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Melanophryniscus admirabilis tadpoles’ responses to sulfentrazone and glyphosate-based herbicides: an approach on metabolism and antioxidant defenses

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Abstract

Melanophryniscus admirabilis is a frog endemic to the southern Atlantic Forest (Brazil), with restricted distribution and considered as critically endangered. The aim of this study was to evaluate possible alterations in biomarkers of metabolism (glycogen, proteins, and uric acid) and oxidative balance (superoxide dismutase, catalase, glutathione S-transferase, and lipoperoxidation) of tadpoles of Melanophryniscus admirabilis exposed to commercial herbicide formulations containing sulfentrazone (Boral® 500 SC: 130 and 980 μg a.i./L) and glyphosate (Roundup® Original: 234 and 2340 μg a.i./L). Mortality was not observed in any of the groups studied. Our results show that a 96-h exposure to the herbicides decreased glycogen levels, indicating increased energy demand for xenobiotic metabolism. Protein levels increased in the Boral group but decreased in the higher concentration of Roundup, and uric acid levels did not change significantly between the experimental groups. Lipoperoxidation decreased in the Boral group and in the higher concentration of Roundup. Decreased levels of superoxide dismutase in both treatments and of catalase in the lowest concentration of the herbicides were observed. Glutathione S-transferase activity increased in the Roundup group; this enzyme seems to be crucial in the metabolization of the herbicides and in the survival of the tadpoles. Our results suggest that M. admirabilis has a high antioxidant capacity, which guaranteed the survival of tadpoles. Nevertheless, exposure to pesticides could impose a serious risk to this species, especially considering its restricted distribution, habitat specificity, and high physiological demand to metabolize xenobiotics.

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The datasets used and/or analyzed during the current study are available from the corresponding author on reasonable request.

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Acknowledgments

We would like to thank Michelle Abadie, Thayná Mendes, Juliane Heyde, and Matheus Kingeski for their sample support and information on the species studied, and Luis Esteban Krause Lanes (PUCRS) for his valuable help in the statistical analysis of the work. We thank the Fundação Grupo O Boticário and RAN/ICMBio for their financial and logistical support and the National Council for Scientific and Technological Development (CNPq) for granting a master’s degree grant to the first author and for providing a productivity grant to the corresponding author.

Funding

This study was funded by the Fundação Grupo O Boticário and RAN/ICMBio, the National Council for Scientific and Technological Development (CNPq) (case number 307071/2015-4), and the Higher Education Personnel Improvement Coordination—Brazil (CAPES) (Financial Code 001).

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Authors and Affiliations

  1. Laboratório de Fisiologia da Conservação, Departamento de Ciências Morfológicas, Programa de Pós-Graduação em Ecologia e Evolução da Biodiversidade, Escola de Ciências da Saúde e da Vida, Pontifícia Universidade Católica do Rio Grande do Sul (PUCRS), Porto Alegre, Brazil

    Patrícia Rodrigues da Silva & Guendalina Turcato Oliveira

  2. Laboratório de Herpetologia, Departamento de Zoologia, Programa de Pós-Graduação em Biologia Animal, Instituto de Biociências, Universidade Federal do Rio Grande do Sul (UFRGS), Porto Alegre, Brazil

    Márcio Borges-Martins

Authors
  1. Patrícia Rodrigues da Silva
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  2. Márcio Borges-Martins
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  3. Guendalina Turcato Oliveira
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Contributions

Conceptualization: Guendalina Turcato Oliveira, Márcio Borges-Martins, and Patrícia Rodrigues da Silva. Data curation: Guendalina Turcato Oliveira, Márcio Borges-Martins, and Patrícia Rodrigues da Silva. Formal analysis: Guendalina Turcato Oliveira, Márcio Borges-Martins, and Patrícia Rodrigues da Silva. Funding acquisition: Guendalina Turcato Oliveira and Márcio Borges-Martins. Investigation: Guendalina Turcato Oliveira and Patrícia Rodrigues da Silva. Methodology: Guendalina Turcato Oliveira, Márcio Borges-Martins, and Patrícia Rodrigues da Silva. Project administration: Guendalina Turcato Oliveira. Resources: Guendalina Turcato Oliveira and Márcio Borges-Martins. Software: Guendalina Turcato Oliveira. Supervision: Guendalina Turcato Oliveira and Márcio Borges-Martins. Validation: Guendalina Turcato Oliveira and Márcio Borges-Martins. Visualization: Guendalina Turcato Oliveira, Márcio Borges-Martins, and Patrícia Rodrigues da Silva. Writing—original draft: Guendalina Turcato Oliveira, Márcio Borges-Martins, and Patrícia Rodrigues da Silva. Writing—review and editing: Guendalina Turcato Oliveira, Márcio Borges-Martins, and Patrícia Rodrigues da Silva.

Corresponding author

Correspondence to Guendalina Turcato Oliveira.

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Competing interests

The authors declare that they have no competing interests.

Ethical approval

All procedures involving animals were authorized by the Committee on Animal Research and Ethics from the Pontifícia Universidade Católica do Rio Grande do Sul (CEUA/PUCRS) (Permit n° 6879). Sampling size and procedures were authorized by the Instituto Chico Mendes de Conservação da Biodiversidade (ICMBio/SISBio) (Permit n° 40004-4) and followed the legal precepts of the Federative Republic of Brazil.

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Responsible Editor: Philippe Garrigues

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Highlights

• Tadpoles were exposed to commercial herbicide formulations containing sulfentrazone and glyphosate.

• Mortality was not observed.

• Glycogen has been mobilized as an energy substrate for the detoxification process.

• Only uric acid levels and catalase activity did not vary significantly.

• No increase in lipid peroxidation was observed in any of the herbicides.

• GST increases at all herbicide concentrations.

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da Silva, P.R., Borges-Martins, M. & Oliveira, G.T. Melanophryniscus admirabilis tadpoles’ responses to sulfentrazone and glyphosate-based herbicides: an approach on metabolism and antioxidant defenses. Environ Sci Pollut Res 28, 4156–4172 (2021). https://doi.org/10.1007/s11356-020-10654-x

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  • DOI: https://doi.org/10.1007/s11356-020-10654-x

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