Interactions between Nosema microspores and a neonicotinoid weaken honeybees (Apis mellifera)

Abstract

Global pollinators, like honeybees, are declining in abundance and diversity, which can adversely affect natural ecosystems and agriculture. Therefore, we tested the current hypotheses describing honeybee losses as a multifactorial syndrome, by investigating integrative effects of an infectious organism and an insecticide on honeybee health. We demonstrated that the interaction between the microsporidia Nosema and a neonicotinoid (imidacloprid) significantly weakened honeybees. In the short term, the combination of both agents caused the highest individual mortality rates and energetic stress. By quantifying the strength of immunity at both the individual and social levels, we showed that neither the haemocyte number nor the phenoloxidase activity of individuals was affected by the different treatments. However, the activity of glucose oxidase, enabling bees to sterilize colony and brood food, was significantly decreased only by the combination of both factors compared with control, Nosema or imidacloprid groups, suggesting a synergistic interaction and in the long term a higher susceptibility of the colony to pathogens. This provides the first evidences that interaction between an infectious organism and a chemical can also threaten pollinators, interactions that are widely used to eliminate insect pests in integrative pest management.

Resistance of developing honeybee larvae during chronic exposure to dietary nicotine

“…For example, sublethal neonicotinoid exposure can impair learning and memory in honeybee foragers (Williamson and Wright, 2013), and combined pesticide exposure reduces the foraging performance and colony growth of bumblebees (Gill et al, 2012). Pesticide exposure can increase vulnerability to a range of other stressors: for example, laboratory studies have shown increased worker bee mortality and energetic stress due to interactions between Nosema ceranae infection and sublethal doses of pesticides (Alaux et al, 2010a;Vidau et al, 2011). At the colony level, previous exposure to sublethal doses of neonicotinoid led to higher infection levels after challenge with N. ceranae (Pettis et al 2012).…”

Effects of host age on susceptibility to infection and immune gene expression in honey bee queens (Apis mellifera) inoculated with Nosema ceranae

“…N. ceranae infection has been reported to suppress the honey bee immune response (Antúnez et al 2009;Chaimanee et al 2012) and to affect hormone production by increasing ethyl oleate content . Moreover, N. ceranae induces an energetic stress (Mayack and Naug 2009;Alaux et al 2010;Martín-Hernández et al 2011) and oxidative stress in honey bees (Dussaubat et al 2012) and decreases the carbohydrate level in honeybee forager hemolymph (Mayack and Naug 2010). Similar to N. apis infection, honey bees, when infected with N. ceranae, have a shorter life span (Malone et al 1995;Goblirsch et al 2013).…”

Distribution, epidemiological characteristics and control methods of the pathogen Nosema ceranae Fries in honey bees Apis mellifera L. (Hymenoptera, Apidae)

“…As a consequence of the damage to their epithelial cells, the bees necessarily suffer energy stress (Alaux et al 2010), since the microsporidia use their remaining mitochondrial organelles to absorb the ATP of the host cell environment (Williams 2009). For this reason, honey bees affected by N. ceranae consume more food to meet their increased energy demand (Alaux et al 2010); because they are hungrier they are also more reluctant to share food, thus reducing the connectivity of the network within the colony (Naug and Gibbs 2009). In addition, there is significantly less trehalose in the hemolymph of foraging honey bees infected with N. ceranae than in uninfected foragers.…”