dynamics of pcdds/dfs and coplanar-pcbs in an aquatic food chain of tokyo bay
TRANSCRIPT
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: [email protected] (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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etal./Chem
osphere
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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osphere
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
etal./Chem
osphere
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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.