The defensive function of a pollinator-attracting floral volatile

Benzyl acetone (4-phenylbutan-2-one; BA), the dominant floral fragrance of the wild tobacco Nicotiana attenuata, is known to attract night-time pollinators, such as Manduca sexta hawkmoths. For this pollinator, BA is not only essential for the pollen transport between conspecific plants, but also for the moth’s short-distance handling of flowers at night. The emission of BA from the corolla limb, however, starts up to 4 hr before dusk, peaks at dusk and continues throughout the first half of the night. While the function of the nocturnal part of the emission is well studied, the function of the early part of the peak emission remained unknown. By using plants silenced in the expression of the biosynthetic gene of BA (Nachal1), we investigated the function of this early peak emission of BA in the plants´ native habitat in Southwestern Utah. By emitting BA before dusk, N. attenuata is able to prevent the establishment and resulting floral damage by a florivore, the cucumber beetle (Diabrotica undecimpunctata). Plants lacking BA emissions (CHAL) were not only more often colonized by florivores, but also suffered significantly more damage, than control empty vector plants (EV). Choice assays revealed that D. undecimpunctata feeding required the absence of BA. While feeding damage to CHAL flowers was higher than to EV flowers in the early night hours, the effect disappeared during the second half of the night, when flowers stop emitting BA. The close proximity of BA-emitting flowers to non-emitting CHAL flowers prevented D. undecimpunctata feeding. In the field, the emission of BA at dusk was sufficient to protect plants for the entire night, as beetles search for new hosts during the early evening hours and remain for the duration of the night, once a host is chosen. Floral BA emission before dusk may have evolved as a consequence of antagonistic interactions with florivores. A single floral volatile can thus simultaneously function as an important floral attractant for pollinators and as effective feeding deterrent against florivores in the same plant species. A plain language summary is available for this article.