Accumulation Features of Polychlorinated Biphenyls and OrganochlorinePesticides 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, Japan2201 Pesticide Research Center, Michigan State University, East Lansing, Michigan 48824, USA3Center of Advanced Studies in Marine Biology, Porto Novo 608502, Tamil Nadu, India

Received: 22 May 1997/Accepted: 7 October 1997

Abstract. Persistent organochlorines such as DDT and itsmetabolites (DDTs), hexachlorocyclohexane isomers (HCHs),chlordane compounds (CHLs), hexachlorobenzene (HCB), andpolychlorinated biphenyls (PCBs) were determined in whole-body homogenates of resident and migratory birds collectedfrom South India. Organochlorine contamination pattern inbirds varied depending on their migratory behaviour. Residentbirds contained relatively greater concentrations of HCHs(14–8,800 ng/g wet wt) than DDTs and PCBs concentrations. Incontrast, migrants exhibited elevated concentrations of PCBs(20–4,400 ng/g wet wt). The sex differences in concentrationsand burdens of organochlorines in birds were pronounced, withfemales containing lower levels than males. Inland piscivoresand scavengers accumulated greater concentrations of HCHsand DDTs while coastal piscivores contained comparable orgreater amounts of PCBs. Global comparison of organochlorineconcentrations indicated that resident birds in India had thehighest residues of HCHs and moderate to high residues ofDDTs. It is, therefore, proposed that migratory birds winteringin India acquire considerable amounts of HCHs and DDTs.Estimates of hazards associated with organochlorine levels inresident and migratory birds in India suggested that PondHeron, Little Ringed Plover, and Terek Sandpiper may be at riskfrom exposure to DDTs.

Modern technology, agriculture, and associated development ofchemical industries has resulted in the production and release ofvast quantities of man-made chemicals. However, while contrib-uting to improvements in our standard of living, some persistentchemicals pose serious environmental problems and ecologicalimpacts. Organochlorine compounds (OCs) such as PCBs andDDTs (DDT, DDE, DDD) are among the most widely knownclass of contaminants because of their ubiquity, potential formagnification in the food chain, and harmful biological effects.For example, in avifauna,p,p8-DDE [(1,1-dichloro-2, 2-bis

(p-chlorophenyl) ethylene)], a metabolite ofp,p8-DDT, hasbeen linked to eggshell thinning and diminished reproductivesuccess in a variety of species including gulls, eagles, terns, andcormorants (Ratcliffe 1967, 1970; Andersonet al. 1969;Koemanet al.1972; Cooke 1979; Lundholm 1987; Pearceet al.1989). Similarly, PCBs have been shown to effect mortality ofembryos and chicks (Kubiaket al.1989) and cause morphologi-cal aberrations in chicks (Gilbertsonet al. 1991). Studies inNorth America and Europe have linked the decline in popula-tions of several species of birds to OC exposure (Stickelet al.1984; Newton 1988; Douthwaite and Tingle 1992). Eventually,production and usage of PCBs, DDTs, and HCHs have beenbanned or restricted in developed nations since the 1970s.Notwithstanding the adverse effects of organochlorine pesti-cides, little is known about their contamination and toxicimpacts on birds in developing countries.

While contamination in birds with small home ranges reflectlocal or regional exposure, migratory birds can acquire contami-nants from a wide range of geographical areas, includingwintering grounds. The impact of migration on contaminantaccumulation in birds has been the subject of several studiesconducted in North America and Europe (Cadeet al. 1971;Persson 1972; Whiteet al.1981; Hennyet al.1982; Springeretal. 1984; Moraet al. 1987; Fyfeet al. 1991). Sharp-shinnedhawk (Accipiter striatus) breeding in the United States andCanada also experienced population declines due to theirexposure to DDTs on wintering grounds in Latin America(Berdnardzet al. 1990). Recent studies by Joneset al. (1996)showed the presence of elevated concentrations of DDTs andPCBs in albatrosses collected from Sand Island, Midway Atoll,in the central North Pacific Ocean, and suggested the possibleexposure of these birds while migrating to Asian waters.Despite the continuing usage of OC pesticides in India, theexposure of birds wintering in this country has not been studied.India hosts a multitude of waterfowl migrating from relativelyremote breeding areas such as Central and North Asia (Wood-cock 1980; Grewal 1990). Therefore, the magnitude of expo-sure to OCs such as DDTs and HCHs in wintering birds in Indiais of concern.

Our group has made extensive investigations on the contami-nation of various abiotic and biotic matrices including air,Correspondence to:S. Tanabe

Arch. Environ. Contam. Toxicol. 34, 387–397 (1998) A R C H I V E S O F

EnvironmentalContaminationa n d Toxicologyr 1998 Springer-Verlag New York Inc.

water, soil, sediments, fish, human breast milk, and foodstuffscollected from various locations in India, and suggested thepredominance of DDT and HCH residues in these environmen-tal components (Rameshet al.1989, 1990, 1992; Tanabeet al.1990; Iwataet al. 1994; Kannanet al. 1992, 1995). Elevatedcontamination of these environmental matrices suggested theexistence of potential impacts on humans and wildlife. Thepresent study was conducted to elucidate the accumulationpattern of DDTs, HCHs, CHLs, HCB, and PCBs in resident andmigratory birds collected from South India. Influence of diet,sex, and migratory routes on contamination levels were exam-ined. In addition, potential hazards associated with the extent ofDDT concentrations measured in selected birds was evaluatedto delineate the species at risk. In this study, the four migrantclasses were represented by anywhere from three to 12 specieswith one to six individuals each. Thus we are not makingcomparisons between species (many of which were representedby only one to three individuals) but between migrant classes.

Materials and Methods

Sampling

Resident and migratory birds (n5 74) were collected from the wetlandand coastal areas of Porto Novo, Cuddalore, Pudukottai, and Mandapamin Tamil Nadu, Southern India, during November and December 1995(Figure 1). Birds were trapped by mist nets, while a few of them wereobtained from bird-trapping nomads. Immediately after collection,birds were iced, transported to laboratory, and shipped to Japan withdry ice. The biometrical data (sex, growth stages, standard length, andbody weight) were recorded; birds were then defeathered. The wholebody was homogenized using a homogenizer and stored at220°C untilanalysis. The data of biological characteristics and ecological informa-tion on birds analyzed are presented in Table 1.

According to Hoyoet al. (1996), bird species analyzed in this studywere classified into four groups, namely (1) strict residents living in thesame region all year for their entire life span; (2) local migrants, whoonly migrate between Himalaya and South Indian regions; (3) short-distance migrants, those breeding in central China (e.g., commonredshank), eastern USSR (Mongolian plover), and Middle East coun-tries (white-cheeked tern); and (4) long-distance migrants, which havetheir breeding grounds in eastern Europe to southeastern USSR (e.g.,white-winged tern and terek sandpiper), western Europe to easternUSSR (common sandpiper), Arctic USSR (curlew sandpiper) andMiddle East, Papua New Guinea, and Australia (lesser-crested tern), forfurther discussions.

Chemical Analysis

For all birds, whole-body homogenates without feathers were em-ployed for chemical analysis. To examine the magnitude of contami-nants in feathers in comparison with those in whole-body homoge-nates, feathers and whole body of short- and long-billed Mongolianplover were analyzed. OC pesticides and PCBs in the whole-bodyhomogenates were analyzed following the method described by Tanabeet al. (1994). Briefly, samples were homogenized with anhydroussodium sulfate and Soxhlet extracted with a mixture of 300 ml diethylether 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 todetermine lipid content. The remaining 4–5 ml of the extract was

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 ofnitrogen. OCs adsorbed on Florisil were eluted with a mixture of 120ml acetonitrile and 30 ml water, transferring the eluate to a seperatoryfunnel containing 600 ml water and 100 ml hexane. After partitioning,the hexane layer was concentrated to 6 ml and then cleaned with equalvolume of concentrated sulfuric acid. The cleaned extract was fraction-ated by passing through a column of 12 g of wet Florisil eluting withhexane (90 ml; first fraction) and then with 20% dichloromethane inhexane (150 ml; second fraction). The first fraction contained PCBs,HCB, p,p8-DDE andtrans-nonachlor, second fraction containedp,p8-DDT, p,p8-DDD, HCH isomers (a-, b-, andg-), cis-nonachlor,trans-nonachlor,cis-chlordane,trans-chlordane, and oxychlordane. Eachfraction was concentrated and injected into a gas chromatographcoupled with63Ni electron capture detector (GC-ECD) for identifica-tion of OCs.

Feather samples were washed with detergent (confirmed that thesolution was free from OCs), dried, cut into a tiny pieces, Soxhletextracted, and then subjected to chemical analysis as described above.

Quantification of OCs was performed by injecting an aliquot of thefinal extract into a GC-ECD (Hewlett-Packard 5890 Series II with amoving needle-type injection system). The column consisted of fusedsilica capillary (0.25 mm i.d.3 25 mm length), coated with a 0.25-µmthickness of DB-1 (100% dimethyl polysiloxane) stationary phase(J&W Scientific Co., USA). The oven temperature was programmedfrom 60°C (1 min hold) to 160°C (10 min hold) at a rate of 20°C/minand then to 270°C (15 min hold) at a rate of 2°C/min. Injector anddetector 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 withknown PCB composition and content was used as a standard. Concen-trations of individually resolved peaks of PCB isomers and congenerswere summed to obtain total PCB concentrations. OC pesticides werequantified by comparing individual peak area of sample to thecorresponding peak area of the standard.

The recovery of OC pesticides and PCBs in fortified samples werebetween 90 and 110% (n5 3). Procedural blanks were run with everyset of five samples to check for cross-contamination and to correctsample values if needed. The detection limit was 0.2 ng/g (wet wt) forOC pesticides and 1 ng/g (wet wt) for PCBs. The concentrations of OCsare expressed as ng/g on a wet weight basis, unless specified otherwise.DDTs represent the sum ofp,p8-DDE, p,p8-DDD, andp,p8-DDT whileCHLs include cis-chlordane,trans-chlordane,cis-nonachlor, trans-nonachlor, and oxychlordane. HCHs includea-, b-, andg- isomers.

Fig. 1. Map showing sampling locations

388 S. Tanabeet al.

Results and Discussion

Suitability of Whole-Body Homogenates as Indicators

In several studies, bird eggs have been used to indicate local orregional contamination. However, in migratory birds, contami-nants present in females at laying could have been accumulatedin wintering grounds. Similarly, migratory birds use fat reservesas a source of energy during migration; consequently, contami-nants 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 birdswere used in this study. Because feathers were not included inthe analysis, OC burdens in the feathers of long- and short-billed Mongolian plover, representing short-distance migrants,were analyzed and compared with those measured in whole-body homogenates (Table 2). Feather weight accounted for13–16% of the whole body mass in these birds. The concentra-tions of OCs were much lower in feathers than in carcasses.Based on the total weight and concentrations measured, bur-dens of OCs in feathers were estimated to be,4% of the totalloads for both long- and short-billed Mongolian plover. Promi-nently elevated burdens of OC pesticides and PCBs in thewhole-body homogenates suggest suitability of this matrix asan indicator of exposure to OCs. Elimination of feathers fromanalysis may not have significant effect on OC concentrations/

burdens. Further, use of whole-body homogenates will not onlyindicate contamination levels but also provide a means forestimating total body burdens of OCs in birds, which in turnwill help evaluate sex differences in concentrations and transferrates of OCs via egg-laying.

Contamination Pattern

OC pesticides and PCBs were detected in all the samples ofwhole-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 birdsanalyzed in this study followed the order of HCHs. DDTs .PCBs. CHLs 5 HCB. Concentrations of HCHs in residentbirds were in the range of 14–8,800 ng/g. DDTs were thesecond highest, ranging in concentrations from 0.3 to 3,600ng/g. Among various resident birds, pond heron contained thehighest mean concentrations of both DDTs and HCHs of 3,400and 1,100 ng/g, respectively. This feature is similar to thatfound in our earlier study (Rameshet al.1992). High concentra-tion of DDTs and HCHs in pond heron may be explained by itshabitat and feeding near agricultural fields, canals, and ditches(Ali 1979) where applications of these insecticides for agricul-tural and vector control operations have been common. WhileHCHs predominated in most resident birds, pond heron and

Table 1. Biometry and ecological data of birds collected from South India

Species Sample Size and Sex Standard Length (cm) Weight (g) Sampling Sitea

Strict residentBlack drongo (Dicrurus adsimilis) 2 (1 M, 1 F) 23 (22–24) 49 (48–49) 1Black-winged kite (Elanus caeruleus) 1 (F) 30 232 2Common myna (Acridotheres tritis) 3 (1 M, 2 F) 24 (23–24) 133 (118–154) 1Cotton teal (Nettapus coromandelianus) 2 (1 M, 1 F) 39 (39–39) 318 (301–335) 3Crested kingfisher (Ceryle rudis) 1 (M) 25 79 2House crow (Corvus splendens) 2 (M) 37 (37–37) 175 (134–216) 1Little egret (Egretta garzetta) 1 (F) 74 415 3Moorhen (Gallinula chloropus) 1 (F) 37 235 3Pond heron (Ardeola grayii) 2 (1 M, 1 F) 53 (52–53) 212 (203–221) 1 and 3Spotted dove (Streptopelia chinensis) 2 (F) 26 (26–26) 94 (86–102) 1Whitebreasted kingfisher (Halcyon smyrnensis) 1 (F) 26 77 1

Local migrantBlack-winged Stilt (Himantopus himantopus) 1 (M) 58 175 3Kentish Plover (Charadrius alexandrinus) 5 (1 M, 4 F) 16 (15–17) 31 (28–35) 1Little Ringed Plover (Charadrius dubius) 5 (2 M, 3 F) 16 (15–17) 30 (27–32) 1

Short-distance migrantCommon redshank (Tringa totanus) 5 (3 M, 2 F) 30 (28–34) 104 (88–118) 1Long-billed Mongolian plover (Charadrius mongolus;

sub sp.C. atrifrons) 6 (1 M, 5 F) 20 (19–20) 66 (60–69) 1Short-billed Mongolian plover (Charadrius mongolus;

sub sp.C. schaeferi) 6 (5 M, 1 F) 17 (15–19) 45 (36–49) 1White-cheeked tern (Sterna repressa) 5 (3 M, 2 F) 37 (35–38) 94 (88–108) 1

Long-distance migrantCommon sandpiper (Actitis hypoleucos) 5 (4 M, 1 F) 19 (18–20) 43 (39–45) 1Curlew sandpiper (Calidris ferruginea) 5 (2 M, 3 F) 21 (20–22) 51 (44–61) 4Lesser-crested tern (Thalasseus bengalensis) 5 (3 M, 2 F) 41 (39–43) 189 (177–196) 1Terek sandpiper (Xenus cinereus) 3 (1 M, 2 F) 25 (23–26) 51 (51–51) 1White-winged tern (Chlidonias leucopterus) 5 (3 M, 2 F) 24 (23–25) 34 (29–39) 1

Numbers in parentheses represent range of length and weighta See Figure 1 (15 Porto Novo, 25 Cuddalore, 35 Pudukottai, and 45 Mandapam)

389PCBs and Pesticide Accumulation in South Indian Birds

moorhen contained greater DDT concentrations than those ofHCHs. Next to pond heron, the little egret, whose diet ispredominantly grasshoppers, lizards, and frogs, contained ele-vated concentrations of HCHs (8,800 ng/g) and DDTs (970ng/g). Spotted doves contained the lowest mean HCHs andDDTs concentration of 16 and 0.5 ng/g respectively, which wasapparently one to three orders of magnitude lower than thosefound in other birds. PCB concentrations were generally less inresident birds, with the highest value noticed in crestedkingfisher (160 ng/g), which feed primarily on fish. Concentra-tions 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 (30–640ng/g) recorded slightly higher than strict residents (, 20–160ng/g). Little ringed plover revealed highest DDT concentrationof 4,400 ng/g with a wide range of 760–13,000 ng/g measuredamong all the analyzed species. Generally, the observed patternin local migrants can be rated as follows: HCHs$ DDTs .PCBs . CHLs $ HCB. The local migrants are assumed tomigrate from South to North India (i.e., foot Himalayas andKashmir) to avoid hot summer months (March to May) in SouthIndia. Ecological studies have indicated that these three speciesmigrate along the coastal areas of East India ranging fromCalcutta to Madras (Ali 1979) spending most of their time inurbanized and industrialized areas like Visakapatnam, Calcutta,and Madras. This might explain the occurrence of relativelyelevated concentrations of PCBs. Black-winged stilts forage notonly in estuarine marshes, but also agricultural fields and inlandmarshes during their local migration (Goriup 1982), whichexplains lower levels of PCBs but higher levels of HCHs thanother two species of local migrants.

Of the four species of short-distance migrants, commonredshank and white-cheeked tern contained apparently lower

HCH concentrations than those of resident birds and localmigrants (Table 3). Both long- and short-billed Mongolianplovers showed a similar residue pattern; however, the formerexhibited slightly higher concentrations of all OCs except HCB.Interestingly, short-distance migrants (except common reds-hank) accumulated comparable or greater concentrations ofPCBs than DDTs. Furthermore, all five white-cheeked ternsanalyzed in this study contained very high concentrations ofPCBs (430–4,400 ng/g). It can be suggested that the breedinggrounds (Persian Gulf and Red Sea) of white-cheeked ternsmay be heavily contaminated by PCBs.

Long-distance migrants exhibited a different pattern of OCconcentrations compared to short-distance migrants (Table 3).Common sandpipers, terek sandpipers, and white-winged ternshad greater concentrations of DDTs, followed by HCHs orPCBs. Curlew sandpipers exhibited the lowest concentrationamong all long-distance migratory birds with comparable levelsof PCBs, DDTs, and HCHs. Lesser-crested terns recordedgreater PCBs, followed by DDTs and HCHs, probably reflect-ing the magnitude of contamination pattern in breeding groundsin Persian Gulf, similar to white-cheeked terns. The usage ofPCBs in petroleum-based industries in Arabian countries mighthave influenced the excessive exposure of PCBs in this species.Fish collected from coastal waters in Kuwait contained greaterconcentrations of PCBs than DDT (Villeneuveet al. 1987). Theelevated concentration of PCBs as well as other OCs inwhite-cheeked terns may be due to their shoreline feeding habit,while lesser-crested terns mainly feed on pelagic fish, whichmight explain relatively lower concentrations in this speciescompared to white-cheeked terns.

Contamination patterns observed in birds, in general, indicatethat exposure to HCHs and DDTs occurs mainly in India asevidenced from their predominance in local migrants and strictresident birds. Uniformly lower concentrations of PCBs inresident birds suggest that its contamination is lower than those

Table 2. Organocholorine concentrations and burdens in whole-body homogenates and feather of long- and short-billed Mongolian plover

Sample PCBs DDTs HCHs CHLs HCB % of Body Weight

Long-billed Mongolian plover (n5 1)Whole-body homogenatesa 87

Concentration (ng/g on wet wt) 180 600 60 8.3 1.2Burden (µg) 11 35 3.5 0.49 0.071Burden % .98 99 99 .99 96

Feather 13Concentration (ng/g on wet wt) ,20 34 4.4 ,0.2 0.3Burden (µg) ,0.2 0.32 0.040 ,0.002 0.003Burden % ,2 1 1 ,1 4

Short-billed Mongolian plover (n5 1)Whole-body homogenatesa 84

Concentration (ng/g on wet wt) 300 360 450 1.6 1.6Burden (µg) 14 16 16 0.074 0.074Burden % .99 99 99 .99 97

Feather 16Concentration (ng/g on wet wt) ,20 26 17 ,0.2 0.3Burden (µg) ,0.2 0.074 0.11 ,0.001 0.002Burden % ,1 1 1 ,1 3

HCHs5 a 1 b 1 g-isomersDDTs5 p,p8-DDE 1 p,p8-DDD 1 p,p8-DDTCHLs5 oxychlordane1 trans-chlordane1 cis-chlordane1 trans-nonachlor1 cis-nonachlora Excluding feather

390 S. Tanabeet al.

of DDTs and HCHs in India. Earlier studies have shown thepresence of lower concentrations of PCBs compared to DDTsand HCHs in biological samples from India (Tanabeet al.1990;Rameshet al. 1992; Kannanet al. 1992, 1995). India is thegreatest consumer of HCHs in the world (Dave 1996; Liet al.1996). Under the National Malaria Eradication Program ofGovernment of India, about 85% of the DDT produced in Indiais used for vector control (Singhet al. 1988). In contrast toresident birds, migrating birds wintering in India containedrelatively elevated concentrations of PCBs. Such a patternreflects the contamination trend observed in the industrializedcountries of northern hemisphere (White and Krynitsky 1986;Becker 1989; Barronet al. 1995). The exposure to PCBs instopover sites during migration should also be taken intoconsideration. It should be mentioned that some migrants haveaccumulated comparable levels of DDTs and HCHs to those ofresident birds. This may have implications on the samplingperiod of migratory birds in India. Birds were sampled in earlywinter (November and December) and migratory birds maytherefore have acquired HCHs and DDTs in wintering groundsin India, even though for short duration.

The concentrations of CHLs and HCB were uniformly low(Table 3). Little ringed plovers and long-billed Mongolianplovers showed higher mean concentrations of 14 and 12 ng/gof CHLs, respectively. Short-billed Mongolian plovers re-

corded elevated HCB concentration of 11 ng/g, while theresidue levels in most of the other species were, 5 ng/g.Contamination by CHLs and HCB in environmental matrices inIndia is minimal (Kannanet al. 1995). In contrast, CHLs havebeen a prominent contaminant in Australia, New Zealand,Japan, USA, and Canada (Kannanet al. 1994). Low levels ofCHLs measured in most of the migratory birds suggest that thefeeding grounds of these birds may not have been in the abovementioned countries. In addition, relatively faster depuration orelimination of CHLs and HCB during migratory flight shouldbe considered as a possible cause.

Bioaccumulation Features

OC contamination levels in individual species may vary withfeeding habits. The residual concentrations of OCs in birdswereassessed in light of their dietary habits and ecology (Table 4).Generally, among resident birds, inland piscivores andscavengersaccumulated greater concentrations of OC pesticides than thoseof coastal piscivores, omnivores, and granivores. However,accumulation of PCBs were greater among coastal piscivoresthan the other groups, suggesting the presence of major PCBpollution sources in coastal waters of South India.

Table 3. Concentrations of persistent organochlorine residues in resident and migratory birds collected from South India

Species nFatContent (%)

Mean Concentration (ng/g wet wt.)

PCBs DDTs HCHs CHLs HCB

Strict residentBlack drongo 2 6.8 (6.1–7.5) 31 (31–31) 180 (140–210) 680 (600–750) 0.2 (0.2–0.2) 0.7 (0.5–0.8)Black-winged kite 1 11.2 29 640 1,900 0.6 4Common myna 3 5.1 (3.9–6.6) 26 (,20–37) 64 (52–74) 250 (63–570) 0.1 (0.1–0.1) 0.2 (0.2–0.2)Cotton teal 2 11.6 (11.4–11.7),20 (,20–,20) 67 (48–85) 120 (72–160) 0.1 (0.1–0.1) 0.2 (0.2–0.2)Crested kingfisher 1 8.5 160 290 310 0.1 0.3House crow 2 5.9 (5.5–6.2) 42 (39–45) 160 (47–280) 1,000 (820–1,200) 0.4 (0.2–0.6) 0.3 (0.2–0.3)Little egret 1 12 33 970 8,800 0.3 1.2Moorhen 1 13 ,20 510 87 0.1 0.3Pond heron 2 13.1 (10.2–16.3) 44 (22–65) 3,400 (3,100–3,600) 1,100 (1,100–1,100) 2.9 (1.5–4.3) 1.0 (0.9–1.1)Spotted dove 2 8.4 (8.1–8.7) ,20 (,20–,20) 0.5 (0.3–0.7) 16 (14–18) 0.1 (0.1–0.1),0.1 (,0.1–,0.1)Whitebreasted king-

fisher1 9.9 40 410 420 0.4 0.3

Local migrantBlack-winged stilt 1 15.9 30 510 4,100 0.6 2Kentish plover 5 9.1 (7.6–11.0) 150 (69–300) 210 (67–330) 450 (280–590) 1.0 (0.6–1.3) 0.8 (,0.1–1.4)Little Ringed plover 5 7.6 (7.3–8.9) 210 (40–640) 4,400 (760–13,000) 1,000 (390–1,400) 14 (0.8–45) 0.4 (0.3–0.5)

Short-distance migrantCommon redshank 5 10.9 (9.2–12.8) 90 (40–210) 600 (160–1,100) 54 (19–89) 1.4 (0.9–3.0) 1.5 (0.9–3.4)Long-billed Mongo-

lian plover6 7.6 (6.1–9.9) 250 (130–420) 260 (120–620) 310 (62–480) 12 (1.7–24) 3.4 (1.3–4.6)

Short-billed Mongo-lian plover

6 6.7 (6.1–7.8) 160 (71–300) 110 (17–370) 320 (180–470) 1.9 (0.5–3.3) 11 (4.4–23)

White-cheeked tern 5 6.7 (5.2–8.9) 2,700 (430–4,400) 1,000 (220–1,800) 84 (15–200) 2.6 (0.5–3.7) 1.8 (0.8–4.0)Long-distance migrant

Common sandpiper 5 7.4 (4.9–10.3) 120 (70–170) 620 (140–1,900) 230 (82–380) 0.5 (0.3–0.7) 0.6 (0.3–1.6)Curlew sandpiper 5 12.7 (10.2–16.1) 36 (27–48) 11 (9.2–16) 54 (40–82) 1.1 (0.5–2.6) 0.4 (0.2–0.6)Lesser-crested tern 5 11.9 (7.2–16.6) 320 (170–520) 92 (52–170) 32 (19–47) 2.0 (0.8–3.4) 0.9 (0.7–1.3)Terek sandpiper 3 5.6 (4.4–7.4) 550 (37–1,400) 1,200 (180–3,300) 750 (140–5,500) 2.4 (1.0–4.8) 0.8 (0.5–1.2)White-winged tern 5 12.2 (11.1–13.6) 550 (210–850) 1,300 (850–1,700) 360 (36–710) 5.7 (3.9–10) 1.4 (1.1–1.8)

Numbers in parentheses indicate the range

391PCBs and Pesticide Accumulation in South Indian Birds

Wild birds in some Latin American and African countriesrevealed an identical trend. For example, Fyfeet al. (1991)reported higher concentrations of insecticide residues in carnivo-rous and insectivorous birds than in omnivorous and granivo-rous birds. Franket al. (1977) documented a similar trend inKenya, where carnivorous birds from agricultural watershedshad greater residue levels. Generally, birds positioned at the topof the food chain, such as kites, gulls, and eagles, accumulateelevated levels of OC contaminants (Newton 1988).

Among migrants, coastal piscivores accumulated greateramounts of PCBs than inland piscivores and insectivores,similar to the pattern observed for resident birds. In avianspecies, PCB accumulation is related to the content andcomposition of prey, age, and residence time at contaminatedsites (Struger and Weseloh 1985). Bird species that primarilyprey on fish and other birds accumulate PCBs to a greater extentthan birds that feed on lower trophic level organisms (Ram andGillet 1993). Additionally, unlike OC pesticides, PCB usage hasbeen concentrated in high industrial activity areas along coastalwaters, and therefore, serious contamination by PCBs is foundin the coastal environment (Tanabeet al. 1989). This may alsosupport the elevated concentrations of PCBs in coastal piscivo-rous birds.

Sex Differences

Differences in the concentrations of OCs between male andfemale birds of a few species were examined. The species withtwo to three individuals of each sex were used for this purpose;sex difference in concentrations and burdens of OCs arepresented in Table 5. In three species (except white-wingedtern), higher concentrations of OCs were found in males than infemales. Only DDT and HCH residue levels were lower inmales than females of white-winged tern. A similar pattern wasalso observed in whole-body burdens of OCs in these fourspecies of birds. Information pertaining to sex difference in OCresidues in birds varied. While a few studies reported thepresence of elevated concentrations in OCs in males (Larssonand Lindegren 1987; Duursmaet al. 1989), several reportsindicated comparable or greater concentrations in females thanin males (e.g.,Norstromet al.1976; Lemmetyinenet al.1982;Elliott and Shutt 1993). However, no study has discussed sexdifference in OC levels based on whole-body burdens. Al-though some exceptions were found in the present study, mostbirds had a male–female difference in OC burdens. Thereduction of OC whole-body burdens in females suggestsexcretion through egg laying in breeding grounds. However, thedefinitive conclusion should be gained using larger number ofsamples in a future study.

HCH and DDT Compositions

Among various HCH isomersb-HCH was the most predomi-nantly noticed contaminant in all the species of birds analyzed(Figure 2), reflecting more stable natrue ofb-HCH thana- andg- isomers to enzymatic degradation. Interestingly, some resi-dents and migrants such as cotton teal, spotted dove, black-winged stilt, and lesser-crested tern comprised relatively largerproportions ofa- and g-isomers than those in other birds,suggesting recent exposure to technical HCH mixture (contain-ing 70%a-, 15%g-, 6%b-, and 9%d-HCH) used in India.

The composition ofp,p8-DDE was the most abundant ofvarious DDT compounds measured in both resident and migra-tory birds (Figure 3). In some birds, it contributed to more than90% of the total load. Higher composition ofp,p8-DDE in birdsclearly suggests greater ability to transformp,p8-DDT intop,p8-DDE. Similarly, Harperet al. (1996) noticed the presenceof elevated proportion ofp,p8-DDE in neotropical birds col-lected in the U.S. after wintering in Latin America. Relativelylarger proportion ofp,p8-DDT, which is the major constituent(80%) of the technical mixture of DDT in pond heron andspotted dove, suggests that recent exposure to DDT has occuredin India (Figure 3). Slightly higher proportion ofp,p8-DDT inlong- and short-billed Mongolian plovers and curlew sandpip-ers may reflect exposures not only in India but also in breedinggrounds.

Global and Temporal Comparison

The concentrations of HCHs, DDTs, and PCBs measured in thepresent study were compared with those of the values reportedfrom various parts of the world in 1980s and 1990s (Figure 4). Itis noteworthy that HCH residues in Indian birds, both residents

Table 4. Mean concentrations (ng/g wet wt) of organochlorinesin resident and migratory birds according to food habits

Groups n PCBs DDTs HCHs CHLs HCB

Strict residentInland piscivore and

scavenger (BK, LE,PH)

4 37 2,100 3,200 1.7 1.8

Coastal piscivore (CK,WK)

2 100 350 370 0.3 0.3

Omnivore (BD, CM,HC)

7 32 120 590 0.2 0.3

Granivore/occasionallyinsectivore (CT, MH,SD)

5 ,20 130 70 0.1 0.1

Local migrantInland piscivore (BS) 1 30 510 4,100 0.6 2.0Costal piscivore (KP,

LR)10 180 2,300 750 7.2 0.6

Short-distance migrantInland/coastal piscivore

(CR, LP, SP)17 170 310 240 5.2 5.3

Costal piscivore (WT) 5 2,700 1,000 84 2.6 1.8Long-distance migrant

Inland/coastal piscivore(LT, WW)

10 430 680 200 3.9 1.1

Insectivore/piscivore(CS, CA, TS)

13 190 530 280 1.2 0.6

BK 5 black-winged kite, LE5 little egret, PH5 pond heron, CK5crested kingfisher, WK5 whitebreasted kingfisher, BD5 blackdrongo, CM5 common myna, HC5 house crow, CT5 cotton teal,MH 5 moorhen, SD5 spotted dove, BS5 black-winged stilt, KP5kentish plover, LR5 little ringed plover, CR5 common redshank,LP 5 long-billed Mongolian plover, SP5 short-billed Mongolianplover, WT 5 white-cheeked tern, LT5 lesser-crested tern, WW5white-winged tern, CS5 common sandpiper, CA5 curlew sandpiper,TS5 terek sandpiper

392 S. Tanabeet al.

and local migrants, were greater than those reported from otherparts of the world. In fact, recent HCH concentrations recordedin resident birds (in the present study) were greater than thoserecorded in 1987–91 sampling period (Rameshet al. 1992),suggesting continuing or increasing exposure of birds to HCH.Concentrations of DDE in Indian birds were either comparableor lower than those in birds from other parts of the world inrecent years. However, when compared to those of the valuesreported in 1987–91 (Rameshet al. 1992), concentrations ofDDE have increased slightly. It should be noted that DDEconcentration in North American and European birds were highin the early 1980s and declined dramatically due to restriction

on DDT usage. The DDT contamination in Indian birds inrecent years seems to be higher than those in North Americanand European countries. Unless adequate precautions are taken,birds residing and wintering in India will experience harmfuleffects such as population decline, as was observed in NorthAmerica. The concentrations of PCBs in resident birds wereless than those reported from other parts of the world. However,compared to the concentrations reported in 1987–91 (Rameshetal. 1992), there has been a sign of increase in PCB concentra-tions in resident birds. It is assumed that PCB contaminationmay increase in India due to rapid industrialization anddevelopment.

Table 5. Mean concentrations and burdens of organochlorines in whole-body homogenates of male and female birds

Species Sex nFatContent (%)

BW-F(HBW)a (g)

Concentration (ng/g wet wt) Burden (µg)

PCBs DDTs HCHs PCBs DDTs HCHs

Local migrantLittle ringed plover M 3 7.4 26.3 (28.5) 310 6,600 1,300 8.2 170 34

F 2 7.8 29.0 (31.7) 55 930 600 1.6 27 17Short-distance migrant

Common redshank M 3 10.9 93.9 (102.3) 120 750 65 11 70 6.1F 2 11.1 98.5 (107.4) 52 380 37 5.1 37 3.6

White-cheeked tern M 3 6.9 85.3 (95.6) 3,600 1,200 110 310 100 9.4F 2 6.4 77.1 (91.6) 1,300 710 43 100 55 3.3

Long-distance migrantWhite-winged tern M 3 12.7 31.4 (35.6) 700 1,100 270 22 35 8.5

F 2 11.5 27.2 (31.4) 330 1,500 510 8.9 41 14

a BW-F (HBW) denotes body weight without feather and (whole-body weight including feather)

Fig. 2. Percentage composition of HCH isomers in strictresidents, local migrants, short- and long-distance mi-grants collected in South India

393PCBs and Pesticide Accumulation in South Indian Birds

Hazard Evaluation

Since Ratcliffe (1967) first related eggshell thinning to insecti-cides (especially DDT and its metabolites), many authors havecontributed to the knowledge of this phenomenon. It is gener-ally accepted thatp,p8-DDE is a major factor in causing birds tolay thinner eggs, although the mechanism is not yet completelyunderstood (e.g.,Lundholm 1987). Average concentrations ofp,p8-DDE of 20–1,000 µg/g on a lipid weight basis in the liverof birds considered to pose a threat to individual bird reproduc-tion and therefore on the population as a whole (Koemanet al.1973; Platteeuwet al. 1995). The lipid-normalized concentra-tions ofp,p8-DDE in little ringed plover, pond heron, and tereksandpiper were high: 58, 23, and 27 µg/g, respectively, whichare in the range of those values that may cause reproductiveabnormalities in birds, though those values were on thewhole-body lipid weight basis.

Studies relating changes in eggshell thickness as well aspopulation changes in bird species in India are not available. Weestimated the whole-body burden ofp,p8-DDE for selected birdspecies based on their body weight and concentrations ofp,p8-DDE measured in whole-body homogenates to understandthe toxic implications of DDT residues. The body burdens ofp,p8-DDE in two individuals of little ringed plover, oneindividual of pond heron, and one individual of terek sandpiperwere 120–350, 770, and 160 µg, respectively. Assuming atransfer rate of 20% (an average value from Barronet al. 1995)of maternal DDTs to the eggs weighing 20% of the whole bodyweight, the concentrations ofp,p8-DDE in eggs would be

between 3.2–13 µg/g wet wt. Approximately 5% eggshellthinning or more were reported to occur at a concentration ofabout 4 µg/g (wet wt) ofp,p8-DDE in eggs (Dirksenet al.1995).Newton (1988) stated thatp,p8-DDE concentrations greaterthan 3 µg/g (wet wt) in peregrine falcons resulted in reducedbreeding success. Our initial evaluation suggests that pondherons, little ringed plovers, and terek sandpipers may be closeto the threshold of risk. Although our hazard estimate involvesassumptions on egg weight and transfer rate ofp,p8-DDE forgeneral comparative purposes, species-specific hazard assess-ment associated with exposure to DDTs and HCHs is necessaryfor Indian birds.

Conclusions

To our knowledge, this is a first study comparing concentrationsof OCs in migratory and resident birds comprising a wide rangeof species in India. An overall appraisal of OC concentrations inIndian birds suggested greater contamination by HCHs inresident birds. This feature is characteristic for Indian biotabecause most of the studies with wild birds from other parts ofthe world have shown the prevalence of DDTs or PCBs.Therefore, it can be suggested the birds migrating from thenorth acquire considerable levels of HCHs while wintering inIndia. The residue concentrations of DDTs and HCHs in birdshave not shown any sign of reduction. Verma (1990) suggestedthat DDT levels in Indian fauna might decline in the future dueto the recent ban of DDT from agricultural usage. The

Fig. 3. Percentage composition of DDT compounds instrict residents, local migrants, short- and long-distancemigrants collected in South India.

394 S. Tanabeet al.

magnitude of exposure to various contaminants in winteringgrounds in India can be assessed by collecting birds at the endof the wintering season. Further, comparison of the concentra-tions of PCBs in resident birds collected in 1987–91 with thoseof 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 experiencegreater risks from DDT exposure in India. Further studiesmeasuring the concentrations of DDTs in eggs of residentavifauna are necessary to elucidate vulnerable species.

Fig. 4. International comparision of PCBs, DDE andHCHs levels in birds. Serial number correspond to thefollowing references: 1: Ohlendorf and Miller (1984),2: Fitzneret al.(1988), 3: Elliottet al.(1996), 4: Fal-andyszet al.(1994), 5: Scharenberg (1991), 6: Olafs-dottir et al.(1995), 7: Lambertini and Leonzio (1986),8: Castilloet al.(1994), 9: Everaartset al.(1991), 10:Daelemanset al.(1992), 11: Gurugeet al.(1997), 12:Rameshet al.(1992), 13: White and Krynitsky (1986),14: Rumboldet al (1996), 15: Harperet al.(1996), 16:Mora (1997), 17: Olsenet al.(1992), 18: Niethammeret al (1984), 19: Fyfeet al.(1991), 20: Tarhanenet al.(1989), 21: Falandyszet al.(1988), 22: Kaphaliaet al.(1981), *present study: *1strict residents, *2local mi-grants, *3short-distance migrants, *4long-distance mi-grants

395PCBs and Pesticide Accumulation in South Indian Birds

Acknowledgments.The authors wish to thank the staff of the Centerof Advanced Study in Marine Biology, Annamalai University, fortheir help in sample collection. This research was supported by aGrant in Aid for the Scientific Research from the Ministry ofEducation, Science and Culture of Japan (Project Nos. 09041163 and09306021).

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