Carbofuran and its Toxic Metabolites Provide Forensic Evidence for Furadan Exposure in Vultures (Gyps africanus) in Kenya

  • Peter O. Otieno
  • Joseph O. LalahEmail author
  • Munir Virani
  • Isaac O. Jondiko
  • Karl-Werner Schramm


Forensic analysis of carbofuran residues in weathered tissue samples for evidence of Furadan exposure in vultures (Gps africanus) by HPLC gave concentration (mg/Kg dry tissue weight) ranges of bdl – 0.07 (carbofuran), bdl – 0.499 (3-ketocarbofuran) and 0.013–0.147 (3-hydroxycarbofuran) in beaks, bdl–0.65 (carbofuran), 0.024–0.190 (3-ketocarbofuran) and 0.017–0.098 (3-hydroxycarbofuran) in feet, 0.179–0.219 (3-ketocarbofuran) and 0.081–0.093 (3-hydroxycarbofuran) in crop content, 0.078–0.082 (3-ketocarbofuran) and 0.091–0.101 (3-hydroxycarbofuran) in muscle of a laced carcass and 0.006–0.014 (carbofuran), 0.590–1.010 (3-ketocarbofuran) and 0.095–0.135 (3-hydroxycarbofuran) in soil sampled from a poisoning site. These compounds were confirmed by GC-MS. The results showed that HPLC combined with GC-MS is suitable for forensic analysis of carbofuran residues in bird tissue samples and that forensic investigation should include its two toxic metabolites, 3-hydroxycarbofuran and 3-ketocarbofuran.


Forensic analysis Carbofuran metabolites Furadan poisoning Vultures Kenya 



This study was kindly funded by the Peregrine Fund, through the Africa Project. The authors also wish to thank Simon Thomsett of Athi River conservancy, Ian Craig, Chege, Joanne, Richard and all staff of Lewa wildlife conservancy, Kuki Gallman and Philip Ochieng of Gallman Memorial wildlife conservancy, Mbirikani and Kilimanjaro ranches, Darcy Ogada and all staff of the National Museum of Kenya, technical staff of Chemistry Department, Maseno University, Pierre Mineau and Ngaio Richard of Canadian Wildlife Service for the references. We also thank the German Academic Exchange Service (DAAD) for a visiting fellowship to J. O. Lalah at Bayreuth University, Germany, which enabled the preparation of the manuscript.


  1. Allen GT, Veach JK, Stroud RK, Vendel CG (1996) Winter poisoning of coyots and raptors with Furadan-laced carcass baits. J Wildl Dis 32:385–389Google Scholar
  2. Argauer RJ, Eller KI, Ibrahim MA, Brown RT (1995) Determination of propoxur and other carbamates in meat using HPLC fluorescence and gas chromatography/ion trap mass spectrometry after supercritical fluid extraction. J Agric Food Chem 43:2774–2778CrossRefGoogle Scholar
  3. Bishop CA, Ng P, Mineau P, Quinn JS, Strugger J (2000a) Effects of pesticide spraying on chick growth, behaviour, and parental care in tree swallows (Tachycineta bicolour) nesting in an apple orchard in Ontario, Canada. Environ Toxicol Chem 19:2286–2297Google Scholar
  4. Bishop CA, Collins B, Mineau P, Burgess NM, Read WF, Risley C (2000b) Reproduction of cavity-nesting birds in pesticide-sprayed apple orchards in southern Ontario, Canada, 1988–1994. Environ Toxicol Chem 19:588–599Google Scholar
  5. Brown P (1997) Identification of pesticide poisoning in wildlife. J Chromatogr 541:463–478Google Scholar
  6. Crocker DR (2005) Estimating the exposure of birds and mammals to pesticides in longer-term risk assessments. Ecotoxicol 14:833–851CrossRefGoogle Scholar
  7. Ecobischon DJ (1993) Toxic effects of pesticides. In: Amdur MO, Doull J, Klaasen CD (eds) Casarett and Doull’s toxicology: the basic sciences of poisons, 4th edn. Macmillan Press, New York, pp 565–589Google Scholar
  8. Eisler R (1985) Carbofuran hazards to fish, wildlife, and invertebrates: a synoptic review. U.S. Fish Wildlife Service Biology Reproduction 85(1.3). 36 ppGoogle Scholar
  9. Elliott JE, Langlier KM, Mineau P, Wilson LK (1996) Poisoning of bald eagles and red-tailed hawks by carbofuran and fensulfothion in the Fraser Delta of British Columbia, Canada. J Wildl Dis 32:486–491Google Scholar
  10. Frank RP, Mineau P, Braun IK, Barker SW, Trudeau S (1991) Deaths of Canada geese following spraying of turf with diazinon. Bull Environ Contam Toxicol 46:852–858CrossRefGoogle Scholar
  11. Hassall K (1990) The biochemistry and uses of pesticides, 2nd edn. Macmillan Press Ltd, Hong Kong, pp 140–143Google Scholar
  12. Hayes W (2001) Principles and methods of toxicology, 4th edn. Taylor and Francis, London, pp 587–591Google Scholar
  13. Hayes WJ Jr (1982) Metabolism of pesticides. In: Pesticides studied in man. Williams and Wilkins, BaltimoreGoogle Scholar
  14. Hill EF (1989) Brain divergent effects of post-mortem ambient temperature on organophosphorus and carbamate-inhibited brain cholinesterase activity in birds. Pestic Biochem Physiol 33:264–275CrossRefGoogle Scholar
  15. Hill EF, Fleming WJ (1982) Anticholinesterase poisoning in birds. Field monitoring and diagnosis of acute poisoning. Environ Toxicol Chem 1:27–38CrossRefGoogle Scholar
  16. Hodgson E, Roe RM, Motoyama N (1991) Pesticides and the future: toxicological studies of risks and benefits. Rev Pestic Toxicol 1:3–12Google Scholar
  17. Hopkins AW, Scholz LN (2006) Ecotoxicology of anticholinesterase pesticides: data gaps and research challenges. Environ Toxicol Chem 25(5):1185–1186CrossRefGoogle Scholar
  18. Kawamoto T, Makthata N (2003) Development of a simultaneous analysis method for carbofuran and its three derivative pesticides in water by GC/MS with temperature programmable inlet on-column injection. Analyt Sci 19:1605–1609CrossRefGoogle Scholar
  19. KWS (2009) The Kenya Wildlife Service report. In: Furadan Taskforce Proceedings. Furadan Taskforce Meeting, July 2009, Wildlife Direct, Nairobi, KenyaGoogle Scholar
  20. Lalah JO, Wandiga SO (1996) Distribution and dissipation of carbofuran in a paddy field in Kano plains of Kenya. Bull Environ Contam Toxicol 56:584–593CrossRefGoogle Scholar
  21. Lalah JO, Kaigwara PN, Getenga Z, Mghenyi JM, Wandiga SO (2001) The major environmental factors that influence rapid disappearance of pesticides from tropical soils in Kenya. Toxicol Environ Chem 81:161–197CrossRefGoogle Scholar
  22. Martin PA, Forsyth DJ (1996) Effects of exposure to vegetation sprayed with dimethoate or chlorpyrifos on mallard ducklings (Anas platyrynchos). Ecotoxicol 7:81–87CrossRefGoogle Scholar
  23. McRae IC (1989) Microbial metabolism of pesticides and structurally related compounds. Rev Environ Contam Toxicol 109:1–34Google Scholar
  24. Mineau P (1993) The hazard of carbofuran to birds and other vertebrate wildlife. Canadian Wildlife Service Technical Report No. 177. Headquarters, Canadian Wildlife Service, Environment Canada, Ottawa, Canada, 96Google Scholar
  25. Mineau P (2001) Pesticide acute toxicity: reference values for birds. Rev Environ Contam Toxicol 13:71–80Google Scholar
  26. Mineau P (2002) Estimating the probability of bird mortality from pesticide sprays on the basis of the field study record. Environ Toxicol Chem 21(7):1497–1506CrossRefGoogle Scholar
  27. Mineau P (2003) Avian species. In: Plimmer JR, Gammon DW, Ragsdale NN (eds) Encyclopedia of agrochemicals. Wiley, New York, pp 1–27Google Scholar
  28. Mineau P, Collins M (1988) Avian mortality in agro-ecosystems 2. Methods of detection. British Crop Protection Council Report, pp 13–27Google Scholar
  29. Mineau P, Tucker KR (2002a) Improving detection of pesticide poisoning in birds. J Wildl Rehabil 25(2):4–13Google Scholar
  30. Mineau P, Tucker KR (2002b) Improving detection of pesticide poisoning in birds, part II. J Wildl Rehabil 25(3):4–12Google Scholar
  31. Mineau P, Fletcher MR, Glaser LC, Thomas NJ, Brassard C, Wilson LK, Elliot JE, Lyon L, Henny CJ, Bollinger P, Porter SL (1999) Poisoning of raptors with organophosphorous and carbamate pesticides with emphasis on Canada, US and U.K. J Raptor Res 33(1):1–37Google Scholar
  32. Mineau P, Downes CM, Kirk DA, Byane E, Csizy M (2005) Patterns of bird species abundance in relation to granular insecticide use in the Canadian prairies. Ecoscience 12:267–278CrossRefGoogle Scholar
  33. Ogada DL, Keesing F (2009) Rapid decline of vultures over a three-year period in Laikipia, Central Kenya. J Raptor Res (submitted)Google Scholar
  34. Otieno PO (2009) Monitoring carbofuran residues in Laikipia and Isiolo districts in Kenya for ecological risk assessment. MSc thesis, Department of Chemistry, Maseno University, Maseno, KenyaGoogle Scholar
  35. PCPB (1992) Pest control products board of Kenya annual report 1992. Ministry of Agriculture, NairobiGoogle Scholar
  36. Pogacnik L, Franko M (1999) Determination of organophosphate and carbamate pesticides in spiked samples of tap water and fruit juices by a senor with photothermal detection. Biosens Bioelectron 14:569–578CrossRefGoogle Scholar
  37. Prakash V (2004) Diclofenac poisoning as cause of vulture population decline across the Indian subcontinent. J Appl Ecol 41:793–823CrossRefGoogle Scholar
  38. Raminderjit SB, Ranjinder LK, Ranjit SD (2000) Estimating of residues of carbofuran and its metabolites in sugarcane and soil by derivation with 1-flouro-2,4-dinitrobenzene and GC with NPD. J AOAC Int 83:569–573Google Scholar
  39. Richards NL, Mineau P, Bird DM (2005) A risk assessment approach to DDE exposure based on the case of the Eastern Screech-owl (Megascops asio) in apple orchards of southern Quebec, Canada. Arch Environ Contam Toxicol 49:403–409CrossRefGoogle Scholar
  40. Sanchez-Fortun S, Barahona MV (2001) The use of carbamates, atropine, and 2-PAM in the protection of Artemia salina against poisoning by carbophenothion. Environ Toxicol Chem 20:2008–2013Google Scholar
  41. Slotta-Bachmayr L, Bogel R, Camina CA (2004) The Eurasian Griffon vulture in Europe and Mediterranean: status and action planGoogle Scholar
  42. Stroud RK, Adrian WJ (1996) Forensic investigational techniques for wildlife law enforcement investigations, 2nd edn. Iowa state university press, USA, pp 3–18Google Scholar
  43. Suett DL (1986) Effects of formation of dimethylamine and diethylamine in soil treated with pesticides. Crop Protect 5:16–167Google Scholar
  44. Takino M, Yamaguchi K, Nakahara T (2004) Determination of carbamate pesticide residues in vegetables and fruits by liquid chromatography-atmospheric pressure photoionization-mass spectrometry and atmospheric pressure chemical ionization-mass spectrometry. J Agric Food Chem 52:727–735CrossRefGoogle Scholar
  45. Trotter DM, Kent RA, Wong MP (1991) Aquatic fate and effects of carbofuran. Crit Rev Environ Contam 21(2):137–176CrossRefGoogle Scholar
  46. Trudeau S, Sans Cartier (2000) Biochemical methods to determine cholinesterase activity in wildlife exposed to pesticides. National Wildlife Research Centre, Canadian Wildlife Service, Environment Canada. Technical Series No. 338Google Scholar
  47. USEPA (2002) Drinking water standards and health advisories. Report EPA-822-R-02-038, Washington DC, USAGoogle Scholar
  48. VUE (2005) Vulture Unit Education: De wild cheetah and wildlife (a report), South AfricaGoogle Scholar
  49. Vyas NB (1999) Factors influencing the estimation of pesticide elated wildlife mortality. J Toxicol Ind Health 15:186–191CrossRefGoogle Scholar
  50. Vyas NB, Spann JW, Albers E, Patterson D (2003) Pesticide-laced predator baits: considerations for prosecution and sentencing. Environ Lawyer 9:589–608Google Scholar
  51. Vyas NB, Spann JW, Hulse CS, Bauer W, Olson S (2005) From the field: carbofuran detected on weathered raptor carcass feet. Wildl Soc Bull 33:1178–1182CrossRefGoogle Scholar
  52. Yang SS, Goldsmith AI, Smetena I (1996) Recent advances in the residue analysis of N-methylcarbamate pesticides. J Chromatogr A 754:3–16CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2010

Authors and Affiliations

  • Peter O. Otieno
    • 1
  • Joseph O. Lalah
    • 1
    Email author
  • Munir Virani
    • 2
    • 3
  • Isaac O. Jondiko
    • 1
  • Karl-Werner Schramm
    • 4
  1. 1.Department of ChemistryMaseno UniversityMasenoKenya
  2. 2.The Peregrine FundBoiseUSA
  3. 3.Ornithology Section, Department of ZoologyNational Museum of KenyaNairobiKenya
  4. 4.Helmholtz Zentrum, German National Research Centre for Environmental Health, Institute of Ecological ChemistryNeuherbergGermany

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