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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...

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Autores principales: Palmer-Young, Evan C., Hogeboom, Alison, Kaye, Alexander J., Donnelly, Dash, Andicoechea, Jonathan, Connon, Sara June, Weston, Ian, Skyrm, Kimberly, Irwin, Rebecca E., Adler, Lynn S.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2017
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5568382/
https://www.ncbi.nlm.nih.gov/pubmed/28832668
http://dx.doi.org/10.1371/journal.pone.0183729
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author Palmer-Young, Evan C.
Hogeboom, Alison
Kaye, Alexander J.
Donnelly, Dash
Andicoechea, Jonathan
Connon, Sara June
Weston, Ian
Skyrm, Kimberly
Irwin, Rebecca E.
Adler, Lynn S.
author_facet Palmer-Young, Evan C.
Hogeboom, Alison
Kaye, Alexander J.
Donnelly, Dash
Andicoechea, Jonathan
Connon, Sara June
Weston, Ian
Skyrm, Kimberly
Irwin, Rebecca E.
Adler, Lynn S.
author_sort Palmer-Young, Evan C.
collection PubMed
description 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.
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spelling pubmed-55683822017-09-09 Context-dependent medicinal effects of anabasine and infection-dependent toxicity in bumble bees Palmer-Young, Evan C. Hogeboom, Alison Kaye, Alexander J. Donnelly, Dash Andicoechea, Jonathan Connon, Sara June Weston, Ian Skyrm, Kimberly Irwin, Rebecca E. Adler, Lynn S. PLoS One Research Article 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. Public Library of Science 2017-08-23 /pmc/articles/PMC5568382/ /pubmed/28832668 http://dx.doi.org/10.1371/journal.pone.0183729 Text en © 2017 Palmer-Young et al http://creativecommons.org/licenses/by/4.0/ This is an open access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
spellingShingle Research Article
Palmer-Young, Evan C.
Hogeboom, Alison
Kaye, Alexander J.
Donnelly, Dash
Andicoechea, Jonathan
Connon, Sara June
Weston, Ian
Skyrm, Kimberly
Irwin, Rebecca E.
Adler, Lynn S.
Context-dependent medicinal effects of anabasine and infection-dependent toxicity in bumble bees
title Context-dependent medicinal effects of anabasine and infection-dependent toxicity in bumble bees
title_full Context-dependent medicinal effects of anabasine and infection-dependent toxicity in bumble bees
title_fullStr Context-dependent medicinal effects of anabasine and infection-dependent toxicity in bumble bees
title_full_unstemmed Context-dependent medicinal effects of anabasine and infection-dependent toxicity in bumble bees
title_short Context-dependent medicinal effects of anabasine and infection-dependent toxicity in bumble bees
title_sort context-dependent medicinal effects of anabasine and infection-dependent toxicity in bumble bees
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5568382/
https://www.ncbi.nlm.nih.gov/pubmed/28832668
http://dx.doi.org/10.1371/journal.pone.0183729
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