Context-dependent medicinal effects of anabasine and infection-dependent toxicity in bumble bees

PLoS One. 2017 Aug 23;12(8):e0183729. doi: 10.1371/journal.pone.0183729. eCollection 2017.

Abstract

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.

MeSH terms

  • Anabasine / toxicity*
  • Animals
  • Bees / drug effects*
  • Bees / parasitology
  • Host-Parasite Interactions / drug effects
  • Infections / drug therapy*

Substances

  • Anabasine

Grants and funding

This research was funded by the National Science Foundation (NSF: nsf.gov) under NSFDEB-1258096 (to LSA and REI), NSF GRFP (DGE-0907995 to ECPY), and NSF DDIG (NSFDEB-1501907 to ECPY and LSA); by the National Research Initiative (NRI) Arthropod and Nematode Biology and Management Program of the United States Department of Agriculture (USDA: usda.gov) Cooperative State Research, Education, and Extension Service (CSREES) Grant USDA-AFRI 2013-02536 (to LSA and REI); by a National Institute of Food and Agriculture Predoctoral Fellowship (USDA-AFRI-2016-67011-24698 to EPY), and by the Garden Club of America (www.gcamerica.org) Centennial Pollinator Fellowship (ECPY). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.