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A comprehensive review of strobilurin fungicide toxicity in aquatic species: Emphasis on mode of action from the zebrafish model

Journal

ENVIRONMENTAL POLLUTION
Volume 275, Issue -, Pages -

Publisher

ELSEVIER SCI LTD
DOI: 10.1016/j.envpol.2021.116671

Keywords

Strobilurin fungicides; Aquatic species; Mitochondrial function; Toxic effects

Funding

  1. National Key R&D Program of China [2016YFA0203103]
  2. National Natural Science Foundation of China [22036002, 91643204]
  3. Pearl River Talent Recruitment Program of Guangdong Province [2019ZT08L387]

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Strobilurins are widely used fungicides in agriculture and can have varying toxicities on aquatic species, affecting mitochondrial functions and physiological processes in organisms. Studies suggest potential risks of endocrine disruption and other adverse effects on aquatic ecosystems, highlighting the importance of further research on the toxicity mechanisms of strobilurin fungicides.
Strobilurins are popular fungicides used in agriculture on a global scale. Due to their widespread use as agrochemicals, they can enter aquatic environments at concentrations that can elicit adverse effects in organisms. This review synthesizes the current state of knowledge regarding the toxic effects of strobilurin fungicides on aquatic species, including algal species, Daphnia magna, and fish species, to determine risk to aquatic organisms and ecosystems. Data show that the toxicities of strobilurins vary widely across aquatic species. Strobilurins bind cytochrome bc1 in mitochondrial complex III in fungi, and as such, research in aquatic species has focused on mitochondria-related endpoints following exposures to strobilurins. In fish, studies into the activities of mitochondrial complexes and the expression of genes involved in the electron transfer chain have been conducted, converging on the theme that mitochondrial complexes and their enzymes are impaired by strobilurins. In general, the order of toxicity of strobilurins for fish species are pyraoxystrobin > pyraclostrobin approximate to trifloxystrobin > picoxystrobin > kresoxim-methyl > fluoxastrobin > azoxystrobin. In addition to mitochondrial toxicity, studies also report genotoxicity, immunotoxicity, cardiotoxicity, neurotoxicity, and endocrine disruption, and each of these events can potentially impact whole organism-level processes such as development, reproduction, and behavior. Screening data from the US Environmental Protection Agency ToxCast database supports the hypothesis that these fungicides may act as endocrine disruptors, and high throughput data suggest estrogen receptor alpha and thyroid hormone receptor beta can be activated by some strobilurins. It is recommended that studies investigate the potential for endocrine disruption by strobilurins more thoroughly in aquatic species. Based on molecular, physiological, and developmental outcomes, a proposed adverse outcome pathway is presented with complex III inhibition in the electron transfer chain as a molecular initiating event. This review comprehensively addresses sub-lethal toxicity mechanisms of strobilurin fungicides, important as the detection of strobilurins in aquatic environments suggests exposure risks in wildlife. (C) 2021 Elsevier Ltd. All rights reserved.

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