Environmental Pollution 136 (2005) 303e313

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Global pollution monitoring of polychlorinated dibenzo-p-dioxins(PCDDs), furans (PCDFs) and coplanar polychlorinated

biphenyls (coplanar PCBs) using skipjacktuna as bioindicator

Daisuke Uenoa, Mafumi Watanabea, Annamalai Subramaniana, Hiroyuki Tanakab,Gilberto Fillmannc, Paul K.S. Lamd, Gene J. Zhengd, Muswerry Muchtare,

Hamidah Razake, Maricar Prudentef, Kyu-Hyuck Chungg, Shinsuke Tanabea,*

aCenter for Marine Environmental Studies (CMES), Ehime University, Bunkyo-cho 2-5, Matsuyama 790-8577, JapanbNational Research Institute of Fisheries and Environment of Inland Sea, Japan

cFundacao Universidade Federal do Rio Grande, BrazildDepartment of Biology and Chemistry, City University of Hong Kong, Hong Kong

eResearch and Development Center for Oceanology, Indonesian Institute of Sciences, IndonesiafScience Education Department, De La Salle University, Philippines

gCollege of Pharmacy, Sungkyunkwan University, Korea, South Korea

Received 6 August 2004; accepted 28 December 2004

Global pollution monitoring of PCDD/Fs and coplanar PCBs in offshore water and open sea were conducted usingskipjack tuna as bioindicator.

Abstract

In order to elucidate the global distribution of dioxins and related compounds, such as PCDDs, PCDFs and coplanar PCBs,

levels of these compounds were determined in the muscle of skipjack tuna (Katsuwonus pelamis) collected from the offshore watersand open seas near Japan, Taiwan, Philippines, Indonesia, Seychelles and Brazil, and the Japan Sea, the East China Sea, the SouthChina Sea, the Indian Ocean and the North Pacific Ocean. PCDDs, PCDFs and coplanar PCBs were detected in almost all the

specimens collected from all the locations surveyed, indicating widespread contamination by these compounds in the marineenvironment. Higher concentrations of dioxins and coplanar PCBs were detected in the samples from temperate Asian regions,plausibly due to larger usage and anthropogenic generation in highly industrialized countries around the East China Sea and theSouth China Sea, such as Japan, Korea, Taiwan, Hong Kong and coastal China.

� 2005 Elsevier Ltd. All rights reserved.

Keywords: Organochlorine; POPs; TEQs; Fish; Offshore water and open sea

1. Introduction

Worldwide contamination by dioxins and relatedcompounds, such as polychlorinated dibenzo-p-dioxins(PCDDs), polychlorinated dibenzofurans (PCDFs) and

* Corresponding author. Tel./fax: C81 89 927 8171.

E-mail address: shinsuke@agr.ehime-u.ac.jp (S. Tanabe).

0269-7491/$ - see front matter � 2005 Elsevier Ltd. All rights reserved.

doi:10.1016/j.envpol.2004.12.036

coplanar polychlorinated biphenyls (coplanar PCBs) hasbeen of great concern due to their persistency in theenvironment, highly bioaccumulative nature and ad-verse effects on wildlife and humans (van den Berg et al.,1998). Contamination of these persistent organic pollu-tants (POPs) is widespread in the environment asevidenced by their detection in a wide range of environ-mental media, such as air (Lohmann et al., 2001), soil

304 D. Ueno et al. / Environmental Pollution 136 (2005) 303e313

(e.g. Wagrowski and Hites, 2000; Minh et al., 2003), andbiota (e.g. Corsolini et al., 2002; Jarvinen and Ankley,1999). Moreover, several studies on air samples andmarine organisms from open seas implied a long rangetransport of these compounds through the atmosphere(Ono et al., 1987; Kannan et al., 1989; Hashimoto et al.,1995; Lohmann et al., 2001; Tanabe et al., 2004).Although several investigators have monitored contam-ination status of dioxins and coplanar PCBs in open seasand remote areas, information on the global distributionof these compounds which can provide significant andnecessary insight into their transport behavior and fateis still limited.

In order to elucidate the global distribution of dioxinsand coplanar PCBs in offshore waters and open seas, thepresent study used skipjack tuna (Katsuwonus pelamis)as a bioindicator. Skipjack tuna is primarily distributedfrom offshore waters to open seas in tropical andtemperate regions almost all over the world such as thePacific, Atlantic and Indian Oceans (Collette andNauen, 1983). This species is an important commercialfish and its ecology and biology have been well studied(Collette and Nauen, 1983; Japanese Society of FisheriesScience, 1975; Nihira, 1996). Moreover, the suitability ofskipjack tuna for global monitoring of organic pollu-tants (PCBs, DDTs, PBDEs, organotins, etc.) has beenestablished in our previous studies (Ueno et al., 2003,2004a,b). These studies indicated that migration pattern,growth stage and sex had no or little influence on thevariations of POPs residue levels in their bodies due torapid equilibrium partitioning between seawater andbody lipid. Hence this species reflected POPs pollutionlevels in seawater when and where they were collected.On this basis, skipjack tuna is considered as a suitablebioindicator for monitoring contamination status ofdioxins and coplanar PCBs on a global scale.

The objectives of this study were to elucidate theglobal distribution of PCDDs, PCDFs and coplanarPCBs in offshore waters and open seas and to un-derstand the transport of these chemicals using skipjacktuna as a bioindicator. In addition, toxic equivalents ofdioxins and PCBs (TEQs) in this species were estimatedto evaluate the toxic potential of these compounds inoffshore waters and open seas.

2. Materials and methods

2.1. Sample collection

Skipjack tuna (Katsuwonus pelamis) were collectedfrom various regions in the world (offshore waters ofJapan, Taiwan, Philippines, Indonesia, Seychelles andBrazil, and the Japan Sea, the East China Sea, the SouthChina Sea, the Indian Ocean and the North PacificOcean) between 1997 and 2001 (Fig. 1). Skipjack tuna

were obtained from fish market and fishermen villagesafter confirming the fishing areas. The samples from theNorth Pacific Ocean and off-Brazil were caught duringa research cruise. Muscle tissues were dissected fromthese individuals and kept in clean plastic bags andstored at �20 �C until chemical analysis. The pooledmuscles of five fish from each location were employedfor chemical analysis. Details of the samples are shownin Table 1.

2.2. Chemical analysis

Chemical analysis of PCDDs, PCDFs (PCDD/Fs)and coplanar PCBs followed the method described ina previous report (Tanabe et al., 2004) with slightmodification. Briefly, about 20 g of muscle samples werehomogenized with anhydrous Na2SO4 and extractedusing a Soxhlet apparatus with dichloromethane (DCM)for 9 h. The extract was concentrated up to 20 ml usinga rotary evaporator, and a 2 ml aliquot of the extractwas used for lipid content determination by gravimetricmethod. 13C12-labeled PCDD/Fs and coplanar PCBs(2,3,7,8-T4CDD/F, 1,2,3,7,8-P5CDD/F, 1,2,3,6,7,8-H6CDD/F, 1,2,3,7,8,9-H6CDF, 1,2,3,4,6,7,8-H7CDD/F, O8CDD/F, CB77, CB81, CB118, CB126, CB156,CB167, CB169 and CB189) were spiked into theconcentrated extract as internal standards. Lipid andbiogenic materials in this solution were removed by gelpermeation chromatography (GPC) using a Bio-BeadS-X3 packed glass column (50!2 cm i.d., Bio-RadLaboratories, USA). A mixture of 50% hexane in DCMwas used as mobile phase at a flow rate of 5 ml/min. Thefirst 120 ml of eluted solvent was discarded, and the 100ml of the second fraction, which contained PCDD/Fsand coplanar PCBs, was collected. The organochlorinefraction after GPC was concentrated and passedthrough a 3 g activated silicagel packed in a glasscolumn (1 cm i.d., Wako-gel S-1, Wako Pure ChemicalIndustries Ltd., Japan) for clean up with 220 ml ofhexane. Eluted hexane was concentrated and spiked intoa 10 g activated alumina packed glass column (1 cm i.d.,Alumina oxide 90, Brockman activity I, 70-230 mesh,Merck, Germany). The first fraction eluted with hexanecontained PCB isomers including most of the mono-ortho coplanar congeners, and the second fraction elutedwith 50% of DCM in hexane contained the remainingmono-ortho coplanar PCBs, non-ortho coplanar PCBsand PCDD/Fs. The second fraction eluted from theactivated alumina column was then passed through a 1 gactivated carbon dispersed silica gel packed glasscolumn (1 cm i.d., Kanto Chemical Co. Inc, Japan).The first fraction from carbon-dispersed silica gelcolumn eluted with 25% of DCM in hexane for mono-ortho coplanar PCBs was combined with the firstfraction from the alumina column. The second fraction

305D. Ueno et al. / Environmental Pollution 136 (2005) 303e313

off-Philippines

N-Pacific-3

N-Pacific-2

N-Pacific-1

off-Indonesia

S-China Sea

Bay of Bengal

off-Seychelles

off Taiwan

Japan Sea

E-China Sea-1

E-China Sea-2

off-Japan-2

off-Japan-1

off-Brazil

Fig. 1. Map showing sampling locations of skipjack tuna.

from carbon-dispersed silica gel column eluted with 220ml of toluene contained non-ortho coplanar PCBs andPCDD/Fs. Both fractions were concentrated to neardryness. The 13C12-labeled CB105, CB157 and CB180

Table 1

Biometric data of skipjack tuna collected from Asian offshore waters,

off-Seychelles, off-Brazil and open seas

Location Month/year n BL (cm) BW (kg)

N-Pacific-1 08/1998 5 44 (43e45) 1.8 (1.7e2.0)N-Pacific-2 05/1997 5 47 (43e54) 2.2 (1.7e3.5)

N-Pacific-3 03/1998 5 79 (75e80) 11 (9.0e12)

off-Japan-1 10/1997 5 49 (49e50) 2.6 (2.6e2.7)off-Japan-2 10/1997 5 52 (49e55) 3.3 (3.1e3.7)

Japan Sea 10/1997 5 63 (62e65) 5.6 (5.5e5.8)

E-China Sea-1 10/1997 5 58 (55e60) 3.9 (3.4e4.5)

E-China Sea-2 10/1997 5 61 (60e63) 5.2 (4.9e5.4)off-Taiwan 11/1998 5 61 (59e63) 4.9 (4.9e5.0)

S-China Sea 06/2001 1 31 0.5

off-Philippines 12/1997 5 42 (41e45) 1.5 (1.3e1.6)

Bay of Bengal 10/1998 5 47 (46e47) 2.0 (2.0e2.0)off-Indonesia 01/1999 2 47 (46e48) 2.0 (2.0e2.0)

off-Seychelles 01/1999 3 55 (54e55) 3.6 (3.4e3.8)

off-Brazil 09/2000 4 55 (53e57) 3.7 (3.1e4.4)

Figures in parentheses indicate the range. n, number of samples. BL,

body length (fork length); BW, body weight; N-Pacific, the North

Pacific Ocean; E-China Sea, the East China Sea; S-China Sea, the

South China Sea.

prepared in decane were then added to the combinedfirst fraction, and 13C12-labeled 1,2,3,4-T4CDD and1,2,3,7,8,9-H6CDD with decane were added to thesecond fraction as a recovery spike. Recovery of 13C12

labeled compounds ranged between 60 and 120%.The identification and quantification of mono-ortho

coplanar PCBs were performed using a gas chromato-graph (GC) (Agilent 6890 series, USA) with a highresolution mass selective detector (MSD) (JEOL GC-Mate II, JEOL, Japan) at a resolving power of morethan 2000. The GC column used was a DB-1 fused silicacapillary (60 m length, 0.25 mm i.d., 0.25 mm filmthickness, J&W Scientific Inc., USA) with deactivatedfused silica guard columns on both ends. The identifi-cation and quantification of non-ortho coplanar PCBsand PCDD/Fs were performed using a GC (Agilent 6890series) with a high resolution mass selective detector(JEOL JMS-700D, JEOL, Japan) at a resolving power ofmore than 10,000. Separation was accomplished by DB-5ms fused silica capillary column (60 m length, 0.25 mmi.d., 0.25 mm film thickness, J&W Scientific Inc., USA)for non-ortho coplanar PCBs and H7-O8CDD/Fs, andby a capillary column coated with CP-Sil 88 for dioxins(60 m length, 0.25 mm i.d., 0.1 mm film thickness, VarianInc., USA) for T4-H6CDD/Fs with deactivated fused

306 D. Ueno et al. / Environmental Pollution 136 (2005) 303e313

silica guard columns on both ends. MSD was operatedat an electron impact and monitored by selective ionmonitoring mode (EI-SIM). All the congeners werequantified using the isotope dilution method to thecorresponding 13C12-congeners. The detection limit forindividual congeners was 0.2e4 pg/g lipid wt for PCDD/Fs and non-ortho coplanar PCBs, and 15 pg/g lipid wtfor mono-ortho coplanar PCBs.

3. Results and discussion

3.1. Contamination status

Concentrations of PCDD/Fs and coplanar PCBs inthe muscle of skipjack tuna are shown in Table 2. Thesecompounds were detected in almost all the specimenscollected from all the sampling locations indicatinga widespread contamination of these compounds in theglobal marine environment. Concentrations of totalPCDD/Fs and total coplanar PCBs ranged from belowdetection limit to 79, and 4200 to 62000 pg/g lipid wt,respectively (Table 2). Total concentrations of coplanarPCBs were three orders of magnitude higher than thoseof total PCDD/Fs. This may be due to the higherbioaccumulative properties of PCBs (Niimi, 1996) and/or more serious contamination of these compounds inoffshore waters and open seas environment (Lohmannet al., 2001) compared with PCDD/Fs. Mean and rangeof PCDD/Fs and coplanar PCBs concentrations inskipjack tuna collected from offshore waters aroundJapan in this study (Table 1) were apparently lower thanthose in fish collected from coastal waters of Japan(Japan Environmental Agency, 1998; Iimura et al., 2002;Seike et al., 2002), Korea (Choi et al., 2002) andMediterranean Sea (Corsolini et al., 1995; Kannan et al.,2002). It may be due to the fact that samples analyzed inthis study were collected from waters far from anthro-pogenic activities.

3.2. Geographical distribution of PCDD/Fsand coplanar PCBs

Geographical distribution of PCDD/Fs and coplanarPCBs concentrations in the muscle of skipjack tunaanalyzed in this study are shown in Fig. 2. Despite thesmaller number of sampling locations in the southernhemisphere (off-Indonesia, off-Seychelles and off-Bra-zil), residue levels of these compounds in skipjack tunafrom the northern hemisphere were found to be ap-parently higher than those from the southern hemi-sphere (Fig. 2 and Table 2). A similar distributionpattern of these compounds was also reported in the airand avian samples from the open sea (Lohmann et al.,2001; Tanabe et al., 2004). It is plausibly due to larger

usage and anthropogenic generation of PCDD/Fs andcoplanar PCBs in the northern hemisphere.

Among the regions surveyed in this study, highercontamination levels of PCDD/Fs and coplanar PCBswere found in offshore waters around temperate Asianregions (Fig. 2 and Table 2). The highest concentrationof PCDDs was detected in S-China Sea (13 pg/g lipidwt), followed by E-China Sea-2 and off-Taiwan (9.2 and8.4 pg/g lipid wt, respectively). The highest concen-trations of PCDFs and coplanar PCBs were found off-Taiwan (66 and 62000 pg/g lipid wt, respectively)followed by PCDFs in S-China Sea (65 pg/g lipid wt),and coplanar PCB in E-China Sea-2 (32000 pg/g lipidwt). These results may suggest that these compoundshave been used and generated in highly industrializedcountries around the East China Sea and the SouthChina Sea (Japan, Korea, Taiwan, Hong Kong, coastalChina, etc.). Another possible source of PCDFs may bethe technical PCBs used in industrialized countriesaround the East China Sea and the South China Sea.It has also been reported that technical PCBs containedPCDFs as impurity (Wakimoto et al., 1988). Actually,clear correlation is found between PCDFs and PCBsconcentrations in these samples ( p!0.01, Spearman’srank correlation). PCBs also could be one of the sourcesfor PCDFs pollution in skipjack tuna. However, a recentstudy pointed out that sources of dioxins were not onlyindustrialized countries but also developing countriesaround the Asian region. Hileman (2002) reportedthat massive amounts of electric/electronic products(televisions, computers, etc.) used in developed nationssuch as USA, Japan, Canada, Korea and Europe wereexported as trash to Asian developing countries suchas China, India or Pakistan, and this waste electricequipment was burned in the open air in those countries.Combustion processes are believed to be one of the majorsources of PCDD/Fs to the environment (e.g. Fiedler,1996). Indeed, notable contamination of PCDD/Fs andcoplanar PCBs was found in soil from open dumpingsites in Asian developing countries, such as Philippines,Cambodia and India (Minh et al., 2003). Minh et al.(2003) and the present findings suggest recent formationof PCDD/Fs and coplanar PCBs in open dumping sites inAsian developing countries, and these areas may be oneof the potential sources of dioxins to the marineenvironment around Asian regions. Further investiga-tions of the marine environment along Asian developingcountries are required.

Apparently lower residue levels of PCDDs (less thandetection limit) were found in the samples from openseas (N-Pacific-1 and -3) compared with those fromwaters around the Asian region (off-Japan, Japan Sea,E-China Sea and S-China Sea) (Fig. 2 and Table 2). Onthe other hand, concentrations of PCDFs and coplanarPCBs observed in samples from open seas (N-Pacific-1and -3) and those around the Asian region (off-Japan,

Table 2

ls (coplanar PCBs) (pg/g lipid wt) in the muscle of

pines

off-

Indonesia

Bay of

Bengal

off-

Seychelles

off-

Brazil

1.1 1.5 1.2 3.4

ND ND ND ND

ND ND ND ND

ND ND ND ND

ND ND ND ND

ND ND ND ND

ND ND ND ND

ND ND ND ND

ND ND ND 2.4

ND ND ND ND

2.2 3.1 ND 1.8

ND ND ND ND

ND ND ND ND

ND ND ND ND

ND ND ND ND

ND ND ND ND

ND ND ND ND

ND ND ND ND

78 120 47 87

4.4 5.4 3.8 5.1

60 69 30 91

29 45 31 45

1100 1600 480 2500

85 110 39 160

2900 4000 2300 6900

70 110 54 170

1200 1000 450 1800

270 290 150 460

560 610 390 1100

230 210 170 280

ND ND ND ND

2.2 3.1 ND 4.2

2.2 3.1 ND 4.2

(continued in next page)

307

D.Uenoet

al./Enviro

nmentalPollu

tion136(2005)303e

313

Concentrations of polychlorinated dibenzo-p-dioxins (PCDDs), polychlorinated dibenzofurans (PCDFs) and coplanar polychlorinated bipheny

skipjack tuna collected from Asian offshore waters, off-Seychelles and off-Brazil and open seas

DL Concentration (pg/g lipid wt)

N-

Pacific-1

N-

Pacific-2

N-

Pacific-3

off-

Japan-1

off-

Japan-2

Japan

Sea

E-China

Sea-1

E-China

Sea-2

off-

Taiwan

S-China

Sea

off-

Philip

Lipid (%) 4.6 1.6 5.1 5.8 5.2 4.0 3.8 1.7 0.73 1.6 0.95

Dioxins

2378-T4CDD 0.5 ND ND ND ND ND 1.1 1.6 1.3 ND ND ND

12378-P5CDD 1 ND ND ND 1.8 1.8 2.1 4.3 ND 8.4 7.9 ND

123478-H6CDD 1 ND ND ND ND 1.1 ND ND ND ND ND ND

123678-H6CDD 1 ND ND ND ND 1.8 2.6 ND ND ND 5.2 ND

123789-H6CDD 1 ND ND ND ND 1.1 ND ND ND ND ND ND

1234678-H7CDD 1 ND ND ND ND ND ND ND ND ND ND ND

O8CDD 4 ND ND ND ND ND ND ND 7.9 ND ND ND

Furans

2378-T4CDF 0.5 3.7 ND 1.8 5.3 8.3 8.7 9.5 7.6 11 5.9 ND

12378-P5CDF 0.5 1.2 ND 0.67 2.6 2.3 2.6 3.1 2.6 7.2 11 ND

23478-P5CDF 0.5 4.1 ND 4.1 7.9 13 9.9 14 8.3 27 17 3.0

123478-H6CDF 1 ND ND ND 2.3 1.7 ND 1.4 ND 5.4 6.6 ND

123678-H6CDF 1 ND ND ND 3.2 2.8 1.5 2.2 1.6 6.2 8.9 ND

123789-H6CDF 1 ND ND ND ND ND ND ND ND ND ND ND

234678-H6CDF 1 ND ND ND 4.8 4.4 ND 2.4 2.0 9.1 15 ND

1234678-H7CDF 1 ND ND ND 1.8 ND ND ND ND ND ND ND

1234789-H7CDF 1 ND ND ND ND ND ND ND ND ND ND ND

O8CDF 4 ND ND ND ND ND ND ND ND ND ND ND

Non-ortho

coplanar PCBs

#77 2 270 110 75 140 510 450 370 360 400 240 79

#81 2 17 13 5.2 21 44 32 31 29 49 39 6.1

#126 2 150 76 170 100 310 280 290 280 570 260 78

#169 3 58 27 140 42 120 130 140 140 350 150 55

Mono-ortho

coplanar PCBs

#105 15 2200 1100 2800 1800 4900 4600 5300 5000 9400 3300 1400

#114 15 200 110 320 180 420 400 480 500 1100 350 130

#118 15 7000 3100 12000 5900 17000 16000 17000 18000 32000 10000 4000

#123 15 160 99 330 160 330 360 280 370 860 290 110

#156 15 920 720 2900 760 2600 3200 3500 3700 8000 2200 120

#157 15 290 210 690 230 670 770 850 1000 2100 720 340

#167 15 580 480 2200 490 1500 1900 1900 2200 4800 1300 830

#189 15 200 210 590 170 540 690 740 860 2100 870 350

Total PCDDs ND ND ND 1.8 5.8 5.8 5.9 9.2 8.4 13 ND

Total PCDFs 8.9 ND 6.6 28 33 23 33 22 66 65 3.0

Total PCDD/Fs 8.9 ND 6.6 30 38 29 39 31 74 79 3.0

308 D. Ueno et al. / Environmental Pollution 136 (2005) 303e313

Table

2(continued)

DL

Concentration(pg/g

lipid

wt)

N-

Pacific-1

N-

Pacific-2

N-

Pacific-3

off-

Japan-1

off-

Japan-2

Japan

Sea

E-C

hina

Sea-1

E-C

hina

Sea-2

off-

Taiwan

S-C

hina

Sea

off-

Philippines

off-

Indonesia

Bayof

Bengal

off-

Seychelles

off-

Brazil

Totalnon-ortho

PCBs

490

230

390

300

980

890

820

810

1400

680

220

170

240

110

230

Totalmono-ortho

PCBs

12000

6100

22000

9700

28000

28000

30000

32000

60000

19000

8300

6300

7900

4100

13000

Totalcoplanar

PCBs

12000

6300

22000

10000

29000

29000

31000

32000

62000

20000

8500

6500

8100

4200

14000

DL,detectionlimit;ND,less

thandetectionlimit;N-Pacific,theNorthPacificOcean;E-C

hinaSea:theEast

ChinaSea;S-C

hinaSea:theSouth

ChinaSea;Lipid,lipid

contentsin

pooledmuscles.

Japan Sea, E-China Sea and S-China Sea) were

comparable. In order to make clear the differences ingeographical distribution of PCDD/Fs and coplanarPCBs from Asian region to open seas, concentrationratios of these compounds in skipjack tuna were com-pared (Fig. 3). As shown in Fig. 3, the concentrationratios of PCDDs to PCDFs in the samples from openseas (N-Pacific-1 and -2) were higher than those fromAsian regions (relatively coastal). Similarly, concentra-tion ratios of PCDDs to non-ortho coplanar PCBs alsoshowed higher values in open seas as compared to Asiancoastal regions, and these differences were greater thanthe ratios of PCDDs to PCDFs (Fig. 3). Concentrationratios in several species of sea birds collected fromcoastal areas and open seas also showed a similarpattern (Tanabe et al., 2004). It was already shown thatPCDFs and coplanar PCBs have higher vapor pressure(PL) and lower octanoleair partition coefficient (KOA)than PCDDs (Wania and Mackay, 1996; Mackay et al.,1992a,b; Beyer et al., 2000). In addition, it is reportedthat PCDDs have shorter half-lives than PCDFsand coplanar PCBs in the atmosphere (reviewed byLohmann and Jones, 1998). These results imply thatcoplanar PCBs may have the highest transportabilitythrough the atmosphere among these compounds, andthose of PCDFs were lower than PCBs but higher thanPCDDs. Other possible reasons for the higher concen-trations of PCDFs and coplanar PCBs than PCDDs inopen seas is that these chemicals might have beenreleased from international vessels passing through theNorth Pacific Ocean because technical PCBs have beenused on vessels as antifouling paints in the past(Maruyama et al., 1983) containing PCDFs as impurity(Wakimoto et al., 1988). On the other hand, naturalformation of dioxins was also found in the sedimentcore from the Pacific Ocean, estimated to be 1e10million years of age (Hashimoto et al., 1995). However,only very low concentrations of PCDDs were detectedand no PCDFs were found in these sediments (Hashi-moto et al., 1995). A similar profile of PCDD/Fs andnon-detectable levels of PCBs have been reported insediment core of older period from coastal Australia(Gaus et al., 2001) and archived soil from the UK(Green et al., 2001). In addition, contribution by PCDFsfrom natural origin to skipjack tuna seems to be lowbecause the concentrations in this species are apparentlyhigher than concentrations derived by using the datafrom sediment core (Hashimoto et al., 1995) and biota-sediment accumulation factors (BSAFs) (Loonen et al.,1994; Kim et al., 1996). These results suggest very littlecontribution of PCDD/Fs from natural origin toskipjack tuna, and the possibility of long range trans-port of anthropogenic sources of these chemicals fromcoastal regions to open oceans. In this context, coplanarPCBs may have a higher potency for long rangetransport among these compounds. Transportability of

309D. Ueno et al. / Environmental Pollution 136 (2005) 303e313

PCDDs

60°N

0°

nd

nd

nd

nd

nd

nd

nd

nd

pg/g

lipid wt

0

3

60°N

60°S

0°

nd

nd

pg/g

lipid wt

0

15

PCDFs

60°S

60°S

60°N

0°

pg/g

lipid wt

0

400

non-ortho PCBs

60°N

60°S

0°

ng/g

lipid wt

0

15

mono-ortho PCBs

Fig. 2. Geographical distribution of PCDD/Fs and coplanar PCBs in the muscle of skipjack tuna.

PCDFs seems to be lower than PCBs, but relativelyhigher potency than PCDDs.

3.3. Congener specific accumulation of PCDD/Fsand coplanar PCBs

Congener specific accumulation of PCDD/Fs andcoplanar PCBs in skipjack tuna are shown in Table 2.Among PCDD/Fs congeners, 2,3,4,7,8-P5CDF was thepredominant congener in all the skipjack tuna analyzed,followed by 2,3,7,8-T4CDFO1,2,3,6,7,8-H6CDFZ2,3,4,6,7,8-H6CDF (Table 2). This is a typical patternobserved in marine fish species around the Asian region(Japan Environmental Agency, 1998; Iimura et al., 2002;Seike et al., 2002). It has been reported that 2,3,4,7,8-P5CDF is one of the major congener in technical PCBsas impurity (Wakimoto et al., 1988). PCBs could be oneof the sources of 2,3,4,6,7,8-H6CDF in skipjack tuna.The congener pattern of PCDDs could not be discussedhere due to their lower concentrations (below detectionlimit). In the congener patterns of coplanar PCBs,CB77 and CB118 were the most prevalent congenersamong non-ortho and mono-ortho coplanar PCBs,respectively (Table 2). These patterns were commonlyobserved in fish species around the Asian region (Japan

Environmental Agency, 1998; Iimura et al., 2002;Nakata et al., 1998).

In order to examine the geographical distributionof the congener profile, the percentage contribution ofindividual congeners of PCDFs and non-ortho coplanarPCBs was compared among the locations from south tonorth (Fig. 4). As seen in Fig. 4, the tetra-chlorinatedcongener of PCB (CB77) in the sample from N-Pacific-1accounted for a higher proportion than that fromsouthern regions such as off-Taiwan. In contrast,proportions of penta- and hexa-chlorinated congeners(CB126 and CB169) were higher in southern regions suchas off-Taiwan than those from northern regions suchas N-Pacific-1. A similar pattern has previously beenobserved in marine mammals (Minh et al., 2000). It hasbeen reported that 1e4 chlorinated PCBs may posepreferential deposition and accumulation in polar lat-itudes, and 4e8 chlorinatedPCBsdeposit inmid-latitudesfrom themodel using the value ofPL andKOA (Wania andMackay, 1996). This is again evident in this study.

On the other hand, no compositional trend wasobserved in PCDFs in this study (Fig. 4). Wania andMackay (1996) noted that 2e4 chlorinated PCDD/Fsmay show preferential deposition and accumulation inmid-latitudes, and 4e8 chlorinated PCDD/Fs deposit

310 D. Ueno et al. / Environmental Pollution 136 (2005) 303e313

rapidly close to source from the model using PL andKOA.It has also been reported that lower chlorinated con-geners of PCDFs have shorter half-lives than higherchlorinated congeners in the atmosphere (reviewed byLohmann and Jones, 1998). As another possible reason,PCDFs from natural origin also may be considered.Indeed, Hashimoto et al. (1995) analyzed sediment coresfrom the Pacific Oceans, and detected the predominance

0

10

20

0

500

1000

Asian regions

off-T

aiw

an

E-C

hin

a-S

ea-1

N-P

acific-3

N-P

acific-1

Open sea

Co

ncen

tratio

n ratio

DFs / DDs

non-PCBs / DDs

Fig. 3. Concentration ratios of PCDD/Fs and coplanar PCBs from

Asian coastal regions and open seas. (DDs, DFs and non-PCBs

indicate sum of PCDDs, PCDFs and non-ortho coplanar PCBs; The

values of detection limit were used when the values were below

detection limit).

of O8CDD from natural origin in the cores of approx-imately 1e10 million years of age. However, thecontribution of PCDFs from natural origin in skipjacktuna seem to be low, as discussed previously (see Section3.2). These results indicate that relatively lower trans-portability of PCDFs than PCBs and preferentialdegradation of lower chlorinated congeners in theatmosphere seem to explain the absence of any compo-sitional trend of PCDFs in the specimens from south tonorth in the present study. Otherwise, local anthropo-genic sources of these compounds are more predominantthan those transported through the atmosphere.

3.4. Toxic potential of PCDD/Fs andcoplanar PCBs

In this study, the human specific 2,3,7,8-TCDDtoxic equivalents factors (TEFs) developed by WHO(van den Berg et al., 1998) were used for hazard and riskassessment. The estimated toxic equivalents (pg TEQs/gwet wt) of PCDD/Fs and coplanar PCBs in the muscle ofskipjack tuna are shown in Table 3. The total TEQs werein the range of 0.092e2.4 pg TEQs/g wet wt (Table 3).The highest value of TEQs was detected in the location,off-Japan-2 (2.4 pg TEQs/g wet wt), followed by E-China Sea-1OJapan Sea (1.8 and 1.7 pg TEQs/g wetwt). These TEQs values found in skipjack tuna wereapparently lower than those in fishes collected fromcoastal waters around Japan (Japan EnvironmentalAgency, 1998; Japan Fisheries Agency, 2003; Iimuraet al., 2002).

The relative contribution of TEQs by PCDD/Fs andcoplanar PCBs is shown in Fig. 5. Coplanar PCBs-TEQsaccounted for 60e100% of total-TEQs in skipjack tuna,and more than 80% of coplanar PCBs-TEQs wereattributed to non-ortho coplanar PCBs-TEQs (Fig. 5).In coastal regions around Japan, the relative contri-bution of coplanar PCB-TEQs in several fish showed

500 25 75 100 500 25 75 100

Contribution (%)

Northward

Southward

CB77 CB81 CB126 CB169

N-Pacific-1

off-Japan-1

off-Japan-2

E-China Sea-1

E-China Sea-2

off-Taiwan

2378-

T4CDF

12378-

P5CDF

23478-

P5CDF

123478-

H6CDF123678-

H6CDF

234678-

H6CDF

1234678-

H7CDF

non-ortho PCBs PCDFs

Fig. 4. North-south profile of non-ortho coplanar PCBs and PCDFs in skipjack tuna from Asia-Pacific region.

311D. Ueno et al. / Environmental Pollution 136 (2005) 303e313

comparable or smaller percentage than PCDD/Fs-TEQs(Japan Environmental Agency, 1998; Japan FisheriesAgency, 2003; Iimura et al., 2002). These results indicatethat the relative potential of coplanar PCBs as toxiccontaminants may be greater in offshore waters andopen seas, due to the higher transportability of thesecompounds than PCDD/Fs.

4. Conclusion

To elucidate the global distribution of PCDD/Fs andcoplanar PCBs in offshore waters and open seas, thepresent study determined the concentrations of thesecompounds in the muscle of skipjack tuna (Katsuwonus

Table 3

TEQ values of dioxin related compounds (pg/g wet wt) in the muscle of

skipjack tuna collected from Asian offshore waters, off-Seychelles and

off-Brazil and open seas

TEQs (pg/g wet wt)

PCDDs PCDFs non-

ortho-PCBs

mono-

ortho-PCBs

Total

TEQs

N-Pacific-1 NA 0.020 0.71 0.076 0.81

N-Pacific-2 NA NA 0.12 0.015 0.14

N-Pacific-3 NA 0.11 0.87 0.18 1.2

off-Japan-1 0.11 0.33 0.58 0.080 1.1

off-Japan-2 0.12 0.44 1.6 0.21 2.4

Japan Sea 0.14 0.24 1.1 0.17 1.7

E-China Sea-1 0.23 0.34 1.1 0.18 1.8

E-China Sea-2 0.022 0.091 0.47 0.084 0.67

off-Taiwan 0.061 0.12 0.42 0.072 0.68

S-China Sea 0.13 0.21 0.41 0.048 0.79

off-Philippines NA 0.014 0.074 0.013 0.10

off-Indonesia NA 0.012 0.066 0.013 0.092

Bay of Bengal NA 0.023 0.10 0.019 0.14

off-Seychelles NA NA 0.037 0.0074 0.044

off-Brazil NA 0.039 0.31 0.074 0.43

NA, no data available.

N-Pacific-1

N-Pacific-2

N-Pacific-3

off-Japan-1

off-Japan-2

Japan Sea

E-China Sea-1

E-China Sea-2

off-Taiwan

S-China Sea

off-Philippines

off-Indonesia

Bay of Bengal

off-Seychelles

off-Brazil

non-ortho PCBs mono-ortho PCBs

0 25 7550 100

Contribution to total TEQs (%)

TEQ

PCDDs

PCDFs

Fig. 5. Percentage contribution of PCDD/Fs and coplanar PCBs for

total TEQ values in the muscle of skipjack tuna.

pelamis) collected from various regions of offshorewaters and open seas. Higher concentrations ofPCDD/Fs and coplanar PCBs were detected in thesamples from the temperate Asian region, plausibly dueto larger usage and anthropogenic generation in highlyindustrialized countries around the East China Sea andthe South China Sea. In addition, this result also suggeststhe possibility of the generation of these contaminantsthrough combustion processes in open dumping sites inAsian developing countries. Comparable or relativelylower concentrations of PCDFs and coplanar PCBs wereobserved in mid-Pacific compared with Asian regions,and the preferential atmospheric transport of thesecompounds from pollution sources to remote regions ismade clear. This indicates that PCDFs and coplanarPCBs could cause global pollution through the atmo-sphere due to their higher transportable nature, and openseas and/or polar regions may play a role as final sinksfor these compounds. Moreover, more than 60% ofTEQs were attributed to coplanar PCBs in skipjack tunaindicating the importance of coplanar PCBs as toxiccontaminants in the offshore waters and open seasecosystem.

Acknowledgements

The authors thank Dr A. Nihira (Ibaraki PrefecturalFisheries Experimental Station, Japan), Dr J. Takeuchi(Wakayama Research Center of Agriculture, Forestryand Fisheries, Japan), Dr H. Tameishi (Japan FisheriesInformation Service Center, Japan) and Dr I. Nakamura(Kyoto University, Japan) for providing the ecologicalinformation of skipjack tuna and Mr M. Nakamuraand Ms M. Takahashi (Hiraki-no-Takahashi, Co. Ltd.,Japan) for collecting skipjack tuna around Japan. Thisstudy was supported partly by a Fund ‘‘21st CenturyCOE Program’’ from the Ministry of Education,Culture, Sports, Science and Technology of Japan,‘‘Japan-Korea Co-operative Joint Research Programon Endocrine Disrupting Chemicals’’ from the Minis-try of the Environment, Japan and ‘‘Material CyclesModeling of Persistent Toxic Chemicals and its PolicyResearch Applications for Recycling and Waste Man-agement’’ from theWaste Management Research Grantsof the Ministry of the Environment. One of the authors(Dr Ueno) thanks the Grant-in-Aid for JSPS Fellowsfrom Japan Society for the Promotion of Science for thefellowship provided to him during the course of thisstudy.

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