, Volume 16, Issue 8, pp 533–539 | Cite as

Plasma B-esterase and glutathione S-transferase activity in the toad Chaunus schneideri (Amphibia, Anura) inhabiting rice agroecosystems of Argentina

  • Andrés Maximiliano AttademoEmail author
  • Paola M. Peltzer
  • Rafael C. Lajmanovich
  • Mariana Cabagna
  • Gabriela Fiorenza


B-esterase (BChE: butyrylcholinesterase and CbE: carboxylesterase) and glutathione S-transferase (GST) activity were measured in the plasma of Chaunus schneideri collected in rice fields and surrounding environments and in a reference pristine forest. The chemical criterion based on in-vitro reactivation of BChE activity using pyridine-2-aldoxime methochloride (2-PAM) was also determined. Mean values of plasma BchE, CbE, and GST activity for samples from agricultural areas were different from those for samples from pristine forest. Plasma samples from the two agricultural areas showed positive reactivation of BChE activity after incubation with 2-PAM. Based on our experimental evidence we suggest B-esterases and gluthatione S-transferases can be used in field monitoring as biomarkers of exposure of wildlife to pesticides, because the analysis in non-destructive and is sensitive to anti-ChE agrochemicals. Chemical reactivation of BChE is also a complementary method for assessing the effects of pesticides on toads inhabiting rice fields. Further studies are urgently needed to investigate adverse effects of massive exposure to pesticides experienced by native populations of anurans.


B-esterases Chaunus schneideri Gutathione S-transferase Pesticide Rice fields 



We wish to thank Donald Sparling, S. Pflugmacher, and Juan C. Sánchez-Hernandez for helpful comments and for checking the language. We thank farmers for permission to work in their fields. This work was supported in part by grants SEED GRANT DAPFT-2005 (Director: Dra. Paola M. Peltzer) and PIP-CONICET no. 5618−2006 (Director: Dr Rafael C. Lajmanovich).


  1. Angermann JE, Fellers GM, Matsumura F (2002) Polychlorinated biphenyls and toxaphene in Pacific tree frog tadpoles (Hyla regilla) from the California Sierra Nevada, USA. Environ Toxicol Chem 21(10):2209–2215CrossRefGoogle Scholar
  2. Bagenal TB, Tesch FW (1978) Methods for assessment of a fish production in fresh 376 waters. In: Bagenal TB (ed) Age and growth, vol 377. Blackwell Scientific Publications, Oxford, UK, pp 101–136Google Scholar
  3. Bambaradeniya CNB, Edirisinghe JP, De Silva DN, Gunatilleke CVS, Ranawana KB, Wijekoon S (2004) Biodiversity associated with an irrigated rice agroecosystem in Sri Lanka. Biodiv Conserv 13:1715–1753CrossRefGoogle Scholar
  4. Bertonatti C, Carguera J (2000) Situación ambiental Argentina 2000. Fundación vida silvestre Argentina, Buenos AiresGoogle Scholar
  5. Bridges CM, Boone MD (2003) The interactive effects of UV-B and insecticide exposure on tadpole survival, growth and development. Biol Conserv 113:49–522CrossRefGoogle Scholar
  6. Bucciarelli T, Sacchetta P, Pennelli A, Cornelio L, Romagnoli R, Melino S (1999) Characterisation of toad glutathione transferase. Biochim Biophys Acta 1431:189–198Google Scholar
  7. Bunyan PJ, Jennings DM (1968) Organophosphorus poisoning; some properties of avian esterase. J Agric Food Chem 16:326–331CrossRefGoogle Scholar
  8. Cabagna M, Lajmanovich RC, Stringhini G, Peltzer PM (2005) Hematological studies in the common toad (Bufo arenarum) in agrosystems of Argentina. Applied Herpetol 2:373–380CrossRefGoogle Scholar
  9. CASAFE (1999) Cámara de sanidad agropecuaria y fertilizantes de la República Argentina. Buenos Aires, Guía de Productos Fitosanitarios para la República Argentina, pp 635 Google Scholar
  10. Davidson C, Shaffer HB, Jennings MR (2002) Spatial tests of the pesticide drift, habitat destruction, UV-B, and climate-change hypotheses for California amphibian declines. Conserv Biol 16:1588–1601CrossRefGoogle Scholar
  11. Dettbarn WD, Yang ZP, Milatovic D (1999) Different role of carboxylesterases in toxicity and tolerance to paraoxon and DFP. Chem Biol Interact 120:445–454CrossRefGoogle Scholar
  12. Eaton DL, Bammler TK (1999) Concise review of the glutathione S-transferases and their significance to toxicology. Toxicol Sci 49:156–164CrossRefGoogle Scholar
  13. Elphick CS (2000) Functional equivalency between Rice fields and seminatural wetland habitats. Conserv Biol 14:181–191CrossRefGoogle Scholar
  14. Ellman GL, Courtney KD, Andres V, Featherstone RM (1961) A new and rapid colorimetric determination of acetylcholinesterase activity. Biochem Pharmacol 7:88–95CrossRefGoogle Scholar
  15. Fellers GM, McConnell LL, Pratt D, S Datta (2004) Pesticides in mountain yellow-legged frogs (Rana muscosa) from the Sierra Nevada Mountains of California, USA. Environ Toxicol Chem 23(9):2170–2177CrossRefGoogle Scholar
  16. Greulich K, Pflugmacher S (2004) Uptake and Effects on detoxication enzymes of Cypermethrin in embryos and tadpoles of amphibians. Arch Environ Contam Toxicol 47:489–495CrossRefGoogle Scholar
  17. Gruber SJ, Munn MD (1998) Organophosphate and carbamate insecticides in agricultural waters and cholinesterase (ChE) inhibition in common carp (Cyprinus carpio). Arch Environ Contam Toxicol 35:391–396CrossRefGoogle Scholar
  18. Gomori G (1953) Human esterases. J Lab Clin Med 42:445–453Google Scholar
  19. Fildes K, Astheimer LB, Store P, Buttemer W, Hooper MJ (2006) Cholinesterase response in native birds exposed to fenitrothion during locust control operations in eastern Australia. Environ Toxicol Chem 25:2964–2970CrossRefGoogle Scholar
  20. Fossi MC, Leonzio C (1994) Nondestructive biomarkers in vertebrates. Lewis Publishers, CRC Press, USA, pp 345Google Scholar
  21. Habig WH, Pabst MJ, Jakoby WB (1974) Glutathione S-transferases: The first enzymatic step in mercapturic acid formation. J Biol Chem 249:7130–7139Google Scholar
  22. Iko WM, Archuleta AS, Knopf F (2003) Plasma cholinesterase levels of mountain plovers (Charadrius montanus) wintering in Central California, USA. Environ Toxicol Chem 22:119–125CrossRefGoogle Scholar
  23. Kaaya A, Najimi S, Ribera D, Narbonne JF, Moukrim A (1999) Characterisation of glutathione-S-transferases (GST) activities in Perna perna and Mytilus galloprovincialis used as biomarkers of pollution the Agadir Marine Bay (South of Morocco) Bull Environ Contam Toxicol 62:623–629CrossRefGoogle Scholar
  24. Kiesecker JM, Blaustein AR, Belden LK (2001) Complex causes of amphibian population declines. Nature 410:681–684CrossRefGoogle Scholar
  25. Lagadic L, Caquet T, Ramade F (1994) The role of biomarkers in environmental assessment Invertebrate populations and communities. Ecotoxicology 3:193–208CrossRefGoogle Scholar
  26. Lajmanovich RC, Lorenzatti E, De la Sierra P, Marino F, Peltzer PM (2002) First registrations of organochlorine pesticides residues in amphibians of the Mesopotamic region, Argentina. Froglog 54:4–5Google Scholar
  27. Lajmanovich RC, Sánchez-Hernández JC, Stringhini G, Peltzer PM (2004) Levels of serum cholinesterase activity in the rococo toad (Bufo paracnemis) in agrosystems of Argentina. Bull Environ Contam Toxicol 72:548–591CrossRefGoogle Scholar
  28. Lajmanovich RC, Cabagna M, Peltzer PM, Stringhini GA, Attademo AM (2005a) Micronucleus induction in erythrocytes of the Hyla pulchella tadpoles (Amphibia: Hylidae) exposed to insecticide endosulfan. Mutat Res 587:67–72Google Scholar
  29. Lajmanovich R, De La Sierra P, Marino F, Peltzer P, Lenardón A, Lorenzatti E (2005b) Determinación de residuos de organoclorados en vertebrados silvestres del litoral fluvial de Argentina. In: FC Aceñolaza (ed) Temas de la biodiversidad del litoral fluvial Argentino II, INSUGEO, Miscelánea, Tucuman, Argentina, pp 255–262Google Scholar
  30. Maul JD, Farris JL (2004) Monitoring exposure of passerines to acephate, dicrotophos, and malathion using cholinesterase reactivation. Bull Environ Contam Toxicol 73:682–689CrossRefGoogle Scholar
  31. Maul JD, Farris JL (2005) Monitoring exposure of northern cardinals, Cardinalis cardinalis, to cholinesterase-inhibiting pesticides: enzyme activity, reactivations, and indicators of environmental stress. Environ Toxicol Chem 24:1721–1730CrossRefGoogle Scholar
  32. McCarthy J, Shugart L (1990) Biological markers of environmental contamination. In: McCarthyand J, Shugart L (eds) Biomarkers of environmental contamination. Lewis, Boca Raton, FL, pp 3–14Google Scholar
  33. McInnes P, Andersen DE, Hoff DJ, Hooper MJ, Kinkel LL (1996) Monitoring exposure of nestling songbirds to agricultural application of an organophosphorus insecticide using cholinesterase activity. Environ Toxicol Chem 15:544–552CrossRefGoogle Scholar
  34. Moses M (1989) Pesticide-related health problems and farmworkers. AAOHN J 37:115–130Google Scholar
  35. Ognjanović BI, Pavlović SZ, Maletić SD, Zikić RV, Stajn AS, Radojičić RM, Saičić ZS, Petrović VM (2003) Protective Influence of Vitamin E on antioxidant defense system in the blood of rats treated with cadmium. Physiol Res 52: 563–570Google Scholar
  36. Parsons K, Matz AC, Hooper MJ, Pokras MA (2000) Monitoring wading bird exposure to agricultural chemicals using serum cholinesterase activity. Environ Toxicol Chem 19:1317–1323CrossRefGoogle Scholar
  37. Plimmer JR (1991) Dissipation of pesticides in the environment. In: JL Schnoor (ed) Fate of pesticides and chemicals in the environment. Wiley, New York, pp 79–91Google Scholar
  38. Relyea RA (2006) The effects of pesticides, pH, and predatory stress on amphibians under mesocosm conditions. Ecotoxicology 15:503–511CrossRefGoogle Scholar
  39. Relyea RA, Schoeppner NM, Hoveman JT (2005) Pesticides and amphibians: the importance of community context. Ecol Applic 15:1125–1134CrossRefGoogle Scholar
  40. Sánchez-Hernández JC (2003) Evaluating reptile exposure to cholinesterase-inhibiting agrochemicals by serum butyrylcholinesterase activity. Environ Toxicol Chem 22:296–301CrossRefGoogle Scholar
  41. Sánchez-Hernández JC, Carbonell R, Henríquez-Pérez A, Montealegre M, Gómez L (2004) Inhibition of plasma butyrylcholinesterase activity in the lizard Gallotia galloti palmae by pesticides: a field study. Environ Pollut 132:479–488CrossRefGoogle Scholar
  42. Simcox NJ, Fenske RA, Wolz SA, Lee IC, Kalman DA (1995) Pesticides in household dust and soil: Exposure pathways for children of agricultural families. Environ Health Perspect 103:1126–1134CrossRefGoogle Scholar
  43. Sparling DW, Fellers GM, McConnell L (2001) Pesticides and amphibian population declines in California USA. Environ Toxicol Chem 20:1591–1595CrossRefGoogle Scholar
  44. Sogorb MA, Vilanova E (2002) Enzymes involved in the detoxification of organophosphorus, carbamatos and pyrethroid insecticides through hydrolysis. Toxicol Lett 128:215–228CrossRefGoogle Scholar
  45. Trimboli G, Vicino R, Peart M (2003) Análisis de la producción de Arroz en la provincia Centro Regional Santa Fe. Estación Experimental Agropecuaria Reconquista (INTA). Agencia de Extensión Rural San Javier. Información para Extensión No 77, pp 11Google Scholar
  46. Venturino A, Rosenbaum E, Caballero de Castro A, Anguiano OL, Gauna L, Fonovich de Schroeder T, Pechen de D’Angelo AM (2003) Biomarkers of effect in toads and frogs. Biomarkers 8:167–186CrossRefGoogle Scholar
  47. Vernadakis A, Routledge CO (1973) Effects of ether and Phenobarbital anaesthesia on the activities of brain acetylcholinesterase and butyrylcholinesterase in young adult rats. J Neurochem 20:1503–1504CrossRefGoogle Scholar
  48. Walker CH (1998) The use of biomarkers to measure the interactive effects of chemicals. Ecotoxicol Environ safety 40:65–70 CrossRefGoogle Scholar
  49. Wheelock CE, Miller JL, Miller MG, Shan G, Gee SJ, Hammock BD (2004) Development of toxicity identification evaluation (TIE) procedures for pyrethroid detection using esterase activity. Environ Toxicol Chem 11:2699–2708CrossRefGoogle Scholar
  50. Wilczek G, Majkus Z, Migula P, Bednarska K, Swierczek E (1997) Heavy metals and detoxifying enzymes in spiders from coal and metallurgic dumps near Ostrava (Czech Republic). Proceedings of the 16th European colloidal arachnology siedlce, pp 317–328Google Scholar

Copyright information

© Springer Science+Business Media, LLC 2007

Authors and Affiliations

  • Andrés Maximiliano Attademo
    • 1
    • 2
    Email author
  • Paola M. Peltzer
    • 1
    • 2
  • Rafael C. Lajmanovich
    • 1
    • 2
  • Mariana Cabagna
    • 2
  • Gabriela Fiorenza
    • 2
  1. 1.National Council for Scientific and Technical Research (CONICET)Santa FeArgentina
  2. 2.Faculty of Biochemistry and Biological SciencesESS-FBCB-UNL (3001)Santa FeArgentina

Personalised recommendations