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

Authors: CANE, JAMES - Retired ARS Employee; Gardner, Dale; WEBER, MELISSA - Utah State University

Submitted to: Biological Journal of the Linnean Society, London
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 9/8/2020
Publication Date: 10/30/2020
Citation: Cane, J., Gardner, D.R., Weber, M. 2020. Neurotoxic alkaloid in pollen and nectar excludes generalist bees from foraging at death-camas, Toxicoscordion paniculatum (Melanthiaceae). Biological Journal of the Linnean Society, London. 131(4):927-935. https://doi.org/10.1093/biolinnean/blaa159.
DOI: https://doi.org/10.1093/biolinnean/blaa159

Interpretive Summary: Many plants produce toxins in foliage, fruits or seeds that only specialist insects can tolerate or detoxify. Often such plants produce "safe" pollen and nectar. Pollen and nectar of death-camas is shown to have the same neurotoxic alkaloids as are in its foliage. Both larvae and adults of a non-specialist native bee were sickened and sometimes died when consuming this alkaloid or the plant's actual nectar. The toxin is a fast-acting irritant, however, which saves most bees from ingesting a lethal dose of the nectar or collecting it to feed their progeny. Honey bees are occasional victims when alternative bloom is absent and colony stores are low. This is a rare case of floral specialization by bees being enforced by a toxin in the pollen and nectar.

Technical Abstract: Many plants produce toxins to which specialist herbivores – typically insects – have evolved counter-adaptations, sometimes spawning a co-evolutionary arms race. Although many non-social bee species are likewise taxonomic host specialists, pollination guilds at the specialists’ pollen hosts frequently include diverse floral generalists as well, even on plants that are otherwise chemically defended. In this study, we show that pollen and nectar of foothills death-camas (Toxicoscordion [=Zigadenus] paniculatum) contains zygacine, the alkaloid responsible for this plant’s notorious mammalian toxicity. Adults of the generalist solitary bee, Osmia lignaria (Megachilidae), were repelled, paralyzed and sometimes died when fed biologically relevant doses of zygacine in nectar or syrup; larval progeny eating dosed provision masses were likewise sickened and sometimes died. When offered death-camas racemes, hungry adults soon transitioned from feeding to prolonged bouts of proboscis grooming. Such deterrence probably explains the absence of this and 50+ other vernal bee species from death-camas flowers. The sole pollinating bee, Andrena astragali, is apparently monolectic, collecting only death-camas pollen and nectar to feed itself and its progeny. Thus, pollen and nectar toxins exclude generalist pollinators from foraging at death-camas, despite demonstrated benefits of pollinators for its seed set.