Skip to main content
SpringerLink
Log in

B-esterase activities and blood cell morphology in the frog Leptodactylus chaquensis (Amphibia: Leptodactylidae) on rice agroecosystems from Santa Fe Province (Argentina)

  • Published:
Ecotoxicology Aims and scope Submit manuscript

Abstract

Activity of B-esterases (BChE: butyrylcholinesterase and CbE: carboxylesterase using two model substrates: α-naphthyl acetate and 4-nitrophenyl valerate) in a native frog, Leptodactylus chaquensis from rice fields (RF1: methamidophos and RF2: cypermethrin and endosulfan sprayed by aircraft) and non-contaminated area (pristine forest) was measured. The ability of pyridine-2-aldoxime methochloride (2-PAM) to reactivate BChE levels was also explored. In addition, changes in blood cell morphology and parasite infection were determined. Mean values of plasma BChE activities were lower in samples from the two rice fields than in those from the reference site. CbE (4-nitrophenyl valerate) levels varied in the three sites studied, being highest in RF1. Frog plasma from RF1 showed positive reactivation of BChE activity after incubation with 2-PAM. Blood parameters of frogs from RF2 revealed morphological alterations (anisochromasia and immature erythrocytes frequency). Moreover, a major infection of protozoan Trypanosoma sp. in individuals from the two rice fields was detected. We suggest that integrated use of several biomarkers (BChE and CBEs, chemical reactivation of plasma with 2-PAM, and blood cell parameters) may be a promising procedure for use in biomonitoring programmes to diagnose pesticide exposure of wild populations of this frog and other native anuran species in Argentina.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Allender MC, Fry MM (2008) Amphibian hematology. Vet Clin N Am 11:463–480. doi:10.1016/j.cvex.2008.03.006

    Google Scholar 

  • Alvisio A (1998) Arroz. Modelos zonales de producción en el movimiento CREA: Región Litoral Norte. Cuad Act Téc 61:141–145

    Google Scholar 

  • Aranguren JD (1998) Evolución del cultivo del arroz en el movimiento CREA. Cuad Act Téc 61:6–8

    Google Scholar 

  • Arshad N, Yunus S, Adan GE (2001) Endosulfan induced changes in hematological and some immunological parameters in mice. Punjab Univ J Zool 16:147–154

    CAS  Google Scholar 

  • Attademo AM, Peltzer PM, Lajmanovich RC, Cabagna M, Fiorenza G (2007) Plasma B-esterases and glutathione S-transferase activities in the toad Chaunus schneideri (Amphibia, Anura) inhabiting rice agroecosystems of Argentina. Ecotoxicology 16:533–539. doi:10.1007/s10646-007-0154-0

    Article  CAS  Google Scholar 

  • 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, pp 101–136

    Google Scholar 

  • Bain D, Buttemer WA, Astheimer L, Fildes K, Hooper MJ (2004) Effects of sublethal fenitrothion ingestion on cholinesterase inhibition, standard metabolism, thermal preference, and prey capture ability in the Australian central bearded dragon (Pogona vitticeps: Agamidae). Environ Toxicol Chem 23:109–116. doi:10.1897/02-555

    Article  CAS  Google Scholar 

  • Bambaradeniya CNB, Edirisinghe JP, De Silva DN, Gunatilleke CVS, Ranawana KB, Wijekoon S (2004) Biodiversity associated with an irrigated rice agroecosystem in Sri Lanka. Biodivers Conserv 13:1715–1753. doi:0.1023/B:BIOC.0000029331.92656.de

    Article  Google Scholar 

  • Barni S, Boncompagni E, Grosso A, Bertone V, Freitas I, Fasola M, Fenoglio C (2007) Evaluation of Rana snk esculenta blood cell response to chemical stressors in the environment during the larval and adult phases. Aquat Toxicol 81:45–54. doi:10.1016/j.aquatox.2006.10.012

    Article  CAS  Google Scholar 

  • Begenesic F (1998) Arróz. Panorama Agrícola. Informe de la Secretaría de Agricultura, Ganadería, Pesca y Alimentación 2:1–47

  • Bunyan PJ, Jennings DM (1968) Organophosphorus poisoning; some properties of avian esterase. J Agric Food Chem 16:326–331

    Article  CAS  Google Scholar 

  • Burkart R, Barbaro NO, Sánchez RO, Gómez DA (1999) Eco-regiones de la Argentina. PRODIA, Buenos Aires

    Google Scholar 

  • Busk M, Jensen FB, Wang T (2000) Effects of feeding on metabolism, gas transport and acid base balance in the bullfrog Rana Catesbiana. Am J Physiol Regul Integr Comp Physiol 278:85–95

    Google Scholar 

  • Cabagna M, Lajmanovich RC, Stringhini G, Peltzer PM (2005) Hematological studies in the common toad (Bufo arenarum) in agrosystems of Argentina. Appl Herpetol 2:373–380. doi:10.1163/157075405774483085

    Article  Google Scholar 

  • Carr RL, Chambers JE (1991) Acute effects of the organophosphate paraoxon on schedule-controlled behaviour and esterase activity in rats: dose–response relationships. Pharmacol Biochem Behav 40:929–936. doi:10.1016/0091-3057(91)90108-E

    Article  CAS  Google Scholar 

  • CASAFE (2005) Cámara de sanidad agropecuaria y fertilizantes de la República Argentina. Guía de Productos Fitosanitarios para la República Argentina, Buenos Aires

    Google Scholar 

  • Chambers JE, Levi PE (1992) Organophosphates: chemistry, fate and effects. Academic Press, San Diego

    Google Scholar 

  • Chuiko GM, Podgornaya VA, Zhelnin YY (2003) Acetylcholinesterase and butyrylcholinesterase activities in brain and plasma of freshwater teleosts: cross-species and cross-family. Comp Biochem Physiol 135:55–61. doi:10.1016/S1096-4959(03)00048-4

    CAS  Google Scholar 

  • Cordi B, Fossi C, Depledge MH (1997) Temporal biomarker responses in wild passerine birds exposed to pesticide spray drift. Environ Toxicol Chem 16:2118–2124. doi:10.1897/1551-5028(1997)016<2118:TBRIWP>2.3.CO;2

    Article  CAS  Google Scholar 

  • Dacie JV, Lewis SM (1984) Practical hematology. Churchill Livingstone, New York

    Google Scholar 

  • 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 16:1588–1601. doi:10.1046/j.1523-1739.2002.01030.x

    Article  Google Scholar 

  • Davis AK, Maney DL, Maerz JC (2008) The use of leukocyte profiles to measure stress in vertebrates: a review for ecologists. Funct Ecol 22:760–772. doi:10.1111/j.1365-2435.2008.01467.x

    Article  Google Scholar 

  • DeJong RJ, Muzzall PM (2000) Hematozoa of waterfowl from the Kellogg Biological Station area in southwestern Michigan. J Wildl Dis 36:767–773

    Google Scholar 

  • Dettbarn WD, Yang ZP, Milatovic D (1999) Different role of carboxylesterases in toxicity and tolerance to paraoxon and DFP. Chem Biol Interact 120:445–454. doi:10.1016/S0009-2797(99)00057-5

    Article  Google Scholar 

  • Duré MI, Kehr AI, Schaefer EF, Marangoni F (2008) Diversity of amphibians in rice fields from north-eastern Argentina. Interciencia 33:523–527

    Google Scholar 

  • Ellman GL, Courtney KD, Andreas V Jr, Featherstone RM (1961) A new and rapid calorimetric determination of cholinesterase activity. Biochem Pharmacol 7:88–95. doi:10.1016/0006-2952(61)90145-9

    Article  CAS  Google Scholar 

  • Gomori G (1953) Human esterases. J Lab Clin Med 142:445–453

    Google Scholar 

  • Grue CE, Gilbert PL, Seeley ME (1997) Neurophysiological and behavioral changes in nontarget wildlife exposed to organophosphate and carbamate pesticides: thermoregulation, food consumption, and reproduction. Am Zool 37:369–388

    CAS  Google Scholar 

  • Guilherme S, Válega M, Pereira ME, Santos MA, Pacheco M (2008) Erythrocytic nuclear abnormalities in wild and caged fish (Liza aurata) along an environmental mercury contamination gradient. Ecotoxicol Environ Saf 70:411–421. doi:10.1016/j.ecoenv.2007.08.016

    Article  CAS  Google Scholar 

  • Hii YS, Lee MY, Chuah TS (2007) Acute toxicity of organochlorine insecticide endosulfan and its effect on behaviour and some hematological parameters of Asian swamp eel (Monopterus albus, Zuiew). Pestic Biochem Physiol 89:46–53. doi:10.1016/j.pestbp.2007.02.009

    Article  CAS  Google Scholar 

  • Iko WM, Archuleta AS, Knopf F (2003) Plasma cholinesterase levels of mountain plovers (Charadrius montanus) wintering in central California, USA. Environ Toxicol Chem 22:119–125. doi:10.1897/1551-5028(2003)022<0119:PCLOMP>2.0.CO;2

    CAS  Google Scholar 

  • Jergentz S, Mugni H, Bonetto C, Schulz YR (2005) Assessment of insecticide contamination in runoff and stream water of small agricultural streams in the main soybean area of Argentina. Chemosphere 61:817–826. doi:10.1016/j.chemosphere.2005.04.036

    Article  CAS  Google Scholar 

  • Johnson PT, Chase JM (2004) Parasites in the food web: linking amphibian malformations and aquatic eutrophication. Ecol Lett 7:521–526. doi:10.1111/j.1461-0248.2004.00610.x

    Article  Google Scholar 

  • Kaplan HM, Glaczenski SS (1965) Hematological effects of organophosphate insecticides in the frog (Rana pipiens). Life Sci 4:1213–1219. doi:10.1016/0024-3205(65)90335-8

    Article  CAS  Google Scholar 

  • Khan MZ (2005) Effects of agro pesticides cypermethrin and malathion on cholinesterase activity in liver and kidney of Calotes versicolor Daudin (Agamidae: Reptilia). Turk J Zool 29:77–81

    CAS  Google Scholar 

  • Khan MZ, Maria Z, Fatima F (2003) Effect of Lambda cyhalothrin (pyrethroid) and Monocrotophos (organophosphate) on cholinesterase activity in liver, kidney and brain of Rana cyanophlystis. Korean J Biol Sci 7:165–168

    CAS  Google Scholar 

  • Kornienko IA, Maslov SP, Shilov IA (1965) Some general principles of adaptation in biological systems. Zh Obshch Biol 1:121–126

    Google Scholar 

  • Laguerre C, Sánchez-Hernández JC, Kohler HR, Triebskorn R, Capowiez Y, Rault M, Mazzia C (2009) B-type esterases in the snail Xeropicta derbentina: an enzymological analysis to evaluate their use as biomarkers of pesticide exposure. Environ Pollut 157:199–207. doi:10.1016/j.envpol.2008.07.003

    Article  CAS  Google Scholar 

  • 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 72:586–591. doi:10.1007/s00128-004-0284-5

    Article  CAS  Google Scholar 

  • Lajmanovich RC, Sánchez-Hernández JC, Peltzer PM, Attademo AM, Fiorenza GS, Cabagna MC, Bassó A (2008) Levels of plasma B-esterases and glutathione-S-transferase activities in three South American toad species. Toxicol Environ Chem 90:1145–1161. doi:10.1080/02772240801923107

    Article  CAS  Google Scholar 

  • Mann RM, Hyne RV, Choung CB, Wilson SP (2009) Amphibians and agricultural chemicals: review of the risks in a complex environment. Environ Pollut 157:2903–2927. doi:10.1016/j.envpol.2009.05.015

    Article  CAS  Google Scholar 

  • Marcogliese DJ, King KC, Salo HM, Fournier M, Brousseau P, Spear P, Champoux L, McLaughlin JD, Boily M (2009) Combined effects of agricultural activity and parasites on biomarkers in the bullfrog, Rana catasbeiana. Aquat Toxicol 91:126–134. doi:10.1016/j.aquatox.2008.10.001

    Article  CAS  Google Scholar 

  • Marques SM, Antunes SC, Pissarra H, Pereira ML, Gonçalves F, Pereira R (2009) Histopathological changes and erythrocytic nuclear abnormalities in Iberian green frogs (Rana perezi, Seoane) from a uranium mine pond. Aquat Toxicol 91:187–195. doi:10.1016/j.aquatox.2008.04.010

    Article  CAS  Google Scholar 

  • 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 24:1721–1730. doi:10.1007/s00128-004-0480-3

    Article  CAS  Google Scholar 

  • Maxwell DM, Brecht KM (2001) Carboxylesterase: specific and spontaneous reactivation of an endogenous scavenger for organophosphorus compounds. J Appl Toxicol 21:103–107. doi:10.1002/jat.833

    Article  Google Scholar 

  • McCarthy J, Shugart L (1990) Biological markers of environmental contamination. In: McCarthyand J, Shugart L (eds) Biomarkers of environmental contamination. Lewis Publishers, Boca Raton, pp 3–14

    Google Scholar 

  • Mor F, Ozmen O (2010) Endosulfan-induced neurotoxicity and serum acetylcholinesterase inhibition in rabbits: the protective effect of Vit C. Pestic Biochem Physiol 96:108–112. doi:10.1016/j.pestbp.2009.10.004

    Article  CAS  Google Scholar 

  • Olmos S (2006) Prácticas para el manejo de arroz Cátedra de Cultivos II. Facultad de Ciencias Agrarias, UNNE, Corrientes, Argentina

    Google Scholar 

  • Parsons KC, Matz AC, Hooper MJ, Pokras MA (2000) Monitoring wading bird exposure to agricultural chemicals using serum cholinesterase activity. Environ Toxicol Chem 19:1317–1323. doi:10.1897/1551-5028(2000)019<1317:MWBETA>2.3.CO;2

    Article  CAS  Google Scholar 

  • Peltzer PM, Lajmanovich RC, Sánchez-Hernández JC, Cabagna MC, Attademo AM, Bassó A (2008) Assessment of agricultural pond eutrophication on survival and health status of the Scinax nasicus tadpoles. Environ Ecotoxicol Saf 70:185–197. doi:10.1016/j.ecoenv.2007.06.005

    Article  CAS  Google Scholar 

  • Pistl J, Kovalkovicova N, Kacmar P, Kosava I, Mikula I, Sutiakova I (2001) Effect of endosulfan on peripheral sheep leukocytes in vitro. Vet Hum Toxicol 43:78–82

    CAS  Google Scholar 

  • Pough F (1980) The advantages of ectothermy for tetrapods. Am Nat 115:92–112

    Article  Google Scholar 

  • Ruiz A (1998) Caracterización del área arrocera de la Región CREA Litoral Norte. CREA. Cuad Act Téc 61:10–13

    Google Scholar 

  • Sánchez JC, Fossi MC, Focardi S (1997) Serum B esterases as an nondestructive biomarker for monitoring the exposure of reptiles to organophosphorus insecticides. Ecotoxicol Environ Saf 38:45–52. doi:10.1006/eesa.1997.1560

    Article  Google Scholar 

  • Sánchez-Hernández JC (2003) Evaluating reptile exposure to cholinesterase-inhibiting agrochemicals by serum butyrylcholinesterase activity. Environ Toxicol Chem 22:296–301

    Article  Google Scholar 

  • Sánchez-Hernández JC (2006) Ecotoxicological perspectives of B-esterases in the assessment of pesticide contamination. In: Plattenberg RH (ed) Environmental pollution: new research. Nova Science Publishers, New York

    Google Scholar 

  • Sánchez-Hernández JC, Moreno-Sánchez B (2002) Lizard cholinesterases as biomarkers of pesticide exposure: enzymological characterization. Environ Toxicol Chem 21:2319–2325. doi:10.1897/1551-5028(2002)021<2319:LCABOP>2.0.CO;2

    Article  Google Scholar 

  • 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 132:479–488. doi:10.1016/j.envpol.2004.05.008

    Article  Google Scholar 

  • Silva C, Boia C, Valente J, Borrego C (2005) Pesticides in Esteros del Iberá (AR): evaluation of impacts and proposal of guidelines for water quality protection. Ecol Model 186:85–97. doi:10.1016/j.ecolmodel.2005.01.018

    Article  CAS  Google Scholar 

  • Sogorb MA, Vilanova E (2002) Enzymes involved in the detoxification of organophosphorus, carbamatos and pyrethroid insecticides through hydrolysis. Toxicol Lett 128:215–228. doi:10.1016/S0378-4274(01)00543-4

    Article  CAS  Google Scholar 

  • Soler-Rodríguez F, Miguez-Santiyan MP, Reja-Sánchez A, Roncero-Cordero V, Garcia-Cambero JP (1998) Recovery of brain acetylcholinesterase and plasma cholinesterase activities in quail (Coturnix coturnix) after chlorpyriphos administration and effect of pralidoxime treatment. Environ Toxicol Chem 17:1835–1839. doi:10.1897/1551-5028(1998)017<1835:ROBAAP>2.3.CO;2

    Google Scholar 

  • Sparling DW, Fellers GM, McConnell L (2001) Pesticides and amphibian population declines in California USA. Environ Toxicol Chem 20:1591–1595. doi:10.1897/1551-5028(2001)020<1591:PAAPDI>2.0.CO;2

    Article  CAS  Google Scholar 

  • Stansley W, Roscoe DE (1996) The uptake and effects of lead in small mammals and frogs at a trap and skeet range. Arch Environ Contam Toxicol 30:220–226. doi:10.1007/BF00215801

    Article  CAS  Google Scholar 

  • Thompson HM, Walker CH (1994) Blood esterases as indicators of exposure to organophosphorus and carbamate insecticides. In: Fossi MC, Leonzio C, Chelsea MI (eds) Non-destructive biomarkers in vertebrates. Lewis Publishers, Boca Raton, pp 37–62

    Google Scholar 

  • Tyler MJ (1999) Frogs and toads as experimental animals. ANZCCAR News 12:1–4

    Google Scholar 

  • Udroiu I (2006) The micronucleus test in piscine erythrocytes. Aquat Toxicol 79:201–204. doi:10.1016/j.aquatox.2006.06.013

    Article  CAS  Google Scholar 

  • Varela ME, Sellarés ME (1938) Variations annuelles du sang du crepaud Bufo arenarum Hensel. C R Soc Biol 129:1248–1249

    Google Scholar 

  • 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 20:1503–1504. doi:10.1111/j.1471-4159.1973.tb00267.x

    Article  CAS  Google Scholar 

  • Walker CH (1998) The use of biomarkers to measure the interactive effects of chemicals. Ecotoxicol Environ Saf 40:65–70. doi:10.1006/eesa.1998.1643

    Article  CAS  Google Scholar 

  • 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 11:2699–2708. doi:10.1897/03-544

    Article  Google Scholar 

  • Wheelock CE, Phillips BM, Anderson BS, Miller JL, Miller MJ, Hammock BD (2008) Applications of carboxylesterase activity in environmental monitoring and toxicity identification evaluations (TIEs). Rev Environ Contam Toxicol 195:117–178. doi:10.1007/978-0-387-77030-7_5

    Article  CAS  Google Scholar 

Download references

Acknowledgments

We wish to thank Mateo R. and Chuiko G. for critical comments and valuable suggestions that improved the manuscript. We thank Elberg G. for help during sample collection and farmers for permission to work in their rice fields. This work was supported by PICT-SECYT No. 1148 (Director: Dr. Rafael C. Lajmanovich).

Author information

Authors and Affiliations

  1. Laboratory of Ecotoxicology, Faculty of Biochemistry and Biological Sciences (ESS-FBCB-UNL), Pje. El Pozo S/N., 3000, Santa Fe, Argentina

    Andrés M. Attademo, Mariana Cabagna-Zenklusen, Rafael C. Lajmanovich, Paola M. Peltzer, Celina Junges & Agustín Bassó

  2. National Council for Scientific and Technical Research (CONICET), ESS-FBCB-UNL, Santa Fe, Argentina

    Andrés M. Attademo, Rafael C. Lajmanovich, Paola M. Peltzer & Celina Junges

Authors
  1. Andrés M. Attademo
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Mariana Cabagna-Zenklusen
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Rafael C. Lajmanovich
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Paola M. Peltzer
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Celina Junges
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Agustín Bassó
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Andrés M. Attademo.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Attademo, A.M., Cabagna-Zenklusen, M., Lajmanovich, R.C. et al. B-esterase activities and blood cell morphology in the frog Leptodactylus chaquensis (Amphibia: Leptodactylidae) on rice agroecosystems from Santa Fe Province (Argentina). Ecotoxicology 20, 274–282 (2011). https://doi.org/10.1007/s10646-010-0579-8

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10646-010-0579-8

Keywords

Search

Navigation