Honeybees Tolerate Cyanogenic Glucosides from Clover Nectar and Flowers

Overview

Journal Insects

Specialty Biology

Date 2018 Mar 14

PMID 29534004

Citations 7

Authors

Antoine Lecocq

Amelia A Green

Erika Cristina Pinheiro de Castro

Carl Erik Olsen

Annette B Jensen

Mika Zagrobelny

Affiliations

Soon will be listed here.

Abstract

Honeybees () pollinate flowers and collect nectar from many important crops. White clover () is widely grown as a temperate forage crop, and requires honeybee pollination for seed set. In this study, using a quantitative LC-MS (Liquid Chromatography-Mass Spectrometry) assay, we show that the cyanogenic glucosides linamarin and lotaustralin are present in the leaves, sepals, petals, anthers, and nectar of . Cyanogenic glucosides are generally thought to be defense compounds, releasing toxic hydrogen cyanide upon degradation. However, increasing evidence indicates that plant secondary metabolites found in nectar may protect pollinators from disease or predators. In a laboratory survival study with chronic feeding of secondary metabolites, we show that honeybees can ingest the cyanogenic glucosides linamarin and amygdalin at naturally occurring concentrations with no ill effects, even though they have enzyme activity towards degradation of cyanogenic glucosides. This suggests that honeybees can ingest and tolerate cyanogenic glucosides from flower nectar. Honeybees retain only a portion of ingested cyanogenic glucosides. Whether they detoxify the rest using rhodanese or deposit them in the hive should be the focus of further research.

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References

Anderson K, Sheehan T, Mott B, Maes P, Snyder L, Schwan M . Microbial ecology of the hive and pollination landscape: bacterial associates from floral nectar, the alimentary tract and stored food of honey bees (Apis mellifera). PLoS One. 2013; 8(12):e83125. PMC: 3866269. DOI: 10.1371/journal.pone.0083125. View

Mustard J, Dews L, Brugato A, Dey K, Wright G . Consumption of an acute dose of caffeine reduces acquisition but not memory in the honey bee. Behav Brain Res. 2012; 232(1):217-24. DOI: 10.1016/j.bbr.2012.04.014. View

Lee F, Rusch D, Stewart F, Mattila H, Newton I . Saccharide breakdown and fermentation by the honey bee gut microbiome. Environ Microbiol. 2014; 17(3):796-815. DOI: 10.1111/1462-2920.12526. View

Ayestaran A, Giurfa M, de Brito Sanchez M . Toxic but drank: gustatory aversive compounds induce post-ingestional malaise in harnessed honeybees. PLoS One. 2010; 5(10):e15000. PMC: 2965165. DOI: 10.1371/journal.pone.0015000. View

Bruni I, Galimberti A, Caridi L, Scaccabarozzi D, De Mattia F, Casiraghi M . A DNA barcoding approach to identify plant species in multiflower honey. Food Chem. 2014; 170:308-15. DOI: 10.1016/j.foodchem.2014.08.060. View

Erler S, Denner A, Bobis O, Forsgren E, Moritz R . Diversity of honey stores and their impact on pathogenic bacteria of the honeybee, Apis mellifera. Ecol Evol. 2014; 4(20):3960-7. PMC: 4242578. DOI: 10.1002/ece3.1252. View

Hurst V, Stevenson P, Wright G . Toxins induce 'malaise' behaviour in the honeybee (Apis mellifera). J Comp Physiol A Neuroethol Sens Neural Behav Physiol. 2014; 200(10):881-90. PMC: 4169619. DOI: 10.1007/s00359-014-0932-0. View

Lai D, Picmanova M, Hachem M, Motawia M, Olsen C, Moller B . Lotus japonicus flowers are defended by a cyanogenic β-glucosidase with highly restricted expression to essential reproductive organs. Plant Mol Biol. 2015; 89(1-2):21-34. DOI: 10.1007/s11103-015-0348-4. View

Manson J, Otterstatter M, Thomson J . Consumption of a nectar alkaloid reduces pathogen load in bumble bees. Oecologia. 2009; 162(1):81-9. DOI: 10.1007/s00442-009-1431-9. View

10.

Wright G, Mustard J, Simcock N, Ross-Taylor A, McNicholas L, Popescu A . Parallel reinforcement pathways for conditioned food aversions in the honeybee. Curr Biol. 2010; 20(24):2234-40. PMC: 3011020. DOI: 10.1016/j.cub.2010.11.040. View

11.

Singaravelan N, Neeman G, Inbar M, Izhaki I . Feeding responses of free-flying honeybees to secondary compounds mimicking floral nectars. J Chem Ecol. 2005; 31(12):2791-804. DOI: 10.1007/s10886-005-8394-z. View

12.

Moller B . Functional diversifications of cyanogenic glucosides. Curr Opin Plant Biol. 2010; 13(3):338-47. DOI: 10.1016/j.pbi.2010.01.009. View

13.

Furstenberg-Hagg J, Zagrobelny M, Jorgensen K, Vogel H, Moller B, Bak S . Chemical defense balanced by sequestration and de novo biosynthesis in a lepidopteran specialist. PLoS One. 2014; 9(10):e108745. PMC: 4191964. DOI: 10.1371/journal.pone.0108745. View

14.

Klein A, Vaissiere B, Cane J, Steffan-Dewenter I, Cunningham S, Kremen C . Importance of pollinators in changing landscapes for world crops. Proc Biol Sci. 2006; 274(1608):303-13. PMC: 1702377. DOI: 10.1098/rspb.2006.3721. View

15.

Pentzold S, Zagrobelny M, Roelsgaard P, Moller B, Bak S . The multiple strategies of an insect herbivore to overcome plant cyanogenic glucoside defence. PLoS One. 2014; 9(3):e91337. PMC: 3953384. DOI: 10.1371/journal.pone.0091337. View

16.

Zagrobelny M, Bak S, Moller B . Cyanogenesis in plants and arthropods. Phytochemistry. 2008; 69(7):1457-68. DOI: 10.1016/j.phytochem.2008.02.019. View

17.

Pentzold S, Zagrobelny M, Bjarnholt N, Kroymann J, Vogel H, Olsen C . Metabolism, excretion and avoidance of cyanogenic glucosides in insects with different feeding specialisations. Insect Biochem Mol Biol. 2015; 66:119-28. DOI: 10.1016/j.ibmb.2015.10.004. View

18.

Palmer-Young E, Tozkar C, Schwarz R, Chen Y, Irwin R, Adler L . Nectar and Pollen Phytochemicals Stimulate Honey Bee (Hymenoptera: Apidae) Immunity to Viral Infection. J Econ Entomol. 2017; 110(5):1959-1972. DOI: 10.1093/jee/tox193. View

19.

Zagrobelny M, Scheibye-Alsing K, Jensen N, Moller B, Gorodkin J, Bak S . 454 pyrosequencing based transcriptome analysis of Zygaena filipendulae with focus on genes involved in biosynthesis of cyanogenic glucosides. BMC Genomics. 2009; 10:574. PMC: 2791780. DOI: 10.1186/1471-2164-10-574. View

20.

Hawkins J, de Vere N, Griffith A, Ford C, Allainguillaume J, Hegarty M . Using DNA Metabarcoding to Identify the Floral Composition of Honey: A New Tool for Investigating Honey Bee Foraging Preferences. PLoS One. 2015; 10(8):e0134735. PMC: 4550469. DOI: 10.1371/journal.pone.0134735. View