Compound-Specific Behavioral and Enzymatic Resistance to Toxic Milkweed Cardenolides in a Generalist Bumblebee Pollinator

Jones, Patricia L.; Martin, Kyle R; Prachand, Sejal V; Hastings, Amy P.; Duplais, Christophe; Agrawal, Anurag A.

doi:10.1007/s10886-023-01408-3

Cited by 4 publications

(6 citation statements)

References 51 publications

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“…We show that the same secondary metabolite can be preferred at low concentrations while being avoided at the high end of the natural range. We have used a commercially available cardenolide, ouabain, which does not naturally occur in milkweed plants, but is similar in structure and polarity to many of the wide range of cardenolides that do occur in milkweeds (Jones et al 2023a). Ouabain is reported from the tissues of two East African plants in the Apocynaceae: A. schimperi (Fraser and Tillie 1895) and S. gratus (Rowe 1916).…”

Section: Discussionmentioning

confidence: 99%

“…Milkweed nectar contains multiple different cardenolide compounds (Manson et al 2012, Villalona et al 2020). For example, Asclepias syriaca nectar contains ~ seven different cardenolides (Jones et al 2023a). None of these compounds is commercially available.…”

Section: Introductionmentioning

confidence: 99%

“…Similarly, ouabain has antimicrobial effects, evidenced in the reduction of the proportion of sugars microbes consumed (Vannette and Fukami 2016), highlighting that cardenolides like ouabain may act as nectar preservatives. One recent study did examine the effect of a milkweed‐specific cardenolide, glycosylated aspeciocide, on bumblebee behavior and found that bees were both behaviorally and enzymatically resistant to the toxic effects of glycosylated aspeciocide in comparison to ouabain (Jones et al 2023a). Bumblebees consumed less nectar with ouabain than nectar with glycosylated aspeciocide at the same concentration of 137 mmol ml –1 (the equivalent of 100 ng μl –1 for ouabain), and there was less inhibition of the bumblebee sodium‐potassium ATP‐ase with glycosylated aspeciocide than with ouabain.…”

Section: Introductionmentioning

confidence: 99%

“…Bumblebees consumed less nectar with ouabain than nectar with glycosylated aspeciocide at the same concentration of 137 mmol ml –1 (the equivalent of 100 ng μl –1 for ouabain), and there was less inhibition of the bumblebee sodium‐potassium ATP‐ase with glycosylated aspeciocide than with ouabain. In contrast, Drosophila melanogaster sodium–potassium ATP‐ases were equally inhibited by these two cardenolides (Jones et al 2023a). This study demonstrated compound‐specific effects of cardenolides on bumblebees, but milkweed cardenolides remain prohibitively labor‐intensive to obtain, especially at the levels necessary to conduct behavioral experiments with bees.…”

Section: Introductionmentioning

confidence: 99%

“…We tested a range of concentrations that occur for other cardenolides in milkweed nectar, from 10 to 100 ng μl –1 (Manson et al 2012). Only one of the many milkweed‐specific cardenolides, glycosylated aspeciocide, has been tested for its effects on bees, and was shown to inhibit the Na + /K + ATP‐ase less than ouabain (Jones et al 2023a). It is possible, therefore, that these concentrations of ouabain, while within the natural range of milkweed cardenolides, may have stronger (or otherwise different) effects on bees than milkweed‐specific compounds.…”

Section: Introductionmentioning

confidence: 99%

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Plant secondary metabolite has dose‐dependent effects on bumblebees

Jones,

Warburton,

Martin

2023

Oikos

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The presence of secondary metabolites in flower nectar can mediate interactions between plants, pollinators, herbivores, and microbes. Milkweeds range in concentrations of cardenolides in flower nectar from ~ 1 to 100 ng μl–1. Using three different behavioral assays with bumblebees Bombus impatiens, we examined the impacts of the commercially available cardenolide ouabain at the range of concentrations at which cardenolides naturally occur in milkweeds. We show that after four days of exposure bees in consumption assays drank more of a nectar solution with a low ouabain concentration of 10 ng μl–1 than the control sucrose nectar, and over the course of the experiment bees consumed less of the 100 ng μl–1 ouabain solution than the control. Bee activity levels in Petri dish arena assays were not impacted by ouabain consumption, even at the highest concentrations; however, in free‐flying choice assays, bees preferentially visited artificial flowers containing 10 ng μl–1 ouabain more than flowers with sucrose control, or flowers with 100 ng μl–1 of ouabain. We therefore conclude that cardenolides may provide plants advantages to pollination at the low end of the naturally occurring range of concentrations for cardenolides, but may be costly to plants at the high end of the range. This research highlights that secondary metabolites in nectar may be under selection to be maintained at low concentrations, and species with high concentrations of secondary metabolites may be under conflicting selection pressures to maintain high circulating levels to deter herbivores at the cost of reduced pollination.

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Section: Discussionmentioning

confidence: 99%