Nocturnal burst emissions of germacrene D from the open disk florets of pyrethrum flowers induce moths to oviposit on a nonhost and improve pollination success

Recent studies show that nocturnal pollinators may be more important to ecosystem function and food production than is currently appreciated. Here, we describe an agricultural field study of pyrethrum (Tanacetum cinerariifolium) flower pollination. Pyrethrum is genetically self-incompatible and thus is reliant on pollinators for seed set. Our pollinator exclusion experiment showed that nocturnal insects, particularly moths, significantly contribute to seed set and quality. We discovered that the most abundant floral volatile, the sesquiterpene (-)-germacrene D (GD), is key in attracting the noctuid moths Peridroma saucia and Helicoverpa armigera. Germacrene D synthase (GDS) gene expression regulates the specific GD production and accumulation in flowers, which, in contrast to related species, lose the habit of closing at night. We did observe that female moths also oviposited on pyrethrum leaves and flower peduncles, but found that only a small fraction of those eggs hatched. Larvae were severely stunted in development, most likely due to the presence of pyrethrin defense compounds. This example of exploitative mutualism, which blocks the reproductive success of the moth pollinator and depends on nocturnal interactions, is placed into an ecological context to explain why it may have developed.