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

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.

Looking for the causes of and solutions to the issue of honey bee colony losses

“…Moreover, prochloraz altered the immune-gene expression in honey bees used alone and in combination with coumaphos [63,151]. Recently, Glavinic et al [138] monitored the expression of 15 immune-related genes in adult honey bees, and found that it may be affected when food contaminated with prochloraz was consumed by bee larvae (Figure 9). The results were obtained using a combination of a fi eld and laboratory experiment which simulated the conditions where N. ceranae-infected and uninfected bee colonies are close enough to crop fi elds treated with prochloraz.…”

“…Far more frequently it was detected that N. ceranae and synergistic factors have deleterious effects on bees. For example, concurrent presence of N. ceranae and viruses have been confi rmed to be capable of producing severe losses of honeybee colonies [132][133][134], while combinations of N. ceranae and pesticides were proved to increase the mortality of bees and alter the expression of immunity-related genes [135][136][137][138]. However, in the case of N. ceranae and thiacloprid combination, only the higher pesticide dose elicited signifi cant mortality in bees, since thiacloprid showed a negative impact on N. ceranae reproduction [139].…”

“…Therefore, a great probability of crop contamination and, consequently, of the brood intended to produce the population of winter bees is likely. This new experimental approach introduced by Glavinic et al [138] enables the insight into the realistic situation when beekeepers move their hives to sunfl ower forage, which is frequently the last one, so the bees are wintered on sunfl ower-derived food. In the control of Nosema infection the introduction of good apitechnical practice is proposed, which includes: replacement of the queen with a new, young, promiscuous and healthy one [152], feeding colonies with high-quality food (honey and bee bread), additional feeding with sugar syrup enriched with pollen and/or supplements, disinfection of hives and other equipment, sterilization of combs and removal of excess humidity from the hives.…”

“…In Serbia, like in the majority of the world, the use of fumagillin is not recommended due to its adverse effects on bees [154,155], the quality of bee products and consumer health, which result from its inadequate use [44,45,47,156,157]. Boxes marked with an asterisk show statistically signifi cant effects of the treatment on gene expression, when p-value was equal or less than 0.05 [138].…”

Impact of Protoporphyrin Lysine Derivatives on the Ability of Nosema ceranae Spores to Infect Honeybees

“…However, in North America and Europe, infections caused by N. ceranae have become increasingly common, and N. ceranae exhibits stronger virulence than N. apis [14][15][16][17]. Exposure of honeybees to xenobiotic pesticides and other environmental chemicals increases their susceptibility to N. ceranae infection upon exposure to the parasite [18,19]. The synergic interaction between chemicals and Nosema is reflected in the low survival rate of honeybees exposed to both of these factors [20].…”