Environmental Pollution 144 (2006) 238e247www.elsevier.com/locate/envpol

Distribution and transportability of hexabromocyclododecane(HBCD) in the Asia-Pacific region using skipjack

tuna as a bioindicator

Daisuke Ueno a,b,*, Mehran Alaee a, Chris Marvin a, Derek C.G. Muir a,Gordia Macinnis a, Eric Reiner c, Patrick Crozier c, Vasile I. Furdui c,

Annamalai Subramanian b, Gilberto Fillmann d, Paul K.S. Lam e,Gene J. Zheng e, Muswerry Muchtar f, Hamidah Razak f,

Maricar Prudente g, Kyu-hyuck Chung h,Shinsuke Tanabe b

a National Water Research Institute, Environment Canada, 867 Lakeshore Road, P.O. Box 5050,

Burlington ON L7R 4A6, Canadab Center for Marine Environmental Studies (CMES), Ehime University, Ehime, Japan

c Ontario Ministry of the Environment, Toronto, ON, Canadad Department of Oceanography, Fundac~ao Universidade Federal do Rio Grande, Rio Grande, Brazil

e Department of Biology and Chemistry, City University of Hong Kong, Hong Kongf Research and Development Center for Oceanology, Indonesian Institute of Sciences,

Jakarta, Indonesiag Science Education Department, De La Salle University, Manila, Philippines

h College of Pharmacy, Sungkyunkwan University, Seoul, South Korea

Received 26 November 2005; accepted 11 December 2005

Geographical distribution of hexabromocyclododecane (HBCD) in offshore waterof Asia-Pacific region was investigated using skipjack tuna as a bioindicator.

Abstract

The geographical distribution of hexabromocyclododecane (HBCD) was investigated through analysis of muscle tissue of skipjack tuna (Kat-suwonus pelamis) collected from offshore waters of Asia-Pacific region (Japan, Taiwan, Philippines, Indonesia, Seychelles, Brazil, Japan Sea,East China Sea, South China Sea, Indian Ocean and North Pacific Ocean). HBCD was detected in almost all samples analyzed (<0.1 to 45 ng/glipid weight basis), indicating widespread presence of this compound in the marine environment. Elevated concentrations of HBCD were foundin skipjack tuna from areas around Japan, which have the larger modern industrial/urban societies, and implicated these areas as primary regionalsources. All three individual HBCD isomers (a-, g- and b-HBCD) were detected in almost all samples; the percentage contribution of the a-isomer to total HBCD increased with increasing latitude. The estimated empirical 1/2 distance for a-HBCD was 8500 km, which is one of thehighest atmospheric transportability among various halogenated persistent organic pollutants (POPs).� 2006 Elsevier Ltd. All rights reserved.

Keywords: Brominated flame retardant; Hexabromocyclododecanes; Persistent organic pollutants; Fish; Atmospheric transport

* Corresponding author. Faculty of Agriculture, Saga University, Honjo-cho 1, Saga 840-8502, Japan.

E-mail address: ueno@qg8.so-net.ne.jp (D. Ueno).

0269-7491/$ - see front matter � 2006 Elsevier Ltd. All rights reserved.

doi:10.1016/j.envpol.2005.12.024

239D. Ueno et al. / Environmental Pollution 144 (2006) 238e247

1. Introduction

Flame retardants are substances added or applied tocombustible materials to increase fire resistance (Alaeeet al., 2003). Hexabromocyclododecane (HBCD) is the prin-cipal brominated flame retardant (BFR) in polystyrenefoams used as thermal insulation in building materials. Sec-ondary applications include use in residential and commer-cial upholstery, transportation upholstery, draperies, andwall coverings (de Wit, 2002). HBCD is an additive flameretardant; therefore, this compound is not covalently bondedto the material and may migrate out of products into the en-vironment during use or after disposal (Marvin et al., inpress).

Use of HBCD has increased as with implementation ofmandatory (EU), or voluntary (Japan), restrictions of otherBFRs including the penta- and octa-brominated diphenylethers (PBDEs) formulations (Kemmlein et al., 2003). Ofthe estimated world market demand for HBCD of 17 kilotonsin 2001, 9.5 kilotons (57%) was consumed in Europe, fol-lowed by Asia (23%) (BSEF, 2005). Among the usage ofHBCD in Asian region, half of the Asian demand was attrib-uted to Japan where usage of this compound has been increas-ing since 1986 (Watanabe and Sakai, 2003; BSEF, 2005;Kajiwara et al., in press).

Environmental monitoring of HBCD has been conducted inEurope and North America, and this compound has beendetected from some of environmental media and biota(Tomy et al., 2004; Eljarrat et al., 2004, 2005; Morris et al.,2004). Although large amounts of HBCD have been used inthe Asian region, environmental monitoring for this compoundhas not been conducted in this region. Moreover, detection ofHBCD in remote background air sample from Sweden andFinland suggested the potential of long-range atmospherictransport of this compound (Remberger et al., 2004). Accordingto these facts, it is required to understand the contaminationstatus and transport behavior of this compound in Asia-pacificregion.

In order to assess the extent of HBCD contamination inthe Asia-Pacific region including open sea and remote region,this study attempted to use skipjack tuna (Katsuwonus pela-mis) as a bioindicator. Skipjack tuna is principally distributedfrom offshore waters to open seas in tropical and temperateregions in many areas of the world, including the Pacific, At-lantic, and Indian Oceans (Collette and Nauen, 1983). Thisspecies is an important commercial fish, and its ecologyand biology has been well studied (Collette and Nauen,1983; Nihira, 1996). The suitability of skipjack tuna forglobal monitoring of persistent organic pollutants (POPs)has been established in our previous work (Ueno et al.,2003). Our study found that this species reflected water con-centrations of POPs on site quickly resulting from biomagni-fication of those chemicals through the marine food web.Therefore, not only migration pattern, but also growth stage,and sex of these animals had little effect on concentrations ofPOPs on lipid weight basis when this species is used forglobal scale monitoring (Ueno et al., 2003). These attributes

potentially make skipjack tuna a suitable bioindicator formonitoring HBCD pollution as well as PCBs, DDTs, dioxins,butyltins and PBDEs (Ueno et al., 2003, 2004a, b, 2005). Theobjectives of this study were to study the distribution ofHBCD in offshore waters around Asia-Pacific region, andto better understand the global transport behavior of thischemical.

2. Materials and methods

2.1. Sample collection

This study employed the muscle of skipjack tuna (Katsuwonus pelamis) ar-

chived in the Environmental Specimen Bank (es-BANK ) at Ehime University.

Samples were collected from offshore waters of various regions (Japan, Tai-

wan, Philippines, Indonesia, Seychelles, Brazil, Japan Sea, East China Sea,

South China Sea, Indian Ocean, and North Pacific Ocean) during the years

1997e2001 (Fig. 1). Skipjack tuna from North Pacific-1, -3 and Brazil were

caught during a research cruise. Fish from other regions were purchased in lo-

cal fish market; confirmation of sites where fish were collected was obtained

from vendors. Those samples were transported to laboratory and those muscles

taken from individual specimens were kept at �20 �C. Polyethylene bags used

for keeping these samples were tested for potential HBCD interferences.

HBCD was not detected in these bags.

The available amounts of these samples were limited due to archived sam-

ples in specimen bank at Ehime University. Therefore, pooled muscle tissues

of five fish from each location were used for chemical analysis. It was reported

that there was no significant difference between mean concentrations of indi-

vidual samples analysis and those of pooled samples using archived bird eggs

collected from Great Lake (Turle and Collins, 1992). Sample details are shown

in Table 1.

2.2. Analytical method

HBCD (a-HBCD, b-HBCD and g-HBCD) in fish samples was analyzed

using a method modified from Tomy et al. (2004). Briefly, about 20 g of

muscle samples were homogenized with anhydrous Na2SO4 and extracted us-

ing a Soxhlet apparatus with a dichloromethane after adding 4 ng of individ-

ual surrogate standards (13C12-labeled a-HBCD and g-HBCD, Wellington

Laboratories, Guelph, ON, Canada). Extracts were concentrated by rotary

evaporation and subjected to gel permeation chromatography (Bio-Beads

SX3, Bio-Rad Laboratories, USA) with 50% dichloromethane in hexane

for lipid removal. Lipid content was determined gravimetrically using a lipid

fraction (F1) from the GPC cleanup. The GPC fraction containing HBCD

(F2) was concentrated and passed through 8 g of activated silica gel in an

open column. The first fraction eluted with hexane contained some organo-

halogens; the second fraction eluted with 50% dichloromethane in hexane

contained HBCD. The fraction contained HBCD was solvent-exchanged

into methanol for LC/MS/MS analysis. 4 ng of 13C12-labeled b-HBCD

was added to the extract prior to LC-MS/MS analysis as a performance

standard.

Samples were analyzed on a ABI/Sciex API 4000 mass spectrometer

(MDS Sciex, Toronto, ON, Canada) equipped with an Agilent 1100 Series

LC system (Agilent Technology, USA). Separation of HBCD isomers was

achieved on a Vydac 218MS 5 mm Particle size 15 � 2.1 mm i.d. polymeric

reversed phase HPLC column. The mobile phase was consisted of methanol/

acetonitrile/water (60:20:20) for 5 min at 250 mL/min, followed by 100% of

methanol for 7 min. The mass spectrometer was operated in electrospray ion-

ization (ESI) negative ion mode. MS/MS detection used multiple reaction

monitoring (MRM) conditions for the m/z 640.6 ([M � H]�) to Br� transition,

utilizing unit resolution on the first and third quadrupoles and a 100 ms dwell

time.

240 D. Ueno et al. / Environmental Pollution 144 (2006) 238e247

off-Philippines

N-Pacific-3

N-Pacific-1

N-Pacific-2

off-Indonesia

S-China Sea

Bay of Bengal

off-Seychelles

off Taiwan

off-Japan-1

Japan Sea

E-China Sea-1

off-Japan-2

E-China Sea-2

off-Brazil

60° N

60° S

90° W 180° E

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

2.3. Quantification and quality control

HBCD isomers were quantified by isotope dilution using the correspond-

ing 13C12-labeled isomers (b-HBCD was quantified using 13C12-g-HBCD).

Recoveries of 13C12-labeled HBCD during analytical procedure were deter-

mined using 13C12-labeled b-HBCD and these values were ranged between

60% and 120%. The reproducibility of these concentrations analyzed tripli-

cate samples was less than 10%. Method detection limits (MDLs) were

determined using spiked blank (13C12-labeled isomers) samples (n ¼ 3).

MDLs were calculated as three-times standard deviation of background

peaks in the blanks. MDLs of a-HBCD, b-HBCD and g-HBCD were

0.001, 0.001 and 0.004 ng/g wet weight (based on 20 g of sample),

respectively.

2.4. Statistical analysis

Half-decline distances (1/2 distance) were calculated using the HBCD con-

centrations in this study, and POPs concentrations previously reported (Ueno

et al., 2003, 2004a, 2005). Simple regression analysis was used to obtain

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 pooled; 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.

241D. Ueno et al. / Environmental Pollution 144 (2006) 238e247

regression equations, p and r2 values. Statistical analyses were performed us-

ing StatView (Version 5.0, SAS Institute, Cary, NC, USA).

3. Results and discussion

3.1. Contamination status of HBCD

HBCD concentrations in muscle of skipjack tuna from off-shore water of Asia-Pacific region are shown in Table 2.HBCD were detected from all the samples analyzed in thisstudy even in mid of Pacific Ocean, with the exception ofthe off-Seychelles samples. These results indicate a wide-spread presence of HBCD in the global marine environment.Concentrations of total HBCD ranged from <0.1 to 45 ng/glipid weight basis (Table 2). These HBCD concentrations inskipjack tuna were comparable to, or lower than, concentra-tions in fish collected from a Canadian Great Lake (Tomyet al., 2004), the Cinca River in Spain (Eljarrat et al., 2004,2005), the North Sea (Morris et al., 2004), and the Scheldtestuary in the Netherlands (Janak et al., 2005). The lowerlevels of HBCD contamination in fish in this study can beattributed to the remoteness of the offshore sample collection

Table 2

HBCD concentrations (ng/g lipid wt) in pooled muscle of skipjack tuna col-

lected from Asian offshore waters, off-Seychelles, off-Brazil and open seas

Location Lipid Concentration (ng/g lipid wt)

% a-HBCD b-HBCD g-HBCDP

HBCD

N-Pacific-1 3.7 22 0.22 1.6 25

N-Pacific-2 1.8 24 0.63 4.2 29

N-Pacific-3 0.8 0.86 0.25 <0.5 1.1

off-Japan-1 4.9 30 0.27 1.9 32

off-Japan-2 4.8 40 0.30 4.2 45

Japan Sea 7.4 5.0 0.66 1.4 6.5

E-China Sea-1 2.6 29 0.75 14 44

E-China Sea-2 0.8 21 0.41 6.5 28

off-Taiwan 0.4 24 0.38 2.3 27

S-China Sea 1.2 2.5 0.10 0.65 3.2

off-Philippines 0.6 0.86 <0.1 <0.4 0.86

Bay of Bengal 0.8 0.27 <0.1 <0.4 0.27

off-Indonesia 0.8 0.41 <0.1 <0.4 0.41

off-Seychelles 0.7 <0.1 <0.1 <0.4 n.d.

off-Brazil 3.1 0.28 <0.03 <0.1 0.28

n.d., less than detection limit; N-Pacific, the North Pacific; E-China Sea, the

East China Sea; S-China Sea, the South China Sea; Lipid, lipid contents in

pooled muscles;P

HBCD: a þ b þ g-HBCD.

nd: under detection limit

PBDEs

nd

60° N

60° N

60° S

60° S

0°

0°

HBCD

ng/g

lipid wt

0

5

nd

ng/g

lipid wt0

10

90° W 180° E

90° W 180° E

Fig. 2. Geographical distribution ofP

HBCD (a þ b þ g-HBCD) andP

PBDE concentrations in muscle of skipjack tuna. Distribution of PBDEs is cited from

Ueno et al. (2004a).

242 D. Ueno et al. / Environmental Pollution 144 (2006) 238e247

sites, relative to nearshore areas in closer proximity to urban-ized/industrialized areas. Those aspects are similar withPBDEs detected from skipjack tuna (Ueno et al., 2004a)(Fig. 2).

3.2. Geographical distribution of HBCD

Skipjack tuna is principally distributed from offshore wa-ters to open seas in tropical and temperate regions in manyareas of the world, including the Pacific, Atlantic, and IndianOceans (Collette and Nauen, 1983). It is reported that skipjacktuna born in Pacific equatorial waters migrates to watersaround 40 � north and south, and it returns to the equatorialspawning areas (Collette and Nauen, 1983). The suitabilityof skipjack tuna as bioindicator for global monitoring ofPOPs has been established in our previous work (Uenoet al., 2003); which showed that this species reflected waterconcentrations of POPs on site quickly resulting from biomag-nification of those chemicals through the marine food webby comparing the POPs concentrations in water and thosesamples. Therefore, migration pattern, growth stage, and sexof these animals had little effect on concentrations of POPson lipid weight basis when this species is used for global scalemonitoring. Consequently, migration pattern, growth stage,and sex of these specimens would not be considered in thisstudy.

The geographical distribution of HBCD concentrations inskipjack tuna is shown in Fig. 2. Although the numbers ofsamples from the southern hemisphere were small (off-Indone-sia, off-Seychelles, and off-Brazil), residue levels of HBCD inskipjack tuna collected from areas of the northern hemispherewere apparently higher than those from southern hemisphere.Higher concentrations of PBDEs were also found in skipjacktuna from northern hemisphere (Ueno et al., 2004a) (Fig. 2).Similar distributions have also been reported for variousPOPs; greater volumes of these chemicals were consumed in

Table 3

Correlation between HBCD and other organohalogen concentrations detected

from skipjack tuna

Compounds Significance ( p)a ReferenceP

HBCD vs.P

non-ortho-PCBs 0.0030 Ueno et al., 2005P

mono-ortho-PCBs 0.013 Ueno et al., 2005PCHLs 0.017 Ueno et al., 2003PPCDFs 0.023 Ueno et al., 2005

PPCBs 0.031 Ueno et al., 2003

PPCDDs 0.036 Ueno et al., 2005PPBDEs 0.037 Ueno et al., 2004a

HCB 0.037 Ueno et al., 2003P

HCHs 0.056 Ueno et al., 2003P

DDTs 0.37 Ueno et al., 2003

HBCD, a þ b þ g-HBCD;P

CHLs, trans-chlordane þ cis-chlordane þ -

trans-nonachlor þ cis-nonachlor þ oxychlordane;P

PCDDs andP

PCDFs,

sum of 2,3,7,8 substituted congener concentrations;P

PCBs, sum of major

congeners;P

PBDEs, sum of 8 congeners from di to hepta; HCB, hexachlor-

obenzene;P

HCHs, a þ b þ g-HCH;P

DDTs, p,p0-DDT þ p,p0-DDE þ p,p0-DDD.

a Spearman’s rank correlation (n ¼ 15).

the northern hemisphere due to greater degrees of industrialand agricultural activity (Breivik et al., 2002; Voldner et al.,2005). It was reported that 97% of HBCD demand in 2001was attributable to use in areas of the northern hemisphere in-cluding North America, Europe and Asia (3% in rest of world)(BSEF, 2005). The reasons for higher concentrations of HBCDin skipjack tuna from northern hemisphere could be greatervolumes of HBCD usage.

Among the samples collected from northern hemisphere,higher concentrations of HBCD were found in mid-latitudeareas of the Far East (Fig. 2). The highest concentration ofHBCD was detected in a sample collected near Japan (off-Japan-2, 45 ng/g lipid weight); relatively high concentrationswere also found in other areas around Japan (off-Japan-1),the East China Sea (E-China Sea-1 and E-China Sea-2), andN-Pacific-1 (Fig. 2). This distribution of HBCD was similarto PCBs in the same samples of skipjack tuna (Ueno et al.,2003, 2005). HBCD was highly correlated with coplanarPCBs ( p ¼ 0.003), chlordanes ( p ¼ 0.02) and polychlorinateddibenzofurans (PCDFs, p ¼ 0.02) previously reported (Uenoet al., 2003, 2005) (Table 3). Elevated levels of PCBs andPCDFs are associated with areas around Japan, Korea, Taiwanand coastal China (along East China Sea), all of which are as-sociated with high degrees of industrialization/urbanization(Ueno et al., 2003, 2005). It has been reported that Asiancountries are responsible for roughly 30% of global HBCD de-mand, and almost 50% of the Asian consumption was attrib-uted to Japan (Watanabe and Sakai, 2003; BSEF, 2005;Kajiwara et al., in press). Marvin et al. (in press) and Re-mberger et al. (2004) have suggested that large urban areascan act as diffuse sources of HBCD used in modern industrialapplications. These Asian regions have larger modern indus-trial/urban societies with higher income per capita in general,compared with other southern/southeastern Asian developingregions (Asia week, 2001). Greater demand and manufactur-ing of consumer products including building material andtransportation upholstery, in which HBCD is heavily used, inthe higher income per capita Asian regions may be a determin-ing factor in the observed regional distribution of HBCD inskipjack tuna (Fig. 2).

The distribution pattern of PBDEs was generally similarto HBCD, in that concentrations were higher in Far East(Ueno et al., 2004a) (Fig. 2). However, the correlationbetween HBCD and PBDEs ( p ¼ 0.04) was weaker thanbetween HBCD and PCBs ( p ¼ 0.003) (Table 3), and rela-tively higher concentrations of PBDEs were found aroundEast China Sea and southeastern Asian region (Fig. 2). Itwas reported that relatively new pollution sources ofPBDEs might be located in the countries around the EastChina Sea and southeastern Asian countries, rather thanJapan, as many industrial activities and open-dump sites forelectrical waste are located in these regions (Ueno et al.,2004a, 2005). It is reported that many industrial manufac-turers (computers, televisions, and other electric householdequipments) are located in coastal areas of Asian developingcountries (American Chemical Society, 2002). The globalmarket demand of BFRs in 2001 showed that, within the

243D. Ueno et al. / Environmental Pollution 144 (2006) 238e247

Asian consumption, 90% of PBDEs were consumed by otherAsian countries while only 10% of PBDEs were used byJapan (Watanabe and Sakai, 2003; BSEF, 2005; Kajiwaraet al., in press). Moreover, massive amounts of waste electricproducts (television, computer etc.) used in developed nationssuch as the USA, Japan, Canada, Korea and Europe were ex-ported as trash to Asian developing countries such as China,India or Pakistan (Hileman, 2002). Actually, the temporaltrend of PBDEs determined using northern fur seals indicatedthat levels of these compounds in Japan have been decreasingsince the mid-1990s after voluntary phasing-out of thesecompound by industry (Kajiwara et al., 2004). These resultssuggested that the pollution sources of PBDEs may haveshifted from Japan to other southeastern Asian countries. Infact, ‘‘Pollution shifting’’ has been reported in some Asiandeveloping countries. For example, it was reported that con-tamination levels of butyltins (BTs) in southeast Asian devel-oping countries increased after production and usage wasbanned in developed countries such as Japan, North Americaand Europe (Tanabe, 1999; Sudaryanto et al., 2002; Uenoet al., 2004b). Similar to PBDEs and BTs, emission sourcesof HBCD may also be shifted from Japan to other south-ern/southeastern Asian countries in near future, which em-phasizes the requirement for continuous environmentalmonitoring of HBCD in those regions.

No significant relationships were found between HBCDand the HCHs ( p ¼ 0.056) or DDTs ( p ¼ 0.37) (Table 3).HBCD is used for industrial purposes, but HCHs and DDTsare used in agricultural and/or public health applications.Higher concentrations of HCH and DDT were found in aquaticorganisms from China and southern/southeastern Asian coun-tries (Monirith et al., 2003; Ueno et al., 2003) where thesecompounds are still being used, but have been banned in Japansince the early 1970s (Voldner and Li, 1995).

Unexpectedly, comparable concentration of HBCD wasfound in skipjack tuna collected from remote northern

cold-water region (N-Pacific-1) compared with coastal Asianregions (off-Japan-1, -2, E-China Sea-1 and -2) (Fig. 2).This distribution pattern was clearly different with PBDEsin skipjack tuna, which showed lower concentrations in north-ern cold-water region (N-Pacific-1) (Ueno et al., 2004a)(Fig. 2). The HBCD distribution was similar to HCHs andHCB in skipjack tuna (Ueno et al., 2003); these compoundshave the highest transportable values among the POPs (Waniaand Mackay, 1996; Beyer et al., 2000). Some POPs can betransported atmospherically to the areas where they condense,deposit and accumulate in cold-water ecosystems througha process known as global distillation. For example, HCHsand HCB have greater tendencies to accumulate in cold-waterremote (polar) regions after transport from pollution sources inmid-latitude areas (reviewed by Wania and Mackay, 1996;Muir et al., 1999; Beyer et al., 2000). Presumably, low volatil-ity (4.7 � 10�7 mmHg) and low water solubility (3.4 mg/L)result in HBCD being primarily adsorbed to sediment(Birnbaum and Staskal, 2004, 2004; Marvin et al., in press)and the compounds having these natures are generally lesstransportable and tend to deposit near primary sources in theenvironment (Watanabe and Sakai, 2003). However, higherconcentration of HBCD was detected in remote northerncolder regions (Fig. 2). Remberger et al. (2004) also detectedHBCD in remote background air sample from Sweden andFinland, and suggested long-range atmospheric transport po-tential of this compound. These results suggest that unknownlocal pollution sources have been existing in this region or/andsignificant long-range atmospheric transport could occur, withthe potential to be distributed globally in a manner similar toPCBs.

3.3. Variation in HBCD isomer profiles

Among the HBCD isomers detected in skipjack tuna, a-HBCD was predominant, followed by g-HBCD > b-HBCD

0 25 7550 100

Composition (%)

Northward

Southward

-HBCD -HBCD -HBCD

N-Pacific-1

off-Japan-1

off-Japan-2

Japan Sea

E-China Sea-2

E-China Sea-1

Fig. 3. North-south profile of HBCD composition in skipjack tuna collected from Asian offshore waters.

244 D. Ueno et al. / Environmental Pollution 144 (2006) 238e247

0

0

1

1

2

2

3

3

4

4

5

50 1 2 3 4 5

0 1 2 3 4 5 0 1 2 3 4 5

Total HBCDs, k=-0.13

-HBCD, k=-0.07

-HBCD, k=-0.43

Log

conc

entra

tion

(ng/

g lip

id w

t)

Distance (x1000 km)

Distance (x1000 km) Distance (x1000 km)

Distance (x1000 km)

-2

-1

0

1

2

3

4

PBDE47, k=-0.37

PBDE153, k=-0.56

PBDE28, k=-0.12

Log

conc

entra

tion

(ng/

g lip

id w

t)-1

0

1

2

3

4

23478-P5CDF, k=-0.34

Log

conc

entra

tion

(pg/

g lip

id w

t)

2378-T4CDF, k=-0.22

12378-P5CDF, k=-0.52

0

2

4

6

8

Total PCBs, k=-0.45

Log

conc

entra

tion

(ng/

g lip

id w

t)p,p’-DDT, k=-0.73

-HCH, k=0.40

HBCDs PBDEs

PCDD/Fs Other POPs

Fig. 4. Linear regression between organohalogen concentrations and distance. The regression slope (k) is given with each line. The solid lines represent significant

correlation ( p < 0.05) of concentrations vs. distances and dashed lines a non-significant relationship ( p > 0.05). Symbols represent a single pool sample of five

fish.

(Table 2). This prevalence of a-HBCD has been observedin other aquatic biota samples including fish and marinemammals (Tomy et al., 2004; Morris et al., 2004; Janaket al., 2005). It was reported that b- and g-HBCD were sig-nificantly metabolized than a-HBCD in the microsomal prep-arations of seal liver (Zegers et al., 2005). Isomer-specificmetabolism might also be occurred in these specimens. Inthis study, b-HBCD was also detected in these samples.Few studies have reported the detection of b-HBCD in biota

samples (Morris et al., 2004; Janak et al., 2005). Our resultsindicate that b-HBCD should be considered as bioaccumula-tive isomer in the same manner as the a- and g-HBCDisomers.

In order to investigate the geographical distribution ofHBCD isomer profiles, percentage contributions of individualisomers were compared from south-to-north through the Asia-Pacific region (Fig. 3). This figure was plotted with Japan asthe source of this compound and the N-Pacific as northern

Table 4

Summary of 1/2 distances and liner regression of (log) concentrations versus distance for organohalogen compounds

Compounds n r2 p 1/2 distance (km) SE (km) Reference

a-HCH 5 0.83 0.03 �1700 480 Ueno et al., 2003

a-HBCD 4* 0.45 0.33 8500 6700 This study

g-HBCD 4* 0.73 0.15 1600 680 This studyPHBCD 4* 0.86 0.08 5300 1600 This study

BDE99 5 0.87 0.02 1400 320 Ueno et al., 2004a

BDE153 5 0.79 0.05 1200 380 Ueno et al., 2004a

2378-T4CDF 5 0.93 0.01 3200 530 Ueno et al., 2005

23478-P5CDF 5 0.87 0.02 2100 470 Ueno et al., 2005P

PCDFs 5 0.87 0.02 2000 440 Ueno et al., 2005

12378-P5CDD 5 0.91 0.01 1300 250 Ueno et al., 2005PPCDDs 5 0.93 0.01 1200 190 Ueno et al., 2005PPCBs 5 0.77 0.05 1500 480 Ueno et al., 2003

p,p0-DDT 5 0.91 0.01 950 170 Ueno et al., 2003P

DDTs 5 0.85 0.03 1100 280 Ueno et al., 2003

N-Pacific-1, off-Japan-1, off-Japan-2, E-China Sea-1 and off-Taiwan were used for calculation except where *N-Pacific-1, off-Japan-1, off-Japan-2 and E-China

Sea-1 were used for calculation. 1/2 distance (km) ¼ 1/slope � log(2); SE (km), standard deviation;P

HBCD, a þ b þ g-HBCD;P

DDTs, p,p0-DDT þ p,p0-DDE þ p,p0-DDD;

PPCDDs and

PPCDFs, sum of 2,3,7,8 substituted congeners;

PPCBs, sum of major congeners.

245D. Ueno et al. / Environmental Pollution 144 (2006) 238e247

remote region. As shown in Fig. 3, the percentage contributionof a-HBCD increased with increasing latitude and the highestratio was found in the sample from the northern cold-waterregion in N-Pacific-1. Correspondingly, the proportion ofg-HBCD decreased with increasing latitude (Fig. 3). A similartrend in isomer profiles was previously observed with theHCHs. A higher percentage of a-HCH, compared to b-HCHand g-HCH, was observed in skipjack tuna collected fromnorthern cold-water regions (Ueno et al., 2003), which couldbe the result of higher vapor pressure of a-HCH relative tob-HCH and g-HCH (reviewed by Wania and Mackay, 1996;Willett et al., 1998). To our knowledge, vapor pressures ofthe individual HBCD isomers have not been reported. a-HBCD may have a higher vapor pressure than b-HBCD andg-HBCD. As another possibility, longer environmental half-life and isomerization of this compound could be considered.Davis et al. (2004) reported relatively longer environmentalhalf-life of a-HBCD than g-HBCD in anaerobic sludge. Bio-isomerization from g-HBCD to a-HBCD has been reported inlaboratory experiment using juvenile rainbow trout (Law et al.,2004). Selective residue of a-HBCD and isomerization ofg-HBCD to a-HBCD may also occur during long-range trans-port through the atmosphere. These results indicate a-HBCDcould have the highest transportable nature among the isomersin the environment.

3.4. Transportability of HBCD and otherhalogenated POPs

Our data for skipjack tuna indicate that HBCD occurrenceis widespread in the global marine environment (Fig. 2). Thedistribution of HBCD was similar to the HCHs, which haveone of the highest mobility among POPs. In order to furtherassess the transportable nature of HBCD, empirical half-decline distances (1/2 distance) were calculated, and com-pared with other halogenated POPs measured in the sameskipjack tuna samples (Ueno et al., 2003, 2004a, 2005).These estimates were calculated using data from samplesrepresentative of areas impacted by local pollution sources(E-China-Sea-1, -2, off-Japan-1, and -2), and remote region(N-Pacific-1). The linear regressions between distance andconcentration were plotted in Fig. 4 (all slope and signifi-cance values are shown in Appendix A). Although the sam-ple numbers were relatively small, lower slopes (highertransportability) were found for HBCD, lower-brominated(3Br-) PBDEs, and a-HCH, compared to higher-brominatedPBDEs, PCDD/Fs and p,p0-DDT (lower transportability)(Fig. 4). The 1/2 distances were calculated using slope valuesof organohalogen compounds, and the compounds showedsignificant values were summarized in Table 4 (all valuesof 1/2 distance and related information are provided in Ap-pendix A). The 1/2 distance for a-HBCD was 8500 km,which is one of the highest values among organohalogencompounds. On the other hand, a-HCH showed opposite

slope (Fig. 4) and negative value of 1/2 distance(�1700 km) (Table 4). It indicated that concentrations ofthis compound were increased trend with increasing distance(much higher transportability).

Beyer et al. (2000) reported in a modeling study that sub-stances having greater 1/2 distances (CTD: characteristictravel distances) than 2000 km are frequently found in theArctic, and occasionally show an increase in concentrationsbetween the 50- and 70-degree latitudes. HBCD may havea potential to accumulate in remote northern cold-water re-gions through atmospheric transport.

4. Conclusion

The geographical distribution of HBCD was investigatedusing skipjack tuna collected from offshore waters of Asia-Pacific region. Elevated concentrations of HBCD were foundin the areas around Japan that have the larger modern indus-trial/urban societies. In addition, relatively higher concentra-tion of HBCD was found in northern cold-water remoteregion, and the estimated empirical 1/2 distance of thiscompound was 8500 km, which is one of the highest atmo-spheric transportability among various POPs. Further investi-gation of HBCD in cold-water remote regions (polar) wouldbe required.

Acknowledgements

The authors thank M. Williamson, C. Spencer, S. Batche-lor, S. Backus and G. Pacepavicius (National Water ResearchInstitute, Environment Canada) for technical support; A.Nihira (Ibaraki Prefectural Fisheries Experimental Station, Ja-pan), J. Takeuchi (Wakayama Research Center of Agriculture,Forestry and Fisheries, Japan), H. Tameishi (Japan FisheriesInformation Service Center, Japan), and I. Nakamura (KyotoUniversity, Japan) for provision of ecological informationon skipjack tuna; M. Nakamura and M. Takahashi (Hiraki-no-Takahashi, Co. Ltd., Japan) for collection of skipjacktuna from areas around Japan. This study was supportedpartly by Environment Canada, Ontario Ministry of Environ-ment, the ‘‘21st Century COE Program’’ from the Ministry ofEducation, Culture, Sports, Science and Technology of Japan,the ‘‘JapaneKorea Co-operative Joint Research Program onEndocrine Disrupting Chemicals’’ and the ‘‘Material CyclesModeling of Persistent Toxic Chemicals and its PolicyResearch Applications for Recycling and Waste Manage-ment’’ from the Waste Management Research Grants of theMinistry of the Environment, Japan, and Grant-in-Aid forScientific Research on Priority Areas (A) (Project No.16201014) and JSPS Research Fellowships for Young Scien-tists for D.U. from the Japan Society for the Promotion ofScience (JSPS).

Appendix A

The 1/2 distances and liner regression of (log) concentrations versus distance for organohalogen compounds

Compounds n r2 Slope (*1000-1) SE (slope) p 1/2 distance (km) SE (km) citation

a-HBCD 4* 0.45 -0.08 0.07 0.33 8400 6700 This studyb-HBCD 4* 0.68 -0.23 0.11 0.17 3000 1400 This studyg-HBCD 4* 0.73 -0.43 0.18 0.15 1600 680 This studyΣHBCD 4* 0.86 -0.13 0.04 0.08 5300 1600 This study

α-HCH 5 0.83 0.40 0.11 0.03 -1700 480 Ueno et al., 2003β-HCH 5 0.002 -0.002 0.07 0.98 350000 12000000 Ueno et al., 2003γ-HCH 5 0.08 0.10 0.19 0.65 -7100 14000 Ueno et al., 2003ΣHCHs 5 0.58 0.22 0.11 0.13 -3200 1600 Ueno et al., 2003

Oxychlordane 3** 0.06 0.03 0.14 0.84 -20000 84000 Ueno et al., 2003trans-chlordane 3** 0.34 -0.28 0.39 0.61 2500 3500 Ueno et al., 2003cis-chlordane 3** 0.31 -0.23 0.34 0.62 3000 4500 Ueno et al., 2003trans-nonachlor 3** 0.25 -0.24 0.41 0.66 2900 4900 Ueno et al., 2003cis-nonachlor 3** 0.58 -0.37 0.31 0.45 1900 1600 Ueno et al., 2003Σchlordanes 3** 0.31 -0.24 0.37 0.63 2900 4500 Ueno et al., 2003

p,p'-DDE 5 0.62 -0.45 0.20 0.11 1500 690 Ueno et al., 2003p,p'-DDD 5 0.75 -0.71 0.24 0.06 1000 330 Ueno et al., 2003p,p'-DDT 5 0.91 -0.73 0.13 0.01 950 170 Ueno et al., 2003ΣDDTs 5 0.85 -0.63 0.16 0.03 1100 280 Ueno et al., 2003

HCB 5 0.54 0.29 0.16 0.16 -2400 1300 Ueno et al., 2003

BDE15 5 0.03 0.17 0.55 0.78 -4100 13000 Ueno et al., 2004aBDE28 5 0.43 -0.12 0.08 0.23 5800 3700 Ueno et al., 2004aBDE47 5 0.74 -0.37 0.13 0.06 1900 660 Ueno et al., 2004aBDE100 5 0.69 -0.53 0.21 0.08 1300 528 Ueno et al., 2004aBDE99 5 0.87 -0.49 0.11 0.02 1400 320 Ueno et al., 2004aBDE154+U* 5 0.68 -0.52 0.21 0.09 1300 540 Ueno et al., 2004aBDE153 5 0.79 -0.56 0.17 0.05 1200 380 Ueno et al., 2004aBDE183 5 0.11 0.37 0.61 0.59 -1800 3100 Ueno et al., 2004aΣPe5BDEs 5 0.83 -0.51 0.14 0.03 1400 370 Ueno et al., 2004aΣHx6BDEs 5 0.71 -0.53 0.20 0.07 1300 490 Ueno et al., 2004aΣTe4+Pe5BDEs 5 0.78 -0.41 0.13 0.05 1700 540 Ueno et al., 2004aΣHx6+Hp7BDEs 5 0.71 -0.52 0.20 0.08 1300 510 Ueno et al., 2004aΣPBDEs 5 0.75 -0.43 0.14 0.06 1600 530 Ueno et al., 2004a

12378-Pe5CDD 5 0.91 -0.52 0.10 0.01 1300 250 Ueno et al., 2005ΣPCDDs 5 0.93 -0.58 0.09 0.01 1200 190 Ueno et al., 2005

2378-Te4CDF 5 0.93 -0.22 0.04 0.01 3200 530 Ueno et al., 200512378-Pe5CDF 5 0.73 -0.29 0.10 0.06 2400 820 Ueno et al., 200523478-Pe5CDF 5 0.87 -0.34 0.08 0.02 2100 470 Ueno et al., 2005123478-Hx6CDF 5 0.61 -0.35 0.16 0.12 2000 920 Ueno et al., 2005123678-Hx6CDF 5 0.74 -0.41 0.14 0.06 1700 580 Ueno et al., 2005234678-Hx6CDF 5 0.65 -0.46 0.19 0.10 1500 620 Ueno et al., 2005ΣPe5DFs 5 0.86 -0.33 0.08 0.02 2100 490 Ueno et al., 2005ΣHx6DFs 5 0.68 -0.41 0.17 0.09 1700 700 Ueno et al., 2005ΣPCDFs 5 0.87 -0.35 0.08 0.02 2000 440 Ueno et al., 2005

CB77 5 0.17 -0.11 0.14 0.49 6300 8000 Ueno et al., 2005CB81 5 0.65 -0.19 0.08 0.10 3700 1600 Ueno et al., 2005CB126 5 0.46 -0.24 0.15 0.21 2900 1800 Ueno et al., 2005CB169 5 0.52 -0.31 0.17 0.17 2200 1200 Ueno et al., 2005Σnon-ortho-Te4CBs 5 0.20 -0.11 0.13 0.45 6300 7400 Ueno et al., 2005Σnon-ortho-PCBs 5 0.39 -0.19 0.14 0.26 3700 2700 Ueno et al., 2005

CB105 5 0.59 -0.27 0.13 0.13 2600 1200 Ueno et al., 2005CB114 5 0.60 -0.29 0.14 0.13 2400 1200 Ueno et al., 2005CB118 5 0.60 -0.28 0.13 0.13 2500 1100 Ueno et al., 2005CB123 5 0.51 -0.25 0.15 0.18 2800 1700 Ueno et al., 2005CB156 5 0.63 -0.40 0.18 0.11 1700 780 Ueno et al., 2005CB157 5 0.58 -0.35 0.17 0.14 2000 960 Ueno et al., 2005CB167 5 0.61 -0.38 0.17 0.12 1700 820 Ueno et al., 2005CB189 5 0.61 -0.42 0.19 0.12 1700 740 Ueno et al., 2005Σmono-ortho-Pe5CBs 5 0.60 -0.28 0.13 0.13 2500 1100 Ueno et al., 2005Σmono-ortho-Hx6CBs 5 0.62 -0.39 0.18 0.12 1800 820 Ueno et al., 2005Σmono-ortho-PCBs 5 0.58 -0.29 0.14 0.13 2400 1200 Ueno et al., 2005

Σcoplaner-PCBs 5 0.60 -0.30 0.14 0.13 2300 1100 Ueno et al., 2005

ΣPCBs 5 0.77 -0.45 0.14 0.05 1500 480 Ueno et al., 2003

1/2 distanse (km) = 1/slope*log(2)N-Pacific-1, off-Japan-1, off-Japan-2, E-China Sea-1 and off-Taiwan were used for calculation.*: N-Pacific-1, off-Japan-1, off-Japan-2 and E-China Sea-1 were used for calculation.**: N-Pacific-1, off-Japan-1 and off-Japan-2 were used for calculation.SE (km): standard deviation

HBCD: a + b + g -HBCDPBDEs: sum of 8 congeners from di to heptacoplaner-PCBs: non-ortho -PCBs + mono-ortho -PCBsPCBs: sum of major congenersPCDDs and PCDFs: sum of 2,3,7,8 substituted congener concentrationsHCHs: a + b + g -HCHDDTs: p,p '-DDT + p,p '-DDE + p,p '-DDDCHLs: trans -chlordane + cis -chlordane + trans -nonachlor + cis -nonachlor + oxychlordane

HCB: hexachlorobenzene

247D. Ueno et al. / Environmental Pollution 144 (2006) 238e247

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