Response of adult honey bees treated in larval stage with prochloraz to infection with Nosema ceranae.

Uros Glavinic,Minja Zorc,Jevrosima Stevanovic,Mojca Narat,Ivanka Cizelj,Zoran Stanimirovic,Tanja Tesovnik

doi:10.7717/peerj.6325

Abstract

Among numerous factors that contribute to honey bee colony losses and problems in beekeeping, pesticides and Nosema ceranae have been often reported. In contrast to insecticides, whose effects on bees have been widely studied, fungicides did not attract considerable attention. Prochloraz, an imidazole fungicide widely used in agriculture, was detected in honey and pollen stored inside hives and has been already proven to alter immune gene expression of honey bees at different developmental stages. The aim of this study was to simulate the realistic conditions of migratory beekeeping, where colonies, both uninfected and infected with N. ceranae, are frequently transported to the vicinity of crop fields treated with prochloraz. We investigated the combined effect of prochloraz and N. ceranae on honey bees that faced fungicide during the larval stage through food consumption and microsporidium infection afterwards. The most pronounced changes in gene expression were observed in newly emerged Nosema-free bees originating from colonies previously contaminated with prochloraz. As exclusively upregulation was registered, prochloraz alone most likely acts as a challenge that induces activation of immune pathways in newly emerged bees. The combination of both stressors (prochloraz and Nosema infection) exerted the greatest effect on six-day-old honey bees. Among ten genes with significantly altered expression, half were upregulated and half downregulated. N. ceranae as a sole stressor had the weakest effects on immune gene expression modulation with only three genes significantly dysregulated. In conclusion, food contaminated with prochloraz consumed in larval stage could present a threat to the development of immunity and detoxification mechanisms in honey bees.

Highlights

The value of honey bees (Apis mellifera), as honey producers, is minor compared to their inestimable role in the pollination of crops and wild plants (De la Rua et al, 2009; Gallai et al, 2009; Moritz et al, 2010)
Significant upregulation of gene expression was noticed for genes encoding Toll (1.88; p < 0.01), Dorsal-1 (1.17; p < 0.01), Kayak (0.80; p < 0.05) and antimicrobial peptide (AMP) Lysozyme-2 (0.88; p < 0.01)
Unlike previous finding of host immune suppression by N. ceranae infection (Antunez et al, 2009; Chaimanee et al, 2012; Glavinic et al, 2017), it seems that this study revealed only weak reaction to this parasite as the sole stressor

Summary

Introduction

The value of honey bees (Apis mellifera), as honey producers, is minor compared to their inestimable role in the pollination of crops and wild plants (De la Rua et al, 2009; Gallai et al, 2009; Moritz et al, 2010). Pesticides used in agriculture indirectly contribute to colony collapses and bee declines by increasing negative effects of diseases and/or parasites (Sanchez-Bayo & Goka, 2014). Prochloraz is an imidazole fungicide with an ergosterol-biosynthesis inhibiting (EBI) function that is widely used (Vinggaard et al, 2006) and found in honey and pollen stored inside hives (Lambert et al, 2013). Previous studies have shown that prochloraz, used alone and in combination with coumaphos, inhibited the detoxification activity of cytochrome P450 (Johnson et al, 2006) and altered immune gene expression in honey bees (Cizelj et al, 2016)

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