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Genotoxic Evaluation in Tadpoles Associated with Agriculture in the Central Cerrado, Brazil

  • Rinneu Elias BorgesEmail author
  • Lia Raquel de Souza Santos
  • Marcelino Benvindo-Souza
  • Richelle Sousa Modesto
  • Rhayane Alves Assis
  • Classius de Oliveira
Article

Abstract

Many agricultural practices cause environmental degradation that affects the cellular integrity of anurans. In the present study, we provided in situ data of Dendropsophus minutus, Physalaemus cuvieri, and Scinax fuscovarius collected in soybean/corn and conservation units in the Brazilian Cerrado. The in situ data showed no significant variation in the micronucleus frequency between the sites, only the reniform cells had a higher rate for the agricultural environment. A combined analysis of all nuclear erythrocyte abnormalities (ENAs = nuclear buds, reniform nuclei, apoptotic cell, binucleated, and anucleated cells) was recorded higher frequencies in farmland. Overall, Scinax fuscovarius was considered the best potential bioindicator for soybean/corn plantations. Finally, we recommend expanding the micronucleus test for in situ studies to expand our understanding of the sensitivity of native anuran species and provide a more systematic assessment of the adverse effects of environmental pollutants on wildlife.

Notes

Acknowledgements

The authors are grateful to the Brazilian National Council for Scientific and Technological Development (CNPq), for supporting this study through personal research Grant Number 477044/2013-1, and the São Paulo State Research Foundation (FAPESP) for supporting the analyses (Process No. 2013/02067-5). They also thank the Chico Mendes Institute for Biodiversity Conservation (ICMBio/SISBIO) and the Emas National Park for authorizing fieldwork.

Supplementary material

244_2019_623_MOESM1_ESM.docx (33 kb)
Supplementary material 1 (DOCX 32 kb)

References

  1. Anderson S, Sadinski W, Shugart L, Brussard P, Depledge M, Ford T, Hose J, Stegeman J, Suk W, Wirgin I, Wogan G (1994) Genetic and molecular ecotoxicology: a research framework. Environ Health Perspect 102:3–8CrossRefGoogle Scholar
  2. Antunes SC, Castro BB, Nunes B, Pereira R, Gonçalves F (2008) In situ bioassay with Eisenia andrei to assess soil toxicity in an abandoned uranium mine. Ecotoxicol Environ Saf 71:620–631CrossRefGoogle Scholar
  3. Arcaute CR, Pérez-Inglesis JM, Nikoloff N, Natale GS, Soloneski S, Larramendy ML (2014) Genotoxicity evaluation of the insecticide imidacloprid on circulating blood cells of Montevideo tree frog Hypsiboa spulchellus tadpoles (Anura, Hylidae) by comet and micronucleus bioassays. Ecol Indic 45:632–639CrossRefGoogle Scholar
  4. Babini MS, Bionda CL, Salas NL, Martino AL (2016) Adverse effect of agroecosystem pond water on biological endpoints of common toad (Rhinella arenarum) tadpoles. Environ Monitor Assess 188:459CrossRefGoogle Scholar
  5. Barni S, Boncompagni E, Grosso A, Bertone V, Freitas I, Fasola M, Fenoglio C (2007) Evaluation of Rana snkesculenta blood cell response to chemical stressors in the environment during the larval and adult phases. Aquat Toxicol 81:45–54CrossRefGoogle Scholar
  6. Berger L (1989) Disappearance of amphibian larvae in the agricultural landscape. Ecol Int Bull 17:65–73Google Scholar
  7. 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 Res 26:2623–2634CrossRefGoogle Scholar
  8. Brodeur JC, Svartz G, Perez-Coll CS, Marino DJG, Herkovits J (2009) Comparative susceptibility to atrazine of three developmental stages of Rhinella arenarum and influence on metamorphosis: non-monotonous acceleration of the time to climax and delayed tail resorption. Aquat Toxicol 91:161–170CrossRefGoogle Scholar
  9. Brühl CA, Pieper S, Weber B (2011) Amphibians at risk? Susceptibility of terrestrial amphibian life stages to pesticides. Environ Toxicol Chem 30:2465–2472CrossRefGoogle Scholar
  10. Castro BB, Guilhermino L, Ribeiro R (2003) In situ bioassay chambers and procedures for assessment of sediment toxicity with Chironomus riparius. Environ Pollut 125:325–335CrossRefGoogle Scholar
  11. Cavas 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 74:264–271CrossRefGoogle Scholar
  12. Cruz-Esquivel A, Viloria-Rivas J, Marrugo-Negrete J (2017) Genetic damage in Rhinella marina populations in habitats affected by agriculture in the middle region of the SinA River, Colombia. Environ Sci Pollut Res 24:27392–27401CrossRefGoogle Scholar
  13. Depledge MH, Fossi MC (1994) The role of biomarkers in environmental assessment. Ecotoxicology 3:161–172CrossRefGoogle Scholar
  14. Dias LCP, Pimenta FM, Santos AB, Costa MH, Ladle RJ (2016) Patterns of land use, extensification, and intensification of Brazilian agriculture. Glob Change Biol 22:2887–2903CrossRefGoogle Scholar
  15. Ferreira CM, Guimarães HMB, Ranzani-Paiva MJT, Soares SR, Riviero DHRF, Saldiva PHN (2003) Hematological markers of copper toxicity in Rana catesbeiana tadpoles (Bullfrog). Revista Brasil Toxicol 16:83–88Google Scholar
  16. Garaj-Vrhovac V, Gajski G, Ravlić S (2008) Efficacy of HUMN criteria for scoring the micronucleus assay in human lymphocytes exposed to a low concentration of p,p′-DDT. Braz J Med Biol Res 41:473–476CrossRefGoogle Scholar
  17. Gehara M, Crawford AJ, OrricoVGD RodríguezA et al (2014) High levels of diversity uncovered in a widespread nominal taxon: continental phylogeography of the neotropical tree frog Dendropsophus minutus. PLoS ONE 9:e111829CrossRefGoogle Scholar
  18. GökalpMuranli FD, Güner U (2011) Induction of micronuclei and nuclear abnormalities in erythrocytes of mosquito fish (Gambusia affinis) following exposure to the pyrethroid insecticide lambda-cyhalothrin. Mut Res 726:104–108CrossRefGoogle Scholar
  19. Gonçalves MW, Vieira TB, Maciel NM, Carvalho WF, Lima LSF, Gambale PG, da Cruz AD, Nomura F, Bastos RP, Silva DM (2015) Detecting genomic damages in the frog Dendropsophus minutus: preserved versus perturbed areas. Environ Sci Pollut Res 22:3947–3954CrossRefGoogle Scholar
  20. Gonçalves MW, Gambale PG, Godoy FR, Alves AA, Rezende PHD, Maciel NM, Nomura F, Bastos RP, Marco P (2017a) The agricultural impact of pesticides on Physalaemus cuvieri tadpoles (Amphibia: Anura) ascertained by comet assay. Zoologia 4:e19865. http://zoobank.org/A65FFC07-75B6-4DE4-BE59-8CE6BB2D4448
  21. Gonçalves MW, Campos CBM, Batista VG, Cruz AD, Marco Junior P, Bastos RP, Silva DDM (2017b) Genotoxic and mutagenic effects of Atrazine Atanor 50 SC on Dendropsophus minutus Peters, 1872 (Anura: Hylidae) developmental larval stages. Chemosphere 182:730–737CrossRefGoogle Scholar
  22. Gosner KL (1960) A simplified table for staging anuran embryos and larvae with notes on identification. Herpetologica 16:183–190. https://www.jstor.org/stable/3890061
  23. Hayes TB, Case P, Chui S, Chung D, Haeffele C, Haston K, Lee M, Mai VP, Marjuoa Y, Parker J (2006) Pesticide mixtures, endocrine disruption, and Amphibian declines: are we underestimating the impact? Environ Health Perspect 114:40–50CrossRefGoogle Scholar
  24. Hayes TB, Falso P, Gallipeau S, Stice M (2010) The cause of global amphibian declines: a developmental endocrinologist’s perspective. J Exp Biol 213:921–933CrossRefGoogle Scholar
  25. Jing X, Yao GJ, Liu DH, Liu C, Wang F, Wang P, Zhou ZQ (2017) Exposure of frogs and tadpoles to chiral herbicide fenoxaprop-ethyl. Chemosphere 186:832–838CrossRefGoogle Scholar
  26. Josende ME, Tozetti MA, Alalan TM, Filho MV, Ximenez SS, Silva Júnior FMR, Martins ES (2015) Genotoxic evaluation in two amphibian species from Brazilian subtropical wetlands. Ecol Indic 49:83–87CrossRefGoogle Scholar
  27. Krauter PW, Anderson SL, Harrison FL (1987) Radiation-induced micronuclei in peripheral erythrocytes of Rana catesbeiana: an aquatic animal model for in vivo genotoxicity studies. Environ Molec Mutagenesis 10:285–296CrossRefGoogle Scholar
  28. Kurelec B (1993) The genetic disease syndrome. Mar Environ Res 35:341–348CrossRefGoogle Scholar
  29. Lajmanovich RC, Cabagna-Zenklusen MC, Attademo AM, Junges CM, Peltzer PM, Basso A, Lorenzatti E (2014) Induction of micronuclei and nuclear abnormalities in tadpoles of the common toad (Rhinella arenarum) treated with the herbicides Liberty® and glufosinate–ammonium. Mutat Res Genetic Toxicol Environ Mutagenesis 769:7–12CrossRefGoogle Scholar
  30. Mann RM, Hyne RV, Choung CB, Wilson SP (2009) Amphibians and agricultural chemicals: review of the risks in a complex environment. Environ Pollut 157:2903–2927CrossRefGoogle Scholar
  31. Margarido TCS, Felicio AA, Rossa-Feres DD, de Almeida EA (2013) Biochemical biomarkers in Scinax fuscovarius tadpoles exposed to a commercial formulation of the pesticide fipronil. Mar Environ Res 91:61–67CrossRefGoogle Scholar
  32. Mijares A, Rodrigues MT, Baldo D (2010) Physalaemus cuvieri. Lista Vermelha de Espécies Ameaçadas da IUCN 2010: e.T57250A11609155. http://dx.doi.org/10.2305/IUCN.UK.2010-2.RLTS.T57250A11609155.en
  33. Montalvão MF, Malafaia G (2017) Effects of abamectin on bullfrog tadpoles: insights on cytotoxicity. Environ Sci Pollut Res 24:23411–23416CrossRefGoogle Scholar
  34. Natale GS, Vera-Candioti J, de Arcaute CR, Soloneski S, Larramendy ML, Ronco AE (2018) Lethal and sublethal effects of the pirimicarb-based formulation Aficida (R) on Boana pulchella (Dumeril and Bibron, 1841) tadpoles (Anura, Hylidae). Ecotoxicol Environ Saf 147:471–479CrossRefGoogle Scholar
  35. 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 100:275–281CrossRefGoogle Scholar
  36. 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 119:15–24CrossRefGoogle Scholar
  37. Pérez-Iglesias JM, Franco-Belussi L, Natale GS, Oliveira C (2019) Biomarkers at different levels of organisation after atrazine formulation (SIPTRAN 500SC®) exposure in Rhinella schineideri (Anura: Bufonidae) Neotropical tadpoles. Environ Pollut 244:733–746CrossRefGoogle Scholar
  38. Pignati AW, Lima FANS, Lara SS, Correa MLM, Barbosa JR, Leão LHC, Pignatti MG (2017) Spatial distribution of pesticide use in Brazil: a strategy for health surveillance. Ciência Saúde Coletiva 22:3281–3293CrossRefGoogle Scholar
  39. Pollo FE, Bionda CL, Salinas ZA, Salas 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 Monitor Assess 187:1–9CrossRefGoogle Scholar
  40. 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. Ecotoxicol Environ Saf 133:466–474CrossRefGoogle Scholar
  41. Pollo FE, Grenat PR, Salinas ZA, Otero MA, Salas NE, Martino AL (2017) Evaluation in situ of genotoxicity and stress in South American common toad Rhinella arenarumin environments related to fluorite mine. Environ Sci Pollut Res 24:18179–181872CrossRefGoogle Scholar
  42. Ramos-Neto MB, Pivello VR (2000) Lightning Fires in a Brazilian Savanna National Park: rethinking management strategies. Environ Manag 26:675–684CrossRefGoogle Scholar
  43. Redford KH, Fonseca GAB (1986) The role of Gallery Forests in the Zoogeography of the Cerrado’s non-volant mammalian fauna. Biotropica 18:126–135CrossRefGoogle Scholar
  44. Rossa-Feres DC, Nomura F (2006) Morphological characterization and taxonomic key for tadpoles (Amphibia: Anura) from northwestern region of São Paulo state, Brazil. Biota Neotrop 6:1–26CrossRefGoogle Scholar
  45. Udroiu I, Sgura A, Vignoli L, Bologna MA, D’Amen M, Salvi D, Ruzza A, Antoccia A, Tanzarella C (2015) Micronucleus test on Triturus carnifex as a tool for environmental biomonitoring. Environ Molec Mutagenesis 56:412–417CrossRefGoogle Scholar
  46. 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 104:243–253CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Department of BiologyUniversidade de Rio Verde, UniRVRio VerdeBrazil
  2. 2.Laboratory of Animal BiologyInstituto Federal Goiano, IF GoianoRio VerdeBrazil
  3. 3.Department of BiologyUniversidade Estadual Paulista - Júlio de Mesquita Filho, UNESPSão José do Rio PretoBrazil

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