Abstract
Plant phytochemicals can act as natural "medicines" for animals against parasites [1-3]. Some nectar metabolites, for example, reduce parasite infections in bees [4-7]. Declining plant diversity through anthropogenic landscape change [8-11] could reduce the availability of medicinal nectar plants for pollinators, exacerbating their decline [12]. Existing studies are, however, limited by (1) a lack of mechanistic insights into how phytochemicals affect pollinator diseases and (2) the restriction to few, commercially available chemicals, thereby potentially neglecting plants with the biggest antiparasitic effects. To rapidly identify plants with the greatest potential as natural bee medicines, we developed a bioactivity-directed fractionation assay for nectar metabolites. We evaluated 17 important nectar plants against the bumblebee pathogen Crithidia bombi (Trypanosomatidae) [13-17]. The most bioactive species washeather (Calluna vulgaris), the second most productive UK nectar plant [10]. We identified 4-(3-oxobut-1-enylidene)-3,5,5-trimethylcyclohex-2-en-1-one (callunene) from heather nectar as a potent inhibitor of C.bombi. Wild bumblebees (Bombus terrestris) foraging on heather ingest callunene at concentrations causing complete C.bombi inhibition. Feeding on callunene was prophylactic against infections. We show that C.bombi establishes infections by flagellar anchoring to the ileum epithelium. Short-term callunene exposure induced flagellum loss in C.bombi choanomastigotes, resulting in a loss of infectivity. We conclude that plant secondary metabolites can disrupt parasite flagellum attachment, revealing a mechanism behind their prophylactic effects. The decline of heathlands [18-21] reduces the availability of natural bee "medicine" and could exacerbate the contribution of diseases to pollinator declines. VIDEO ABSTRACT.
Highlights
Honey extracts varied in their inhibitory effects on C. bombi growth (Figure 1A)
As documented by Gorbunov [47] for Bombus pascuorum, we show that active infections with C. bombi in B. terrestris are restricted to the hindgut
Callunene Removes the Flagellum; Crithidia Loses Infectivity To determine the mechanism behind the prophylactic effect of callunene, we microscopically examined its direct effect on after 90 min in medium with 110 ppm callunene versus in control medium without callunene
Summary
Plant phytochemicals can act as natural ‘‘medicines’’ for animals against parasites [1,2,3]. To test the effect of this type of exposure with the associated flagellum loss on infection establishment, we first exposed C. bombi cells in vitro to 200 ppm callunene for 60 min (representing an average B. terrestris foraging bout duration [55], and with a callunene concentration within the range of the values recorded by us for wild B. terrestris crops) immediately before ingestion by bumblebee workers This exposure led to a significantly reduced infection rate in B. terrestris workers relative to controls (GLM, c2 = 5.6, p = 0.018), and an overall lower infection load (F(1,54) = 7.4, p = 0.0089) after 7 days (Figure 3B), with no significant impact of colony identity on infection rate (GLM, c2 = 0.4, p = 0.81) nor infection intensity (F(2,54) = 0.17, p = 0.85). In light of the growing threats to wild animal populations from pathogens, including emerging diseases [69, 70], and synergistic detrimental effects between diseases and man-made stressors such as pesticides [71,72,73,74] or climate change [75], there is an urgent need to identify those natural plant medicines that can mitigate wildlife diseases and act to protect them
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