Exposure to Sublethal Doses of Fipronil and Thiacloprid Highly Increases Mortality of Honeybees Previously Infected by Nosema ceranae

Abstract

BackgroundThe honeybee, Apis mellifera, is undergoing a worldwide decline whose origin is still in debate. Studies performed for twenty years suggest that this decline may involve both infectious diseases and exposure to pesticides. Joint action of pathogens and chemicals are known to threaten several organisms but the combined effects of these stressors were poorly investigated in honeybees. Our study was designed to explore the effect of Nosema ceranae infection on honeybee sensitivity to sublethal doses of the insecticides fipronil and thiacloprid.Methodology/FindingFive days after their emergence, honeybees were divided in 6 experimental groups: (i) uninfected controls, (ii) infected with N. ceranae, (iii) uninfected and exposed to fipronil, (iv) uninfected and exposed to thiacloprid, (v) infected with N. ceranae and exposed 10 days post-infection (p.i.) to fipronil, and (vi) infected with N. ceranae and exposed 10 days p.i. to thiacloprid. Honeybee mortality and insecticide consumption were analyzed daily and the intestinal spore content was evaluated 20 days after infection. A significant increase in honeybee mortality was observed when N. ceranae-infected honeybees were exposed to sublethal doses of insecticides. Surprisingly, exposures to fipronil and thiacloprid had opposite effects on microsporidian spore production. Analysis of the honeybee detoxification system 10 days p.i. showed that N. ceranae infection induced an increase in glutathione-S-transferase activity in midgut and fat body but not in 7-ethoxycoumarin-O-deethylase activity.Conclusions/SignificanceAfter exposure to sublethal doses of fipronil or thiacloprid a higher mortality was observed in N. ceranae-infected honeybees than in uninfected ones. The synergistic effect of N. ceranae and insecticide on honeybee mortality, however, did not appear strongly linked to a decrease of the insect detoxification system. These data support the hypothesis that the combination of the increasing prevalence of N. ceranae with high pesticide content in beehives may contribute to colony depopulation.

Honeybee health in Africa—a review

“…These negative effects can become even more pronounced when honeybees are simultaneously exposed to multiple stressors, i.e. pathogens or parasites (Vidau et al 2011;Köhler et al 2012). Pettis et al (2012) reported a higher infection of Nosema species in honeybees exposed to neonicotinoids, while Aufauvre et al (2012) demonstrated the impact of multiple exposure to both parasites and pesticides.…”

Resistance of developing honeybee larvae during chronic exposure to dietary nicotine

“…For example, sublethal neonicotinoid exposure can impair learning and memory in honeybee foragers (Williamson and Wright, 2013), and combined pesticide exposure reduces the foraging performance and colony growth of bumblebees (Gill et al, 2012). Pesticide exposure can increase vulnerability to a range of other stressors: for example, laboratory studies have shown increased worker bee mortality and energetic stress due to interactions between Nosema ceranae infection and sublethal doses of pesticides (Alaux et al, 2010a;Vidau et al, 2011). At the colony level, previous exposure to sublethal doses of neonicotinoid led to higher infection levels after challenge with N. ceranae (Pettis et al 2012).…”

Distribution, epidemiological characteristics and control methods of the pathogen Nosema ceranae Fries in honey bees Apis mellifera L. (Hymenoptera, Apidae)

“…It is at this point that evidence of degeneration appears, with a mortality rate of 66.7 % on the sixth day, 94.1 % on the seventh day and 100% on the eighth day . Vidau et al (2011) on the other hand reported maximum mortality 20 days after infection (47 %). Higes et al (2013) indicate that the cause of these mortalities is the fact that N. ceranae prevents apoptosis in the epithelial cells of the infected ventricle.…”

“…It has been shown that sub-lethal doses of insecticides may increase mortality in bees previously infected by N. ceranae, making the bees more susceptible to the insecticides (Vidau et al 2011).…”

“…and to imidacloprid (Alaux et al 2010). Likewise the combination of N. ceranae and fipronil has led to a synergetic effect on mortality in honey bees, independent of the order of exposure to the stress factors (Vidau et al 2011, Aufauvre et al 2012.…”