DSpace at VNU: Accumulation features of persistent organochlorines in resident and migratory birds from Asia

Environmental Pollution 125 (2003) 157–172
www.elsevier.com/locate/envpol

Accumulation features of persistent organochlorines in resident
and migratory birds from Asia
Tatsuya Kunisuea, Mafumi Watanabea, Annamalai Subramanianb,
Alagappan Sethuramanb, Alexei M. Titenkoc, Vo Quid,
Maricar Prudentee, Shinsuke Tanabea,*
a
Center for Marine Environmental Studies, Ehime University, Tarumi 3-5-7, Matuyama 790-8566, Japan
Center of Advanced Studies in Marine Biology, Annamalai University, Parangipettai 608502, Tamil Nadu, India
c
Plague Control Research Institute of Siberia and Far East, 78 Trillsser St., Irkutsk 664047, Russia
d
Center for Natural Resources and Environmental Studies, Vietnam National University, 19 Le Thanh Tong Street, Hanoi, Viet Nam
e
Science Education Department, De La Salle University, 2401 Taft Avenue, 1004 Manila, Philippines
b

Received 17 April 2002; accepted 21 February 2003

‘‘Capsule’’: Accumulation features of persistent organochlorines in migratory birds from Asia did not necessarily reflect
only the pollution in the sampling area.
Abstract
Concentrations of organochlorine contaminants including polychlorinated biphenyls (PCBs), dichlorodiphenyltrichloroethane
and its metabolites (DDTs), hexachlorocyclohexane isomers (HCHs), chlordane compounds (CHLs), hexachlorobenzene (HCB)
were determined in the resident and migratory birds, which were collected from India, Japan, Philippines, Russia (Lake Baikal) and
Vietnam. Accumulation patterns of organochlorine concentrations in resident birds suggested that the predominant contaminants
of each country were as follows: Japan—PCBs Philippines—PCBs and CHLs, India—HCHs and DDTs, Vietnam—DDTs, and
Lake Baikal—PCBs and DDTs. The migratory birds from Philippines and Vietnam retained mostly the highest concentrations of
DDTs among the organochlorines analyzed, indicating the presence of stopover and breeding grounds of those birds in China and

Russia. On the other hand, migratory birds from India and Lake Baikal showed different patterns of organochlorine residues,
reflecting that each species has inherent migratory routes and thus has exposure to different contaminants. Species which have
breeding grounds around the Red Sea and Persian Gulf showed high levels of PCBs, indicating the presence of areas heavily polluted by PCBs in the Middle East.
# 2003 Elsevier Science Ltd. All rights reserved.
Keywords: Organochlorines; Resident birds; Migratory birds; Asia

1. Introduction
Persistent organochlorines including PCBs (polychlorinated biphenyls), DDTs (dichlorodiphenyltrichloroethane and its metabolites) and HCHs
(hexachlorocyclohexane isomers) are of great concern as
environmental contaminants due to their bioaccumulative nature and chronic adverse effects on humans and
wildlife. Though these chemicals were banned for manufacture and use in many developed countries during
1970s, they are still used in some developing countries
* Corresponding author. Tel./fax: +81-89-946-9904.
E-mail address: (S. Tanabe).

for public health purposes and to solve problems caused
by increasing population.
In Vietnam, high concentrations of DDTs have been
detected in various foodstuffs involving rice, fish and
meat (Kannan et al., 1992, 1997). It seems that DDT is
still being used for malaria eradication in Vietnam,
while this chemical was banned for agricultural purposes in 1993. In addition, the usage of HCHs and HCB
have been detected in recent investigation of sediments
from north Vietnam shoreline (Nhan et al., 1999).
In India, we conducted extensive investigations on the
contamination of various abiotic and biotic matrices,
and found HCHs residues as predominant contaminant
(Kannan et al., 1993a, 1995; Ramesh et al., 1990, 1991,

0269-7491/03/$ - see front matter # 2003 Elsevier Science Ltd. All rights reserved.

doi:10.1016/S0269-7491(03)00074-5


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T. Kunisue et al. / Environmental Pollution 125 (2003) 157–172

1992; Tanabe et al., 1993, 1998). The cumulative consumption of HCHs in India until 1985 was 575,000 t,
and since then about 45,000 t of HCHs had been used
annually (Kannan et al., 1995). It has been estimated
that usage of HCHs exceeds 1,000,000 t (Kannan et al.,
1995). Additionally, the agricultural chemical industry
in India has developed dramatically, because legal regulation regarding manufacture and use of various
chemicals is not formulated sufficiently (Dave, 1996).
In the Philippines, elevated levels of CHLs were
reported in soils around a major open dumpsite and it
was indicated that CHLs were still used for public
health purposes, whereas contamination of agricultural
fields with organochlorines was much lower than in
other developing countries in Asia due to the imposition
of strict legal regulations on the manufacture, use and
selling (Lee et al., 1997a).
China consumed almost equal amounts of HCHs as
that of India, until its use was prohibited in 1983 (Li et
al., 1996). DDT was also manufactured and widely used
until the same year. The total cumulative usage of DDT
and HCHs was estimated to have exceeded 10,000 and
100,000 t, respectively (Voldner and Li, 1995). Relatively high concentrations of DDTs and HCHs were
detected in fishes, soils and sediments in China, and the
levels were gradually declining in recent years (Wu et

al., 1997; Zhu et al., 1999).
In Russia, about 130,000 t of PCBs were manufactured (Ivanov and Sandell, 1992). While DDT was
excluded from the official list of chemicals in 1969, its
manufacture, usage and environmental contamination
were reported (Fedorov, 1999). HCH has also been used
widely for agricultural purposes (Fedorov, 1999), and
its contamination has also been reported high in the
Black Sea (Tanabe et al., 1997), Caspian Sea (Watanabe
et al., 1999) and Lake Baikal (Iwata et al., 1995).
Japan, the most developed country in Asia, is known
to have serious PCBs contamination in various
environmental media and biota (Guruge et al., 1997;
Minh et al., 2001; Monirith et al., 2000; Prudente et al.,
1997). About 60,000 t of PCBs were manufactured during the period of 1955–1972. Even after manufacture
was banned in 1972, PCBs in electric equipment such as
old transformers and capacitors that were dumped and
stored have been continuously leached into the
environment. In addition, concentrations of CHLs were
higher in fishes from Japan than from other Asian
countries, because this chemical was extensively used as
a termiticide until 1986 (Lee et al., 1997b).
Therefore, organochlorines seem to still contaminate
the Asian environment and may cause adverse effects in
wildlife and humans.
Avian species are useful bioindicators for monitoring
organochlorine contamination of the environment,
because they are often at relatively high positions in the
food chain. Resident birds, which principally have

localized feeding and breeding areas throughout the

year, reflect the background pollution of inhabiting area
through the levels of contaminants in their bodies. On
the other hand, it is suspected that migratory birds
reflect not only local but also global contamination
since they migrate between a wide range of breeding,
stopover and wintering grounds. However, there is little
information regarding the accumulation of organochlorines in the birds, especially migratory birds, in
Asia.
We previously studied accumulation of organochlorines in various birds collected from India (Tanabe
et al., 1998), Vietnam (Minh et al., 2002), and Lake
Baikal in Russia (Kunisue et al., 2002). We reported the
dominant organochlorines in resident birds were HCHs
in India, DDTs in Vietnam, and PCBs and DDTs in
Lake Baikal, Russia, and indicated that exposure to
these contaminants in migratory birds in wintering
grounds might have adversely affected their breeding
activities. However, it is not known which of the breeding grounds, stopover sites and wintering grounds are
associated with significant exposure of the Asian
migratory birds to these compounds. In this study, we
additionally analyzed organochlorines in resident and
migratory birds collected from the Philippines and
India, where migratory birds are wintering every year,
and those in resident birds collected from Japan, a main
stopover site for the Asian migratory birds. The accumulation features of organochlorines in migratory birds
collected from Asian countries are considered using the
data that were reported previously and collected from
this study. We also tried to determine which are the
major sites at which the Asian migratory birds are
exposed to organochlorines on the basis of the accumulation features of organochlorines in resident birds,
those in various biota reported previously, and existing

ecological data for migratory birds.

2. Materials and methods
2.1. Samples
Resident and migratory birds (n=400) were collected
from the wetland and coastal areas of Caratagan in
Philippines on April and December 1994 (n=43), Cuddalore, Parangipettai, Pudukottai and Mandapan in
southern India on November 1995 and March 1998
(n=101), Selenga Delta along Lake Baikal in Russia on
September 1996 and May 1997 (n=98), Con Lu Island
in northern Vietnam on March and October 1997
(n=107), and various regions in Japan from 1993 to
1998 (n=51, only resident birds) (Fig. 1; Appendices A–
C). The biometric data (sex, standard length, and body
weight) were recorded (data not shown) and all the
birds were then defeathered. The pectoral muscles and


T. Kunisue et al. / Environmental Pollution 125 (2003) 157–172

Fig. 1. Map showing sampling locations of birds.

livers removed from their bodies with a dissective scalpel, and the whole body were homogenized using a
homogenizer, and then stored in deep-freezer at À20  C
until analysis.
Based on the studies by Hoyo et al. (1996) and Ali
(1996), avian species analyzed in this study were classified into four groups, namely (1) resident birds, which
live almost in the same region all through the year for
their entire life span; (2) local migrants, which migrate
only between northern and southern Indian regions (e.g.

black-winged stilt, kentish plover and little ringed plover from India); (3) short-distance migrants, which have
their breeding grounds (e.g. species from Philippines,
Vietnam, and common redshank, long-billed mongolian
plover from India) or wintering grounds (species from
Lake Baikal) in central China to Japan, and have their
breeding grounds in western Asia to Middle East
(white-cheeked tern, little tern and whiskered tern from
India); and (4) long-distance migrants, which have their
breeding grounds in wide range of northeastern Europe
to southeastern Russia (e.g. species from Philippines,
Vietnam, and species except lesser-crested tern from
India), southern Europe (lesser-crested tern from India),
and have their wintering grounds in southwestern to
southeastern Asia (species from Lake Baikal), for the
accurate elucidation of accumulation features.
2.2. Chemical analysis
Organochlorine pesticides and PCBs in the wholebody homogenates, pectoral muscles and livers were

159

analyzed following the method described by Tanabe et
al. (1998). Briefly, samples were homogenized with
anhydrous sodium sulfate and Soxhlet extracted with a
mixture of diethyl ether and hexane (3:1) for 7 h. After
Kuderna–Danish (K–D) concentration of the extract, 2
ml of the aliquot were dried at 80  C to determine lipid
contents. The remaining extract was added to a 20 g
Florisil packed glass column and then dried by passing
nitrogen gas. Organochlorines adsorbed onto florisil
were eluted with 150 ml of 20% water in acetonitrile

to a separatory funnel containing hexane and water.
After partitioning, hexane layer was concentrated and
then cleaned with concentrated sulfuric acid. The
cleaned extract was fractionated by passing through a
column of 12 g of activated florisil and eluted with
hexane (first fraction) followed by 20% dichloromethane in hexane (second fraction). The first fraction
contained PCBs, HCB, p,p0 -DDE and trans-nonachlor,
and the second fraction contained p,p0 -DDT,
p,p0 -DDD, HCH isomers (a-, b-, and g-), cis-nonachlor, trans-nonachlor, cis-chlordane, trans-chlordane,
and oxychlordane.
The quantification of organochlorine residues was
performed using a gas chromatograph (Hewlett-Packard
6890 series) equipped with ECD (electron capture
detector) and an automatic injector (Hewlett-Packard
7683 series). The GC column used was a fused silica
capillary (DB-1; J&W Scientific, 30 m length, 0.25 mm
i.d. and 0.25 mm film thickness). Helium was used as the
carrier gas while nitrogen was the make-up gas. The
concentration of individual organochlorines was quantified from the peak area of the samples to that of the
corresponding external standard. The PCB standard
used for quantification was an equivalent mixture of
Kanechlor preparations (KC-300, KC-400, KC-500 and
KC-600) with known PCB composition and content.
Concentrations of individually resolved peaks of PCB
isomers and congeners were summed to obtain total
PCB concentrations. Recoveries through this analytical
method were 97.0 Æ 4.2% for PCBs, 105.0 Æ 5.7% for
DDTs, 98.9 Æ 6.3% for HCHs, 103.9 Æ 4.3% for CHLs
and 104.1 Æ 7.9% for HCB, respectively. Concentrations
were not corrected for recovery rates.

For quality assurance and quality control, our
laboratory participated in the Intercomparison Exercise
for Persistent Organochlorine Contaminants in Marine
Mammal Blubber organized by the National Institute of
Standards and Technology (Gaithersburg, MD) and
Marine Mammal Health and Stranding Response Program of the National Oceanic and Atmospheric
Administration’s National Marine Fisheries Service
(Silver Spring, MD). Standard reference material SRM
1945 was analyzed for selected PCB congeners and persistent organochlorines. Reliable results were obtained
by comparison of data from our laboratory with those
from material reference values.


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T. Kunisue et al. / Environmental Pollution 125 (2003) 157–172

Fig. 2. Mean relative concentrations of organochlorines to PCBs in
resident birds from various Asian countries.

3. Results and discussion
3.1. Accumulation features in resident birds
The concentrations of organochlorines and mean
relative concentrations of other organochlorines to
PCBs in resident birds from each country are shown in
Appendices A, B and Fig. 2. A wide variation of organochlorine concentrations was observed among avian
species because they were collected and analyzed in a
wide range of avian species from different nutritive
phases (Appendices A and B). So, we evaluated the
accumulation features of organochlorines by estimating

their relative concentrations (Fig. 2), because this
approach makes the range of absolute concentrations
among species small and it is also easy to understand
which organochlorines mainly remain in avian species.
In resident birds from Japan, PCBs were the dominant contaminants, followed by DDTs > CHLs >
HCHs > HCB (Fig. 2). This pattern of organochlorine
concentrations is commonly found in other biota from
Japan (Lee et al., 1997b; Monirith et al., 2000). This
result suggests that notable PCBs contamination of
biota in Japan is still occurring.
The accumulation pattern in resident birds from
Philippines was similar to that from Japan, and relative
concentration for CHLs was higher than that from
other countries (Fig. 2), while the residue levels of

organochlorines were generally low (Appendix A). In
the Philippines, elevated concentrations of CHLs in
dumpsite soils and sediments were reported and the use
of CHLs for public health purposes was suspected (Lee
et al., 1997a). The accumulation pattern in resident
birds from the Philippines observed in present study
supports the above fact.
In resident birds from Lake Baikal in Russia, the
highest relative concentration of PCBs was recorded,
followed by DDTs. In contrast to these chemicals, the
residue levels of HCHs and CHLs were relatively low
(Fig. 2). It is reported that high concentrations of PCBs
and DDTs were detected in Baikal seals (Phoca sibirica)
and fishes collected from Lake Baikal (Kucklick et al.,
1994; Nakata et al., 1995). In addition, the study investigated residue levels in air, water and soil from the

Lake Baikal region suggested that there was potential
input of PCBs and DDTs into the watershed of this lake
(Iwata et al., 1995).
The accumulation patterns of organochlorines in
resident birds from India and Vietnam were notably
different from those in birds from Japan, Philippines
and Lake Baikal (Fig. 2). In resident birds from India,
HCHs were the dominant contaminant, followed by
DDTs > PCBs > CHLs5HCB. On the other hand, the
resident birds from Vietnam revealed a predominance of
DDTs and relatively low residue levels for other organochlorines. These observations imply that these countries are still using organochlorine insecticides such as
HCHs and DDTs for agricultural and public health
purposes. In fact, we previously reported relatively high
ratios of p,p0 -DDT and a-HCH (compounds abundantly present in technical DDT and HCH) in some
resident species from Vietnam and India, respectively
(Minh et al., 2002; Tanabe et al., 1998). Vietnam is predominantly an agricultural country and has used pesticides for various agricultural crops including rice and
sugar cane. High concentrations of DDTs have been
detected from various foodstuffs such as rice, fish, meat
etc. (Kannan et al., 1997), even though use of this chemical for agricultural purposes was banned in Vietnam
in 1993. High residue levels of DDTs and particularly
HCHs have also been detected in various biotic and
abiotic samples from India; use of HCHs continued in
India until very recently (Kan-atireklap et al., 1998;
Kannan et al., 1993a; Ramesh et al., 1990, 1991, 1992;
Tanabe et al., 1993, 1998, 2000).
Among birds analyzed in this study, black-winged
stilt, little ringed plover and kentish plover collected
from India are described as ‘local migrants’, which travel between the Himalayas and southern India (Ali,
1996), and so these birds can be considered as almost the
resident birds of India and they also indicate pollution

status of various regions in India. These three species had
relatively high levels of DDTs and HCHs (Fig. 3). Calamari et al. (1991) reported that concentrations of HCHs


T. Kunisue et al. / Environmental Pollution 125 (2003) 157–172

161

in their bodies (Fig. 4). Interestingly, in all the migratory birds from the Philippines and Vietnam, DDTs
were the most dominant organochlorines. This indicates
that many migratory species wintering in these two
countries are migrating and feeding in areas of high use
of DDT on their migratory routes, while migrants from
Vietnam may be exposed to DDTs in Vietnam also
while wintering there. On the other hand, in migratory
birds from India and Lake Baikal, the dominant organochlorine varied between species, indicating that
migratory birds wintering or breeding in these two
countries may have species-specific migratory routes.
In addition, accumulation patterns in birds of ‘shortdistance’ and ‘long-distance’ migration (Fig. 5) were
apparently different from those in resident birds (Fig. 2),
except migratory birds from Vietnam and short-distance
migrants from Lake Baikal. These results suggest that
accumulation features of organochlorines in migratory
birds reflect not only the status of pollution in area of
collection, but also those in stopover sites, breeding and
wintering grounds.

Fig. 3. Organochlorine residue patterns in local migratory birds collected from India. Relative concentration indicates ratio of individual
organochlorine concentration to that of PCBs, which was treated as 1.0.

in plants and air from northern Indian regions were
higher than those from 25 other areas of the world. In
addition, Nayak et al. (1995) and Senthilkumar et al.
(1999) reported that relatively high levels of DDTs and
HCHs were detected in water and dolphins from the
Ganges River. These observations imply that pollution
sources of these chemicals are still present in India and
resident and migratory birds may be exposed to these
contaminants throughout this country.
Collectively, these results suggest that the dominant
organochlorine contaminants in Japan, Philippines,
India, Vietnam, and Lake Baikal were PCBs, PCBs and
CHLs, HCHs and DDTs, DDTs, and PCBs and DDTs,
respectively.
3.2. Accumulation features in migratory birds
The migratory birds analyzed in this study were classified according to dominant residues of organochlorines

3.2.1. Short-distance migrant
Concentrations of organochlorines and their mean
relative concentrations to PCBs in short-distance
migrants were shown in Appendix C and Fig. 5,
respectively. In short-distance migrants from the Philippines and India, DDTs and PCBs were the dominant
contaminants, respectively, while PCBs and HCHs were
the dominant contaminants in resident birds. It is
known that many species of short-distance migrants
collected from India have their breeding grounds
around Persian Gulf, Red Sea and Caspian Sea (Hoyo
et al., 1996). Relative concentrations of PCBs accumulated in these species were higher than in resident birds
from India, indicating that there may be notable PCBs
contamination around their breeding grounds. High

concentrations of PCBs were also detected in Caspian
seals (Phoca caspica) and fishes from Caspian Sea, and
PCBs release into this environment might be continuing
(Kajiwara et al., 2002; Watanabe et al., 1999).
The accumulation pattern in short-distance migrants
from the Philippines was almost similar to that from
Vietnam (Fig. 5). In both countries, the relative concentrations of HCHs in short-distance migrants were
slightly higher than those in resident birds. These results
indicate that short-distance migrants collected from
Philippines and Vietnam may have their breeding
grounds or stopover sites in China, since China is
known to have widely used HCHs and DDTs (Li et al.,
1996). Relatively high concentrations of DDTs and
HCHs were detected in fishes from Lake Baiyangdian
situated about 300 km south of Beijing and in soils and
sediments from Lake Ya-Er along the middle-lower
reaches of the Yangtze River, respectively, although
their concentrations had been gradually declining (Wu


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T. Kunisue et al. / Environmental Pollution 125 (2003) 157–172

Fig. 4. Classification of migratory avian species from Philippines, Vietnam, India and Russia—Lake Baikal based on dominant organochlorine
residues in their bodies. RB in a square represents resident bird. >PCBs and >HCHs show second dominant organochlorine.

Fig. 5. Organochlorine residue patterns in short-distance (S) and long-distance (L) migratory birds collected from Philippines, Vietnam, India and
Russia—Lake Baikal. Relative concentration indicates ratio of individual organochlorine concentration to that of PCBs, which was treated as 1.0.

et al., 1997; Zhu et al., 1999). However, it was suspected
that short-distance migrants collected from Vietnam
might have been exposed to DDTs not only in their
breeding grounds or stopover sites but also in Vietnam
itself, because Vietnamese environment was highly polluted by DDTs as evidenced by the fact that resident birds
showed elevated levels of DDTs (Fig. 2 and Appendix A).

Accumulation pattern in short-distance migrants
from Lake Baikal was comparable to that in resident
birds (Figs. 2 and 5), implying that many species of
short-distance migrants from Lake Baikal may be wintering in the areas which have similar contamination
pattern as in Lake Baikal, or may be less exposed to
organochlorines in their wintering ground.


T. Kunisue et al. / Environmental Pollution 125 (2003) 157–172

3.2.2. Long-distance migrant
Accumulation patterns of organochlorines in longdistance migrants from India and Lake Baikal (Fig. 5)
were different from those in resident birds (Fig. 2) and
short-distance migrants (Fig. 5).
In long-distance migrants collected from India, DDTs
were the dominant contaminants, suggesting that longdistance migrant species may have different stopover
sites, breeding and wintering grounds from short-distance migrants. It is known that long-distance migrants
from India principally have their breeding grounds in
Russia (Hoyo et al., 1996). Noticeably high levels of
DDTs were detected in ringed seals (Phoca hispida)
from the Russian Arctic, suggesting the presence of significant local sources of DDTs in a wide range of this
region (Nakata et al., 1998). Considering the earlier,
long-distance migrants collected from India may have

their breeding grounds in Russia, while short-distance
migrants collected may have those in Middle Eastern
Asia. In addition, it is suspected that China may be a
possible stopover site for these species, and it is a
dominant source of DDTs contamination.
In long-distance migrants from Lake Baikal, levels of
DDTs and HCHs were higher than in resident birds
(Fig. 5). It has been reported that pollution sources of
DDTs are present in the watershed of Lake Baikal
(Iwata et al., 1995, Nakata et al., 1995). However, PCBs
were the dominant contaminants and levels of HCHs
were relatively low in resident birds from Lake Baikal
(Fig. 2). Considering the accumulation pattern found in
resident birds, it is suspected that long-distance
migrants collected from Lake Baikal have wintering
grounds in tropical Asia such as Vietnam and India, or
their stopover sites in China.
Long-distance migrants from the Philippines and
Vietnam showed almost similar trends to short-distance
migrants (Fig. 5), indicating that long-distance migrants
might be exposed to high level of DDTs in their stopover site and breeding ground in China and Russia, or
in their wintering ground in Vietnam. In addition, relative concentrations of HCHs in long-distance migrants
from the Philippines and Vietnam were slightly higher
than those in short-distance migrants. This indicates
that long-distance migrants are exposed to HCHs in
Arctic regions, which are known to be polluted by
HCHs due to the long-range atmospheric transport
from the south (Muir et al., 1999).
3.3. Species-specific accumulation
Accumulation patterns of organochlorines in same

species of migratory birds are shown in Fig. 6a and b.
Kentish plovers from the Philippines and Vietnam and
whiskered terns from India and Vietnam, which are
short-distance migrants, showed similar accumulation
patterns (Fig. 6a). This indicates that these two species

163

collected from each country are exposed to similar pollution sources of organochlorines on their migratory
routes. Given the accumulation pattern of resident birds
(Fig. 2), it seems likely that kentish plovers from the
Philippines are mainly exposed to contaminants in
breeding grounds or stopover sites rather than in their
Philippine wintering ground. In kentish plovers from
Vietnam, relative concentration of HCHs was higher
than that in resident birds, while this species was suggested to be exposed to DDTs in Vietnam. In addition,
accumulation pattern of kentish plovers from Vietnam
was extremely similar to that from the Philippines. This
result implies that kentish plovers wintering in the Philippines and Vietnam may have identical breeding
grounds and stopover sites. On the other hand, it is
ecologically known that whiskered terns wintering in
India have their breeding grounds around Caspian Sea,
while ones wintering in Vietnam have their breeding
grounds around eastern region in China (Hoyo et al.,
1996). This indicates that pollution patterns of organochlorines between the regions around Caspian Sea and
the eastern China may be similar, that is,
DDTs > PCBs > HCHs > CHLs=HCB.
Relative concentrations of HCHs were higher in
common redshanks from Vietnam than in birds from
India, and the whole pattern of organochlorines differed

between birds from these two regions. Accumulation
pattern of organochlorines in this species from India
was similar to that in whiskered terns, indicating that
these two species might migrate from almost similar
breeding ground to India. On the other hand, the accumulation pattern of organochlorines in common redshanks from Vietnam was similar to that in kentish
plovers except for HCHs. This implies that common
redshanks from Vietnam may migrate from agricultural
fields of China to Vietnam.
In little terns and long-billed mongolian plovers,
accumulation pattern of organochlorines was apparently different between sampling locations (Fig. 6a).
Little terns that winter in southern India have breeding
grounds around the Red Sea, Persian Gulf or Caspian
Sea, whereas those that winter in northern Vietnam
have breeding grounds in eastern China (Hoyo et al.,
1996). The accumulation patterns in organochlorines
reflected differences in migratory routes. Given the differences in accumulation pattern of migrant and resident birds (Fig. 2), it is suggested that little terns from
India are greatly exposed to PCBs in their breeding
grounds.
In long-billed mongolian plovers, DDTs were the
dominant organochlorines in the Philippines and Vietnam, but HCHs were dominant in India (Fig. 6a). This
trend was also observed in short-billed mongolian plovers
from these three countries (Fig. 6b). Though the reason
for this pattern is unclear, birds collected from India may
be influenced by HCH applications. Considering the high


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T. Kunisue et al. / Environmental Pollution 125 (2003) 157–172

Fig. 6. (a) Organochlorine residue patterns in same species among short-distance migratory birds collected from Philippines, Vietnam, India and
Russia—Lake Baikal. Relative concentration indicates ratio of individual organochlorine concentration to that of PCBs, which was treated as 1.0;
(b) Organochlorine residue patterns in same species among long-distance migratory birds collected from Philippines, Vietnam, India and Russia—
Lake Baikal. Relative concentration indicates ratio of individual organochlorine concentration to that of PCBs, which was treated as 1.0.

relative concentrations of PCBs, it is suggested that
long- and short-billed mongolian plovers collected from
India have different migratory routes from those from
the Philippines and Vietnam, and they have stopover
and breeding grounds that are highly contaminated by
PCBs than by DDTs.
DDTs were the predominant contaminants in terek
sandpipers from India and Vietnam (Fig. 6b). However,
sandpipers from India accumulated relatively higher
levels of HCHs than those from Vietnam. This may
indicate that terek sandpipers collected from India
migrate from agricultural fields of China to India, or
may be influenced by the sporadic applications of
HCHs in India.
Common terns and marsh sandpipers were compared
between breeding grounds and wintering grounds, while
all avian species described earlier were compared
between wintering grounds. Common terns collected

from India and Lake Baikal showed similar accumulation pattern of organochlorines (Fig. 6b), implying that
populations from India and Lake Baikal may have their
breeding grounds in Lake Baikal and wintering grounds
in India, respectively. Interestingly, common terns were
the only species accumulating highest relative concentrations of PCBs among the avian species (Fig. 6b).
It is suspected that high relative concentrations of PCBs

in common terns reflect the specific pollution in Lake
Baikal, considering the accumulation patterns of resident birds (Fig. 2) and fish (Nakata et al., 1995) from
this lake. However, exposure to PCBs in India seems to
be greatly low, because PCBs levels in various biotic and
abiotic samples are low (Kannan et al., 1993a; Ramesh
et al., 1990, 1991, 1992; Tanabe et al., 1993, 1998), and
the same was found in resident Indian birds (Fig. 2).
This means that common terns collected from India
were exposed to higher levels of PCBs in their breeding


T. Kunisue et al. / Environmental Pollution 125 (2003) 157–172

grounds at Lake Baikal, or in stopover sites in industrial
regions such as Japan and Korea.
Relative concentrations of HCHs observed in marsh
sandpipers from Lake Baikal were higher than those
from Vietnam (Fig. 6b). This suggests that marsh sandpipers from Lake Baikal may be influenced by exposure
to HCHs in stopover sites, probably China, as HCHs
pollution in Lake Baikal are known to be low (Nakata
et al., 1995) and resident birds from this lake also contained less HCHs contamination (Fig. 2).
While most migratory birds analyzed in this study
accumulated greater concentrations of DDTs than other
organochlorines, some species from India and Lake
Baikal were predominantly contaminated with PCBs
(Fig. 4). As described earlier, it was observed that little
terns and white-cheeked terns are exposed to PCBs in
the Middle East areas. The migratory patterns of lessercrested terns that over-winter in India are not clearly
understood because of a lack of ecological data. It is
suspected that this species migrates to breed around the

Mediterranean Sea (Hoyo et al., 1996). Concentrations
of PCBs were detected high in marine mammals collected from the Mediterranean Sea that has large PCBs

165

sources (Kannan et al., 1993b; Corsolini et al., 1995).
This is consistent with the idea that lesser-crested terns
wintering in India may have their breeding grounds
around the Mediterranean Sea. It is known that lapwing, herring gulls and gadwalls breeding in Lake Baikal
have their wintering grounds in a region from eastern
China to Japan (Hoyo et al., 1996). It was predicted
that these species are greatly exposed to PCBs during
winter in Japan or Korea, because it is reported that
high concentrations of PCBs were detected in bird species collected there (Guruge et al., 1997; Choi et al.,
1999).
Additionally, migratory species that accumulated the
highest concentrations of HCHs were also from India
and Lake Baikal (Fig. 4). In India, the accumulation
patterns in resident birds and local migrants suggested
the existence of large sources of HCHs (Fig. 2 and 3).
Although all of resident birds and local migrants accumulated high concentrations of HCHs, most of migratory birds from India did not. This implies that these
migratory birds from India with high concentrations of
HCHs may be greatly exposed to HCHs not only in
India but also in their stopover sites or breeding

Fig. 7. Migratory patterns predicted from accumulation features of organochlorines in migartory birds collected from Philippines, Vietnam, India
and Russia—Lake Baikal. Organochlorines in a square represent dominant contaminants.


166

T. Kunisue et al. / Environmental Pollution 125 (2003) 157–172

grounds. Species that accumulated higher concentrations
of HCHs than PCBs and DDTs included migratory birds
from Asia, and this indicates the presence of large HCHs
sources in Asian areas other than India.

4. Conclusion
Accumulation patterns of organochlorines in resident
birds collected from Asian countries suggested that the
dominant contaminants of Japan, Philippines, India,
Vietnam, and Lake Baikal were PCBs, PCBs and
CHLs, HCHs and DDTs, DDTs, PCBs and DDTs,
respectively.
In addition, accumulation features of organochlorines
in migratory birds from Asia suggested that the migratory birds reflect not only the pollution in the area of
sampling but also those in their stopover sites, and their
breeding or wintering grounds. It was indicated that
most of migratory birds collected from the Philippines
and Vietnam have their stopover sites or breeding
grounds in China or Russia and do not migrate through
industrial areas such as Japan and Korea (Fig. 7). Also,
it was indicated that migratory birds collected from
Lake Baikal, Russia have their stopover sites or wintering grounds in China, Japan or southeast Asia, and
those from India have their stopover sites or breeding
grounds in China, Russia or around Persian Gulf, Red
Sea, Caspian Sea and Mediterranean Sea regions (Fig. 7),
and thus the migratory birds collected from these two
countries have species-specific migratory routes.

It appears that avian species are useful bioindicators
to elucidate contamination status of organochlorines in

breeding grounds, stopover sites and wintering grounds,
because resident birds directly reflect the specific local
pollution status of sampling area, and migratory birds
reflect not only the pollution status of sampling area but
also those on their migratory routes.
Furthermore, the fact that migratory birds did not
necessarily reflect only the pollution in sampling area
indicates strongly, even though pollution in their
breeding grounds would be low, that exposure to organochlorines during their stay in wintering grounds or
stopover sites may adversely affect their reproductive
activities. This means that it is necessary to improve the
environment not only in breeding grounds but also in
stopover sites and wintering grounds, for protecting the
migratory birds.

Acknowledgements
The authors wish to thank the staff of the Center of
Advanced Studies in Marine Biology, Annamalai University, India, the Plague Control Research Institute of
Siberia and Far East, Russia, Center for Natural
Resources and Environmental Studies, Hanoi National
University, Vietnam, Science Education Department,
De La Salle University, Philippines, for their help in
sample collection. This study was supported by Grantsin-Aid for Scientific Research (A) (No. 12308030) from
Japan Society for the Promotion of Science and for
Scientific Research on Priority Areas (A) (No.
13027101) and ‘‘21st Century COE Program’’ from the
Ministry of Education, Culture, Sports, Science and

Technology, Japan.


Appendix A. Concentrations (ng/g fat wt.) of organochlorines in resident birds collected from the Philippines, India, Russia—Lake Baikal and Vietnam
Bird species

Painted snipe
(Rostratula benghalensis)
Chinese little bittern
(Ixobrychus sinensis)
Schrenck’s little bittern
(Ixobrychus eurhythmus)
Green backed heron
(Butrides striatus)

LC
LC

LC

Collected
year

Analyzed
tissue

n

Fat content
(%)a

Concentrationa
PCBs

DDTs

HCHs

CHLs

HCB

Philippines

1994

Whole body

6

5.9 (3.6–6.8)

270 (48–650)

120 (9.7–250)

3.4 (1.0–6.1)

38 (5.3–87)

1.7 (0.9–2.4)

Philippines

1994

Whole body

3

11 (6.2–18)

370 (110–890)

230 (130–430)

4.6 (1..7–8.9)

44 (15–100)

3.0 (1.9–4.3)

Philippines

1994

Whole body

2

11 (7.9–14)

460 (290–630)

140 (62–210)

9.8 (3.5–16)

91 (31–150)

4.4 (2.0–6.8)

Philippines

1994

Whole body

3

14 (13–14)

610 (310–1000)

420 (190–750)

6.8 (6.5–7.4)

78 (44–110)

4.9 (1.6–6.7)

India

1995

Whole body

2

6.8 (6.1–7.5)

460 (410–510)

2600 (2300–2800)

10,000 (7900–12,000)

3.0 (2.7–3.3)

9.9 (6.7–13)

India

1995

Whole body

3

5.1 (3.9–6.6)

490 (410–560)

1300 (970–1500)

4200 (1600–8700)

1.8 ( < 0.1–2.0)

3.2 (2.6–4.1)

India

1995

Whole body

2

12 (11–12)

180 (170–180)

590 (400–770)

980 (660–1300)

0.9 (0.8–0.9)

1.8 (1.7–1.8)

India

1995

Whole body

2

5.9 (5.5–6.2)

730 (630–820)

3000 (680–5100)

18,000 (15,000–20,000)

7.1 (3.2–11)

4.2 (3.6–4.8)

India

1995

Whole body

1

12

280

8100

73,000

2.5

10

India

1995

Whole body

2

13 (10–16)

320 (220–410)

27,000 (23,000–31,000)

8800 (6600–11,000)

26 (2.5–43)

8.3 (5.6–11)

India

1995

Whole body

2

8.4 (8.1–8.7)

240 (230–250)

6.0 (3.4–8.6)

200 (180–210)

0.6 ( < 0.1–1.2)

< 0.1 ( < 0.1–< 0.1)

India

1995

Whole body

1

9.9

400

4300

4200

4.0

3.0

India

1995

Whole body

1

16

190

3200

10,000

3.8

13

India

1995

Whole body

5

9.1 (7.6–11)

1800 (690–3800)

2400 (670–4300)

5100 (2800–10,000)

11 (3.8–17)

8.5 (6.0–13)

India

1995

Whole body

5

7.6 (7.3–8.9)

2800 (600–8500)

57,000 (11,000–170,000)

14,000 (6000–19,000)

180 (12–600)

5.5 (4.5–6.7)

India

1998

Whole body

10

3.7 (2.4–4.6)

200 (34–780)

430 (75–1300)

5100 (1900–12,000)

2.9 (0.9–7.0)

3.3 (1.4–4.7)

India

1998

Whole body

2

5.6 (4.3–7.0)

1000 (910–1100)

780 (740–820)

1100 (810–1400)

4.6 (4.1–5.2)

3.3 (3.3–3.3)

House sparrow
(Passer domesticus)c
Carrion crow
(Corvus corone)c
Grey heron
(Ardea cinerea)c

Russia—

Lake Baikal
Russia—
Lake Baikal
Russia—
Lake Baikal

1996–1997

Whole body

6

5.2 (2.5–6.8)

1000 (550–1500)

190 (140–230)

60 (25–92)

20 (1.2–67)

NAf

1996–1997

Whole body

3

4.3 (2.0–7.2)

5000 (3400–7200)

2700 (2000–3500)

240 (130–370)

120 (59–160)

NA

1996–1997

Breast muscle

2

3.2 (2.5–3.9)

240 (160–310)

840 (370–1300)

75 (40–110)

27 (23–30)

NA

Black-capped kingfisher
(Halcyon pileata)d
Common kingfisher
(Alcedo atthis)d

Vietnam

1997

Whole body

2

8.4 (6.7–10)

680 (460–900)

4400 (3000–5700)

310 (250–360)

18 (15–20)

26 (21–31)

Vietnam

1997

Whole body

7

7.1 (2.3–15)

1500 (270–3600)

7700 (710–20,000)

110 (27–220)

22 (6.9–52)

28.0 (3.3–43)

Black drongo
(Dicrurus macrocercus)b
Common myna
(Acridotheres tristis)b
Cotton teal
(Nettapus coromandelianus)b
House crow
(Corvus splendens)b
Little egret
(Egretta garzetta)b
Pond heron
(Ardeola grayii)b
Spotted dove
(Steptopelia chinensis)b
White-breasted kingfisher

(Halcyon smymensis)b
Black-winged stilt
(Himantopus himantopus)b
Kentish plover
(Charadrius alexandrinus)b
Little ringed plover
(Charadris dubius)b
Common myna
(Acridotheres tristis)
Kentish plover
(Charadrius alexandrinus)

167

(continued on next page)

T. Kunisue et al. / Environmental Pollution 125 (2003) 157–172

LCe

Country


168

Appendix A. (continued)
Bird species

Country

Slaty-breasted rail
(Gallirallus striatus)d
White-throasted kingfisher
(Halcyon smyrnensis)d
Common moorhen
(Gallinula chloropus)d
Cinnamon bittern
(Ixobrychus cinnamomeus)d
White-breasted waterhen
(Amaurornis phoenicurus)d

b
c
d
e
f

Analyzed
tissue

n

Concentrationa

Fat content
(%)a

PCBs

DDTs

HCHs

CHLs

HCB

Vietnam

1997

Whole body

2

4.2 (1.7–6.7)

770 (340–1200)

13,000 (5500–21,000)

59 (30–88)

100 (8.41–200)

63 (48–77)

Vietnam

1997

Whole body

1

16

250

1800

23

5.0

11

Vietnam

1997

Whole body

1

1.9

840

11,000

280

120

110

Vietnam

1997

Whole body

1

6.7

480

9600

240

550

25

Vietnam

1997

Whole body

3

14 (5.8–24)

280 (130–370)

27,000 (420–77,000)

46 (6.4–100)

20 (5.0–46)

6.9 (2.2–15)

Fat contents and concentrations were shown as arithmetic mean and range (in parentheses).
Tanabe et al. (1998).
Kunisue et al. (2002).
Minh et al. (2002).
LC=local migrant.
NA=not analysed.

Appendix B. Concentrations (ng/g fat wt.) of organochlorines in resident birds collected from Japan
Bird species

Common cormorant
(Phalacrocorax carbo)b
Common cormorant

(Phalacrocorax carbo)b
Carrion crow
(Corvus corone)
Jungle crow
(Corvus macrorhynchos)
Jungle crow
(Corvus macrorhynchos)
Jungle crow
(Corvus macrorhynchos)
Golden eagle
(Aquila chrysaetos)
Golden eagle
(Aquila chrysaetos)
White-tailed sea-eagle
(Haliaeetus albicilla)
White-tailed sea-eagle
(Haliaeetus albicilla)
a
b

Country

Collected
year

Analyzed
tissue

n

Fat content
(%)a

Concentrationa
PCBs

DDTs

HCHs

CHLs

HCB

Japan—Shinobazu pond

1993

Liver

8

3.6 (1.8–5.7)

1,100,000 (14,000–2,400,000)

380,000 (83,000–790,000)

4600 (680–13,000)

9600 (1900–25,000)

4300 (680–12,000)

Japan—Lake Biwa

1993

Liver

9

4.4 (3.0–7.3)

180,000 (34,000–830,000)

64,000 (12,000–130,000)

2800 (770–6000)

1300 (540–2600)

360 (28–580)

Japan—Hokkaido

1999

Breast muscle

5

3.7 (3.5–3.8)

2300 (600–3900)

7300 (410–33,000)

120 (33–320)

180 (59–340)

94 (32–200)

Japan—Tokyo

1998

Breast muscle

5

2.2 (1.1–3.4)

6600 (1100–26,000)

1400 (340–5400)

110 (17–440)

870 (220–3300)

110 (17–440)

Japan—Osaka

1998

Breast muscle

5

1.1 (1.0–1.1)

12,000 (8300–14,000)

2900 (740–5500)

390 (130–690)

3900 (1600–11,000)

110 (40–220)

Japan—Hiroshima

1998

Breast muscle

5

1.2 (0.34–3.0)

14,000 (1700–34,000)

690 (330–1800)

110 (30–300)

610 (170–1300)

57 (10–140)

Japan

1993–1995

Breast muscle

3

3.5 (1.0–5.9)

44,000 (610–120,000)

33,000 (6600–84,000)

2900 (550–4600)

3300 (250–8100)

220 (62–380)

Japan

1996–1998

Liver

8

5.2 (2.3–16)

140,000 (1600–500,000)

34,000 (2000–86,000)

2200 (260–4900)

14,000 (170–47,000)

1200 (10–8500)

Japan—Hokkaido

1997

Liver

2

5.1 (4.4–5.8)

68,000 (36,000–100,000)

29,000 (14,000–43,000)

1200 (740–1600)

2700 (2400–3000)

200 (170–220)

Japan—Hokkaido

1998

Breast muscle

1

5.2

35,000

24,000

490

3000

220

Fat contents and concentrations were shown as arithmetic mean and range (in parentheses).
Cited from Guruge et al. (1997).

T. Kunisue et al. / Environmental Pollution 125 (2003) 157–172

a

Collected
year


Appendix C. Concentrations (ng/g fat wt.) of organochlorines in migratory birds collected from the Philippines, India, Russia–Lake Baikal and Vietnam
Bird species

S

b

S
S
LD

S
S
S
S

S
LD
LD
LD
LD
LD
LD
LD
LD
S
S
S
S
S
S
S
S
LD
LD
LD

Collected
year

Analyzed
tissue

n

Fat content

(%)a

Concentrationa
PCBs

DDTs

HCHs

CHLs

HCB

Long-billed Mongolian plover
(Chradrius mongolus)
Kentish plover
(Chradrius alexandrinus)
Little ringed plover
(Chladrius dubius)
Ruddy turnstone
(Arenaria interpres)
Short-billed Mongolian plover
(Chradrius mongolus)

Philippines

1994

Whole body

5

12 (5.1–29)

570 (290–920)

13,000 (330–34,000)

570 (140–1200)

62 (18–150)

15 (4.5–50)

Philippines

1994

Whole body

13

15 (8.7–21)

1700 (94–14,000)

4100 (160–20,000)

810 (29–3700)

52 (4.1–100)

71 (0.1–920)

Philippines

1994

Whole body

3

12 (6.2–18)

1400 (400–2200)

8600 (1900–12,000)

590 (230–1100)

45 (6.7–82)

23 (7.6–48)

Philippines

1994

Whole body

3

9.7 (7.9–12)

690 (280–1400)

1200 (140–2800)

120 (23–190)

25 (20–33)

5.4 (3.4–8.3)

Philippines

1994

Whole body

5

12 (8.4–17)

450 (200–730)

1000 (170–3100)

860 (110–2000)

52 (7.1–110)

16 (3.1–57)

Common redshank
(Tringa totanus)d
Long-billed Mongolian plover
(Chradrius mongolus)d
White-cheeked tern
(Sterna repressa)d
Little tern (Sterna albifrons)
Whiskered tern (Chlidonias hybrida)
Short-billed Mongolian plover
(Chradrius mongolus)d
Common sandpiper
(Actitis hypoleucos)d
Common sandpiper
(Actitis hypoleucos)
Curlew sandpiper
(Calidris ferruginea)d
Lesser-crested tern
(Chlidonias leucoprerus)d
Terek sandpiper (Xenus cinereus)d
White-winged tern
(Chlidonias leucopterus)d
Common tern (Sterna hirundo)

India

1995

Whole body

5

11 (9.2–13)

820 (310–1800)

5800 (1300–12,000)

510 (160–970)

13 (6.9–25)

13 (7.6–28)

India

1995

Whole body

6

7.6 (6.1–9.9)

3400 (1800–5400)

3200 (2000–6300)

4400 (630–7800)

170 (17–390)

47 (13–62)

India

1995

Whole body

5

6.7 (5.2–8.9)

44,000 (5700–78,000)

15,000 (2900–23,000)

1200 (260–2200)

43 (6.7–66)

30 (9.0–71)

India
India
India

1998
1998
1995

Whole body
Whole body
Whole body

2
5
6

8.3 (7.7–9.0)
8.7 (6.7–11)
6.7 (6.1–7.8)

9200 (7400–11,000)
3600 (1900–5900)
2400 (1100–4400)

4600 (3400–5700)
7600 (3100–15,000)
1600 (230–5500)

1300 (1100–1400)
850 (78–3000)
4700 (3000–6800)

27 (26–28)

38 (18–54)
29 (7.7–54)

12 (4.9–20)
7.2 (5.3–9.1)
170 (24–350)

India

1995

Whole body

5

7.4 (4.9–10)

1700 (810–2500)

10,000 (2900–37,000)

3400 (1000–7400)

7.0 (3.8–9.8)

8.1 (3.4–16)

India

1998

Whole body

6

6.2 (3.5–9.5)

910 (480–2000)

7500 (2300–15,000)

1100 (600–1900)

8.8 (4.9–16)

2.3 (1.3–4.3)

India

1995

Whole body

5

13 (10–16)

300 (170–440)

96 (58–150)

440 (240–740)

7.8 (3.6–16)

3.3 (2.0–5.5)

India

1995

Whole body

5

12 (7.2–17)

3000 (1300–7200)

810 (430–1300)

270 (150–410)

16 (7.3–24)

7.4 (4.6–9.7)

India
India

1995
1995

Whole body
Whole body

3
5

5.6 (4.4–7.4)
12 (11–14)

12,000 (500–32,000)
4400 (1800–6600)

27,000 (2400–75,000)
10,000 (6700–13,000)

15,000 (1900–29,000)
3100 (390–5900)

51 (14–110)
46 (30–83)

16 (6.8–27)
22 (14–33)

India

1998

Whole body

5

11 (6.4–16)

6200 (2200–9100)

5500 (2800–8800)

210 (150–320)

12 (4.2–27)

8.4 (5.6–14)

Baikal
Baikal
Baikal
Baikal
Baikal
Baikal

1996–1997
1996–1997
1996–1997
1996–1997
1996–1997
1996–1997

Whole body
Breast muscle
Whole body
Whole body
Whole body
Whole body

9
8
6
6
9
5

5.7 (3.0–7.8)
4.0 (3.5–4.9)
3.6 (2.3–6.1)
3.9 (4.1–5.8)
2.0 (1.4–2.9)
2.7 (1.7–4.0)

2000 (210–5300)
7900 (2500–28,000)
63,000 (17,000–140,000)
3800 (960–7000)
1100 (150–5100)
250 (170–360)

150 (26–740)

10,000 (2700–22,000)
15,000 (4000–26,000)
5700 (610–16,000)
1400 (30–6100)
2000 (180–6100)

1500 (96–7400)
540 (170–1000)
1000 (110–3400)
500 (50–1200)
190 (3.0–540)
2600 (10–9000)

130 (10–520)
230 (59–390)
570 (210–1300)
71 (7.1–270)
66 (6.8–300)
21 (11–32)

NAf
NA
NA
NA
NA
NA

Russia—Lake Baikal
Russia—Lake Baikal

1996–1997
1996–1997

Whole body
Whole body

4
9

2.0 (1.6–2.4)
2.5 (2.0–3.1)

180 (65–370)
450 (140–1400)

1500 (30–4600)
210 (15–750)

430 (23–810)
44 (7.6–110)

24 (8.9–48)
17 (8.5–49)

NA
NA

Russia—Lake Baikal
Russia—Lake Baikal
Russia—Lake Baikal

1996–1997
1996–1997
1996–1997

Whole body
Whole body
Whole body

12
8
4

10 (6.5–15)
11 (2.8–18)
11 (8.0–14)

13,000 (2900–39,000)
240 (56–880)
830 (50–2300)

8700 (650–16,000)
1700 (60–5800)
2300 (100–5200)

790 (83–3300)
66 (10–190)
1300 (23–5900)

90 (2.2–680)

21 (4.2–34)
37 (7.3–120)

NA
NA
NA

e

Lapwing (Vanellus vanellus)
Common gull (Larus canus)e
Herring gull (Larus argentatus)e
Black-headed gull (Larus ridibundus)e
Pochard (Aythya ferina)e
Shoveler
(Anas clypeata)e
Garganey (Anas querquedula)e
Gadwall
(Anas strepera)e
Common tern (Sterna hirundo)e
Black-tailed godwit (Limosa limasa)e
Marsh sandpiper (Tringa stagnatilis)e

Russia—Lake
Russia—Lake
Russia—Lake
Russia—Lake
Russia—Lake
Russia—Lake

169

(continued on next page)

T. Kunisue et al. / Environmental Pollution 125 (2003) 157–172

LD

c

Country


170

Appendix C. (continued)
Bird species

Country

e

Collected
year

Analyzed
tissue

n

Fat content
(%)a

Concentrationa
PCBs

DDTs

HCHs

CHLs

HCB

Ruff (Philomachus pugnax)
Mallard (Anas platyrhynchos)e

Russia—Lake Baikal
Russia—Lake Baikal

1996–1997
1996–1997

Whole body
Whole body

2
5

10 (8.6–12)

2.2 (1.8–3.5)

100 (20–180)
350 (39–1100)

1200 (56–2300)
610 (9.2–2000)

500 (8.3–1000)
100 (16–150)

50 (15–84)
18 (6.6–34)

NA
NA

S
S

Common redshank (Tringa totanus)g
Long-billed Mongolian plover
(Chradrius mongolus)g
Whiskered tern (Chlidonias hybrida)g
Kentish plover
(Chradrius alexandrinus)g
gull-billed tern (Gelochelidon nilotica)g
Little tern (Sterna albifrons)g
Whimbrel (Numenius phaeopus)g
Dunlin (Calidris alpina)g

Great knot (Calidris tenuirostris)g
Marsh sandpiper (Tringa stagnatilis)g
Short-billed Mongolian plover
(Chradrius mongolus)g
Rufous-necked sandpiper
(Calidris ruficolis)g
Bar-tailed godwit (Limosa lapponica)g
Grey plover (Pluvialis squatarola)g
Red knot (Calidris canutus)g
Spotted redshank (Tringa erythropus)g
Terek sandpiper (Xenus cinereus)g

Vietnam
Vietnam

1997
1997

Whole body
Whole body

15
4

9.0 (3.6–16)
17 (11–23)

330 (110–620)
350 (63–910)

3000 (660–6000)
2800 (520–6200)

380 (40–2800)
210 (160–250)

13 (2.6–72)
15 (8.4–28)

15 (5.8–73)
13 (1.3–28)

Vietnam
Vietnam

1997
1997

Whole body
Whole body

4
10

9.4 (6.2–17)
14.7 (9.2–30)

1600 (1300–1900)
270 (110–740)

4600 (2700–7800)
2300 (1100–3200)

190 (120–290)
130 (50–290)

25 (8.5–45)
20 (3.9–57)

100 (16–250)
11 (3.7–23)

Vietnam
Vietnam
Vietnam
Vietnam
Vietnam
Vietnam
Vietnam

1997
1997
1997
1997
1997
1997
1997

Whole body
Whole body

Whole body
Whole body
Whole body
Whole body
Whole body

1
1
1
14
4
14
5

6.6
6.5
17
16 (5.8–32)
25 (12–38)
9.2 (2.0–16)
9.8 (7.4–13)

1300
1000
110
360 (70–1000)
260 (160–380)
410 (150–850)
490 (190–890)

6800
5700
770
2400 (700–5700)
1500 (390–2100)
2700 (1000–13,000)
2400 (1600–3600)

1700
97
20
250 (9.5–920)
740 (210–1200)
340 (110–740)
320 (110–960)

130
18
10
18 (3.7–34)
6.8 (1.8–12)
17 (2.9–110)
24 (9.3–55)

230
38
3.4
16 (2.3–44)
21 (9.3–39)
26 (5.1–70)

12 (1.0–28)

Vietnam

1997

Whole body

5

8.6 (6.2–11)

170 (100–270)

4000 (2000–6200)

45 (22–54)

17 (9.3–41)

18 (11–31)

Vietnam
Vietnam
Vietnam
Vietnam
Vietnam

1997
1997

1997
1997
1997

Whole body
Whole body
Whole body
Whole body
Whole body

1
3
5
1
2

10
7.6 (3.9–13)
11 (8.1–15)
4.1
12 (10–13)

340
320 (220–470)
300 (87–720)
980
440 (310–570)

790
1400 (870–1800)

1700 (610–2200)
1200
5600 (4700–6400)

180
110 (27–240)
290 (26–1100)
390
77 (60–94)

23
22 (19–27)
11 (4.4–19)
36
27 (19–34)

21
16 (3.8–28)
37 (6.6–130)
20
8.9 (7.7–10)

S
S
S
S
LD
LD
LD
LD

LD
LD
LD
LD
LD
LD
LD
a
b
c
d
e
f
g

Fat contents and concentrations were shown as arithmetic mean and range (in parentheses).
S=short-distance migrant.
LD=long-distance migrant.
Tanabe et al. (1998).
Kunisue et al. (2002).
NA=not analysed.
Minh et al. (2002).

T. Kunisue et al. / Environmental Pollution 125 (2003) 157–172

LD
LD


T. Kunisue et al. / Environmental Pollution 125 (2003) 157–172

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