 ng/g, wet wt, respectively. Long-chain perfluorocarboxylates such as perfluorodecanoic
Bioindicator
acid (PFDA) and perfluorododecanoic acid (PFDoDA) were common in the tuna livers. In
Asia
livers of tuna from several offshore and open-ocean locations, concentrations of PFUnDA were greater than the concentrations of PFOS. The profiles and concentrations of PFCs in tuna livers suggest that the sources in East Asia are dominated by long-chain perfluorocarboxylates, especially PFUnDA. High concentrations of PFUnDA in tuna may indicate a shift in sources of PFCs in East Asia. The spatial distribution of PFOS in skipjack tuna reflected the concentrations previously reported in seawater samples from the Pacific and Indian Oceans, suggesting that tuna are good bioindicators of pollution by PFOS. Despite its predominance in ocean waters, PFOA was rarely found in tuna livers, indicative of the low bioaccumulation potential of this compound. Our study establishes baseline concentrations of PFCs in skipjack tuna from the oceans of the Asia-Pacific region, enabling future temporal trend studies of PFCs in oceans. © 2008 Elsevier B.V. All rights reserved.
1.
Introduction
Worldwide contamination by persistent, bioaccumulative, and toxic compounds such as perfluorochemicals (PFCs) is of great concern. PFCs have been detected in a wide range of
environmental and biological matrices including air (Wallington et al., 2006; Kim and Kannan, 2007), surface water (Yamashita et al., 2005; Sinclair et al., 2006; Wei et al., 2007), snow (Young et al., 2007), sediment (Higgins et al., 2005; Nakata et al., 2006), wildlife (Giesy and Kannan, 2001; Tao
⁎ Corresponding author. Wadsworth Center, New York State Department of Health, Empire State Plaza, PO Box 509, Albany, NY 12201-0509 USA. Tel.: +1 518 474 0015; fax: +1 518 473 2895. E-mail address: [email protected] (K. Kannan). 0048-9697/$ – see front matter © 2008 Elsevier B.V. All rights reserved. doi:10.1016/j.scitotenv.2008.05.035
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et al., 2006), and humans (Kannan et al., 2004). Because of the persistence and relatively high water solubilities of PFCs (on the order of several hundreds to thousands of parts-permillion), surface water is considered to be a reservoir for PFCs (Prevedouros et al., 2006). The most probable environmental sink for PFCs is the open ocean, as has been reported for other persistent organic pollutants (Loganathan and Kannan, 1994; Yamashita et al., 2005). It has been estimated that N80% of the global inventory of perfluorooctanoate (PFOA) is present in the world’s oceans (Armitage et al., 2006). Despite the importance of the oceans as a final sink for PFCs, few studies have examined the distribution of PFCs in biota from offshore waters and open oceans. The characteristics of PFCs that cause them to persist in the environment are also the characteristics that made them attractive compounds for industrial usage for over 50 years. PFCs have been used as surface protectants on textiles and specialty papers, and as surface tension-lowering agents in fire-fighting foams. In 2000, a voluntary phase-out of manufacturing of certain perfluorooctanesulfonyl-based compounds such as perfluorooctanesulfonate (PFOS) was undertaken by a leading manufacturer, because of concerns about these compounds' widespread environmental occurrence and potential toxic effects. Chronic health effects of PFCs in humans are still under debate, because of interspecies variation in the mode of action. Laboratory animal studies and in vitro tests have suggested that certain PFCs can act as potent peroxisome proliferators, inhibitors of gapjunction intercellular communication, and tumor promoters (Andersen et al., 2008). Although, the occurrence of PFCs in inland and coastal waters of many countries and in remote polar regions has been studied, few reports have documented the distribution of PFCs in the open ocean (Yamashita et al., 2004; Yamashita et al., 2005; Tao et al., 2006; Yamashita et al., 2008). In the present study, distribution and profiles of PFCs were assessed in offshore waters and open-ocean waters of the Asia-Pacific region, using skipjack tuna (Katsuwonus pelamis) as a bioindicator. Skipjack tuna are distributed in offshore and open-ocean tropical and temperate waters, in the Pacific, the Atlantic, and the Indian Oceans. This species has been shown to be a suitable bioindicator for monitoring global oceanic pollution by polychlorinated biphenyls (PCBs), dichloro-diphenyl-trichloroethane (DDTs), polychlorinated dibenzo-p-dioxins (PCDDs) and dibenzofurans (PCDFs), polybrominated diphenyl ethers (PBDEs), and organotins (Ueno et al., 2003, 2004a,b, 2005, 2006). Skipjack tuna are an important commercial species, and its ecology and biology are well studied. Since they are also a dominant product in the world's tuna market, measurement of PFCs in skipjack tuna would also help in the assessment of potential exposures to humans. Additionally, monitoring of PFCs in oceans is required so that we can understand the sources and transport of these contaminants. The objectives of this study were to determine the concentrations, spatial distribution, and profiles of PFCs in skipjack tuna collected from offshore and open oceans along the Pacific Rim, and to examine the suitability of skipjack tuna as a bioindicator of PFCs in global pollution monitoring. The data presented in this study will provide baseline information for future monitoring studies, contributing to an understanding of global trends of PFCs.
2.
Materials and methods
2.1.
Standards and reagents
PFOA and potassium salt of PFOS were purchased from Tokyo Chemical Industries (Portland, OR). Perfluorononanoate (PFNA), perfluorodecanoate (PFDA), and perfluoroheptanoate (PFHpA) were from Fluorochem Ltd (Glossop, Derbyshire, UK). Perfluoroundecanoate (PFUnDA) and perfluorododecanoate (PFDoDA) were from Aldrich (St. Louis, MO). Perfluorooctanesulfonamide (PFOSA), potassium salts of perfluorobutanesulfonate (PFBS) and perfluorohexanesulfonate (PFHxS), 13C2-PFNA, and 13C2-PFDA were provided by the 3 M Company (St. Paul, MN). 13 C4-PFOS and 13C4-PFOA were purchased from Wellington Laboratories (Guelph, ON, Canada). Purities of all standards were ≥95%. All solvents were HPLC grade and reagents were ACS grade (J.T.Baker, Phillipsburg, NJ).
2.2.
Sample collection
During 1997-1999, skipjack tuna were collected from oceanic waters off Japan, the Sea of Japan, the East China Sea (off Taiwan), off Indonesia, the Indian Ocean, and the (mid) North Pacific Ocean (Fig. 1). Skipjack tuna were obtained from fish markets and fishing villages after confirmation of the origin of the catch, while the tuna collected from the (mid) North Pacific Ocean and the Indian Ocean were caught during a research cruise. The latitude and longitude of sampling locations of tuna are given in Table 1. Liver and muscle tissues were dissected out and kept in polyethylene bags, stored at −20 °C until analysis. Tuna livers archived at environmental specimen bank (ES-Bank) of Center for Marine Environmental Studies, Ehime University, Japan, were used.
2.3.
Chemical analysis
Concentrations of PFCs in livers of skipjack tuna were determined according to the procedure described previously (Kannan et al., 2001). The liver sample (0.7–0.9 g) was homogenized with 5 mL of Milli-Q water, and then 1 mL of the homogenate was transferred into a polypropylene tube (PP tube) and 100 μl of 2.5 ng/mL internal standard mixture (13C4-PFOS, 13C4-PFOA, 13C2-PFDA, and 13C2-PFNA), 2 mL of 0.25 M sodium carbonate buffer, 1 mL of 0.5 M tetrabutylammonium hydrogensulfate solution (adjusted to pH 10) were added and mixed thoroughly. Extraction was carried out by addition of 5 mL of methyl-tert-butyl ether (MTBE), with vigorous shaking for 40 min. The sample was then centrifuged at 4000 rpm for 5 min to separate the organic layer from the aqueous layer. The aqueous layer was transferred into another PP tube, and the extraction was repeated with 3 mL of MTBE. After extraction, the two organic layers were combined and evaporated to near-dryness under a stream of nitrogen. The sample was then reconstituted with 1 mL of methanol, vortexed for 30 s, centrifuged at 4000 rpm for 2 min, and transferred into a 2-mL autosampler vial. The target analytes were detected and quantified on an Agilent 1100 Series high performance liquid chromatograph (HPLC), coupled with an Applied Biosystems API 2000
S CIE N CE OF T H E TOT AL E N V I RO N ME N T 4 0 3 ( 2 00 8 ) 2 1 5–2 21
217
Fig. 1 – Map showing the sampling locations for skipjack tuna, with an enlarged map of Japan. electrospray triple-quadrupole mass spectrometer (ESI-MS/ MS). Ten microliters of the extract were injected into a Betasil C18 (100 mm × 2.1 mm) column with a (20 mm × 2.1 mm) guard column, both with a 5-μm particle size (Thermo Electron Corporation, Waltham, MA). The mobile phase consisted of a gradient elution of 2 mM ammonium acetate and methanol. The gradient started at 10% methanol and increased to 100% after 10 min; it was held at 100% for 2 min, then reversed back down to 10% methanol. The MS/MS was operated in a multiple reaction monitoring (MRM) mode and the mass transitions monitored were: 399 N 80 for PFHxS, 499 N 99 for PFOS, 503 N 99 for 13C4-PFOS, 498 N 78 for PFOSA, 363 N 319 for PFHpA, 413 N 369 for PFOA, 417 N 372 for 13C4-PFOA, 463 N 419 for PFNA, 465 N 420 for 13C2-PFNA, 513 N 469 for PFDA, 515 N 470 for 13C2-PFDA, 563 N 519 for PFUnDA, and 613 N N569 for PFDoDA. The sum of the concentrations of the nine PFCs measured in this study is denoted as total PFCs (ΣPFC).
were prepared in methanol at concentrations ranging from 0.1 to 50 ng/mL. Calibration standards were injected every day before and after a batch of samples was analyzed. A midpoint calibration standard was injected after every 10 samples, throughout the instrumental analysis, to check for instrument response and drift. Procedural blanks were analyzed by passage of water and reagents through the entire analytical procedure, to monitor for contamination in reagents and glassware. Concentrations were not corrected for the recoveries of internal standards, because recoveries were within an acceptable level of 70% for all compounds. Quantitation of PFCs was performed using a quadratic regression fit analysis weighted by 1/x of the matrix extracted calibration curve. The limit of quantitation (LOQ) was considered to be the lowest acceptable standard within ±30% of the theoretical value, and has a peak area twice as large as that of the blanks. The LOQ of PFCs ranged from 0.9 to 1.8 ng/g, wet wt, while that for PFHpA and PFOA was 2.5 and 3.2 ng/g, wet wt, respectively.
2.4.
2.5.
Quality assurance and quality control
A known concentration (10 ng each) of target compounds was spiked into an aliquot of the sample matrix (i.e., matrix spikes) and then run through the analytical procedure as a check for matrix effects, through calculation of the recoveries. Overall, mean matrix spike recoveries ranged from 65 to 98% (n=12). Mean recoveries of PFNA and PFUnDA were 65±10%, whereas the mean recoveries of the other seven compounds were 76±14%. 13Clabelled internal standards (13C4-PFOS, 13C4-PFOA, 13C2-PFDA, and 13 C2-PFNA) were spiked into all of the samples for the calculation of recoveries. Mean internal standard recoveries in samples for 13C2-PFNA was 64 ±9%, whereas the recoveries of other internal standards were 74±14%. External calibration standards
Statistical analysis
Statistical analyses were performed using Statgraphics plus 5.1 (Manugistics Inc., Rockville, MD). Concentrations that were below the LOQ were assigned a value of half the LOQ, for statistical analyses.
3.
Results and discussion
3.1.
PFC concentrations
Concentrations of total PFCs in skipjack tuna livers ranged from b1 to 82.9, ng/g wet wt (Table 1). PFOS and PFUnDA
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Table 1 – Mean (range), and total PFC concentrations (ng/g, wet wt.) in the livers of skipjack tuna collected from open ocean and offshore waters of the Pacific Rim* Sampling Location Geographical coordinates Off-shore sites Izu, Japan N33,50-34/E140,50 Miyagi-1, Japan N38,E142 Miyagi-2, Japan N38,E144 Chiba, Japan N34,E140 Kochi-1, Japan N33,E134 Kochi-2, Japan N33,E134 Kagoshima, Japan N30,E130 Sea of Japan N37,E135 Tsushima, Japan N33,E129 East China Sea (Taiwan) N25/E125 Jakarta, Indonesia
Open-Ocean sites W. North Pacific Ocean N44,29/E175,31 Mauritius, Indian Ocean % detectable samples
Collection Date
n
Jun-97
5
Oct-97
4
Jul-99
5
Oct-97
4
Oct-97
5
Nov-98
9
Oct-97
5
Oct-97
5
Oct-97
5
Nov-98
2
Jan-99
5
Aug-98
3
Jan-99
3
PFOS
PFOSA
PFNA
PFDA
PFUnDA
PFDoDA
ΣPFCs⁎⁎⁎
3.30 (2.2–4.8) 4.51 (2.5–5.8) 8.49 (6.3–11.1) 51.2 (34.4–58.9) 9.08 (1.5–21.1) 19.8 (2.4–45.6) 5.91 (2.4–10.6) 10.9 (7.6–13.9) 17.5 (9.6–34.5) 6.12 (5.1–7.1) 4.09 [3.38] (b 1–7.5)
b 1 [0.51]⁎⁎ (b 1) b1 [0.65] (b 1) 4.29 (2.9–5.9) 2.96 (1.9–3.7) 2.5 [1.73] (b1–5.0) 1.92 [1.45] (b1–2.4) b1 [0.62] (b1–1.1) 1.27 [1.12] (b1–1.5) 1.84 (1.3–2.8) b1 [0.77] (b1–1.0) b1 [0.51] (b 1)
b1.1[0.55] (b1.1) b 1.1 [0.55] (b1.1) b1.1 [0.55] (b1.1) 1.88 [1.21] (b 1.1–2.38) b 1.1 [0.55] (b1.1) 1.14 [0.62] (b 1.1–1.14) b 1.1 [0.55] (b1.1) b 1.1 [0.55] (b1.1) 2.48 [0.94] (b 1.1–2.48) b 1.1 [0.55] (b1.1) b 1.1 [0.55] (b1.1)
b0.9 [0.46] (b 0.9) b0.9 [0.46] (b 0.9) b0.9 [0.46] (b 0.9) 1.84 (1.1–3.3) 1.3 [0.90] (b0.9–1.7) 2.04 [1.34] (b0.9–2.7) b0.9 [0.46] (b 0.9) 0.93 [0.55] (b0.9–0.93) 1.47 [0.86] (b0.9–1.9) b0.9 [0.46] (b 0.9) b0.9 [0.46] (b 0.9)
6.40 (3.0–9.8) 8.35 (3.5–12.5) 7.60 (5.5–9.1) 17.9 (13.4–21) 13.63 (3.5–28.7) 19.8 (8.7–31.6) 10.1 (6.0–13.2) 7.59 (2.5–11.3) 3.55 (2.4–5.3) 12.5 (11.1–14.0) 2.41 (1.3–4.3)
2.87 [2.09] (b 1.8–3.35) 2.90 [2.41] (b 1.8–4.2) 2.0 [1.12] (b 1.8–1.97) 5.29 (4.4–6.5) 4.02 [3.40] (b 1.8–7.2) 4.50 (2.1–7.3) 2.82 (1.9–4.0) 3.35 (2.6–4.4) 3.55 (2.7–4.7) 2.57 (2.1–3.0) b1.8 [0.91] (b 1.8)
13.2
2.13 [1.07] (b 1–2.1) b 1 [0.54] (b1) 100
b1 [0.51] (b 1) b1
b1.1 b1.1
b0.9 [0.46] (b 0.9) b 1.1
2.71 (1.9–4.3) b 1.8
83
57
93
4.25 (1.3–7.9) b1 [0.50] (b1) 100
16.7 22.4 82.9 29.0 47.5 20.0 23.7 23.0 28.6 9.00
7.30 [1.04]
95
⁎PFHpA, PFOA, and PFHxS were not detected in more than 10% of the samples analyzed. ⁎⁎There are two mean values for certain compounds. Values in brackets [] represent mean concentrations for all values while assigning a value half of the LOQ, for those samples that had values below LOQ. Values in front of [] refers to the mean of detectable concentrations (NLOQ) only. ⁎⁎⁎ΣPFCs refer to average of the sum of all nine detectable perfluorochemical concentrations, while assigning a value of half the LOQ to those samples detected below the LOQ.
were the predominant compounds found, with concentrations ranging from b1 to 58.9 and b1 to 31.6 ng/g, wet wt, respectively. PFOSA, PFNA, PFDA, and PFDoDA were detected in 83, 93, 57 and 95% of the tuna liver samples, respectively. PFHxS, PFHpA, and PFOA were each detected in less than 10% of the samples analyzed. The highest concentration of PFOS (58.9 ng/g, wet wt) was found in tuna from Chiba, Japan. High concentrations of PFUnDA were found at offshore sites around Japan, particularly near Chiba and Kochi (mean: 17.9 and 19.8 ng/g, wet wt); PFOS concentrations were also elevated at these sites (mean: 51.2 and 19.8 ng/g, wet wt). Mean concentrations of PFUnDA in tuna from the East China Sea (off Taiwan) and in samples from Izu and Kagoshima, Japan, were 2-fold greater than the mean concentrations of PFOS at these sites. The mean concentrations of PFUnDA were higher than the concentrations of PFOS in tuna livers from five of 11 offshore locations, and the open-ocean site in the (mid) North Pacific Ocean. PFOS was found in tuna livers from the Indian Ocean at concentrations below the LOQ (~0.5 ng/g, wet wt). Total PFC concentrations in skipjack tuna from the Indian Ocean were at least 10-times lower than those in samples
from the (mid) North Pacific Ocean (Table 1). The low concentrations of PFCs in skipjack tuna from the Indian Ocean are similar to that reported for seawater collected from the Indian Ocean, in which PFC concentrations were at trace to undetectable levels (Wei et al., 2007; Yamashita et al., 2008). The spatial differences in PFOS concentrations in tuna livers were similar to those reported for albatross livers from the North Pacific Ocean and the Indian Ocean. Mean PFOS concentrations in albatross livers from the North Pacific Ocean and the Indian Ocean were 5.1 and 3.2 ng/g, wet wt, respectively (Tao et al., 2006) and the corresponding concentrations in tuna livers were 1.1 and ~0.5 ng/g, wet wt. Tuna samples collected from the western North Pacific Ocean, along the Pacific Rim, contained 10-fold higher concentrations of PFCs than did tuna from the middle of North Pacific Ocean. The east-west gradient in PFC concentrations in the Pacific Ocean waters has been reported earlier (i.e., greater concentrations of PFCs in waters of the western North Pacific than in the middle or Eastern North Pacific; Yamashita et al., 2008). The occurrence of long-chain perfluorocarboxylates (PFDA, PFUnDA, and PFDoDA) has been reported in water samples
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Table 2 – Spearman's correlation among major perfluoro chemicals found in livers of skipjack tuna (n = 60) from offshore and open ocean waters
PFOS PFOSA PFDA PFUnDA PFDoDA
PFOSA
PFDA
PFUnDA
PFDoDA
PFNA
0.81⁎⁎
0.78⁎⁎ 0.61⁎⁎
0.63⁎⁎ 0.52⁎⁎ 0.65⁎⁎
0.74⁎⁎ 0.51⁎⁎ 0.79⁎⁎ 0.70⁎⁎
0.58⁎⁎ 0.53⁎⁎ 0.57⁎⁎ 0.44⁎⁎ 0.42⁎⁎
⁎⁎Correlation is significant at the 0.01 level (2-tailed t test).
collected from coastal and offshore waters of the western North Pacific Ocean, along the Pacific Rim (Wei et al., 2007). However, long-chain PFCs were not found in waters of the open (mid) North Pacific Ocean (Wei et al., 2007). Long-chain perfluorocarboxylates were found in tuna livers from the middle of the North Pacific Ocean as well as in offshore waters along Japan, in the East China Sea (off Taiwan), and off Indonesia. Although PFOA was the most abundant PFC in seawater samples from the Pacific Ocean (Yamashita et al., 2005), this compound was rarely detected in our tuna livers. Low concentrations of PFOA in tuna livers can be attributed to the low bioaccumulation potential of PFOA (Conder et al., 2008). Conversely, long-chain perfluorocarboxylates, such as PFUnDA, were rarely found in open ocean water samples (Wei et al., 2007); however because of the relatively high bioaccumulation potential they were found in tuna livers (Conder et al., 2008). High concentrations of PFUnDA in tuna samples analyzed in this study, particularly in the samples collected from the East China Sea (off Taiwan) and in samples collected off Japan, suggest the existence of distinctive sources of PFCs that are enriched in long-chain perfluorocarboxylates. PFUnDA was not found in seawater collected from offshore waters of the East China Sea, although PFDA and PFDoDA were found in seawater samples from this region (Wei et al., 2007). High concentrations of PFUnDA in our tuna livers suggest the exposure of fish to fluorotelomerbased compounds produced or used in industrialized regions of East Asia; several fluorotelomer-based industries are located in Japan and China (Prevedouros et al., 2006). Production of 8:2 fluorotelomer alcohols (FTOHs) or fluorotelomer olefins (FTOs) primarily in Japan has been reported (Prevedouros et al., 2006); however occurrence of PFUnDA in tuna livers is indicative of degradation of 10:2 FTOH or 10:2 FTO. FTOHs are mainly manufactured in even chain lengths, but have been reported to yield odd- and even-chain length perfluorocarboxylates upon degradation. For example, 10:2 FTOH (CF3(CF2)9CH2CH2OH) can degrade to PFDA and PFUnDA in sewage sludge and in the environment (Wang et al., 2005; Sinclair and Kannan, 2006; Wallington et al., 2006). These results suggest that PFUnDA and other long-chain perfluorocarboxylates in livers from tuna collected in offshore waters along the Pacific Rim originate from the degradation of 10:2 FTOH. A significant correlation existed between the liver concentrations of PFUnDA and PFDA/PFDoDA (Table 2). Concentrations of PFOS in the livers of skipjack tuna from Chiba, Japan (34–59 ng/g, wet wt) were similar to the concentrations reported for livers of bluefin tuna from the Italian coast of the Mediterranean Sea (21–87 ng/g, wet wt) (Kannan et al., 2002a) and in the blood of cod (6.1–52 ng/g, wet wt) from the
Fig. 2 – Relationship between PFOS concentrations in liver and body weight of skipjack tuna. southern Baltic Sea (Falandysz et al., 2006). Concentrations of PFOS in tuna livers from the offshore and oceanic waters were 10to 100-fold lower than the concentrations reported for fish from inland waters of New York State, USA (Sinclair et al., 2006) and in fish from Tokyo Bay, Japan (Taniyasu et al., 2003). Concentrations of PFOS in skipjack tuna livers were not correlated with body weight (p≥0.1) (Fig. 2). Similarly, no significant difference existed in the concentrations of PFOS between the genders (p≥0.05) (Fig. 3). An earlier study showed that liver concentrations of PFOS in female smallmouth bass were lower than in males (Sinclair et al., 2006).
3.1.1.
Geographic distribution and PFC profiles
The mean concentration of PFOS in tuna livers from offshore sites (off Japan, off Taiwan, and off Indonesia) was approximately 10 to 20-fold higher than the mean concentration found for tuna livers from open ocean waters (i.e., the mid Pacific Ocean and the Indian Ocean). The highest concentrations of several of the PFCs were found in locations near industrialized areas such as Chiba, which is a major commercial and industrial center surrounding Tokyo Bay. Livers of birds collected from Chiba, Japan, during 1997–1999 showed high PFOS concentrations (19 to 650 ng/g, wet wt) (Kannan et al., 2002b). Between the two open-ocean locations, higher concentrations of PFOS and PFUnDA were found in tuna from the (mid) North Pacific Ocean than in tuna from the Indian Ocean. PFOSA, PFDA, and PFDoDA were found in tuna livers from the (mid) North Pacific Ocean (Table 1), but not in tuna from the Indian Ocean. The large spatial variation in PFC concentrations between the open-oceans and the offshore sites suggests the influence of local sources from nearby coastal areas.
Fig. 3 – Concentrations of PFOS in male and female tuna livers from various sampling locations (value above each bar indicates the mean concentration).
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Fig. 4 – Profiles of perfluorochemical composition in skipjack tuna livers from offshore sites and from open water sites in the mid-North Pacific and Indian Oceans. Concentrations of PFCs in waters of the eastern North Pacific Ocean were lower than the concentrations in western North Pacific Ocean waters (Yamashita et al., 2008). Further, concentrations of PFCs in waters of the Atlantic Ocean were higher than the concentrations in the Pacific Ocean waters (Yamashita et al., 2005). In the present study, tuna samples were not available from the Atlantic Ocean or the eastern North Pacific Ocean. Further investigation into concentrations of PFCs in tuna from the Atlantic Ocean would help in understanding the sources and pathways of PFCs to the oceans. The profiles of PFC concentrations in livers from tuna collected off Japan were different from the profiles found for the open-ocean tuna samples (Fig. 4). PFOS was the predominant compound in tuna samples from offshore sites in Miyagi (the samples from 1999), Chiba, Kochi (the samples from 1998), Tsushima, the Sea of Japan, the Indian Ocean, and Indonesia, contributing from 38% to 61% of the ΣPFC concentrations. PFUnDA was the predominant compound in tuna livers from Izu, Miyagi (the samples from 1997), Kochi (the samples from 1997), Kagoshima, the East China Sea, and the (mid) North Pacific Ocean, accounting for 47 to 54% of the ΣPFC concentrations. Although PFUnDA was the predominant compound in tuna collected in 1997 from Miyagi and Kochi, PFOS was predominant in samples collected from these locations in 1998 and 1999. These results may indicate temporal/seasonal differences in sources and/or the movement of tuna along the offshore/coastal waters of Japan. Tuna collected from the pelagic waters of the (mid) North Pacific Ocean contained notable proportions of PFUnDA and PFDoDA (47% and 30%, respectively) within the ΣPFC concentrations. Elevated concentrations of PFUnDA and PFDoDA in tuna from the (mid) North Pacific Ocean when compared to the Indian Ocean samples indicate sources enriched with long-chain perfluoroalkylcarboxylates arising from countries of East Asia. The correlations among the six major PFCs found in tuna livers from the offshore and open ocean locations are presented in Table 2. Concentrations of PFOS in tuna livers were significantly correlated (p ≤ 0.01) with the concentrations of PFOSA, PFDA, PFUnDA, PFDoDA, and PFNA. Concentrations of long-chain perfluorocarboxylates were significantly posi-
tively inter-correlated (Table 2). Concentrations of long-chain carboxylates (i.e., C10 to C12) were greater than the concentrations of PFOA (C8) and PFNA (C9). Furthermore, the concentration of the odd-carbon chain perfluorocarboxylate (i.e., C11; PFUnDA) exceeded the concentrations of the neighboring even-carbon chain compounds (C10 and/or C12). Another remarkable characteristic of the PFC profile in tuna livers was the lower PFNA/PFUnDA ratio, as compared with fish collected from the Arctic waters and European coastal waters (Houde et al., 2006; Falandysz et al., 2006). PFNA/ PFUnDA ratios in fish livers from the Canadian Arctic and the Baltic Sea were in the range of 0.65–0.75 (Houde et al., 2006; Falandysz et al., 2006), whereas the ratios in tuna livers from the offshore waters of Asia, in our study, were 0.04–0.06. The low proportions of PFNA and high proportions of PFUnDA in skipjack tuna livers indicate distinctive sources of PFCs arising from East Asian countries. PFOS concentrations in surface seawater of the western North Pacific Ocean were 10 to 15 times higher than the concentrations determined for the South Pacific and the Indian Oceans (Yamashita et al., 2005, 2008). PFOS concentrations in coastal waters of Tokyo Bay were approximately two to three orders of magnitude greater than the concentrations found at offshore locations around Japan. The pattern of elevated concentrations of PFOS in coastal waters near Tokyo Bay was similar to the pattern of concentrations of PFOS found in tuna livers collected in waters off Japan (Taniyasu et al, 2003; Yamashita et al., 2005, 2008). Similarly, elevated concentrations of PFOS in tuna livers from the East China Sea reflect the high concentrations found in water samples from this sea (So et al., 2004). The overall trend of PFOS contamination in seawater is comparable to the trend found in livers of skipjack tuna (Table 3). This suggests the utility of skipjack tuna as a bioindicator for monitoring PFOS in oceans. Nevertheless, it should be noted that PFOA was the predominant PFC in seawater from almost all global oceans. However, PFOA was not detected in livers of tuna, because of its low bioaccumulation potential, as mentioned earlier (Conder et al., 2008). In summary, our results demonstrate spatial differences in concentrations of PFCs in livers from tuna sampled in offshore waters and open oceans along the Pacific Rim. Concentration profiles and correlations among the PFCs indicate the presence of distinct sources arising from East Asia. This study demonstrates the suitability of skipjack tuna as a bioindicator to monitor contamination by bioaccumulative PFCs such as PFOS in world’s oceans. Earlier studies have reported greater concentrations of PFCs in waters of the Table 3 – Range of PFOS concentrations in seawater (pg/L) and skipjack tuna livers (ng/g wet wt.) from waters off Japan and from open ocean sites Location
Seawater (pg/L)⁎
Tuna liver (ng/g)
Tokyo Bay/Chiba Offshore waters of Japan Japan Sea South/East China Sea Central to Eastern Pacific Ocean Indian Ocean
338–57700 40–75 2–15 8–113 1.1–20 5–11
34.4–58.9 1.5–45.6 8–14 5–7 1.1–2.1 b 1.1
⁎Yamashita et al. (2005, 2008).
S CIE N CE OF T H E TOT AL E N V I RO N ME N T 4 0 3 ( 2 00 8 ) 2 1 5–2 21
Atlantic than in waters of the Pacific. Tuna samples were not available from the Atlantic Ocean for this study, and future research should assess the levels and profiles of PFCs in tuna from the oceans of the Western Hemisphere.
Acknowledgements Financial support for the sampling part of the study was provided by Grants-in-Aid for Scientific Research (S) (No. 20221003) from the Japan Society for the Promotion of Science (JSPS) and the Waste Management Research Grants (K1821 and K1836) from the Ministry of Environment, Japan. This study was supported by the “Global COE Program” of the Japanese Ministry of Education, Culture, Sports, Science and Technology (MEXT), Japan.
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a v a i l a b l e a t w w w. s c i e n c e d i r e c t . c o m
w w w. e l s e v i e r. c o m / l o c a t e / s c i t o t e n v
Skipjack tuna as a bioindicator of contamination by perfluorinated compounds in the oceans Kimberly Harta , Kurunthachalam Kannana,⁎, Lin Taoa , Shin Takahashib , Shinsuke Tanabeb a Wadsworth Center, New York State Department of Health, and Department of Environmental Health Sciences, School of Public Health, State University of New York, Albany, New York 12201-0509, USA b Center for Marine Environmental Studies (CMES), Ehime University, Matsuyama 790-8577, Japan
AR TIC LE I N FO
ABS TR ACT
Article history:
Perfluorinated chemicals (PFCs) have emerged as global environmental contaminants.
Received 28 April 2008
Studies have reported the widespread occurrence of PFCs in biota from marine coastal
Received in revised form 19 May 2008
waters and in remote polar regions. However, few studies have reported the distribution of
Accepted 20 May 2008
PFCs in biota from offshore waters and open oceans. In this study, concentrations of nine PFCs were determined in the livers of 60 skipjack tuna (Katsuwonus pelamis) collected from
Keywords:
offshore waters and the open ocean along the Pacific Rim, including the Sea of Japan, the
PFOS
East China Sea, the Indian Ocean, and the Western North Pacific Ocean, during 1997–1999. At
Tuna
least one of the nine PFCs was found in every tuna sample analyzed. Overall,
Pacific Ocean
perfluorooctanesulfonate (PFOS) and perfluoroundecanoic acid (PFUnDA) were the
PFOA
predominant compounds found in livers of tuna at concentrations of b 1–58.9 and b1–
Perfluoroundecanoic acid
31.6 ng/g, wet wt, respectively. Long-chain perfluorocarboxylates such as perfluorodecanoic
Bioindicator
acid (PFDA) and perfluorododecanoic acid (PFDoDA) were common in the tuna livers. In
Asia
livers of tuna from several offshore and open-ocean locations, concentrations of PFUnDA were greater than the concentrations of PFOS. The profiles and concentrations of PFCs in tuna livers suggest that the sources in East Asia are dominated by long-chain perfluorocarboxylates, especially PFUnDA. High concentrations of PFUnDA in tuna may indicate a shift in sources of PFCs in East Asia. The spatial distribution of PFOS in skipjack tuna reflected the concentrations previously reported in seawater samples from the Pacific and Indian Oceans, suggesting that tuna are good bioindicators of pollution by PFOS. Despite its predominance in ocean waters, PFOA was rarely found in tuna livers, indicative of the low bioaccumulation potential of this compound. Our study establishes baseline concentrations of PFCs in skipjack tuna from the oceans of the Asia-Pacific region, enabling future temporal trend studies of PFCs in oceans. © 2008 Elsevier B.V. All rights reserved.
1.
Introduction
Worldwide contamination by persistent, bioaccumulative, and toxic compounds such as perfluorochemicals (PFCs) is of great concern. PFCs have been detected in a wide range of
environmental and biological matrices including air (Wallington et al., 2006; Kim and Kannan, 2007), surface water (Yamashita et al., 2005; Sinclair et al., 2006; Wei et al., 2007), snow (Young et al., 2007), sediment (Higgins et al., 2005; Nakata et al., 2006), wildlife (Giesy and Kannan, 2001; Tao
⁎ Corresponding author. Wadsworth Center, New York State Department of Health, Empire State Plaza, PO Box 509, Albany, NY 12201-0509 USA. Tel.: +1 518 474 0015; fax: +1 518 473 2895. E-mail address: [email protected] (K. Kannan). 0048-9697/$ – see front matter © 2008 Elsevier B.V. All rights reserved. doi:10.1016/j.scitotenv.2008.05.035
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et al., 2006), and humans (Kannan et al., 2004). Because of the persistence and relatively high water solubilities of PFCs (on the order of several hundreds to thousands of parts-permillion), surface water is considered to be a reservoir for PFCs (Prevedouros et al., 2006). The most probable environmental sink for PFCs is the open ocean, as has been reported for other persistent organic pollutants (Loganathan and Kannan, 1994; Yamashita et al., 2005). It has been estimated that N80% of the global inventory of perfluorooctanoate (PFOA) is present in the world’s oceans (Armitage et al., 2006). Despite the importance of the oceans as a final sink for PFCs, few studies have examined the distribution of PFCs in biota from offshore waters and open oceans. The characteristics of PFCs that cause them to persist in the environment are also the characteristics that made them attractive compounds for industrial usage for over 50 years. PFCs have been used as surface protectants on textiles and specialty papers, and as surface tension-lowering agents in fire-fighting foams. In 2000, a voluntary phase-out of manufacturing of certain perfluorooctanesulfonyl-based compounds such as perfluorooctanesulfonate (PFOS) was undertaken by a leading manufacturer, because of concerns about these compounds' widespread environmental occurrence and potential toxic effects. Chronic health effects of PFCs in humans are still under debate, because of interspecies variation in the mode of action. Laboratory animal studies and in vitro tests have suggested that certain PFCs can act as potent peroxisome proliferators, inhibitors of gapjunction intercellular communication, and tumor promoters (Andersen et al., 2008). Although, the occurrence of PFCs in inland and coastal waters of many countries and in remote polar regions has been studied, few reports have documented the distribution of PFCs in the open ocean (Yamashita et al., 2004; Yamashita et al., 2005; Tao et al., 2006; Yamashita et al., 2008). In the present study, distribution and profiles of PFCs were assessed in offshore waters and open-ocean waters of the Asia-Pacific region, using skipjack tuna (Katsuwonus pelamis) as a bioindicator. Skipjack tuna are distributed in offshore and open-ocean tropical and temperate waters, in the Pacific, the Atlantic, and the Indian Oceans. This species has been shown to be a suitable bioindicator for monitoring global oceanic pollution by polychlorinated biphenyls (PCBs), dichloro-diphenyl-trichloroethane (DDTs), polychlorinated dibenzo-p-dioxins (PCDDs) and dibenzofurans (PCDFs), polybrominated diphenyl ethers (PBDEs), and organotins (Ueno et al., 2003, 2004a,b, 2005, 2006). Skipjack tuna are an important commercial species, and its ecology and biology are well studied. Since they are also a dominant product in the world's tuna market, measurement of PFCs in skipjack tuna would also help in the assessment of potential exposures to humans. Additionally, monitoring of PFCs in oceans is required so that we can understand the sources and transport of these contaminants. The objectives of this study were to determine the concentrations, spatial distribution, and profiles of PFCs in skipjack tuna collected from offshore and open oceans along the Pacific Rim, and to examine the suitability of skipjack tuna as a bioindicator of PFCs in global pollution monitoring. The data presented in this study will provide baseline information for future monitoring studies, contributing to an understanding of global trends of PFCs.
2.
Materials and methods
2.1.
Standards and reagents
PFOA and potassium salt of PFOS were purchased from Tokyo Chemical Industries (Portland, OR). Perfluorononanoate (PFNA), perfluorodecanoate (PFDA), and perfluoroheptanoate (PFHpA) were from Fluorochem Ltd (Glossop, Derbyshire, UK). Perfluoroundecanoate (PFUnDA) and perfluorododecanoate (PFDoDA) were from Aldrich (St. Louis, MO). Perfluorooctanesulfonamide (PFOSA), potassium salts of perfluorobutanesulfonate (PFBS) and perfluorohexanesulfonate (PFHxS), 13C2-PFNA, and 13C2-PFDA were provided by the 3 M Company (St. Paul, MN). 13 C4-PFOS and 13C4-PFOA were purchased from Wellington Laboratories (Guelph, ON, Canada). Purities of all standards were ≥95%. All solvents were HPLC grade and reagents were ACS grade (J.T.Baker, Phillipsburg, NJ).
2.2.
Sample collection
During 1997-1999, skipjack tuna were collected from oceanic waters off Japan, the Sea of Japan, the East China Sea (off Taiwan), off Indonesia, the Indian Ocean, and the (mid) North Pacific Ocean (Fig. 1). Skipjack tuna were obtained from fish markets and fishing villages after confirmation of the origin of the catch, while the tuna collected from the (mid) North Pacific Ocean and the Indian Ocean were caught during a research cruise. The latitude and longitude of sampling locations of tuna are given in Table 1. Liver and muscle tissues were dissected out and kept in polyethylene bags, stored at −20 °C until analysis. Tuna livers archived at environmental specimen bank (ES-Bank) of Center for Marine Environmental Studies, Ehime University, Japan, were used.
2.3.
Chemical analysis
Concentrations of PFCs in livers of skipjack tuna were determined according to the procedure described previously (Kannan et al., 2001). The liver sample (0.7–0.9 g) was homogenized with 5 mL of Milli-Q water, and then 1 mL of the homogenate was transferred into a polypropylene tube (PP tube) and 100 μl of 2.5 ng/mL internal standard mixture (13C4-PFOS, 13C4-PFOA, 13C2-PFDA, and 13C2-PFNA), 2 mL of 0.25 M sodium carbonate buffer, 1 mL of 0.5 M tetrabutylammonium hydrogensulfate solution (adjusted to pH 10) were added and mixed thoroughly. Extraction was carried out by addition of 5 mL of methyl-tert-butyl ether (MTBE), with vigorous shaking for 40 min. The sample was then centrifuged at 4000 rpm for 5 min to separate the organic layer from the aqueous layer. The aqueous layer was transferred into another PP tube, and the extraction was repeated with 3 mL of MTBE. After extraction, the two organic layers were combined and evaporated to near-dryness under a stream of nitrogen. The sample was then reconstituted with 1 mL of methanol, vortexed for 30 s, centrifuged at 4000 rpm for 2 min, and transferred into a 2-mL autosampler vial. The target analytes were detected and quantified on an Agilent 1100 Series high performance liquid chromatograph (HPLC), coupled with an Applied Biosystems API 2000
S CIE N CE OF T H E TOT AL E N V I RO N ME N T 4 0 3 ( 2 00 8 ) 2 1 5–2 21
217
Fig. 1 – Map showing the sampling locations for skipjack tuna, with an enlarged map of Japan. electrospray triple-quadrupole mass spectrometer (ESI-MS/ MS). Ten microliters of the extract were injected into a Betasil C18 (100 mm × 2.1 mm) column with a (20 mm × 2.1 mm) guard column, both with a 5-μm particle size (Thermo Electron Corporation, Waltham, MA). The mobile phase consisted of a gradient elution of 2 mM ammonium acetate and methanol. The gradient started at 10% methanol and increased to 100% after 10 min; it was held at 100% for 2 min, then reversed back down to 10% methanol. The MS/MS was operated in a multiple reaction monitoring (MRM) mode and the mass transitions monitored were: 399 N 80 for PFHxS, 499 N 99 for PFOS, 503 N 99 for 13C4-PFOS, 498 N 78 for PFOSA, 363 N 319 for PFHpA, 413 N 369 for PFOA, 417 N 372 for 13C4-PFOA, 463 N 419 for PFNA, 465 N 420 for 13C2-PFNA, 513 N 469 for PFDA, 515 N 470 for 13C2-PFDA, 563 N 519 for PFUnDA, and 613 N N569 for PFDoDA. The sum of the concentrations of the nine PFCs measured in this study is denoted as total PFCs (ΣPFC).
were prepared in methanol at concentrations ranging from 0.1 to 50 ng/mL. Calibration standards were injected every day before and after a batch of samples was analyzed. A midpoint calibration standard was injected after every 10 samples, throughout the instrumental analysis, to check for instrument response and drift. Procedural blanks were analyzed by passage of water and reagents through the entire analytical procedure, to monitor for contamination in reagents and glassware. Concentrations were not corrected for the recoveries of internal standards, because recoveries were within an acceptable level of 70% for all compounds. Quantitation of PFCs was performed using a quadratic regression fit analysis weighted by 1/x of the matrix extracted calibration curve. The limit of quantitation (LOQ) was considered to be the lowest acceptable standard within ±30% of the theoretical value, and has a peak area twice as large as that of the blanks. The LOQ of PFCs ranged from 0.9 to 1.8 ng/g, wet wt, while that for PFHpA and PFOA was 2.5 and 3.2 ng/g, wet wt, respectively.
2.4.
2.5.
Quality assurance and quality control
A known concentration (10 ng each) of target compounds was spiked into an aliquot of the sample matrix (i.e., matrix spikes) and then run through the analytical procedure as a check for matrix effects, through calculation of the recoveries. Overall, mean matrix spike recoveries ranged from 65 to 98% (n=12). Mean recoveries of PFNA and PFUnDA were 65±10%, whereas the mean recoveries of the other seven compounds were 76±14%. 13Clabelled internal standards (13C4-PFOS, 13C4-PFOA, 13C2-PFDA, and 13 C2-PFNA) were spiked into all of the samples for the calculation of recoveries. Mean internal standard recoveries in samples for 13C2-PFNA was 64 ±9%, whereas the recoveries of other internal standards were 74±14%. External calibration standards
Statistical analysis
Statistical analyses were performed using Statgraphics plus 5.1 (Manugistics Inc., Rockville, MD). Concentrations that were below the LOQ were assigned a value of half the LOQ, for statistical analyses.
3.
Results and discussion
3.1.
PFC concentrations
Concentrations of total PFCs in skipjack tuna livers ranged from b1 to 82.9, ng/g wet wt (Table 1). PFOS and PFUnDA
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Table 1 – Mean (range), and total PFC concentrations (ng/g, wet wt.) in the livers of skipjack tuna collected from open ocean and offshore waters of the Pacific Rim* Sampling Location Geographical coordinates Off-shore sites Izu, Japan N33,50-34/E140,50 Miyagi-1, Japan N38,E142 Miyagi-2, Japan N38,E144 Chiba, Japan N34,E140 Kochi-1, Japan N33,E134 Kochi-2, Japan N33,E134 Kagoshima, Japan N30,E130 Sea of Japan N37,E135 Tsushima, Japan N33,E129 East China Sea (Taiwan) N25/E125 Jakarta, Indonesia
Open-Ocean sites W. North Pacific Ocean N44,29/E175,31 Mauritius, Indian Ocean % detectable samples
Collection Date
n
Jun-97
5
Oct-97
4
Jul-99
5
Oct-97
4
Oct-97
5
Nov-98
9
Oct-97
5
Oct-97
5
Oct-97
5
Nov-98
2
Jan-99
5
Aug-98
3
Jan-99
3
PFOS
PFOSA
PFNA
PFDA
PFUnDA
PFDoDA
ΣPFCs⁎⁎⁎
3.30 (2.2–4.8) 4.51 (2.5–5.8) 8.49 (6.3–11.1) 51.2 (34.4–58.9) 9.08 (1.5–21.1) 19.8 (2.4–45.6) 5.91 (2.4–10.6) 10.9 (7.6–13.9) 17.5 (9.6–34.5) 6.12 (5.1–7.1) 4.09 [3.38] (b 1–7.5)
b 1 [0.51]⁎⁎ (b 1) b1 [0.65] (b 1) 4.29 (2.9–5.9) 2.96 (1.9–3.7) 2.5 [1.73] (b1–5.0) 1.92 [1.45] (b1–2.4) b1 [0.62] (b1–1.1) 1.27 [1.12] (b1–1.5) 1.84 (1.3–2.8) b1 [0.77] (b1–1.0) b1 [0.51] (b 1)
b1.1[0.55] (b1.1) b 1.1 [0.55] (b1.1) b1.1 [0.55] (b1.1) 1.88 [1.21] (b 1.1–2.38) b 1.1 [0.55] (b1.1) 1.14 [0.62] (b 1.1–1.14) b 1.1 [0.55] (b1.1) b 1.1 [0.55] (b1.1) 2.48 [0.94] (b 1.1–2.48) b 1.1 [0.55] (b1.1) b 1.1 [0.55] (b1.1)
b0.9 [0.46] (b 0.9) b0.9 [0.46] (b 0.9) b0.9 [0.46] (b 0.9) 1.84 (1.1–3.3) 1.3 [0.90] (b0.9–1.7) 2.04 [1.34] (b0.9–2.7) b0.9 [0.46] (b 0.9) 0.93 [0.55] (b0.9–0.93) 1.47 [0.86] (b0.9–1.9) b0.9 [0.46] (b 0.9) b0.9 [0.46] (b 0.9)
6.40 (3.0–9.8) 8.35 (3.5–12.5) 7.60 (5.5–9.1) 17.9 (13.4–21) 13.63 (3.5–28.7) 19.8 (8.7–31.6) 10.1 (6.0–13.2) 7.59 (2.5–11.3) 3.55 (2.4–5.3) 12.5 (11.1–14.0) 2.41 (1.3–4.3)
2.87 [2.09] (b 1.8–3.35) 2.90 [2.41] (b 1.8–4.2) 2.0 [1.12] (b 1.8–1.97) 5.29 (4.4–6.5) 4.02 [3.40] (b 1.8–7.2) 4.50 (2.1–7.3) 2.82 (1.9–4.0) 3.35 (2.6–4.4) 3.55 (2.7–4.7) 2.57 (2.1–3.0) b1.8 [0.91] (b 1.8)
13.2
2.13 [1.07] (b 1–2.1) b 1 [0.54] (b1) 100
b1 [0.51] (b 1) b1
b1.1 b1.1
b0.9 [0.46] (b 0.9) b 1.1
2.71 (1.9–4.3) b 1.8
83
57
93
4.25 (1.3–7.9) b1 [0.50] (b1) 100
16.7 22.4 82.9 29.0 47.5 20.0 23.7 23.0 28.6 9.00
7.30 [1.04]
95
⁎PFHpA, PFOA, and PFHxS were not detected in more than 10% of the samples analyzed. ⁎⁎There are two mean values for certain compounds. Values in brackets [] represent mean concentrations for all values while assigning a value half of the LOQ, for those samples that had values below LOQ. Values in front of [] refers to the mean of detectable concentrations (NLOQ) only. ⁎⁎⁎ΣPFCs refer to average of the sum of all nine detectable perfluorochemical concentrations, while assigning a value of half the LOQ to those samples detected below the LOQ.
were the predominant compounds found, with concentrations ranging from b1 to 58.9 and b1 to 31.6 ng/g, wet wt, respectively. PFOSA, PFNA, PFDA, and PFDoDA were detected in 83, 93, 57 and 95% of the tuna liver samples, respectively. PFHxS, PFHpA, and PFOA were each detected in less than 10% of the samples analyzed. The highest concentration of PFOS (58.9 ng/g, wet wt) was found in tuna from Chiba, Japan. High concentrations of PFUnDA were found at offshore sites around Japan, particularly near Chiba and Kochi (mean: 17.9 and 19.8 ng/g, wet wt); PFOS concentrations were also elevated at these sites (mean: 51.2 and 19.8 ng/g, wet wt). Mean concentrations of PFUnDA in tuna from the East China Sea (off Taiwan) and in samples from Izu and Kagoshima, Japan, were 2-fold greater than the mean concentrations of PFOS at these sites. The mean concentrations of PFUnDA were higher than the concentrations of PFOS in tuna livers from five of 11 offshore locations, and the open-ocean site in the (mid) North Pacific Ocean. PFOS was found in tuna livers from the Indian Ocean at concentrations below the LOQ (~0.5 ng/g, wet wt). Total PFC concentrations in skipjack tuna from the Indian Ocean were at least 10-times lower than those in samples
from the (mid) North Pacific Ocean (Table 1). The low concentrations of PFCs in skipjack tuna from the Indian Ocean are similar to that reported for seawater collected from the Indian Ocean, in which PFC concentrations were at trace to undetectable levels (Wei et al., 2007; Yamashita et al., 2008). The spatial differences in PFOS concentrations in tuna livers were similar to those reported for albatross livers from the North Pacific Ocean and the Indian Ocean. Mean PFOS concentrations in albatross livers from the North Pacific Ocean and the Indian Ocean were 5.1 and 3.2 ng/g, wet wt, respectively (Tao et al., 2006) and the corresponding concentrations in tuna livers were 1.1 and ~0.5 ng/g, wet wt. Tuna samples collected from the western North Pacific Ocean, along the Pacific Rim, contained 10-fold higher concentrations of PFCs than did tuna from the middle of North Pacific Ocean. The east-west gradient in PFC concentrations in the Pacific Ocean waters has been reported earlier (i.e., greater concentrations of PFCs in waters of the western North Pacific than in the middle or Eastern North Pacific; Yamashita et al., 2008). The occurrence of long-chain perfluorocarboxylates (PFDA, PFUnDA, and PFDoDA) has been reported in water samples
S CIE N CE OF T H E TOT AL E N V I RO N ME N T 4 0 3 ( 2 00 8 ) 2 1 5–2 21
219
Table 2 – Spearman's correlation among major perfluoro chemicals found in livers of skipjack tuna (n = 60) from offshore and open ocean waters
PFOS PFOSA PFDA PFUnDA PFDoDA
PFOSA
PFDA
PFUnDA
PFDoDA
PFNA
0.81⁎⁎
0.78⁎⁎ 0.61⁎⁎
0.63⁎⁎ 0.52⁎⁎ 0.65⁎⁎
0.74⁎⁎ 0.51⁎⁎ 0.79⁎⁎ 0.70⁎⁎
0.58⁎⁎ 0.53⁎⁎ 0.57⁎⁎ 0.44⁎⁎ 0.42⁎⁎
⁎⁎Correlation is significant at the 0.01 level (2-tailed t test).
collected from coastal and offshore waters of the western North Pacific Ocean, along the Pacific Rim (Wei et al., 2007). However, long-chain PFCs were not found in waters of the open (mid) North Pacific Ocean (Wei et al., 2007). Long-chain perfluorocarboxylates were found in tuna livers from the middle of the North Pacific Ocean as well as in offshore waters along Japan, in the East China Sea (off Taiwan), and off Indonesia. Although PFOA was the most abundant PFC in seawater samples from the Pacific Ocean (Yamashita et al., 2005), this compound was rarely detected in our tuna livers. Low concentrations of PFOA in tuna livers can be attributed to the low bioaccumulation potential of PFOA (Conder et al., 2008). Conversely, long-chain perfluorocarboxylates, such as PFUnDA, were rarely found in open ocean water samples (Wei et al., 2007); however because of the relatively high bioaccumulation potential they were found in tuna livers (Conder et al., 2008). High concentrations of PFUnDA in tuna samples analyzed in this study, particularly in the samples collected from the East China Sea (off Taiwan) and in samples collected off Japan, suggest the existence of distinctive sources of PFCs that are enriched in long-chain perfluorocarboxylates. PFUnDA was not found in seawater collected from offshore waters of the East China Sea, although PFDA and PFDoDA were found in seawater samples from this region (Wei et al., 2007). High concentrations of PFUnDA in our tuna livers suggest the exposure of fish to fluorotelomerbased compounds produced or used in industrialized regions of East Asia; several fluorotelomer-based industries are located in Japan and China (Prevedouros et al., 2006). Production of 8:2 fluorotelomer alcohols (FTOHs) or fluorotelomer olefins (FTOs) primarily in Japan has been reported (Prevedouros et al., 2006); however occurrence of PFUnDA in tuna livers is indicative of degradation of 10:2 FTOH or 10:2 FTO. FTOHs are mainly manufactured in even chain lengths, but have been reported to yield odd- and even-chain length perfluorocarboxylates upon degradation. For example, 10:2 FTOH (CF3(CF2)9CH2CH2OH) can degrade to PFDA and PFUnDA in sewage sludge and in the environment (Wang et al., 2005; Sinclair and Kannan, 2006; Wallington et al., 2006). These results suggest that PFUnDA and other long-chain perfluorocarboxylates in livers from tuna collected in offshore waters along the Pacific Rim originate from the degradation of 10:2 FTOH. A significant correlation existed between the liver concentrations of PFUnDA and PFDA/PFDoDA (Table 2). Concentrations of PFOS in the livers of skipjack tuna from Chiba, Japan (34–59 ng/g, wet wt) were similar to the concentrations reported for livers of bluefin tuna from the Italian coast of the Mediterranean Sea (21–87 ng/g, wet wt) (Kannan et al., 2002a) and in the blood of cod (6.1–52 ng/g, wet wt) from the
Fig. 2 – Relationship between PFOS concentrations in liver and body weight of skipjack tuna. southern Baltic Sea (Falandysz et al., 2006). Concentrations of PFOS in tuna livers from the offshore and oceanic waters were 10to 100-fold lower than the concentrations reported for fish from inland waters of New York State, USA (Sinclair et al., 2006) and in fish from Tokyo Bay, Japan (Taniyasu et al., 2003). Concentrations of PFOS in skipjack tuna livers were not correlated with body weight (p≥0.1) (Fig. 2). Similarly, no significant difference existed in the concentrations of PFOS between the genders (p≥0.05) (Fig. 3). An earlier study showed that liver concentrations of PFOS in female smallmouth bass were lower than in males (Sinclair et al., 2006).
3.1.1.
Geographic distribution and PFC profiles
The mean concentration of PFOS in tuna livers from offshore sites (off Japan, off Taiwan, and off Indonesia) was approximately 10 to 20-fold higher than the mean concentration found for tuna livers from open ocean waters (i.e., the mid Pacific Ocean and the Indian Ocean). The highest concentrations of several of the PFCs were found in locations near industrialized areas such as Chiba, which is a major commercial and industrial center surrounding Tokyo Bay. Livers of birds collected from Chiba, Japan, during 1997–1999 showed high PFOS concentrations (19 to 650 ng/g, wet wt) (Kannan et al., 2002b). Between the two open-ocean locations, higher concentrations of PFOS and PFUnDA were found in tuna from the (mid) North Pacific Ocean than in tuna from the Indian Ocean. PFOSA, PFDA, and PFDoDA were found in tuna livers from the (mid) North Pacific Ocean (Table 1), but not in tuna from the Indian Ocean. The large spatial variation in PFC concentrations between the open-oceans and the offshore sites suggests the influence of local sources from nearby coastal areas.
Fig. 3 – Concentrations of PFOS in male and female tuna livers from various sampling locations (value above each bar indicates the mean concentration).
220
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Fig. 4 – Profiles of perfluorochemical composition in skipjack tuna livers from offshore sites and from open water sites in the mid-North Pacific and Indian Oceans. Concentrations of PFCs in waters of the eastern North Pacific Ocean were lower than the concentrations in western North Pacific Ocean waters (Yamashita et al., 2008). Further, concentrations of PFCs in waters of the Atlantic Ocean were higher than the concentrations in the Pacific Ocean waters (Yamashita et al., 2005). In the present study, tuna samples were not available from the Atlantic Ocean or the eastern North Pacific Ocean. Further investigation into concentrations of PFCs in tuna from the Atlantic Ocean would help in understanding the sources and pathways of PFCs to the oceans. The profiles of PFC concentrations in livers from tuna collected off Japan were different from the profiles found for the open-ocean tuna samples (Fig. 4). PFOS was the predominant compound in tuna samples from offshore sites in Miyagi (the samples from 1999), Chiba, Kochi (the samples from 1998), Tsushima, the Sea of Japan, the Indian Ocean, and Indonesia, contributing from 38% to 61% of the ΣPFC concentrations. PFUnDA was the predominant compound in tuna livers from Izu, Miyagi (the samples from 1997), Kochi (the samples from 1997), Kagoshima, the East China Sea, and the (mid) North Pacific Ocean, accounting for 47 to 54% of the ΣPFC concentrations. Although PFUnDA was the predominant compound in tuna collected in 1997 from Miyagi and Kochi, PFOS was predominant in samples collected from these locations in 1998 and 1999. These results may indicate temporal/seasonal differences in sources and/or the movement of tuna along the offshore/coastal waters of Japan. Tuna collected from the pelagic waters of the (mid) North Pacific Ocean contained notable proportions of PFUnDA and PFDoDA (47% and 30%, respectively) within the ΣPFC concentrations. Elevated concentrations of PFUnDA and PFDoDA in tuna from the (mid) North Pacific Ocean when compared to the Indian Ocean samples indicate sources enriched with long-chain perfluoroalkylcarboxylates arising from countries of East Asia. The correlations among the six major PFCs found in tuna livers from the offshore and open ocean locations are presented in Table 2. Concentrations of PFOS in tuna livers were significantly correlated (p ≤ 0.01) with the concentrations of PFOSA, PFDA, PFUnDA, PFDoDA, and PFNA. Concentrations of long-chain perfluorocarboxylates were significantly posi-
tively inter-correlated (Table 2). Concentrations of long-chain carboxylates (i.e., C10 to C12) were greater than the concentrations of PFOA (C8) and PFNA (C9). Furthermore, the concentration of the odd-carbon chain perfluorocarboxylate (i.e., C11; PFUnDA) exceeded the concentrations of the neighboring even-carbon chain compounds (C10 and/or C12). Another remarkable characteristic of the PFC profile in tuna livers was the lower PFNA/PFUnDA ratio, as compared with fish collected from the Arctic waters and European coastal waters (Houde et al., 2006; Falandysz et al., 2006). PFNA/ PFUnDA ratios in fish livers from the Canadian Arctic and the Baltic Sea were in the range of 0.65–0.75 (Houde et al., 2006; Falandysz et al., 2006), whereas the ratios in tuna livers from the offshore waters of Asia, in our study, were 0.04–0.06. The low proportions of PFNA and high proportions of PFUnDA in skipjack tuna livers indicate distinctive sources of PFCs arising from East Asian countries. PFOS concentrations in surface seawater of the western North Pacific Ocean were 10 to 15 times higher than the concentrations determined for the South Pacific and the Indian Oceans (Yamashita et al., 2005, 2008). PFOS concentrations in coastal waters of Tokyo Bay were approximately two to three orders of magnitude greater than the concentrations found at offshore locations around Japan. The pattern of elevated concentrations of PFOS in coastal waters near Tokyo Bay was similar to the pattern of concentrations of PFOS found in tuna livers collected in waters off Japan (Taniyasu et al, 2003; Yamashita et al., 2005, 2008). Similarly, elevated concentrations of PFOS in tuna livers from the East China Sea reflect the high concentrations found in water samples from this sea (So et al., 2004). The overall trend of PFOS contamination in seawater is comparable to the trend found in livers of skipjack tuna (Table 3). This suggests the utility of skipjack tuna as a bioindicator for monitoring PFOS in oceans. Nevertheless, it should be noted that PFOA was the predominant PFC in seawater from almost all global oceans. However, PFOA was not detected in livers of tuna, because of its low bioaccumulation potential, as mentioned earlier (Conder et al., 2008). In summary, our results demonstrate spatial differences in concentrations of PFCs in livers from tuna sampled in offshore waters and open oceans along the Pacific Rim. Concentration profiles and correlations among the PFCs indicate the presence of distinct sources arising from East Asia. This study demonstrates the suitability of skipjack tuna as a bioindicator to monitor contamination by bioaccumulative PFCs such as PFOS in world’s oceans. Earlier studies have reported greater concentrations of PFCs in waters of the Table 3 – Range of PFOS concentrations in seawater (pg/L) and skipjack tuna livers (ng/g wet wt.) from waters off Japan and from open ocean sites Location
Seawater (pg/L)⁎
Tuna liver (ng/g)
Tokyo Bay/Chiba Offshore waters of Japan Japan Sea South/East China Sea Central to Eastern Pacific Ocean Indian Ocean
338–57700 40–75 2–15 8–113 1.1–20 5–11
34.4–58.9 1.5–45.6 8–14 5–7 1.1–2.1 b 1.1
⁎Yamashita et al. (2005, 2008).
S CIE N CE OF T H E TOT AL E N V I RO N ME N T 4 0 3 ( 2 00 8 ) 2 1 5–2 21
Atlantic than in waters of the Pacific. Tuna samples were not available from the Atlantic Ocean for this study, and future research should assess the levels and profiles of PFCs in tuna from the oceans of the Western Hemisphere.
Acknowledgements Financial support for the sampling part of the study was provided by Grants-in-Aid for Scientific Research (S) (No. 20221003) from the Japan Society for the Promotion of Science (JSPS) and the Waste Management Research Grants (K1821 and K1836) from the Ministry of Environment, Japan. This study was supported by the “Global COE Program” of the Japanese Ministry of Education, Culture, Sports, Science and Technology (MEXT), Japan.
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