Neurotoxic alkaloid in pollen and nectar excludes generalist bees from foraging at death-camas,Toxicoscordion paniculatum(Melanthiaceae)

Abstract

Many plants produce broadly active toxins to which specialist herbivores—typically insects—have evolved counter-adaptations, sometimes spawning co-evolutionary arms races. Many non-social bee species are likewise taxonomic host specialists, but the specialists’ pollen hosts frequently attract diverse floral generalists as well, even to flowers of plants that are otherwise chemically defended. In this study of foothills death-camas, Toxicoscordion paniculatum (Nutt.) Rydberg (formerly Zigadenus), we show that its pollen and nectar both contain zygacine, the steroidal alkaloid responsible for this plant’s notorious mammalian toxicity. Hungry naïve adults of a generalist solitary bee, Osmia lignaria Say (Megachilidae), would briefly drink death-camas nectar or biologically relevant doses of zygacine in syrup, followed by prolonged bouts of irritable tongue grooming; many became paralyzed and some even died. Larvae fed dosed provision masses likewise often ceased feeding and sometimes died. Prolonged irritation and subsequent deterrence of foraging O. lignaria likely illustrates why it and 50+ other vernal bee species were absent from death-camas flowers in a five-state survey. The sole visiting bee, Andrena astragali, foraged exclusively at death-camas flowers for pollen and nectar. Thus, a toxic alkaloid found in death-camas pollen and nectar deters generalist bees from flowers of this pollinator-dependent monocot, restricting visitation to a single specialist bee that tolerates death-camas toxins and is its likely pollinator.

Regional plant abundance explains patterns of host use by pollen‐specialist bees in eastern North America

“…Thus, the pollen used by specialists is not avoided by generalists. Our results contrast with previous studies that focused on single genera or families of specialist host plants and found that generalist bees did not collect pollen from these plants (specifically, plants in the genera Cucurbita [Brochu et al, 2020] and Toxicoscordion [Cane et al, 2020], and in the family Asteraceae [Müller & Kuhlmann, 2008; Praz et al, 2008]). By sampling a wider range of host plant taxa, our study provides a broader test of the pollen quality hypothesis, and our results are consistent with those of another study that sampled a range of host plant taxa used by bees in the genus Andrena (Wood & Roberts, 2018).…”

“…The first hypothesis proposes that bees specialize on plants whose pollen is avoided by other bees. According to what we will call the "pollen quality hypothesis," pollen-specialist bees developed adaptations to feed on plants with low-quality pollen-pollen that possesses secondary compounds or other deterrents (Irwin et al, 2014;Rivest & Forrest, 2020;Stevenson, 2020) or that is low in protein content-and is thus avoided by other bee species (Brochu et al, 2020;Cane et al, 2020;McAulay et al, 2020;Müller & Kuhlmann, 2008;Praz et al, 2008;Trunz et al, 2020;Vanderplanck et al, 2020). This strategy could evolve to allow the bee to use an unexploited resource (Danforth et al, 2019), because low-quality and/ or defended pollen protects the bee and its offspring from brood parasites or fungal pathogens (Bernays & Graham, 1988;Giacomini et al, 2018;LoCascio et al, 2019;Spear et al, 2016;Wynns, 2012) or because a coevolutionary arms race occurred between the bee and its host plant during their evolutionary history (Danforth et al, 2019;Wcislo & Cane, 1996).…”

“…This strategy could evolve to allow the bee to use an unexploited resource (Danforth et al, 2019), because low-quality and/ or defended pollen protects the bee and its offspring from brood parasites or fungal pathogens (Bernays & Graham, 1988;Giacomini et al, 2018;LoCascio et al, 2019;Spear et al, 2016;Wynns, 2012) or because a coevolutionary arms race occurred between the bee and its host plant during their evolutionary history (Danforth et al, 2019;Wcislo & Cane, 1996). In support of this hypothesis are studies showing that generalist bees do not collect pollen from some plants used by specialists or that pollen used by specialists is harmful to some generalists (Brochu et al, 2020;Cane et al, 2020;Müller & Kuhlmann, 2008;Praz et al, 2008;Vanderplanck et al, 2017); however, these studies have mostly been conducted on single plant species (though see Trunz et al [2020]; Wood & Roberts [2018]). To our knowledge, there have been no attempts to test this hypothesis as a general explanation for specialization, across many bee and plant families.…”

Distribution of photoactive β‐carboline alkaloids across Passiflora caerulea floral organs

“…They also contain various plant metabolites, including alkaloids, that may act as repellents for herbivores and exhibit bactericidal and fungicidal properties. [58][59][60] In particular, Ha, Hol, and Hlol have been reported to have anti-herbivory properties against lepidopteran larvae, 61-64 as well as a significant antimicrobial activity. 25,34,[39][40][41] Therefore, their presence in the anthers could be related to their potential role either as repellent and/or antimicrobial agents.…”

“…Anthers are reproductive structures in plants that contain pollen, which is essential for plant reproduction. They also contain various plant metabolites, including alkaloids, that may act as repellents for herbivores and exhibit bactericidal and fungicidal properties 58–60 . In particular, Ha, Hol, and Hlol have been reported to have anti‐herbivory properties against lepidopteran larvae, 61–64 as well as a significant antimicrobial activity 25,34,39–41 .…”