A Semivolatile Floral Scent Marks the Shift to a Novel Pollination System in Bromeliads

• DOI: 10.1016/j.cub.2020.11.012
• Publication Date: 2020-12-17T23:58:06Z
• Authors: Paulo Milet-Pinheiro; Arthur Domingos-Melo; João B. Olivera; Nayara S.L. Albuq...; Ana Carolina G. C...; Sinzinando Albuqu...; Marcelo F.R. Silva; Daniela M.A.F. Na...; Artur C.D. Maia; Lise-Lotte Gundersen; Mario Schubert; Stefan Dötterl; Isabel C. Machado
• Keywords: Bromeliaceae; hummingbirds; 0106 biological sciences; pollination; Plant Nectar; semivolatile organic compounds; labdane-related diterpenes; Flowers; Bees; floral scents; orchid bees; 01 natural sciences; Pheromones; Perfume; Odorants; Animals; Cryptanthus; SVOCs; Pollination; copalol

Perfume flowers (sensu Vogel1) produce intense scents that function both as attractants and as the sole rewards for pollinators. The scent is collected exclusively by male euglossine bees and used during pre-mating behavior.2-5 Perfume flowers have evolved independently in 15 angiosperm families, with over 1,000 reported species across the Neotropical region.6 Members of Cryptanthus (Bromeliaceae) represent a puzzling exception among perfume flowers, as flowers produce nectar and do not emit a noticeable scent yet still attract euglossine males.7 Here, we studied the pollination ecology of Cryptanthus burle-marxii and decode the chemical communication between its flowers and euglossine males. Field observations revealed euglossine males and hummingbirds as potential pollinators. The bees always contacted anthers/stigma of C. burle-marxii while scraping the petals to obtain chemicals, whereas nectar-seeking hummingbirds normally only contacted the anthers. Based on gas chromatography-mass spectrometry/nuclear magnetic resonance analyses of flower scent samples and bioassays, we identified the diterpene copalol as the only floral scent compound triggering scent-gathering behavior in euglossine males. Unlike euglossine-bee-mediated pollination, hummingbird pollination is ancestral in the Cryptanthus clade, suggesting a case of an ongoing pollinator shift8-10 mediated by the evolution of perfume as a reward. Copalol was previously unknown as a floral scent constituent and represents the heaviest and least-volatile compound known to attract euglossine males. Our study provides the first experimental evidence that semivolatile floral compounds can mediate euglossine bee interactions. Male euglossine pollination in other plant species lacking noticeable floral scents11-13 suggests that semivolatile-mediated pollinator attraction is more widespread than currently appreciated.