[en] Understanding the impact of pesticides in amphibians is of growing concern to assess the causes of their decline. Among pesticides, endosulfan belongs to one of the potential sources of danger because of its wide use and known effects, particularly neurotoxic, on a variety of organisms. However, the effect of endosulfan was not yet evaluated on amphibians at levels encompassing simultaneously brain neurotransmitters and behavioural endpoints. In this context, tadpoles of the African clawed frog Xenopus laevis were submitted to four treatments during 27 d: one control, one ethanol control, and two low environmental concentrations of endosulfan (0.1 and 1 μg L−1). Endosulfan induced a significant increase of brain serotonin level at both concentrations and a significant increase of brain dopamine and GABA levels at the lower exposure but acetylcholinesterase activity was not modified by the treatment. The gene coding for the GABA transporter 1 was up-regulated in endosulfan contaminated tadpoles while the expression of other genes coding for the neurotransmitter receptors or for the enzymes involved in their metabolic pathways was not significantly modified by endosulfan exposure. Endosulfan also affected foraging, and locomotion in links with the results of the physiological assays, but no effects were seen on growth. These results show that low environmental concentrations of endosulfan can induce adverse responses in X. laevis tadpoles. At a broader perspective, this suggests that more research using and linking multiple markers should be used to understand the complex mode of action of pollutants.
Research center :
AFFISH-RC - Applied and Fundamental FISH Research Center - ULiège
Preud'Homme, Valérie; Université de Namur & Université de Liège > URBO & Unité de Biologie du Comportement
Milla, Sylvain; Université de Namur > URBO
Gillardin, Virginie; Université de Namur > URBO
De Pauw, Edwin ; Université de Liège - ULiège > Département de chimie (sciences) > Laboratoire de spectrométrie de masse (L.S.M.)
Denoël, Mathieu ; Université de Liège - ULiège > Département de Biologie, Ecologie et Evolution > Biologie du comportement - Ethologie et psychologie animale
Kestemont, Patrick; Université de Namur > URBO
Language :
English
Title :
Effects of low dose endosulfan exposure on brain neurotransmitter levels in the African clawed frog Xenopus laevis
Publication date :
February 2015
Journal title :
Chemosphere
ISSN :
0045-6535
eISSN :
1879-1298
Publisher :
Elsevier Science, Oxford, United Kingdom
Volume :
120
Issue :
2
Pages :
357-364
Peer reviewed :
Peer Reviewed verified by ORBi
Funders :
FRFC - Fonds de la Recherche Fondamentale Collective [BE] F.R.S.-FNRS - Fonds de la Recherche Scientifique [BE]
Agrawal A.K., Anand M., Zaidi N.F., Seth P.K. Involvement of serotonergic receptors in endosulfan toxicity. Biochem. Pharmacol. 1983, 32:3591-3593.
Ballesteros M.L., Wunderlin D.A., Bistoni M.A. Oxidative stress responses in different organs of Jenynsia multidentata exposed to endosulfan. Ecotox. Environ. Safe. 2009, 72:199-205.
Bernabò I., Brunelli E., Berg C., Bonacci A., Tripepi S. Endosulfan acute toxicity in Bufo bufo gills: ultrastructural changes and nitric oxide synthase localization. Aquat. Toxicol. 2007, 86:447-456.
Bist R., Bhatt D.K. The evaluation of effect of alpha-lipoic acid and vitamin E on the lipid peroxidation, gamma amino butyric acid and serotonin level in the brain of mice (Mus musculus) acutely intoxicated with lindane. J. Neurol. Sci. 2009, 276:99-102.
Bonfanti P., Colombo A., Orsi F., Nizzetto I., Andrioletti M., Bacchetta R., Mantecca P., Fascio U., Vailati G., Vismara C. Comparative teratogenicity of chlorpyrifos and malathion on Xenopus laevis development. Aquat. Toxicol. 2004, 10:189-200.
Bradford M.M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein in a sample. Anal. Biochem. 1976, 72:248-254.
Broomhall S. The effects of endosulfan and variable water temperature on survivorship and subsequent vulnerability to predation in Litoria citropa tadpoles. Aquat. Toxicol. 2002, 61:243-250.
Broomhall S., Shine R. Effects of the insecticide endosulfan and presence of congeneric tadpoles on Australian treefrog (Litoria freycineti) tadpoles. Arch. Environ. Contam. Toxicol. 2003, 45:221-226.
Brunelli E., Bernabò I., Berg C., Lundstedt-Enkel K., Bonacci A., Tripepi S. Environmentally relevant concentrations of endosulfan impair development, metamorphosis and behaviour in Bufo bufo tadpoles. Aquat. Toxicol. 2009, 91:135-142.
Cabaleiro T., Caride A., Romero A., Lafuente A. Effects of in utero and lactational exposure to endosulfan in prefrontal cortex of male rats. Toxicol. Lett. 2008, 176:58-67.
Chomczynski P., Sacchi N. Single-step method of RNA isolation by acid guanidium thiocyanate-phenol-chloroform extraction. Anal. Biochem. 1987, 162:156-159.
Chopra A.K., Sharma M.K., Chamoli S. Bioaccumulation of organochlorine pesticides in aquatic system - an overview. Environ. Monit. Assess. 2010, 173:905-916.
Christin M.S., Ménard L., Gendron A.D., Ruby S., Cyr D., Marcogliese J., Rollins-Smith L., Fournier M. Effects of agricultural pesticides on the immune system of Xenopus laevis and Rana pipiens. Aquat. Toxicol. 2004, 67:33-43.
Colombo A., Orsi F., Bonfanti P. Exposure to the organophosphorus pesticide chlorpyrifos inhibits acetylcholinesterase activity and affects muscular integrity in Xenopus laevis larvae. Chemosphere 2005, 61:1665-1671.
Conners D.E., Rogers E.D., Armbrust K.L., Kwon J.W., Black M.C. Growth and development of tadpoles (Xenopus laevis) exposed to selective serotonin reuptake inhibitors, fluoxetine and sertraline, throughout metamorphosis. Environ. Toxicol. Chem. 2009, 28:2671-2676.
Delcourt J., Denoël M., Ylieff M., Poncin P. Video multitracking of fish behaviour: a review and future perspectives. Fish Fisher 2013, 14:186-204.
Denoël M., Džukić G., Kalezić M.L. Effect of widespread fish introductions on paedomorphic newts in Europe. Conserv. Biol. 2005, 19:162-170.
Denoël M., Bichot M., Ficetola G.F., Delcourt J., Ylieff M.Y., Kestemont P., Poncin P. Cumulative effects of a road de-icing salt on amphibian behavior. Aquat. Toxicol. 2010, 99:275-280.
Denoël M., D'Hooghe B., Ficetola G.F., Brasseur C., De Pauw E., Thomé J.P., Kestemont P. Using sets of behavioral biomarkers to assess short-term effects of pesticide: a study case with endosulfan on frog tadpoles. Ecotoxicology 2012, 21:1240-1250.
Denoël M., Libon S., Kestemont P., Brasseur C., Focant J.F., De Pauw E. Effects of a sublethal pesticide exposure on locomotor behavior: a video-tracking analysis in larval amphibians. Chemosphere 2013, 90:945-951.
Denoël M., Perez A., Cornet Y., Ficetola G.F. Similar local and landscape processes affect both a common and a rare newt species. PLoS ONE 2013, 8:e62727.
Dimitrie, D., 2010. The effects of two insecticides on California anurans (Rana sierrae and Pseudacris sierra) and the implications for declining amphibian populations. PhD thesis Southern Illinois University Carbondale.
Dutta H.M., Arends D.A. Effects of endosulfan on brain acetylcholinesterase activity in juvenile bluegill sunfish. Environ. Res. 2003, 91:157-162.
Egea-Serrano A., Tejedo M., Torralva M. Behavioral responses of the Iberian waterfrog, Pelophylax perezi (Seoane, 1885), to three nitrogenous compounds in laboratory conditions. Ecotoxicology 2011, 20:1246-1257.
Ellman G.L., Courtney K.D., Andres V., Featherstone R.M. A new and rapid colorimetric determination of acetylcholinesterase activity. Biochemistry 1961, 7:88-95.
Environmental Protection Agency (EPA), 2002. Registration eligibility decisions for endosulfan. Red Facts. United States Environmental Protection Agency, Office of Prevention, Pesticides and toxic substances.
Faro L.R.F., Alfonso M., Cervantes R., Duran R. Comparative effects of pesticides on in vivo dopamine release in freely moving rats. Basic Clin. Pharmacol. Toxicol. 2009, 105:395-400.
Gillardin V., Silvestre F., Divoy C., Thomé J.P., Kestemont P. Effects of Aroclor 1254 on oxidative stress in developing Xenopus laevis tadpoles. Ecotox. Environ. Safe. 2009, 72:546-551.
Gillardin V., Silvestre F., Dieu M., Delaive E., Raes M., Thomé J.P., Kestemont P. Protein expression profiling in the African clawed frog Xenopus laevis tadpoles exposed to the PolyChlorinated Biphenyls mixture Aroclor 1254. Mol. Cell. Proteomics 2009, 8:596-611.
Jones D., Hammond J.I., Relyea R.A. Very highly toxic effects of endosulfan across nine species of tadpoles: lag effects and family-level sensitivity. Environ. Toxicol. Chem. 2009, 28:1939-1945.
Kiesecker J.M., Blaustein A.R., Belden L.K. Complex causes of amphibian population declines. Nature 2001, 410:681-684.
Lafuente A., Pereiro N. Neurotoxic effects induced by endosulfan exposure during pregnancy and lactation in female and male rat striatum. Toxicology 2013, 311:35-40.
Lakshmana M.K., Raju T.R. Endosulfan induces small but significant changes in the levels of noradrenaline, dopamine and serotonin in the developing rat brain and deficits in the operant learning performance. Toxicology 1994, 91:139-150.
Lavorato M., Bernabò I., Crescente A., Denoël M., Tripepi S., Brunelli E. Endosulfan effects on Rana dalmatina tadpoles: quantitative developmental and behavioural analysis. Arch. Environ. Contam. Toxicol. 2013, 64:253-262.
Liu J., Morrow A.L., Devaud L., Grayson D.R., Lauder J.M. GABAa receptors mediate trophic effects of GABA on embryonic brainstem monoamine neurons in vitro. J. Neurosci. 1997, 17:2420-2428.
Meguid M.M., Fetissov S.O., Varma M., Sato T., Zhang L., Laviano A., Rossi-Fanelli F. Hypothalamic dopamine and serotonin in the regulation of food intake. Nutrition 2000, 10:843-847.
Naqvi S.M., Vaishnavi C. Bioaccumulative potential and toxicity of endosulfan insecticide to non-target animals. Biocomp. Biochem. Physiol. 1993, 105:347-361.
Nieuwkoop P.D., Faber J. Normal Table of Xenopus laevis (Daudin) 1994, Garlan Publishing Inc., New-York and London, p. 252.
Paul V., Balasubramaniam E., Kazi M. The neurobehavioural toxicity of endosulfan in rats: a serotonergic involvement in learning impairment. Europ. J. Pharmacol. 1994, 270:1-7.
Rohr J.R., Elskus A.A., Shepherd B.S., Crowley P.H., McCarthy T.M., Niedzwiecki J.H., Sager T., Sih A., Palmer B.D. Lethal and sublethal effects of atrazine, carbaryl, endosulfan, and octylphenol on the streamside salamander (Ambystoma barbouri). Environ. Toxicol. Chem. 2003, 10:2385-2392.
Rui L. Brain regulation of energy balance and body weight. Rev. End. Metabol. Dis. 2013, 1-21.
Shenoy K., Cunningham B.T., Renfroe J.W., Crowley P.H. Growth and survival of northern leopard frog (Rana pipiens) tadpoles exposed to two common pesticides. Environ. Toxicol. Chem. 2009, 28:1469-1474.
Sillar K.T., Reith C.A., McDearmid J.R. Development and aminergic neuromodulation of a spinal locomotor network controlling swimming in Xenopus larvae. Ann. New-York Acad. Sci. 1998, 16:318-332.
Sparling D.W., Fellers G.M. Toxicity of two insecticides to California, USA, anurans and its relevance to declining amphibian populations. Environ. Toxicol. Chem. 2009, 28:1696-1703.
Stuart S.N., Chanson J.S., Cox N.A., Young B.E., Rodrigues A.S.L., Fischman D.L., Waller D.W. Status and trends of amphibian declines and extinctions worldwide. Science 2004, 306:1783-1786.
UN, 2011. Stockholm convention on Persistent Organic Pollutants. Adoption of an amendment to Annex A. United Nations.
Usha, S., Harikrishnan, V.R., 2004. Endosulfan - Fact Sheet and Answers to Common Questions. IPENPesticide Working Group Project.
Venesky M.D., Parris M.J., Storfer A. Impacts of Batrachochytrium dendrobatidis infection on tadpole foraging performance. EcoHealth 2010, 6:565-575.
Wake D.B., Vredenburg V.T. Are we in the midst of the sixth mass extinction? A view from the world of amphibians. Proc. Natl. Acad. Sci. USA 2008, 105:11466-11473.
Weber J., Halsall C.J., Muir D., Teixeira C., Small J., Solomon K., Hermanson M., Hung H., Bidleman T. Endosulfan, a global pesticide: a review of its fate in the environment and occurrence in the Arctic. Sci. Tot. Environ. 2009, 408:2966-2984.
Yu A., Wang X., Zuo Z., Cai J., Wang C. Tributyltin exposure influences predatory behavior, neurotransmitter content and receptor expression in Sebastiscus marmoratus. Aquat. Toxicol. 2013, 128-129:158-162.
