Abstract Concentrations of organochlorine contaminants including polychlorinated biphenyls PCBs, dichlorodiphenyltrichloroethane and its metabolites DDTs, hexachlorocyclohexane isomers H
Trang 1Accumulation features of persistent organochlorines in resident
and migratory birds from Asia
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
b 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
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 pol-luted 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
(poly-chlorinated biphenyls), DDTs
(dichlorodiphenyl-trichloroethane and its metabolites) and HCHs
(hexachlorocyclohexane isomers) are of great concern as
environmental contaminants due to their
bioaccumula-tive nature and chronic adverse effects on humans and
wildlife Though these chemicals were banned for
man-ufacture and use in many developed countries during
1970s, they are still used in some developing countries
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 pur-poses 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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* Corresponding author Tel./fax: +81-89-946-9904.
E-mail address: shinsuke@agr.ehime-u.ac.jp (S Tanabe).
Trang 21992; Tanabe et al., 1993, 1998) The cumulative
con-sumption 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
reg-ulation 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)
Rela-tively 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
manu-factured (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
dur-ing 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 organo-chlorines in the birds, especially migratory birds, in Asia
We previously studied accumulation of organo-chlorines 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 breed-ing grounds, stopover sites and winterbreed-ing 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 accu-mulation 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 accumu-lation 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), Cud-dalore, 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
Trang 3livers removed from their bodies with a dissective
scal-pel, and the whole body were homogenized using a
homogenizer, and then stored in deep-freezer at 20C
until analysis
Based on the studies by Hoyo et al (1996) and Ali
(1996), avian species analyzed in this study were
classi-fied 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
plo-ver 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
whole-body homogenates, pectoral muscles and livers were
analyzed following the method described byTanabe 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 80C 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% dichloro-methane 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-nona-chlor, trans-nonacis-nona-chlor, 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 quan-tified 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 4.2% for PCBs, 105.0 5.7% for DDTs, 98.9 6.3% for HCHs, 103.9 4.3% for CHLs and 104.1 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 Pro-gram 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 per-sistent organochlorines Reliable results were obtained
by comparison of data from our laboratory with those from material reference values
Fig 1 Map showing sampling locations of birds.
Trang 43 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, Band Fig 2 A wide variation of
orga-nochlorine 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
domi-nant 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 inves-tigated 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 orga-nochlorines These observations imply that these coun-tries 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 abun-dantly 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 pre-dominantly an agricultural country and has used pesti-cides 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 che-mical 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 tra-vel 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) Cala-mari et al (1991)reported that concentrations of HCHs
Fig 2 Mean relative concentrations of organochlorines to PCBs in
resident birds from various Asian countries.
Trang 5in 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
classi-fied according to dominant residues of organochlorines
in their bodies (Fig 4) Interestingly, in all the migra-tory 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 orga-nochlorine 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 ‘short-distance’ and ‘long-‘short-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
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 Phi-lippines 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 accumu-lated 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 con-centrations 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
Fig 3 Organochlorine residue patterns in local migratory birds
col-lected from India Relative concentration indicates ratio of individual
organochlorine concentration to that of PCBs, which was treated as 1.0.
Trang 6et 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
pol-luted by DDTs as evidenced by the fact that resident birds
showed elevated levels of DDTs (Fig 2andAppendix 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 win-tering in the areas which have similar contamination pattern as in Lake Baikal, or may be less exposed to organochlorines in their wintering ground
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.
Trang 73.2.2 Long-distance migrant
Accumulation patterns of organochlorines in
long-distance 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
long-distance migrant species may have different stopover
sites, breeding and wintering grounds from
short-dis-tance migrants It is known that long-disshort-dis-tance 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
sig-nificant 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
stop-over site and breeding ground in China and Russia, or
in their wintering ground in Vietnam In addition,
rela-tive 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
collected from each country are exposed to similar pol-lution 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 sug-gested 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 Phi-lippines 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 organo-chlorines between the regions around Caspian Sea and
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 accu-mulation pattern of organochlorines in common red-shanks 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 appar-ently 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 dif-ferences in accumulation pattern of migrant and resi-dent 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 Viet-nam, 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
Trang 8relative 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 accumula-tion 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 con-centrations 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 resi-dent 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
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.
Trang 9grounds 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
sand-pipers 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
con-tained 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
lesser-crested 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
col-lected from the Mediterranean Sea that has large PCBs
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 lapw-ing, 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 spe-cies 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 accu-mulated high concentrations of HCHs, most of migra-tory 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.
Trang 10grounds 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
migra-tory 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
winter-ing 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 orga-nochlorines 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 Uni-versity, 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 Grants-in-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