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

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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.

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Acknowledgments

We thank the Núcleo Santa Virgínia staff, COTEC/IF 41.065/2005and IBAMA/CGEN 093/2005 permits for the logistic help in field work, and MSc. Daniela de Cássia Bená and Prof. Dr. SérgioVanin for identifying the Montella sp. n. weevils. We also thank Arodi and Felipe Goulart Gonçalves for technical support for the laboratory bioassays at ESALQ, and Ludmila M. Pansarin, Jeff Ollerton, Fábio Pinheiro, Felipe Amorim, Kayna Agostini, Alexandre Neutzling and Pietro Kiyoshi Maruyama for the helpful comments on the previous versions of the manuscript. This work was supported by the Conselho Nacional de Desenvolvimento Científico e Tecnológico (Grant nos. 148221/2012-2 to C.E.P.N. and 303084/2011-1 to M.S.) and the National Institute of Science and Technology (INCT) Semiochemicals in Agriculture (CNPq Process 573761/2008-6 and FAPESP Process 2008/57701-2).

Author contribution statement

CEPN conceived the idea for the study. CEPN and MFGVP performed the experiments and analysed the data. CEPN, MFGVP, JMB, MJS and MS discussed the results. CEPN wrote the first draft; CEPN, MFGVP, JMB, MJS and MS contributed to the writing of the manuscript.

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Authors and Affiliations

  1. Graduate Program in Plant Biology, University of Campinas, Rua Monteiro Lobato 255, Cidade Universitária “Zeferino Vaz”, Campinas, 13083-970, Brazil

    Carlos E. P. Nunes

  2. Department of Entomology and Acarology, University of São Paulo, Escola Superior de Agricultura “Luiz de Queiroz” (ESALQ), Piracicaba, Brazil

    Maria Fernanda G. V. Peñaflor & José Maurício S. Bento

  3. Department of Plant Biology, Institute of Biology, University of Campinas, Campinas, Brazil

    Marcos José Salvador & Marlies Sazima

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  1. Carlos E. P. Nunes
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  2. Maria Fernanda G. V. Peñaflor
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  3. José Maurício S. Bento
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  4. Marcos José Salvador
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  5. Marlies Sazima
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Correspondence to Carlos E. P. Nunes.

Additional information

Communicated by Martin Heil.

In a multidisciplinary and innovative way, this study provides not only basic novel information about the reproductive ecology and pollination mechanism of an orchid but also presents fresh data on the functional chemical ecology of the interaction between the plant and its florivores, providing us with a mechanistic understanding of two plant–animal interactions: pollination and herbivory.

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Nunes, C.E.P., Peñaflor, M.F.G.V., Bento, J.M.S. et al. The dilemma of being a fragrant flower: the major floral volatile attracts pollinators and florivores in the euglossine-pollinated orchid Dichaea pendula . Oecologia 182, 933–946 (2016). https://doi.org/10.1007/s00442-016-3703-5

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