Changes in innate immune response and detoxification in Melipona quadrifasciata (Apinae: Meliponini) on oral exposure to

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Original article

Changes in innate immune response and detoxification in Melipona quadrifasciata (Apinae: Meliponini) on oral exposure to azadirachtin and spinosad Thaís Andrade VIANA1 , Wagner Faria BARBOSA1 , Anete Pedro LOURENÇO2 , Weyder Cristiano SANTANA1 , Lúcio Oliveira CAMPOS3 , Gustavo Ferreira MARTINS3 1 Departamento de Entomologia, Universidade Federal de Viçosa, Viçosa, MG 36570-900, Brazil Departamento de Ciências Biológicas, Universidade Federal dos Vales do Jequitinhonha e Mucuri, Diamantina, MG 39100-000, Brazil 3 Departamento de Biologia Geral, Universidade Federal de Viçosa, Viçosa, MG 36570-900, Brazil

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Received 19 February 2020 – Revised 17 July 2020 – Accepted 29 September 2020

Abstract – Exposure to agrochemicals and pathogens has been indicated as critical factors of declining pollinator populations, including species of native tropical bees. In the present study, we investigated the sublethal effects of acute oral exposure to azadirachtin and spinosad bioinsecticides on the expression of immunity-related genes and the number of hemocytes in uninfected and Escherichia coli –infected workers of the stingless bee Melipona quadrifasciata . Expression of the immune-related gene vitellogenin decreased and the number of circulating hemocytes increased in bioinsecticide-exposed uninfected bees and in unexposed E. coli –infected bees as compared with unexposed uninfected bees. Our results show that though bioinsecticides are considered safe, contamination by sublethal doses of azadirachtin and spinosad can interfere with the immune system of bees. bioinsecticides / hemocytes / spinosad / stingless bees / vitellogenin

1. INTRODUCTION Control of insects using insecticides is a critical process in agriculture. Different types of insecticides have been used for pest control, with bioinsecticides (i.e., insecticides from natural origin) being an important group (Gullan and Cranston 2012). This is because the use of bioinsecticides is considered to mitigate environmental impacts, including risk to

Supplementary Information The online version of this article (https://doi.org/10.1007/s13592-020-00814-w) contains supplementary material, which is available to authorized users.

Corresponding author: G. Martins, [email protected] Manuscript editor: Michelle L Flenniken

pollinators, due to their natural origin (Barbosa et al. 2015a; Lima et al. 2016). Insecticides cause diverse sublethal effects to insects (Desneux et al. 2007), and irrespective of their origin, their usage may lead to a decline in pollinator populations (Potts et al. 2010). Pollinators can be affected by (bio) insecticides via contact with contaminated surfaces of plants (Koch and Weisser 1997) or ingestion when collecting contaminated food (Guedes et al. 2016). Forager bees, for instance, can take contaminated supplies to their colonies, where they distribute them through trophallaxis or larval feeding (Rortais et al. 2005; Krupke et al. 2012; Lima et al. 2016). Stingless bees (Meliponini) are pollinators under high risk of exposure to p