, Volume 22, Issue 10, pp 1490–1497 | Cite as

Age-dependent accumulation of heavy metals in liver, kidney and lung tissues of homing pigeons in Beijing, China

  • Jia Cui
  • Bin Wu
  • Richard S. Halbrook
  • Shuying Zang


Biomonitoring provides direct evidence of the bioavailability and accumulation of toxic elements in the environment. In the current study, 1–2, 5–6, and 9–10+ year old homing pigeons collected from the Haidian District of Beijing during 2011 were necropsied and concentrations of cadmium, lead, and mercury were measured in liver, lung, and kidney tissue. At necropsy, gray/black discoloration of the margins of the lungs was observed in 98 % of the pigeons. There were no significant differences in metal concentrations as a function of gender. Cadmium concentrations in all tissues and Pb concentrations in the lung tissues were significantly greater in 9–10+ year old pigeons compared to other age groups indicating that Cd and Pb were bioavailable. Mercury concentrations were not significantly different among age groups. Cadmium concentrations in kidney and lung tissues of 9–10+ year old pigeons were similar to or exceeded concentrations of Cd reported in pigeons from another high traffic urban area and most wild avian species from Korea suggesting that Cd in this region of Beijing may be of concern. Homing pigeons provide valuable exposure and bioaccumulation data not readily available from air monitoring alone, thus providing information regarding potential health effects in wildlife and humans in urban areas. As environmental quality standards are implemented in China, homing pigeons will serve as a valuable bio-monitor of the efficacy of these actions.


Heavy metals Homing pigeons Tissues Distribution Age 



This research was financially supported by the key National Natural Science Foundation of China (No. 41030743), the Science and Technology Innovative Programs Foundation of Higher Education of Heilongjiang Province, China (No. 2010td10). We are grateful to Zhai Dan Lei for her assistance and support of our research. The authors also thank Mr. Xinmin Liu for providing the pigeons from Beijing for our research.

Conflict of interest

The authors declare that they have no conflict of interest.


  1. Bafundo KW, Baker DH, Fitzgerald PR (1984) Eimeria acervulina infection and the zinc–cadmium interrelationship in the chick. Poult Sci 63:1828–1832CrossRefGoogle Scholar
  2. Brown RE, Brain JD, Wang N (1997) The avian respiratory system: a unique model for studies of respiratory toxicosis and for monitoring air quality. Environ Health Perspect 105:188–200CrossRefGoogle Scholar
  3. Bull KR, Murton RK, Osborn D, Ward P, Chen G (1977) High cadmium levels in Atlantic sea birds and seaskaters. Nature 269:507–509CrossRefGoogle Scholar
  4. Carey JR, Judge DS (2000) Longevity records: life spans of mammals, birds, amphibians, reptiles, and fish. Odense University Press, OdenseGoogle Scholar
  5. Cheng L, Schulz-Baldes M, Harrison CS (1984) Cadmium in ocean-skaters, (Halobates sericeus (lnsecta)), and in their seabird predators. Mar Biol 79:321–324CrossRefGoogle Scholar
  6. Cizdziel JV, Dempsey S, Halbrook RS (2013) Preliminary evaluation of the use of homing pigeons as biomonitors of mercury in urban areas of the USA and China. Bull Environ Contam Toxicol 90:302–307CrossRefGoogle Scholar
  7. Clark RB (1992) Marine pollution. Clarendon Press, Oxford, pp 61–79Google Scholar
  8. Connors PG, Anderlini VC, Risebrough RW, Gilbertson M, Hays H (1975) Investigations of metals in common tern populations. Can Field Nat 89:157–162Google Scholar
  9. Custer TW, Franson JC, Pattee OH (1984) Tissue lead distribution and hematologic effects in American kestrels (Falco sparverius L.) fed biologically incorporated lead. J Wildl Dis 20:39–43CrossRefGoogle Scholar
  10. Di Giulio RT, Scanlon PF (1984) Heavy metals in tissues of waterfowl from the Chesapeake Bay USA. Environ Pollut Ser 35:29–48CrossRefGoogle Scholar
  11. Eens M, Pinxten R, Verheyen RF, Blust R, Bervoets I (1999) Great and blue tits as indicators of heavy metal contamination in terrestrial ecosystems. Ecotoxicol Environ Safe 44:81–85CrossRefGoogle Scholar
  12. Falandysz J (1994) Some toxic and trace metals in big game hunted in the northern part of Poland in 1987–1991. Sci Total Environ 141:59–73CrossRefGoogle Scholar
  13. Finley MT, Stickel WH, Christensen RE (1979) Mercury residues in tissues of dead and surviving birds fed methylmercury. Bull Environ Contam Toxicol 21:105–110CrossRefGoogle Scholar
  14. Furness RW (1996) Cadmium in birds. In: Beyer WN, Heinz GH, Redmon AW (eds) Interpreting environmental contaminants in animal tissues. Lewis Publishers, Boca RatonGoogle Scholar
  15. Gragnaniello S, Fulgione D, Milone M, Soppelsa O, Cacace P, Perrara L (2001) Sparrows as possible heavy metal biomonitors of polluted environments. Bull Environ Contam Toxicol 66:719–726CrossRefGoogle Scholar
  16. Harrop DO, Mumby K, Ashworth J, Nolan J, Price M, Pepper B (1990) Air quality in the vicinity of urban roads. Sci Total Environ 93:285–292CrossRefGoogle Scholar
  17. Heinz G (1976) Methylmercury: second-year feeding effects on mallard reproduction and duckling behaviour. J Wildl Manage 40:82–90CrossRefGoogle Scholar
  18. Heinz G (1980) Comparison of game-farm and wild-strain mallard ducks in accumulation of methylmercury. J Environ Pathol Toxicol 3:379–386Google Scholar
  19. Hutton M, Goodman GT (1980) Metal contamination of feral pigeons Columba livia from the London area. Part I: tissue accumulation of lead cadmium and zinc. Environ Pollut Ser A 22:207–217CrossRefGoogle Scholar
  20. Ikeda M, Zhang ZW, Shimbo S, Watanabe T, Nakatsuka H, Moon CS, Matsuda-Inoguchi N, Higashikawa K (2000) Urban population exposure to lead and cadmium in east and south-east Asia. Sci Total Environ 249:373–384CrossRefGoogle Scholar
  21. Johnston RF, Janiga M (1995) Feral Pigeons. Oxford University Press, New YorkGoogle Scholar
  22. Kendall RJ, Scanlon PF (1981) Effects of chronic lead ingestion on reproductive characteristics of ringed turtle doves (Streptopelia risoria) and on tissue lead concentrations of adults and their progeny. Environ Pollut 26:203–213CrossRefGoogle Scholar
  23. Kim J, Shin JR, Koo TH (2009) Heavy metal distribution in some wild birds from Korea. Arch Environ Contam Toxicol 56:317–324CrossRefGoogle Scholar
  24. Lee DP, Honda K, Tatsukawa R (1987) Comparison of tissue distributions of heavy metals in birds in Japan and Corea. J Yamashina Inst Ornithol 9:103–116CrossRefGoogle Scholar
  25. Liu WX, Ling X, Halbrook RS, Martineau D, Dou H, Liu X, Zhang G, Tao S (2010) Preliminary evaluation on the use of homing pigeons as a biomonitor in urban areas. Ecotoxicology 19:295–305CrossRefGoogle Scholar
  26. Lock JW, Thompson DR, Furness RW, Bartle JA (1992) Metal concentrations in seabirds of the New Zealand region. Environ Pollut 75:289–300CrossRefGoogle Scholar
  27. Mailman RB (1980) Heavy metals. In: Perry JJ (ed) Introduction to environmental toxicology. Elsevier, New York, pp 34–43Google Scholar
  28. Merian E (1991) Metals and their compounds in the environment; occurrence, analysis and biological relevance. VCH, WeinheimGoogle Scholar
  29. Mohammed AS, Kapri A, Goel R (2011) Heavy metal pollution: source, impact, and remedies. Environ Pollut 20:1–28CrossRefGoogle Scholar
  30. Nam DH, Lee DP (2006) Monitoring for Pb and Cd pollution using feral pigeons in rural, urban, and industrial environments of Korea. Sci Total Environ 357:288–295CrossRefGoogle Scholar
  31. Ohi G, Seki H, Akiyama K, Yagyu H (1974) The pigeon, a sensor of lead pollution. Bull Environ Contam Toxic 12:92–98CrossRefGoogle Scholar
  32. Ohi G, Seki H, Minowa K, Ohsawa M, Mizoguchi I, Sugimoro F (1981) Lead pollution in Tokyo-the pigeon reflects its amelioration. Environ Res 26:125–129CrossRefGoogle Scholar
  33. Pass DA, Little PB, Karstad LA (1975) The pathology of subacute and chronic methylmercury poisoning of mallard ducks (Anas platyrhynchos). J Comp Pathol 85:7–21CrossRefGoogle Scholar
  34. Richardson ME, Fox MRS (1974) Dietary cadmium and enteropathy in the Japanese quail. Lab Invest 31:722–731Google Scholar
  35. Scheuhammer AM (1987) The chronic toxicity aluminium, cadmium, mercury and lead in birds: a review. Environ Pollut 46:263–295CrossRefGoogle Scholar
  36. Schilderman PAEL, Hoogewerff JA, Schooten FJV, Maas LM, Moonen EJC, Os BJHV, Wijnen JHV, Kleinjans JCS (1997) Possible relevance of pigeons as an indicator species for monitoring air pollution. Environ Health Perspect 3(105):322–330CrossRefGoogle Scholar
  37. Stickel LF, Stickel WH, McLane MAR, Bruns M (1977) Prolonged retention of methyl mercury by mallard drakes. Bull Environ Contain Toxicol 18:393–400CrossRefGoogle Scholar
  38. Stuart BO (1976) Deposition and clearance of inhaled particles. Environ Health Perspect 16:41–53CrossRefGoogle Scholar
  39. Swaileh KM, Sansur R (2006) Monitoring urban heavy metal pollution using the House Sparrow (Passer domesticus). J Environ Monit 8:209–213CrossRefGoogle Scholar
  40. Tansy MF, Roth RP (1970) Pigeons: a new role in air pollution. J Air Pollut Control Assoc 20:307–309CrossRefGoogle Scholar
  41. Thompson DR (1990) Metal levels in marine vertebrates. In: Furness RW, Rainbow PS (eds) Heavy metals in the marine environment. CRC Press, Boca Raton, pp 197–204Google Scholar
  42. USEPA (1994) Method 200.8: Determination of trace elements in waters and wastes by inductively coupled plasma-mass spectrometry—revision 5.4. US Environmental Protection Agency, Office of Research and Development, Cincinnati, OhioGoogle Scholar
  43. USEPA (1996) Method 3050B: Acid digestion of sediments, sludges, soils, and oils: revision 2. US Environmental Protection Agency, Washington DCGoogle Scholar
  44. White DH, Finley MT (1978) Uptake and retention of dietary cadmium in mallard ducks. Environ Res 17:53–59CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2013

Authors and Affiliations

  • Jia Cui
    • 1
  • Bin Wu
    • 1
  • Richard S. Halbrook
    • 2
  • Shuying Zang
    • 1
  1. 1.Key Laboratory of Remote Sensing Monitoring of Geographic EnvironmentHarbin Normal UniversityHarbinPeople’s Republic of China
  2. 2.Cooperative Wildlife Research LaboratorySouthern Illinois University (Emeritus)CarbondaleUSA

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