Context-Dependent Medicinal Effects of Anabasine and Infection-Dependent Toxicity in Bumble Bees

Background Floral phytochemicals are ubiquitous in nature, and can function both as antimicrobials and as insecticides. Although many phytochemicals act as toxins and deterrents to consumers, the same chemicals may counteract disease and be preferred by infected individuals. The roles of nectar and pollen phytochemicals in pollinator ecology and conservation are complex, with evidence for both toxicity and medicinal effects against parasites. However, it remains unclear how consistent the effects of phytochemicals are across different parasite lineages and environmental conditions, and whether pollinators actively self-medicate with these compounds when infected. Approach Here, we test effects of the nectar alkaloid anabasine, found in Nicotiana, on infection intensity, dietary preference, and survival and performance of bumble bees (Bombus impatiens). We examined variation in the effects of anabasine on infection with different lineages of the intestinal parasite Crithidia under pollen-fed and pollen-starved conditions. Results We found that anabasine did not reduce infection intensity in individual bees infected with any of four Crithidia lineages that were tested in parallel, nor did anabasine reduce infection intensity in microcolonies of queenless workers. In addition, neither anabasine nor its isomer, nicotine, was preferred by infected bees in choice experiments, and infected bees consumed less anabasine than did uninfected bees under no-choice conditions. Furthermore, anabasine exacerbated the negative effects of infection on bee survival and microcolony performance. Anabasine reduced infection in only one experiment, in which bees were deprived of pollen and post-pupal contact with nestmates. In this experiment, anabasine had antiparasitic effects in bees from only two of four colonies, and infected bees exhibited reduced—rather than increased—phytochemical consumption relative to uninfected bees. Conclusions Variation in the effect of anabasine on infection suggests potential modulation of tritrophic interactions by both host genotype and environmental variables. Overall, our results demonstrate that Bombus impatiens prefer diets without nicotine and anabasine, and suggest that the medicinal effects and toxicity of anabasine may be context dependent. Future research should identify the specific environmental and genotypic factors that determine whether nectar phytochemicals have medicinal or deleterious effects on pollinators

Plant secondary metabolites enhance survival and pathogen tolerance in the European honey bee: a structure-function study

2019 Spring.Includes bibliographical references.Adequate nutrition is essential for European honey bee (Apis mellifera) colony growth, and productivity, yet foraging limitations resulting from factors such as habitat loss often lead to dietary deficiencies. Plant secondary metabolites are key constituents of floral nectar that support physiological processes in honey bees, however, these compounds are only available to bees with access to a diversity of floral resources. Furthermore, the relationship between different classes of plant secondary metabolites and their function within honey bee diets requires further investigation. Using a structure-function framework, we evaluated whether four structurally similar plant secondary metabolites found in the nectar of common agricultural crops elicit comparable effects on honey bee survival and pathogen tolerance. The addition of plant secondary metabolites to artificial nectar solution enhanced median survival, in some cases more than doubling the lifespan of worker honey bees. Moreover, plant secondary metabolites demonstrated nutraceutical effects, and sometimes elicited medicinal effects on honey bees infected with Nosema ceranae. Our findings provide a platform to identify plant secondary metabolites which can augment current management techniques to support the long-term sustainability of the apiculture industry

Dietary Phytochemicals, Honey Bee Longevity and Pathogen Tolerance

Continued loss of natural habitats with native prairies and wildflower patches is eliminating diverse sources of pollen, nectar and phytochemicals therein for foraging bees. The longstanding plant-pollinator mutualism reiterates the role of phytochemicals in sustaining plant-pollinator relationship and promoting honey bee health. We studied the effects of four phytochemicals—caffeine, gallic acid, kaempferol and p-coumaric acid, on survival and pathogen tolerance in the European honey bee, Apis mellifera (L.). We recorded longevity of worker bees that were provided ad libitum access to sugar solution supplemented with different concentrations of phytochemicals. We artificially infected worker bees with the protozoan parasite, Nosema ceranae. Infected bees were provided access to the same concentrations of the phytochemicals in the sugar solution, and their longevity and spore load at mortality were determined. Bees supplemented with dietary phytochemicals survived longer and lower concentrations were generally more beneficial. Dietary phytochemicals enabled bees to combat infection as seen by reduced spore-load at mortality. Many of the phytochemicals are plant defense compounds that pollinators have evolved to tolerate and derive benefits from. Our findings support the chemical bases of co-evolutionary interactions and reiterate the importance of diversity in floral nutrition sources to sustain healthy honey bee populations by strengthening the natural mutualistic relationships

Effects of <i>Crithidia</i> infection on microcolony performance in the Life History Experiment.

<p>Microcolonies were observed daily for (A) deaths, (B) time to first egg production, and (C) time to first honeypot construction. Line type represents infection treatment (solid lines for uninfected microcolonies; dotted lines for infected microcolonies). Line color represents anabasine treatment (red lines for 30% sucrose control; blue lines for 30% sucrose with 5 ppm anabasine). Crosses represent events (i.e., deaths, egg production, or honeypot construction) or censoring due to removal of the microcolony from the experiment.</p

Effects of 5 ppm anabasine treatment on <i>Crithidia</i> infection intensity in <i>Bombus impatiens</i> across three experiments.

<p>(A) Parasite Variation Experiment that tested effects of anabasine on infection of individual bees with one of four <i>Crithidia</i> lineages and reared individually. (B) Life History Experiment in which bees were reared in microcolonies of three workers. (C) Pollen Deprivation Experiment in which individual bees were deprived of pollen. Significance of terms in generalized linear mixed-effects models were tested by χ² tests. <i>Crithidia</i> cell counts were ln(x+1)-transformed to better conform to model assumptions. Marginal cell length refers to length of the right forewing marginal cell, used to estimate bee size (see <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0183729#sec010" target="_blank">Materials and Methods</a>). Colony refers to the bee’s experimental colony of origin.</p