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 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: shinsuke@agr.ehime-u.ac.jp (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)00074-5 158 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 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 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 h After Kuderna–Danish (K–D) concentration of the extract, 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 Ỉ 4.2% for PCBs, 105.0 Ỉ 5.7% for DDTs, 98.9 Ỉ 6.3% for HCHs, 103.9 Ỉ 4.3% for CHLs and 104.1 Ỉ 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 160 T Kunisue et al / Environmental Pollution 125 (2003) 157–172 Fig Mean relative concentrations of organochlorines to PCBs in resident birds from various Asian countries 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 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 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 162 T Kunisue et al / Environmental Pollution 125 (2003) 157–172 Fig 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 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 and Appendix A) Accumulation pattern in short-distance migrants from Lake Baikal was comparable to that in resident birds (Figs 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 164 T Kunisue et al / Environmental Pollution 125 (2003) 157–172 Fig (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 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 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 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 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 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 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 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 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 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 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 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 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 12 280 8100 73,000 2.5 10 India 1995 Whole body 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 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 9.9 400 4300 4200 4.0 3.0 India 1995 Whole body 16 190 3200 10,000 3.8 13 India 1995 Whole body 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 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 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 5.2 (2.5–6.8) 1000 (550–1500) 190 (140–230) 60 (25–92) 20 (1.2–67) NAf 1996–1997 Whole body 4.3 (2.0–7.2) 5000 (3400–7200) 2700 (2000–3500) 240 (130–370) 120 (59–160) NA 1996–1997 Breast muscle 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 8.4 (6.7–10) 680 (460–900) 4400 (3000–5700) 310 (250–360) 18 (15–20) 26 (21–31) Vietnam 1997 Whole body 7.1 (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 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 16 250 1800 23 5.0 11 Vietnam 1997 Whole body 1.9 840 11,000 280 120 110 Vietnam 1997 Whole body 6.7 480 9600 240 550 25 Vietnam 1997 Whole body 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 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 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 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 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 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 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 3.5 (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 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 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 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 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 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 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 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 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 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 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 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 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 6.2 (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 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 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 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 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 6 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 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 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 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 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 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 14 14 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 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 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 References Ali, S., 1996 The Book of Indian Birds Bombay Natural History Society, India Calamari, D., Bacci, E., Focardl, S., Gaggi, C., Morosini, M., Vighi, M., 1991 Role of plant biomass in the global environmental partitioning of chlorinated hydrocarbons Environ Sci Technol 25, 1489–1495 Choi, J.W., Matsuda, M., Kawano, M., Wakimoto, T., Min, B.Y., 1999 Contamination of PCBs in Nakdong river estuary, Korea Toxicol Environ Chem 72, 233–243 Corsolini, S., Focardi, S., Kannan, 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birds in. .. of organochlorines to PCBs in resident birds from various Asian countries Results and discussion 3.1 Accumulation features in resident birds The concentrations of organochlorines and mean relative