Flight behavior and pheromone changes associated to Nosema ceranae infection of honey bee workers (Apis mellifera) in field conditions.

Parasites are known to cause the loss of individuals in social insects. In honey bee colonies the disappearance of foragers is a common factor of the wide extended colony losses. The emergent parasite of the European honey bee Nosema ceranae has been found to reduce homing and orientation skills and alter metabolism of forager bees. N. ceranae-infected bees also show changes in Ethyl Oleate (EO) levels, which is so far the only primer pheromone identified in workers that is involved in foraging behavior. Thus, we hypothesized that N. ceranae (i) modifies flight activity of honey bees and (ii) induces EO changes that can alter foraging behavior of nestmates. We compared flight activity of infected bees and non-infected bees in small colonies using an electronic optic bee counter during 28 days. We measured EO levels by gas chromatography-mass spectrometry and spore-counts. Bee mortality was estimated at the end of the experiment. Infected bees showed precocious and a higher flight activity than healthy bees, which agreed with the more elevated EO titers of infected bees and reduced lifespan. Our results suggest that the higher EO levels of infected bees might delay the behavioral maturation of same age healthy bees, which might explain their lower level of activity. We propose that delayed behavioral maturation of healthy bees might be a protective response to infection, as healthy bees would be performing less risky tasks inside the hive, thus extending their lifespan. We also discuss the potential of increased flight activity of infected bees to reduce pathogen transmission inside the hive. Further research is needed to understand the consequences of host behavioral changes on pathogen transmission. This knowledge may contribute to enhance natural colony defense behaviors through beekeeping practices to reduce probability of colony losses.