Nosema parasitism in honey bees (Apis mellifera) impacts olfactory learning and memory and neurochemistry

Authors: Gage, Stephanie; KRAMER, CATHERINE - University Of Arizona; Calle, Samantha; Carroll, Mark; HEIEN, MICHAEL - University Of Arizona; DeGrandi-Hoffman, Gloria

Submitted to: Journal of Experimental Biology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 12/8/2017
Publication Date: 2/19/2018
Citation: Gage, S.L., Kramer, C., Calle, S.N., Carroll, M.J., Heien, M., Hoffman, G.D. 2018. Nosema parasitism in honey bees (Apis mellifera) impacts olfactory learning and memory and neurochemistry. Journal of Experimental Biology. https://doi.org/10.1242/jeb.161489.
DOI: https://doi.org/10.1242/jeb.161489

Interpretive Summary: Nosema sp. is an internal parasite of the honey bee, Apis mellifera, and one of the most significant factors contributing to colony losses (Goulson et al., 2015). Given the global importance of honey bee pollination to the reproduction of floral species and to agricultural productivity, it is important to understand how Nosema sp. parasitism affects honey bee health. In this study, we were interested to see whether Nosema affects the brain of the honey bee. There are reports of bees foraging poorly under infection, and we speculated that this parasite may affect the honey bee brain. To test this hypothesis, we used a behavioral test to assess whether the honey bee could smell properly, and whether they could learn and remember odors. These olfactory tasks are an important aspect of foraging behavior. We also analyzed brain chemistry of parasitized bees to see whether they were physiological changes in the brain. We found that nurse-aged bees outperform control bees in odor learning and memory, which suggests that parasitized bees are maturing faster. By forager age, however, Nosema-infected bees are slower to learn and show memory deficits. We also found significant differences in amino acids and important neurochemicals for behavior that were altered with infection. These findings suggest Nosema affects the brain and that cognitive tasks may be compromised. These results shed light into the relationship that exists between Nosema and the honey bee and gives us a new understanding of how this parasite may spread in managed colonies.

Technical Abstract: Nosema sp. is an internal parasite of the honey bee, Apis mellifera, and one of the leading contributors to colony losses worldwide. This parasite is found in the honey bee midgut, and has profound consequences on the host’s physiology. There are reports that Nosema sp. impairs foraging performance in honey bees, yet, it is unclear whether this parasite affects the bee’s neurobiology. In this study, we examine whether Nosema sp. affects odor learning and memory and whether the brains of parasitized bees show differences in amino acids and biogenic amines. We took newly emerged bees and fed them with a Nosema ceranae. At approximate nurse and forager ages, we employed an odor-associative conditioning assay using the proboscis extension reflex and two bioanalytical techniques to measure changes in brain chemistry. We found that nurse-aged bees infected with N. ceranae significantly outperform controls in odor learning and memory—suggestive of precocious foraging; but by forager age, infected bees were slower to learn and showed memory impairment. We also detected significant differences in amino acid concentrations, some of which are age-specific; as well as altered serotonin, octopamine, dopamine, and L-dopa concentrations in the honey bee brain of parasitized bees. These findings suggest N. ceranae parasitism extends to the brain and behavioral tasks may be compromised. These results yield new insight into the host—parasite dynamic of honey bees and N. ceranae, as well the neurochemistry of odor learning and memory under normal, and parasitic conditions.