Chemosphere 53 (2003) 347–362

www.elsevier.com/locate/chemosphere

Dynamics of PCDDs/DFs and coplanar-PCBsin an aquatic food chain of Tokyo Bay

Wataru Naito a,b,*, Jiancheng Jin a, Youn-Seok Kang a,c, Masumi Yamamuro d,Shigeki Masunaga a,c, Junko Nakanishi a,b,c

a Graduate School of Environment and Information Sciences, Yokohama National University, 79-7 Tokiwadai, Hodogaya-ku,

Yokohama 240-8501, Japanb Research Center for Chemical Risk Management, National Institute of Advanced Industrial Science and Technology,

16-1 Onogawa, Tsukuba, Ibaraki 305-8569, Japanc CREST, Japan Science and Technology Corporation, Kawaguchi 332-0012, Japan

d Institute for Marine Resources and Environment, National Institute of Advanced Industrial Science and Technology,

Tsukuba Central 7, Tsukuba 305-8567, Japan

Received 19 November 2001; accepted 28 February 2002

Abstract

Concentrations and accumulation profiles of PCDDs/DFs and coplanar-PCBs (co-PCBs) in aquatic biota (e.g.,

plankton, shellfish, benthic invertebrate, and fish) and sediment from Tokyo Bay were examined to elucidate the re-

lationship between bioaccumulation and trophic level in the food web as determined by the stable nitrogen isotope

analysis. Bioaccumulation patterns of PCDDs/DFs and co-PCBs varied greatly among congeners. Accumulation

patterns of PCDDs/DFs and co-PCBs are not solely explained by their physicochemical properties. Biota-sediment

accumulation factors (BSAFs) for co-PCBs in biota from Tokyo Bay were significantly greater than those of PCDDs/

DFs. Furthermore, the slopes of the plots of d 15N and BSAF values and water solubility of 2,3,7,8-substituted PCDDs/

DFs and co-PCBs were highly correlated. The results of our study would provide the valuable information to un-

derstand the accumulation properties of PCDDs/DFs and co-PCBs that can be used as a scientific basis to determine

the sediment quality criteria of PCDDs/DFs and co-PCBs.

� 2003 Elsevier Ltd. All rights reserved.

Keywords: PCDDs/DFs; Co-PCBs; Food web; BSAF; Tokyo Bay; Stable nitrogen isotope analysis

1. Introduction

Polychlorinated dibenzo-p-dioxins and dibenzofurans

(PCDDs/DFs) and some non- and mono-ortho-poly-

chlorinated biphenyl congeners that can attain planar

configuration (co-PCBs) are chemically stable and per-

sistent hydrophobic organic chemicals that pervaded the

environment and are thought to be biomagnified via food

*Corresponding author. Tel.: +81-29-861-8299; fax: +81-29-

861-8411.

E-mail address: w-naito@aist.go.jp (W. Naito).

0045-6535/$ - see front matter � 2003 Elsevier Ltd. All rights reserv

doi:10.1016/S0045-6535(03)00046-8

chain. Many studies have revealed that these compounds

are found in a variety of environmental media, including

air, water, soil, sediment, animals and human (e.g.,

Schcter et al., 1989; Broman et al., 1991; Brzuzy and

Hites, 1996). Due to their inherent chemical and physical

properties, bioaccumulation of these compounds in

aquatic biota is of increasing concern.

It is known that the major route of exposure of

PCDDs/DFs and co-PCBs to human is through dietary

uptake. Consumption of fish and shellfish has contrib-

uted significantly to the exposure of these compounds to

the Japanese population (MHW, 1999). The concentra-

tions of these compounds are, therefore, of concern to

ed.

348 W. Naito et al. / Chemosphere 53 (2003) 347–362

those who consume fish and shellfish. In order to eval-

uate the potential risk of PCDDs/DFs and co-PCBs to

humans, it is important to understand the levels and

characteristics of bioaccumulation of PCDDs/DFs and

co-PCBs in the aquatic food web. Such information will

help to set for the acceptable daily intake of fish and

shellfish and determine the environmental quality crite-

ria of PCDDs/DFs and PCBs in the aquatic environ-

ment (e.g., water, sediment).

Only a few studies have been conducted, which

quantitatively examine the relationship between accu-

mulation patterns of congeners of PCDDs/DFs and

co-PCBs and trophic level in the aquatic food webs.

Furthermore, the accumulation pattern of each con-

gener is expected to vary greatly because each congener

possesses different chemical and physical properties.

Trophic levels of food chain traditionally have been

vaguely defined using food composition analysis and

expressed in discrete terms as producer, primary con-

sumers, secondary consumers and so on. The limita-

tions of the traditional method have been documented

elsewhere (e.g., Broman et al., 1992). In recent years,

biological interpretations of changes in the relative

abundance of naturally occurring stable isotopes of N

and C have provided an alternative method to charac-

terize food web dynamics and trophic levels (e.g., Wada

and Hattori, 1991; Yamada and Yoshioka, 1999). The

strength of this method is that trophic levels can be ex-

pressed numerically as continuous variable. If the 15N/14N ratio increases by 3–5‰, the organisms are generally

assumed to belong to different trophic levels (e.g., Wada

and Hattori, 1991).

Considering those observations, in this study, stable

isotope analysis of N was used to quantitatively deter-

mine trophic levels of organisms to elucidate relationship

between trophic levels and contaminant accumulation

characteristics in aquatic biota. We also investigated the

concentrations and accumulation profiles of PCDDs/

DFs and co-PCBs in aquatic biota (e.g., plankton,

shellfish, benthic invertebrate, and fish) and sediment

from Tokyo Bay and examined the relationship between

bioaccumulation patterns of these compounds and

trophic level in the food web as determined by stable

nitrogen isotope analysis.

2. Materials and methods

2.1. Samples

The sampling has been done in Tokyo Bay which is

approximately 3 km offshore (35�380 N, 139�580 E) of

the northern part of Tokyo in December 1998. Fish

sample includes sea bass (Lateolabrax japonicus), stinray

(Dasyatis akajei), conger-eel (Conger myriaster), gizzard

shad (Konosirus punctatus), stone flounder (Kareius

bicoloratus) and marbled sole (Limanda yokohamae).

Shellfish samples include littleneck clam (Ruditapes

philippinarum), mactidae (Mactra chinesis philippi), hard-

shell clam (Chloromytilus viridis) and akanishi (Rapana

venosa). All the forementioned sample matrix were col-

lected using trawling and gill net. Polychaetes were

collected using benthic grab sampler. Plankton (which

comprise phytoplankton, zooplankton, debris of sur-

face sediment) was sampled by plankton net with the

mesh size of 0.095 mm. Immediately after collection, the

samples were transported to the laboratory by dry ice

and stored at )20 �C until analyzed. Information re-

garding species collected, sample size, lipid content and

stable nitrogen isotope ratios of samples are listed in

Table 1.

Along with biological samples, surface sediment

samples were collected from four stations, Station 1

(ST.1) [35�38.2600 N, 139�58.3850 E], ST.2 [35�38.4560 N,

139�58.9990 E], ST.3 [35�38.3680 N, 139�59.2370 E] andST.4 [35�38.7460 N, 139�59.5390 E]. Water depth of ST.1,

ST.2, ST.3 and ST.4 were 5.1, 5.4, 7.3 and 10 m, re-

spectively. The average total organic carbon content of

the sediments at this site was approximately 2.3%. Sed-

iment samples were stored in ice-filled portable con-

tainers after the collection and freeze-dried until

analyzed.

2.2. Stable nitrogen isotope analysis

Stable nitrogen isotope analysis was performed for

individual biological samples. Fat in biological samples

was removed with 50% ethanol in benzene. These sam-

ples were dried using a vacuum dryer at 30 �C and then

ground to a fine powder. Subsequently, samples were set

in an elemental analyzer and combusted at 1050 �C.Nitrogen gas was then carried through the interface

(ConFlo II, Finnigan MAT) and analyzed using a mass

spectrometer (Delta plus, Finnigan MAT). Stable iso-

tope ratios are expressed by d as parts per thousand

according to

d 15N ¼ fðRsample=RstandardÞ � 1g � 1000ð‰Þ;

where R is the corresponding ratio 15N/14N and Rstandard

for 15N is the atmospheric nitrogen.

2.3. Determination of PCDDs/DFs and coplanar-PCBs

Whole body homogenates of fish and shelled soft

tissue homogenates of shellfish were used for the Soxh-

let extraction. The extract was then concentrated to

about 10 ml with a Kuderna–Danish concentrator.

One ml of the extract was used for lipid determination

gravimetrically. A total of 16 13C-labelled 2,3,7,8-

chlorine-substituted PCDDs/DFs, four 13C-labelled

non-ortho-substituted CBs and 8 mono-ortho-substituted

Table 1

Details of biological samples collected from Tokyo Bay

Common name

(Japanese)

Scientific name na Analyzed

tissue

Sample weightb

(g)

Lipid contentb

(%)

d 15Nc (‰)

Fish Sea bass

(suzuki)

Lateolabrax

japonicus

3 Whole 673 (599–798) 6.2 (4.6–7.0) 17.3� 0.7

Stinray (akaei) Dasyatis akajei 3 Whole 115 (73–141) 2.2 (1.3–2.8) 16.8� 0.7

Conger-eel

(anago)

Conger myriaster 1 Whole 371 17.9 16.2

Gizzard shad

(konoshiro)

Konosirus punctatus 3 Whole 204 (172–253) 5.0 (1.9–7.3) 13.4� 1.9

Stone flounder

(ishigarei)

Kareius bicoloratus 3 Whole 716 (587–789) 4.0 (3.4–4.8) 14.8� 0.5

Marbled sole

(makogarei)

Limanda yokohamae 1 Whole 660 2 13.5

Shellfish Littleneck clam

(asari)

Ruditapes

philippinarum

1 (5) Soft tissue 11.5 1.5 12

Mactidae

(bakagai)

Mactra chinesis

Philippi

2 (13) Soft tissue 43 (37–49) 0.5 (0.4–0.6) 11.9� 0.2

Hard-shell clam

(midorigai)

Chloromytilus viridis 2 (22) Soft tissue 33 (25–41) 2.2 (1.9–2.5) 11.5� 0.3

(akanishi) Rapana venosa 1 (2) 68.6 0.3 13.3

Benthic

organisms

Polychaete Parapriosonospio sp.

Type A

1 Whole – 0.4 12.9

Planktonsd 1 Whole – 0.3 11.3� 0.8

aValues in parentheses indicate the number of sample pooled.b If more than one sample available, max and minimum indicated.cAverage and standard deviation indicated.d Planktons include mixture of phytoplankton, zooplankton and debris.

W. Naito et al. / Chemosphere 53 (2003) 347–362 349

CBs were used as internal standards, spiked to the re-

maining extract. Then the extract was transferred into a

separatory funnel containing 100 ml of n-hexane and

cleaned with concentrated sulfuric acid. Further cleaned

extract was then passed through 2 g of silica gel packed

in a glass column and eluted with 130 ml of hexane to

separate PCDD/DFs and co-PCBs. The extract was

again passed through 5 g alumina packed in a glass

column to separate mono- and di-ortho-PCBs. Eventu-

ally, the final extract was then passed through a carbon

column packed with 1 g of activated carbon-impreg-

nated silica gel. The first fraction eluted with 20 ml of

25% dichloromethane in hexane was used to determine

mono-ortho-PCBs. The second fraction eluted with 250

ml of toluene contained 2,3,7,8-substituted PCDDs and

PCDFs and non-ortho-co-PCB congeners.

PCDDs/DFs and non-ortho-co-PCBs were analyzed

using a high-resolution gas chromatography (Hewlett

Packard 6890 Series) coupled with high-resolution mass

spectrometry (Micromass Autospec-Ultima) [HRGC–

HRMS]. PCDD and PCDF congeners were separated

on a DB-5 capillary column coated at 0.25 lm (60 m�0:25 mm i.d.). The column oven temperature was pro-

grammed from 160 �C (3 min) to 200 �C at a rate of

40 �C/min with a 2 min holding time, and to 310 �C at

2 �C/min, with a holding time of 1 min. Injector and

transfer line/ion source temperatures were held at 280

and 250 �C, respectively. The mass spectrometer was

operated at an EI energy of 40 eV and the ion current

was 600 pA. PCDD/DF congeners were monitored by

SIM at the two most intensive ions of the molecular ion

cluster. Recoveries of 13C-labelled PCDD and PCDF

congeners through the analytical procedure ranged from

63% to 90%. The detection limits for PCDDs, PCDFs

and co-PCBs were 0.001 pg/g wet weight. Concentra-

tions of certain PCDD/DF congeners were confirmed

using DB-17 (60 m� 0:25 rrm i.d., 0.25 lm film thick-

ness) column. Non-ortho-PCBs were separated on a DB-

5 capillary column coated at 0.25 lm (60 m� 0:25 mm

i.d.) and analyzed using SIM mode.

Determination of PCDDs/DFs and co-PCBs con-

centrations in sediment was based on the method de-

scribed previously (Sakurai et al., 1996).

3. Results

3.1. Trophic levels of aquatic organisms in Tokyo Bay

The d 15N values in Tokyo Bay food chain studied

were presented in Table 1 and Fig. 1. Tokyo Bay food

Fig. 1. The Tokyo Bay food chain in terms of average d 15N values (max and minimum indicated) (PKT¼ plankton; HSC¼ hard-shell

clam; MAC¼mactidae; LNC¼ littleneck clam; PLC¼polychaete; AKA¼ akanishi; GS¼ gizzard shad; MS¼marbled sole;

SF¼ stone flounder; Conger-eel¼CE; STI¼ stinray; SB¼ sea bass).

350 W. Naito et al. / Chemosphere 53 (2003) 347–362

chain described in terms of average d 15N values can be

classified by the following order; plankton (phyto-

plankton+ zooplankton+debris which comprise fecal

pellets from zooplankton, fish, fish egg and bacte-

ria)< littleneck clam, hard-shell clam and mactri-

dae< polychaete< akanishi< gizzard shad<marbled

sole< stone flounder< conger eel, stingray and sea bass.

Considerably, d 15N values (Fig. 1) correspondingly in-

crease from the lowermost trophic animals (e.g.,

plankton) to the higher trophic level (e.g., sea bass).

In general it can be safely explained that planktons in-

gested by suspension-feeding omnivores such as hard-

shell clam, mactidae and littleneck clam had greater

d 15N values with the average of 12‰ (Fig. 1). Poly-

chaetes followed next and other shellfish eating akanishi

had 1‰ greater d 15N value than shellfish. The bivalve

consumers like stone flounder and marbled sole and

phytoplankton feeders like gizzard shad classify to be

next group. Eventually conger eel, stingray and sea bass

are classified as top predators among the biological

samples in this study. The ecological studies, stomach

contents of these predators and analysis of d 15N values

also supported that these top predators feeds on small

fish and crustaceans. The orders of the above classi-

fication determined by d 15N values are qualitatively

consistent with the conceptions of the trophic levels

judging from biological information (e.g., Kanbara and

Okamura, 1985) in the marine aquatic food chains.

3.2. Concentrations of PCDDs/DFs and coplanar-PCBs

The congener-specific concentrations of PCDDs/DFs

and co-PCBs in biota and sediment samples from Tokyo

Bay are listed in Table 2. When more than one sample

was measured for a single species, the geometric mean

was calculated and listed. Total PCDD/DF concentra-

tion in Tokyo Bay biota ranged from 8.52 for akanishi to

259 pg/g wet weight for plankton. The total PCDD/DF

concentration in Tokyo Bay sediment was 147 pg/g dry

weight. Total co-PCB concentration in Tokyo Bay biota

ranged from 267 for akanishi to 29 900 pg/g wet weight

for sea bass. The total co-PCB concentration in the

Tokyo Bay sediment was 69 pg/g dry weight. In order to

estimate toxic equivalency (TEQ) for biota and sedi-

ments, we follow WHO-TEFs for mammal proposed by

Van den Berg et al. (1998). The total TEQ concentration

of PCDDs/DFs in biota ranged from 0.05 for akanishi

to 2.41 pg TEQ/g wet weight for sea bass. The total TEQ

concentration of PCDDs/DFs in the sediment was 0.50

pg TEQ/g wet weight. Furthermore, the total TEQ

concentration (pg TEQ/g) of co-PCBs in biota ranged

from 0.033 for akanishi to 8.13 for sea bass, whereas

that of sediment was 0.03.

3.3. Relationship between d 15N and concentrations of

PCDDs/DFs and co-PCBs

In order to elucidate the relationship between the

trophic level of organisms sampled from Tokyo Bay and

the concentrations of PCDDs/DFs and co-PCBs, re-

gression analysis of the relationship between d 15N and

congener-specific concentrations of PCDDs/DFs and

co-PCBs was conducted. Table 3 shows the slopes,

coefficients of determination (r2) and p values of the

relationship between d 15N and the congener-specific

concentrations of PCDDs/Fs and co-PCBs. For non-

2,3,7,8-substituted congeners, slopes and r2 of the rela-

tionship between the d 15N and the concentrations of

total non-2,3,7,8-substituted congener concentrations

within the same homologue were calculated and are also

Table 2

PCDD, PCDF, and co-PCBs concentrationsa in aquatic organismsb (pg/g wet weight) and sedimentb (pg/g dry weight for sediment) from Tokyo Bay

Homologue Isomersc PKT PLC Shellfish Fish SED

MAC LNC HSC AKA SF STI GS MS CE SB

TCDD 1368 8.83 71.22 6.50 10.62 17.74 3.33 3.27 2.30 1.06 9.35 3.03 3.55 11.28

1379 3.19 18.80 1.52 2.98 3.70 0.93 0.10 0.29 0.19 0.15 0.21 0.16 4.11

1369 0.92 0.11 0.34 0.03 0.04 0.01 0.03 0.02 0.04 0.02 0.18

1247/1248/1378/1469 0.32 1.15 0.21 0.37 0.52 0.07 0.01 0.04 0.03 0.03 0.25

1246/1249/1268/1478 0.02 0.01

1279 0.17 0.03

1234/1236/1269 0.17 0.01

1237/1238 2.48 8.20 1.49 3.49 2.74 0.10 0.03 0.09 0.02 0.07 0.79

2378d 0.24 0.15 0.22 0.30 0.50 0.46 0.01

TCDF 1368 0.45 0.66 0.05 0.07 0.12 0.22 0.09 0.08 0.28 0.05 0.15 0.15

1468 0.65 0.52 0.19 0.30 0.32 0.09 0.14 0.16 0.06 0.45 0.04 0.10 0.08

2468 0.72 3.44 0.52 1.33 2.72 0.38 0.08 0.24 0.08 0.26 0.11 0.13 0.62

1247/1347/1378/1346/1246e 0.72 1.31 0.46 0.70 0.87 0.12 0.18 0.13 0.05 0.57 0.07 0.12 0.31

1247/1347/1378/1346/1246e 0.71 0.21 0.37 0.39 0.01 0.14 0.02 0.03

1367/1348/1379/1248 0.58 2.50 0.53 1.26 1.62 0.16 0.20 0.16 0.15 1.24 0.13 0.17 0.43

1268/1467/1478e 0.70 0.17 0.44 0.07 0.07 0.03 0.07 0.21 0.03 0.06 0.17

1268/1467/1478e 0.37 1.82 0.27 0.53 0.10 0.15 0.02 0.04 0.02 0.13 0.04

1369/1237/2368 0.44 1.57 0.29 0.70 1.36 0.10 0.09 0.13 0.06 0.14 0.09 0.11 0.25

2467/1238/1236/1469/1678/1234e 1.13 1.68 0.50 0.67 0.96 0.11 0.05 0.11 0.06 0.08 0.04 0.03 0.30

2467/1238/1236/1469/1678/1234e 0.96 0.06 0.81 0.25 0.03 0.04 0.04 0.12 0.02 0.16

1278 0.29 0.70 0.24 0.52 0.23 0.01 0.01 0.02 0.03 0.04 0.04 0.04 0.18

1267/1349 0.06 0.03

2378d 0.49 0.06 0.40 0.63 0.02 1.48 1.75 0.62 2.76 3.43 2.68 0.20

2367 0.30 0.87 0.40 0.68 0.75 0.03 0.27 0.05 0.10 0.38 0.05 0.16 0.17

3467/1269 0.22 0.74 0.28 0.29 0.02 0.03 0.04 0.02 0.02 0.15

1239 0.16 0.01 0.02 0.02 0.07 0.27 0.01

1289 0.18 0.03 0.03 0.02

PeCDD 12468/12479 1.07 3.62 0.38 1.00 0.71 0.11 0.04 0.06 0.08 0.05 0.04 0.04 0.93

12469 1.70 0.08 0.04 0.02 0.01 0.03 0.01 0.05 0.02 0.13

12368 2.15 5.47 0.59 1.36 0.93 0.25 0.11 0.15 0.17 0.10 0.10 0.12 1.82

12478 0.38 0.24 0.15 0.01 0.02 0.02 0.02 0.13

12379 0.87 1.25 0.20 0.25 0.05 0.02 0.03 0.07 0.01 0.67

12369 0.83 0.03 0.01 0.05

12467/12489 0.62 0.13 0.08

12347 0.20 0.07

12346 0.03

12378d 0.27 0.23 0.07 0.23 0.13 0.02 0.27 0.21 0.58 0.31 0.45 0.69 0.07

12367 0.27 0.03

12389 0.18 0.04

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53(2003)347–362

351

Table 2 (continued)

Homologue Isomersc PKT PLC Shellfish Fish SED

MAC LNC HSC AKA SF STI GS MS CE SB

PeCDF 13468/12468 1.40 4.67 1.63 2.23 3.06 0.39 1.23 0.94 0.85 2.57 0.58 0.80 1.18

13678 0.20 0.24 0.03 0.12 0.03 0.03 0.02 0.04 0.01 0.06

12368/12478/13467/13478/12467 1.24 1.78 0.52 0.98 0.15 0.69 0.84 0.18 1.21 1.05 0.91 0.85

13479/14678 0.37 0.12 0.18 0.04 0.05 0.05 0.07 0.16 0.02 0.16

12479 0.02 0.02 0.04 0.04 0.03 0.02

13469 0.03 0.02 0.02 0.01 0.02 0.01 0.02 0.03

23468/12469/12347/12346e 0.88 0.84 0.28 0.30 0.10 0.04 0.07 0.05 0.06 0.08 0.06 0.51

23468/12469/12347/12346e 0.33 0.03 0.04 0.02 0.05 0.09 0.02 0.02

12348 0.18 0.07 0.01 0.02 0.05

12378d 0.23 0.09 0.48 0.43 0.38 0.38 1.06 0.54 0.12

12367 0.07 0.12 0.15 0.16 0.04 0.16 0.11 0.15 0.10

12678/12379 0.30 0.09 0.12 0.02 0.02 0.01 0.02 0.17

23478d 0.91 0.35 0.12 0.24 0.14 0.02 0.66 1.16 1.24 0.97 1.24 1.60 0.18

23467 0.56 0.74 0.27 0.36 0.43 0.03 0.12 0.56 0.22 0.18 0.14 0.15 0.19

12349 0.06 0.05 0.02 0.02

12389 0.04 0.07 0.06 0.25

HxCDD 124679/124689 0.92 7.47 0.24 0.56 0.30 0.03 0.03 0.04 0.06 0.05 0.01 1.00

123468 0.96 0.63 0.21 0.55 0.27 0.00 0.03 0.03 0.03 0.02 0.01 0.80

123679/123689 1.40 2.23 0.25 0.79 0.31 0.03 0.05 0.02 0.11 0.05 0.02 1.02

123469 0.99 0.01 0.03

123478d 0.16 0.07 0.31 0.04 0.02 0.05 0.12 0.16 0.02 0.06 0.10 0.13

123678d 0.47 0.10 0.62 0.15 0.03 0.41 0.31 0.44 0.39 0.81 0.55 0.31

123789d 0.24 0.06 0.31 0.07 0.01 0.07 0.12 0.11 0.05 0.08 0.04 0.20

HxCDF 123468 0.79 0.39 0.21 0.60 0.10 0.03 0.07 0.08 0.08 0.11 0.10 0.11 0.51

134678/124678 2.60 2.18 1.10 2.29 1.40 0.14 0.28 0.47 0.37 0.50 0.55 0.49 2.11

134679 0.12 0.02 0.05 0.02 0.01 0.03 0.02 0.02 0.08

124679 0.23 0.07 0.10 0.10 0.09 0.08 0.18 0.21 0.22 0.16

124689 2.26 0.68 0.89 0.62 0.09 1.55 0.66 1.13 2.85 1.22 1.56 1.10

123478d 0.62 0.25 0.13 0.49 0.09 0.18 0.32 0.22 0.24 0.26 0.31 0.43

123678 0.17 0.03 0.20 0.08 0.01 0.18 0.19 0.18 0.21 0.23 0.20 0.29

123479 0.02 0.01 0.07

123469/123679 0.10 0.02 0.03 0.01 0.07 0.04

123689 0.11 0.02 0.06 0.18 0.06 0.16 0.29 0.08 0.09

234678d 0.92 0.34 0.17 0.15 0.03 0.38 0.48 0.45 0.39 0.65 0.35 0.49

123789d 0.38 0.02 0.20 0.02 0.01 0.04 0.02 0.04 0.04

123489 0.02 0.01 0.01 0.12

HpCDD 1234679 9.02 17.06 0.82 2.09 1.05 0.06 0.05 0.13 0.46 0.06 0.04 0.03 6.43

1234678d 11.03 3.96 0.96 2.15 0.72 0.08 0.57 0.79 1.03 0.39 0.53 0.28 6.52

HpCDF 1234678d 6.03 1.47 0.53 1.04 0.37 0.04 0.27 0.40 0.50 0.33 0.53 0.37 3.38

1234679 0.78 0.17 0.12 0.10 0.05 0.02 0.06 0.10 0.23 0.06 0.48

352

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53(2003)347–362

1234689 10.68 1.65 0.72 1.17 0.34 0.07 0.31 0.60 0.72 0.82 1.17 1.15 4.60

1234789d 0.91 0.14 0.03 0.46 0.04 0.03 0.09 0.09 0.06 0.07 0.06 0.35

OCDDd 166.00 39.50 7.99 10.50 4.83 0.69 0.82 1.83 5.23 0.65 0.56 0.52 81.06

OCDFd 16.04 1.88 0.80 1.47 0.57 0.06 0.08 0.17 0.76 0.13 0.14 0.19 7.64

Total PCDDs 208.50 187.76 21.92 38.98 34.69 5.88 6.22 6.80 10.10 12.07 6.49 6.64 118.15

Total PCDFs 51.00 40.39 12.18 19.90 20.72 2.63 10.05 11.23 9.41 18.69 14.20 14.03 28.92

Total PCDDs/DFs 259.50 228.14 34.10 58.88 55.42 8.52 16.27 18.02 19.52 30.76 20.69 20.67 147.07

Total PCDDs/DFs-

TEQ

1.11 0.69 0.21 0.64 0.34 0.05 1.15 1.30 1.68 1.53 2.19 2.41 0.50

Non-ortho-PCBs 3,4,40,5-TCB (81) 1.36 1.91 1.21 1.69 1.56 0.07 11.2 1.9 5.3 21.0 10.3 16.1 0.22

3,30,4,40-TCB (77) 22.40 39.20 28.40 28.30 29.80 1.39 246.5 42.5 127.6 368.0 214.0 377.4 6.36

3,30,4,40,5-PcCB (126) 1.00 2.59 0.99 2.98 1.67 0.03 14.9 20.6 23.4 31.7 36.3 42.3 0.22

3,30,4,40,5,50-HxCB (169) 0.78 0.57 0.15 0.54 0.06 2.6 6.5 5.8 5.7 4.1 9.1 0.09

Mono-ortho-PCBs 2,3,30,4,40,5-PeCB (123) 24.5 6.9 9.0 9.0 6.9 138 86 287 514 674 773 1.01

20,3,4,40,5-PeCB (118) 315 678 250 214 214 178 5385 9776 14 754 16 700 19 200 19 973 38.86

2,3,30,40,5-PeCB (114) 12.0 4.5 7.2 7.2 95 141 251 281 293 468 0.65

2,3,30,4,40-PeCB (105) 94 187 77 72 72 64 1509 2416 4342 5120 5300 5331 15.17

2,30,4,40,5,50-HxCB (167) 31 7.2 8.4 8.4 7.4 182 484 702 665 922 960 1.56

2,3,30,4,40,50-HxCB (156) 50 8.2 15.5 15.5 9.1 288 850 1246 1080 1400 1403 2.37

2,3,30,4,40,50-HxCB (157) 13 3.5 5.4 5.4 72 223 277 235 346 321 0.71

2,3,30,4,40,5,50-HpCB (189) 4.8 1.2 3.2 3.2 25 84 139 91 111 103 0.62

Total non-ortho-PCBs 25.5 44.3 30.8 33.0 33.6 1.55 275.3 79.4 165.3 427.0 265.0 445.9 6.9

Total mono-ortho-

PCBs

409 1000 358 334 334 265 7707 14 091 22 122 24 700 28 200 29 411 62

Total non-ortho-PCBs

and mono-ortho-PCBs

435 1044 388 367 368 267 7982 14 171 22 287 25 127 28 465 29 857 69

Total TEQ PCBs 0.150 0.400 0.239 0.340 0.240 0.033 2.30 3.44 5.34 6.310 7.240 8.13 0.03

Total TEQ (PCDDs/

DFs+ co-PCBs)

1.26 1.09 0.45 0.98 0.58 0.08 3.45 4.74 7.02 7.84 9.43 10.53 0.53

aWhen more than one was measured for a single species or sediment, the geometric mean was calculated. No value in space represents ND for all the samples in a single species or

sediment.b PKT¼ plankton; PLC¼polychaete; MAC¼mactidae; LNC¼ littleneck clam; HSC¼ hard-shell clam; AKA¼ akanishi; SF¼ stone flounder; STI¼ stinray; GS¼ gizzard shad;

MS¼marbled sole; Conger-eel¼CE; SB¼ sea bass; SED¼ sediment.c The values in parentheses represent IUPAC number.d 2,3,7,8-Chlorine substituted congeners.e Each isomer was assigned to be in either of the two adjacent peaks.

W.Naito

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osphere

53(2003)347–362

353

Table 3

Slope, r2, p values of the plot of d 15N versus log congener concentrations (pg/g wet wt.) of PCDDs/DFs and co-PCBs in biota from

Tokyo Bay

Homologue Congeners Slope r2 p

TCDD 2378 0.03 0.053 0.66

PeCDD 12378 0.08 0.180 0.169

HxCDD 123478 0.01 0.004 0.859

HxCDD 123678 0.08 0.165 0.215

HxCDD 123789 )0.03 0.022 0.661

HpCDD 1234678 )0.12 0.221 0.123

OCDD )0.27 0.479 0.013

Total TCDDs without 2,3,7,8-substituted congener )0.15 0.352 0.042

Total PeCDDs without 2,3,7,8-substituted congeners )0.22 0.515 0.009

Total HxCDDs without 2,3,7,8-substituted congeners )0.27 0.487 0.017

Total HpCDDs without 2,3,7,8-substituted congeners )0.33 0.522 0.008

TCDF 2378 0.21 0.364 0.05

PeCDF 12378 0.12 0.634 0.018

PeCDF 23478 0.14 0.282 0.076

HxCDF 123478 0.01 0.011 0.758

HxCDF 123678 0.09 0.183 0.189

HxCDF 234678 0.05 0.061 0.464

HxCDF 123789 )0.11 0.176 0.301

HpCDF 1234678 )0.08 0.109 0.294

HpCDF 1234789 )0.08 0.122 0.293

OCDF )0.21 0.395 0.029

Total TCDFs without 2,3,7,8-substituted congener )0.15 0.481 0.012

Total PeCDFs without 2,3,7,8-substituted congeners )0.02 0.025 0.623

Total HxCDFs without 2,3,7,8-substituted congeners )0.01 0.002 0.89

Total HpCDFs without 2,3,7,8-substituted congeners )0.04 0.026 0.617

Total PCDDs )0.19 0.479 0.013

Total PCDFs )0.05 0.099 0.319

Total PCDDs/DFSs )0.12 0.320 0.055

Total PCDDs/DFs-TEQ 0.12 0.262 0.089

Non-ortho-PCBs 3,4,40,5-TCB (81) 0.15 0.217 0.127

3,30,4,40-TCB (77) 0.17 0.249 0.099

3,30,4,40,5-PcCB (126) 0.28 0.368 0.036

3,30,4,40,5,50-HxCB (169) 0.23 0.438 0.026

Mono-ortho-PCBs 2,3,30,4,40,5-PeCB (123) 0.31 0.544 0.01

20,3,4,40,5-PeCB (118) 0.35 0.631 0.002

2,3,30,40,5-PeCB (114) 0.30 0.638 0.006

2,3,30,4,40-PeCB (105) 0.33 0.616 0.002

2,30,4,40,5,50-HxCB (167) 0.37 0.621 0.004

2,3,30,4,40,50-HxCB (156) 0.37 0.596 0.005

2,3,30,4,40,50-HxCB (157) 0.32 0.659 0.004

2,3,30,4,40,5,50-HpCB (189) 0.29 0.592 0.009

Total non-ortho-PCBs 0.18 0.277 0.068

Total mono-ortho-PCBs 0.35 0.632 0.002

Total non-ortho-PCBs and mono-ortho-PCBs 0.34 0.629 0.002

Total TEQ PCBs 0.28 0.518 0.008

Total TEQ (PCDDs/DFs+ co-PCBs) 0.20 0.413 0.024

354 W. Naito et al. / Chemosphere 53 (2003) 347–362

listed in Table 3. The slopes of the regression line vary

among the congeners with the ranges of )0.3 to 0.4. A

positive slope suggests an increase in congener concen-

tration with increasing trophic level, while, negative

slope suggests a decrease in congener concentration with

increasing trophic level.

Table 4

The BSAFa values of 2,3,7,8-substituted PCDDs/DFs and co-

PCBs for sea bass

Homologue Congeners BSAF

TCDD 2378 12

PeCDD 12378 4

HxCDD 123478 0.3

HxCDD 123678 0.6

HxCDD 123789 0.1

HpCDD 1234678 0.02

OCDD 0.002

TCDF 2378 5

PeCDF 12378 2

PeCDF 23478 3

HxCDF 123478 0.3

HxCDF 123678 0.3

HxCDF 234678 0.3

HxCDF 123789 0.08

HpCDF 1234678 0.04

HpCDF 1234789 0.06

OCDF 0.01

Non-ortho-PCBs 3,4,40,5-TCB (81) 27

3,30,4,40-TCB (77) 22

3,30,4,40,5-PcCB (126) 71

3,30,4,40,5,50-HxCB (169) 39

Mono-ortho-PCBs 2,3,30,4,40,5-PeCB (123) 283

20,3,4,40,5-PeCB (118) 190

2,3,30,40,5-PeCB (114) 267

2,3,30,4,40-PeCB (105) 130

2,30,4,40,5,50-HxCB (167) 228

2,3,30,4,40,50-HxCB (156) 219

2,3,30,4,40,50-HxCB (157) 167

2,3,30,4,40,5,50-HpCB (189) 62

a BSAF is derived by dividing lipid-normalized concentra-

tions in biota (Cb) by carbon-normalized concentrations in

sediment (Cs), i.e., BSAF¼Cb/Cs.

W. Naito et al. / Chemosphere 53 (2003) 347–362 355

The slopes were positive for total co-PCB, total

PCDDs/DFs-TEQ and total co-PCBs-TEQ, neverthe-

less, they were negative for total PCDDs/DFs. To be

specific, the congeners of 2,3,7,8-substituted tetra- and

penta-CDD/Fs showed a positive slope, the congeners of

2,3,7,8-substituted hepta- and octa-CDD/Fs showed a

negative slope, and the congeners of 2,3,7,8-substituted

hexa-CDD/Fs showed either positive or negative slopes.

For co-PCBs, the slopes were positive for all congeners

and ranged from 0.15 to 0.37. The slopes increased as

the degree of chlorination increased from tetra- through

hexa-CBs however, decreasing trend was noticed for the

hepta-CBs.

3.4. Biota-sediment accumulation factors

The biota-sediment accumulation factor (BSAF)

values were derived in order to examine the relationship

between concentrations of PCDDs/DFs and co-PCBs in

biota and sediment in Tokyo Bay. The BSAF values

were calculated from lipid-normalized concentrations in

biota (Cb) and organic carbon-normalized concentra-

tions in sediment (Cs) (i.e. BSAF¼Cb/Cs).

For illustrative purposes, the BSAF values of sea

bass, the top predator analyzed in this study were pre-

sented (Table 4). For 2,3,7,8-substituted PCDDs/DFs,

the BSAF values were greater than 1 for tetra- and penta-

congeners, while they were less than 1 for higher chlori-

nated congeners. For non-2,3,7,8-substituted congeners,

the BSAF values were very small, ranging from 1/10 to

1/100 (data not shown) when compared to 2,3,7,8-

substituted PCDD/DFs. On the other hand, the BSAF

values for co-PCBs were much higher than those for

PCDDs/DFs. For example, BSAF values for the four

non-ortho-PCB congeners (#81, #77, #126, and #169)

were less than 100, while those for all mono-ortho-PCBs

it was greater than 100 excluding #189 (2,3,30,4,40,5,50).

The relationship between log BSAF values of sea

bass and log Kow for the congeners of 2,3,7,8-substituted

PCDDs/DFs and co-PCBs are shown in Fig. 2. Overall,

the relationship between log BSAF and log Kow was not

clear when the log Kow values were below 7.5, but after

reaching the log Kow values exceeding 7.5, the log BSAF

value decreased greatly.

In addition, the relationship between log BSAF val-

ues of sea bass and log Ss (water solubility for solid-

phase chemical, pg/l) were conducted for analytes and is

presented in Fig. 3. A linear regression was obtained

from the plot of log BSAFs of sea bass versus log Ss,

namely:

log BSAF� sea bass ¼ 0:85 � log Ss� 3:68 ðr2 ¼ 0:90Þð1Þ

The r2 was 0.90, and these results suggested that BSAF

and water solubility are highly correlated. However, for

non-2,3,7,8-substituted congeners, the BSAF values and

their water solubilities are poorly correlated (data not

shown).

3.5. BSAF and d 15N

In the previous section, we demonstrated that con-

centrations of PCDDs/DFs and some of co-PCBs were

highly correlated with d 15N. Based on these observa-

tions, it is expected that BSAFs and d 15N may also be

correlated. Consequently, we performed regression ana-

lysis of the relationship between d 15N and log BSAF for

the 2,3,7,8-substituted PCDDs/DFs and co-PCB cong-

eners, and calculated the slope and the intercept of the

d 15N versus log BSAF plots. Table 5 presents the

log BSAF of the organisms and the slope, the r2 and pvalue of d 15N versus log BSAF plots. The BSAF values

for all of the 2,3,7,8-substituted CDDs decreased as the

Fig. 2. The relationship between ocatanol/water partition coefficient ðlog KowÞ and the log BSAF values of suzuki for 2,3,7,8-

substituted PCDDs/DFs and co-PCBs. Kow values were derived based on Govers and Krop (1998) for PCDDs/DFs and Hansen et al.

(1999) for co-PCBs.

Fig. 3. The relationship between water solubility for solid-phase chemical (log Ss, pg/l) and the log BSAF values of suzuki for 2,3,7,8-

substituted PCDDs/DFs and co-PCBs. Water solubility values (log Ss) of each compound were derived based on Ruelle and Kesselring

(1997).

356 W. Naito et al. / Chemosphere 53 (2003) 347–362

trophic level increased. This tendency was particularly

marked for congeners with a high degree of chlorination.

For 2,3,7,8-substituted CDFs, the slopes were positive

for tetra-congeners, and negative for penta-, hexa-,

hepta-, and octa-congeners. The absolute values of the

slopes for penta-, hexa-, hepta, and octa-CDF congeners

increased with an increase in the degree of chlorination.

For co-PCB congeners, the slopes were positive for

all congeners except congeners #77 and #81, with the

slopes of mono-ortho-congeners being greater than those

of non-ortho-congeners. The slopes increased with an

increase in the degree of chlorination, reached a peak for

hexachlorinated congeners, and decreased for the hepta-

congener. Besides, the slope of the log BSAF values

versus d 15N plots for 2,3,7,8-substituted CDDs/DFs and

co-PCBs is strongly correlated with log Ss and the r2 is

0.81 (Fig. 4). A linear regression obtained from the plot

of the slope versus log Ss was indicated below.

Slopeðlog BSAFs� d 15NÞ¼ 0:10 � log Ss� 0:53 ðr2 ¼ 0:81Þ ð2Þ

Table 5

LogBSAF values of biotaa and slope, r2 and p values of d15N and BSAF values for 2,3,7,8-substituted PCDDs/DFs and co-PCBs

Homo-

logue

Congeners PKT PLC Shellfish Fish Slopeb r2 p

MAC LNC HSC AKA SF STI GS MS CE SB

TCDD 2378 1.01 1.07 0.93 1.40 0.66 1.10 )0.04 0.092 0.563

PeCDD 12378 1.47 1.29 0.70 0.72 0.31 0.41 0.36 0.52 0.65 0.71 )0.08 0.58 )0.09 0.204 0.108

HxCDD 123478 0.84 0.37 0.55 )0.55 0.03 )0.62 0.00 )0.19 )0.88 )1.27 )0.55 )0.15 0.221 0.146

HxCDD 123678 0.92 0.18 0.47 )0.32 )0.14 )0.13 0.03 )0.14 0.14 )0.49 )0.19 )0.08 0.155 0.232

HxCDD 123789 0.82 0.13 0.37 )0.44 )0.28 )0.71 )0.20 )0.54 )0.54 )1.29 )1.08 )0.19 0.383 0.043

HpCDD 1234678 1.10 0.53 )0.17 )0.30 )0.94 )1.02 )1.30 )0.88 )1.08 )1.17 )1.99 )1.80 )0.30 0.443 0.011

OCDD OCDD 1.19 0.44 )0.34 )0.71 )1.21 )1.20 )2.24 )1.61 )1.47 )2.04 -3.06 )2.63 )0.45 0.523 0.005

TCDF 2378 1.15 0.17 0.48 0.52 )0.11 0.63 0.98 0.21 1.19 0.34 0.70 0.05 0.056 0.486

PeCDF 12378 1.05 )0.09 0.36 0.59 0.22 0.56 0.05 0.22 )0.01 0.001 0.935

PeCDF 23478 1.58 1.04 0.49 0.30 )0.08 )0.03 0.33 0.84 0.56 0.79 )0.06 0.52 )0.03 0.010 0.636

HxCDF 123478 1.04 0.52 0.14 0.23 )0.66 )0.61 )0.10 )0.57 )0.20 )1.12 )0.58 )0.16 0.278 0.071

HxCDF 123678 0.51 )0.29 0.02 )0.55 )0.48 )0.44 )0.15 )0.48 )0.10 )1.00 )0.60 )0.07 0.147 0.247

HxCDF 234678 1.15 0.59 0.19 )0.51 )0.37 )0.35 0.03 )0.32 )0.04 )0.78 )0.58 )0.14 0.239 0.091

HxCDF 123789 1.88 0.36 0.91 0.59 )0.72 0.06 )0.59 )0.84 )0.32 0.450 0.047

HpCDF 1234678 1.13 0.39 )0.14 )0.34 )0.94 )1.03 )1.33 )0.89 )1.11 )0.96 )1.71 )1.39 )0.25 0.389 0.019

HpCDF 1234789 1.29 0.36 )0.44 0.30 )0.93 )1.26 )0.55 )0.85 )0.72 )1.61 )1.22 )0.24 0.351 0.037

OCDF OCDF 1.20 0.14 )0.32 )0.54 )1.11 )1.26 )2.20 )1.62 )1.29 )1.73 )2.64 )2.03 )0.39 0.514 0.005

Non-ortho-

PCBs

3,4,40,5-TCB (81) 1.67 1.69 1.32 1.07 0.93 0.41 1.47 1.02 1.11 2.04 0.78 1.44 )0.02 0.010 0.711

3,30,4,40-TCB (77) 1.42 1.54 1.22 0.82 0.74 0.22 1.35 0.90 1.02 1.81 0.63 1.34 )0.01 0.001 0.874

3,30,4,40,5-PcCB (126) 1.53 1.82 1.23 1.31 0.95 )0.05 1.59 2.04 1.75 2.21 1.32 1.85 0.11 0.128 0.274

3,30,4,40,5,50-HxCB (169) 1.83 1.57 0.82 0.87 0.69 1.24 1.95 1.55 1.88 0.78 1.59 0.05 0.052 0.568

2,3,30,4,40,5-PeCB (123) 2.13 1.50 1.12 1.02 1.71 1.89 1.96 2.17 2.76 1.92 2.45 0.14 0.305 0.075

20,3,4,40,5-PeCB (118) 1.78 1.99 1.47 0.92 0.81 1.54 1.90 2.43 2.30 2.68 1.79 2.28 0.17 0.356 0.046

Mono-

ortho-

PCBs

2,3,30,40,5-PeCB (114) 2.02 1.50 1.22 1.12 1.93 2.37 2.30 2.69 1.75 2.43 0.15 0.359 0.065

2,3,30,4,40-PeCB (105) 1.67 1.84 1.37 0.85 0.75 1.50 1.76 2.24 2.17 2.58 1.64 2.11 0.15 0.320 0.061

2,30,4,40,5,50-HxCB (167) 2.05 1.33 0.91 0.81 1.55 1.83 2.52 2.37 2.68 1.87 2.36 0.21 0.422 0.029

2,3,30,4,40,50-HxCB (156) 2.07 1.20 0.99 0.89 1.46 1.84 2.59 2.44 2.71 1.87 2.34 0.21 0.414 0.032

2,3,30,4,40,50-HxCB (157) 2.02 1.36 1.06 0.96 1.76 2.53 2.31 2.57 1.79 2.22 0.17 0.387 0.053

2,3,30,4,40,5,50-HpCB (189) 1.64 0.86 0.89 0.79 1.36 2.16 2.07 2.22 1.35 1.79 0.14 0.307 0.094

a PKT¼plankton; PLC¼ polychaete; MAC¼mactidae; LNC¼ littleneck clam; HSC¼ hard-shell clam; AKA¼ akanishi; SF¼ stone flounder; STI¼ stinray; GS¼ gizzard shad;

MS¼marbled sole; Conger-eel¼CE; SB¼ sea bass; SED¼ sediment.b Slopes of the plots between 15N and BSAF values for biota from Tokyo Bay.

W.Naito

etal./Chem

osphere

53(2003)347–362

357

Fig. 4. The relationship between water solubility for solid-phase chemical (log Ss, pg/l) and the slopes of d 15N and log BSAF of

organisms for 2,3,7,8-substituted PCDDs/DFs and co-PCBs.

358 W. Naito et al. / Chemosphere 53 (2003) 347–362

4. Discussion

4.1. PCDDs/DFs and co-PCBs accumulation in biota

from Tokyo Bay

The results of this investigation showed that bio-

accumulation patterns of PCDDs/DFs and co-PCBs vary

greatly among congeners. The patterns of total PCDDs/

DFs and total TEQ-PCDDs/DFs reported by Broman

et al. (1992) from the Baltic Sea food webs are similar to

those observed in this study. Decreasing concentrations

of non-2,3,7,8-PCDDs/DFs congeners with an increase

in trophic level, imply that these congeners were effi-

ciently eliminated through the food chain, while the

concentrations of co-PCBs increased with an increase

in the trophic level. As shown in Table 3, 2,3,7,8-

substituted PCDD/DF congeners exhibited the charac-

teristics of both non-2,3,7,8-substituted PCDDs/DFs

and co-PCBs. The 2,3,7,8-substituted PCDDs/DFs

congeners with a lower degree of chlorination are similar

to co-PCB (i.e., increasing concentrations with an increase

in trophic level), whereas those with a higher chlorinated

PCDDs/DFs are similar to non-2,3,7,8-substituted cong-

eners (i.e., decreasing concentrations with an increase

in trophic level). Regardless of similar structures and

properties of PCDDs/DFs, the bioaccumulation poten-

tial of co-PCBs were significantly higher than that of

PCDDs/DFs. As can be seen from the results of this

study, the values of the slopes may serve as a good in-

dicator of the accumulation potential of the congeners

of PCDDs/DFs and co-PCBs.

Several studies have shown a congener-specific ac-

cumulation of PCDDs/DFs in organisms (e.g., Opper-

huizen et al., 1985; Van den Berg et al., 1986;

Opperhuizen and Sijm, 1990). Opperhuizen and Sijm

(1990) reviewed the literature on the bioconcentration

and biomagnification of PCDDs/DFs and proposed an

overall explanation of the bioaccumulation characteris-

tics into three groups in which 2,3,7,8-TeCDD like

congeners are taken up and eliminated at constant rate

on the basis of their physicochemical properties. Sec-

ondly, some of 2,3,7,8-unsubstituted congeners are

taken up at normal rate and eliminated rapidly due

to biotransformation and enzymatic oxidation. Third

group of congeners are taken up extremely low rate due

to the inhibited membrane permeation. Examples of

such congeners include OCDD and OCDF with a high

molecular structure. Furthermore, bioaccumulation of

hydrophobic compounds with a high Kow are less effec-

tive because these compounds tend to partition strongly

to sediment and decrease their bioavailability to organ-

isms (e.g., Loonen et al., 1994; Stange and Swackhamer,

1994; Kannan et al., 1998; Parkerton et al., 1993).

Broman et al. (1992) also reported the lack of food chain

biomagnification of compounds with a higher degree

of chlorination. Examples of such congeners include

OCDD and OCDF. Our result supported such studies

and concluded that the patterns of bioaccumulation

among PCDDs/DFs and co-PCBs are not solely ex-

plained by their physicochemical properties.

4.2. BSAF values of PCDDs/DFs and co-PCBs for biota

in Tokyo Bay

Due to their inherent chemical and physical proper-

ties, PCDDs/DFs and co-PCBs are expected to partition

primarily on sediment. Field monitoring and mesocosm

studies have demonstrated that the concentrations of

these compounds are generally too low to be measured

in a water column, unless they are in association with

W. Naito et al. / Chemosphere 53 (2003) 347–362 359

suspended solids or dissolved organic carbon (Pavlou

and Dexter, 1979; Tsushimoto et al., 1982). It has been

demonstrated that the concentration of hydrophobic

chemical in sediment can be related to tissue concen-

tration in aquatic species through the use of biota-

to-sediment accumulation factors (BSAFs) (Cook et al.,

1991; Kannan et al., 1998; Kannan, 1999). The BSAF

approach has been proposed for use as a regulatory tool

in risk assessment methodologies for contaminated

sediment (Starodub et al., 1996; Kannan et al., 1998).

As shown in Tables 3 and 5, the signs of the slopes in

the plots of d 15N versus the log concentrations of

2,3,7,8-substituted PCDDs/DFs and co-PCBs congeners

(slope I) are not always in accordance with those of the

slopes in the plots of d 15N versus log BSAF values

(slope II) for the corresponding congeners. The slopes of

some of the congeners have been reversed to the oppo-

site sign. This is explained by the lipid content that

varied among the organisms investigated in this study

(Table 1). The BSAF values were calculated using the

lipid-normalized concentrations in biota and the lipid

contents generally increased with an increase in the

trophic level. This explains the pattern that the magni-

tude of slope II values is smaller than that of slope I

values. A previous study (Kucklick and Baker, 1998)

and our results implied that bioaccumulation of PCDDs/

DFs and co-PCBs in the food web can be partly related

to an increase in the lipid content of biota.

The r2s of log BSAF values versus d 15N plots were

small in this study, probably because of the limited

number of samples investigated as well as significant

variation among concentrations. In general, the results

of this study indicated that the r2s were small for

congeners with small absolute values of the slope, while

their r2s were relatively large for congeners with large

absolute values of the slope. In addition, the results of

the BSAF analyses suggest that the accumulation po-

tential of co-PCBs in fish is significantly greater than

that of PCDDs/DFs. The accumulation potential of

these compounds was found to be in the order of mono-

ortho-PCBs > non-ortho-PCBs > 2,3,7,8-substituted con-

geners> non-2,3,7,8-substituted congeners.

In general, BSAF is location specific that has been

discussed in several parts of the world (Parkerton et al.,

1993; US EPA, 1993; Loonen et al., 1994; Kim et al.,

1996; Kannan et al., 1998; Kannan, 1999; Currie

et al., 2000; Sakurai et al., 2000). The BSAF values for

2,3,7,8-TCDD ranged from 0.03 to 0.20 for fish in Lake

Ontario and 0.05 for brown bullheads in the Fox River

near Green Bay (US EPA, 1993). The BSAF values for

2,3,7,8-TCDD in fish from Tokyo Bay estimated in this

study were approximately 10- to 100-fold higher than

those from other area. Since the BSAF values varied

greatly among species, sediment organic carbon, con-

taminant concentration and geography (Lake et al.,

1990; Kannan et al., 1998; Kannan, 1999). However, the

BSAF values derived in this study might be higher than

the ‘‘average’’ BSAF values for biota in Tokyo Bay.

Some possible explanations of such discrepancy among

BSAF values for aquatic organisms in Tokyo Bay were

discussed later.

The BSAF values calculated in this study for co-PCBs

were between 22 and 283 for piscivorous fish, sea bass,

whereas the congeners of 2,3,7,8-substituted PCDDs/

DFs were less than 5 except TeCDD. This implied

that co-PCBs possess significantly high bioaccumulation

potential compared to PCDDs/DFs. Parkerton et al.

(1993) found that the BSAFs for PCDDs/DFs in fish and

benthic organisms are lower than those for PCBs at the

same locations. BSAF for total PCBs were also varied

between locality, species and habitat characteristics of

organisms (Endicott and Cook, 1994; Froese et al.,

1998).

4.3. Bioaccumulation through the food web and water

solubility

The results of our study between d 15N and BSAF

relationship implied that some 2,3,7,8-substituted cong-

eners with lower degrees of chlorination (e.g. TeCDF)

and co-PCBs tend to be biomagnified through the food

web. The co-PCB congeners with a higher degree of

chlorination were especially marked by great biomag-

nification. In other words, BSAF values for biota in this

study indicated that fish occupying the top of the food

web accumulated more co-PCBs than benthic organisms

belongs to a lower trophic level, implying that trophic

transfer (i.e., biomagnification) is the important process

determining levels of highly chlorinated congeners for

co-PCBs in aquatic biota. This pattern was supported by

Zaranko et al. (1997) who concluded from their study

regarding biomagnification of PCBs through a riverrine

food web that biomagnification through trophic transfer

is the primary mechanism governing contaminant levels

in biota and not bioconcentration.

The relationship between log Kow and log BSAF for

2,3,7,8-substituted congeners and co-PCBs observed in

this study were in accordance with that of the previous

studies (e.g., Muir et al., 1985; Opperhuizen and Sijm,

1990). Collectively, BSAF values for PCDD/DFs and

other organochlorine have been shown to have a para-

bolic relationship with log Kow, with highest BSAFs

observed at approximately log Kow ¼ 6:0–6.5, and dras-

tically declined as Kow value increases. A negative rela-

tionship of log Kow and BSAF for superhydrophobic

congeners has also been reported in other studies (Lake

et al., 1990; Kannan et al., 1998; Kannan, 1999).

The results of the analyses for the BSAF values for

sea bass and the slope of the plot of d 15N and BSAF

showed that they are correlated with water solubility

of 2,3,7,8-substituted PCDDs/DFs and co-PCB cong-

eners. This suggested that BSAF values increased with

360 W. Naito et al. / Chemosphere 53 (2003) 347–362

an increase in the trophic level for the congeners with

high water solubility, whereas the BSAF values de-

creased with an increase in the trophic level for the

congeners with low water solubility. This implied that

water solubility of the 2,3,7,8-substituted PCDDs/DFs

and few co-PCBs congeners has a great influence upon

bioaccumulation process of the compounds. Some pos-

sible explanations are as follows; Congeners with high

water solubility likely would have more bioavailable

dissolved phase in the water column. These congeners

tend to accumulate during intestinal and gill absorption

and less metabolized in aquatic organisms. Congeners

with low water solubility likely have less bioavailable

phase in the water column because these compounds

show preferential retention in particulated organic

matter or sediment (Maruya et al., 1997; Kannan, 1999).

In addition to this, steric hindrance and membrane

permeation resistance would slow the uptake process of

greater chlorinated congeners during intestinal and gill

absorption in aquatic organisms (Opperhuizen et al.,

1985; Loonen et al., 1994; Kannan et al., 1998). Water

solubility of a individual congener is, therefore, an im-

portant determinant for governing accumulation pat-

terns of PCDDs/DFs and co-PCBs.

From Figs. 2–4, Kow or water solubility and the

2,3,7,8-substituted PCDDs/DFs and co-PCBs congeners

were highly correlated. However, to be specific, co-PCB

congeners seem to be poorly correlated. Due to the

limited data available in our study, it is difficult to

identify such relationship for co-PCB congener profile.

A possible explanation of this could be that sediment

concentrations of some congeners such as 3,4,40,5-

TCB(#81), 3,30,4,40,5,50-HxCB(#169), and 2,3,30,4,40,5-

PeCB(#123) in this study were nearly detection limits

therefore this might have influenced this contradiction.

Although such uncertainty must be confirmed with more

data, the result shows that the BSAF values and the

slope of d 15N versus the log BSAF plot can be esti-

mated using equations (1) and (2), respectively, using

water solubility of the congeners of 2,3,7,8-substituted-

PCDDs/DFs and co-PCBs. This suggests that the BSAF

value for any combination of a specific congener and a

specific organism can be estimated based on the d 15N

value of an organism.

4.4. Uncertainties in sampling sites and the mobility of

organisms

Concentrations of PCDDs/DFs in sediment of

Tokyo Bay reported in this study were one order of

magnitude less than that reported in previous study (e.g.

Sakurai et al., 2000). Despite similar congener profiles in

both the studies, the different concentrations can be

explained as different sampling location/date/season,

different species of fish which have different movements/

food habit and also the influence of the organic carbon

determination among the studies.

Although such uncertainties are present in the data

analyzed in this study, since there are few studies that

have attempted to quantitatively analyze the relation-

ship between specific congener concentrations of

PCDDs/DFs and co-PCBs and the d 15N values for biota

in Tokyo Bay, the results of our study would provide

valuable information to understand the accumulation

properties of PCDDs/DFs and co-PCBs.

5. Conclusions

The bioaccumulation patterns of PCDDs/DFs and

co-PCBs in biota from Tokyo Bay are probably best

explained by a combination of various factors such as

physicochemical properties of the compounds and bio-

transformation, food selection, and habitat characteris-

tics of organisms. Furthermore, our results suggested

that the slopes of the plots of BSAF values and d 15N

varied among the congeners and the slopes and the

water solubility for the congeners of 2,3,7,8-substituted

PCDDs/DFs and co-PCBs were highly correlated. This

suggested that the congeners with relatively high water

solubility tend to accumulate with an increase in trophic

level in the food web, while the congeners with low water

solubility tend to be less accumulated or eliminated with

an increase in the trophic level. Water solubility of a

congener can be, therefore, an important determinant

governing bioaccumulation of PCDDs/DFs and co-

PCBs in aquatic environment.

The results of this study suggested that BSAF in

a specific organism for specific congeners of 2,3,7,8-

substituted PCDDs/DFs and co-PCBs could be estimated

using the relationship between water solubility of spe-

cific congeners and the slope of log BSAF versus d 15N

plot. It would be possible to estimate concentrations of

2,3,7,8-substituted PCDDs/DFs and co-PCB congeners

in aquatic organisms in aquatic biota using the equation

that was formulated based on the concentrations of

these compounds in representative organisms and sedi-

ment. Such information could be used to assess the

health effects of 2,3,7,8-substituted PCDDs/DFs and co-

PCBs on those who consume fish and shellfish from the

aquatic biota.

Acknowledgements

This research was supported by CREST (Core Re-

search for Evolutional Science and Technology) of the

Japan Science and Technology Corporation (JST) and a

grant-in-aid for Scientific Research (no. 11680527) from

Japanese Ministry of Education, Science, Sports and

Culture. The authors thank Isamu Ogura for helping to

W. Naito et al. / Chemosphere 53 (2003) 347–362 361

derive water solubility values of the compounds. The

authors thank K. Senthil Kumar for providing valuable

comments and helping to improve the standard of

English of the manuscript.

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Wataru Naito is a research scientist at Research Centre forChemical Risk Management (CRM), National Institute ofAdvanced Industrial Science and Technology (AIST). He re-ceived his B.S. in Environmental Science from Virginia Poly-technic Institute and State University (Virginia Tech) in 1996and his Ph.D. in engineering from Yokohama National Uni-versity, Japan. His current work activities include developmentof methods for predicting POPs bioaccumulation levels inaquatic organisms, ecological risk assessment of chemicals, riskanalysis.

Jiancheng Jin is a former graduate student at Yokohama Na-tional University, Japan. He received his master�s degree inengineering from Yokohama National University in 2001. Thetopic of his thesis was the analyses of the levels of dioxin-like-compounds in biota from Tokyo Bay. He is currentlyworking for a private corporation as a systems engineer.

Youn-Seok Kang is a postdoctoral fellow of CREST, JapanScience and Technology Corporation. He received his doctoraldegree from Ehime University, Japan. His research interests arein the analyses of dioxin-like-compounds in various media suchas biota, sediment and humans. He is currently working atLabFrontier Co. Ltd., Korea.

Dr. Yamamuro is a senior researcher at Institute for MarineResources and Environment, National Institute of AdvancedIndustrial Science and Technology. She has worked on bio-geochemical cycling of carbon, nitrogen and phosphorous inshallow waters. Her special interest has been paid to the role ofmacrosized organisms, such as fish, bivalves and birds, in thematerial cycling.

Shigeki Masunaga is a professor at Graduate School of Envi-ronment and Information Sciences, Yokohama National Uni-versity. Prior to his professorship, he was a senior researcher atNational Institute for Pollution and Resources. He received hisdoctoral degree in Engineering from the University of Tokyo.His major interest is to study behaviors of chemical pollutantsin the environment.

Junko Nakanishi is a Professor at Graduate School of Envi-ronment and Information Sciences, Yokohama National Uni-versity and director at Research Center for Chemical RiskManagement (CRM), National Institute of Advanced Indus-trial Science and Technology (AIST). She received her Ph.D. inEngineering from the University of Tokyo.