Skip to main content
SpringerLink
Log in

An imazethapyr-based herbicide formulation induces genotoxic, biochemical, and individual organizational effects in Leptodactylus latinasus tadpoles (Anura: Leptodactylidae)

  • Research Article
  • Published:
Environmental Science and Pollution Research Aims and scope Submit manuscript

Abstract

Genotoxic, biochemical, and individual organizational effects on Leptodactylus latinasus tadpoles were evaluated after exposure to an imazethapyr (IMZT)-based commercial herbicide formulation, Pivot® H (10.59% IMZT). A determination of the value of the lethal concentration (LC50) was determined as a toxicological endpoint. Alterations in animal behavior and morphological abnormalities as well as cholinesterase (ChE), catalase (CAT), and glutathione S-transferase (GST) activities were employed as individual sublethal endpoints. Micronuclei frequencies (MNs), binucleated cells (BNs), blebbed nuclei (BLs), lobed nuclei (LBs), notched nuclei (NTs), erythroplastids (EPs), and evaluation of DNA strand breaks were employed as genotoxic endpoints. All biomarkers were evaluated after 48 and 96 h of exposure to concentrations of IMZT within 0.07–4.89 mg/L. LC5096h values of 1.01 and 0.29 mg/L IMZT were obtained for Gosner stages 25 and 36, respectively. Irregular swimming, diamond body shape, and decreased frequency of keratodonts were detected at both sampling times. Results showed that IMZT increased GST activity and MN frequency at 48 and 96 h of exposure. Other nuclear abnormalities were also observed in the circulating erythrocytes of tadpoles, i.e., NT and BL values after 48 h, and LN, BL, and EP values after 96 h. Finally, results showed that IMZT within 0.07–0.22 mg/L increased the genetic damage index in tadpoles exposed for both exposure times (48 and 96 h). This study is the first to report the sublethal biochemical effects of IMZT in anurans and is also the first report using L. latinasus tadpoles as a bioindicator for ecotoxicological studies.

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

Access this article

Log in via an institution

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.

Similar content being viewed by others

References

  • Agostini MG, Saibene PE, Roesler I, Bilenca D (2016) Amphibians of northwestern Buenos Aires province, Argentina: checklist, range extensions and comments on conservation. Check List 12:1998

  • Amiard-Triquet C, Amiard JC, Rainbow PS (2013) Ecological biomarkers: indicators of ecotoxicological effects. CRC Press, Boca Raton, 451

    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 ASIH. American Society of Ichthyologists and Herpetologists, Washington, DC

    Google Scholar 

  • ASTM (2007): Standard guide for conducting acute toxicity tests with fishes, macroinvertebrates, and amphibians. Biological effects and environmental fate. ASTM E 729-96

  • Ateeq B, Ali MN, Ahmad W (2002) Induction of micronuclei and erythrocyte alterations in the catfish Clarias batrachus by 2, 4-dichlorophenoxyacetic acid and butachlor. Mutat Res 518:135–144

    Article  CAS  Google Scholar 

  • Attademo AM, Peltzer PM, Lajmanovich RC, Cabagna-Zenklusen MC, Junges CM, Basso A (2014) Biological endpoints, enzyme activities, and blood cell parameters in two anuran tadpole species in rice agroecosystems of mid-eastern Argentina. Environ Monit Assess 186:635–649

    Article  CAS  Google Scholar 

  • Bach NC, Natale GS, Somoza GM, Ronco AE (2016) Effect on the growth and development and induction of abnormalities by a glyphosate commercial formulation and its active ingredient during two developmental stages of the South-American creole frog, Leptodactylus latrans. Environ Sci Pollut Res 23:23959–23971

    Article  CAS  Google Scholar 

  • Balmus G, Karp NA, Ling BN, Jackson SP, Adams DJ, McIntyre RE (2015) A high-throughput in vivo micronucleus assay for genome instability screening in mice. Nature Protoc 10:205–215

    Article  Google Scholar 

  • Bantle JA, Dumont JN, Finch RA, Linder G, Fort DJ (1998): Atlas of abnormalities: a guide for the performance of FETAX. Oklahoma State Publications Department, Stillwater

  • Barni S, Boncompagni E, Grosso A, Bertone V, Freitas I, Fasola M, Fenoglio C (2007) Evaluation of Rana snk esculenta blood cell response to chemical stressors in the environment during the larval and adult phases. Aquat Toxicol 81:45–54

    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, risk and opportunities of soy production in Argentina and Brazil. Wageningen, Plant Research International, 50

    Google Scholar 

  • Brodeur JC, Vera Candioti J (2017) Impacts of agriculture and pesticides on amphibian terrestrial life stages: potential biomonitor/bioindicator species for the Pampa Region of Argentina. In: Larramendy ML (ed) Ecotoxicology and genotoxicology: non-traditional terrestrial models. The Royal Society of Chemistry, Cambridge, pp 163–194

    Chapter  Google Scholar 

  • Brodeur JC, Suarez RP, Natale GS, Ronco AE, Zaccagnini ME (2011) Reduced body condition and enzymatic alterations in frogs inhabiting intensive crop production areas. Ecotoxicol Environ Saf 74:1370–1380

    Article  CAS  Google Scholar 

  • Brodeur JC, Sanchez M, Castro L, Rojas DE, Cristos D, Damonte MJ, Poliserpi MB, D'Andrea MF, Andriulo AE (2017) Accumulation of current-use pesticides, cholinesterase inhibition and reduced body condition in juvenile one-sided livebearer fish (Jenynsia multidentata) from the agricultural Pampa region of Argentina. Chemosphere 185:36–46

    Article  CAS  Google Scholar 

  • Brühl CA, Schmidt T, Pieper S, Alscher A (2013) Terrestrial pesticide exposure of amphibians: an underestimated cause of global decline? Sci Rep 3:1135

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • CASAFE (2017-2019) Guía de Productos Fitosanitarios para la República Argentina

  • Çavaş T, Ergene-Gözükara S (2003) Evaluation of the genotoxic potential of lambda-cyhalothrin using nuclear and nucleolar biomarkers on fish cells. Mutat Res 534:93–99

    Article  Google Scholar 

  • Çavaş T, Ergene-Gözükara S (2005) Induction of micronuclei and nuclear abnormalities in Oreochromis niloticus following exposure to petroleum refinery and chromium processing plant effluents. Aquat Toxicol 74:264–271

    Article  CAS  Google Scholar 

  • Çavaş T, Könen 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 

  • 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 

  • Ellman GL, Courtney KD, Andres V, Featherstone RM (1961) A new and rapid colorimetric determination of acetylcholinesterase activity. Biochem Pharmacol 7:88–95

    Article  CAS  Google Scholar 

  • Fenech M (2007) Cytokinesis-block micronucleus cytome assay. Nature Protoc 2:1084–1104

    Article  CAS  Google Scholar 

  • Fernandes TCC, Mazzeo DEC, Marin-Morales MA (2007) Mechanism of micronuclei formation in polyploidizated cells of Allium cepa exposed to trifluralin herbicide. Pest Biochem Physiol 88:252–259

    Article  CAS  Google Scholar 

  • Ferrari A, Anguiano L, Lascano C, Sotomayor V, Rosenbaum E, Venturino A (2008) Changes in the antioxidant metabolism in the embryonic development of the common South American toad Bufo arenarum: differential responses to pesticide in early embryos and autonomous-feeding larvae. J Biochem Mol Toxicol 22:259–267

    Article  CAS  Google Scholar 

  • Ferrari A, Lascano C, Pechen de D’Angelo AM, Venturino A (2011) Effects of azinphos methyl and carbaryl on Rhinella arenarum larvae esterases and antioxidant enzymes. Comp Biochem Physiol 153:34–39

    Google Scholar 

  • Glomski CA, Tamburlin J, Hard R, Chainani M (1997) The phylogenetic odyssey of the erythrocyte. IV. The amphibians. Histol Histopathol 12:147–170

    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 

  • Guerra C, Aráoz E (2016) Amphibian malformations and body condition across an agricultural landscape of northwest Argentina. Dis Aquat Organ 121:105–116

    Article  Google Scholar 

  • Hagger JA, Jones MB, Leonard DP, Owen R, Galloway TS (2006) Biomarkers and integrated environmental risk assessment: are there more questions than answers? Int Environ Assess Manag 2:312–329

    Article  CAS  Google Scholar 

  • Harris ML, Chora L, Bishop CA, Bogart JP (2000) Species- and age-related differences in susceptibility to pesticide exposure for two amphibians, Rana pipiens, and Bufo americanus. Bull Environ Contam Toxicol 64:263–270

    Article  CAS  Google Scholar 

  • Hartmann A, Agurell E, Beevers C, Brendler-Schwaab S, Burlinson B, Clay P, Collins A, Smith A, Speit G, Thybaud V, Tice RR (2003) Recommendations for conducting the in vivo alkaline comet assay. Mutagenesis 18:45–51

    Article  CAS  Google Scholar 

  • Hayashi M (2016) The micronucleus test - Most widely used in vivo genotoxicity test. Genes Environ 38:18

    Article  CAS  Google Scholar 

  • He JL, Chen WL, Jin LF, Jin HY (2000) Comparative evaluation of the in vitro micronucleus test and the comet assay for the detection of genotoxic effects of X-ray radiation. Mutat Res 469:223–231

    Article  CAS  Google Scholar 

  • Heddle JA, Cimino MC, Hayashi M, Romagna F, Shelby MD, Tucker JD, Vanparys P, MacGregor JT (1991) Micronuclei as an index of cytogenetic damage: past, present, and future. Environ Mol Mutagen 18:277–291

    Article  CAS  Google Scholar 

  • IUCN (2019) The International Union for Conservation of Nature Red List of Threatened Species. Version 2016-2

  • Jackson DA (1993) Stopping rules in principal components analysis: a comparison of heuristical and statistical approaches. Ecology 74:2204–2214

    Article  Google Scholar 

  • Jha AN (2008) Ecotoxicological applications and significance of the comet assay. Mutagenesis 23:207–221

    Article  CAS  Google Scholar 

  • Josende ME, Tozetti AM, Alalan MT, Mathies Filho V, da Silva XS, da Silva Júnior FMR, Martins SE (2015) Genotoxic evaluation in two amphibian species from Brazilian subtropical wetlands. Ecol Indic 49:83–87

    Article  CAS  Google Scholar 

  • Junges CM, Lajmanovich RC, Peltzer PM, Attademo AM, Bassó A (2010) Predator–prey interactions between Synbranchus marmoratus (Teleostei: Synbranchidae) and Hypsiboas pulchellus tadpoles (Amphibia: Hylidae): importance of lateral line in nocturnal predation and effects of fenitrothion exposure. Chemosphere 81:1233–1238

    Article  CAS  Google Scholar 

  • Kegley SE, Hill BR, Orme S, Choi AH (2016): PAN Pesticide Database, Pesticide Action Network. PAN Pesticide Database website, Oakland. http://www.pesticideinfo.org. Accessed 01 Feb 2019

  • Kiesecker JM, Blaustein AR, Belden LK (2001) Complex causes of amphibian population declines. Nature 410:681–684

    Article  CAS  Google Scholar 

  • Larramendy ML (2017) Ecotoxicology and genotoxicology: non-traditional aquatic models. The Royal Society of Chemistry, Cambridge, 538

    Book  Google Scholar 

  • Linder G, Barbitta J, Kwaiser T (1990) Short-term amphibian toxicity tests and paraquat toxicity assessment. Thirteenth Volume. ASTM International, Aquatic Toxicology and Risk Assessment

    Book  Google Scholar 

  • MacBean C (2012) The pesticide manual: a world compendium. British Crop Production Council, Alton, Hampshire, United Kingdom

    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 

  • Mattice JD, Smartt A, Teubl S, Scott T, Norman RJ (2011) Pest management: weeds. environmental implications of pesticides in rice production. AAES Research Series 591:141–153

    Google Scholar 

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

    Article  CAS  Google Scholar 

  • Medina RG, Ponssa ML, Aráoz E (2016) Environmental, land cover and land use constraints on the distributional patterns of anurans: Leptodacylus species (Anura, Leptodactylidae) from Dry Chaco. PeerJ 4:e2605

    Article  Google Scholar 

  • Moraes BS, Clasen B, Loro VL, Pretto A, Toni C, de Avila LA, Marchesan E, de Oliveira 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, Landois P, Datsyuk V, Puech P, Pinelli E, Flahaut E, Gauthier L (2011) International amphibian micronucleus standardized procedure (ISO 21427-1) for in vivo evaluation of double-walled carbon nanotubes toxicity and genotoxicity in water. Environ Toxicol 26:136–145

    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 

  • Newman MC (2014) Fundamentals of ecotoxicology: the science of pollution. CRC Press, Boca Ratón

    Book  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Ossana NA, Castañé PM, Salibián A (2013) Use of Lithobates catesbeianus tadpoles in a multiple biomarker approach for the assessment of water quality of the Reconquista river (Argentina). Arch Environ Contam Toxicol 65:486–497

    Article  CAS  Google Scholar 

  • Pasha F (2013) Enzyme inhibition (AChE) in brain of Oreochromis mossambicus due to pesticidal pollution of herbicide Pursuit. J Biol Sci 1:91–100

    Google Scholar 

  • Pasha F, Singh R (2005) Enzyme inhibition (AChE) in muscles and skin of Oreochromis mossambicus due to pesticidal pollution of herbicide Pursuit. Asian J Exp Sci 19:119–126

    CAS  Google Scholar 

  • Peltzer PM, Lajmanovich RC, Attademo AM, Junges CM, Cabagna-Zenklusen MC, Repetti MR, Sigrist ME, Beldoménico H (2013) Effect of exposure to contaminated pond sediments on survival, development, and enzyme and blood biomarkers in veined treefrog (Trachycephalus typhonius) tadpoles. Ecotoxicol Environ Saf 98:142–151

    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 

  • 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 

  • Pérez-Iglesias JM, Franco-Belussi L, Moreno L, Tripole S, de Oliveira C, Natale GS (2016) Effects of glyphosate on hepatic tissue evaluating melanomacrophages and erythrocytes responses in neotropical anuran Leptodactylus latinasus. Environ Sci Pollut Res 23:9852–9861

    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 

  • 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 

  • Pollo FE, Grenat PR, Otero MA, Salas NE, Martino A (2016) Assessment in situ of genotoxicity in tadpoles and adults of frog Hypsiboas cordobae (Barrio 1965) inhabiting aquatic ecosystems associated to fluorite mine. Ecotoxicol Environ Saf 133:466–474

    Article  CAS  Google Scholar 

  • Qian H, Li Y, Sun C, Lavoie M, Xie J, Bai X, Fu Z (2015) Trace concentrations of imazethapyr (IM) affect floral organs development and reproduction in Arabidopsis thaliana: IM-induced inhibition of key genes regulating anther and pollen biosynthesis. Ecotoxicology 24:163–171

    Article  CAS  Google Scholar 

  • Ruiz de Arcaute C, Pérez-Iglesias JM, Nikoloff N, Natale GS, Soloneski S, Larramendy M (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 

  • Sanders HO (1970) Pesticide toxicities to tadpoles of the western chorus frog Pseudacris triseriata and Fowler’s toad Bufo woodhousii fowleri. Copeia 2:246–251

    Article  Google Scholar 

  • Senseman SA (2007) Herbicide handbook. Weed Science Society of America. Weed Science Society of America, Lawrence, 458

    Google Scholar 

  • Shimizu N, Itoh N, Utiyama H, Wahl GM (1998) Selective entrapment of extrachromosomally amplified DNA by nuclear budding and micronucleation during S phase. J Cell Biol 140:1307–1320

    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, pp 3–24

    Chapter  Google Scholar 

  • Siu WHL, Cao J, Jack RW, Wu RSS, Richardson BJ, Xu L, Lam PKS (2004) Application of the comet assay and micronucleus assays to the detection of B[a]P genotoxicity in haemocytes of the green-lipped mussel (Perna viridis) Aquat Toxicol 66, 381-392

  • Smalling KL, Reeves R, Muths E, Vandever M, Battaglin WA, Hladik ML, Pierce CL (2015) Pesticide concentrations in frog tissue and wetland habitats in a landscape dominated by agriculture. Sci Total Environ 502:80–90

    Article  CAS  Google Scholar 

  • Souza Caldas S, Zanella R, Primel EG (2011) Risk estimate of water contamination and occurrence of pesticides in the South of Brazil. In: Kortekamp A (ed) Herbicides and environment. InTech, Rijeka

    Google Scholar 

  • Sparling DW, Linder G, Bishop CA, Krest SK (2010): Ecotoxicology of amphibians and reptiles. CRC Press, Second Edition. SETAC Books, Boca Raton, FL, 916

  • Suárez RP, Zaccagnini ME, Babbitt KJ, Calamari NC, Natale GS, Cerezo A, Codugnello N, Boca T, Damonte MJ, Vera-Candioti J (2016) Anuran responses to spatial patterns of agricultural landscapes in Argentina. Journal of Landscape Ecology 31:2485–2505

    Article  Google Scholar 

  • TOXNET (2019) Toxicology Data Network. Hazardous Substances Data Bank (HSDB), Imazethapyr https://toxnet.nlm.nih.gov/cgi-bin/sis/search2/r?dbs+hsdb:@term+@rn+@rel+81335-77-5. Accessed 28 Dec 2018

  • UN (2011) Peligros para el medioambiente, In: United Nations (Ed.), pp. 229–268

  • USEPA (1975) Methods for acute toxicity tests with fish, macroinvertebrates, and amphibians. USEPA 660/3-75-009, 62

  • USEPA (1982) Pesticides Assessment Guidelines Subdivision E. Hazard Evaluation: Wildlife and Aquatic Organism, United States Environmental Protection Agency, Washington DC

  • USEPA (2002) Methods for measuring the acute toxicity of effluents and receiving waters to freshwater and marine organisms. Fifth edition

  • Vaira M, Akmentins M, Attademo M, Baldo D, Barrasso D, Barrionuevo S, Basso N, Blotto B, Cairo S, Cajade R, Céspedez J, Corbalán V, Chilote P, Duré M, Falcione C, Ferraro DF, Gutierrez R, Ingaramo MR, Junges C, Lajmanovich R, Lescano J, Marangoni F, Martinazzo L, Marti R, Moreno L, Natale GS, Pérez Iglesias JM, Peltzer P, Quiroga L, Rosset S, Sanabria E, Sanchez L, Schaefer E, Úbeda C, Zaracho V (2012) Categorización del estado de conservación de los anfibios de la República Argentina. Cuadernos Herpetol 26:131–159

    Google Scholar 

  • Venturino A, Pechen de D'Angelo AM (2005) Biochemical targets of xenobiotics: biomarkers in amphibian ecotoxicology. Appl Herpetol 2:335–353

    Article  Google Scholar 

  • Venturino A, Rosenbaum E, Caballero De Castro A, Anguiano OL, Gauna L, Fonovich De Schroeder T, Pechen De D'Angelo AM (2003) Biomarkers of effect in toads and frogs. Biomarkers 8:167–186

    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 

  • Vera-Candioti J, Soloneski S, Larramendy M (2013) Evaluation of the genotoxic and cytotoxic effects of glyphosate-based herbicides in the ten spotted live-bearer fish Cnesterodon decemmaculatus (Jenyns, 1842). Ecotoxicol Environ Saf 89:166–173

    Article  CAS  Google Scholar 

  • Walker CH (2009) Organic pollutants: an ecotoxicological perspective. CRC Press, Boca Raton

    Google Scholar 

  • Yin X, Zhu G, Li XB, Liu S (2009) Genotoxicity evaluation of chlorpyrifos to amphibian Chinese toad (Amphibian: Anura) by comet assay and micronucleus test. Mutat Res 680:2–6

    Article  CAS  Google Scholar 

  • Zar JH (2010) Biostatistical analysis, Fifth edn. Pearson Education India, Upper Saddle River

Download references

Acknowledgments

This study was supported by grants from the National University of La Plata (Grants 11/N817 and 11/N847) of Argentina.

Author information

Authors and Affiliations

  1. Cátedra de Citología, Facultad de Ciencias Naturales y Museo, Universidad Nacional de La Plata, Calle 64 No. 3 (esq. 120), B1904AMA, La Plata, Argentina

    Juan M. Pérez-Iglesias & Marcelo L. Larramendy

  2. Centro de Investigaciones del Medio Ambiente (CIMA), Facultad de Ciencias Exactas, Universidad Nacional de La Plata, La Plata, Argentina

    Juan M. Pérez-Iglesias

  3. Instituto de Recursos Biológicos, Centro de Investigaciones de Recursos Naturales (CIRN), Instituto Nacional de Tecnología Agropecuaria (INTA), Hurlingham, Buenos Aires, Argentina

    Julie C. Brodeur

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

    Juan M. Pérez-Iglesias, Julie C. Brodeur & Marcelo L. Larramendy

Authors
  1. Juan M. Pérez-Iglesias
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Julie C. Brodeur
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Marcelo L. Larramendy
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Marcelo L. Larramendy.

Ethics declarations

Conflict of interest

The authors declare that there are no conflicts of interest.

Additional information

Responsible editor: Philippe Garrigues

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Pérez-Iglesias, J.M., Brodeur, J.C. & Larramendy, M.L. An imazethapyr-based herbicide formulation induces genotoxic, biochemical, and individual organizational effects in Leptodactylus latinasus tadpoles (Anura: Leptodactylidae). Environ Sci Pollut Res 27, 2131–2143 (2020). https://doi.org/10.1007/s11356-019-06880-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11356-019-06880-7

Keywords

Search

Navigation