Dave PP (1996) India: a generics giant. Farm Chem Int (November) 10: .... Tanabe S, Sung JK, Choi DY, Baba N, Kiyota M, Yoshida K,. Tatsukawa R (1994) ...
Arch. Environ. Contam. Toxicol. 34, 387–397 (1998)
A R C H I V E S O F
Environmental Contamination a n d Toxicology r 1998 Springer-Verlag New York Inc.
Accumulation Features of Polychlorinated Biphenyls and Organochlorine Pesticides in Resident and Migratory Birds from South India S. Tanabe,1 K. Senthilkumar,1 K. Kannan,2 A. N. Subramanian3 1Department
of Environment Conservation, Ehime University, Tarumi 3-5-7, Matsuyama 790, Japan Pesticide Research Center, Michigan State University, East Lansing, Michigan 48824, USA 3Center of Advanced Studies in Marine Biology, Porto Novo 608502, Tamil Nadu, India 2201
Received: 22 May 1997/Accepted: 7 October 1997
Abstract. Persistent organochlorines such as DDT and its metabolites (DDTs), hexachlorocyclohexane isomers (HCHs), chlordane compounds (CHLs), hexachlorobenzene (HCB), and polychlorinated biphenyls (PCBs) were determined in wholebody homogenates of resident and migratory birds collected from South India. Organochlorine contamination pattern in birds varied depending on their migratory behaviour. Resident birds contained relatively greater concentrations of HCHs (14–8,800 ng/g wet wt) than DDTs and PCBs concentrations. In contrast, migrants exhibited elevated concentrations of PCBs (20–4,400 ng/g wet wt). The sex differences in concentrations and burdens of organochlorines in birds were pronounced, with females containing lower levels than males. Inland piscivores and scavengers accumulated greater concentrations of HCHs and DDTs while coastal piscivores contained comparable or greater amounts of PCBs. Global comparison of organochlorine concentrations indicated that resident birds in India had the highest residues of HCHs and moderate to high residues of DDTs. It is, therefore, proposed that migratory birds wintering in India acquire considerable amounts of HCHs and DDTs. Estimates of hazards associated with organochlorine levels in resident and migratory birds in India suggested that Pond Heron, Little Ringed Plover, and Terek Sandpiper may be at risk from exposure to DDTs.
Modern technology, agriculture, and associated development of chemical industries has resulted in the production and release of vast quantities of man-made chemicals. However, while contributing to improvements in our standard of living, some persistent chemicals pose serious environmental problems and ecological impacts. Organochlorine compounds (OCs) such as PCBs and DDTs (DDT, DDE, DDD) are among the most widely known class of contaminants because of their ubiquity, potential for magnification in the food chain, and harmful biological effects. For example, in avifauna, p,p8-DDE [(1,1-dichloro-2, 2-bis
Correspondence to: S. Tanabe
(p-chlorophenyl) ethylene)], a metabolite of p,p8-DDT, has been linked to eggshell thinning and diminished reproductive success in a variety of species including gulls, eagles, terns, and cormorants (Ratcliffe 1967, 1970; Anderson et al. 1969; Koeman et al. 1972; Cooke 1979; Lundholm 1987; Pearce et al. 1989). Similarly, PCBs have been shown to effect mortality of embryos and chicks (Kubiak et al. 1989) and cause morphological aberrations in chicks (Gilbertson et al. 1991). Studies in North America and Europe have linked the decline in populations of several species of birds to OC exposure (Stickel et al. 1984; Newton 1988; Douthwaite and Tingle 1992). Eventually, production and usage of PCBs, DDTs, and HCHs have been banned or restricted in developed nations since the 1970s. Notwithstanding the adverse effects of organochlorine pesticides, little is known about their contamination and toxic impacts on birds in developing countries. While contamination in birds with small home ranges reflect local or regional exposure, migratory birds can acquire contaminants from a wide range of geographical areas, including wintering grounds. The impact of migration on contaminant accumulation in birds has been the subject of several studies conducted in North America and Europe (Cade et al. 1971; Persson 1972; White et al. 1981; Henny et al. 1982; Springer et al. 1984; Mora et al. 1987; Fyfe et al. 1991). Sharp-shinned hawk (Accipiter striatus) breeding in the United States and Canada also experienced population declines due to their exposure to DDTs on wintering grounds in Latin America (Berdnardz et al. 1990). Recent studies by Jones et al. (1996) showed the presence of elevated concentrations of DDTs and PCBs in albatrosses collected from Sand Island, Midway Atoll, in the central North Pacific Ocean, and suggested the possible exposure of these birds while migrating to Asian waters. Despite the continuing usage of OC pesticides in India, the exposure of birds wintering in this country has not been studied. India hosts a multitude of waterfowl migrating from relatively remote breeding areas such as Central and North Asia (Woodcock 1980; Grewal 1990). Therefore, the magnitude of exposure to OCs such as DDTs and HCHs in wintering birds in India is of concern. Our group has made extensive investigations on the contamination of various abiotic and biotic matrices including air,
water, soil, sediments, fish, human breast milk, and foodstuffs collected from various locations in India, and suggested the predominance of DDT and HCH residues in these environmental components (Ramesh et al. 1989, 1990, 1992; Tanabe et al. 1990; Iwata et al. 1994; Kannan et al. 1992, 1995). Elevated contamination of these environmental matrices suggested the existence of potential impacts on humans and wildlife. The present study was conducted to elucidate the accumulation pattern of DDTs, HCHs, CHLs, HCB, and PCBs in resident and migratory birds collected from South India. Influence of diet, sex, and migratory routes on contamination levels were examined. In addition, potential hazards associated with the extent of DDT concentrations measured in selected birds was evaluated to delineate the species at risk. In this study, the four migrant classes were represented by anywhere from three to 12 species with one to six individuals each. Thus we are not making comparisons between species (many of which were represented by only one to three individuals) but between migrant classes.
Materials and Methods Sampling Resident and migratory birds (n 5 74) were collected from the wetland and coastal areas of Porto Novo, Cuddalore, Pudukottai, and Mandapam in Tamil Nadu, Southern India, during November and December 1995 (Figure 1). Birds were trapped by mist nets, while a few of them were obtained from bird-trapping nomads. Immediately after collection, birds were iced, transported to laboratory, and shipped to Japan with dry ice. The biometrical data (sex, growth stages, standard length, and body weight) were recorded; birds were then defeathered. The whole body was homogenized using a homogenizer and stored at 220°C until analysis. The data of biological characteristics and ecological information on birds analyzed are presented in Table 1. According to Hoyo et al. (1996), bird species analyzed in this study were classified into four groups, namely (1) strict residents living in the same region all year for their entire life span; (2) local migrants, who only migrate between Himalaya and South Indian regions; (3) shortdistance migrants, those breeding in central China (e.g., common redshank), eastern USSR (Mongolian plover), and Middle East countries (white-cheeked tern); and (4) long-distance migrants, which have their breeding grounds in eastern Europe to southeastern USSR (e.g., white-winged tern and terek sandpiper), western Europe to eastern USSR (common sandpiper), Arctic USSR (curlew sandpiper) and Middle East, Papua New Guinea, and Australia (lesser-crested tern), for further discussions.
Chemical Analysis For all birds, whole-body homogenates without feathers were employed for chemical analysis. To examine the magnitude of contaminants in feathers in comparison with those in whole-body homogenates, feathers and whole body of short- and long-billed Mongolian plover were analyzed. OC pesticides and PCBs in the whole-body homogenates were analyzed following the method described by Tanabe et al. (1994). Briefly, samples were homogenized with anhydrous sodium sulfate and Soxhlet extracted with a mixture of 300 ml diethyl ether and 100 ml hexane for 7 h. After Kuderna-Danish (K-D) concentration of the extract, 1 ml of the aliquot was dried at 80°C to determine lipid content. The remaining 4–5 ml of the extract was
S. Tanabe et al.
Fig. 1. Map showing sampling locations
transferred to a 20-g Florisil (Floridin Co., USA) packed dry column (15 mm i.d. 3 26 cm); the solvents were dried by gentle flow of nitrogen. OCs adsorbed on Florisil were eluted with a mixture of 120 ml acetonitrile and 30 ml water, transferring the eluate to a seperatory funnel containing 600 ml water and 100 ml hexane. After partitioning, the hexane layer was concentrated to 6 ml and then cleaned with equal volume of concentrated sulfuric acid. The cleaned extract was fractionated by passing through a column of 12 g of wet Florisil eluting with hexane (90 ml; first fraction) and then with 20% dichloromethane in hexane (150 ml; second fraction). The first fraction contained PCBs, HCB, p,p8-DDE and trans-nonachlor, second fraction contained p,p8DDT, p,p8-DDD, HCH isomers (a-, b-, and g-), cis-nonachlor, transnonachlor, cis-chlordane, trans-chlordane, and oxychlordane. Each fraction was concentrated and injected into a gas chromatograph coupled with 63Ni electron capture detector (GC-ECD) for identification of OCs. Feather samples were washed with detergent (confirmed that the solution was free from OCs), dried, cut into a tiny pieces, Soxhlet extracted, and then subjected to chemical analysis as described above. Quantification of OCs was performed by injecting an aliquot of the final extract into a GC-ECD (Hewlett-Packard 5890 Series II with a moving needle-type injection system). The column consisted of fused silica capillary (0.25 mm i.d. 3 25 mm length), coated with a 0.25-µm thickness of DB-1 (100% dimethyl polysiloxane) stationary phase (J&W Scientific Co., USA). The oven temperature was programmed from 60°C (1 min hold) to 160°C (10 min hold) at a rate of 20°C/min and then to 270°C (15 min hold) at a rate of 2°C/min. Injector and detector temperatures were kept at 250°C and 300°C, respectively. Helium was used as the carrier gas while nitrogen was the make-up gas. An equivalent mixture of Kanechlor 300, 400, 500, and 600 with known PCB composition and content was used as a standard. Concentrations of individually resolved peaks of PCB isomers and congeners were summed to obtain total PCB concentrations. OC pesticides were quantified by comparing individual peak area of sample to the corresponding peak area of the standard. The recovery of OC pesticides and PCBs in fortified samples were between 90 and 110% (n 5 3). Procedural blanks were run with every set of five samples to check for cross-contamination and to correct sample values if needed. The detection limit was 0.2 ng/g (wet wt) for OC pesticides and 1 ng/g (wet wt) for PCBs. The concentrations of OCs are expressed as ng/g on a wet weight basis, unless specified otherwise. DDTs represent the sum of p,p8-DDE, p,p8-DDD, and p,p8-DDT while CHLs include cis-chlordane, trans-chlordane, cis-nonachlor, transnonachlor, and oxychlordane. HCHs include a-, b-, and g- isomers.
PCBs and Pesticide Accumulation in South Indian Birds
Table 1. Biometry and ecological data of birds collected from South India Species Strict resident Black drongo (Dicrurus adsimilis) Black-winged kite (Elanus caeruleus) Common myna (Acridotheres tritis) Cotton teal (Nettapus coromandelianus) Crested kingfisher (Ceryle rudis) House crow (Corvus splendens) Little egret (Egretta garzetta) Moorhen (Gallinula chloropus) Pond heron (Ardeola grayii) Spotted dove (Streptopelia chinensis) Whitebreasted kingfisher (Halcyon smyrnensis) Local migrant Black-winged Stilt (Himantopus himantopus) Kentish Plover (Charadrius alexandrinus) Little Ringed Plover (Charadrius dubius) Short-distance migrant Common redshank (Tringa totanus) Long-billed Mongolian plover (Charadrius mongolus; sub sp. C. atrifrons) Short-billed Mongolian plover (Charadrius mongolus; sub sp. C. schaeferi) White-cheeked tern (Sterna repressa) Long-distance migrant Common sandpiper (Actitis hypoleucos) Curlew sandpiper (Calidris ferruginea) Lesser-crested tern (Thalasseus bengalensis) Terek sandpiper (Xenus cinereus) White-winged tern (Chlidonias leucopterus)
Sample Size and Sex
Standard Length (cm)
2 (1 M, 1 F) 1 (F) 3 (1 M, 2 F) 2 (1 M, 1 F) 1 (M) 2 (M) 1 (F) 1 (F) 2 (1 M, 1 F) 2 (F) 1 (F)
23 (22–24) 30 24 (23–24) 39 (39–39) 25 37 (37–37) 74 37 53 (52–53) 26 (26–26) 26
49 (48–49) 232 133 (118–154) 318 (301–335) 79 175 (134–216) 415 235 212 (203–221) 94 (86–102) 77
1 2 1 3 2 1 3 3 1 and 3 1 1
1 (M) 5 (1 M, 4 F) 5 (2 M, 3 F)
58 16 (15–17) 16 (15–17)
175 31 (28–35) 30 (27–32)
3 1 1
5 (3 M, 2 F)
6 (1 M, 5 F)
6 (5 M, 1 F) 5 (3 M, 2 F)
17 (15–19) 37 (35–38)
45 (36–49) 94 (88–108)
5 (4 M, 1 F) 5 (2 M, 3 F) 5 (3 M, 2 F) 3 (1 M, 2 F) 5 (3 M, 2 F)
19 (18–20) 21 (20–22) 41 (39–43) 25 (23–26) 24 (23–25)
43 (39–45) 51 (44–61) 189 (177–196) 51 (51–51) 34 (29–39)
1 4 1 1 1
Numbers in parentheses represent range of length and weight a See Figure 1 (1 5 Porto Novo, 2 5 Cuddalore, 3 5 Pudukottai, and 4 5 Mandapam)
Results and Discussion Suitability of Whole-Body Homogenates as Indicators In several studies, bird eggs have been used to indicate local or regional contamination. However, in migratory birds, contaminants present in females at laying could have been accumulated in wintering grounds. Similarly, migratory birds use fat reserves as a source of energy during migration; consequently, contaminants stored in fat deposits are mobilized to other body tissues, causing fluctuations of OC concentrations in subcutaneous fat. To overcome this limitation, whole-body homogenates of birds were used in this study. Because feathers were not included in the analysis, OC burdens in the feathers of long- and shortbilled Mongolian plover, representing short-distance migrants, were analyzed and compared with those measured in wholebody homogenates (Table 2). Feather weight accounted for 13–16% of the whole body mass in these birds. The concentrations of OCs were much lower in feathers than in carcasses. Based on the total weight and concentrations measured, burdens of OCs in feathers were estimated to be ,4% of the total loads for both long- and short-billed Mongolian plover. Prominently elevated burdens of OC pesticides and PCBs in the whole-body homogenates suggest suitability of this matrix as an indicator of exposure to OCs. Elimination of feathers from analysis may not have significant effect on OC concentrations/
burdens. Further, use of whole-body homogenates will not only indicate contamination levels but also provide a means for estimating total body burdens of OCs in birds, which in turn will help evaluate sex differences in concentrations and transfer rates of OCs via egg-laying.
Contamination Pattern OC pesticides and PCBs were detected in all the samples of whole-body homogenates of resident birds as well as local-, short-distance, and long-distance migratory birds (Table 3). Residue pattern of OCs in most species of resident birds analyzed in this study followed the order of HCHs . DDTs . PCBs . CHLs 5 HCB. Concentrations of HCHs in resident birds were in the range of 14–8,800 ng/g. DDTs were the second highest, ranging in concentrations from 0.3 to 3,600 ng/g. Among various resident birds, pond heron contained the highest mean concentrations of both DDTs and HCHs of 3,400 and 1,100 ng/g, respectively. This feature is similar to that found in our earlier study (Ramesh et al. 1992). High concentration of DDTs and HCHs in pond heron may be explained by its habitat and feeding near agricultural fields, canals, and ditches (Ali 1979) where applications of these insecticides for agricultural and vector control operations have been common. While HCHs predominated in most resident birds, pond heron and
S. Tanabe et al.
Table 2. Organocholorine concentrations and burdens in whole-body homogenates and feather of long- and short-billed Mongolian plover Sample Long-billed Mongolian plover (n 5 1) Whole-body homogenatesa Concentration (ng/g on wet wt) Burden (µg) Burden % Feather Concentration (ng/g on wet wt) Burden (µg) Burden % Short-billed Mongolian plover (n 5 1) Whole-body homogenatesa Concentration (ng/g on wet wt) Burden (µg) Burden % Feather Concentration (ng/g on wet wt) Burden (µg) Burden %
180 11 .98
600 35 99
8.3 0.49 .99
1.2 0.071 96
% of Body Weight 87
60 3.5 99
13 ,20 ,0.2 ,2
34 0.32 1
4.4 0.040 1
,0.2 ,0.002 ,1
0.3 0.003 4
1.6 0.074 .99
1.6 0.074 97
,0.2 ,0.001 ,1
0.3 0.002 3
84 300 14 .99
360 16 99
450 16 99
16 ,20 ,0.2 ,1
26 0.074 1
17 0.11 1
HCHs 5 a 1 b 1 g-isomers DDTs 5 p,p8-DDE 1 p,p8-DDD 1 p,p8-DDT CHLs 5 oxychlordane 1 trans-chlordane 1 cis-chlordane 1 trans-nonachlor 1 cis-nonachlor a Excluding feather
moorhen contained greater DDT concentrations than those of HCHs. Next to pond heron, the little egret, whose diet is predominantly grasshoppers, lizards, and frogs, contained elevated concentrations of HCHs (8,800 ng/g) and DDTs (970 ng/g). Spotted doves contained the lowest mean HCHs and DDTs concentration of 16 and 0.5 ng/g respectively, which was apparently one to three orders of magnitude lower than those found in other birds. PCB concentrations were generally less in resident birds, with the highest value noticed in crested kingfisher (160 ng/g), which feed primarily on fish. Concentrations of CHLs and HCB were the lowest in all the resident birds, with concentrations of ,5 ng/g. Among three species of local migrants, the black-winged stilt (n 5 1) showed the highest HCH concentrations of 4,100 ng/g (Table 3). Concentrations of PCBs in all local migrants (30–640 ng/g) recorded slightly higher than strict residents (, 20–160 ng/g). Little ringed plover revealed highest DDT concentration of 4,400 ng/g with a wide range of 760–13,000 ng/g measured among all the analyzed species. Generally, the observed pattern in local migrants can be rated as follows: HCHs $ DDTs . PCBs . CHLs $ HCB. The local migrants are assumed to migrate from South to North India (i.e., foot Himalayas and Kashmir) to avoid hot summer months (March to May) in South India. Ecological studies have indicated that these three species migrate along the coastal areas of East India ranging from Calcutta to Madras (Ali 1979) spending most of their time in urbanized and industrialized areas like Visakapatnam, Calcutta, and Madras. This might explain the occurrence of relatively elevated concentrations of PCBs. Black-winged stilts forage not only in estuarine marshes, but also agricultural fields and inland marshes during their local migration (Goriup 1982), which explains lower levels of PCBs but higher levels of HCHs than other two species of local migrants. Of the four species of short-distance migrants, common redshank and white-cheeked tern contained apparently lower
HCH concentrations than those of resident birds and local migrants (Table 3). Both long- and short-billed Mongolian plovers showed a similar residue pattern; however, the former exhibited slightly higher concentrations of all OCs except HCB. Interestingly, short-distance migrants (except common redshank) accumulated comparable or greater concentrations of PCBs than DDTs. Furthermore, all five white-cheeked terns analyzed in this study contained very high concentrations of PCBs (430–4,400 ng/g). It can be suggested that the breeding grounds (Persian Gulf and Red Sea) of white-cheeked terns may be heavily contaminated by PCBs. Long-distance migrants exhibited a different pattern of OC concentrations compared to short-distance migrants (Table 3). Common sandpipers, terek sandpipers, and white-winged terns had greater concentrations of DDTs, followed by HCHs or PCBs. Curlew sandpipers exhibited the lowest concentration among all long-distance migratory birds with comparable levels of PCBs, DDTs, and HCHs. Lesser-crested terns recorded greater PCBs, followed by DDTs and HCHs, probably reflecting the magnitude of contamination pattern in breeding grounds in Persian Gulf, similar to white-cheeked terns. The usage of PCBs in petroleum-based industries in Arabian countries might have influenced the excessive exposure of PCBs in this species. Fish collected from coastal waters in Kuwait contained greater concentrations of PCBs than DDT (Villeneuve et al. 1987). The elevated concentration of PCBs as well as other OCs in white-cheeked terns may be due to their shoreline feeding habit, while lesser-crested terns mainly feed on pelagic fish, which might explain relatively lower concentrations in this species compared to white-cheeked terns. Contamination patterns observed in birds, in general, indicate that exposure to HCHs and DDTs occurs mainly in India as evidenced from their predominance in local migrants and strict resident birds. Uniformly lower concentrations of PCBs in resident birds suggest that its contamination is lower than those
PCBs and Pesticide Accumulation in South Indian Birds
Table 3. Concentrations of persistent organochlorine residues in resident and migratory birds collected from South India
Species Strict resident Black drongo Black-winged kite Common myna Cotton teal Crested kingfisher House crow Little egret Moorhen Pond heron Spotted dove Whitebreasted kingfisher Local migrant Black-winged stilt Kentish plover Little Ringed plover Short-distance migrant Common redshank Long-billed Mongolian plover Short-billed Mongolian plover White-cheeked tern Long-distance migrant Common sandpiper Curlew sandpiper Lesser-crested tern Terek sandpiper White-winged tern
Fat n Content (%) 2 1 3 2 1 2 1 1 2 2 1
6.8 (6.1–7.5) 11.2 5.1 (3.9–6.6) 11.6 (11.4–11.7) 8.5 5.9 (5.5–6.2) 12 13 13.1 (10.2–16.3) 8.4 (8.1–8.7) 9.9
Mean Concentration (ng/g wet wt.) PCBs
31 (31–31) 180 (140–210) 29 640 26 (,20–37) 64 (52–74) ,20 (,20–,20) 67 (48–85) 160 290 42 (39–45) 160 (47–280) 33 970 ,20 510 44 (22–65) 3,400 (3,100–3,600) ,20 (,20–,20) 0.5 (0.3–0.7) 40 410
680 (600–750) 1,900 250 (63–570) 120 (72–160) 310 1,000 (820–1,200) 8,800 87 1,100 (1,100–1,100) 16 (14–18) 420
1 15.9 5 9.1 (7.6–11.0) 5 7.6 (7.3–8.9)
30 150 (69–300) 210 (40–640)
5 10.9 (9.2–12.8) 6 7.6 (6.1–9.9)
90 (40–210) 250 (130–420)
54 (19–89) 310 (62–480)
5 7.4 (4.9–10.3) 5 12.7 (10.2–16.1) 5 11.9 (7.2–16.6) 3 5.6 (4.4–7.4) 5 12.2 (11.1–13.6)
510 4,100 210 (67–330) 450 (280–590) 4,400 (760–13,000) 1,000 (390–1,400)
2,700 (430–4,400) 1,000 120 (70–170) 36 (27–48) 320 (170–520) 550 (37–1,400) 550 (210–850)
620 (140–1,900) 11 (9.2–16) 92 (52–170) 1,200 (180–3,300) 1,300 (850–1,700)
84 (15–200) 230 (82–380) 54 (40–82) 32 (19–47) 750 (140–5,500) 360 (36–710)
0.2 (0.2–0.2) 0.7 (0.5–0.8) 0.6 4 0.1 (0.1–0.1) 0.2 (0.2–0.2) 0.1 (0.1–0.1) 0.2 (0.2–0.2) 0.1 0.3 0.4 (0.2–0.6) 0.3 (0.2–0.3) 0.3 1.2 0.1 0.3 2.9 (1.5–4.3) 1.0 (0.9–1.1) 0.1 (0.1–0.1) ,0.1 (,0.1–,0.1) 0.4 0.3
0.6 1.0 (0.6–1.3) 14 (0.8–45)
2 0.8 (,0.1–1.4) 0.4 (0.3–0.5)
1.4 (0.9–3.0) 12 (1.7–24)
1.5 (0.9–3.4) 3.4 (1.3–4.6)
1.9 (0.5–3.3) 11
0.5 (0.3–0.7) 1.1 (0.5–2.6) 2.0 (0.8–3.4) 2.4 (1.0–4.8) 5.7 (3.9–10)
0.6 (0.3–1.6) 0.4 (0.2–0.6) 0.9 (0.7–1.3) 0.8 (0.5–1.2) 1.4 (1.1–1.8)
Numbers in parentheses indicate the range
of DDTs and HCHs in India. Earlier studies have shown the presence of lower concentrations of PCBs compared to DDTs and HCHs in biological samples from India (Tanabe et al. 1990; Ramesh et al. 1992; Kannan et al. 1992, 1995). India is the greatest consumer of HCHs in the world (Dave 1996; Li et al. 1996). Under the National Malaria Eradication Program of Government of India, about 85% of the DDT produced in India is used for vector control (Singh et al. 1988). In contrast to resident birds, migrating birds wintering in India contained relatively elevated concentrations of PCBs. Such a pattern reflects the contamination trend observed in the industrialized countries of northern hemisphere (White and Krynitsky 1986; Becker 1989; Barron et al. 1995). The exposure to PCBs in stopover sites during migration should also be taken into consideration. It should be mentioned that some migrants have accumulated comparable levels of DDTs and HCHs to those of resident birds. This may have implications on the sampling period of migratory birds in India. Birds were sampled in early winter (November and December) and migratory birds may therefore have acquired HCHs and DDTs in wintering grounds in India, even though for short duration. The concentrations of CHLs and HCB were uniformly low (Table 3). Little ringed plovers and long-billed Mongolian plovers showed higher mean concentrations of 14 and 12 ng/g of CHLs, respectively. Short-billed Mongolian plovers re-
corded elevated HCB concentration of 11 ng/g, while the residue levels in most of the other species were , 5 ng/g. Contamination by CHLs and HCB in environmental matrices in India is minimal (Kannan et al. 1995). In contrast, CHLs have been a prominent contaminant in Australia, New Zealand, Japan, USA, and Canada (Kannan et al. 1994). Low levels of CHLs measured in most of the migratory birds suggest that the feeding grounds of these birds may not have been in the above mentioned countries. In addition, relatively faster depuration or elimination of CHLs and HCB during migratory flight should be considered as a possible cause.
Bioaccumulation Features OC contamination levels in individual species may vary with feeding habits. The residual concentrations of OCs in birds were assessed in light of their dietary habits and ecology (Table 4). Generally, among resident birds, inland piscivores and scavengers accumulated greater concentrations of OC pesticides than those of coastal piscivores, omnivores, and granivores. However, accumulation of PCBs were greater among coastal piscivores than the other groups, suggesting the presence of major PCB pollution sources in coastal waters of South India.
S. Tanabe et al.
Table 4. Mean concentrations (ng/g wet wt) of organochlorines in resident and migratory birds according to food habits
Differences in the concentrations of OCs between male and female birds of a few species were examined. The species with two to three individuals of each sex were used for this purpose; sex difference in concentrations and burdens of OCs are presented in Table 5. In three species (except white-winged tern), higher concentrations of OCs were found in males than in females. Only DDT and HCH residue levels were lower in males than females of white-winged tern. A similar pattern was also observed in whole-body burdens of OCs in these four species of birds. Information pertaining to sex difference in OC residues in birds varied. While a few studies reported the presence of elevated concentrations in OCs in males (Larsson and Lindegren 1987; Duursma et al. 1989), several reports indicated comparable or greater concentrations in females than in males (e.g., Norstrom et al. 1976; Lemmetyinen et al. 1982; Elliott and Shutt 1993). However, no study has discussed sex difference in OC levels based on whole-body burdens. Although some exceptions were found in the present study, most birds had a male–female difference in OC burdens. The reduction of OC whole-body burdens in females suggests excretion through egg laying in breeding grounds. However, the definitive conclusion should be gained using larger number of samples in a future study.
Strict resident Inland piscivore and scavenger (BK, LE, PH) Coastal piscivore (CK, WK) Omnivore (BD, CM, HC) Granivore/occasionally insectivore (CT, MH, SD) Local migrant Inland piscivore (BS) Costal piscivore (KP, LR) Short-distance migrant Inland/coastal piscivore (CR, LP, SP) Costal piscivore (WT) Long-distance migrant Inland/coastal piscivore (LT, WW) Insectivore/piscivore (CS, CA, TS)
PCBs DDTs HCHs CHLs HCB 4
37 2,100 3,200
30 510 4,100 180 2,300 750
5 2,700 1,000
BK 5 black-winged kite, LE 5 little egret, PH 5 pond heron, CK 5 crested kingfisher, WK 5 whitebreasted kingfisher, BD 5 black drongo, CM 5 common myna, HC 5 house crow, CT 5 cotton teal, MH 5 moorhen, SD 5 spotted dove, BS 5 black-winged stilt, KP 5 kentish plover, LR 5 little ringed plover, CR 5 common redshank, LP 5 long-billed Mongolian plover, SP 5 short-billed Mongolian plover, WT 5 white-cheeked tern, LT 5 lesser-crested tern, WW 5 white-winged tern, CS 5 common sandpiper, CA 5 curlew sandpiper, TS 5 terek sandpiper
Wild birds in some Latin American and African countries revealed an identical trend. For example, Fyfe et al. (1991) reported higher concentrations of insecticide residues in carnivorous and insectivorous birds than in omnivorous and granivorous birds. Frank et al. (1977) documented a similar trend in Kenya, where carnivorous birds from agricultural watersheds had greater residue levels. Generally, birds positioned at the top of the food chain, such as kites, gulls, and eagles, accumulate elevated levels of OC contaminants (Newton 1988). Among migrants, coastal piscivores accumulated greater amounts of PCBs than inland piscivores and insectivores, similar to the pattern observed for resident birds. In avian species, PCB accumulation is related to the content and composition of prey, age, and residence time at contaminated sites (Struger and Weseloh 1985). Bird species that primarily prey on fish and other birds accumulate PCBs to a greater extent than birds that feed on lower trophic level organisms (Ram and Gillet 1993). Additionally, unlike OC pesticides, PCB usage has been concentrated in high industrial activity areas along coastal waters, and therefore, serious contamination by PCBs is found in the coastal environment (Tanabe et al. 1989). This may also support the elevated concentrations of PCBs in coastal piscivorous birds.
HCH and DDT Compositions Among various HCH isomers b-HCH was the most predominantly noticed contaminant in all the species of birds analyzed (Figure 2), reflecting more stable natrue of b-HCH than a- and g- isomers to enzymatic degradation. Interestingly, some residents and migrants such as cotton teal, spotted dove, blackwinged stilt, and lesser-crested tern comprised relatively larger proportions of a- and g-isomers than those in other birds, suggesting recent exposure to technical HCH mixture (containing 70% a-, 15% g-, 6% b-, and 9% d-HCH) used in India. The composition of p,p8-DDE was the most abundant of various DDT compounds measured in both resident and migratory birds (Figure 3). In some birds, it contributed to more than 90% of the total load. Higher composition of p,p8-DDE in birds clearly suggests greater ability to transform p,p8-DDT into p,p8-DDE. Similarly, Harper et al. (1996) noticed the presence of elevated proportion of p,p8-DDE in neotropical birds collected in the U.S. after wintering in Latin America. Relatively larger proportion of p,p8-DDT, which is the major constituent (80%) of the technical mixture of DDT in pond heron and spotted dove, suggests that recent exposure to DDT has occured in India (Figure 3). Slightly higher proportion of p,p8-DDT in long- and short-billed Mongolian plovers and curlew sandpipers may reflect exposures not only in India but also in breeding grounds.
Global and Temporal Comparison The concentrations of HCHs, DDTs, and PCBs measured in the present study were compared with those of the values reported from various parts of the world in 1980s and 1990s (Figure 4). It is noteworthy that HCH residues in Indian birds, both residents
PCBs and Pesticide Accumulation in South Indian Birds
Table 5. Mean concentrations and burdens of organochlorines in whole-body homogenates of male and female birds
Species Local migrant Little ringed plover Short-distance migrant Common redshank White-cheeked tern Long-distance migrant White-winged tern a
Fat Content (%)
BW-F (HBW)a (g)
26.3 (28.5) 29.0 (31.7)
M F M F
3 2 3 2
10.9 11.1 6.9 6.4
93.9 (102.3) 98.5 (107.4) 85.3 (95.6) 77.1 (91.6)
31.4 (35.6) 27.2 (31.4)
Concentration (ng/g wet wt)
120 52 3,600 1,300
750 380 1,200 710
65 37 110 43
11 5.1 310 100
70 37 100 55
6.1 3.6 9.4 3.3
BW-F (HBW) denotes body weight without feather and (whole-body weight including feather)
Fig. 2. Percentage composition of HCH isomers in strict residents, local migrants, short- and long-distance migrants collected in South India
and local migrants, were greater than those reported from other parts of the world. In fact, recent HCH concentrations recorded in resident birds (in the present study) were greater than those recorded in 1987–91 sampling period (Ramesh et al. 1992), suggesting continuing or increasing exposure of birds to HCH. Concentrations of DDE in Indian birds were either comparable or lower than those in birds from other parts of the world in recent years. However, when compared to those of the values reported in 1987–91 (Ramesh et al. 1992), concentrations of DDE have increased slightly. It should be noted that DDE concentration in North American and European birds were high in the early 1980s and declined dramatically due to restriction
on DDT usage. The DDT contamination in Indian birds in recent years seems to be higher than those in North American and European countries. Unless adequate precautions are taken, birds residing and wintering in India will experience harmful effects such as population decline, as was observed in North America. The concentrations of PCBs in resident birds were less than those reported from other parts of the world. However, compared to the concentrations reported in 1987–91 (Ramesh et al. 1992), there has been a sign of increase in PCB concentrations in resident birds. It is assumed that PCB contamination may increase in India due to rapid industrialization and development.
S. Tanabe et al.
Fig. 3. Percentage composition of DDT compounds in strict residents, local migrants, short- and long-distance migrants collected in South India.
Hazard Evaluation Since Ratcliffe (1967) first related eggshell thinning to insecticides (especially DDT and its metabolites), many authors have contributed to the knowledge of this phenomenon. It is generally accepted that p,p8-DDE is a major factor in causing birds to lay thinner eggs, although the mechanism is not yet completely understood (e.g., Lundholm 1987). Average concentrations of p,p8-DDE of 20–1,000 µg/g on a lipid weight basis in the liver of birds considered to pose a threat to individual bird reproduction and therefore on the population as a whole (Koeman et al. 1973; Platteeuw et al. 1995). The lipid-normalized concentrations of p,p8-DDE in little ringed plover, pond heron, and terek sandpiper were high: 58, 23, and 27 µg/g, respectively, which are in the range of those values that may cause reproductive abnormalities in birds, though those values were on the whole-body lipid weight basis. Studies relating changes in eggshell thickness as well as population changes in bird species in India are not available. We estimated the whole-body burden of p,p8-DDE for selected bird species based on their body weight and concentrations of p,p8-DDE measured in whole-body homogenates to understand the toxic implications of DDT residues. The body burdens of p,p8-DDE in two individuals of little ringed plover, one individual of pond heron, and one individual of terek sandpiper were 120–350, 770, and 160 µg, respectively. Assuming a transfer rate of 20% (an average value from Barron et al. 1995) of maternal DDTs to the eggs weighing 20% of the whole body weight, the concentrations of p,p8-DDE in eggs would be
between 3.2–13 µg/g wet wt. Approximately 5% eggshell thinning or more were reported to occur at a concentration of about 4 µg/g (wet wt) of p,p8-DDE in eggs (Dirksen et al. 1995). Newton (1988) stated that p,p8-DDE concentrations greater than 3 µg/g (wet wt) in peregrine falcons resulted in reduced breeding success. Our initial evaluation suggests that pond herons, little ringed plovers, and terek sandpipers may be close to the threshold of risk. Although our hazard estimate involves assumptions on egg weight and transfer rate of p,p8-DDE for general comparative purposes, species-specific hazard assessment associated with exposure to DDTs and HCHs is necessary for Indian birds.
Conclusions To our knowledge, this is a first study comparing concentrations of OCs in migratory and resident birds comprising a wide range of species in India. An overall appraisal of OC concentrations in Indian birds suggested greater contamination by HCHs in resident birds. This feature is characteristic for Indian biota because most of the studies with wild birds from other parts of the world have shown the prevalence of DDTs or PCBs. Therefore, it can be suggested the birds migrating from the north acquire considerable levels of HCHs while wintering in India. The residue concentrations of DDTs and HCHs in birds have not shown any sign of reduction. Verma (1990) suggested that DDT levels in Indian fauna might decline in the future due to the recent ban of DDT from agricultural usage. The
PCBs and Pesticide Accumulation in South Indian Birds
Fig. 4. International comparision of PCBs, DDE and HCHs levels in birds. Serial number correspond to the following references: 1: Ohlendorf and Miller (1984), 2: Fitzner et al. (1988), 3: Elliott et al. (1996), 4: Falandysz et al. (1994), 5: Scharenberg (1991), 6: Olafsdottir et al. (1995), 7: Lambertini and Leonzio (1986), 8: Castillo et al. (1994), 9: Everaarts et al. (1991), 10: Daelemans et al. (1992), 11: Guruge et al. (1997), 12: Ramesh et al. (1992), 13: White and Krynitsky (1986), 14: Rumbold et al (1996), 15: Harper et al. (1996), 16: Mora (1997), 17: Olsen et al. (1992), 18: Niethammer et al (1984), 19: Fyfe et al. (1991), 20: Tarhanen et al. (1989), 21: Falandysz et al. (1988), 22: Kaphalia et al. (1981), *present study: *1strict residents, *2local migrants, *3short-distance migrants, *4long-distance migrants
magnitude of exposure to various contaminants in wintering grounds in India can be assessed by collecting birds at the end of the wintering season. Further, comparison of the concentrations of PCBs in resident birds collected in 1987–91 with those of the present study indicates that PCB pollution is increasing in
recent years. DDT burdens in little ringed plover, pond heron, and terek sandpiper suggested that these species experience greater risks from DDT exposure in India. Further studies measuring the concentrations of DDTs in eggs of resident avifauna are necessary to elucidate vulnerable species.
Acknowledgments. The authors wish to thank the staff of the Center of Advanced Study in Marine Biology, Annamalai University, for their help in sample collection. This research was supported by a Grant in Aid for the Scientific Research from the Ministry of Education, Science and Culture of Japan (Project Nos. 09041163 and 09306021).
References Ali S (1979) The book of Indian birds. Bombay Natural History Society, Bombay, 187 pp Anderson DW, Hickey JJ, Risebrough RW, Hughes DF, Christensen RE (1969) Significance of chlorinated hydrocarbon residues to breeding pelicans and cormorants. Can Field Nat 83:91–112 Barron MG, Galbraith H, Beltman D (1995) Comparitive reproduction and developmental toxicology of birds. Comp Biochem Physiol 112C:1–14 Becker PH (1989) Seabirds as monitor organisms of contaminants along the German North Sea coast. Helgolander Meeresunter 43:395–403 Berdnardz JC, Klem D, Goodrich LJ, Senner SE (1990) Migration counts of raptors at Hawk Mountain, Pennsylvania, as indicators of population trends, 1934–1986. Auk 107:96–109 Cade TJ, Lincer JL, White CM, Rosenau DG, Swartz LG (1971) DDE residues and eggshell changes in Alaskan falcons and hawks. Science 172:955–957 Castillo L, Thybaud E, Caquet T, Ramade F (1994) Organochlorine contaminants in common tern (Sterna hirundo) eggs and young from the Rhine River area (France). Bull Environ Contam Toxicol 53:759–764 Cooke AS (1979) Egg shell characteristic of gannets Sula bassana, shags Phalacrocorax aristotelis and great black-baked gulls Larus marinus exposed to DDE and other environmental pollutants. Environ Pollut 19:47–65 Daelemans FF, Mahlum F, Shepens JC (1992) Polychlorinated biphenyls in two species of Arctic sea birds from the Svalbard area. Bull Environ Contam Toxicol 48:824–834 Dave PP (1996) India: a generics giant. Farm Chem Int (November) 10: 36–37 Dirksen S, Boudewijn TJ, Slager LK, Mes RG, van Schaick MJM, de Voogt P (1995) Reduced breeding success of cormorants (Phalacrocorax carbo sinensis) in relation to persistent organochlorine pollution of aquatic habits in the Netherlands. Environ Pollut 88:119–132 Douthwaite RJ, Tingle CCD (1992) Effects of DDT treatments applied for tsete fly control on white-headed black chat (Thamnolaea arnoti) populations in Zimbabwe. Part II. Cause of decline. Ecotoxicol 1:101–115 Duursma EK, Nieuwenhuize J, van Liere JM, Hillebrand MTHJ (1989) Partitioning of organochlorines between water, particulate matter and some organisms in estuarine and marine systems of The Netherlands. Neth J Sea Res 20:239–251 Elliott JE, Shutt L (1993) Monitoring organochlorines in blood of sharp-shinned hawks (Accipiter striatus) migrating through the Great Lakes. Environ Toxicol Chem 12:241–250 Elliott JE, Norstrom RJ, Smith GEJ (1996) Patterns, trends, and toxicological significance of chlorinated hydrocarbon and mercury contaminants in bald eagle eggs from the Pacific Coast of Canada, 1990–1994. Arch Environ Contam Toxicol 31:354–367 Everaarts JM, De Buck A, Hillebrand MTHJ, Boon JP (1991) Residues of chlorinated biphenyl congeners and pesticides in brain and liver of the oystercatcher (Haematopus ostralegis) in relation to age, sex and biotransformation capacity. Sci of Total Environ 100:483–499 Falandysz J, Jakuczun B, Mizera T (1988) Metals and organochlorines in four female white-tailed eagles. Mar Pollut Bull 19:521–526
S. Tanabe et al.
Falandysz J, Yamashita N, Tanabe S, Tatsukawa R, Rucinska L, Mizera T, Jakuczun B (1994) Highly toxic non-ortho chlorine substituted coplanar PCBs in white-tailed sea eagles (Haliaetus albicilla) from Poland. In: Mayburg BU, Chancellor RD (eds) Raptor conservation today. WWGBP, Pica Press, Gdan´sk, pp 725–730 Fitzner RE, Blus LJ, Henny CJ, Carlile DW (1988) Organochlorine residues in great blue herons from North Western United States. Rep Colonial Waterbirds 11(2):293–300 Frank LG, Jackson RM, Cooper JE, French MC (1977) A survey of chlorinated hydrocarbon residues in Kenyen birds of prey. E Afr Wildl J 15:295–304 Fyfe RW, Banasch U, Benevides V, de Benavides NH, Luscombe A, Sanchez J (1991) Organochlorine residues in potential prey of peregrine falcons Falco peregrines in Latin America. Field Nat 104:285–292 Gilbertson M, Kubiak T, Ludwig J, Fox G (1991) Great Lakes embryo mortality, edema and deformities syndrome (GLEMEDS) in colonial fish-eating birds: similarity to chich-edema disease. J Toxicol Environ Health 33:455–520 Goriup PD (1982) Behaviour of black-winged stilts. British Birds 75:12–29 Grewal B (1990) Birds of India. Guide book Co. Ltd., Hong Kong, in conjucation with Gulmohr Press Pvt, Ltd., New Delhi, 193 pp. Guruge KS, Tanabe S, Fukuda M, Yamagishi S, Tatsukawa R (1997) Accumulation pattern of persistent organochlorine residues in common cormorants (Phalacrocorax carbo) from Japan. Mar Poll Bull 34:186–193 Harper RG, Frick JA, Capparella AP, Borup B, Nowak M, Biesinger D, Thompson CF (1996) Organochlorine pesticide contamination in neotropical migrant passerines. Arch Environ Contam Toxicol 31:386–390 Henny CJ, Ward FP, Riddle KE, Prouty RM (1982) Migratory peregrine falcons, (Falco peregrines) accumulated pesticides in Latin America during winter. Can Field Nat 96:333–338 Hoyo JD, Elliott A, Sargatal J, eds. (1996) Handbook of the birds of the world, vol 3. Lynx Edicions, Barcelona, 821 pp Iwata H, Tanabe S, Sakai N, Nishimura A, Tatsukawa R (1994) Geographical distribution of persistent organochlorines in air, water and sediments from Asia and Oceania, and their implications for global redistribution from lower latitudes. Environ Pollut 85:15–33 Jones PD, Hannah DJ, Buckland SJ, Day PJ, Leathem SV, Porter LJ, Auman HJ, Sanderson JT, Summer C, Ludwig JP, Colborn TL, Giesy JP (1996) Persistent synthetic chlorinated hydrocarbons in albatross tissue samples from Midway Atoll. Environ Toxicol Chem 15:1793–1800 Kannan K, Tanabe S, Ramesh A, Subramanian AN, Tatsukawa R (1992) Persistent organochlorine residues in food stuffs from India and their implications on human dietary exposure. J Agric Food Chem 40:518–524 Kannan K, Tanabe S, Tatsukawa R, Sinha RK (1994) Biodegradation capacity and residue pattern of organochlorines in Ganges river dolphin from India. Toxicol and Environ Chem 42:249–261 Kannan K, Tanabe S, Tatsukawa R (1995) Geographical distribution and accumulation features of organochlorine residues in fish in Tropical Asia and Oceania. Environ Sci Technol 29:2673– 2683 Kaphalia BS, Hussain MM, Seth TD, Kumar A, Murti RK (1981) Organochlorine pesticide residues in some Indian wild birds. Pestic Monit J 15:9–13 Koeman JH, Bothof TH, Devries R, Vanvelzen-bland H, Vos JG (1972) The impact of persistent pollutants on piscivorous and molluscivorous birds. TNO Nieuws 27:561–569 Koeman JH, Vanvelzen-blad HCW, Devries R, Vos JG (1973) Effects of PCB and DDE in cormorants and evaluation of PCB residues from an experimental study. J Reprod Fert Suppl 19:353–364
PCBs and Pesticide Accumulation in South Indian Birds
Kubiak TJ, Harris HJ, Smith LM, Schwartz TR, Stalling PL, Trick L, Sielo DE, Pocherty PD, Erdman TC (1989) Microcontaminants and reproductive impairment of the Forster’s tern on Green Bay, Lake Michigan 1983. Arch Environ Contam Toxicol 18:706–727 Lambertini G, Leonzio C (1986) Pollutant levels and their effects on Mediterranean sea birds. In: Medmaravis X, Monballiu (eds) Mediterranean marine avifauna. NATO Series G12:359–378 Larsson P, Lindegren A (1987) Animals need not be killed to reveal their body burdens of chlorinated hydrocarbons. Environ Pollut 45:73–78 Lemmetyinen R, Rantamaki P, Karlin (1982) Levels of DDT and PCBs in different stages of life cycle of the Arctic terns (Sterna paradisaea) and herring gull (Larus argentatus). Chemosphere 11:1059–1068 Li YF, Mcmillan A, Scholtz MT (1996) Global HCH usage with 1° 3 1° longitude/latitude resolution. Environ Sci Technol 30:3525– 3533 Lundholm E (1987) Thinning of eggshells in birds by DDE: mode of action on the eggshell gland. Comp Biochem Physiol 88C:1–22 Mora MA, Anderson DW, Mount ME (1987) Seasonal variation of body condition and organochlorines in wild ducks from California and Mexico. J Wildl Manage 51:132–141 Mora MA (1997) Transboundary pollution: persistent organochlorine pesticides in migrant birds of the southwestern United States and Mexico. Environ Toxicol Chem 16:3–11 Newton I (1988) Determination of critical pollutant levels in wild populations, with examples from organochlorine insecticides in birds of prey. Environ Pollut 55:29–40 Norstrom RJ, Risebrough RW, Cartwright DJ (1976) Elimination of chlorinated dibenzofurans associated with polychlorinated biphnyl fed to mallard (Anas platyrhynchos). Toxicol Appl Pharmacol 37:217–228 Niethammer KR, Baskett TS, White DH (1984) Organochlorine residues in three heron species as resulted to their diet and age. Bull Environ Contam Toxicol 33:491–498 Ohlendorf HM, Miller MR (1984) Organochlorine contaminants in California waterfowl. J Wildl Manage 48:867–877 Olafsdottir K, Petersen E, Thordardottir S, Johannesson T (1995) Organochlorine residues in Gryfalcons (Falco rusticolus) in Iceland. Bull Environ Contam Toxicol 55:382–389 Olsen P, Emison B, Mooney N, Brothers N (1992) DDT and dieldrin: effects on resident peregrine falcon populations in south-eastern Australia. Ecotoxicol 1:89–100 Pearce PA, Elliott JE, Peakall DB, Norstrom RJ (1989) Organochlorine contaminants in eggs of seabirds in the Northwest Atlantic, 1968–1984. Environ Pollut 56:217–235 Persson B (1972) DDT content of whitethroats after summer stay in Sweden. Ambio 1:34–35 Platteeuw M, van Eerden MR, av de Guchte K (1995) Variation in contaminant content of livers of cormorants Phalacrocorax carbo sinensis living near polluted sedimentation area in Lake Ijsselmeer in the Netherlands. Ardea 83:315–324 Ram RN, Gillett JW (1993) An aquatic terrestrial food web model for polychlorinated biphenyls (PCBs). In: American Society for Testing and Materials, Environmental toxicology and risk assessment. ASTM STP 1179, Philadelphia, PA, pp 192–212 Ramesh A, Tanabe S, Tatsukawa R, Subramanian AN, Palanichamy S, Mohan D, Venugopalan VK (1989) Seasonal variation of persistent organochlorine insecticide residues in air from Porto Novo, South India. Environ Pollut 62:213–222 Ramesh A, Tanabe S, Iwata H, Tatsukawa R, Subramanian AN, Mohan D, Venugopalan VK, (1990) Seasonal variation of persistent
organochlorine insecticide residues in Vellar river waters in Tamil Nadu, South India. Environ Pollut 67:289–304 Ramesh A, Tanabe S, Kannan K, Subramanian AN, Kumaran PL, Tatsukawa R (1992) Characteristic trend of persistent organochlorine contamination in wildlife from tropical agricultural watershed, South India. Arch Environ Contam Toxicol 23:26–36 Ratcliffe DA (1967) Decrease in eggshell weight in certain birds of prey. Nature 215:208–210 Ratcliffe DA (1970) Changes attributable to pesticides in egg-breakage frequency and egg shell thickness in some British birds. J Appl Ecol 7:76–115 Rumbold DG, Bruner MC, Mihalik MB, Marti EA, White LL (1996) Organochlorine pesticides in anhingas, white ibises and apple snails collected in Florida, 1989–1991. Arch Environ Contam Toxicol 30:379–383 Scharenberg W (1991) Prefledging terns (Sterna paradosea, Sterna hirundo) as bioindicators for organochlorine residues in the German Wadden Sea. Arch Environ Contam Toxicol 21:102–105 Singh PP, Battu RS, Kalra RL (1988) Insecticide residues in wheat grains and straw arising from their storage in premises treated with BHC and DDT under malaria control program. Bull Environ Contam Toxicol 40:696–702 Springer AM, Walker W, Risebrough RW, Benfield D, Ellis DH, Mattox WG, Mindell DP, Roseneau DG (1984) Origins of organochlorines accumulated by peregrine falcons, Falco peregrinus breeding in Alaska Greenland. Can Field Nat 98:159–166 Stickel WH, Stickel LF, Dryland RA, Hughes DL (1984) DDE in birds: lethal residues and loss rates. Arch Environ Contam Toxicol 13:1–6 Struger J, Weseloh DV (1985) Great Lakes Caspian terns: egg contaminants and biological implications. Colonial Waterbirds 8:142–149 Tanabe S, Kannan N, Fukushima M, Okamoto T, Wakimoto T, Tatsukawa R (1989) Persistent organochlorines in Japanese coastal waters: an introspective summary from a far east developed nation. Mar Pollut Bull 20:344–352 Tanabe S, Gondair F, Subramanian AN, Ramesh A, Mohan D, Kumaran P, Venugopalan VK, Tatsukawa R (1990) Specific pattern of persistent organochlorine residues in human breast milk from South India. J Agric Food Chem 38:899–903 Tanabe S, Sung JK, Choi DY, Baba N, Kiyota M, Yoshida K, Tatsukawa R (1994) Persistent organochlorine residues in Northern fur seal from the Pacific Coast of Japan since 1971. Environ Pollut 85:305–314 Tarhanen J, Koistinen J, Passivirta J, Vuorinen PJ, Koivusaari J, Nuuja I, Kannan N, Tatsukawa R (1989) Toxic significance of planar aromatic compound in Baltic ecosystem—new studies on extremely toxic coplanar PCBs. Chemosphere 18:1067–1077 Verma JS (1990) India agrochemical industry comes of age. Farm Chem Int 4:20–21 Villeneuve JP, Fowler SW, Anderlini VC (1987) Organochlorine levels in edible marine organisms from Kuwait coastal waters. Bull Environ Contam Toxicol 38:266–270 White DH, King KA, Mitchell CA, Krynitsky AJ (1981) Body lipids and pesticide burdens on migrant blue-winged teal. J Field Ornithol 52:23–28 White DH, Krynitsky (1986) Wildlife in some areas of New Mexico and Texas accumulate elevated DDE residues, 1983. Arch Environ Contam Toxicol 15:149–157 Woodcock MW (1980) Birds of India, Nepal, Pakistan, Bangladesh & Srilanka. Harper Collins Publishers, London, 176 pp