The combined effect of clethodim (herbicide) and nitrogen variation on allelopathic interactions between Microcystis aer

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RESEARCH ARTICLE

The combined effect of clethodim (herbicide) and nitrogen variation on allelopathic interactions between Microcystis aeruginosa and Raphidiopsis raciborskii Fernanda Brêda-Alves 1

&

Valéria de Oliveira Fernandes 1 & Micheline Kézia Cordeiro-Araújo 2 & Mathias Ahii Chia 2,3

Received: 12 June 2020 / Accepted: 21 October 2020 # Springer-Verlag GmbH Germany, part of Springer Nature 2020

Abstract The large-scale use of herbicides deteriorates water quality and threatens aquatic biodiversity. Unfortunately, there are few studies on the ecological effects of herbicides on toxin-producing strains of cyanobacteria under changing nutrient conditions. The objective of the present study was to investigate the effects of the herbicide clethodim and nitrogen variation on the allelopathic interactions and toxin production of Microcystis aeruginosa BCCUSP232 and Raphidiopsis raciborskii (formerly known as Cylindrospermopsis raciborskii) ITEPA1. M. aeruginosa had increased cell density when exposed to the clethodim (H +) (23.55 mg/L), whereas the highest cell density of R. raciborskii was observed in the treatment with clethodim plus limited nitrogen. Also, the cell-free exudate of R. raciborskii significantly stimulated the growth of M. aeruginosa on day 3 of the experiment. The concentration of chlorophyll-a in M. aeruginosa cultures generally increased in all the treatments, while in R. raciborskii cultures, the opposite occurred. Total microcystins (MCs) content of M. aeruginosa in the mixed cultures was 68% higher in nitrogen-enriched conditions than the control. A similar increase in MC content occurred in M. aeruginosa unialgal culture treated with R. raciborskii exudate. Total saxitoxin concentration was 81% higher in mixed cultures of R. raciborskii simultaneously exposed to high nitrogen and clethodim. Similarly, unialgal cultures of R. raciborskii exposed to either high nitrogen or clethodim had higher saxitoxins concentrations than the control. The intracellular H2O2 content of M. aeruginosa cultures decreased, whereas, in R. raciborskii cultures, it increased during exposure to high nitrogen and clethodim. Only R. raciborskii had a significant variation in peroxidase activity. The activities of glutathione S-transferase of both strains were higher in the presence of clethodim. These results revealed that nitrogen enrichment and the presence of clethodim might lead to the excessive proliferation of M. aeruginosa and R. raciborskii and increased production of cyanotoxins in aquatic environments. Keywords Cyanobacteria . Microcystis . Raphidiopsis . Cyanotoxins . Allelopathy . Herbicides . Clethodim

Introduction Responsible Editor: Vitor Manuel Oliveira Vasconcelos * Fernanda Brêda-Alves [email protected] Mathias Ahii Chia [email protected] 1

Laboratório de Taxonomia e Ecologia de Algas Continentais, Departamento de Botânica, Universidade Federal do Espírito Santo, Av., Fernando Ferrari, Vitoria 29075-015, Brasil

2

Department of Biological Sciences, Luiz de Queiroz College of Agriculture,