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More than euglossines: the diverse pollinators and floral scents of Zygopetalinae orchids

Abstract

Floral volatile organic compounds (VOCs) play important roles in plant-pollinator interactions. We investigated the reproductive ecology and floral VOCs of Zygopetalinae orchids to understand the relationship between floral scents and pollinators. We performed focal observations, phenological censuses and breeding system experiments in eight species in southeast Brazil. Floral scents were collected and analysed using SPME/GC-MS. We performed multivariate analyses to group species according to affinities of their VOCs and define compounds associated to each plant. Dichaea cogniauxiana was pollinated by weevils which use their developing ovules, while D. pendula was pollinated by the same weevils and perfume-collecting male euglossine bees. The other species were deceit-pollinated by bees. Zygopetalum crinitum was pollinated by carpenter bees, while W. warreana, Z. mackayi and Z. maxillare were bumblebee-pollinated. The latter was also pollinated by Centris confusa. Breeding system varied widely with no association to any pollinator group. Most VOCs are common to other floral scents. Zygopetalum crinitum presented an exclusive blend of VOCs, mainly composed of benzenoids. The scents of Pabstia jugosa, Promenaea xanthina and the Zygopetalum spp. were similar. The bumblebee-pollinated species have flowering periods partially overlapped, thus neither phenology nor pollinators constitute hybridization barriers among these species. Euglossines are not the only pollinators of Zygopetalinae. Different VOCs, size and lifespan of flowers are associated with distinct pollinators. A distinctive VOC bouquet may determine specialisation in carpenter bees or male euglossines within bee-pollinated flowers. Finally, visitation of deceit-pollinated flowers by perfume-collecting euglossines allows us to hypothesise how pollination by this group of bees had evolved.

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Acknowledgements

We thank the São Paulo Research Foundation (FAPESP) and the Thematic Project Functional Gradient (Process Number 03/12595-7) within the BIOTA/FAPESP Program - The Biodiversity Virtual Institute (http://www.biota.org.br/). We thank the Serra do Mar State Park (Núcleo Santa Virgínia) for permits (COTEC/IF 41.065/2005 and IBAMA/CGEN 093/2005) and logistic assistance during fieldwork. We thank MSc. Daniela de Cássia Bená and Prof. Dr. Sérgio Vanin for identifying the Montella spec. nov. weevils. We thank Maria E. P. Martucci and Leonardo Gobbo-Neto for additional fragrance headspace analyses of Z. crinitum, Ivan Sazima for the focal observations and pollinator images of Z. maxillare in Itatiaia National Park and H. Heider for additional observations and images of a euglossine floral visitor in W. warreana in Bolivia. C.E.P.N. thanks the National Counsel of Technological and Scientific Development (CNPq) for the PhD scholarship (148221/2012-2). M.W. thanks FAPESP for the post-doctoral fellowship (2013/15129-9). M.S. thanks CNPq for the research grant (303084/2011-1).

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Correspondence to Carlos E. P. Nunes.

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Communicated by: Sven Thatje

Electronic supplementary material

Visit of a female carpenter bee (Xylocopa sp.) to flowers of Zygopetalum crinitum. Note that the bee comes with a pollinarium from other individual, deposes it in the first visit to a flower, removes and carries on a pollinarium on its head after visiting different flowers from the inflorescence. (WMV 1632 kb)

Visit of a male euglossine bee (Euglossa sp.) to flowers of Zygopetalum crinitum. Note that the bee only lands several times onto sepals and lateral petals to collect perfumes, but do not touch the lip or the anthers, without removing or carrying pollen. (WMV 95261 kb)

Video 1

Visit of a female carpenter bee (Xylocopa sp.) to flowers of Zygopetalum crinitum. Note that the bee comes with a pollinarium from other individual, deposes it in the first visit to a flower, removes and carries on a pollinarium on its head after visiting different flowers from the inflorescence. (WMV 1632 kb)

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(DOCX 54458 kb)

Video 2

Visit of a male euglossine bee (Euglossa sp.) to flowers of Zygopetalum crinitum. Note that the bee only lands several times onto sepals and lateral petals to collect perfumes, but do not touch the lip or the anthers, without removing or carrying pollen. (WMV 95261 kb)

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Nunes, C.E.P., Wolowski, M., Pansarin, E.R. et al. More than euglossines: the diverse pollinators and floral scents of Zygopetalinae orchids. Sci Nat 104, 92 (2017) doi:10.1007/s00114-017-1511-3

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Keywords

  • Apidae
  • Atlantic forest
  • Bee
  • Chemical ecology
  • Deceit-pollination
  • Orchidaceae