Skip to main content

Advertisement

SpringerLink
Log in

Bioaccumulation of pesticides and genotoxicity in anurans from southern Brazil

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

Abstract

The expansion of agricultural activities causes habitat loss and fragmentation and the pollution of natural ecosystems through the intense use of pesticides, which may affect the populations of amphibian anurans that inhabit agricultural areas. The present study evaluated the in situ bioaccumulation of pesticides in a population of Leptodactylus luctator that occupies farmland in southern Brazil. We also compared the genotoxicity of L. luctator populations from farmland and forested areas in the same region. We analyzed the micronuclei and nuclear abnormalities of 34 adult anurans, 19 from farmland, and 15 from the forested area. We also assessed the presence of 32 pesticides in liver samples obtained from 18 farmland-dwelling anurans, using chromatographic analysis. We recorded significantly higher rates of nuclear abnormalities in the individuals from the farmland, in comparison with the forest. We detected nine pesticides in the liver samples, of which, deltamethrin was the most common and carbosulfan was recorded at the highest concentrations. The bioaccumulation of pesticides and the higher levels of genotoxic damage found in the anurans from agricultural areas, as observed in the present study, represent a major potential problem for the conservation of these vertebrates, including the decline of their populations and the extinction of species.

Graphical abstract

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

Similar content being viewed by others

Data Availability

We declare that all the data supporting the results of this paper were generated during the study. The additional data that support the findings of this study are available from the corresponding author (T. Ascoli-Morrete).

References 

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

    Article  CAS  Google Scholar 

  • Agostini MG, Roesler I, Bonetto C, Ronco AE, Bilenca D (2020) Pesticides in the real world: the consequences of GMO-based intensive agriculture on native amphibians. Biol Conserv 241:1–8

    Article  Google Scholar 

  • Albert A, Drouillard K, Haffner GD, Dixon B (2007) Dietary exposure to low pesticide doses causes long-term immunosuppression in the Leopard Frog (Rana pipiens). Environ Toxicol Chem 26:1179–1185

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Arikan K, Arikan ZY, Turan SL (2018) Persistent organochlorine contaminant residues in tissues of hedgehogs from Turkey. Bull Environ Contam Toxicol 100:361–368

    Article  CAS  Google Scholar 

  • Ascoli-Morrete T, Signor E, Santos-Pereira M, Zanella N (2019) Morphological abnormalities in anurans from southern Brazil. Austral Ecol 44:1025–1029

    Article  Google Scholar 

  • Babini MS, Bionda CL, Salinas ZA, Salas NE, Martino NS (2018) Reproductive endpoints of Rhinella arenarum (Anura, Bufonidae): populations that persist in agroecosystems and their use for the environmental health assessment. Ecotox Environ Safe 154:294–301

    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 

  • Bach NC, Marino DJG, Natale GS, Somoza GM (2018) Effects of glyphosate and its commercial formulation, Roundup® Ultramax, on liver histology of tadpoles of the neotropical frog, Leptodactylus latrans (amphibia: Anura). Chemeosphere 202:289–297

    Article  CAS  Google Scholar 

  • Benvindo-Souza M, Oliveira EAS, Assis RA, Santos CGA, Borges RE, Silva DM, Santos LRS (2020) Micronucleus test in tadpole erythrocytes: trends in studies and new paths. Chemosphere 240:124910

    Article  CAS  Google Scholar 

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

    Article  Google Scholar 

  • Boissinot A, Besnard A, Lourdais O (2019) Amphibian diversity in farmlands: combined influences of breeding-site and landscape attributes in western France. Agr Ecosyst Environ 269:51–61

    Article  Google Scholar 

  • Borges RE, Santos LRS, Assis RA, Benvindo-Souza M, Franco-Belussi L, Oliveira C (2019) Monitoring the morphological integrity of neotropical anurans. Environ Sci Pollut R 26:2623–2634

    Article  CAS  Google Scholar 

  • Burlibaşa L, Gavrila L (2011) Amphibians as model organisms for study environmental genotoxicity. Appl Ecol Env Res 9:1–15

    Article  Google Scholar 

  • Carrasco HG, Benvindo-Souza M, Santos LRS (2021) Effect of multiple stressors and population decline of frog. Environ Sci Poll R. https://doi.org/10.1007/s11356-021-16247-6

    Article  Google Scholar 

  • Carrasco KR, Tilbury KL, Myers MS (1990) Assessment of the piscine micronucleus test as an in situ biological indicator of chemical contaminant effects. Can J Fish Aquat Sci 47:2123–2136

    Article  CAS  Google Scholar 

  • Carvalho WF, Franco FC, Godoy FR, Folador D, Avelar JB, Nomura F, Cruz AD, Sabóia-Morais SMT, Bastos RP, Silva DM (2018) Evaluation of genotoxic and mutagenic effects of glyphosate roundup original in Dendropsophus minutus Peters, 1872 Tadpoles. S Am J Herpetol 13:220–229

    Article  Google Scholar 

  • Crump ML, Scott NJ Jr (1994) Standard techniques for inventory and monitoring: visual encounter surveys. In: Heyer WR, Donnelly MA, Mcdiarmid RW, Hayek RW, Foster MS (eds) Measuring and Monitoring Biological Diversity: Standard Methods for Amphibians. Smithsonian Institution Press, Washington, USA, pp 84–91

    Google Scholar 

  • Cui J, Wang F, Gao J, Zhai W, Zhou Z, Liu D, Wang P (2019) Bioaccumulation and metabolism of Carbosulfan in Zebrafish (Danio rerio) and the toxic effects of its metabolites. J Agr Food Chem 67:12348–12356

    Article  CAS  Google Scholar 

  • Dal Pizzol GE, Rosano VA, Rezende E, Kilpp JC, Ferretto MM, Mistura E, Silva AN, Bertol CD, Rodrigues LB, Friedrich MT, Rossato-Grando LG (2021) Pesticide and trace element bioaccumulation in wild owls in Brazil. Environ Sci Pollut Res. https://doi.org/10.1007/s11356-021-13210-3

    Article  Google Scholar 

  • Elgue E, Maneyro R (2017) Reproductive biology in a Uruguayan population of Elachistocleis bicolor (Guérin-Meneville, 1838) (Anura, Microhylidae). Cuad Herpetol 31:5–10

    Google Scholar 

  • Ferrante L, Leonel ACM, Gaia R, Kaefer IL, Fearnside PM (2019) Local extinction of Scinax caldarum, a treefrog in Brazil’s Atlantic forest. Herpetol J 29:295–298

    Article  Google Scholar 

  • Ghodageri MG, Pancharatna K (2011) Morphological and behavioral alterations induced by endocrine disrupters in amphibian tadpoles. Toxic Environ Chem 10:2012–2021

    Article  CAS  Google Scholar 

  • Gonçalves MW, Campos CBM, Godoy FR, Gambale PG, Nunes HF, Nomura F, Bastos RP, Cruz AD, Silva DM (2019) Assessing genotoxicity and mutagenicity of three common amphibian species inhabiting agroecosystem environment. Arch Environ Con Tox 77:409–420

    Article  CAS  Google Scholar 

  • Greenberg DA, Palen WJ, Chan KC, Jetz W, Mooers AO (2018) Evolutionarily distinct amphibians are disproportionately lost from human-modified ecosystems. Ecol Lett 21:1530–1540

    Article  CAS  Google Scholar 

  • Gregorio LS, Franco-Belussi L, De Oliveira C (2019) Genotoxic effects of 4-nonylphenol and Cyproterone Acetate on Rana catesbeiana (anura) tadpoles and juveniles. Environ Pollut 251:879–884

  • Haas SE, Reeves MK, Pinkney AE, Johnson PTJ (2017) Continental-extent patterns in amphibian malformations linked to parasites, chemical contaminants, and their interactions. Glob Change Biol 24:275–288

    Google Scholar 

  • Hammer O, Harper DAT, Ryan PD (2001) Past: Paleontological Statistics Software Package for Education and Data Analysis. Palaeontol Electron 4:1–9

  • Hegde G, Krishnamurthy SV, Berger G (2019) Common frogs response to agrochemicals contamination in coffee plantations, Western Ghats, India. Chem Ecol 35:397–407

    Article  CAS  Google Scholar 

  • Instituto Brasileiro do Meio Ambiente e dos Recursos Naturais Renováveis (IBAMA) (2019) Relatórios de comercialização de agrotóxicos. http://ibama.gov.br/agrotoxicos/relatorios-de-comercializacao-de-agrotoxicos#boletinsanuais Acessed 31 Oct 2020 (in Portuguese)

  • Kwet A, Lingnau R, Di-Bernardo M (2010) Pró-Mata: Anfíbios da Serra Gaúcha, sul do Brasil – Amphibien der Serra Gaúcha, Sudbrasilien – Amphibians of the Serra Gaúcha, South of Brazil. Brasilien-Zentrum, University of Tubingen, Germany, pp. 148 (in Portuguese)

  • Lajmanovich R, Cabagna M, Peltzer PM, Stringhini GA, Attademo AM (2005) Micronucleus induction in erythrocytes of the Hyla pulchella tadpoles (Amphibia: Hylidae) exposed to insecticide endosulfan. Mutat Res 587:67–72

    Article  CAS  Google Scholar 

  • Langerveld AJ, Celestine R, Zaya R, Mihako D, Ide CF (2009) Chronic exposure to high levels of atrazine alters expression. Of genes that regulate immune and growth-related functions in developing Xenopus laevis tadpoles. Environ Res 109:379–389

    Article  CAS  Google Scholar 

  • Leeb C, Bruhl C, Theissinger K (2020) Potential pesticide exposure during the post-breeding migration of the common toad (Bufo bufo) in a vineyard dominated landscape. Sci Total Environ 706:1–12

    Article  CAS  Google Scholar 

  • Lettoof DC, Lohr MT, Busetti F, Bateman PW, Davis RA (2020) Toxic time bombs: frequent detection of anticoagulant rodenticides in urban reptiles at multiple trophic levels. Sci Total Environ 724:2–7

    Article  CAS  Google Scholar 

  • Lopes A, Benvindo-Souza M, Carvalho WF, Nunes HF, Lima PN, Costa MS, Benetti EJ, Guerra V, Saboia-Morais SMT, Santos CE, Simões K, Bastos RP, Silva DM (2021) Evaluation of the genotoxic, mutagenic, and histopathological hepatic effects of polyoxyethylene amine (POEA) and glyphosate on Dendropsophus minutus tadpoles. Environ Poll 289:117911

    Article  CAS  Google Scholar 

  • Macagnan N, Rutkoski C, Kolcenti C, Vanzetto GV, Macahnan LP, Sturza PF, Hartmann PA, Hartmann MT (2017) Toxicity of cypermethrin and deltamethrin insecticides on embryos and larvae of Physalaemus gracilis (Anura: Leptodactylidae). Environ Sci Pollut Res 24:20699–20704

    Article  CAS  Google Scholar 

  • Magalhães FM, Lyra ML, Carvalho TR, Baldo D, Brusquetti F, Burella P, Colli GR, Gehara MC, Giarreta AA, Haddad CFB, Langone JÁ, López JÁ, Napoli MF, Santana DJ, Sá RO, Garda AA (2020) Taxonomic review of South American butter frogs: phylogeny, geographic patterns, and species distribution in the Leptodactylus latrans species group (Anura: Leptodactylidae). Herpetol Monogr 34:131–177

    Article  Google Scholar 

  • Maragno FP, Cechin SZ (2009) Reproductive biology of Leptodactylus fuscus (Anura, Leptodactylidae) in the subtropical climate, Rio Grande do Sul, Brazil. Iheringia Sér Zool 99:237–241

    Article  Google Scholar 

  • Mayer M, Duan X, Sunde P, Topping CJ (2020) European hares do not avoid newly pesticide-sprayed fields: Overspray as unnoticed pathway of pesticide exposure. Sci Total Environ 715:1–8

    Article  CAS  Google Scholar 

  • McClelland SJ, Bendis RJ, Relyea RA, Woodley SK (2018) Insecticide-induced changes in amphibian brains: how sublethal concentrations of chlorpyrifos directly affect neurodevelopment. Environ Toxicol Chem 37:2692–2698

    Article  CAS  Google Scholar 

  • Moutinho MF, Almeida EA, Espíndola ELG, Daam MA, Schiesari L (2020) Herbicides employed in sugarcane plantations have lethal and sublethal effects to larval Boana pardalis (Amphibia, Hylidae). Ecotoxicology. https://doi-org.ez116.periodicos.capes.gov.br/https://doi.org/10.1007/s10646-020-02226-z

  • Nwani CD, Lakra WS, Nagpure NS, Kumar R, Kushwaha B, Srivastava SK (2010) Mutagenic and genotoxic effects of carbosulfan in freshwater fish Channa punctatus (Bloch) using micronucleus assay and alcaline single-cell gel electrophoresis. Food Chem Toxicol 48:202–208

    Article  CAS  Google Scholar 

  • Pazinato DMM, Trindade AO, Oliveira SV, Cappellari LH (2011) Dieta de Leptodactylus latrans (Steffen, 1815) na Serra do Sudeste, Rio Grande do Sul, Brasil. Biotemas 24:147–151 ((in Portuguese))

    Article  Google Scholar 

  • Peluso J, Aronzon CM, Acquaroni M, Coll CSP (2020) Biomarkers of genotoxicity and health status of Rhinella fernandezae populations from the lower Paraná River Basin. Argentina. Ecol Indic 117:106588

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Pérez-Iglesias JM, Brodeur J, Larramendy ML (2020) An imazethapyr-based herbicide formulation induces genotoxic, biochemical, and individual organizational effects in Leptodactylus latinasus tadpoles (Anura: Leptodactylidae). Environ Sci Poll R 27:2131–2143

    Article  CAS  Google Scholar 

  • Pollo FE, Bionda CL, Salinas ZA, Sala NE, Martino AL (2015) Common toad Rhinella arenarum (Hensel, 1867) and its importance in assessing environmental health: test of micronuclei and nuclear abnormalities in erythrocytes. Environ Monit Assess 187:1–9

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • R Core Team (2020) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. URL https://www.r-project.org/. Acessed 25 Nov 2021

  • Rezende WR, Santos LRS, Franco-Belussi L (2021) Testicular morphometric changes in neotropical anurans from agroecosystems. Environ Poll 271:116265

    Article  CAS  Google Scholar 

  • Ribeiro J, Colli GR, Soares AMVM (2017) The anurofauna of a vanishing savana: the case of the Brazilian Cerrado. Biodivers Conserv 29:1993–2015

    Article  Google Scholar 

  • Rocha DG, Santos FA, Gomes AA, Faria AF (2017) Validation of a LC-MS/MS Multiresidue Methodology Based on a QuEChERS Approach for the Determination of Fluoroquinolones, Sulfonamides and Trimethoprim in Poultry and Porcine Kidney According to the Normative Instruction 24/2009-MAPA. J Braz Chem Soc 28:76–86

    CAS  Google Scholar 

  • Rohr JR, Brown J, Battaglin WA, McMahon TA, Relyea RA (2017) A pesticide paradox: fungicide indirectly increase fungal infections. Ecol Appl 27:2290–2302

    Article  Google Scholar 

  • Ruggeri J, Ribeiro LP, Pontes MR, Toffolo C, Candido M, Carriero ZN, Souza RLM, Toledo LF (2019) First Case of Wild Amphibians Infected with Ranavirus in Brasil. Short Commun 55:1–6

    Google Scholar 

  • Rumschlag SL, Rohr JR (2018) The influence of pesticide use on amphibian chytrid fungal infections varies with host life stage across broad spatial scales. Global Ecol Biogeogr 27:1277–1287

    Article  Google Scholar 

  • Rumschlag SL, Halstead NT, Hoverman JT, Raffel TR, Carrick HJ, Hudson PJ, Rohr J (2019) Effects of pesticides on exposure and susceptibility to parasites can be generalised to pesticide class and type in aquatic communities. Ecol Lett 22:962–972

    Article  Google Scholar 

  • Ruso GE, Morrissey CA, Hogan NS, Sheedy C, Gallant MJ, Jardine TD (2019) Detecting amphibians in agricultural landscapes using environmental DNA reveals the importance of wetland condition. Environ Toxicol Chem 38:2750–2763

    Article  CAS  Google Scholar 

  • Rutkoski CF, Macagnan N, Folador A, Skovronski VJ, Amaral A, Leitemperger J, Costa MD, Hartmann PA, Muller C, Loro VL, Hartmann MT (2020) Morphological and biochemical traits and mortality in Physalaemus gracilis (Anura: Leptodactylidae) tadpoles exposed to the insecticide chlorpyrifos. Chemosphere 250:1–9

    Article  CAS  Google Scholar 

  • Sansiñena JA, Peluso L, Costa CS, Demetrio PM, Loughlin TMM, Marino DJG, Alcalde L, Natale GS (2018) Evaluation of the toxicity of the sediments from an agroecosystem to two native species, Hyalella curvispina (CRUSTACEA: AMPHIPODA) and Boana pulchella (AMPHIBIA: ANURA), as potential environmental indicators. Ecol Indic 93:100–110

    Article  CAS  Google Scholar 

  • Scheele BC, Pasmans F, Skerratt LF, Berger L, Martel A, Beukem W, Acevedo AA, Burrowea PA, Carvalho T, Catenazzi A et al (2019) Amphibian fungal panzootic causes catastrophic and ongoing loss of biodiversity. Science 363:1459–1463

    Article  CAS  Google Scholar 

  • Sievers M, Hale R, Parris KM, Melvin SD, Lanctôt CM, Swearer SE (2019) Contaminant-induced behavioural changes in amphibians: A meta-analysis. Sci Total Environ 693:1–11

    Article  CAS  Google Scholar 

  • Silva MB, Fraga RE, Nishiyama PB, Costa NLB, Silva ISS, Queiroz TS, Rocha MA, Juncá FA (2020a) Genotoxic effect of the insecticide Chlorpyrifos on the erythrocytes of Odontophrynus carvalhoi tadpoles (Amphibia: Odontophrynidae). Ecotoxicol Environ Contam 15:9–13

    Google Scholar 

  • Silva MB, Fraga RE, Nishiyama PB, Costa NLB, Silva ISS, Brandão DA, Queiroz TS, Rocha MA, Juncá FA (2020b) In situ assessment of genotoxicity in tadpoles (Amphibia: Anura) in impacted and protected areas of Chapada Diamantina. Brazil. Scientia Plena 17:021701

    Google Scholar 

  • Slaby S, Titran P, Marchand G, Hanotel J, Lescuyer A, Leprêtre A, Bodart JF, Marin M, Lemiere S (2020) Effects of glyphosate and a commercial formulation roundup exposures on maturation of Xenopus laevis oocytes. Environ Sci Pollut R 27:3697–3705

    Article  CAS  Google Scholar 

  • Smalling KL, Fellers GM, Kleeman PM, Kuivila KM (2013) Accumulation of pesticides in pacific chorus frogs (Pseudacris regilla) from California’s Sierra Nevada Mountains, USA. Environ Toxic Chem 32:2026–2034

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Suárez RP, Goijman AP, Cappelletti S, Solari LM, Cristos D, Rojas D, Krug P, Babbitt KJ, Gavier-Pizarro GI (2021) Combined effects of agrochemical contamination and forest loss on anuran diversity in agroecosystems of east-central Argentina. Sci Total Environ 759:143435

    Article  CAS  Google Scholar 

  • Tsygankov VY, Lukyanova ON, Boyarova MD (2018) Organochlorine pesticide accumulation in seabirds and marine mammals from the Northwest Pacific. Mar Pollut Bull 128:208–213

    Article  CAS  Google Scholar 

  • Udroiu I, Sgura A, Vignoli L, Bologna MA, D’Amen M, Salvi D, Ruzza A, Antoccia A, Tanzarella (2014) Micronucleus test on Triturus carnifez as a tool for environmental biomonitoring. Environ Mol Mutagen 56:412–417

    Article  CAS  Google Scholar 

  • Valdespino C, Sosa VJ (2017) Effect of landscape tree cover, sex and season on the bioaccumulation of persistent organochlorine pesticides in fruit bats of riparian corridors in eastern Mexico. Chemosphere 175:373–382

    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 

  • Vanzetto GV, Slaviero JG, Sturza PF, Rutkoski CF, Macagnan N, Kolcenti C, Hartmann PA, Ferreira CM, Hartmann MT (2019) Toxic effects of pyrethroids in tadpoles of Physalaemus gracilis (Anura: Leptodactylidae). Ecotoxicology 28:1105–1114

    Article  CAS  Google Scholar 

  • Venables WN, Ripley BD (2002) Modern Applied Statistics with S. Fourth Edition. Springer, New York. ISBN 387-95457-0

  • Watson FL, Schmidt H, Turman ZK, Hole N, Garcia H, Gregg J, Tilghman J, Fradinger EA (2014) Organophosphate pesticides induce morphological abnormalities and decrease locomotor activity and heart rate in Danio rerio e Xenopus laevis. Environm Toxic Chem 33:1337–1345

    Article  CAS  Google Scholar 

  • Wang Y, Yu D, Xu P, Guo B, Zhang Y, Li J, Wang H (2014) Stereoselective metabolism, distribution, and bioaccumulation brof triadimefon and triadimenol in lizards. Ecotox Environ Saf 107:276–283

    Article  CAS  Google Scholar 

  • Wu JP, Zhang Y, Luo XJ, Chen SJ, Mai BX (2012) DDTs in rice frogs (Rana limnocharis) from an agricultural site, South China: tissue distribution, magnification, and potential toxic effects assessment. Environ Toxicol Chem 31:705–711

    Article  CAS  Google Scholar 

  • Zabel F, Delzeit R, Schneider JM, Seppelt R, Mauser W, Václavík T (2019) Global impacts of future cropland expansion and intensification on agricultural markets and biodiversity. Nat Commun 10:2844

    Article  CAS  Google Scholar 

  • Zipkin EF, DiRenzo GV, Ray JM, Rossman S, Lips KR (2020) Tropical snake diversity collapses after widespread amphibian loss. Science 367:814–816

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We thank the teams of the Herpetology and Ecology labs and the Augusto Ruschi Zoobotanical Museum (Muzar) of the University of Passo Fundo (UPF) for their support during data collection. We thank Marina S. Dalzochio for performance of ran the statistical analyses. We also thank the Postgraduate Program in Environmental Sciences/UPF for funding the chromatographic analysis and the University of Passo Fundo Foundation (FUPF) for granting a scholarship.

Funding

This study was supported by the Postgraduate Program in Environmental Sciences/UPF, which financed the chromatographic analysis.

Author information

Authors and Affiliations

  1. Programa de Pós-Graduação em Ciências Ambientais, Universidade de Passo Fundo (UPF), Passo Fundo, RS, Brazil

    Thaís Ascoli-Morrete & Noeli Zanella

  2. Instituto de Ciências Biológicas (ICB), Universidade de Passo Fundo (UPF), Passo Fundo, RS, Brazil

    Thaís Ascoli-Morrete, Humberto A. Gazola, Rhaíssa Biondo, Luciana G. Rossato-Grando & Noeli Zanella

  3. Centro de Pesquisa em Alimentação (CEPA), Universidade de Passo Fundo (UPF), Passo Fundo, RS, Brazil

    Nelson M. G. Bandeira & Elias Signor

  4. Programa de Pós-Graduação em Biologia Animal, Universidade Federal Do Rio Grande Do Sul (UFRGS), Porto Alegre, RS, Brazil

    Isis S. Homrich

  5. Programa de Pós-Graduação em Bioexperimentação, Universidade de Passo Fundo (UPF), Passo Fundo, RS, Brazil

    Luciana G. Rossato-Grando

Authors
  1. Thaís Ascoli-Morrete
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Nelson M. G. Bandeira
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Elias Signor
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Humberto A. Gazola
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Isis S. Homrich
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Rhaíssa Biondo
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Luciana G. Rossato-Grando
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Noeli Zanella
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

T. Ascoli-Morrete elaborated the research project, coordinated data collection, ran the laboratory, and wrote the manuscript. N. Zanella coordinated the elaboration and execution of the research and wrote and revised the manuscript. L. Rossato-Grando coordinated the elaboration of the research and revised the manuscript. N. Bandeira elaborated the techniques and ran the chromatographic analyses and wrote and revised the manuscript. E. Signor, H. Gazola, I. Homrich, and R. Biondo collected data and revised the manuscript.

Corresponding author

Correspondence to Thaís Ascoli-Morrete.

Ethics declarations

Ethics approval and consent to participate

This study had ethical approval from SISBIO (Sistema de Autorização e Informação em Biodiversidade—n° 68671–1) and CEUA-UPF (Comissão de Ética no Uso de Animais—n° 005/2019).

Consent for publication

Not applicable.

Competing interests

The authors declare no competing interests.

Additional information

Responsible Editor: Bruno Nunes

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

Ascoli-Morrete, T., Bandeira, N.M.G., Signor, E. et al. Bioaccumulation of pesticides and genotoxicity in anurans from southern Brazil. Environ Sci Pollut Res 29, 45549–45559 (2022). https://doi.org/10.1007/s11356-022-19042-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11356-022-19042-z

Keywords

Search

Navigation