Deep-sea Fauna and Pollutants off Pacific Coast of Northern Japan, edited by T. Fujita, National Museum of Nature andScience Monographs, No. 39, pp. 737-755, 2009

Contamination by Persistent Organohalogen Compounds in Deep-sea Fishes
from off the Pacific Coast of Northern Japan
Shin Takahashi1*, Tomoko Oshihoi1, Tomohiko Isobe1, Karri Ramu1, Koji Ohmori1,
Tsunemi Kubodera2 and Shinsuke Tanabe1
1Center for Marine Environmental Studies, Ehime University,
Bunkyo-cho 2 5, Matsuyama, Ehime, 790 8577 Japan
E-mail: shint@agr.ehime-u.ac.jp
2
Department of Zoology, National Museum of Nature and Science,
3 23 1 Hyakunin-cho, Shinjuku-ku, Tokyo, 169 0073 Japan

Abstract: Twelve species of deep-sea fishes collected in 2005 from off the Pacific coast of northern Japan
from depths ranging from 400 1000 m were analyzed for persistent organochlorine compounds (OCs), including PCBs and organochlorine pesticides and brominated flame retardants (BFRs) such as polybrominated diphenyl ethers (PBDEs) and hexabromocyclododecane isomers (HBCDs). Among OCs, concentrations of
DDTs and PCBs (up to 23000 and 12400 ng/g lipid wt, respectively) were the highest and other OCs wereapproximately in the order of CHLs > HCHs ≥ HCB. PBDEs and HBCDs were also detected in almost all the
deep-sea fishes. The present study is the foremost to report the occurrence of BFRs in deep-sea fishes from theNorth Pacific region. Although magnitude of contamination by these organohalogen compounds in most of the
fish species analyzed was comparable or lower than that reported in shallow-water and deep-sea fishes fromJapanese coastal waters, snubnosed eels accumulated some hydrophobic compounds like PCBs, DDTs and
PBDEs at extremely high concentrations. Significant positive correlations found between δ15N (‰) and PCBs,
DDTs and PBDEs suggest the high biomagnification potential of these contaminants in food web. Nevertheless, large variation in δ13C (‰) values observed between the species indicate multiple sources of carbon in thefood web and specific accumulation of hydrophobic organohalogen compounds in benthic dwelling species
like snubnosed eel. It is noteworthy that no significant declining trends of PCBs, HCB and HCHs levels wereobserved in fishes collected in 1995 and 2005, suggesting continuous input of the contaminants into the environment. The results obtained in this study highlight the usefulness of deep-sea fishes as sentinel species tomonitor the deep-sea environment.
Key words: organochlorines, brominated flame retardants, stable isotopes, deep-sea fishes, Tohoku region

Introduction
The long-range transport, persistence, and global dynamics of persistent organic pollutants(POPs) are issues of increasing concern in recent years. Organochlorine compounds (OCs), a representative group of classical POPs, are ubiquitous contaminants entering the marine environment
in coastal areas, mainly by river inflow and continental runoff and in the open sea by atmosphericdeposition. In the global marine environment, the apparent fate of these compounds is to adsorb to
the detritus and marine snow and eventually carried to the deep-sea where they biomagnify in thefood web (Froescheis et al., 2000). Several models suggested that deep-sea sediments are the final
accumulation site for OCs (Woodwell et al., 1971; Tatsukawa and Tanabe, 1984), and fish livingin association with sediments are exposed to and accumulate these compounds (Berg et al., 1997).
Increasing concern that the deep-sea might act as an ultimate sink for such contaminants and thegrowing importance of deep-sea commercial fisheries around the world have resulted in numerous＊

To whom correspondence should be addressed.

738

Shin Takahashi et al.

monitoring studies on the accumulation of OCs in deep-sea organisms (Berg et al., 1997, 1998;
Lee et al., 1997; Takahashi et al., 1998, 2000, 2001; Looser et al., 2000; Froescheis et al., 2000;
Sole et al., 2001; de Brito et al., 2002a; Mormede and Davies, 2003; Storelli et al., 2004). Although our previous study also found significant levels of OC contaminants in some deep-sea organisms collected from off the Pacific coast of northern Japan, during 1994-1995 (de Brito et al.,2002a), no recent information is available on the contamination status of OCs in the ecosystem ofthis region.
In addition to OC contamination, aquatic pollution resulting from widespread usage of brominated flame retardants (BFRs) such as polybrominated diphenyl ethers (PBDEs) and hexabromocyclododecanes (HBCDs) deserves concern because of the bioaccumulation potential, persistence and endocrine disrupting effects of the contaminants (Watanabe and Sakai, 2003, Tanabe etal., 2008). Therefore, these compounds have been recently reported as emerging global environmental contaminants. Nevertheless, compared to OCs, there is still little information on contamination by BFRs in the Asia-Pacific region, and studies addressing the contamination of deep-sea
areas by BFRs are scarce (Ramu et al., 2006).
Concerned over the possible flux of such persistent organohalogen contaminants to the bottom of the oceans, the present study attempted to investigate the contamination and accumulationof OCs, such as polychlorinated biphenyls (PCBs), DDT and its metabolites (DDTs), chlordanerelated compounds (CHLs), hexachlorocyclohexane isomers (HCHs) and hexachlorobenzene(HCB), and BFRs such as PBDEs and HBCDs, in deep-sea fishes from off the Pacific coast ofnorthern Japan (Tohoku region). Additionally, the data on OCs in deep-sea fishes reported in ourearlier study (de Brito et al., 2002a) were compared with that observed in this study to delineate
the temporal trend of OCs contamination during the last decade from 1994/95 to 2005.
Stable isotope analysis is generally used to investigate energy flow through an ecosystem.
The δ15N and δ13C values in animals reflect their diets. Thus, trophic relationships can successfully
be derived using relative abundances of naturally occurring stable isotopes of nitrogen (15N/14N,
expressed as δ15N values) (Hobson and Welch, 1992). Furthermore, measurements of δ15N as acontinuous trophic-level variable enable to quantitatively estimate the magnitude of contaminantbiomagnification within food webs (Ruus et al., 2002). Hence, to examine the biomagnification of
OCs and BFRs through the deep-sea food web, δ15N and δ13C analyses were performed on deepsea fishes from off the Pacific coast of northern Japan.
The present study was conducted as part of a joint research project entitled “Study on DeepSea Fauna and Conservation of Deep-Sea Ecosystem” between the Department of Zoology, National Museum of Nature and Science and Center for Marine Environmental Studies, Ehime University.
Materials and Methods
SamplesTwelve species of deep-sea fishes collected from off the Pacific coast of northern Japan(36 38˚N, 141 142˚E) from depths ranging from 400 to 1000 m during October to November 2005
were analyzed in this study. The fish samples were collected by the R/V Wakataka-maru of theFisheries Research Agency (FRA) using a research bottom trawl. Sampling location and biologicalinformation of the samples are shown in Fig. 1 and Table 1, respectively. The collected samples
were placed in polyethylene bags and frozen in a deep-freezer at 25˚C until chemical analysis.
The whole body of individual specimens belonging to the same species collected from the same
sampling location were pooled and homogenized to prepare a composite sample for chemical
analysis.

739

Contaminants in Deep-sea Fishes from off Tohoku

Table 1. Sample details of deep-sea fishes from off the Pacific coast of northern Japan. n.m: not measured.
Sample No.

Common nameScientific namenSampling
year

Depth
Mean
Mean
(m) length (cm) weight (g)Fish-1Fish-2
Fish-3Fish-4Fish-5Fish-6
Fish-7
Fish-8Fish-9Fish-10
Fish-11
Fish-12
Fish-13
Fish-14
Fish-15
Fish-16
Fish-17
Fish-18
Fish-19
Fish-20

Flathead flounder
Flathead flounderLongfin codlingKaup’s arrowtooth eel
Kaup’s arrowtooth eel
Kaup’s arrowtooth eel
Spinyhead sculpin
Snubnosed eel
Snubnosed eel
Snubnosed eel
Snubnosed eel
Sake-bikunin
Longarm grenadierLongarm grenadierLargenose grenadierBlackbelly lanternshark
Pacific cod
Pacific cod
Eelpout
Brokenline laternfish

Hippoglossoides dubius
Hippoglossoides dubius
Laemonema longipes
Synaphobranchus kaupii
Synaphobranchus kaupii
Synaphobranchus kaupii
Dasycottus setiger
Simenchelys parasitica
Simenchelys parasitica
Simenchelys parasitica
Simenchelys parasitica
Careproctus rastrinus
Coelorinchus macrochir
Coelorinchus macrochir
Coryphaenoides nasutus
Etmopterus lucifer
Gadus macrocephalus
Gadus macrocephalus
Lycodes hubbsi
Lampanyctus jordani

1
1
1
1
1
1
1
1
1
1
1
2
1
1
5
3
1
1
2
14

2005
2005
2005
2005
2005
2005
2005
2005
2005
2005
2005
2005
2005
2005
2005
2005
2005
2005
2005
2005

650
650
650
550
550
550
450
900
900
900
900
425
410
410
900
480
450
450
750
480

37
36
47
67
61
69
26
44
41
36
38
n.m
59
59
31
50
39
38
38
13

610
500
500
450
290
610
290
140
100
65
100
160
620
720
71
230
610
760
130
17

HabitatDemersal
Demersal
Bathydemersal
Bathydemersal
Bathydemersal
Bathydemersal
Demersal
Bathydemersal
Bathydemersal
Bathydemersal
Bathydemersal
Bathydemersal
Bathydemersal
Bathydemersal
Bathydemersal
Benthopelagic
Demersal
Demersal
Bathydemersal
Bathypelagic

Fig. 1. Map showing the sampling area (shaded portion) off the Pacific coast of northern Japan (Tohoku region).

740

Shin Takahashi et al.

Chemical analysis
Analysis of PBDEs and HBCDs was performed following the procedures described by Ueno
et al. (2004, 2006) with slight modifications, while OCs such as DDTs, CHLs, HCHs, HCB, and
PCBs were analyzed following the method described by Kajiwara et al. (2003).
Briefly, 15 30 g of the homogenized tissue sample was ground with anhydrous sodium sulfate
and extracted in a Soxhlet apparatus with a mixture of diethyl ether and hexane for 7 8 h. An aliquot of the extract, after spiking 5 ng of internal standards for PBDEs (13C12-labeled BDE-3, BDE15, BDE-28, BDE-47, BDE-99, BDE-153, BDE-154, BDE-183, BDE-197, BDE-207 and BDE209) and 10 ng of internal standards for HBCDs (13C12-labeled α-, β- and γ-HBCD), was added toa gel permeation chromatography column (GPC) for lipid removal. The GPC fraction containing
organohalogens was concentrated and passed through 4 g of activated silica gel (Wakogel DX,
Wako Pure Chemical Industries Ltd., Japan) column. The first fraction eluted with 5% dichloromethane in hexane for cleanup contained PBDEs, while the second fraction eluted with 25%
dichloromethane in hexane contained HBCDs. 13C12-labled BDE-139 was added to the final first
fraction solution prior to GC-MS analysis for PBDEs. Quantification was performed using a GC
(Agilent 6890N) equipped with MS (Agilent 5973N) for mono- to hepta-BDEs, and GC coupledwith MS (JEOL GCmate II) for octa- to deca-BDEs, using electron ionization with selective ion
monitoring (EI-SIM) mode. GC columns used for quantification were DB-1 fused silica capillary(J&W Scientific Inc.) having 30 m x 0.25 mm i.d. x 0.25 μm film thickness for mono- to heptaBDEs, and 15 m x 0.25 mm i.d. x 0.1 μm film thickness for octa- to deca-BDEs. Fourteen majorcongeners of PBDEs (BDE-3, BDE-15, BDE-28, BDE-47, BDE-99, BDE-100, BDE-153, BDE154, BDE-183, BDE-196, BDE-197, BDE-206, BDE-207 and BDE-209) were quantified in thisstudy. All the congeners were quantified using the isotope dilution method to the corresponding
13
C12-labeled congener. Recovery of 13C12-labeled BDE ranged between 60 and 120%.
The fraction containing HBCDs was solvent exchanged into methanol and 10 ng of d18-labeled α-, β- and γ-HBCD was added to the final solution prior to liquid chromatography combinedwith tandem mass spectrometry (LC-MS-MS) analysis as a performance standard. The diastereomeric analysis of HBCDs was performed on the basis of an analytical method reported by Tomy etal. (2004). Samples were analyzed with Quattro Micro API triple-quadrupole mass spectrometer(Waters/Micromass, Tokyo, Japan) equipped with Alliance 2795 LC separation module (Waters,
Tokyo, Japan). Separation of HBCD isomers (α-, β- and γ-) was achieved with an Extend-C18 column (2.1 mm i.d. x 150 mm, 5 μm particle size). The mobile phase consisted of water/acetonitrile/methanol (20:30:50) at 200 μL/min in initial condition for 2 min and then ramped to acetonitrile/methanol (30:70) in 5 min, and this was then maintained for 6 min. The MS-MS analysis, which
was operated in negative mode of electrospray ionization (ESI), was performed in multiple reaction monitoring mode (MRM). Quantification of native HBCDs was achieved from mean value ofthe response of two MRM transitions (i.e., m/z 640 > 81, m/z 642 > 81) corrected with response of
13
C12-HBCDs (i.e., m/z 652 > 81 MRM transition). HBCD isomers were quantified by isotope dilution using the corresponding 13C12-labeled isomers. Recoveries of 13C12-labeled HBCDs during
analytical procedure were determined using d18-labeled isomers and the values ranged between
60% and 120%.
For analysis of OCs an aliquot of the extract was subjected to GPC for lipid removal. The
GPC fraction containing OCs was concentrated and passed through an activated Florisil column
for clean-up and fractionation. Quantification of PCBs and most of the organochlorine pesticides
was performed using a GC equipped with a microelectron capture detector (micro-ECD) and anauto-injection system (Agilent 7683 Series Injector). The GC column used for OC analysis was afused silica capillary (DB-1; 30 m x 0.25 mm i.d. x 0.25 μm film thickness, J&W Scientific Inc.).
The concentration of individual OCs was quantified from the peak area of the sample to that of theContaminants in Deep-sea Fishes from off Tohoku

741

corresponding external standard. The PCB standard used for quantification was a mixture of 62
PCB isomers and congeners (BP-MS) obtained from Wellington Laboratories Inc., Ontario, Canada. Concentrations of individually resolved peaks of PCB isomers and congeners were summed
to obtain total PCB concentrations.
Procedural blanks were analyzed simultaneously with every batch of five samples to checkfor interferences or contamination from solvents and glassware. Lipid contents were determinedby measuring the total nonvolatile solvent extractable material on subsamples taken from the original extracts. The concentrations of organohalogens are expressed on lipid weight basis unlessotherwise specified.
Stable isotope analysis
Sub-samples from the homogenized samples were dried for 24 hours at 60˚C and ground into
powder with a mortar and pestle. The solvent-extractable lipid fraction was removed from thesubsample by extraction with a mixture of chloroform: methanol (2:1), and the lipid free residues
were centrifuged using micro-tubes and dried at room temperature and later at 60˚C for 24 hours.
One mg powder subsamples were packed into 4 x 6 mm tin capsules for stable isotope measurements. Stable isotopes were measured using ANCA-SL mass spectrometer (PDZ Europa Ltd.).
Isotope ratios of carbon (δ13C) and nitrogen (δ15N) are expressed as the deviation from standards inparts per thousand (‰) according to the following equation:
δ13C, δ15N = [(Rsample/Rstandard)-1] X 1000 (‰)
where R = 13C/12C or 15N/14N. Pee Dee Belemnite (PDB) limestone carbonate and atmospheric nitrogen (N2) were used as standards for carbon and nitrogen isotope ratios, respectively.
Results and Discussion
Contamination status of OCs
Concentrations of organohalogen compounds in deep-sea fishes from off the Pacific coast ofnorthern Japan are shown in Table 2. Although concentrations of organohalogen compounds varied among the species, concentrations of PCBs and DDTs were the highest among the OCs analyzed, and other compounds were approximately in the order of CHLs > HCHs ≥ HCB. The predominance of DDTs and PCBs in the fishes analyzed in this study is similar to that in deep-seaorganisms from Suruga Bay, Japan (Lee et al., 1997); Tosa Bay, Japan (Takahashi et al., 2001),
western North Pacific, off-Tohoku, Japan (de Brito et al., 2002a), the East China Sea (Tanabe etal., 2005) and the Sulu Sea (Ramu et al., 2006). This may be due to the higher bioaccumulative
properties and the continuous input of these compounds into the environment.
Concentrations of OCs such as PCBs and DDTs in deep-sea fishes from off the Pacific coastof northern Japan were lower than those in deep-sea fishes from the Atlantic Ocean (Meith-Avcin
et al., 1973; Harvey et al., 1974; Barber and Warlen, 1979; Krämer et al., 1984; Looser et al.,
2000; Froescheis et al., 2000), Gulf of Mexico (Baird et al., 1975), US coasts (Stegeman et al.,
1986; Melzian et al., 1987) and the Arctic region (Hargrave et al., 1992; Berg et al., 1997, 1998;
Mormede and Davies, 2003) (Table 3). The relatively low contamination by OCs in the present
study area might be due to the less usage of these compounds in this region compared to that in the
Atlantic countries. In addition to this, decreasing trends of OCs have been noticed globally in recent years in the marine environment even in the deep-sea, as evidenced in the Atlantic Ocean
between the 1970s and 1992. The samples analyzed in the present study were collected in 2005 andfactors like variations in analytical methods and fish species compared between the studies mayFish-1
Fish-2
Fish-3Fish-4Fish-5Fish-6
Fish-7
Fish-8Fish-9Fish-10
Fish-11
Fish-12
Fish-13
Fish-14
Fish-15
Fish-16
Fish-17
Fish-18
Fish-19
Fish-20

Flathead flounder
Flathead flounderLongfin codlingKaup’s arrowtooth eel
Kaup’s arrowtooth eel
Kaup’s arrowtooth eel
Spinyhead sculpin
Snubnosed eel
Snubnosed eel
Snubnosed eel
Snubnosed eel
Sake-bikunin
Longarm grenadierLongarm grenadierLargenose grenadierBlackbelly lanternshark
Pacific cod
Pacific cod
Eelpout
Brokenline laternfish

Sample No. Common name

Hippoglossoides dubius
Hippoglossoides dubius
Laemonema longipes
Synaphobranchuskaupii
Synaphobranchuskaupii
Synaphobranchuskaupii
Dasycottus setiger
Simenchelys parasitica
Simenchelys parasitica
Simenchelys parasitica
Simenchelys parasitica
Careproctus rastrinus
Coelorinchus macrochir
Coelorinchus macrochir
Coryphaenoides nasutus
Etmopterus lucifer
Gadus macrocephalus
Gadus macrocephalus
Lycodes hubbsi
Lampanyctus jordani

Scientific name
5.7
5.4
7.4
22
20
25
1.4
15
8.6
8.9
18
1.2
7.5
9.3
3.8
13
2.5
2.8
2.2
11

Fat (%)
82
70
150
120
290
100
390
8800
2300
12400
1500
189
120
90
140
170
36
73
390
34

PCB
74
82
120
130
97
36
220
16000
4700
23000
2600
200
110
110
120
120
68
120
180
47

DDTs
39
32
120
56
100
38
77
1900
580
2500
270
83
51
44
19
47
29
47
55
21

CHLs

HCB
18
14
16
15
21
24
21
43
13
25
22
37
15
29
45
15
18
21
13
6.9

17
16
16
46
32
22
69
5.7
13
5.7
12
19
40
19
13
5.2
20
23
16
33

HCHs
3.7
3.2
3.5
1.8
2.1
1.9
4.6
24
21
53
12
4.1
2.6
2.1
1.9
3.9
5.8
8.5
6.2
1.3

PBDEs
34
11
22
24
32
18
31
24
38
110
57
45
26
22
5.4
18
< 0.05< 0.05
13
12

HBCDs

Table 2. Concentrations of organohalogen compounds (ng/g lipid wt), δ15N and δ13C in deep-sea fishes from off the Pacific coast of northern Japan. n.a.: not analyzed.

13.17
11.49
12.17
11.53
11.55
11.69
13.64
13.99
14.33
13.86
14.61
12.03
12.02
11.51
12.82
13.06
13.97
13.26
14.77
n.a.

δ15N

17.91
19.23
19.39
22.53
19.92
20.12
17.44
21.24
19.03
19.70
19.50
18.42
20.15
19.62
18.17
19.10
18.80
18.70
16.86
n.a.

δ13C

742
Shin Takahashi et al.

Snubnosed eel
Fish (11 spp.)
Chauliodontidae
Stenophoridae
Gonostanomiae
Blue hake(Antimora rostrata)
Mesopelagic fish
Black Scabbard
Rattail(Coryphaenoides armatus)
Dover sole
(Microstomus pacificus)(Anoplopoma fimbria)
Glacial eelpout
Cartilagenous fish (2 spp.)
Bony fish (6 spp.)
Fish (6 spp.)
Cartilagenous fish (1 spp.)
Bony fish (3 spp.)
Armed grenadierBlack halibut
Kingclip
Dover soleLongspine thornyhead
Fish (20 spp.)
Snubnosed eel
Fish (21 spp.)
Skate
Ghostshark
Roundnose grenadierRoundnose grenadierFish (37 spp.)
Fish (10 spp.)

Species

2005
2005
1970-72
1972
1972
1972
1972-74
1973
—
—
—
1985
1985
1985
1983
1992
1992
1993-94
1992
1992
1992
1994-98
1994-98
1995
1995
1997-98
1995
1995
2000
2000
1999
1999
2001-03
2002

Sampling
Year

Northern Japan (off Tohoku)
Northern Japan (off Tohoku)
North & South Atlantic
North & South Atlantic
North & South Atlantic
Atlantic (Cape Hatteras)
Atlantic (Cape Hatteras)
Gulf of Mexico
Atlantic (Madeira Is.)
Hudson Canyon
Carson Canyon
Farallon Is.
off California
off California
off California
Davis Strait (Greenland)
Davis Strait (Greenland)
Suruga Bay, Japan
Norway (Nordfjord)
Norway (Nordfjord)
North Atlantic
North Atlantic
South AtlanticMonterey Bay Canyon
Monterey Bay Canyon
Tosa Bay, Japan
Northern Japan (off Tohoku)
Northern Japan (off Tohoku)
Southern Adriatic Sea
Southern Adriatic Sea
West of IrelandWest of Ireland
East China Sea
Sulu Sea

Location

400-1000
400-1000
450-900
130-660510-660
2500
2501
0-760
800-1200
3200
1700-2300
500
1000
1000
1001
800-2200
200-2100
200-740
400
400
2900
—
—
—
—
150-4001000
150-1300
—
—
1000
2000
89-512292-1015

(m)

Depth

720
12
26
33
70
—
—
200
—
2700
360
830
980
7000
—
310
300
160
1800
3900
—
—
—
—
—
39
1100
81
—
—
450
800
6.2
0.59

wet wt

PCBs (ng/g)

6300
150
3000
2200
15000
—
—
13000
5800
—
—
11000
12000
56000
2300
430
790
1000
2400
8700
2100
1000
1400
2200
3700
350
6700
400
890
387
770
1900
230
58

lipid wt
1300
8.2
6.2
8.3
14
5400
6900
19
—
—
—
760
2300
8700
—
490
250
60
4600
8800
—
—
—
—
—
31
2100
30
—
—
730
1000
30
1.8

wet wtDDTs (ng/g)

Table 3. Comparison of mean concentrations of PCBs and DDTs in deep-sea fishes from various parts of the world. — : not available.

12000
100
760
480
4300
—
—
2000
9200
—
—
11000
22000
74000
1500
690
670
390
6000
20000
1090
390
190
2400
2400
290
13000
220
—
—
1300
2400
700
150

lipid wt
This study
This study
Harvey et al. (1974)
Harvey et al. (1974)
Harvey et al. (1974)
Meith-Avcin et al. (1973)
Barber and Warlen (1979)
Baird et al. (1975)
Krämer et al. (1984)
Stegeman et al. (1986)
Stegeman et al. (1986)
Melzian et al. (1987)
Melzian et al. (1987)
Melzian et al. (1987)
Melzian et al. (1987)
Berg et al. (1997)
Berg et al. (1997)
Lee et al. (1997)
Berg et al. (1998)
Berg et al. (1998)
Looser et al. (2000)
Froescheis et al. (2000)
Froescheis et al. (2000)
Froescheis et al. (2000)
Froescheis et al. (2000)
Takahashi et al. (2001)
de Brito et al. (2002)de Brito et al. (2002)
Storelli et al. (2004)
Storelli et al. (2004)
Mormede and Davies (2003)
Mormede and Davies (2003)
Tanabe et al. (2005)
Ramu et al. (2006)

ReferenceContaminants in Deep-sea Fishes from off Tohoku

743

744

Shin Takahashi et al.

also influence the differences in the OC levels.
To understand the current status of OCs pollution in deep-sea fishes from off the Pacific coastof northern Japan residue levels found in the present study were compared the with studies on
deep-sea fishes in adjoining areas carried out by our group (Table 4). Except for snubnosed eels
(Simenchelys parasitica), which contained some OCs at extremely high concentrations, the concentrations of PCBs, DDTs, CHLs and HCB in deep-sea fishes collected from off the Pacific coastof northern Japan were comparable or lower than the data so far reported in our related studies in
the western North Pacific region (Lee et al., 1997; Takahashi et al., 1998, 2000, 2001; de Brito etal., 2002a) and the East China Sea (Tanabe et al., 2005). It was noted that PCBs used in electricalequipment are continuously released into the environment (Hirai et al., 2003). In Japan, CHLs
were used largely as a termiticide until 1986. Higher levels of PCBs and CHLs found in fishes
from other locations such as Suruga Bay were due to their proximity to urban cities with more
intensive human activities. In addition, large scale use of DDT in agricultural practices and thesubsequent runoff in the waterways have resulted in their accumulation in the freshwater, estuarine
and marine environment of China (Yuan et al., 2001). This might explain the reason for the elevated levels of DDT observed in deep-sea fishes from the East China Sea. On the other hand, concentrations of HCHs in deep-sea fishes from off the Pacific coast of northern Japan were higher thanthose from other locations along the warm Kuroshio Current. Higher concentrations of HCHs in
cold waters along the Oyashio Current than other offshore waters around Japan were also observedin a monitoring study using skipjack tuna (Katsuwonus pelamis) (Ueno et al., 2003). Due to highvapor pressure, HCHs are known to rapidly evaporate and be transported from their pollution
Table 4. Comparison of mean and range concentrations of organochlorines (ng/g lipid wt) between fishes from the western
North Pacific and East China Sea. Figures in parentheses indicate the range of concentrations. n.d.: not detected (forcalculation of mean, n.d. was assumed to be 0). *Data without snubnosed eel.
Location
Northern Japan (off Tohoku)
Deep-sea fish*Tosa Bay
Shallow-water fish
Deep-sea fish

Suruga Bay
Shallow-water fish
Deep-sea fish

Northern Japan (off Tohoku)
Deep-sea fish*

East China Sea
Shallow-water fish
Deep-sea fish

PCBs

DDTs

CHLs

HCHs

150
(n.d. 2200)

110(14 830)54(3.9 640)

25(n.d. 150)

21This study(n.d. 100)

310
(n.d. 1100)
340(n.d. 1600)

220(38 1200)290(7.1 1200)

46(n.d. 200)44
(5.6 220)5.3(n.d. 14)
11
(n.d. 21)5.7
(n.d. 13)
11
(n.d. 61)

Takahashi et al. (2001)

1600(540 2600)
1000(450 1900)

390(80 1700)
390(51 910)140(46 320)260(69 770)

4.1(n.d. 8.0)
25
(10 37)8.8(3.7-24)
20(9.9 50)

Lee et al. (1997)

420(n.d. 2200)

230(14 830)110(3.9 640)30(n.d. 150)

16
de Brito et al. (2002)(n.d. 100)39
(5.9 180)40(3.7 240)11(2.2 62)11(1.4 41)

17
Tanabe et al. (2005)(<n.d. 70)
18
Tanabe et al. (2005)(1.7 290)

150
330(20 830) (110 1200)
230
720(36 1400) (<n.d. 7900)

HCB

Reference

Takahashi et al. (2001)

Lee et al. (1997)

Contaminants in Deep-sea Fishes from off Tohoku

745

sources in the tropics and temperate regions to colder regions via the atmosphere (Iwata et al.,
1993; Wania and Mackay 1996; Beyer et al., 2000). The distribution patterns of HCHs found in thebiota reflect such highly transportable nature of HCHs and its accumulation in the cold water current of the western North Pacific. Considering the above, the contamination status of OCs in deepsea fishes analyzed in this study seems to reflect typical magnitude of OCs pollution in open water
ecosystems of the western North Pacific.
Contamination status of BFRs
Polybrominated diphenyl ethers which are one of the most commonly used flame retardants
were detected in all the deep-sea fishes from off the Pacific coast of northern Japan (Table 2). The
present study is the foremost to report the occurrence of PBDEs in deep-sea fishes from the North
Pacific region. The concentrations of PBDEs (ranged from 1.3 to 8.5 ng/g with mean 3.6 ng/g
lipid wt) in deep-sea fishes (except for snubnosed eels) from this region were lower than the levels
reported for marine fish from Japanese coastal waters (Akutsu et al., 2001), various species of fishfrom the Belgian North Sea (Voorspoels et al., 2003) and coastal fishes from Florida (JohnsonRestrepo et al., 2005), but comparable to those found in skipjack tuna from offshore waters of theNorth Pacific (Ueno et al., 2004) and higher than the levels in deep-sea fishes from Sulu Sea(Ramu et al., 2006). Despite the low levels of PBDEs found in offshore waters, the detection ofthese compounds in deep-sea fishes confirms that PBDEs, like the classical POPs, are transportable to the deep oceans and, thus, can cause global environmental contamination.
In addition to PBDEs, HBCDs were detected in almost all the deep-sea fishes analyzed in thisstudy. To our knowledge, this is the first report on the detection of HBCDs in deep-sea biota. This
result again indicates the widespread presence of such ‘emerging POPs’ even in deep oceans. The
concentrations of HBCDs (ranged from 5.4 to 45 ng/g with mean 22 ng/g lipid wt) in deep-sea
fishes (except for snubnosed eels) from this region were lower than those in fish collected from theNorth Sea (Morris et al., 2004) and the Scheldt estuary in the Netherlands (Janak et al., 2005), but
comparable to those found in skipjack tuna from offshore waters around Japan (Ueno et al., 2006).
On the other hand, concentrations of HBCDs in deep-sea fishes were higher than those of PBDEs(Table 2). Higher concentrations of HBCDs than PBDEs were also observed in skipjack tuna collected from offshore waters around Japan (Ueno et al., 2004, 2006). Increasing levels of HBCDs,
which appear to exceed those of PBDEs in recent years, were noted in recent studies on temporal
trends of BFRs contamination in marine mammals stranded and collected around Japanese coastal
waters (Tanabe et al., 2008). In Japan, consumption of HBCDs increased continuously from around
600 tons in 1986 to 2200 tons in 2001, while the use of PentaBDE and OctaBDE was withdrawn
from the Japanese market in 1991 and 2000, respectively (Watanabe and Sakai, 2003). Considering the remarkable increase in market demand for HBCDs in Japan, it can be anticipated that
contamination by HBCDs in marine ecosystems around Japan may further increase because, unlike PBDEs, HBCDs are currently not regulated.
Species-specific accumulation of organohalogen compounds
It has been well demonstrated that gill-breathing organisms exchange OCs through the gills
and equilibrate the levels between ambient water and body lipids (Clayton et al., 1977; Tanabe etal., 1984). In this study, concentrations of OCs and BFRs (wet wt basis) in deep-sea fishes (except
for snubnosed eels) were significantly correlated with their body lipid content, but considerable
variation between the species was observed even in the concentrations of OCs and BFRs on lipid
weight basis. Particularly, snubnosed eel accumulated hydrophobic organohalogens (with log Kow
ca. 6 to 8) such as PCBs, DDTs, CHLs and PBDEs at extremely high concentrations (Table 2).
This is quite similar to the results found in our previous study on OCs in snubnosed eel (de Brito

746

Shin Takahashi et al.

et al., 2002a). This species can be considered as an organism at a high trophic level in the food web
due to its strong carnivorous and unique feeding habit; this fish has been found to burrow into thebody of large fish such as halibut and shark and feed on their intestine and blood (Caira et al.,1997). Relatively higher concentrations of the hydrophobic OCs and PBDEs were also found inlarge carnivore and/or bottom dwelling fishes (e.g., blackbelly lanternshark (Etmopterus lucifer),
eelpout (Lycodes hubbsi) and Kaup’s arrowtooth eel (Synaphobranchus kaupii)) (Table 2). Theseobservations suggest that accumulation of these contaminants is influenced by biomagnification
and/or feeding habits of organisms and their long biological half-lives, i.e., higher uptake rate via
food and slower equilibrium between ambient water and body lipids. In contrast, less lipophiliccompounds (with log Kow less than 6), HCHs, HCB and HBCDs, showed smaller variation in concentrations among species of different trophic levels and feeding habits, owing to their faster rates
of attaining equilibrium water concentrations (Ellgehausen et al., 1980; Tanabe et al., 1984; Kelly
et al., 2007). In addition to the difference in physico-chemical properties of the compounds, differing rates of uptake and elimination which are dependent on biological factors, like respiration rate,
lipid composition and metabolic activities of the organism, may influence the accumulation patternof organic contaminants in organisms. Importance of these factors should be examined in futurestudies incorporating experiments and statistical models, including various biological processes
for bioaccumulation/biomagnification (Kelly et al., 2007) as well as further field monitoring ofvarious organohalogen compounds in marine ecosystems.
Food web structure and biomagnification of organohalogen compounds
Increase in contaminant concentrations in a marine food web is difficult to assess because thepredators diet often consists of prey organisms from different trophic levels and also depend on theavailability of prey organisms. Hence, for further discussion of the biomagnification of organohalogen compounds, δ15N and δ13C analyses were performed on deep-sea fishes collected in thisstudy to understand their general trophic level and differences in feeding habits. Fig. 2 shows theδ13C and δ15N map of deep-sea fishes from off the Pacific coast of northern Japan. The stable isotope ratios of nitrogen δ15N reflect the trophic level of organisms in a food web (Hobson andWelch, 1992) and, thus, δ15N analysis is often used to assess trophic transfer of contaminants (Fisk

Fig. 2. The food-web of deep-sea fishes on the δ13C-δ15N map.

Contaminants in Deep-sea Fishes from off Tohoku

747

et al., 2001; Das et al., 2003; Kelly et al., 2007). It has been assumed that an increase in δ15N
value of ca. 3.8 with δ13C value of ca. 1.0 corresponds to one trophic level (Hobson and Welch,
1992; Fisk et al., 2001). Although an eelpout and snubnosed eels showed relatively high δ15N values, the maximum difference of δ15N values between the fishes analyzed in this study was only 3.4.
This implies that almost all the fishes are included within one trophic level, and snubnosed eels inthis region probably do not prey upon higher trophic animals like shark and halibut.
On the other hand, large variation in δ13C values was observed among the deep-sea fishes(Fig. 2). The stable isotope ratios of δ13C are varied due to different carbon sources. For example,
organisms dependent on primary production from phytoplankton in offshore surface waters can be
expected to have higher δ13C values than those living in coastal regions affected by fresh water
inputs (Michener and Schell, 1994). Fry and Wainright (1991) demonstrated that diatoms can be asource of 13C-rich carbon in many marine food webs. In Fig. 2, snubnosed eels and one Kaup’s
arrowtooth eel appear to be outliers. A significant positive correlation was found between δ15N andδ13C in deep-sea fishes when the data of snubnosed eels and one Kaup’s arrowtooth eel were excluded (p < 0.01, Speaman’s rank order correlation test). However, a wide range of δ13C values(more than ca. 1.0) between fishes was observed even after the exclusion of outliers, implying theexistence of multiple carbon sources in the food web of this region. Although there are still unclear
factors, lower δ13C values observed in some fishes, particularly snubnosed eels, may indicate thatthey are related to the food web which depends on carbon sources in sediments rather than fresh
atmospheric carbon (enriched 13C) assimilated by phytoplankton in surface waters. To make clear
such variation of carbon isotope in the food web it is necessary to collect surface sediments andparticulate organic matter (POM) in the benthic and epibenthic ecosystems of deep-seas.
Significant positive correlations were found between δ15N (‰) and lipid normalized concentrations of PCBs, DDTs and PBDEs (p < 0.05) showing their high biomagnification potential in
marine food webs (Fig. 3). No such relationship was found for HCB, HCHs and HBCDs (Fig. 3).
The rapid elimination of these compounds through gills to surrounding water and by excretion via
other means may prevent biomagnification of these compounds. Similar results on HCB and HCHs
were observed in marine food webs (Ruus et al., 2002; Kelly et al., 2007). Relatively high watersolubility of α-HBCD isomer (48.8 μg/l, Hunziker et al., 2004), which is a major contributor to
total HBCD concentration as shown in the later section, may also result in lower biomagnificationof HBCDs than other hydrophobic organohalogen compounds such as PCBs, DDTs and PBDEs.
On the other hand, biomagnification of α− and γ-HBCD isomers was reported in a Lake Ontario
food web (Tomy et al., 2004). Less biomagnification observed for some organohalogen compounds in this study may be due to smaller difference in trophic levels of fishes as noted above. In
fact, there were no significant correlations between δ15N values and the concentrations of almost
all the compounds analyzed when the data of snubnosed eels was excluded (p > 0.05 for all OCs
and HBCDs, only a significant relationship for PBDEs with p < 0.05, Spearman’s rank order correlation test). In addition, such accumulation profiles of organohalogen compounds in deep-sea
fishes may reflect not only their trophic transfer but also different sources of the substances in thefood web and/or species-specific distribution of fishes. As noted above, fishes showing lower δ13C
values such as snubnosed eels may be affected by substances originated from sediments. Interestingly, snubnosed eels showed lower concentrations of HCHs than other fishes with significantly
higher concentrations of other hydrophobic OCs and PBDEs (Table 2 and Fig. 3). In our earlier
studies on deep-sea fishes from the western North Pacific, off-Tohoku, Japan (Takahashi et al.,
2000; de Brito et al., 2002a) higher concentrations of PCBs, DDTs and CHLs were found in nonmigratory fishes from deeper waters and, on the contrary, HCHs and HCB were accumulated at
higher concentrations in shallow/migratory fishes. These observations may reflect the vertical distribution of these contaminants in the water column of this region (until at least ca. 1000 m depth).

748

Shin Takahashi et al.

Fig. 3. Relationship between δ15N (‰) and organohalogen compounds (ng/g lipid wt) in deep-sea fishes from off
the Pacific coast of northern Japan.

Contaminants in Deep-sea Fishes from off Tohoku

749

Tanabe and Tatsukawa (1983) showed that the concentrations of HCHs significantly decreased
with depth in the open water column of the Pacific Ocean. Hargrave et al. (1992) reported thatbenthic amphipods from the Arctic continental shelf accumulated between ten to sixty times theconcentrations of PCBs, DDTs and CHLs but only two to five times those of HCHs and HCB
found in pelagic plankton, and suggested that OCs with lower water solubility and higher affinity
for absorption to particles will be transported to deeper waters and incorporated into the benthic
food web more readily than higher water soluble compounds. Snubnosed eel, a bathydemersal fish
species, was collected from the deepest waters (900 m) in this study area. Therefore, results of thisstudy are also suggestive of the distribution of OCs and BFRs in the ecosystem and the accumulation of hydrophobic OCs and PBDEs in the demersal fauna.
Composition of OCs
The residue patterns of OCs in organisms are influenced by the patterns in food, habitat andmetabolism of the fishes and reflect environmental inputs of these compounds. Among DDT compounds, p, p’-DDE and p, p’-DDT were the predominant constituents in almost all the deep-sea
fishes (Fig. 4). Relatively high proportions (> 40%) of p, p’-DDT were found in some deep-sea
fishes compared to those reported in Suruga (Lee et al., 1997) and Tosa Bay, Japan (Takahashi etal., 2001). The present study area lies in the Kuroshio-Oyashio transitional zone which is a confluence of various currents resulting in the formation of diverse water masses. Takahashi et al. (2000)
analyzed myctophid fishes from the western North Pacific, Japan and reported high proportion ofp, p’-DDT (>50%) in non- or less-migratory fishes living in mesopelagic waters. Similarly highproportions of p, p’-DDT (> 40%) were also found in Japanese common squid (Todarodes pacificus) from off Sanriku, Japan even though this location seems to be far away from the sources of
DDT (Ueno et al., 2003). It has been suggested that the North Pacific Intermediate Water (NPIW),
which is found at depths of 300 800 m in the North Pacific subtropical gyre, originates from theFig. 4. Composition of DDTs, HCHs and CHLs in deep-sea fishes from off the Pacific coast of northern Japan.

750

Shin Takahashi et al.

watermass in the Okhotsk Sea, and new NPIW is formed along the Kuroshio-Oyashio interfrontal
zone (Yasuda, 1997). Elevated background levels of DDTs in the Okhotsk Sea have been reported
in several studies (Iwata et al., 1995, 2000). In this context, the intermediate water in the study area
can be expected to have relatively fresh input of DDTs, which originate from more contaminatedOkhotsk Sea. However, information on the distribution of OCs and geophysical and geochemical
studies, which can support this hypothesis, is very limited.
Among HCHs isomers, α-HCH was the predominant isomer in all the deep-sea fishes of thepresent study (Fig. 4). It has been reported that the ratio of α-HCH to total HCH concentrations inseawater and fish has a tendency to increase with the increasing latitude (Iwata et al., 1993; Ueno
et al., 2003). α-HCH is preferentially transported to northern colder regions due to higher vapor
pressure among various HCH isomers. Higher proportion of α-HCH was found in fishes from
northern part of Japan, such as off-Tohoku and Japan Sea (Takahashi et al., 2000; de Brito et al.,2002). In case of CHLs, the most predominant CHL-related compound was trans-nonachlor, which
is a stable form of the CHL-related compounds, followed by cis-chlordane, trans-chlordane, cisnonachlor and oxychlordane (Fig. 4). Similar pattern was noted for walleye Pollock (Theragra
chalcogramma) from the North Pacific and the Bering Sea (de Brito et al., 2002b).
Congener/isomer profiles of BFRs
Of the fourteen PBDE congeners analyzed, a total of nine congeners from tri- to deca-BDE
were identified in deep-sea fishes of the present study (Fig. 5). The congener profiles of PBDEs
varied between the species and, in most fish samples, the congeners from tri- to hexa-BDEs (BDE28, BDE-47, BDE-99, BDE-100, BDE-154) were predominant. The PBDE congener profiles varied between the species and the different profiles in the fish species could be related to specificuptake, metabolism, storage and excretion mechanisms. The higher contribution of BDE-47 tototal BDE burdens could be attributable to a higher bioaccumulation potential of this congener andpossible debromination of BDE-99 or other BDE congeners in biota tissues. In the present study,
BDE-183 was not detected in any of the fish samples. Debromination of BDE-183 to lower congeners may be the reason, as experimental studies in fish have shown debromination of BDE-183 toBDE-154 (Stapleton et al., 2004). The higher brominated congeners from octa- to deca-BDE weredetected in few samples, suggesting the relatively low bioaccumulation potential as well as the low
bioavailability of these congeners. Accumulation of BDE-209 in some fishes such as spinyhead
sculpin (Dasycottus setiger) and largenose grenadier (Coryphaenoides nasutus) can be explainedby their sediment dwelling habit as BDE-209 is mainly associated with sediments.
Among the HBCD isomers, α- and γ-HBCD were detected in all the samples, while β-isomer
was below detection limits in most of the samples. The prevalence of α-HBCD has been observedin other aquatic biota samples like fish, shrimp and mussels (Morris et al., 2004; Tomy et al., 2004;
Janak et al., 2005; Ueno et al., 2006; Ramu et al., 2007). The dominance of α-HBCD over theother two isomers could be due to the isomer specific metabolism as well as the potential of
α-HBCD for long range atmospheric transport. Zegers et al. (2005) reported that β- and γ-HBCD
were significantly metabolized when compared to α-HBCD, in the microsomal preparations of seal
liver. Ueno et al. (2006) observed that, like that of α-HCH, the percentage contribution of α-HBCD
also increased with increasing latitude and a high proportion of α-HBCD was found in skipjack
tuna from the northern cold-water region of North Pacific, Japan. These results may indicate that
α-HBCD could have the highest transportable potential among the HBCD isomers in the environment.
Temporal trends of OCs
To elucidate the temporal trend of OCs contamination during the last decade, the results of theContaminants in Deep-sea Fishes from off Tohoku

751

Fig. 5. Congener/isomer profiles of BFRs (PBDEs and HBCDs) in deep-sea fishes from off the Pacific coast ofnorthern Japan.

present study were compared with the data reported for deep-sea fishes in our earlier study (deBrito et al., 2002), in which the area of survey, off the Pacific coast of northern Japan, almost overlapped the sampling locations of the present study. In Fig. 6, the concentrations of OCs (ng/g lipidwt) and ratios of parent to stable compounds of DDTs and CHLs were compared between the same
species of fishes collected in 1995 and 2005 (the data for snubnosed eels were excluded from thecomparison because of the species-specific accumulation of OCs and large variation of data between the individual specimens). Decreasing trends in the concentrations of DDTs and CHLs from1995 to 2005 were observed in almost all the fish species analyzed. It is also noteworthy that ratiosof parent compounds, p, p’-DDT and trans-chlordane, to stable compounds, p, p’-DDE and transnonachlor, respectively, which are an indication of recent input of technical DDTs and CHLs into
the environment, decreased during this period. These results suggest declining environmentalloads of DDTs and CHLs in this region during the last decade. On the other hand, no significant
trend was observed for the concentrations of PCBs, HCB and HCHs between 1995 and 2005.
Tanabe et al. (1994) reported residue levels of PCBs and DDTs in archived fat tissues of northern
fur seals (Callorhinus ursinus) collected from northern North Pacific; 1) DDT levels declined
continuously even in the 1980s and 1990s, and those levels at the end of the 1990s reached about
one thirtieth of the maximum values found in the early 1970s; Nevertheless, 2) PCB levels in the
1980s and the 1990s showed a steady-state condition of about half the maximum value found in
the 1970s; and 3) HCH and CHL levels were stable and no apparent decline was noticed since1971. In addition, Kajiwara et al. (2004) confirmed no apparent decline of HCB levels during 1971
to the 1990s by analyzing the same archived samples of northern fur seals. Except for CHLs, theresults of the present study agree well with the data reported for OCs in northern fur seals.

752

Shin Takahashi et al.

Fig. 6. Comparison of the concentrations of OCs (ng/g lipid wt) (a) and ratios of parent to stable compounds (b) in
deep-sea fishes from off the Pacific coast of northern Japan sampled in 1995 and 2005.

Chlordane was used largely as a termitcide in Japan until 1986, even after the prohibition of its use
as pesticide, and thus, it can be hypothesized that environmental levels of CHLs have not declined
significantly during the 1980s/90s. On the other hand, continuous release of PCBs and HCB fromvarious sources (e.g., PCB containing wastes such as stored transformers and obsolete electricaland electric products, secondary formation of dioxin-like PCBs and HCB in combustion processes,
generation of HCB as by-product in manufacturing processes etc.) has been suggested in Japan(Sakai et al., 2001; Hirai et al., 2003). No declining trend of HCH levels may be attributable totheir long range atmospheric transport and cold condensation in the colder regions (Iwata et al.,
1993; Wania and Mackay 1996; Beyer et al., 2000). In addition to the present study, further monitoring studies are required to delineate contamination status by organohalogen compounds including emerging POPs such as PBDEs and HBCDs and their temporal trends in deep-sea fauna because of their significant increasing levels during the last decades in marine mammals and sedimentcores from Japanese waters (Tanabe et al., 2008).

Contaminants in Deep-sea Fishes from off Tohoku

753

Acknowledgments
We thank the crew and staff members of the R/V Wakataka-maru and Fisheries Research
Agency (FRA) for their help during the sampling. This study was supported by Global Center of
Excellence (COE) Program of the Japanese Ministry of Education, Culture, Sports, Science andTechnology and Grants-in-Aid for Scientific Research (S) (No. 20221003), (A) (No. 20241017)
and (B) (18310046) from Japan Society for the Promotion of Science (JSPS). The award of JSPS
Postdoctoral Fellowship to K. Ramu (No. P07153) is acknowledged.
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