[en] Pesticides and other chemicals often have detrimental effects at environmental concentrations. Many amphibian species are particularly threatened because of their susceptibility but also because wetlands are often polluted. Behavioral assessments of toxicity have the advantage of showing sublethal effects but quantitative measures at varied scales of integrations are rarely considered together. In this study, we aimed at showing that these behavioral endpoints could be differently affected across time and concentrations, and be biomarkers of toxicity. To this end, we tested the effects of an organochlorine pesticide (endosulfan) on amphibians during a standard 96 h test. We evaluated possible lag effects in continuing the analyses after removal of the pesticide. The study was based on 240 tadpoles (4 pesticide treatments: 0.4, 3, 22, and 282 lg/l, 1 control and 1 solvent-control). Abnormal behaviors such as lying and swirling rapidly were exhibited only in the presence of the pesticide. Essential functions such as breathing and feeding were deeply affected by the pesticide: contaminated tadpoles breathed and fed less than control tadpoles. They also moved less and occupied a more central position in the aquariums in the presence of the pesticide. A higher mortality was only found at the highest concentration. These results suggest that endosulfan is toxic to amphibians at environmental concentrations. Behavioral markers showed potential as early warning systems. They should thus be used in complement to other markers to detect sublethal effects only a few days after application of the pesticide and at concentrations where mortality does not occur.
Denoël, Mathieu ; Université de Liège - ULiège > Département de Biologie, Ecologie et Evolution > Biologie du comportement - Ethologie et psychologie animale
D'hooghe, Bastien; Université de Liège - ULiège > Bioloogie, Ecologie et Evolution > Unité de Biologie du Comportement
Ficetola, G. Francesco; University of Milano-Bicocca > Department of Environmental Sciences
Brasseur, Catherine ; Université de Liège - ULiège > Département de chimie (sciences) > GIGA-R : Laboratoire de spectrométrie de masse (L.S.M.)
De Pauw, Edwin ; Université de Liège - ULiège > Département de chimie (sciences) > GIGA-R : Laboratoire de spectrométrie de masse (L.S.M.)
Thomé, Jean-Pierre ; Université de Liège - ULiège > Département de Biologie, Ecologie et Evolution > Ecologie animale et écotoxicologie
Kestemont, Patrick; Université Npotre-Dame de la Paix > Research Unit in Environmental and Evolutionary Biology
Language :
English
Title :
Using sets of behavioral biomarkers to assess short-term effects of pesticide: a study case with endosulfan on frog tadpoles
Publication date :
2012
Journal title :
Ecotoxicology
ISSN :
0963-9292
eISSN :
1573-3017
Publisher :
Kluwer Academic Publishers, Boston, United States - Massachusetts
Volume :
21
Issue :
4
Pages :
1240-1250
Peer reviewed :
Peer Reviewed verified by ORBi
Funders :
F.R.S.-FNRS - Fonds de la Recherche Scientifique FRFC - Fonds de la Recherche Fondamentale Collective
AlfordRA(1999) Ecology. Resource use, competition, and predation. In: McDiarmid RW, Altig R (eds) Tadpoles. The biology of anuran larvae. The University of Chicago Press, Chicago, pp 240-278
APHA (1985) Standard methods for the examination of water and wastewater, 16th edn. American Health Association, Washington, D.C.
Bates D, Maechler M (2010) Lme4: linearmixed-effectsmodels using S4 classes. R package version 0.999375-37. www.r-project.org
Bernabò I, Brunelli E, Berg C, Bonacci A, Tripepi S (2008) Endosulfan acute toxicity in Bufo bufo gills: ultrastructural changes and nitric oxide synthase localization. Aquat Toxicol 86:447-456
Berrill M, Coulson D, McGillivray L, Pauli B (1998) Toxicity of endosulfan to aquatic stages of anuran amphibians. Environ Toxicol Chem 17:1738-1744
Boone MD, Cowman D, Davidson C, Hayes TB, Hopkins WA, Relyea R, Schiesari L, Semlitsch R (2007) Evaluating the role of environmental contamination in amphibian population decline. In: Gascon C, Collins JP, Moore RD, Church DR, McKay JE, Mendelson III JR (eds) Amphibian conservation action plan. Proceedings: IUCN/SSC Amphibian Conservation Summit 2005. The World Conservation Union (IUCN), Gland, Switzerland, pp 32-35
Bromhall SD (2005) Measuring chemical impacts on amphibians: ecotoxicity and behavioural data in governmental regulation. Appl Herpetol 2:259-285
Broomhall S, Shine R (2003) Effects of the insecticide endosulfan and presence of congeneric tadpoles on Australian treefrog (Litoria freycineti) tadpoles. Arch Environ Contam Toxicol 45:221-226
Brunelli E, Bernabò I, Berg C, Lundstedt-Enkel K, Bonacci A, Tripepi S (2009) Environmentally relevant concentrations of endosulfan impair development, metamorphosis and behaviour in Bufo bufo tadpoles. Aquat Toxicol 91:135-142
Brunelli E, Bernabò I, Sperone E, Tripepi S (2010) Gill alterations as biomarkers of chronic exposure to endosulfan in Bufo bufo tadpoles. Histol Hispathol 25:1519-1529
Caride A, Lafuente A, Cabaleiro T (2010) Endosulfan effects on pituitary hormone and both nitrosative and oxidative stress in pubertal male rats. Toxicol Lett 197:106-112
Carlile WR (2006) Pesticide selectivity, health and the environment. Cambridge University Press, Cambridge
Carriger JF, Hoang TC, Rand GM, Gardinali PR, Castro J (2011) Acute toxicity and effects analysis of endosulfan sulfate to freshwater fish species. Arch Environ Contam Toxicol 60:281-289
Close B, Banister K, Baumans V, Bernoth E-M, Bromage N, Bunyan J, Erhardt W, Flecknell P, Gregory N, Hackbarth H, Morton D, Warwick C (1996) Recommendations for euthanasia of experimental animals: part 1. Lab Anim 30:293-313
Croteau MC, Hogan N, Gibson JC, Lean D, Trudeau VL (2008) Toxicological threats to amphibians and reptiles in urban environments. In: Mitchell JC, Jung Brown RE, Bartholomew B (eds) Urban herpetology. Herpetological Conservation 3. Society for the Study of Amphibians and Reptiles, Salt Lake City, Utah, pp 197-209
De la Colina C, Peña A, Mingorance MD, Sanchez Rasero F (1996) Influence of the solid-phase extraction process on calibration and performance parameters for the determination of pesticide residues in water by gas chromatography. J Chromatogr 733A:275-281
De Lange HJ, Noordoven W, Murk AJ, Lurling M, Peeters E (2006) Behavioural responses of Gammarus pulex (Crustacea, Amphipoda) to low concentrations of pharmaceuticals. Aquat Toxicol 78:209-216
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
Dorts J, Silvestre F, Tu HT, Tyberghein A-E, Phuong NT, Kestemont P (2009) Oxidative stress, protein carbonylation and heat shock proteins in the black shrimp, Penaeus monodon, following exposure to endosulfan and deltamethrin. Env Toxicol Pharmacol 28:302-310
Eddins D, Cerutti D, Williams P, Linney E, Levin ED (2010) Zebrafish provide a sensitive model of persisting neurobehavioral effects of developmental chlorpyrifos exposure: comparison with nicotine and pilocarpine effects and relationship to dopamine deficits. Neurotoxicol Teratol 32:99-108
Egea-Serrano A, Tejedo M, Torralva M (2009) Populational divergence in the impact of three nitrogenous compounds and their combination on larvae of the frog Pelophylax perezi (Seoane, 1885). Chemosphere 76:869-877
Egea-Serrano A, Tejedo M, Torralva M (2011) Behavioral responses of the Iberian waterfrog, Pelophylax perezi (Seoane, 1885), to three nitrogenous compounds in laboratory conditions. Ecotoxicology 20:1246-1257
Ernst WR, Jonah P, Doe K, Julien G, Hennigar P (1991) Toxicity to aquatic organisms of off-target deposition of endosulfan applied by aircraft. Environ Toxicol Chem 10:103-114
Eterovick PC, Oliveira FFR, Tattersall GJ (2010) Threatened tadpoles of Bokermannohyla alvarengai (Anura: Hylidae) choose backgrounds that enhance crypsis potential. Biol J Linn Soc 101:437-446
Fordham CL, Tessari JD, Ramsdell HS, Keefe TJ (2001) Effects of malathion on survival, growth, development, and equilibrium posture of bullfrog tadpoles (Rana catesbeiana). Environ Toxicol Chem 20:179-184
Friberg-Jensen U, Nachman G, Christoffersen KS (2010) Early signs of lethal effects in Daphnia magna (Branchiopoda, Cladocera) exposed to the insecticide Cypermehtin and the fungicide Azoxystrobin. Environ Toxicol Chem 29:2371-2378
Gdovin MJ, Jackson VV, Zamora DA, Leiter JC (2006) Effect of prevention of lung inflation on metamorphosis and respiration in the developing bullfrog tadpole, Rana catesbeiana. J Exp Zool Part A Comp Exp Biol 305A:335-347
Gillardin V, Silvestre F, Dieu M, Delaive E, Raes M, Thome JP, Kestemont P (2009a) Protein expression profiling in the African clawed frog Xenopus laevis tadpoles exposed to the Polychlorinated Biphenyl Mixture Aroclor 1254. Mol Cell Proteomics 8:596-611
Gillardin V, Silvestre F, Divoy C, Thomé JP, Kestemont P (2009b) Effects of Aroclor 1254 on oxydative stress in developing Xenopus laevis tadpoles. Ecotoxicol Environ Saf 72:546-551
Giusi G, Facciolo RM, Alo R, Carelli A, Madeo M, Brandmayr P, Canonaco M (2005) Some environmental contaminants influence motor and feeding behaviors in the ornate wrasse (Thalassoma pavo) via distinct cerebral histamine receptor subtypes. Environ Health Perspect 113:1522-1529
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
Gosner KL (1960) A simplified table for staging anuran embryos and larvae with notes on identification. Herpetologica 16:183-190
Guerin TF (2001) Abiological loss of endosulfan and related chlorinated organic compounds from aqueous systems in the presence and absence of oxygen. Environ Pollut 115:219-230
Hayes TB, Khoury V, Narayan A, Nazir M, Park A, Brown T, Adame L, Chan E, Buchholz D, Stueve T, Gallipeau S (2010) Atrazine induces complete feminization and chemical castration in male African clawed frogs (Xenopus laevis). Proc Natl Acad Sci USA 107:4612-4617
Hoke RA, Ankley GT (2005) Application of frog embryo teratogenesis assay-Xenopus to ecological risk assessment. Environ Toxicol Chem 24:2677-2690
Hopkins WA (2007) Amphibians as models for studying environmental change. ILAR J 48:270-277
Jia H, Li Y-F, Wang D, Cai D, Yang M, Ma J, Hu J (2009) Endosulfan in China 1 - gridded usage inventories. Environ Sci Pollut Res 16:295-301
Jones D, Hammond J, Relyea R (2009) Very highly toxic effects of endosulfan across nine species of tadpoles: lag effects and family-level sensitivity. Environ Toxicol Chem 28:1939-1945
Kang HS, Gye MC, Kim MK (2008) Effects of endosulfan on survival and development of Bombina orientalis (Boulenger) embryos. Bull Environ Contam Toxicol 81:262-265
Kelly BC, Ikonomou MG, Blair JD, Morin AE, Gobas F (2007) Food web-specific biomagnification of persistent organic pollutants. Science 317:236-239
Kvarnryd M, Grabic R, Brandt I, Berg C (2011) Early life progestin exposure causes arrested oocyte development, oviductal agenesis and sterility in adult Xenopus tropicalis frogs. Aquat Toxicol 103:18-24
Laurila A (2000) Behavioural responses to predator chemical cues and local variation in antipredator performance in Rana temporaria tadpoles. Oikos 88:159-168
Mandrillon AL, Saglio P (2007) Herbicide exposure affects the chemical recognition of a non native predator in common toad tadpoles (Bufo bufo). Chemoecology 17:31-36
Marquis O, Millery A, Guittonneau S, Miaud C (2006) Solvent toxicity to amphibian embryos and larvae. Chemosphere 63:889-892
Marquis O, Miaud C, Ficetola GF, Boscher A, Mouchet F, Guittonneau S, Devaux A (2010) Variation in genotoxic stress tolerance among frog populations exposed to UV and pollutant gradients. Aquat Toxicol 95:152-161
McIntyre PB, McCollum SA (2000) Responses of bullfrog tadpoles to hypoxia and predators. Oecologia 125:301-308
McWilliam RA, Baird DJ (2002) Postexposure feeding depression: a new toxicity endpoint for use in laboratory studies with Daphnia magna. Environ Toxicol Chem 21:1198-1205
Newman MC, Crane M, Holloway G (2006) Does pesticide risk assessment in the European Union assess long-term effects? Rev Environ Contam Toxicol 187:3-65
Palma P, Alvarenga P, Palma V, Matos C, Fernandes RM, Soares A, Barbosa IR (2010) Evaluation of surface water quality using an ecotoxicological approach: a case study of the Alqueva Reservoir (Portugal). Environ Sci Pollut Res 17:703-716
Park D, Hempleman SC, Propper CR (2001) Endosulfan exposure disrupts pheromonal systems in the red-spotted newt: a mechanism for subtle effects of environmental chemicals. Environ Health Perspect 109:669-673
Pinheiro P, Bates D (2000) Mixed-effect models in S and S-Plus. Springer, New York
Rangaswamy C, Naidu B (1999) Effect of endosulfan on oxygen equilibrium curves of blood of food fish Oreochromis mossambicus (Peters). Indian J Exp Biol 37:166-168
Relyea RA, Hoverman JT (2006) Assessing the ecology in ecotoxicology: a review and synthesis in freshwater systems. Ecol Lett 9:1157-1171
Saiyed H, Dewan A, Bhatnagar V, Shenoy U, Shenoy R, Rajmohan H, Patel K, Kashyap R, Kulkarni P, Rajan B, Lakkad B (2003) Effect of endosulfan on male reproductive development. Environ Health Perspect 111:1958-1962
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
Srivastava N, Harit G, Srivastava R (2009) A study of physicochemical characteristics of lakes around Jaipur, India. J Environ Biol 30:889-894
Stanley KA, Curtis LR, Simonich SLM, Tanguay RL (2009) Endosulfan I and endosulfan sulfate disrupts zebrafish embryonic development. Aquat Toxicol 95:355-361
Stebbins RC, Cohen NW (1995) A natural history of amphibians. Princeton University Press, Princeton
Stuart SN, Chanson JS, Cox NA, Young BE, Rodrigues ASL, Fischman DL, Waller DW (2004) Status and trends of amphibian declines and extinctions worldwide. Science 306:1783-1786
Thangavel P, Sumathiral K, Maheswari S, Rita S, Ramaswamy M (2010) Hormone profile of an edible, freshwater teleost, Sarotherodon mossambicus (Peters) under endosulfan toxicity. Pestic Biochem Physiol 97:229-234
Tu HT, Silvestre F, Scippo M-L, Thome J-P, Phuong NT, Kestemont P (2009) Acetylcholinesterase activity as a biomarker of exposure to antibiotics and pesticides in the black tiger shrimp (Penaeus monodon). Ecotoxicol Environ Saf 72:1463-1470
Tu HT, Silvestre F, Phuong NT, Kestemont P (2010) Effects of pesticides and antibiotics on penaeid shrimp with special emphases on behavioral and biomarker responses. Environ Toxicol Chem 29:929-938
U.S.EPA (2010) Endosulfan: 2010 environmental fate and ecological risk assessment. United States Environmental Protection Agency, Office of Chemical Safety and Pollution Prevention
Venables WN, Ripley BD (2002) Modern applied statistics with S, 4th edn. Springer, New York
Venturino A, Rosenbaum E, De Castro AC, Anguiano OL, Gauna L, De Schroeder TF, De D'Angelo AMP (2003) Biomarkers of effect in toads and frogs. Biomarkers 8:167-186
Walker CH, Hopkin SP, Sibly RM, Peakall DB (2006) Principles of ecotoxicology. Taylor & Francis, Boca Raton
Weber J, Halsall CJ, Muir D, Teixeira C, Small J, Solomon K, Hermanson M, Hung H, Bidleman T (2010) Endosulfan, a global pesticide: a review of its fate in the environment and occurrence in the Arctic. Sci Total Environ 408:2966-2984
Wells KD (2007) The ecology and behavior of amphibians. The University of Chicago Press, Chicago
Westman AD, Elliott J, Cheng K, van Aggelen G, Bishop CA (2010) Effects of environmentally relevant concentrations of Endosulfan, Azinphosmethyl, and Diazinon on Great Basin spadefoot (Spea intermontana) and Pacific treefrog (Pseudacris regilla). Environ Toxicol Chem 29:1604-1612
Winandy L, Denoël M (2011) The use of visual and automatized behavioral markers to assess methodologies: a study case on PIT-tagging in the alpine newt. Behav Res Methods 43:568-576
Wolfenson S, Lloyd M (2003) Handbook of laboratory animal - management and welfare. Blackwell Publishing, Oxford