The dilemma of being a fragrant flower: the major floral volatile attracts pollinators and florivores in the euglossine-pollinated orchid Dichaea pendula.

Abstract

Volatile organic compounds (VOCs) mediate both mutualistic and antagonistic plant-animal interactions; thus, the attraction of mutualists and antagonists by floral VOCs constitutes an important trade-off in the evolutionary ecology of angiosperms. Here, we evaluate the role of VOCs in mediating communication between the plant and its mutualist and antagonist floral visitors. To assess the evolutionary consequences of VOC-mediated signalling to distinct floral visitors, we studied the reproductive ecology of Dichaea pendula, assessing the effects of florivores on fruit set, the pollination efficiency of pollinators and florivores, the floral scent composition and the attractiveness of the major VOC to pollinators and florivores. The orchid depends entirely on orchid-bees for sexual reproduction, and the major florivores, the weevils, feed on corollas causing self-pollination, triggering abortion of 26.4% of the flowers. Floral scent was composed of approximately 99% 2-methoxy-4-vinylphenol, an unusual floral VOC attractive to pollinators and florivores. The low fruit set from natural pollination (5.6%) compared to hand cross-pollination (45.5%) and low level of pollinator visitation [0.02 visits (flower hour)-1] represent the limitations to pollination. Our research found that 2-methoxy-4-vinylphenol mediates both mutualistic and antagonistic interactions, which could result in contrary evolutionary pressures on novo-emission. The scarcity of pollinators, not florivory, was the major constraint to fruit set. Our results suggest that, rather than anti-florivory adaptations, adaptations to enhance pollinator attraction and cross-pollination might be the primary drivers of the evolution of VOC emission in euglossine-pollinated flowers.