Abstract
Brazil is the largest consumer of pesticides in the world. However, knowledge on how these pesticides affect wildlife is scarce. Among the vertebrates, amphibians are particularly important in research to assess the impact of pesticides because of the correlation between pesticide and the decline of these species. This study aimed to evaluate the acute and chronic toxicity of commercial formulations of pesticides, i.e., atrazine (herbicide), cypermethrin (insecticide), and tebuconazole (fungicide) in Physalaemus cuvieri tadpoles. Eggs were collected in nature and cultivated under controlled conditions in the laboratory. Toxicity tests were carried out under standard conditions to determine the lethal concentration (LC50) after 96 h of exposure and to determine the effect of sublethal concentrations after 7 days. In addition, we performed swimming activity tests on tadpoles exposed to sublethal concentrations. The lethal concentration (LC50) was 19.69 mg/L for atrazine, 0.24 mg/L for cypermethrin and 0.98 mg/L for tebuconazole. In the acute test, atrazine showed lower toxicity than cypermethrin and tebuconazole for P. cuvieri. Swimming activity was affected at sublethal doses of atrazine and cypermethrin, but was not after exposure to tebuconazole. Cypermethrin was the insecticide that most altered the swimming activity of the individuals tested. The risk evaluation analysis indicated risks for tadpoles exposed to three tested pesticides, specially cypermethrin.
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References
Abraham M, Rodrigues MT, Baldo D (2010) Physalaemus cuvieri. The IUCN Red List of Threatened Species 2010: https://doi.org/10.2305/IUCN.UK.2010-2.RLTS.T57250A11609155.en. Accessed 22 Jun 2017
Albuquerque AF, Ribeiro JS, Kummrow F, Nogueira AJA, Montagner CC, Umbuzeiro GA (2016) Pesticides in Brazilian freshwaters: a critical review. Environ Sci Process Impacts 18:779–787
Allran JW, Karasov WH (2000) Effects of atrazine and nitrate on northern Leopard frog (Rana pipiens) larvae exposed in the laboratory from post hatch through metamorphosis. Environ Toxicol Chem 19:2850–2855
Andrei E (2017) Compêndio de defensivos agrícolas: guia prático de produtos fitossanitários para uso agrícola. Andrei, São Paulo
Azevedo-Ramos C, Sluys MV, Hero IM, Magnusson W (1992) Influence of tadpole movement on predation by odonate naiads. J Herpetol 26:335–338
Bernabò I, Guardia A, Macyrella R, Sesti S, Crescente A, Brunelli E (2016) Effects of long-term exposure to two fungicides, pyrimethanil and tebuconazole, on survival and life history traits of Italian tree frog (Hyla intermedia). Aquat Toxicol 172:56–66
Bethsass J, Colangelo A (2006) European union bans atrazine, while the United States negotiates continued use. Int J Occup Environ Health 12:260–267
Biga LM, Blaustein AR (2013) Variations in lethal and sublethal effects of cypermethrin among aquatic stages and species of anuran amphibians. Environ Toxicol Chem 32:2855–2860
Bishop CA, Mahony NA, Struger J, NG P, Pettit KE (1999) Anuran development, density and diversity in relation of agricultural activity in the Holland river watershed, Ontario, Canada (1990–1992). Environ Monit Assess 57:21–43
Boone MD, Bridges CM, Rothermel BB (2001) Growth and development larval green frogs (Rana clamitans) exposed to multiple doses of an insecticide. Oecologia 129:518–524
BRASIL (2005) Resolução 375 do Conselho Nacional do Meio Ambiente, CONAMA. Brasília. http://www.mma.gov.br/port/conama/res/res05/res35705.pdf. Accessed 01 Aug 2017
BRASIL (2011) Portaria No. 2914 do Ministério da Saúde. Brasília. http://portalarquivos.saude.gov.br/images/pdf/2015/maio/25/Portaria-MS-no-2.914-12-12-2011.pdf. Accessed 01 Aug 2017
BRASIL (2014) Portaria Nº 320 da Secretária de Estado da Saúde do Rio Grande do Sul. Porto Alegre. https://www.legisweb.com.br/legislacao/?id=269539. Accessed 01 Aug 2017
BRASIL (2017) Ministério da Agricultura e Pecuária (Ministry of Agriculture and Livestock). AGROFIT. http://www.agricultura.gov.br. Accessed 01 Aug 2017
Brodeur JC, Svartz G, Perez-Coll CS, Marino DJG, Herkovits J (2009) Comparative susceptibility to atrazine of three developmental stages of Rhinella arenarum and influence on metamorphosis: non-monotonous acceleration of the time to climax and delayed tail resorption. Aquat Toxicol 91:161–170
Candioti JV, Natale GS, Soloneskia S, Ronco AE, Larramendy ML (2010) Sublethal and lethal effects on Rhinella arenarum (Anura, Bufonidae) tadpoles exerted by the pirimicarb-containing technical formulation insecticide Aficida®. Chemosphere 78:249–255
Carneiro FF, Rigotto RM, Augusto LGS, Friedrich C, Búrigo AC (2015) Dossiê ABRASCO : um alerta sobre os impactos dos agrotóxicos na saúde. Expressão Popular, EPSJV, Rio de Janeiro, São Paulo, http://www.abrasco.org.br/dossieagrotoxicos/wp-content/uploads/2013/10/DossieAbrasco_2015_web.pdf Accessed 01 Aug 2017
Chung SW, Gu RR (2003) Estimating time-variable transformation rate of atrazine in a reservoir. Adv Environ Res 7:933–947
Damalas CA, Eleftherohorinos IG (2011) Pesticide exposure, safety issues, and risk assessment indicators. Int J Environ Res Public Health 8:1402–1419
EPA. United States Environmental Protection Agency. Available at http://www.epa.gov/pesticides. Accessed 01 Aug 2017
Ezemonye L, Tongo I (2009) Lethal and sublethal effects of atrazine to amphibian larvae. Jordan J Biol Sci 2:29–36
Ferracini VI, Pessoa MCYP, Silva AD, Spadotto CA (2001) Risk analysis of contamination of ground water and surface waters of Petrolina (PE) and Juazeiro (BA). R Ecotoxicol 11:1–16
Frost DR (2017) Amphibian Species of the World: Online Reference. Version 6.0 http://research.amnh.org/herpetology/amphibia/index.html. Accessed 01 Aug 2017
Gerónimo E, Aparicio VC, Bárbaro S, Portocarrero R, Sebastián J, Costa JL (2014) Presence of pesticides in surface water from four sub-basins in Argentina. Chemosphere 107:423–431
GHS (2011) Globally Harmonized System of Classification and Labelling of Chemicals. United Nations, New York and Geneva
Gosner K (1960) A simplified table for staging Anuran Embryos and larvae with notes on identification. Herpetologica 16:183–189
Greulich K, Pflugmacher S (2003) Differences in susceptibility of various life stages of amphibians to pesticide exposure. Aquat Toxicol 65:329–336
Grizolia CK (2005) Agrochemical mutations, cancer and reproduction. UNB, Brasília
Hayes TB, Collins A, Lee M, Mendonza M, Noriega N, Stuart AA, Vonk A (2002) Hermaphroditic, demasculinized frogs after exposure to the herbicide atrazine at low ecologically relevant doses. Proc Natl Acad Sci USA 99:5476–5480.
Hayes T, Haston K, Tsui M, Hoang A, Haeffele C, Vonk A (2003) Atrazine-induced hermaphroditism at 0.1 ppb in American leopard frogs (Rana pipiens): laboratory and field evidence. Environ Health Perspect 111:568–575
Herrero-Hernández E, Andrades MS, Marín-Benito JM, Sánchez-Martín MJ, Rodríguez-Cruz MS (2011) Field-scale dissipation of tebuconazole in a vineyard soil amended with spent mushroom substrate and its potential environmental impact. Ecotoxicol Environ Safe 6:1480–1488.
Howe GE, Gillis R, MowbraY RC (1998) Effect of chemical synergy and larval stage on the toxicity of atrazina and alachlor to amphibian larvae. Environ Toxicol Chem 17:519–525
IBAMA (2010) Brazilian Institute of Environment and Renewable Natural Resources. Pesticides and related products marketed in 2009 in Brazil: an environmental approach. www.ibama.gov.br/areas-tematicas-qa/relatorios-de-comercialzaçao-de-agrotoxicos/pagina2. Accessed 01 Aug 2017
IBAMA (2014) Brazilian Institute of Environment and Renewable Natural Resources Pesticides and related products marketed in 2014 in Brazil. http://www.ibama.gov.br/agrotoxicos/relatorios-de-comercializacao-de-agrotoxicos. Accessed 01 Aug 2017
Izaguirre MF, Lajmanovich RC, Peltzer PM, Soler AP, Casco VH (2000) Cypermethrin-induced apoptosis in thetelencephalon of Physalaemus biligonigerus tadpoles (Anura: Leptodactylidae). Bull Environ Contam Toxicol 65:501–507
Izaguirre MF, Lajmanovich RC, Peltzer PM, Peralta Soler A, Casco VH (2001) Induction of cell death by the synthetic pyrethroid insecticide cypermethrin in the developing brain of Physalaemus biligonigerus tadpoles from Argentina. Froglog 43:3–4
Izaguirre MF, Marín L, Vergara MN, Lajmanovich RC, Peltzer PM, Casco VH (2006a) Experimental models of anurans to study pyrethroid effects. Cienc, Docencia Tecnol 32:181–206
Izaguirre MF, Vergara MN, Casco VH (2006b) CAS role in the brain apoptosis of Bufo arenarum induced by Cypermethrin. Biocell 30:309–320
Jardim ANO, Caldas ED (2012) Brazilian monitoring programs for pesticide residues in food e results from 2001 to 2010. Food Control 25:607
Kreutz LC, Barcellos LJG, Silva TO, Anziliero D, Martins D, Lorenson M, Marteninghe A, Silva LB (2008) Acute toxicity test of agricultural pesticides on silver catfish (Rhamdiaquelen) fingerlings. Ciênc Rural 38:1050–1055
Macagnan N, Rutkoski CF, Kolcenti C, Vanzetto VV, Macagnan L, Sturza P, Hartmann PA, Hartmann MT (2017) Toxicity of cypermethrin and deltamethrin insecticides on embryos and larvae of Physalaemus gracilis (Anura:Leptodactylidae). Environ Sci Pollut Res https://doi.org/10.1007/s11356-017-9727-5
Marino D, Ronco EA (2005) Cypermethrin and chlorpyrifos concentration levels in surface water bodies of the Pampa Ondulada, Argentina. Bull Environ Contam Toxicol 75(4):820–826
Montanha FP, Pimpão CT (2012) Toxicological effects of pyrethroids (cypermethrin and deltamethrin) on fish—Review. Rev Cient Elet Med Vet 18:1–58
Moreira JC, Peres F, Simões AC, Pignati WA, Dores EC, Vieira SN, Strüssmann C, Mott T (2012) Contaminação de águas superficiais e de chuva por agrotóxicos em uma região do estado do Mato Grosso Ciência e Saúde Coletiva 17:1557–1568
Moutinho MF (2013) Comparative ecotoxicity of sugar cane herbicides for amphibian larvae. Dissertation, Universidade de São Paulo
Peltzer PM, Junges CM, Attademo AM, Bassó A, Grenón P, Lajmanovich RC (2013) Cholinesterase activities and behavioral changes in Hypsiboas pulchellus (Anura: Hylidae) tadpoles exposed to glufosinate ammonium herbicide. Ecotoxicology 22:1165–1173
Pérez Iglesias JM (2015) Exposure and effect biomarkers to assess the effects of atrazine at different levels on neotropical anthill tadpoles. Dissertation, Universidade Estadual Paulista Julio de Mesquita Filho
Pignati W, Pereira N, Cândido A (2014) Vigilância aos agrotóxicos: quantificação do uso e previsão de impactos na saúde-trabalho-ambiente para os municípios brasileiros. Ciência Saúde Coletiva 19:4669–4678
Saha S, Kaviraj A (2009) Effects cypermethrin on some biochemical parameters and its amelioration through dietary supplementation os ascorbic acid in freshwater catfish Heteropneustes fossilis. Chemosphere 74:1254–1259
Sancho E, Villarroel MJ, Fernández C, Andreu E, Ferrando MD (2010) Short-term exposure to sublethal tebuconazole induces physiological impairment in male zebrafish (Danio rerio). Ecotoxicol Environ Saf 73:370–376
Sancho E, Villarroel MJ, Ferrando MD (2016) Assessment of chronic effects of tebuconazole on survival, reproduction and growth of Daphnia magna after different exposure times. Ecotoxicol Environ Saf 124:10–17.
Sass JB, Colangelo A (2006) European Union bans Atrazine, while the United States negotiates continued use. Int J Occup Environ Health 12:260–267
Schottler SP, Eisenreich SJ (1997) Mass balance model to quantify atrazina sources, transformation rates, and trends in the Great Lakes. Environ Sci Technol 31:2616–2625
Silva JF, Ferreira LR, Ferreira FA (2007) Herbicides: absorption, translocation, metabolism, formulation and mixtures. In: Silva AA, Silva JF (eds) Topics in weed management. Universidade Federal de Viçosa, Viçosa, Brazil, p 367
Silva HSVP, Loiola C, Pereira SRF, Santos RL, Andrade GV, Nunes SG (2013) Acute toxicity and genotoxicity of Folisuper 600BR commercial pesticide to tadpoles of Physalaemus cuvieri (Anura: Leiuperidae). Pestic: R Ecotoxicol 23:1–10
Silvano DL, Segalla MV (2005) Conservation of amphibians in Brazil. Mega Divers 1:79–86
Silva FR, Santos RS, Nunes M, Rossa-Feres DC (2009) Anuran captured in pitfall traps in three agrossystem in Northwestern São Paulo State, Brazil. Biota Neotrop 9:253–255
Singh PB, Singh V (2008) Cypermethrin induced histological changes in gonadotrophic cells, liver, gonads, plasma levels of estradiol-17β and 11-ketotestosterone, and sperm motility in Heteropneustes fossilis (Bloch). Chemosphere 72:422–431
Smalling KL, Reeves R, Muths E, Vandever M, Battaglin WA, Hladik ML, Pierce CL (2015) Pesticides concentrations is frog tissue and wetland habitats in a landscape dominated by agriculture. Sci Total Environ 502:80–90
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
Sparling DW, Linder G, Bishop CA, Krest SK (2010) Ecotoxicology of Amphibians and Reptiles. CRC Press, SETAC Books, New York
Svartz G, Meijide F, Coll CP (2016) Effects of a fungicide formulation on embryo-larval development, metamorphosis, and gonadogenesis of the South American toad Rhinella arenarum. Environ Toxicol Pharmacol 45:1–7. https://doi.org/10.1016/j.etap.2016.05.008
Svartz GV, Herkovits J, Pérez-Coll CS (2012) Sublethal effects of atrazine on embryo-larval development of Rhinella arenarum (Anura: Bufonidae). Ecotoxicology 21:1251
Svartz GV, Pérez-Coll, CS (2013) Comparative toxicity of cypermethrin and a commercial formulation on Rhinella arenarum larval development (Anura: Bufonidae). Int. J. Environ Health 6. https://doi.org/10.1504/IJENVH.2013.056973
Tavera-Mendoza L, Ruby S, Brousseau P, Fournier M, Cyr D, Marcogliese D (2002a) Response of the amphibian tadpole (Xenopus laevis) to atrazine during sexual differentiation of the testis. Environ Toxicol Chem 21:527–531
Tavera-Mendoza L, Ruby S, Brousseau P, Fournier M, Cyr D, Marcogliese D (2002b) Response of the amphibian tadpole (Xenopus laevis) to atrazine during sexual differentiation of the ovary. Environ Toxicol Chem 21:1264–1267
Toni C, Ferreira D, Kreutz LC, Loro VL, Barcellos LJG (2011) Assessment of oxidative stress and metabolic changes in common carp (Cyprinus carpio) acutely exposed to diferente concentrations of the fungicide tebuconazole. Chemosphere 83:579–584
Vieira EFS, Cestari AR, Chagas RA, Cortes GKR (2014) Collection and characterization of suitable matrix for long-release systems—release studies of Atrazine and Diuron herbicides. Quim Nova 37:398–403
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Wrubleswski, J., Reichert, F.W., Galon, L. et al. Acute and chronic toxicity of pesticides on tadpoles of Physalaemus cuvieri (Anura, Leptodactylidae). Ecotoxicology 27, 360–368 (2018). https://doi.org/10.1007/s10646-018-1900-1
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DOI: https://doi.org/10.1007/s10646-018-1900-1