Skip to main content

Multiple Level Effects of Imazethapyr on Leptodactylus latinasus (Anura) Adult Frogs

Archives of Environmental Contamination and Toxicology volume 81, pages 492–506 (2021)Cite this article

Abstract

Imazethapyr is an herbicide that is used in a variety of crops worldwide, including soybean and corn. The aim of the present study was to evaluate the biomarkers responses of adult Leptodactylus latinasus exposed to the formulation Pivot® H (10.59% imazethapyr) in the laboratory at concentrations and under conditions that simulate two potential field exposure scenarios: an immersion in field runoff (Scenario 1: 10 mg/L) and a direct exposure to the droplets emitted by spray noozles (Scenario 2: 1000 mg/L). In both scenarios, the experimental procedure involved completely immersing the frogs over a period of 15 s. Different endpoints were evaluated at several ecotoxicological levels 48 and 96 h after the herbicide exposure. These included individual (biometric indices and behavior alterations), histological (liver pigments and lesions), biochemical (catalase, glutathione system and cholinesterase activities) and genotoxic effects (micronuclei induction and nuclear abnormalities). Forty-eight hours after imazethapyr exposure, frogs submitted to Scenario 1 presented an inhibition of liver glutathione-S-transferase activity, whereas histological alterations and increased hepatic cholinesterase levels were observed in frogs exposed under Scenario 2. Ninety-six hours after exposure to the imazethapyr formulation, frogs from the Scenario 1 treatment presented a decrease in liver melanin and hemosiderin, increased hepatic catalase activity and micronuclei induction. For their part, frogs exposed to Scenario 2 presented a decrease in the hepatosomatic index, an increase in liver alterations, melanin reduction and micronuclei induction. The multivariate analysis enables correlations to be made between biomarkers of different organizational level in exposed anurans. Our result indicates that real exposure to imazethapyr formulations under field conditions may pose a risk to Leptodactylus latinasus populations living in the agroecosystems.

This is a preview of subscription content, access via your institution.

Access options

Buy single article

Instant access to the full article PDF.

USD 39.95

Price includes VAT (USA)
Tax calculation will be finalised during checkout.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Abbreviations

AChE:

Acetylcholinesterase

BL:

Blebbed nucleus

BN:

Binucleated cell

CAT:

Catalase

ES:

Enlargement of sinusoids

GST:

Glutathione-S-transferase

GSH:

Reduced glutathione

HSI:

Hepatosomatic index

HV:

Vascularization or congestion

IMZT:

Imazethapyr

LB:

Lobed nucleus

MMC:

Melanomacrophages

MNs:

Micronuclei

NT:

Notched nucleus

PCA:

Principal component analysis

References

  • Abercrombie SA, de Perre C, Iacchetta M, Flynn RW, Sepúlveda MS, Lee LS, Hoverman JT (2020) Sublethal effects of dermal exposure to poly- and perfluoroalkyl substances on postmetamorphic amphibians. Environ Toxicol Chem 40(3):717–726

    Article  CAS  Google Scholar 

  • Agius C, Roberts RJ (2003) Melano-macrophage centres and their role in fish pathology. J Fish Dis 26:499–509

    CAS  Article  Google Scholar 

  • Agostini MG, Kacoliris F, Demetrio P, Natale GS, Bonetto C, Ronco AE (2013) Abnormalities in amphibian populations inhabiting agroecosystems in northeastern Buenos Aires Province, Argentina. Dis Aquat Org 104:163–171

    CAS  Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Attademo AM, Peltzer PM, Lajmanovich RC, Cabagna M, Fiorenza G (2007) Plasma B-esterase and glutathione S-transferase activity in the toad Chaunus schneideri (Amphibia, Anura) inhabiting rice agroecosystems of Argentina. Ecotoxicology 16:533–539

    CAS  Article  Google Scholar 

  • Attademo AM, Cabagna-Zenklusen MC, Lajmanovich RC, Peltzer PM, Junges CM, Bassó A (2011) B-esterase activities and blood cell morphology in the frog Leptodactylus chaquensis (Amphibia: Leptodactylidae) on rice agroecosystems from Santa Fe Province (Argentina). Ecotoxicology 20:274–282

    CAS  Article  Google Scholar 

  • Attademo AM, Bionda CL, Peltzer PM, Lajmanovich RC, Seib SN, Basso A, Junges CM (2014) Edad, tamaño corporal en la madurez sexual, longevidad y potencial reproductivo de Leptodactylus latinasus y Leptodactylus mystacinus en un cultivo de soja y un bosque nativo del centro este de Argentina. Revista Mexicana De Biodiversidad 85:315–317

    Article  Google Scholar 

  • Babini MS, Bionda CL, Salas NE, Martino AL (2015) Health status of tadpoles and metamorphs of Rhinella arenarum (Anura, Bufonidae) that inhabit agroecosystems and its implications for land use. Ecotoxicol Environ Saf 118:118–125

    CAS  Article  Google Scholar 

  • Barni S, Boncompagni E, Grosso 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

    CAS  Article  Google Scholar 

  • Beebee TJC, Griffiths RA (2005) The amphibian decline crisis: a watershed for conservation biology? Biol Cons 125:271–285

    Article  Google Scholar 

  • Blaustein AR, Wake DB (1990) Declining amphibian populations: a global phenomenon? Trends Ecol Evol 5:203–204

    Article  Google Scholar 

  • Blaustein AR, Han BA, Relyea RA, Johnson PTJ, Buck JC, Gervasi SS, Kats LB (2011) The complexity of amphibian population declines: understanding the role of cofactors in driving amphibian losses. Ann N Y Acad Sci 1223:108–119

    Article  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. Royal society of chemistry, London, UK.

  • 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

    CAS  Article  Google Scholar 

  • Brodeur JC, Vera-Candioti JV, Soloneski S, Larramendy ML, Ronco AE (2012) Evidence of reduced feeding and oxidative stress in common tree frogs (Hypsiboas pulchellus) from an agroecosystem experiencing severe drought. J Herpetol 46:72–78

    Article  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. https://doi.org/10.1016/j.chemosphere.2017.06.129

    CAS  Article  Google Scholar 

  • Brodeur JC, Damonte MJ, Vera-Candioti J, Poliserpi MB, D’Andrea MF, Bahl MF (2020) Frog body condition: basic assumptions, comparison of methods and characterization of natural variability with field data from Leptodactylus latrans. Ecol Indic 112:106098

    Article  Google Scholar 

  • Brodkin MA, Madhoun H, Rameswaran M, Vatnick I (2007) Atrazine is an immune disruptor in adult northern leopard frogs (Rana pipiens). Environ Toxicol Chem Int J 26:80–84

    CAS  Article  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 

  • Cabagna MC, Lajmanovich RC, Peltzer PM, Attademo AM, Ale E (2006) Induction of micronuclei in tadpoles of Odontophrynus americanus (Amphibia: Leptodactylidae) by the pyrethroid insecticide cypermethrin. Toxicol Environ Chem 88:729–737

    CAS  Article  Google Scholar 

  • Çakici Ö (2015) Histopathologic changes in liver and kidney tissues induced by carbaryl in Bufotes variabilis (Anura: Bufonidae). Exp Toxicol Pathol 67:237–243

    Article  CAS  Google Scholar 

  • CASAFE (2013) Guía de Productos Fitosanitarios para la República Argentina. In: Fertilizantes (ed.). CASAFE, Buenos Aires.

  • Castillo GA, Coviello A, Orce GG (1991) Effect of theophylline on the electrolyte permeability of the isolated skin of the toad Bufo arenarum. Arch Int Physiol Biochim Biophys 99:257–264

    CAS  Google Scholar 

  • Castillo GA, Chanampa Y, Orce G (2005) Effect of mercuric chloride on electrical parameters and anion fluxes in the toad skin. Comp Biochem Physiol c Toxicol Pharmacol 140:21–27

    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 

  • Cei JM (1980) Amphibians of Argentina. Università degli Studi di Firenze, New Series Monografia

    Google Scholar 

  • CONICET (2005) Reference Ethical Framework for Biomedical Research: Ethical Principles for Research with Laboratory, Farm, and Wild Animals. in: Council, N.S.a.T.R. (Ed.).

  • Couillard CM, Hodson PV (1996) Pigmented macrophage aggregates: a toxic response in fish exposed to bleached-kraft mill effluent? Environ Toxicol Chem Int J 15:1844–1854

    CAS  Article  Google Scholar 

  • De Oliveira C, Franco-Belussi L, Fanali LZ, Santos LR (2017) Use of melanin-pigmented cells as a new tool to evaluate effects of agrochemicals and other emerging contaminants in Brazilian anurans. Ecotoxicol Genotoxicol Non-Traditional Terr Models 32:125

    Google Scholar 

  • Dias Martini LF, Mezzomo RF, de Avila LA, Massey JH, Marchesan E, Zanella R, Peixoto SC, Refatti JP, Cassol GV, Marques M (2013) Imazethapyr and imazapic runoff under continuous and intermittent irrigation of paddy rice. Agric Water Manag 125:26–34

    Article  Google Scholar 

  • Edge CB, Gahl MK, Pauli BD, Thompson DG, Houlahan JE (2011) Exposure of juvenile green frogs (Lithobates clamitans) in littoral enclosures to a glyphosate-based herbicide. Ecotoxicol Environ Saf 74:1363–1369

    CAS  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

    CAS  Article  Google Scholar 

  • Ezemonye L, Tongo I (2010) Sublethal effects of endosulfan and diazinon pesticides on glutathione-S-transferase (GST) in various tissues of adult amphibians (Bufo regularis). Chemosphere 81:214–217

    CAS  Article  Google Scholar 

  • Fanali LZ, Franco-Belussi L, Bonini-Domingos CR, de Oliveira C (2018) Effects of benzo [a] pyrene on the blood and liver of Physalaemus cuvieri and Leptodactylus fuscus (Anura: Leptodactylidae). Environ Pollut 237:93–102

    CAS  Article  Google Scholar 

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

    CAS  Article  Google Scholar 

  • Fenoglio C, Boncompagni E, Fasola M, Gandini C, Comizzoli S, Milanesi G, Barni S (2005) Effects of environmental pollution on the liver parenchymal cells and Kupffer-melanomacrophagic cells of the frog Rana esculenta. Ecotoxicol Environ Saf 60:259–268

    CAS  Article  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

    CAS  Article  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 

  • Franco-Belussi L, de Lauro Castrucci AM, de Oliveira C (2013) Responses of melanocytes and melanomacrophages of Eupemphix nattereri (Anura: Leiuperidae) to Nle 4, D-Phe 7-α-melanocyte stimulating hormone and lipopolysaccharides. Zoology 116:316–324

    Article  Google Scholar 

  • Franco-Belussi L, Provete DB, Borges RE, De Oliveira C, Santos LR (2020) Idiosyncratic liver pigment alterations of five frog species in response to contrasting land use patterns in the Brazilian Cerrado. PeerJ 8:e9751

    Article  CAS  Google Scholar 

  • Furlong ET (2001) Methods of Analysis by 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 (No. 1). US Department of the Interior, US Geological Survey.

  • Garber JC, Barbee RW, Bielitzki JT (2011) Guide for the care and use of laboratory animals. Committee for the Update of the Guide for the Care and Use of Laboratory Animals. National Academies Press, Washington, DC

    Google Scholar 

  • Glinski DA, Henderson WM, Van Meter RJ, Purucker ST (2018) Effect of hydration status on pesticide uptake in anurans following exposure to contaminated soils. Environ Sci Pollut Res 25:16192–16201

    CAS  Article  Google Scholar 

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

    Article  Google Scholar 

  • Gürkan M, Hayretdağ S (2012) Morphological and histological effects of copper sulfate on the larval development of green toad, Bufo viridis. Turkish J Zool 36:231–240

    Google Scholar 

  • Hegde G, Krishnamurthy SV (2014) Analysis of health status of the frog Fejervarya limnocharis (Anura: Ranidae) living in rice paddy fields of Western Ghats, using body condition factor and AChE content. Ecotoxicol Environ Contam 9:69–76

    Google Scholar 

  • Houlahan JE, Findlay CS, Schmidt BR, Meyer AH, Kuzmin SL (2000) Quantitative evidence for global amphibian population declines. Nature 404:752–755

    CAS  Article  Google Scholar 

  • Howarth FG (2000) Non-target effects of biological control agents. In: Biological control: measures of success. Springer, pp 369–403.

  • INTA (2008) Guia para cuidado y uso de animales para experimentación. Centro de Investigación en Ciencias Veterinarias, Instituto Nacional de Tecnología Agropecuaria (INTA), Secretaría de Agricultura, Ganadería, Pesca y Alimentación, República Argentina.

  • IUCN (2020) The IUCN Red List of Threatened Species. Version 2020–3. https://www.iucnredlist.org. Acceded on 30th december 2020.

  • 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

    CAS  Article  Google Scholar 

  • Jolliffe IT, Cadima J (2016) Principal component analysis: a review and recent developments. Philos Trans Royal Soc A Math Phys Eng Sci 374:20150202

    Article  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 Ind 49:83–87

    CAS  Article  Google Scholar 

  • Kawai K, Kaku K, Izawa N, Shimizu T, Fukuda A, Tanaka Y (2007) A novel mutant acetolactate synthase gene from rice cells, which confers resistance to ALS-inhibiting herbicides. J Pestic Sci 32:89–98

    CAS  Article  Google Scholar 

  • Kegley SE, Hill BR, Orme S, Choi AH (2020) PAN Pesticide Database. Pesticide Action Network. PAN Pesticide Database website, Oakland, CA. www.pesticideinfo.org. Acceded on 30th december 2020.

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

    CAS  Article  Google Scholar 

  • Köhler HR, Triebskorn R (2013) Wildlife ecotoxicology of pesticides: can we track effects to the population level and beyond? Science 341:759–765

    Article  CAS  Google Scholar 

  • Lajmanovich RC, Peltzer PM, Attademo AM, Colussi CL, Martinuzzi CS (2018) Blood biomarkers of common toad Rhinella arenarum following chlorpyrifos dermal exposure. Interdiscip Toxicol 11:148–154

    CAS  Article  Google Scholar 

  • Leiva-Presa À, Munro Jenssen B (2006) Effects of p, p′-DDE on retinoid homeostasis and sex hormones of adult male European common frogs (Rana temporaria). J Toxicol Environ Health 69:2051–2062

    CAS  Article  Google Scholar 

  • Lin K, Xu C, Zhou S, Liu W, Gan J (2007) Enantiomeric separation of imidazolinone herbicides using chiral high-performance liquid chromatography. Chirality 19:171–178

    CAS  Article  Google Scholar 

  • Lowry OH, Rosebrough NJ, Farr AL, Randall RJ (1951) Protein measurement with the Folin phenol reagent. J Biol Chem 193:265–275

    CAS  Article  Google Scholar 

  • Magdaleno A, Gavensky MP, Fassiano AV, Ríos de Molina MC, Santos M, March H, Moretton J, Juárez ÁB (2015) Phytotoxicity and genotoxicity assessment of imazethapyr herbicide using a battery of bioassays. Environ Sci Pollut Res 22:19194–19202

    CAS  Article  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

    CAS  Article  Google Scholar 

  • McDiarmid RW, Altig R (1999) Tadpoles: the biology of anuran larvae. University of Chicago Press

    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

    CAS  Article  Google Scholar 

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

    Book  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 

  • Păunescu A, Ponepal CM, Drăghici O, Marinescu AG (2010) Histopathological responses of the liver tissues of Rana ridibunda to the champions 50 wp fungicide. Ann Food Sci Technol 11:60–64

    Google Scholar 

  • Peltzer PM, Lajmanovich RC, Sánchez-Hernandez JC, Cabagna MC, Attademo AM, Bassó A (2008) Effects of agricultural pond eutrophication on survival and health status of Scinax nasicus tadpoles. Ecotoxicol Environ Saf 70:185–197

    CAS  Article  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 

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

    Article  CAS  Google Scholar 

  • Pérez-Iglesias JM, Brodeur JC, Larramendy ML (2020) 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

    Article  CAS  Google Scholar 

  • Quaranta A, Bellantuono V, Cassano G, Lippe C (2009) Why amphibians are more sensitive than mammals to xenobiotics. PLoS ONE 4:e7699

    Article  CAS  Google Scholar 

  • Reimche GB, Machado SLO, Oliveira MA, Zanella R, Dressler VL, Flores EMM, Gonçalves FF, Donato FF, Nunes MAG (2015) Imazethapyr and imazapic, bispyribac-sodium and penoxsulam: Zooplankton and dissipation in subtropical rice paddy water. Sci Total Environ 514:68–76

    CAS  Article  Google Scholar 

  • Sanchez LC, Peltzer PM, Lajmanovich RC, Manzano AS, Junges CM, Attademo AM (2013) Reproductive activity of anurans in a dominant agricultural landscape from central-eastern Argentina. Revista Mexicana De Biodiversidad 84:912–926

    Article  Google Scholar 

  • Schulte-Hostedde AI, Zinner B, Millar JS, Hickling GJ (2005) Restitution of mass–size residuals: validating body condition indices. Ecology 86:155–163

    Article  Google Scholar 

  • Selcer KW, Verbanic JD (2014) Vitellogenin of the northern leopard frog (Rana pipiens): development of an ELISA assay and evaluation of induction after immersion in xenobiotic estrogens. Chemosphere 112:348–354

    CAS  Article  Google Scholar 

  • Shutler D, Marcogliese DJ (2011) Leukocyte profiles of northern leopard frogs, Lithobates pipiens, exposed to pesticides and hematozoa in agricultural wetlands. Copeia 2011:301–307

    Article  Google Scholar 

  • Stebbins RC, Cohen NW (1995) A natural history of amphibians. Princeton University Press, Princeton, New Jersey

    Book  Google Scholar 

  • 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. Landscape Ecol 31:2485–2505

    Article  Google Scholar 

  • Tan S, Evans RR, Dahmer ML, Singh BK, Shaner DL (2005) Imidazolinone-tolerant crops: history, current status and future. Pest Manag Sci 61:246–257

    CAS  Article  Google Scholar 

  • USEPA (1975). Methods for acute toxicity tests with fish, macroinvertebrates, and amphibians. in: Agency, U.E.P. (Ed.). USEPA 660/3-75-009,62.

  • USEPA (1989) Imazethapyr Herbicide Profile 3/89. Chemical Fact Sheet for Imazethapyr. United States Environmental Protection Agency, Office of Pesticide Programs, Washington DC. 196 pp.

  • 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 D, Gutierrez FR, Ingaramo MR, Junges C, Lajmanovich R, Lescano JN, 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 De Herpetología 26:131–159

    Google Scholar 

  • Van der Oost R, Beyer J, Vermeulen NPE (2003) Fish bioaccumulation and biomarkers in environmental risk assessment: a review. Environ Toxicol Pharmacol 13:57–149

    Article  Google Scholar 

  • Van Meter RJ, Glinski DA, Hong T, Cyterski M, Henderson WM, Purucker ST (2014) Estimating terrestrial amphibian pesticide body burden through dermal exposure. Environ Pollut 193:262–268

    Article  CAS  Google Scholar 

  • Van Meter RJ, Glinski DA, Henderson WM, Garrison AW, Cyterski M, Purucker ST (2015) Pesticide uptake across the amphibian dermis through soil and overspray exposures. Arch Environ Contam Toxicol 69:545–556

    Article  CAS  Google Scholar 

  • Van Meter RJ, Glinski DA, Purucker ST, Henderson WM (2018) Influence of exposure to pesticide mixtures on the metabolomic profile in post-metamorphic green frogs (Lithobates clamitans). Sci Total Environ 624:1348–1359

    Article  CAS  Google Scholar 

  • Van Meter RJ, Adelizzi R, Glinski DA, Henderson WM (2019) Agrochemical mixtures and amphibians: the combined effects of pesticides and fertilizer on stress, acetylcholinesterase activity, and bioaccumulation in a terrestrial environment. Environ Toxicol Chem 38:1052–1061

    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 

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

    Google Scholar 

  • Wang MZ, Jia XY (2009) Low levels of lead exposure induce oxidative damage and DNA damage in the testes of the frog Rana nigromaculata. Ecotoxicology 18:94–99

    Article  CAS  Google Scholar 

  • Zar JH (2010) Biostatistical analysis, 5th edn. Prentice Hall, New Jersey

    Google Scholar 

  • Zaya RM, Amini Z, Whitaker AS, Kohler SL, Ide CF (2011) Atrazine exposure affects growth, body condition and liver health in Xenopus laevis tadpoles. Aquat Toxicol 104:243–253

    CAS  Article  Google Scholar 

Download references

Acknowledgements

This study was supported by grants from the National University of La Plata (Grants 11/N817 and 11/N847) of Argentina. The National Council for Scientific and Technological Research (CONICET) from Argentina and Graduate Program of UNLP to provided funding for JMPI to carry out the investigations and doctoral studies. CO received a fellowship (304552/2019-4) from CNPq—Conselho Nacional de Desenvolvimento Científico e Tecnológico.

Author information

Authors and Affiliations

  1. Centro de Investigaciones del Medio Ambiente (CIM), CONICET, Facultad de Ciencias Exactas, Universidad Nacional de La Plata, Calle 47 y 115, B1904AMA, La Plata, Argentina

    J. M. Pérez-Iglesias & G. S. Natale

  2. Cátedra de Citología, Facultad de Ciencias Naturales y Museo, CONICET, Universidad Nacional de La Plata, Calle 64 Nº 3, B1904AMA, La Plata, Argentina

    J. M. Pérez-Iglesias & M. L. Larramendy

  3. Instituto de Química de San Luis, CONICET, Facultad de Química, Bioquímica y Farmacia, Universidad Nacional de San Luis, Ejército de los Andes 950, D5700BWS, San Luis, Argentina

    J. M. Pérez-Iglesias

  4. Departamento de Biologia, Universidade Estadual Paulista, IBILCE-UNESP, Rua Cristóvão Colombo, 2265, Jardim Nazareth, São José do Rio Preto, 15054-000, Brazil

    L. Z. Fanali, L. Franco-Belussi & C. De oliveira

  5. Laboratório de Patologia Experimental (LAPEx), Instituto de Biociências (INBIO), Universidade Federal de Mato Grosso do Sul, UFMS, Campo Grande, Mato Grosso do Sul, Brasil

    L. Franco-Belussi

  6. Instituto de Recursos Biológicos, Centro de Investigaciones de Recursos Naturales (CIRN), CONICET, Instituto Nacional de Tecnología Agropecuaria (INTA), B1686 , Hurlingham, Buenos Aires, Argentina

    J. C. Brodeur

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

    You can also search for this author in PubMed Google Scholar

  2. L. Z. Fanali
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. L. Franco-Belussi
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. G. S. Natale
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. C. De oliveira
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. J. C. Brodeur
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. M. L. Larramendy
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to J. M. Pérez-Iglesias.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Pérez-Iglesias, J.M., Fanali, L.Z., Franco-Belussi, L. et al. Multiple Level Effects of Imazethapyr on Leptodactylus latinasus (Anura) Adult Frogs. Arch Environ Contam Toxicol 81, 492–506 (2021). https://doi.org/10.1007/s00244-021-00880-w

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00244-021-00880-w