This usually induces changes in insect development, behavior, reproduction and parasite tolerance. Physiological changes induced by parasitism can render insects more susceptible to environmental stressors such as pollutants and may cause a reduction of insect fitness. This trend is particularly exploited in the concept of integrated pest management where entomopathogenic parasites are used in association with Puromycin aminonucleoside insecticides at low doses. Honeybees are also victim to such joint effects between parasites and insecticides. Potential interactions between Nosema and pesticides have been firstly described by Ladas in 1972. More recently, Alaux et al. demonstrated that coexposure to microsporidian parasites and imidacloprid weakens honeybee. This result corroborates the hypothesis of a multifactorial cause for the massive colony losses observed worldwide. Two microsporidian species, Nosema apis and Nosema ceranae, are the agents of two major diseases known as nosemoses A and C, respectively. Both species are obligate intracellular parasites of adult honeybees. N. ceranae increases energetic demand in honeybees and decreases hemolymph sugar level. Furthermore, N. ceranae infection significantly suppresses the honeybee immune response and increases ethyl -oleate content. In this study, we showed that sublethal doses of a neonicotinoid and of a phenylpyrazole NVP-BAW2881 highly increased mortality of honeybees previously infected by the microsporidian parasite N. ceranae. Although the exact mechanism involved in this synergistic effect remains unclear, our data suggest that the sensitization process is not strongly linked to a decrease of detoxification capacity in infected bees or necessarily by an enhancement of N. ceranae proliferation after exposure to insecticides. During our experiments, no mortality was observed at 10 days p.i. in infected honeybees. Numerous foci were visible in their epithelial cells and a mean of spores/honeybee was measured in their digestive tract. Our results contrast with previous data by Higes et al. who described 100% of honeybee mortality at 8 days p.i. with N. ceranae, but are comparable to mortality rate and spore production observed. In addition, the very highly significant enhanced sucrose consumption by infected honeybees is consistent with the energetic stress recently described by Mayack and Naugh.
In sensitivity to complement and antibody to capsular polysaccharide
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