Skip to main content
Log in

Cholinesterase activities and behavioral changes in Hypsiboas pulchellus (Anura: Hylidae) tadpoles exposed to glufosinate ammonium herbicide

  • Published:
Ecotoxicology Aims and scope Submit manuscript

Abstract

In this study, amphibian tadpoles of Hypsiboas pulchellus were exposed to herbicide Liberty®, which contains glufosinate ammonium (GLA), for 48 h to the following concentrations: 0 (control), 3.55, 4.74, 6.32, 8.43, 11.25, 15, 20, 26.6, and 35.5 mg GLA L−1. Acetylcholinesterase (AChE) and butyrylcholinesterase (BChE) activities, as well as swimming capabilities (swimming speed and mean distance) were measured in tadpoles whose concentrations displayed survival rates >85 %. Our results reveal that sublethal concentrations of GLA significantly inhibited both AChE and BChE activities in tadpoles with respect to the control, showing a concentration-dependent inhibitory effect. The highest inhibition percentages of AChE (50.86 %) and BChE (53.02 %) were registered in tadpoles exposed to 15 mg GLA L−1. At this concentration, a significant increase of the swimming speed and mean distance were found in exposed tadpoles with respect to the control, as well as a negative and significant correlation between swimming speed and BChE activity, thus suggesting that this enzyme inhibition is related to an increase in swimming speed. Therefore, exposure of tadpoles to GLA in the wild at concentrations similar to those tested here may have adverse consequences at population level because neurotransmission and swimming performance are essential for tadpole performance and survival.

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

Access this article

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

Similar content being viewed by others

References

  • Amiard-Triquet C (2009) Behavioral disturbances: the missing link between sub organismal and supra-organismal responses to stress? Prospects based on aquatic research. Hum Ecol Risk Assess 15:87–110. doi:10.1080/10807030802615543

    Article  CAS  Google Scholar 

  • Anonymous (2010) How to feed a hungry world. Nature 466:531–532. doi:10.1038/466531a

    Article  Google Scholar 

  • ASIH (2004) Guidelines for use of live amphibians and reptiles in field and laboratory research, Herpetological Animal Care and Use Committee (HACC) of the American Society of Ichthyologists and Herpetologists. ASIH, Washington DC

    Google Scholar 

  • Avila-Garcia WV, Sanchez-Olguin E, Hulting AG, Mallory-Smith C (2012) Target-site mutation associated with glufosinate resistance in Italian ryegrass (Lolium perenne L. ssp. multiflorum). Pest Manag Sci 68:1248–1254. doi:10.1002/ps.3286

    Article  CAS  Google Scholar 

  • Ballesteros ML, Durando PE, Nores ML, Bistoni MDLA, Wunderlin DA (2009) Endosulfan induces changes in spontaneous swimming activity and acetylcholinesterase activity of Jenynsia multidentata (Anablepidae, Cyprinodontiformes). Environ Pollut 157:1573–1580. doi:10.1016/j.envpol.2009.01.001

    Article  CAS  Google Scholar 

  • Barata C, Solayan A, Porte C (2004) Role of B-esterases in assessing toxicity of organophosphorus (chlorpyrifos, malathion) and carbamate (carbofuran) pesticides to Daphnia magna. Aquat Toxicol 66:125–139. doi:10.1016/j.aquatox.2003.07.004

    Article  CAS  Google Scholar 

  • Bonfanti P, Colombo A, Orsi F, Nizzetto I, Andrioletti M, Bacchetta R, Mantecca P, Fascio U, Vailati G, Vismara C (2004) Comparative teratogenicity of chlorpyrifos and malathion on Xenopus laevis development. Aquat Toxicol 70:189–200. doi:10.1016/j.aquatox.2004.09.007

    Article  CAS  Google Scholar 

  • Boone MD, Semlitsch RD (2002) Interactions of an insecticide with competition and pond drying in amphibian communities. Ecol Appl 12:307–316. doi:10.1111/j.1523-1739.2001.99475.x

    Article  Google Scholar 

  • Britson CA, Threlkeld ST (1998) Abundance, metamorphosis, developmental, and behavioral abnormalities in Hyla chrysoscelis tadpoles following exposure to three agrichemicals and methyl mercury in outdoor mesocosms. Bull Environ Contam Toxicol 61:154–161

    Article  CAS  Google Scholar 

  • Broomhall SD (2004) Egg temperature modifies predator avoidance and the effects of the insecticide endosulfan on tadpoles of an Australian frog. J Appl Ecol 41:105–113. doi:10.1111/j.1365-2664.2004.00883.x

    Article  Google Scholar 

  • Broomhall SD (2005) Measuring chemical impacts on amphibians: ecotoxicity and behavioural data in governmental regulation. Appl Herpetol 2:259–285

    Article  Google Scholar 

  • Brunelli E, Bernabó I, Berg C, Lundstedt-Enkel K, Bonacci A, Tripepsi S (2009) Environmentally relevant concentrations of endosulfan impair development, metamorphosis and behaviour in Bufo bufo tadpoles. Aquat Toxicol 91:135–142. doi:10.1016/j.aquatox.2008.09.006

    Article  CAS  Google Scholar 

  • Cooke AS (1971) Selective predation by newts on frog tadpoles treated with DDT. Nature 229:275–276. doi:10.1038/229275a0

    Article  CAS  Google Scholar 

  • Denoël M, Bichot M, Ficetola GF, Delcourt J, Ylieff MY, Kestemont P, Poncin P (2010) Cumulative effects of a road de-icing salt on amphibian behavior. Aquat Toxicol 99:275–280. doi:10.1016/j.aquatox.2010.05.007

    Article  Google Scholar 

  • Denoël M, D’Hooghe B, Ficetola GF, Brasseur C, De Pauw E, Thomé JP, Kestemont P (2012) Using sets of behavioral biomarkers to assess short-term effects of pesticide: a study case with endosulfan on frog tadpoles. Ecotoxicology 21:1240–1250. doi:10.1007/s10646-012-0878-3

    Article  Google Scholar 

  • Denoël M, Libon S, Kestemont P, Brasseur C, Focant JF, De Pauw E (2013) Effects of a sublethal pesticide exposure on locomotor behavior: a video-tracking analysis in larval amphibians. Chemosphere 90:945–951. doi:10.1016/j.chemosphere.2012.06.037

    Article  Google Scholar 

  • Dinehart SK, Smith LM, McMurry ST, Anderson TA, Smith PN, Haukos DA (2009) Toxicity of a glufosinate-and several glyphosate-based herbicides to juvenile amphibians from the Southern High Plains, USA. Sci Total Environ 407:1065–1071. doi:10.1016/j.scitotenv.2008.10.010

    Article  CAS  Google Scholar 

  • Dinehart SK, Smith LM, McMurry ST, Smith PN, Anderson TA, Haukos DA (2010) Acute and chronic toxicity of roundup weathermax and ignite 280 SL to larval Spea multiplicata and S. bombifrons from the Southern High Plains USA. Environ Pollut 158:2610–2617. doi:10.1016/j.envpol.2010.05.006

    Article  CAS  Google Scholar 

  • Dirzo R, Raven PH (2003) Global state of biodiversity and loss. Annu Rev Env Resour 28:137–167. doi:10.1146/annurev.energy.28.050302.105532

    Article  Google Scholar 

  • Ebert E, Leist KH, Mayer D (1990) Summary of safety evaluation toxicity studies of glufosinate ammonium. Food Chem Toxicol 28:339–349. doi:10.1016/0278-6915(90)90108-Y

    Article  CAS  Google Scholar 

  • EFSA (2005) Conclusion regarding the peer review of the pesticide risk assessment of the active substance glufosinate. Scientific Report 27:1–81

    Google Scholar 

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

    Article  CAS  Google Scholar 

  • Faber MJ, Thompson DG, Stephenson GR, Boermans HJ (1998a) Impact of glufosinate-ammonium and bialaphos on the phytoplankton community of a small eutrophic northern lake. Environ Toxicol Chem 17:1282–1290

    Article  CAS  Google Scholar 

  • Faber MJ, Thompson DG, Stephenson GR, Kreutzweiser DP (1998b) Impact of glufosinate-ammonium and bialaphos on the zooplankton community of a small eutrophic northern lake. Environ Toxicol Chem 17:1291–1299

    Article  CAS  Google Scholar 

  • Ferreira Nunes BV, Durán R, Alfonso M, de Oliveira IM, Ferreira Faro LR (2010) Evaluation of the effects and mechanisms of action of glufosinate, an organophosphate insecticide, on striatal dopamine release by using in vivo microdialysis in freely moving rats. Arch Toxicol 84:777–785. doi:10.1007/s00204-010-0533-9

    Article  CAS  Google Scholar 

  • Giusi G, Alo’ R, Crudo M, Di Vito A, Facciolo RM, Canonaco M (2010) Environmental stressors and neurobiological features of marine teleosts: histamine receptors as targets. Crit Rev Toxicol 40:620–632. doi:10.3109/10408444.2010.487479

    Article  CAS  Google Scholar 

  • Gosner KL (1960) A simplified table for staging anuran embryos and larvae, with notes on identification. Herpetologica 16:183–190

    Google Scholar 

  • Gupta RC (2006) Classification and uses of organophosphates and carbamates. In: Gupta RC (ed) Toxicology of organophosphate and carbamate compounds. Elsevier, San Diego, pp 5–24

    Chapter  Google Scholar 

  • Hamilton MA, Russo RC, Thurston RV (1977) Trimmed Spearman-Karber method for estimating median lethal concentrations in toxicity bioassays. Environ Sci Technol 11:714–719

    Article  CAS  Google Scholar 

  • Hayes TB, Case P, Chui S, Chung D, Haeffele C, Haston K, Lee M, Mai VP, Marjuoa Y, Parker J, Tsui M (2006) Pesticide mixtures, endocrine disruption, and amphibian declines: are we underestimating the impact? Environ Health Perspect 114:40–50. doi:10.1289/ehp.8051

    Article  Google Scholar 

  • IUCN (2010) IUCN red list of threatened species. Version 2010.4. http://www.iucnredlist.org. Accessed 10 Oct 2012.

  • Jalaludin A, Ngim J, Bakar BHJ, Alias Z (2010) Preliminary findings of potentially resistant goosegrass (Eleusine indica) to glufosinate-ammonium in Malaysia. Weed Biol Manag 10:256–260. doi:10.1111/j.1445-6664.2010.00392.x

    Article  Google Scholar 

  • Jones DK, Hammond JI, Relyea RA (2009) Very highly toxic effects of endosulfan across nine species of tadpoles: lag effects and family-level sensitivity. Environ Toxicol Chem 28:1939–1945. doi:10.1897/09-033.1

    Article  CAS  Google Scholar 

  • Junges CM, Peltzer PM, Lajmanovich RC, Attademo AM, Cabagna-Zenklusen MC, Bassó A (2012) Toxicity of the fungicide trifloxystrobin on tadpoles and its effect on fish-tadpole interaction. Chemosphere 87:1348–1354. doi:10.1016/j.chemosphere.2012.02.026

    Article  CAS  Google Scholar 

  • Kane AS, Salierno JD, Brewer SK (2005) Fish models in behavioral toxicology: automated techniques, updates and perspectives. In: Ostrander GK (ed) Techniques in aquatic toxicology. CRC Press, Boca Raton, pp 559–590

    Google Scholar 

  • Kingsley GR (1942) The direct biuret method for the determination of serum proteins as applied to photoelectric and visual calorimetry. J Lab Clin Med 27:840–845

    CAS  Google Scholar 

  • Koyama K, Goto K (1997) Cardiovascular effects of a herbicide containing glufosinate and a surfactant: in vitro and in vivo analyses in rats. Toxicol Appl Pharmacol 145:409–414. doi:10.1006/taap.1997.8196

    Article  CAS  Google Scholar 

  • Kutlesa NJ, Caveney S (2001) Insecticidal activity of glufosinate through glutamine depletion in a caterpillar. Pest Manag Sci 57:25–32. doi:10.1002/1526-4998(200101

    Article  CAS  Google Scholar 

  • Lajmanovich RC, Peltzer PM, Junges CM, Attademo AM, Sanchez LC, Bassó A (2010) Activity levels of B-esterases in the tadpoles of 11 species of frogs in the middle Paraná River floodplain: implication for ecological risk assessment of soybean crops. Ecotoxicol Environ Saf 73:1517–1524. doi:10.1016/j.ecoenv.2010.07.047

    Article  CAS  Google Scholar 

  • Lajmanovich RC, Attademo AM, Peltzer PM, Jungues C, Cabagna M (2011) Toxicity of four herbicide formulations with glyphosate on Rhinella arenarum (Anura: Bufonidae) tadpoles: B-esterases and glutathione S-transferase inhibitions. Arch Environ Contam Toxicol 60:681–689. doi:10.1007/s00244-010-9578-2

    Article  CAS  Google Scholar 

  • Lajmanovich RC, Junges CM, Attademo AM, Peltzer PM, Cabagna Zenklusen M, Bassó A (2013) Individual and mixture toxicity of commercial formulations containing glyphosate, metsulfuron-methyl, bispyribac-sodium, and picloram on Rhinella arenarum tadpoles. Water Air Soil Pollut 112:1404. doi:10.1007/s11270-012-1404-1

    Article  Google Scholar 

  • Larson SJ, Capel PD, Majewski (1997) Pesticides in surface water: distribution trends, and governing factors. Volume 3 of the series pesticides in the hydrologic system. Ann Arbor Press Inc, Chelsea

    Google Scholar 

  • López SL, Aiassa D, Benítez-Leitec S, Lajmanovich RC, Mañas F, Poletta G, Sánchez N, Simoniello MF, Carrasco AE (2012) Pesticides used in South American GMO-based agriculture: a review of their effects on humans and animal models. Adv Mol Toxicol 6:41–75

    Article  Google Scholar 

  • MAFF (1990) Evaluation no. 33: HOE 399866 (glufosinate-ammonium). MAFF, London

    Google Scholar 

  • Mann RM (2000) Toxicological impact of agricultural surfactants on Australian amphibians. Curtin University of Technology, Sydney

    Google Scholar 

  • Mao YC, Wang JD, Hung DZ, Deng JF, Yang CC (2011) Hyperammonemia following glufosinate-containing herbicide poisoning: a potential marker of severe neurotoxicity. Clin Toxicol (Phila) 49:48–52. doi:10.3109/15563650.2010.53918

    Article  CAS  Google Scholar 

  • Mao YC, Hung DZ, Wu ML, Tsai WJ, Wang LM, Ger J, Deng JF, Yang CC (2012) Acute human glufosinate-containing herbicide poisoning. Clin Toxicol (Phila) 50:396–402. doi:10.3109/15563650.2012.676646

    Article  CAS  Google Scholar 

  • Payne JF, Mathiew A, Melving W, Fancey LL (1996) Acetylcholinesterase, an old biomarker with a new future? Field trials in association with two urban rivers and a paper mill in Newfoundland. Mar Pollut Bull 32:225–231. doi:10.1016/0025-326X(95)00112-Z

    Article  CAS  Google Scholar 

  • Peltzer PM, Lajmanovich RC, Attademo AM, Beltzer AH (2006) Diversity of anurans across agricultural ponds in Argentina. Biodivers Conserv 15:3499–3513

    Article  Google Scholar 

  • Punzo F (2005) Effects of insecticide (carbaryl) exposure on activity and swimming performance of tadpoles of the Rio Grande leopard frog, Rana berlandieri (Anura: Ranidae). Tex J Sci 57:263–272

    Google Scholar 

  • Reeves MK, Jensen P, Dolph CL, Holyoak M, Trust KA (2010) Multiple stressors and the cause of amphibian abnormalities. Ecol Monogr 80:423–440. doi:10.1890/09-0879.1

    Article  Google Scholar 

  • Relyea RA, Edwards K (2010) What doesn’t kill you makes you sluggish: how sublethal pesticides alter predator–prey interactions. Copeia 4:558–567. doi:10.1643/CE-09-027

    Article  Google Scholar 

  • Relyea RA, Hoverman JT (2006) Assessing the ecology in ecotoxicology: a review and synthesis in freshwater systems. Ecol Lett 9:1–15. doi:10.1111/j.1461-0248.2006.00966.x

    Article  Google Scholar 

  • Relyea RA, Jones DK (2009) The toxicity of Roundup Original Max® to 13 species of larval amphibians. Environ Toxicol Chem 28:2004–2008. doi:10.1897/09-021.1

    Article  CAS  Google Scholar 

  • Richards SM, Kendall RJ (2003) Physical effects of chlorpyrifos on two stages of Xenopus laevis. J Toxicol Environ Health 66:75–91. doi:10.1080/15287390306461

    Article  CAS  Google Scholar 

  • Robles-Mendoza C, Zúñiga-Lagunes SR, Ponce de León-Hill CA, Hernández-Soto J, Vanegas-Pérez C (2011) Esterases activity in the axolotl Ambystoma mexicanum exposed to chlorpyrifos and its implication to motor activity. Aquat Toxicol 105:728–734. doi:10.1016/j.aquatox.2011.09.001

    Article  CAS  Google Scholar 

  • Royer A, Beguin S, Sochor H, Communal P (2000) Determination of glufosinate ammonium and its metabolite (AT F064619 and AE F061517) residues in water by gas chromatography with tandem mass spectrometry after ion exchange cleanup and derivatization. J Agric Food Chem 48:5184–5189. doi:10.1021/jf000281u

    Article  CAS  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, New York, pp 1–48

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

    Article  Google Scholar 

  • Scott GR, Sloman KA (2004) The effects of environmental pollutants on complex fish behaviour: integrating behavioural and physiological indicators of toxicity. Aquat Toxicol 68:369–392. doi:10.1016/j.aquatox.2004.03.016

    Article  CAS  Google Scholar 

  • Sparling DW, Cowman DF (2003) Amphibians and pesticides in pristine areas. In: Linder G, Krest SK, Sparling DW (eds) Amphibian decline: an integrated analysis of multiple stressor effects. Society of Environmental Toxicology and Chemistry SETAC, Pensacola, pp 257–264

    Google Scholar 

  • Sparling DW, Fellers GM (2009) Toxicity of two insecticides to California, USA, anurans and its relevance to declining amphibian populations. Environ Toxicol Chem 8:1696–1703. doi:10.1897/08-336.1

    Article  Google Scholar 

  • Sturm A, de Assis HC, Hansen PD (1999) Cholinesterases of marine teleost fish: enzymological characterization and potential use in biomonitoring of neurotoxic contamination. Mar Environ Res 47:389–398. doi:10.1016/S0141-1136(98)00127-5

    Article  CAS  Google Scholar 

  • Thompson HM, Walker CH, Hardy AR (1991) Changes in the activity of avian serum esterases following exposure to organophosphorus insecticides. Arch Environ Contam Toxicol 20:514–518. doi:10.1007/BF01065841

    Article  CAS  Google Scholar 

  • USEPA (US Environmental Protection Agency) (1989) Short-term methods for estimating the chronic toxicity of effluents and receiving waters to freshwater organisms. Report EPA/600/4-89/001. Environmental Protection Agency, Cincinnati

    Google Scholar 

  • Van Buskirk J, McCollum SA (2000) Influence of tail shape on tadpole swimming performance. J Exp Biol 203:2149–2158

    Google Scholar 

  • Walker CH, Hopkin SP, Sibly RM, Peakall DB (2001) Principles of ecotoxicology, 2nd edn. Taylor and Francis, New York

    Google Scholar 

  • Wang C, Murphy SD (1982) Kinetic analysis of species difference in acetylcholinesterase sensitivity to organophosphate insecticides. Toxicol Appl Pharmacol 66:409–419

    Article  CAS  Google Scholar 

  • Ware GW, Whitacre DM (2004) The pesticide book, 6th edn. Thompson, Fresno

    Google Scholar 

  • Watanabe T, Sano T (1998) Neurological effects of glufosinate poisoning with a brief review. Hum Exp Toxicol 17:35–39. doi:10.1177/096032719801700106

    Article  CAS  Google Scholar 

  • Weis JS, Smith G, Zhou T, Santiago-Bass C, Weis P (2001) Effects of contaminants on behavior: biochemical mechanisms and ecological consequences. Bioscience 51:209–217. doi:10.1641/0006-3568(2001)051

    Article  Google Scholar 

  • Wharfe J (2004) Hazardous chemicals in complex mixtures-A role for direct toxicity assessment. Ecotoxicology 13:413–421. doi:10.1023/B:ECTX.0000035292.00099.f0

    Article  CAS  Google Scholar 

  • Widder PD, Bidwell JR (2006) Cholinesterase activity and behavior in chlorpyrifos-exposed Rana sphenocephala tadpoles. Environ Toxicol Chem 25:2446–2454. doi:10.1897/05-522R.1

    Article  CAS  Google Scholar 

  • Widder PD, Bidwell JR (2008) Tadpole size, cholinesterase activity and swim speed in four frog species after exposure to sub-lethal concentrations of chlorpyrifos. Aquat Toxicol 88:9–18. doi:10.1016/j.aquatox.2008.02.008

    Article  CAS  Google Scholar 

  • Zar JH (1999) Biostatistical analysis. Prentice-Hall, New Jersey

    Google Scholar 

  • Zeldin EL, Jury TP, Serres RA, McCown BH (2002) Tolerance to the herbicide glufosinate in transgenic cranberry (Vaccinium macrocarpon Ait.) and enhancement of tolerance in progeny. J Amer Soc Hort Sci 127:502–507

    CAS  Google Scholar 

Download references

Acknowledgments

This study was supported in part by Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET) [11220100100009], Agencia Nacional de Promoción Científica y Tecnológica (ANCyT) [1522], and Curso de Acción para la Investigación y Desarrollo (CAI+D-UNL) [2011014]. We also thank two anonymous reviewers who made invaluable comments and suggestions and J. Brasca for English Editing Service.

Conflict of interest

The authors declare that they have no conflicts of interest.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Rafael C. Lajmanovich.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Peltzer, P.M., Junges, C.M., Attademo, A.M. et al. Cholinesterase activities and behavioral changes in Hypsiboas pulchellus (Anura: Hylidae) tadpoles exposed to glufosinate ammonium herbicide. Ecotoxicology 22, 1165–1173 (2013). https://doi.org/10.1007/s10646-013-1103-8

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10646-013-1103-8

Keywords

Navigation