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Neonicotinoid clothianidin adversely affects insect immunity and promotes replication of a viral pathogen in honey bees.

ABSTRACT: Large-scale losses of honey bee colonies represent a poorly understood problem of global importance. Both biotic and abiotic factors are involved in this phenomenon that is often associated with high loads of parasites and pathogens. A stronger impact of pathogens in honey bees exposed to neonicotinoid insecticides has been reported, but the causal link between insecticide exposure and the possible immune alteration of honey bees remains elusive. Here, we demonstrate that the neonicotinoid insecticide clothianidin negatively modulates NF-κB immune signaling in insects and adversely affects honey bee antiviral defenses controlled by this transcription factor. We have identified in insects a negative modulator of NF-κB activation, which is a leucine-rich repeat protein. Exposure to clothianidin, by enhancing the transcription of the gene encoding this inhibitor, reduces immune defenses and promotes the replication of the deformed wing virus in honey bees bearing covert infections. This honey bee immunosuppression is similarly induced by a different neonicotinoid, imidacloprid, but not by the organophosphate chlorpyriphos, which does not affect NF-κB signaling. The occurrence at sublethal doses of this insecticide-induced viral proliferation suggests that the studied neonicotinoids might have a negative effect at the field level. Our experiments uncover a further level of regulation of the immune response in insects and set the stage for studies on neural modulation of immunity in animals. Furthermore, this study has implications for the conservation of bees, as it will contribute to the definition of more appropriate guidelines for testing chronic or sublethal effects of pesticides used in agriculture.

SUBMITTER: Di Prisco G

PROVIDER: S-EPMC3831983 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:Neonicotinoid insecticides applied to flowering crops can have negative impacts on bees, with implications for crop pollination. To assess if exposure to the neonicotinoid clothianidin via a treated crop (rapeseed) affected bee behaviour, pollination performance (to strawberry), and bee reproduction, we provided each of 12 outdoor cages with rapeseed (autumn-sown plants complemented with a few spring-sown plants to extend the flowering period) grown from either clothianidin-treated or untreated (control) seeds, together with strawberry plants and a small population of red mason bees (Osmia bicornis). We expected clothianidin to reduce bee foraging activity, resulting in impaired strawberry pollination and bee reproduction. During the early stage of the experiment, we observed no difference between treatments in the length of entire foraging trips, or the combined number of rapeseed and strawberry flowers that the bees visited during these trips. During the later stage of the experiment, we instead determined the time a female took to visit 10 rapeseed flowers, as a proxy for foraging performance. We found that they were 10% slower in clothianidin cages. Strawberries weighed less in clothianidin cages, suggesting reduced pollination performance, but we were unable to relate this to reduced foraging activity, because the strawberry flowers received equally many visits in the two treatments. Clothianidin-exposed females sealed their nests less often, but offspring number, sex ratio and weight were similar between treatments. Observed effects on bee behaviour appeared by the end of the experiment, possibly because of accumulated effects of exposure, reduced bee longevity, or higher sensitivity of the protocols we used during the later phase of the experiment. Although the lack of a mechanistic explanation calls for interpreting the results with cautiousness, the lower strawberry weight in clothianidin cages highlights the importance of understanding complex effects of plant protection products, which could have wider consequences than those on directly exposed organisms.

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Neonicotinoid clothianidin adversely affects insect immunity and promotes replication of a viral pathogen in honey bees.

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