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Short-term exposure to low doses of rotenone induces developmental, biochemical, behavioral, and histological changes in fish

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Abstract

Rotenone, a natural compound derived from plants of the genera Derris and Lonchocarpus, is used worldwide as a pesticide and piscicide. This study aims to assess short-term toxicity of rotenone to early-life stages of the fish Danio rerio and Poecilia reticulata using a wide and integrative range of biomarkers (developmental, biochemical, behavioral, and histopathological). Moreover, the species sensitivity distribution (SSD) approach was used to compare rotenone acute toxicity to fish species. Toxicity tests were based on the OECD protocols, fish embryo toxicity test (for D. rerio embryos), and fish acute toxicity test (for P. reticulata juveniles). D. rerio embryos were used to estimate lethal concentrations and analyze embryonic and enzymatic alterations (activity of catalase, glutathione-S-transferase, and cholinesterase), while P. reticulata juveniles were used for the assessment of histological damage in the gills and liver. Rotenone induced significant mortality in zebrafish embryos with a 96-h lethal concentration 50 % (LC50) = 12.2 μg/L. Rotenone was embryotoxic, affecting the development of D. rerio embryos, which showed cardiac edema; tail deformities; loss of equilibrium; and a general delay characterized by lack of tail detachment, delayed somite formation, yolk sac absorption, and lack of pigmentation. Biochemical biomarker inhibition was observed for concentrations ≥1 μg/L for CAT and glutathione-S-transferase (GST) and for cholinesterase (ChE) in concentration from 10 μg/L. Behavioral changes were observed for P. reticulata juveniles exposed to concentrations equal to or above 25 μg/L of rotenone; moreover, histological damage in the liver and gills of fish exposed to concentrations equal to or above 2.5 μg/L could be observed. A hazard concentration 5 % (HC5) of 3.2 μg/L was estimated considering the acute toxicity data for different fish species (n = 49). Lethal and sublethal effects of rotenone raise a concern about its effects on nontarget fish species, especially because rotenone and its metabolite rotenolone are frequently reported in the microgram range in natural environments for several days after field applications. Rotenone should be used with caution. Given the high toxicity and wide range of sublethal effects here reported, further studies in a chronic exposure scenario are recommended.

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Acknowledgments

The authors acknowledge the National Council of Technological and Scientific Development (CNPq), Coordination of Improvement of Higher Education Personnel (CAPES; scholarship provided to Karina Motta Melo), Ministry of Education, and Ministry of Science and Technology of Brazil through the program Science without Borders (CNPq; BJT-A scholarship provided to Rhaul Oliveira). The authors also acknowledge the Science Support Foundation of Para (FAPESPA) for financial support through the National Program of Research Excellence (PRONEX, 011/2008) and the Portuguese Fundação para Ciência e Tecnologia (FCT) for the financial support through the grants for the authors (SFRH/BPD/31752/2006, SFRH/BD/62605/2009). CYN, JCP, and CKG are grateful to CNPq for the Bolsas de Produtividade. This study is part of the Master’s Dissertation of KMM. In memoriam José de Souza Filho.

Ethical standards

The experiments are in accordance with the current laws of the country in which they were performed. The study was approved by the ethics committee, at the Federal University of Para (reference BIO036-12).

Conflict of interest

The authors declare that they have no conflict of interest.

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Authors and Affiliations

  1. Laboratório de Citogenética, Departamento de Genética, Instituto de Ciências Biológicas, Universidade Federal do Pará, Campus do Guamá, Av. Perimetral, Guamá, Belém, Pará, 66075-900, Brazil

    Karina Motta Melo, Julio Cesar Pieczarka & Cleusa Yoshiko Nagamachi

  2. Laboratório de Genética Toxicológica, Departamento de Genética e Morfologia, Instituto de Ciências Biológicas, Universidade de Brasília, Asa Norte, Brasília, Distrito Federal, 70910-900, Brazil

    Karina Motta Melo, Rhaul Oliveira, Cesar Koppe Grisolia & José de Souza Filho

  3. Departamento de Biologia & Centro de Estudos do Ambiente e do Mar, Universidade de Aveiro, Campus Santiago, 3810-193, Aveiro, Portugal

    Rhaul Oliveira & Inês Domingues

Authors
  1. Karina Motta Melo
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  2. Rhaul Oliveira
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  3. Cesar Koppe Grisolia
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  4. Inês Domingues
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  5. Julio Cesar Pieczarka
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  6. José de Souza Filho
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  7. Cleusa Yoshiko Nagamachi
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Corresponding author

Correspondence to Cleusa Yoshiko Nagamachi.

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Responsible editor: Cinta Porte

Highlights

- Rotenone is extremely toxic for fish with a HC5 = 3.2 μg/L.

- Behavioral, structural, and developmental changes occur after exposure to low concentrations of rotenone.

- Biomarkers of oxidative (CAT and GST) and neurological (ChE) stress are inhibited by rotenone.

In memoriam of José de Souza Filho.

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Melo, K.M., Oliveira, R., Grisolia, C.K. et al. Short-term exposure to low doses of rotenone induces developmental, biochemical, behavioral, and histological changes in fish. Environ Sci Pollut Res 22, 13926–13938 (2015). https://doi.org/10.1007/s11356-015-4596-2

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