Shagufta NIGHAT, Shahid IQBAL, Muhammad Sajid NADEEM, Tariq MAHMOOD, Syed İsrar SHAH

Estimation of heavy metal residues from the feathers of Falconidae, Accipitridae, and Strigidae in Punjab, Pakistan

The concentrations of heavy metals (Cd, Zn, Ni, Pb, Cu, As) in feather samples of raptors of 3 families were determined from southern, central, and northern parts of Punjab Province. Deposition of metals significantly varied among the families for Cd, Zn, Ni, and Pb; further, these 4 metals also significantly differed between Accipitridae and Falconidae, and between Falconidae and Strigidae. Similarly, Cd, Ni, and As were significantly different among southern, central, and northern Punjab. Falconidae deposited higher concentrations of metals than Accipitridae and Strigidae, with the Common Kestrel being more susceptible. Likewise, central Punjab appeared to be more polluted than northern and southern Punjab. The concentrations of metals reported are alarming and require proper management.

Keywords:

raptors, feathers, Punjab, Heavy metals,

PDF

___

Abbas, S.T., Mehdi, S.M., Sarfraz, M. and Hassan, G. 2004. Contents of heavy-metals in waters of nullahs dek, bisharat and aik, and their effect on soil-health. Science Vision 9: 1–11.
Abernathy, C.O., Y-Liu, D., Longfellow, H.V., Aposhia, B., Beck, B., Fowler, R., Goyer, R., Menzer, T., Rossman, C., Thompson, M. and Waalkes 1999. Arsenic: health effects, mechanisms of actions, and research issues. Environ. Health Perspect. 107: 593–597.
Adrian, W.J. and Stevens, M.L. 1979. Wet versus dry weights for heavy metal toxicity determination in duck liver. J. Wildl. Dis. 15: 125–126.
Aftab, Z., Ali, L., Khan, A.M., Robinson, A.C. and Irshad, I.A. 2000. Industrial policy and the environment in Pakistan, industrial policy and environment, United Nations Industrial Development Organization, pp: 1–117.
Agarwal, S.K., 2002. Pollution management: Heavy metal pollution. APH Publishing Corporation, New Delhi, 4: 7–190.
Baluch, U.K., 1995. Pesticide monitoring programme. WWF Pakistan, Lahore, Mimeo.
Battaglia, A., Ghidini, S., Campanini, G. and Spaggiari, R., 2003. Heavy metal contamination in Little Owl (Athene noayua) and Common Buzzard (Buteo buteo) from Northern Italy. Ecotoxicol. Environ. Saf. 60: 61–66.
Belskii, E.A., Bezel, V.S. and Lyakhov, A.G., 1995. Reproductive characteristics of some birds nesting in hollows under the impact of industrial pollution. Russ. J. Ecol. 26: 126–131.
Boncompagni, E., Muhammad, A., Jabeen, R., Orvini, E., Gandini, C., Sanpera, C., Ruiz, X. and Fasola, M. 2003. Egrets as monitors of trace-metal contamination in wetlands of Pakistan. Arch. Environ. Contam. Toxicol. 45: 399–406.
Bortolotti, G. and Barlow, J., 1985. Neutron activation analysis of bald eagle feathers: analytical precision and sources of sampling variation. Canad. J. Zool. 63: 2707–2718.
Braune, B.M. and Gaskin, D.E. 1987. Mercury levels in Bonaparte’s gulls (Larus philadelphia) during autumn molt in the Quoddy region, New Brunswick, Canada. Arch. Environ. Contam. Toxicol. 16: 539–549.
Buerger, T.T., Mirachi, R.E. and Lisano, M.E. 1986. Effects of lead shot ingestion of captive mourning dove survivability and reproduction. J. Wildl. Manage. 50: 1–8.
Burgat, V. 1990. Un micropollutant: le Cadmium. Bull. O. N. C. 146: 40–
Burger, J. 1993. Metals in avian feathers: bio-indicators of environmental pollution. Rev. Environ. Toxicol. 5: 203–311.
Burger, J. and Gibbons, J.W. 1998. Trace elements in egg contents and egg shells of slider turtles (Trachemys scripta) from the Savannah River site. Arch. Environ. Contam. Toxicol. 34: 382–386.
Burger, J. and Gochfeld, M. 1993. Heavy metal and selenium levels in feathers of young egrets and herons from Hong Kong and Szechuan, China.
Arch. Environ. Contam. Toxicol. 25: 322– 3 Burger, J. and Gochfeld, M. 1997. Heavy metal and selenium concentrations in feathers of egrets from Bali and Sulawesi, Indonesia. Arch. Environ. Contam. Toxicol. 32: 217–221.
Burger, J., Gochfeld, M., Jeitner, C., Burke, S., Volz, C. D., Snigaroff, R., Snigaroff, D., Shukla, T. and Shukla, S. 2009. Mercury and other metals in eggs and feathers of glaucous-winged gulls (Larus glaucescens) in the Aleutians. Environ. Monit. Assess. 152: 179–194.
Cheney, M.A., Hacker, C.S. and Schroder, G.D. 1981. Bioaccumulation of lead and cadmium in the Louisiana heron Hydranassa tricolor and the cattle egret Bubulcus ibis. Ecotoxicol. Environ. Saf. 5: 211–224.
Dauwe, T., Bervoets, L., Pinxten, R., Blust, R. and Eens, M. 2003. Variation of heavy metals within and among feathers of birds of prey : effects of molt and external contamination. Environ. Pollut. 124: 429–436.
Dauwe, T., Janssens, E., Bervoets, L., Blust, R. and Eens, M. 2004. Relationships between metal concentrations in great tit nestlings and their environment and food. Environ. Pollut. 131: 373–380.
Dauwe, T., Janssens, E. and Eens, M., 2006. Effects of heavy metal exposure on the condition and health of adult great tits (Parus major). Environ. Pollut. 140: 71–78.
Dauwe, T., Janssens, E., Pinxten, R. and Eens, M. 2005. The reproductive success and quality of blue tits (Parus caeruleus) in a heavy metal pollution gradient. Environ. Pollut. 136:243– 2
Dauwe, T., Lieven, B., Ellen, J., Rianne, P., Ronny, B. and Marcel, E. 200 Great and blue tit feathers as biomonitors for heavy metal pollution. Ecological Indicators 1: 227–234. Debacker, V., Jauniaux, T., Coignoul, F. and Bouquegneau, J-M. 2000. Heavy metals contamination and body condition of wintering guillemots (Uria aalge) at the Belgian coast from 1993 to 1998. Environ. Res. 84: 310–7.
Denneman, W.D. and Douben, P.E.T. 1993. Trace metals in primary feathers of the Barn Owl (Tyto alba guttattus) in the Netherlands. Environ. Pollut. 82: 301–310.
Doi, R. and Fukuyama, Y. 1983. Metal content in feathers of wild and zoo-kept birds from Hokkaido, 1976-1978. Bull. Environ. Contam. Toxicol. 31: 1–8.
Doneley, R. 1992. Zinc toxicity in caged and aviary birds—new wire disease. Aust. Vet. Pract. 22: 6–11.
Duker, A.A., Carranza, E.J.M. and Hale, M. 2005. Arsenic geochemistry and health. Environ. Int. 31: 631–641.
Eisler, R. 1988. Lead hazards to fish, wildlife and invertebrates: A synoptic review, Biological Report 85, US Fish and Wildlife Service, Laurel, MD.
Fransion, M.A. 1981. Standard methods for determination of wastes and waste water. Method No. 32(D), 15th ed., pp. 225.
Furness, R.W. 1996. Cadmium in birds. In: Beyer, W.N., Heinz, G.H., Redmon-Norwood, A.W., (editors) Environmental Contaminants in Wildlife, Interpreting Tissue Concentrations. Lewis Pub., Boca Raton, p. 389–404.
Furness, R.W., Muirhead, S.J. and Woodburn, M. 1986. Using bird feathers to measure mercury in the environment: relationship between mercury content and moult. Marine Pollut. Bull. 17: 27–
Gasaway, W.C. and Buss, I.O. 1972. Zinc toxicity in the mallard duck. J. Wildlife Manage. 36: 1107–1117.
Gerbersmann, C., Heisterlamp, M., Adams, F.C. and Broekaert, J.A.C. 1997. Two methods for the speciation analysis of mercury in fish involving microwave-assisted digestion and gas chromatography-atomic emission spectrometry. Analytica Chimica Acta. 350: 273–285.
Goede, A.A. and Bruin, M.D. 1984. The use of bird feather parts as a monitor for metal pollution. Environ. Pollut. 8: 281–298.
Grove, R.A., Henny, C.J. and Kaiser, J.L. 2009. Osprey: Worldwide sentinel species for assessing and monitoring environmental contamination in rivers, lakes, reservoirs and estuaries. Toxicol. Environ. Health Part B, 12: 1–20.
Güven, K., Özbay, C., Unlu, E. and Sattar, A. 1999. Acute lethal toxicity and accumulation of copper in Gammarus pulex L. Turk. J. Biol. 23: 513–521.
Hahn, E., Hahn, K. and Stoeppler, M., 1993. Bird feathers as bioindicators in areas of the German Environmental Specimen Bank—bioaccumulation of mercury in food chains and exogenous deposition of atmospheric pollution with lead and cadmium. Sci. Total Environ. 139: 259–270.
Hanif, M., Butt, M.A. and Khattak, M.A. 1987. Hazardous chemical industries and safety measures in Pakistan. Environment and Urban Affairs Division, Ministry of Housing and Works, Govt. of Pakistan, pp. 7.
Hardoy, J.E., Mitlin, D. and Satterhwaite, D. 1992. Environmental Problems in Third World Cities. Earth Scans Publications Ltd, London.
Hernández, L. M., Gómara, B., Fernández, M., Jiménez, B., González, M.J., Baos, R., Hiraldo, F., Ferrer, M., Benito, V., Suñer, M.A., Devesa, V., Muñoz, O. and Montoro, R. 1999. Accumulation of heavy metals and As in wetlands birds in the area around Doñana National Park affected by the Aznalcollar toxic spill. Sci. Total Environ. 242: 293–308.
Hinrichsen, D., Robey, B. and Upadhyay, U.D. 1997. Solutions for a water-short world population reports, Series M, No. 14. Baltimore, Johns Hopkins School of Public Health, Population Information Program.
Honda, K., Min, B.Y. and Tatsukawa, R. 1986. Organ and tissue distribution of heavy metals, and age-related changes in the eastern great white egret Egretta alba modesta in the Korea. Arch. Environ. Contam. Toxicol. 15: 185–197.
Huan, C., Ke, Q., Costa, M. and Shi, X. 2004. Molecular mechanisms of arsenic carcinogenesis. Mol. Cell Biochem. 255: 57–66.
Hui, C.A. 2002. Concentrations of chromium, manganese, and lead in air and in avian eggs. Environ. Pollut. 120:201–6.
Irwin, R.J. 1997. Environmental Contaminants Encyclopedia. National Park Service, Water Resources Division, Colorado.
Jackson, R. and Grainge, J.W. 1975. Arsenic and cancer. Canadian Medical Association Journal 113: 396–401.
Janssens, E., Dauwe, T., Pinxten, R., Bervoets, L., Blust, R. and Eens, M. 200 Effects of heavy metal exposure on the condition and health of nestlings of the great tit (Parus major), a small songbird species. Environ. Pollut. 126: 267–74. Karn, S.K. and Harada, H. 2001. Surface water pollution in three urban territories of Nepal, India, and Bangladesh. Environ. Manage. 28: 483–496.
Kenntner, N., Krone, O., Altenkamp, R. and Tataruch, F. 2003. Environmental contaminants in liver and kidney of freeranging northern goshawks (Accipiter gentilis) from three regions of Germany. Arch. Environ. Contam. Toxicol. 45: 128–135.
Kenntner, N., Crettenand, Y., Funfstuck, H., Janovsky, M. and Tataruch, M. 2007. Lead poisoning and heavy metal exposure of golden eagles (Aquila chrysaetos) from the European Alps. J. Ornith, 148: 173–177.
Koo, J. and Koo, T. 2008. Heavy metal concentrations in feathers of Korean shorebirds, Arch. Environ. Contam. Toxicol. 55: 122– 1
Kushlan, J.A. 1993. Colonial waterbirds as bioindicators of environmental change. Colonial Waterbirds 16: 223–251.
Lee, C.S.L., Li, X., Shi, W., Cheung, S.C. and Thornton, I. 2006. Metal contamination in urban, suburban and country park soils of Hong Kong: a study based on GIS and multivariate statistics. Sci. Total Environ. 356: 45–61.
Levengood, J.M., Sanderson, G.C., Anderson, W.L., Foley, G.L., Skowron, L.M., Brown, P.W. and Seets, J.W. 1999. Acute toxicity of ingested zinc shot in game-farm mallards. Ill. Nat. Hist. Surv. Bull. 36: 1–36.
Malik, R.N. and Zeb, N. 2009. Assessment of environmental contamination using feathers of Bubulcus ibis L., as a biomonitor of heavy metal pollution, Pakistan. Ecotoxicology 18: 522–536.
Martin, M.B., Reiter, R., Pham, T., Avellanet, Y.R., Camara, J. and Lahm, M. 2003. Estrogen-like activity of metals in MCF-7 breast cancer cells. Endocrinology 144: 2425–36.
Mateo, R.J., Estrada, J.Y., Paquet, X., Riera, L., Domínguez, R., Guitart, A. and Martínez-Vilalta. 1999. Lead shot ingestion by marsh harriers (Circus aeruginosus) from Ebro delta, Spain. Environ. Pollut. 104: 435–440.
Mateo, R., Taggart, M. and Meharg, A.A. 2003. Lead and arsenic in bones of birds of prey from Spain. Environ. Pollut. 126(1): 107–114.
Movalli, P.A. 2000. Heavy metal and other residues in feathers of Laggar Falcon (Falco biarmicus juggar) from six districts of Pakistan. Environ. Pollut. 109: 267–275.
Muralidharan, S., Jayakumar, G. and Vishnu, G. 2004. Heavy metals in feathers of six species of birds in the district Nilgris, India. Bull. Environ. Contam. Toxicol. 73: 285–291.
Nemery, B. 1990. Metal toxicity and the respiratory tract. European Respiratory Journal. 3: 202–219.
Nordberg, G.F. 1971. Effects of acute and chronic cadmium exposure on the testicles of mice. Environ. Physio. Biochem. 1: 171–187.
Nyholm, N.E.I. 1993. Heavy metal tissue levels, impact on breeding and nestling development in natural populations of the pied flycatcher (Aves) in the pollution gradient from a smelter. In: Eijsackers, H., Heinbach, F., Donker, M. (Eds.). Ecotoxicology of Test Organisms. Lewis, Chelsee, USA.
Pain, D.J., Sears, J. and Newton, T. 1995. Lead concentrations in birds of prey in Britain. Environ. Pollut. 87: 173–180.
Palma, L., Beja, P., Tavares, P.C. and Monteiro, L.R. 2005. Spatial variation of mercury levels in nesting Bonelli’s eagles from Southwest Portugal: effects of diet composition and prey contamination. Environ. Pollut. 134: 549–557.
Pandey. S. 2006. Water pollution and health (review article). Kathmandu University Medical Journal 4: 128–134.
Pérez-López, M., Cid, F., Oropesa, A.L., Hidalgo, L.E., López-Beceiro, A. and Soler, F. 2008. Heavy metal and arsenic content in raptor species from Galcia (NW Spain). Ecotoxicol. Environ. Saf. 70: 154–162.
Peplow, D, 2000. Environmental impacts of hard-rock mining in Eastern Washington. University of Washington. Fact Sheet No. 8.
Raihan, S., Sarwar, F., Azim, M., Khan, O.Y. and Ahmed, N. 1995. Isolation, characterization and assessment of nickel and cadmium accumulation of bacterial isolates from industrial waste. Biotechnology for Environment and Agriculture. B.C.C. and T. Press, Univ. of Karachi, p. 143–152.
Saeki, K., Okabe, Y., Kim, E.Y., Tanabe, S., Fukuda, M. and Tatsukawa, R. 2000. Mercury and cadmium in common cormorant (Pholacrocorax carbo). Environ. Pollut. 108: 249–255.
Sanpera, C., Morera, M., Ruiz, X. and Jover, L. 2000. Variability of mercury and selenium levels in clutches of Audouin’s gulls (Larus audouinii) breeding at the Chafarinas Islands, Southwest
Mediterranean. Arch. Environ. Contam. Toxicol. 39: 119–123. Scheuhammer, A.M. 1987. The chronic toxicity of aluminium, cadmium, mercury and lead in birds: a review. Environ. Pollut. 46: 263–296.
Sileo, L., Beyer, W.N. and Mateo, R., 2003. Pancreatitis in wild zincpoisoned waterfowl. Avian Pathol. 32: 655–660.
Spahn, S.A. and Sherry, T.W. 1999. Cadmium and lead exposure associated with reduced growth rates, poor fledgling success of Little Blue Heron Chicks (Egretta caerulea) in South Louisiana wetlands. Arch. Environ. Contam. Toxicol. 37: 377–384
Stoica, A., Katzenellenbogen, B.S. and Martin, M.B. 2000. Activation of estrogen receptor α by the heavy metal cadmium. Molecular Endocrinology. 14: 545–53.
Stout, J.H. and Trust, K.A. 2002. Elemental and organochlorine residues in bald eagles from Adak Island, Alaska. J. Wildl. Dis. 38(3): 511–517.
Taggart, M.A., Figuerola, J., Green, A.J., Mateo, R., Deacon, C., Osborn, D. and Meharg, A.A. 2006. After the Aznalcóllar mine spill: arsenic, zinc, selenium, lead and copper levels in the livers and bones of five waterfowl species. Environ. Res. 100: 349–361.
Taggart, M.A., Green, A.J., Mateo, R., Svanberg, F. and Hillstro, L. 200 Ecotoxicology and environmental safety metal levels in the bones and livers of globally threatened marbled teal and white-headed duck from El-Hondo, Spain. Ecotoxicol. Environ. Saf. 72: 1–9. Tahir, M.A., Chandio, B.A., Abdullah, M. and Rashid, A. 1998. Drinking water quality monitoring in the rural areas of Rawalpindi. National Workshop on Quality of Drinking Water.
Pakistan Council of Research in Water Resources, Islamabad. Tahir, S.S. and Naseem, R. 2007. Removal of Cr (III) from tannery wastewater by adsorption onto bentonite clay. Separation and Purification Technology. 53: 312–321.
Tariq, J., Jaffar, M., Ashraf, M. and Moazzam, M. 1994. Trace metal concentration, distribution and correlation in water, sediment and fish from Ravi River, Pak. Fish Res. 19: 131–139.
Tehseen, W.M., Hansen, L.G., Wood, S.G. and Hanif, M. 1994. Assessment of chemical contaminants in water and sediment samples from Degh Nala in Province of Punjab, Pakistan. Arch.
Environ. Contam. Toxicol. 26: 78–89. Thorp, J.H., Geisy, J.P. and Wineriter, S.A. 1979. Effects of chronic exposure cadmium on cray fish survival, growth and tolerance to elevated temperatures. Arch. Environ. Contam. Toxicol. 8: 449–456.
Wayland, M. and Bollinger, T. 1999. Lead exposure and poisoning in bald eagles and golden eagles in the Canadian Prairie Provinces. Environ. Pollut. 104: 341–350.
Wayland, M., Neugebauer, E. and Bollinger, T., 1999. Concentrations of lead in liver, kidney, and bone of bald and golden eagles. Arch. Environ. Contam. Toxicol. 37(2): 267–272.
Webb, J.L. 1966. Enzymes and Metabolic Inhibitors. Vol. 3. Academic Press, New York, pp.595–793.
Wiemeyer, S.N., Thair, G.L. and Locke, L.N., 1980. Residues of environmental pollutants and necropsy data for Eastern United States ospreys 1964–1973. Estuaries 3: 155–167.
Zaccaroni, A., Amorena, M., Naso, B., Castellani, G., Lucisano, A. and Stracciari, G.L. 2003. Cadmium, chromium and lead contamination of Athene noctua, the little owl, of Bologna and Parma, Italy. Chemosphere 52(7): 1251–1258.
Zaman, A. and Ara, I. 2000. Rising urbanization in Pakistan, some facts and suggestions. The Journal of NIP 7: 31–46.
Zhao, C.W., Young, M.R., Biwan, B.A., Coogan, T.P. and Waalkes, M.P. 1997. Association of arsenic-induced malignant transformation with DNA hypomethylation and aberrant gene expression. Proc. Natl. Acad. Sci. USA 94: 10907–10912.
Zolfaghari, G., Esmaili-sari, A. and Mahmoud, S. 2007. Examination of mercury concentration in the feathers of 18 species of birds in southwest Iran. Environmental Research, 104: 258–265.