Abstract

Secondary metabolites in floral nectar have been shown to reduce parasite load in two common bumble bee species. Previous studies on the effects of nectar secondary metabolites on parasitized bees have focused on single compounds in isolation; however, in nature, bees are simultaneously exposed to multiple compounds. We tested for synergistic effects of two alkaloids found in the nectar of Nicotiana spp. plants, nicotine and anabasine, on parasite load and mortality in bumble bees ( Bombus impatiens) infected with the intestinal parasite Crithidia bombi. Adult worker bees inoculated with C. bombi were fed nicotine and anabasine diet treatments in a factorial design, resulting in four nectar treatment combinations: 2 ppm nicotine, 5 ppm anabasine, 2ppm nicotine and 5 ppm anabasine together, or a control alkaloid-free solution. We conducted the experiment twice: first, with bees incubated under variable environmental conditions ('Variable'; temperatures varied from 10-35°C); and second, under carefully controlled environmental conditions ('Controlled'; 27°C incubator, constant darkness). In 'Variable', each alkaloid alone significantly decreased parasite loads, but this effect was not realized with the alkaloids in combination, suggesting an antagonistic interaction. Nicotine but not anabasine significantly increased mortality, and the two compounds had no interactive effects on mortality. In 'Controlled', nicotine significantly increased parasite loads, the opposite of its effect in 'Variable'. While not significant, the relationship between anabasine and parasite loads was also positive. Interactive effects between the two alkaloids on parasite load were non-significant, but the pattern of antagonistic interaction was similar to that in the variable experiment. Neither alkaloid, nor their interaction, significantly affected mortality under controlled conditions. Our results do not indicate synergy between Nicotiana nectar alkaloids; however, they do suggest a complex interaction between secondary metabolites, parasites, and environmental variables, in which secondary metabolites can be either toxic or medicinal depending on context.

Highlights

  • Throughout the past two decades, many wild and managed bee species have experienced severe declines (Allen-Wardell et al, 1998; Cameron et al, 2011; Potts et al, 2010)

  • Honey bees are deterred by nicotine in nectar (Köhler et al, 2012b), and both honey bees (Köhler et al, 2012b; Singaravelan et al, 2006) and bumble bees (Baracchi et al, 2015) are adversely affected by nicotine consumption when they are not infected by parasites

  • Half of bees fed nicotine-containing nectar died within 7 days of inoculation, which was nearly double the frequency of death in treatments without nicotine (Figure 1)

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Summary

Introduction

Throughout the past two decades, many wild and managed bee species have experienced severe declines (Allen-Wardell et al, 1998; Cameron et al, 2011; Potts et al, 2010). In many cases of bee decline, parasitism has been implicated as a potential cause (reviewed in Goulson et al, 2015 and Potts et al, 2010). Infection with the microsporidian pathogen Nosema ceranae may be responsible for cases of honey bee colony collapse in Spain (Higes et al, 2009). Bumble bee species that have experienced recent declines had significantly higher levels of Nosema bombi than the species whose populations were stable (Cameron et al, 2011). Finding means of mitigating the effects of parasitism on bees would be beneficial to the agricultural community as well as natural ecosystems

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