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Tackling pollination of tubular flowers in Rutaceae and a case study of Conchocarpus rubrus (Galipeinae, Rutaceae)

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Abstract

Tubular flowers are only found in two distantly related groups in Rutaceae: the mainly Australian tribe Boronieae and the Neotropical subtribe Galipeinae. It is assumed that these nectar-rewarded, tubular flowers arose from convergent evolution driven by pollinator pressures. However, there are few empirical studies on pollen vectors of Neotropical Rutaceae. We explored the floral biology and pollination of Conchocarpus rubrus (A.St.-Hil.) Bruniera and Groppo (Galipeinae), including details about its nectar-secreting floral structures. We also compared the available records on floral biology and pollination of Boronieae and Galipeinae, aiming to provide a better understanding of the factors that influenced their floral evolution. Conchocarpus rubrus was pollinated by a single species of hermit hummingbird (Phaethornis idaliae Bourcier and Mulsant 1856) and by butterflies (Pyrginae and Pierinae), which take nectar accumulated at the bottom of the tube. Floral features and pollination data indicate that the convergent evolution of floral tubes in Rutaceae resulted from phenotypic specialization toward a subset of nectar-foraging pollinators with long mouth parts. Specifically, while in the Australian Boronieae the evolutive pathway toward sympetaly was likely influenced by Meliphagidae birds, in the Galipeinae, it was influenced by hummingbirds, butterflies, and settling moths. Besides a floral tube, floral features also linked to phenotypic specialization toward Meliphagidae pollination in Boronieae were related not only to birds’ attraction (nectar features, attractive colors, etc.), but also to insect impediments (sensory exclusion, absence of landing platforms, etc.), occurring together with other ornithophilous features. In Galipeinae, floral features are more diverse, and functionally linked to the different groups of pollinators herein found.

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Acknowledgments

The authors thank the technicians of the Plant Anatomy Laboratory (IB-USP), including Gisele R. Oliveira Costa, Tássia Cristina dos Santos, and Irwandro Roberto Pires, for their assistance to the first author; as well as Ludmila M. Pansarin (FFCLRP, São Paulo) for assistance during fieldwork. The first author also thanks Pietro K. Maruyama and Felipe W. Amorin for their helpful suggestions on nocturnal pollination records; David Martin for their linguistics suggestions; Diego Demarco, Maria do Carmo Amaral, Elza Guimarães, Anselmo Nogueira, and Leandro Freitas for their suggestions on a previous version of this manuscript. We also thank Instituto Federal do Espírito Santo for allowing us to work in their forest area. This work was supported by Fundação de Amparo à Pesquisa do Estado de São Paulo [Grant Numbers 09/54569-9 and 09/08764-4 awarded to J. H. L. El Ottra and J. R. Pirani], and Conselho Nacional de Desenvolvimento e Pesquisa for the productivity grant awarded to J. R. Pirani.

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  1. Departamento de Botânica, Instituto de Biociências, Universidade de São Paulo, Rua do Matão 277, São Paulo, São Paulo, 05508-090, Brazil

    Juliana Hanna Leite El Ottra & José Rubens Pirani

  2. Departamento de Biologia, Faculdade de Filosofia, Ciências e Letras de Ribeirão Preto, Av. Bandeirantes, 3900, Ribeirão Preto, São Paulo, 14040-901, Brazil

    Emerson Ricardo Pansarin

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  1. Juliana Hanna Leite El Ottra
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Correspondence to Juliana Hanna Leite El Ottra.

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Figure 1

(Electronic Supplementary Material): Flowers of Conchocarpus rubrus. (A) First-day flower, longitudinally opened, with anthers (white arrow) recessed in relation to the stigma (red arrow); (B) Photomicrograph of a longisection at the upper part of the disc (arrow indicates phloematic bundels). (C) SEM micrograph at the region of the aperture of the extrafloral nectary (arrow). Scale bars (A) = 4 mm; (B) = 50 µm; (C) 100 µm.(EPS 14924 kb)

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El Ottra, J.H.L., Pirani, J.R. & Pansarin, E.R. Tackling pollination of tubular flowers in Rutaceae and a case study of Conchocarpus rubrus (Galipeinae, Rutaceae). Braz. J. Bot 39, 913–924 (2016). https://doi.org/10.1007/s40415-016-0285-8

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