Nosema spp. Infection Alters Pheromone Production in Honey Bees (Apis mellifera)

Abstract

Pheromones in social insects play a key role in the regulation of group homoeostasis. It is well-established that parasites can modify hormone signaling of their host, but less is known about the effect of parasites on pheromone signaling in insect societies. We, thus, tested in honey bees (Apis mellifera) the effect of the widespread parasite Nosema spp. on the production of ethyl oleate (EO), the only identified primer pheromone in honey bee workers. Since environmental stressors like pesticides also can weaken honey bees, we also analyzed the effect of imidacloprid, a neonicotinoid widely used in agriculture, on EO production. We show that, contrary to imidacloprid, Nosema spp. significantly altered EO production. In addition, the level of Nosema infection was correlated positively with the level of EO production. Since EO is involved in the regulation of division of labor among workers, our result suggests that the changes in EO signaling induced by parasitism have the potential to disturb the colony homoeostasis.

The effect of induced queen replacement on Nosema spp. infection in honey bee (Apis mellifera iberiensis) colonies

“…This findings suggest that in these colonies with lower Nosema infection rates the number of sick bees was inferior, and thus, the overall hive performance and health status may present more optimal levels in comparison with colonies with higher number of infected bees. Moreover, Nosema infection has been shown to affect the physiology and behaviour of the infected honey bees, having an impact over their pheromones production (Dussaubat et al ., 2010), immune response (Antúnez et al ., 2009), flight behaviour (Kralj and Fuchs, 2010), and inducing an energetic stress (Mayack and Naug, 2009; Martín‐Hernández et al ., 2011a), behavioural fever (Campbell et al ., 2010) and hunger‐mediated conduct (Naug and Gibbs, 2009) at the individual level. Because variation in individual honey bee behaviour and physiology relates to variation in colony state (Schmid‐Hempel et al ., 1993; Khoury et al ., 2011), all these factors affecting infected bees may cause damage at the social level and have detrimental effects on colony homeostasis, and therefore, the less infected colonies may be less prone to collapse (Higes et al ., 2008) or to suffer other problems associated with more heavily infected colonies (group B2).…”

“…Furthermore, histopathological analysis of the queens removed did not reveal any indication of degeneration in the ovaries due to viral infection (Gauthier et al ., 2011), or signs of Nosema infection in the ventriculi and ovaries (Liu, 1992). The decrease in the adult bee population size may be related to the broodless period observed in colonies that lost their queen (group B1) or to the constant loss of infected adult bees due to the pathogenic effects of Nosema in the case of the highly infected colonies (group B2; Higes et al ., 2008; 2009a; 2010; Dussaubat et al ., 2010; Kralj and Fuchs, 2010; Mayack and Naug, 2010; Suwannapong et al ., 2010).…”

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

“…N. ceranae increases energetic demand in honeybees [20], [22] and decreases hemolymph sugar level [23]. Furthermore, N. ceranae infection significantly suppresses the honeybee immune response [20], [24] and increases ethyl -oleate content (a primer pheromone which regulates worker behavioral maturation) [25]. Finally, N. ceranae -infected honeybees have shorter life-spans than uninfected honeybees [20], [26].…”

Gas chromatography–mass spectrometry metabolite profiling of worker honey bee (Apis mellifera L.) hemolymph for the study of Nosema ceranae infection

“…Microsporidian fungi often alter their host's physiology, suppress their immune system and alter behavior in order to maintain a more favorable environment thus prolonging their ability to reproduce (Antúnez et al, 2009;Fisher, 1963;Fisher and Sanborn, 1964;Keeling and Fast, 2002;Kelly et al, 2002;Mathis, 2000). Recent studies have demonstrated that N. ceranae infections can alter the energy demands of honey bees (Martín-Hernández et al, 2011;Mayack and Naug, 2009;Naug and Gibbs, 2009), suppress their immune system (Antúnez et al, 2009) and alter pheromone production in worker and queen honey bees (Alaux et al, 2011;Dussaubat et al, 2010). The fungal parasite enters the adult bee orally and multiplies in its gut and spreads to different glands (Copley and Jabaji, 2012), imposing a metabolic demand on its host (Naug and Gibbs, 2009) and proliferates until the nutrients in the host-cells are exhausted, which triggers sporulation.…”