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DNA damage exerted by mixtures of commercial formulations of glyphosate and imazethapyr herbicides in Rhinella arenarum (Anura, Bufonidae) tadpoles

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Abstract

Glyphosate (GLY) and imazethapyr (IMZT) are two herbicides commonly used worldwide, either alone or in mixtures. They represent key pesticides in modern agricultural management. The toxicity that results when employed as mixtures has not been characterized so far. Acute toxicity of the 48% GLY-based herbicide (GBH) Credit® and the 10.59% IMZT-based herbicide (IBH) Pivot® H alone and their binary combinations was analyzed in Rhinella arenarum tadpoles exposed in a semi-static renewal test. Lethal effects were determined using mortality as the end-point, whereas sublethal effects were determined employing the single-cell gel electrophoresis (SCGE) bioassay. Based on mortality experiments, results revealed LC5096 h values of 78.18 mg/L GBH and 0.99 mg/L IBH for Credit® and Pivot® H, respectively. An increase in the genetic damage index (GDI) was found after exposure to Credit® or Pivot® H at 5 and 10% of LC5096 h values. The combinations of 5% Credit®-5% Pivot® H LC5096 h and 10% Credit®-10% Pivot® H LC5096 h concentrations significantly enhanced the GDI in comparison with tadpoles exposed only to Credit® or Pivot® H. Thus, the effect of interaction between GBH and IBH inducing DNA damage in R. arenarum blood cells can be considered to be synergistic.

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References

  • Agostini MG, Natale GS, Ronco AE (2009) Impact of endosulphan and cypermethrin mixture on amphibians under field use for biotech soya bean production. Int J Environ Health 3:379–389

    Article  CAS  Google Scholar 

  • ASIH (2004) Guidelines for Use of Live Amphibians and Reptiles in Field and Laboratory Research. Herpetological Animal Care and Use Committee of the American Society of Ichthyologists and Herpetologists, Washington, DC

    Google Scholar 

  • Baas J, Stefanowicz AM, Klimek B, Laskowski R, Kooijman SA (2010) Model-based experimental design for assessing effects of mixtures of chemicals. Environ Pollut 158:115–120

    Article  CAS  Google Scholar 

  • Babini MS, Bionda CdL, Salas NE, Martino AL (2016) Adverse effect of agroecosystem pond water on biological endpoints of common toad (Rhinella arenarum) tadpoles. Environ Monit Asses 188:459

    Article  CAS  Google Scholar 

  • Beebee TJ (2005) Conservation genetics of amphibians. Heredity 95:423–427

    Article  CAS  Google Scholar 

  • Belden J, McMurry S, Smith L, Reilley P (2010) Acute toxicity of fungicide formulations to amphibians at environmentally relevant concentrations. Environ Toxicol Chem 29:2477–2480

    Article  CAS  Google Scholar 

  • Belden JB, Lydy MJ (2000) Impact of atrazine on organophosphate insecticide toxicity. Environ Toxicol Chem 19:2266–2274

    Article  CAS  Google Scholar 

  • Bielecki K, Sarapuk J, Kleszczyńsk H (2004) Binary mixtures of (N-phosphonomethyl)-glycine with new aminophosphonates. Z Naturforsch C 59:515–518

    Article  CAS  Google Scholar 

  • Bindraban PS, Franke AC, Ferraro DO, Ghersa CM, Lotz LAP, Nepomuceno A, Smulders MJM, van de Wiel CCM (2009) GM-Related sustainability: agro-ecological impacts, risks and opportunities of Soy production in Argentina and Brazil. Plant Res Internat B V Wageningen Rep 259, 1–45

  • Blouin D, Webster E, Bond J (2010) On a method of analysis for synergistic and antagonistic joint-action effects with fenoxaprop mixtures in rice (Oryza sativa). Weed Technol 24:583–589

    Article  CAS  Google Scholar 

  • Bolognesi C, Bonatti S, Degan P, Gallerani E, Peluso M, Rabboni R, Roggieri P, Abbondandolo A (1997) Genotoxic activity of glyphosate and its technical formulation Roundup. J Agric Food Chem 45:1957–1962

    Article  CAS  Google Scholar 

  • Bradford DF, Knapp RA, Sparling DW, Nash MS, Stanley KA, Tallent-Halsell NG, McConnell LL, Simonich SM (2011) Pesticide distributions and population declines of California, USA, alpine frogs, Rana muscosa and Rana sierrae. Environ Toxicol Chem 30:682–691

    Article  CAS  Google Scholar 

  • Brodeur JC, Melpel S, Anglesio AB, Cristos D, D’Andrea MA, Poliserpi MB (2016) Toxicities of glyphosate- and cypermethrin-based pesticides are antagonic in the tenspotted livebearer fish (Cnesterodon decemmaculatus). Chemosphere 155:429–435

    Article  CAS  Google Scholar 

  • Brodeur JC, Poliserpi MB, D’Andrea MF, Sanchez M (2014) Synergy between glyphosate- and cypermethrin-based pesticides during acute exposures in tadpoles of the common South American toad Rhinella arenarum. Chemosphere 112:70–76

    Article  CAS  Google Scholar 

  • Brooks TM, Akçakaya HR, Burgess ND, Butchart SH, Hilton-Taylor C, Hoffmann M, Juffe-Bignoli D, Kingston N, MacSharry B, Parr M, Perianin L, Regan EC, Rodrigues AS, Rondinini C, Shennan-Farpon Y, Young BE (2016) Analysing biodiversity and conservation knowledge products to support regional environmental assessments. Sci Data 3:160007

    Article  Google Scholar 

  • Brühl CA, Pieper S, Weber B (2011) Amphibians at risk? Susceptibility of terrestrial amphibian life stages to pesticides. Environ Toxicol Chem 30:2465–2472

    Article  CAS  Google Scholar 

  • Calabrese EJ (1995) Toxicological consequences of multiple chemical interactions: a primer. Toxicology 105:121–135

    Article  CAS  Google Scholar 

  • CASAFE (2017) Guía de Productos Fitosanitarios para la República Argentina. Cámara de Sanidad Agropecuaria y Fertilizantes, Buenos Aires

    Google Scholar 

  • Castro Berman M, Marino DJ, Quiroga MA, Zagarese H (2018) Occurrence and levels of glyphosate and AMPA in shallow lakes from the Pampean and Patagonian regions of Argentina. Chemosphere 200:513–522

    Article  CAS  Google Scholar 

  • Çavaş T, Konen S (2007) Detection of cytogenetic and DNA damage in peripheral erythrocytes of goldfish (Carassius auratus) exposed to a glyphosate formulation using the micronucleus test and the comet assay. Mutagenesis 22:263–268

    Article  CAS  Google Scholar 

  • Cedergreen N, Streibig JC (2005) The toxicity of herbicides to non-target aquatic plants and algae: assessment of predictive factors and hazard. Pest Manag Sci 61:1152–1160

    Article  CAS  Google Scholar 

  • Cei JM (1980) Amphibians of Argentina. Monitore Zoologico Italiano. New Ser Monogr 2:1–609

  • Egea-Serrano A, Relyea RA, Tejedo M, Torralva M (2012) Understanding of the impact of chemicals on amphibians: a meta-analytic review. Ecol Evol 2:1382–1397

    Article  Google Scholar 

  • Feng S, Kong Z, Wang X, Zhao L, Peng P (2004) Acute toxicity and genotoxicity of two novel pesticides on amphibian, Rana N. Hallowell. Chemosphere 56:457–463

    Article  CAS  Google Scholar 

  • Ficetola GF, Maiorano L (2016) Contrasting effects of temperature and precipitation change on amphibian phenology, abundance and performance. Oecologia 181:683–693

    Article  Google Scholar 

  • Finney DJ (1971) Probit Analysis. Cambridge University Press., London

    Google Scholar 

  • Furlong ET, Anderson BD, Werner SL, Soliven PP, Coffey LJ, Burkhardt MR (2011) Methods of analysis but the US Geological Survey National Water Quality Laboratory—Determination of Pesticides in Water by Graphitized Carbon-based Solid-Phase Extraction and High-Performance Liquid Chromatography/Mass Spectrometry. US Geological Survey Water Resources Investigations Report 01-4134: 73.

  • Ge H, Lin Z, Yao Z, Gao Z, Cong Y, Yu H (2014) Balance between herbicidal activity and toxicity effect: a case study of the joint effects of triazine and phenylurea herbicides on Selenastrum capricornutum and Photobacterium phosphoreum. Aquat Toxicol 150:165–174

    Article  CAS  Google Scholar 

  • Giesy JP, Dobson S, Solomon KR (2000) Ecotoxicological risk assessment for Roundup herbicide. Rev Environ Contam Toxicol 167:35–120

    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 

  • Grisolia CK, Bilich MR, Formigli LM (2004) A comparative toxicologic and genotoxic study of the herbicide arsenal, its active ingredient imazapyr, and the surfactant nonylphenol ethoxylate. Ecotoxicol Environ Safe 59:123–126

    Article  CAS  Google Scholar 

  • Güngördü A, Uçkun M, Yoloğlu E (2016) Integrated assessment of biochemical markers in premetamorphic tadpoles of three amphibian species exposed to glyphosate- and methidathion-based pesticides in single and combination forms. Chemosphere 144:2024–2035

    Article  CAS  Google Scholar 

  • Hensel R (1867) Beiträge zur Kenntnis der Wirbelthiere Südbrasilens. Arch Naturgesch 33:120–162

  • IARC (2017) Monographs on the Evaluation of Carcinogenic Risk of Chemicals to Man. Some Organophosphate Insecticides and Herbicides. International Agency for Research on Cancer, Lyon

    Google Scholar 

  • Ippolito A, Kattwinkel M, Rasmussen JJ, Schafer RB, Fornaroli R, Liess M (2015) Modeling global distribution of agricultural insecticides in surface waters. Environ Pollut 198:54–60

    Article  CAS  Google Scholar 

  • Jones DK, Hammond J, Relyea RA (2010) Roundup® and amphibians: the importance of concentration, application time, and stratification. Environ Toxicol Chem 29:2016–2025

    CAS  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

    Article  CAS  Google Scholar 

  • Kehr AI (1987) Crecimiento individual de larvas de Hyla pulchella pulchella y Bufo fernandezae en condiciones controladas de coexistencia y densidad (Amphibia: anura). Cuad Herpetol 3:1–6

    Google Scholar 

  • Kehr AI (1989) Factores dependientes de la densidad y su influencia sobre el crecimiento individual de los estado de Hyla pulchella pulchella (Amphibia: Anura). Limnobios 2:757–761

    Google Scholar 

  • Kwet A, Reichle S, Silvano D, Úbeda C, Baldo D, Di Tada I (2004) Rhinella arenarum The International Union for Conservation of Nature. List Threat Species 2004:e.T54576A11169255

    Google Scholar 

  • Lajmanovich RC, Attademo AM, Peltzer PM, Junges CM, Cabagna MC (2011) Toxicity of four herbicide formulations with glyphosate on Rhinella arenarum (Anura: Bufonidae) tadpoles: B-esterases and glutathione S-transferase inhibitors. Arch Environ Contam Toxicol 60:681–689

    Article  CAS  Google Scholar 

  • Larramendy ML (2017a) Ecotoxicology and Genotoxicology: Non-traditional Aquatic Models. The Royal Society of Chemistry, Cambridge, p 538

    Book  Google Scholar 

  • Larramendy ML (2017b) Ecotoxicology and Genotoxicology: Non-Traditional Terrestrial Models. The Royal Society of Chemistry, Cambridge, p 321

    Book  Google Scholar 

  • LeBlanc GA, Wang G (2006) Chemical Mixtures: Greater-than-Additive Effects? Environ Health Perspect 114:A517–A518

    Article  Google Scholar 

  • Liaud C, Brucher M, Schummer C, Coscolla C, Wolff H, Schwartz J, Yusa V, Millet M (2016) Utilization of long duration high-volume sampling coupled to SPME-GC-MS/MS for the Assessment of airborne pesticides variability in an urban area (Strasbourg, France) during agricultural applications. J Environ Sci Health 0:1–12

    Google Scholar 

  • Lydy M, Belden J, Wheelock C, Hammock B, Denton D (2004) Challenges in regulating pesticide mixtures. Ecol Soc 9:1–13

    Article  Google Scholar 

  • Mann RM, Bidwell JR (1999) The toxicity of glyphosate and several glyphosate formulations to four species of southwestern Australian frogs. Arch Environ Contam Toxicol 36:193–199

    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

    Article  CAS  Google Scholar 

  • Maselli V, Polese G, Rippa D, Ligrone R, Rastogi RK, Fulgione D (2010) Frogs, sentinels of DNA damage induced by pollution in Naples and the neighbouring provinces. Ecotoxicol Environ Saf 73:1525–1529

    Article  CAS  Google Scholar 

  • Mattice JD, Smartt A, Scott T, Norman RJ (2012) Environmental implications of pesticides in rice production. In: Norman RJ, Moldenhauer KAK (Eds.) Rice Research Studies 2011. Arkansas Agricultural Experiment Station, University of Arkansas System Division of Agriculture, Fayetteville, Arkansas, p 165–175

    Google Scholar 

  • Mazzatorta P, Benefenati E, Neagu D, Gini G (2002) The importance of scaling in data mining for toxicity prediction. J Chem Inf Model 42:1250–1255

    CAS  Google Scholar 

  • Meffe R, de Bustamante I (2014) Emerging organic contaminants in surface water and groundwater: a first overview of the situation in Italy. Sci Total Environ 481:280–295

    Article  CAS  Google Scholar 

  • Meza-Joya FL, Ramírez-Pinilla MP, Fuentes-Lorenzo JL (2013) Toxic, cytotoxic, and genotoxic effects of a glyphosate formulation (Roundup®SL-Cosmoflux®411F) in the direct-developing frog Eleutherodactylus johnstonei. Environ Mol Mutagen 54:362–373

    Article  CAS  Google Scholar 

  • Moore LJ, Fuentes L, Rodgers JHJ, Bowerman WW, Yarrow GK, Chao WY, Bridges WCJ (2012) Relative toxicity of the components of the original formulation of Roundup to five North American anurans. Ecotoxicol Environ Saf 78:128–133

    Article  CAS  Google Scholar 

  • Moraes BS, Clasen B, Loro VL, Pretto A, Toni C, de Avila LA, Marchesan E, Machado SL, Zanella R, Reimche GB (2011) Toxicological responses of Cyprinus carpio after exposure to a commercial herbicide containing imazethapyr and imazapic. Ecotoxicol Environ Saf 74:328–335

    Article  CAS  Google Scholar 

  • Mouchet F, Baudrimont M, Gonzalez P, Cuenot Y, Bourdineaud JP, Boudou A, Gauthier L (2006a) Genotoxic and stress inductive potential of cadmium in Xenopus laevis larvae. Aquat Toxicol 78:157–166

    Article  CAS  Google Scholar 

  • Mouchet F, Gauthier L, Baudrimont M, Gonzalez P, Mailhes C, Ferrier V, Devaux A (2007) Comparative evaluation of the toxicity and genotoxicity of cadmium in amphibian larvae (Xenopus laevis and Pleurodeles waltl) using the comet assay and the micronucleus test. Environ Toxicol 22:422–435

    Article  CAS  Google Scholar 

  • Mouchet F, Gauthier L, Mailhes C, Ferrier V, Devaux A (2006b) Comparative evaluation of genotoxicity of captan in amphibian larvae (Xenopus laevis and Pleurodeles waltl) using the comet assay and the micronucleus test. Environ Toxicol 21:264–277

    Article  CAS  Google Scholar 

  • Natale GS, Ammassari LL, Basso NG, Ronco AE (2006) Acute and chronic effects of Cr(VI) on Hypsiboas pulchellus embryos and tadpoles. Dis Aquat Organ 72:261–267

    Article  CAS  Google Scholar 

  • Natale GS, Vera-Candioti J, Ruiz de Arcaute C, Soloneski S, Larramendy ML, Ronco AE (2018) Lethal and sublethal effects of the pirimicarb-based formulation Aficida® on Boana pulchella (Duméril and Bibron, 1841) tadpoles (Anura, Hylidae). Ecotoxicol Environ Saf 147:471–479

    Article  CAS  Google Scholar 

  • Nikoloff N, Larramendy ML, Soloneski S (2014a) Comparative evaluation of the in vitro micronucleus and comet assay for evaluation of fluorochloridone-induced genotoxicity. Environ Toxicol 29:884–892

    Article  CAS  Google Scholar 

  • Nikoloff N, Natale GS, Marino D, Soloneski S, Larramendy ML (2014b) Flurochloridone-based herbicides induced genotoxicity effects on Rhinella arenarum tadpoles (Anura: Bufonidae). Ecotoxicol Environ Saf 100:275–281

    Article  CAS  Google Scholar 

  • Olszyk D, Pfleeger T, Lee EH, Plocher M (2015) Glyphosate and dicamba herbicide tank mixture effects on native plant and non-genetically engineered soybean seedlings. Ecotoxicology 24:1014–1027

    Article  CAS  Google Scholar 

  • Peixoto F (2005) Comparative effects of the Roundup and glyphosate on mitochondrial oxidative phosphorylation. Chemosphere 61:1115–1122

    Article  CAS  Google Scholar 

  • Peluso F, González Castelain J, Varela C, Usunoff E (2008) Evaluación preliminar del riesgo sanitario por agroquímicos en aguas del Arroyo Azul, provincia de Buenos Aires. Biol Acuát 24:123–130

    Google Scholar 

  • Pereira JL, Antunes SC, Castro BB, Marques CR, Gonçalves AMM, Gonçalves F, Pereira R (2009) Toxicity evaluation of three pesticides on non-target aquatic and soil organisms: commercial formulation versus active ingredient. Ecotoxicology 18:455–463

    Article  CAS  Google Scholar 

  • Pérez-Iglesias JM, Natale GS, Soloneski S, Larramendy ML (2018) Are the damaging effects induced by the imazethapyr herbicide formulation Pivot® H in Boana pulchella (Anura, Hylidae) reversible upon ceasing exposure? Ecotoxicol Environ Saf 148:1–10

    Article  CAS  Google Scholar 

  • Pérez-Iglesias JM, Ruiz de Arcaute C, Natale GS, Soloneski S, Larramendy ML (2017) Evaluation of imazethapyr-induced DNA oxidative damage by alkaline Endo III-and Fpg-modified single-cell gel electrophoresis assay in Hypsiboas pulchellus tadpoles (Anura, Hylidae). Ecotoxicol Environ Saf 142:503–508

    Article  CAS  Google Scholar 

  • Pérez-Iglesias JM, Ruiz de Arcaute C, Nikoloff N, Dury L, Soloneski S, Natale GS, Larramendy M (2014) The genotoxic effects of the imidacloprid-based insecticide formulation Glacoxan Imida on Montevideo tree frog Hypsiboas pulchellus tadpoles (Anura, Hylidae). Ecotoxicol Environ Saf 104:120–126

    Article  CAS  Google Scholar 

  • Pérez-Iglesias JM, Soloneski S, Nikoloff N, Natale GS, Larramendy ML (2015) Toxic and genotoxic effects of the imazethapyr-based herbicide formulation Pivot H® on montevideo tree frog Hypsiboas pulchellus tadpoles (Anura, Hylidae). Ecotoxicol Environ Saf 119:15–24

    Article  CAS  Google Scholar 

  • Peruzzo PJ, Porta AA, Ronco AE (2008) Levels of glyphosate in surface waters, sediments and soils associated with direct sowing soybean cultivation in north pampasic region of Argentina. Environ Pollut 156:61–66

    Article  CAS  Google Scholar 

  • Pettersson M, Ekelund NGA (2006) Effects of the herbicides Roundup and Avans on Euglena gracilis. Arch Environ Contam Toxicol 50:175–181

    Article  CAS  Google Scholar 

  • Pimentel D (1995) Amounts of pesticides reaching target pests: Environmental impacts and ethics. J Agric Environ Ethics 8:17–29

    Article  Google Scholar 

  • Pitarque M, Creus A, Marcos R, Hughes AA, Anderson D (1999) Examination of various biomarkers measuring genotoxic endpoints from Barcelona airport personnel. Mutat Res 440:195–204

    Article  CAS  Google Scholar 

  • PPDB (2014) Imazethapyr (Ref: AC 252925). Pesticide Properties DataBase. http://sitem.herts.ac.uk/aeru/ppdb/en/Reports/395.htm (accessed 10.12.2018)

  • Ralph S, Petras M (1998) Caged amphibian tadpoles and in situ genotoxicity monitoring of aquatic environments with the alkaline single cell gel electrophoresis (comet) assay. Mutat Res 413:235–250

    Article  CAS  Google Scholar 

  • Rodney SI, Teed RS, Moore DRJ (2013) Estimating the toxicity of pesticide mixtures to aquatic organisms: A review. Hum Ecol Risk Assess 19:1557–1575

    Article  CAS  Google Scholar 

  • Ruiz de Arcaute C, Pérez-Iglesias JM, Nikoloff N, Natale GS, Soloneski S, Larramendy ML (2014) Genotoxicity evaluation of the insecticide imidacloprid on circulating blood cells of Montevideo tree frog Hypsiboas pulchellus tadpoles (Anura, Hylidae) by comet and micronucleus bioassays. Ecol Indic 45:632–639

    Article  CAS  Google Scholar 

  • Ruiz de Arcaute C, Soloneski S, Larramendy ML (2018) Synergism of binary mixtures of dicamba and 2,4-dichlorophenoxyacetic acid herbicide formulations on the ten spotted live-bearer fish Cnesterodon decemmaculatus (Pisces, Poeciliidae). Environ Pollut 236:33–39

    Article  CAS  Google Scholar 

  • Santos MJ, Morgado R, Ferreira NG, Soares AM, Loureiro S (2011) Evaluation of the joint effect of glyphosate and dimethoate using a small-scale terrestrial ecosystem. Ecotoxicol Environ Saf 74:1994–2001

    Article  CAS  Google Scholar 

  • Silva AR, Cardoso DN, Cruz A, Lourenco J, Mendo S, Soares AM, Loureiro S (2015) Ecotoxicity and genotoxicity of a binary combination of triclosan and carbendizim to Daphnia magna. Ecotoxicol Environ Saf 115:279–290

    Article  CAS  Google Scholar 

  • Singh NP (1996) Microgel electrophoresis of DNA from individual cells: principles and methodology. In: Pfeifer GP (Ed.) Technologies for Detection of DNA Damage and Mutations. Plenum Press, New York, NY, p 3–24

    Chapter  Google Scholar 

  • Sobrero MC, Rimoldi F, Ronco AE (2007) Effects of the glyphosate active ingredient and a formulation on Lemna gibba L. at different exposure levels and assessment end-points. Bull Environ Contam Toxicol 79:537–543

    Article  CAS  Google Scholar 

  • Soloneski S, González NV, Reigosa MA, Larramendy ML (2007) Herbicide 2,4-dichlorophenoxyacetic acid (2,4-D)-induced cytogenetic damage in human lymphocytes in vitro in presence of erythrocytes. Cell Biol Int 31:1316–1322

  • Soloneski S, Larramendy ML (2010) Sister chromatid exchanges and chromosomal aberrations in Chinese hamster ovary (CHO-K1) cells treated with insecticide pirimicarb. J Hazard Mater 174:410–415

    Article  CAS  Google Scholar 

  • Soloneski S, Ruiz de Arcaute C, Larramendy ML (2016) Genotoxic effect of a binary mixture of dicamba- and glyphosate-based commercial herbicide formulations on Rhinella arenarum (Hensel, 1867) (Anura, Bufonidae) late-stage larvae. Environ Sci Pollut Res 23:17811–17821

    Article  CAS  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 28:1696–1703

    Article  CAS  Google Scholar 

  • Svartz GV, Aronzon CM, Perez Coll CS (2016) Combined endosulfan and cypermethrin-induced toxicity to embryo-larval development of Rhinella arenarum. J Toxicol Environ Health A 79:197–209

    Article  CAS  Google Scholar 

  • Tatum VL, Borton DL, Streblow WR, Louch J, Shepard JP (2012) Acute toxicity of commonly used forestry herbicide mixtures to Ceriodaphnia dubia and Pimephales promelas. Environ Toxicol 27:671–684

    Article  CAS  Google Scholar 

  • TOXNET (2017) Toxicology Data Nrtwork, National Institutes of Health, U.S. National Library of Medicine. Bethesda, MD. https://toxnet.nlm.nih.gov/cgi-bin/sis/search/a?dbs+hsdb:@term+@DOCNO+6678.

  • Tsui MTK, Chu LM (2003) Aquatic toxicity of glyphosate-based formulations: comparison between different organisms and the effects of environmental factors. Chemosphere 52:1189–1197

    Article  CAS  Google Scholar 

  • Tsui MTK, Chu LM (2008) Environmental fate and non-target impact of glyphosate-based herbicide (Roundup®) in a subtropical wetland. Chemosphere 71:439–446

    Article  CAS  Google Scholar 

  • UN (2011) Naciones Unidas. Peligros para el medio ambiente. Nac Unidas Parte 4:229–258

  • USEPA (1975) United States Environmental Protection Agency. Methods for Acute Toxicity Tests with Fish, Macroinvertebrates, and Amphibians. U.S. Government Printing Office 660/3-75-009, Washington, DC, p 62

    Google Scholar 

  • USEPA (1982) United States Environmental Protection Agency. Pesticide Assessment Guidelines Subdivision E. Hazard evaluation: wildlife and aquatic organisms U.S. Government Printing Office EPA-540/9-82-024, Washington, DC

    Google Scholar 

  • USEPA (1989) United States Environmental Protection Agency. Short-Term Methods for Estimating the Chronic Toxicity of Effluents and Receiving Waters to Aquatic Organisms. 2nd edition. Report No. EPA/600/4-89/001. U.S. Government Printing Office, Washington, DC

    Google Scholar 

  • USEPA (2002) United States Environmental Protection Agency. Methods for Measuring the Acute Toxicity of Effluents and Receiving Waters to Freshwater and Marine Organisms. Fifth edition. U.S. Government Printing Office 821-R-02-012, Washington, DC

    Google Scholar 

  • USEPA (2017) United States Environmental Protection Agency. Pesticide Science and Assessing Pesticide Risks. Technical Overview. Ecological Risk Assessment. U.S. Government Printing Office, Washington, DC, https://www.epa.gov/pesticide-science-and-assessing-pesticide-risks/technical-overview-ecological-risk-assessment-0#Ecotox

    Google Scholar 

  • Varona-Uribe ME, Torres-Rey CH, Diaz-Criollo S, Palma-Parra RM, Narvaez DM, Carmona SP, Briceño L, Idrovo AJ (2016) Exposure to pesticide mixtures and DNA damage among rice field workers. Arch Environ Occup Health 71:3–9

    Article  CAS  Google Scholar 

  • Vera-Candioti J, Natale GS, Soloneski 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

    Article  CAS  Google Scholar 

  • Wagner N, Lötters S, Veith M, Viertel B (2015) Effects of an environmentally relevant temporal application scheme of low herbicide concentrations on larvae of two anuran species. Chemosphere 135:175–181

    Article  CAS  Google Scholar 

  • Wagner N, Reichenbecher W, Teichmann H, Tappeser B, Lötters S (2013) Questions concerning the potential impact of glyphosate-based herbicides on amphibians. Environ Toxicol Chem 32:1688–1700

    Article  CAS  Google Scholar 

  • Warne MSJ (2003) A review of the ecotoxicity of mixtures, approaches to, and recommendations for their management. In: Langley A., Gilbey M., Kennedy B., (eds.), Proceedings of the Fifth National Workshop on the Assessment of Site Contamination. National Environment Protection Council Service Corporation, Adelaide, Australia, ​p 253–276

  • WHO-FAO (1997) Pesticides Residues in Food. World Health Organization and Food and Agriculture Organization of the United Nations, Report No. WHO/PCS/98.6, Rome. Vol 145, p 359

  • Yin XH, Li SN, Zhang L, Zhu GN, Zhuang HS (2008) Evaluation of DNA damage in Chinese toad (Bufo bufo gargarizans) after in vivo exposure to sublethal concentrations of four herbicides using the comet assay. Ecotoxicology 17:280–286

    Article  CAS  Google Scholar 

  • Zar JH (2010) Biostatistical Analysis, 5th edition. Prentice Hall, New Jersey, p 944

    Google Scholar 

  • Zhelev Z, Tsonev S, Georgieva K, Arnaudova D (2018) Health status of Pelophylax ridibundus (Amphibia: Ranidae) in a rice paddy ecosystem in Southern Bulgaria and its importance in assessing environmental state: haematological parameters. Environ Sci Pollut Res Int 25:7884–7895

    Article  CAS  Google Scholar 

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Acknowledgements

The current study has been included as whole chapter not subjected to peer review in the Doctoral Thesis presented by Wanessa Fernandes-Carvalho entitled “Genotoxic and mutagenic evaluation of herbicides in aquatic organisms” whose complete version is publicly available in the repository of the Universidade Federal de Goiás, Brazil (http://repositorio.bc.ufg.br/tede/handle/tede/8423). The authors acknowledge Guillermo S. Natale, Ph.D., for providing the R. arenarum specimens employed in the study. This study was supported by grants from the National University of La Plata (Grants 11/N817 and 11/N847), and the National Agency of Scientific and Technological Promotion (PICT 2015 Number 3059) from Argentina. W.F. Carvalho is the recipient of a fellowship from “Programa de Doutorado Sanduíche no Exterior (CAPES-PDSE-Edital no. 19/2016, Processo: 88881.135034-2016-01), who is also acknowledged.

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  1. These authors contributed equally: Wanessa F. Carvalho, Celeste Ruiz de Arcaute, Juan Manuel Pérez-Iglesias

Authors and Affiliations

  1. Cátedra de Citología, Facultad de Ciencias Naturales y Museo, Universidad Nacional de La Plata, Calle 64 N° 3, La Plata, 1900, Argentina

    Wanessa F. Carvalho, Celeste Ruiz de Arcaute, Juan Manuel Pérez-Iglesias, Milagros R. R. Laborde, Sonia Soloneski & Marcelo L. Larramendy

  2. Departamento de Genética, Instituto de Ciências Biológicas, Universidade Federal de Goiás, Goiânia, Brazil

    Wanessa F. Carvalho

  3. Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET), Buenos Aires, Argentina

    Celeste Ruiz de Arcaute, Juan Manuel Pérez-Iglesias, Sonia Soloneski & Marcelo L. Larramendy

  4. Agencia Nacional de Promoción Científica y Tecnológica (ANPCyT), Buenos Aires, Argentina

    Milagros R. R. Laborde

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  1. Wanessa F. Carvalho
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  2. Celeste Ruiz de Arcaute
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  3. Juan Manuel Pérez-Iglesias
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  4. Milagros R. R. Laborde
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  5. Sonia Soloneski
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  6. Marcelo L. Larramendy
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Correspondence to Marcelo L. Larramendy.

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Carvalho, W.F., Ruiz de Arcaute, C., Pérez-Iglesias, J.M. et al. DNA damage exerted by mixtures of commercial formulations of glyphosate and imazethapyr herbicides in Rhinella arenarum (Anura, Bufonidae) tadpoles. Ecotoxicology 28, 367–377 (2019). https://doi.org/10.1007/s10646-019-02029-x

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