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Bioinsecticide spinosad poses multiple harmful effects on foragers of Apis mellifera

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Abstract

There are multifactorial causes for the recent decline in bee populations, which has resulted in compromised pollination and reduced biodiversity. Bees are considered one of the most important non-target insects affected by insecticides used in crop production. In the present study, we investigated the effects of acute oral exposure to spinosad on the survival, food consumption, flight behavior, respiration rate, activity of detoxification enzymes, total antioxidant capacity (TAC), brain morphology, and hemocyte count of Apis mellifera foragers. We tested six different concentrations of spinosad for the first two analyses, followed by LC50 (7.7 mg L−1) for other assays. Spinosad ingestion decreased survival and food consumption. Exposure to spinosad LC50 reduced flight capacity, respiration rate, and superoxide dismutase activity. Furthermore, this concentration increased glutathione S-transferase activity and the TAC of the brain. Notably, exposure to LC50 damaged mushroom bodies, reduced the total hemocyte count and granulocyte number, and increased the number of prohemocytes. These findings imply that the neurotoxin spinosad affects various crucial functions and tissues important for bee performance and that the toxic effects are complex and detrimental to individual homeostasis.

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Acknowledgements

We thank the Apiary at the Universidade Federal de Viçosa (UFV) for technical support.

Funding

This work was supported by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior—Brasil (CAPES—Finance Code 001), Fundação de Amparo à Pesquisa do Estado de Minas Gerais (FAPEMIG CBB-APQ-00247–14), and Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq, 151440/2022–0, 124859/20224, 301725/2019–5, and 150813/2022–8).

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All authors contributed to the study conception and design. Material preparation, data collection, and analysis were performed by RSA, MPL, TAV, DSSB, and LLB. The first draft of the manuscript was written by RSA, MPL and GFM and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.

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Correspondence to Renan dos Santos Araújo.

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The authors declare no competing interests.

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11356_2023_27143_MOESM1_ESM.pdf

Supp. Fig. 1. Histological sections of the mushroom bodies of Apis mellifera foragers fed orally with 50% sucrose with spinosad solution (treated) (A, B), or 50% sucrose (control) (C, D). Samples were incubated only with secondary antibody (negative control for immunohistochemistry) and no staining was observed. The cell nucleus was stained with DAPI (blue). Labeled structures are the peduncle (Pe), calyx (Ca), and Kenyon cells (KC). (PDF 108 KB)

11356_2023_27143_MOESM2_ESM.pdf

Supp. Fig. 2. Histological sections of the mushroom bodies of Apis mellifera foragers fed orally with 50% sucrose with spinosad (treated), or with sucrose solution (control) (C, D). Cells positive for caspase-3 (red, arrow and inset) were detected only in exposed bees and not in the control. The cell nucleus was stained with DAPI (blue). Labeled structures are the peduncle (Pe), calyx (Ca), and Kenyon cells (KC). (PDF 166 KB)

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Araújo, R.d.S., Lopes, M.P., Viana, T.A. et al. Bioinsecticide spinosad poses multiple harmful effects on foragers of Apis mellifera. Environ Sci Pollut Res 30, 66923–66935 (2023). https://doi.org/10.1007/s11356-023-27143-6

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  • DOI: https://doi.org/10.1007/s11356-023-27143-6

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