Resupinate Dimorphy, a Novel Pollination Strategy in Two- Lipped Flowers of Eplingiella (Lamiaceae)
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Zurich Open Repository and Archive University of Zurich Main Library Strickhofstrasse 39 CH-8057 Zurich www.zora.uzh.ch Year: 2017 Resupinate dimorphy, a novel pollination strategy in two-lipped flowers of Eplingiella (Lamiaceae) Harley, Raymond M ; Giulietti, Ana Maria ; Abreu, Ivan Silva ; Bitencourt, Cassia ; de Oliveira, Favizia F ; Endress, Peter K DOI: https://doi.org/10.1590/0102-33062016abb0381 Posted at the Zurich Open Repository and Archive, University of Zurich ZORA URL: https://doi.org/10.5167/uzh-136157 Journal Article Published Version Originally published at: Harley, Raymond M; Giulietti, Ana Maria; Abreu, Ivan Silva; Bitencourt, Cassia; de Oliveira, Favizia F; Endress, Peter K (2017). Resupinate dimorphy, a novel pollination strategy in two-lipped flowers of Eplingiella (Lamiaceae). Acta Botanica Brasilica, (ahead):0. DOI: https://doi.org/10.1590/0102-33062016abb0381 Acta Botanica Brasilica doi: 10.1590/0102-33062016abb0381 Resupinate Dimorphy, a novel pollination strategy in two- lipped fl owers of Eplingiella (Lamiaceae) Raymond M. Harley1,2*, Ana Maria Giulietti1,2,3, Ivan Silva Abreu2, Cassia Bitencourt2, Favizia F. de Oliveira4 and Peter K. Endress5 Received: October 28, 2016 Accepted: January 31, 2017 . ABSTRACT Th is work provides a summary of the typical fl oral structure of subtribe Hyptidinae (Lamiaceae), in which both style and stamens are declinate within or near the concave anterior corolla lobe. Cross-pollination is facilitated by protandry, acting in conjunction with the explosive release of the stamens and pollen. In contrast, we report that in the three species of the genus Eplingiella we found individuals with either resupinate or non-resupinate fl owers, which represents a novel fl oral dimorphism. In these species of Eplingiella, the style occupies a position towards the posterior corolla lip and opposes the declinate stamens. Th us, in non-resupinate fl owers the pollinating bee receives pollen on its ventral side and makes contact with the style on its dorsal side, whereas in resupinate fl owers, the bee receives pollen on its dorsal side, and contacts the style on its ventral side. Both fl oral morphs seem to be required to achieve cross-pollination. In the two populations studied, each of the two morphs is present and in similar proportions, providing a novel means of promoting cross-pollination and reducing selfi ng. Th e situation in Eplingiella is compared to some other examples of fl oral polymorphism, but appears to be a unique pollination strategy, here termed Resupinate Dimorphy. Keywords: Brazil, Centris, Eplingiella, Hyptidinae, Lamiaceae, resupinate dimorphy, style position these genera, both the stamens and style are ascending and Introduction positioned under the upper (posterior) corolla lip, and the chance of self-pollination (at least autonomous autogamy, Th e large family Lamiaceae (or Labiatae), to which if not geitonogamy) is reduced by protandry, with the style Eplingiella belongs, contains over 7000 species with an elongating and the stigma receptive only after the pollen almost worldwide distribution. Most species produce nectar, has been shed (Harley et al. 2004). In most such species and many are bee-pollinated. Th e family is notably composed pollination is nototribic, i.e. the pollen is deposited on of self-compatible species, and no self-incompatible species the dorsal surface of the pollinator. In many Salvia species have been recorded (Owens & Ubera-Jiménez 1992). pollen deposition is facilitated by a hinged staminal lever Many Lamiaceae, particularly members of the subfamilies mechanism (Classen-Bockhoff et al. 2004). However, in Nepetoideae and Lamioideae, are characterized by having species of the Ocimeae subtribe Hyptidinae, the central zygomorphic, two-lipped fl owers, as in Salvia and Lamium. In anterior corolla-lobe is boat-shaped, concave, laterally 1 Royal Botanic Gardens, Kew, Richmond, Surrey TW9 3AB, U.K. 2 Programa de Pós-Graduação em Botânica, Departamento de Ciências Biológicas, Universidade Estadual de Feira de Santana, 44036- 900, Feira de Santana, BA, Brazil 3 Instituto Tecnológico Vale de Desenvolvimento Sustentável, Rua Boaventura da Silva 955, 66055-090, Belém, PA, Brazil 4 Museu de História Natural / Zoologia, Instituto de Biologia, Universidade Federal da Bahia, 40170-290, Salvador, BA, Brazil 5 Institute of Systematic Botany, University of Zurich, Zollikerstrasse 107, 8008 Zurich, Switzerland * Corresponding author: [email protected] Diagramação e XML SciELO Publishing Schema: www.editoraletra1.com.br Raymond M. Harley , Ana Maria Giulietti, Ivan Silva Abreu, Cassia Bitencourt, Favizia F. de Oliveira and Peter K. Endress compressed and with an elastic hinge at its base, such that sufficient number of individuals to carry out a survey of at early anthesis, the declinate stamens are trapped within the frequency of the two floral morphs. At each site 100 it and held under tension by the hinge. This creates an individuals were selected at random and scored for whether explosive mechanism of pollen release. The slight movement they had resupinate or non-resupinate flowers. Additionally, of a visiting pollinator (typically a bee) is sufficient to release flowers were photographed, and further studies in the the stamens and their pollen explosively, as the hinged lip herbaria were made for the two species. The bee visitors flicks back, depositing the pollen onto the ventral surface of were collected, and identified by Dr Favizia de Oliveira, the insect (Harley 1971; 1976), and the flowers are therefore and deposited in the BIOSIS Laboratory, Biology Institute, sternotribic. After the pollen is shed, the stamen filaments Universidade Federal da Bahia (UFBA). curl downwards, and the hitherto short style, which lies For E. fruticosa, we were unable to find a suitable slightly above the anterior lip, elongates and the stigma population with enough individuals for a survey of becomes receptive . morph frequencies to be undertaken. However, a cursory The Hyptidinae genus Eplingiella consists of three examination of a range of individuals of this species in shrubby species up to 3 m tall that are all native to semi- the field, in April 2015 and April 2016, evinced that both arid areas in NE Brazil (Harley & Pastore 2012; Harley 2014). resupinate and non-resupinate individuals were present. Eplingiella brightoniae, a multicaulous, fastigiate shrub to 1.5m, is restricted to the municipalities of Umburanas and Sento Sé, in very remote, dry montane habitats (campos Results and discussion rupestres) in Northern Bahia. E. cuniloides with a similar habit to the previous species, is known from a single area Observations in the field, combined with herbarium in the Morro do Chapéu municipality of Central Bahia, over studies at K and HUEFS, confirmed that in the three sands and shallow rocky habitats. E. fruticosa is a much species of Eplingiella, the basic floral structure is, with few branched shrub to 3 m tall, which occurs widely in semi- exceptions, very similar to that found in other Hyptidinae. arid caatinga vegetation and in coastal sands in Bahia, In subtribe Hyptidinae, flowers at the onset of anthesis and in other states in the semi-arid Northeast of Brazil have the stamens/anthers held under tension inside the (Harley 2014). boat-shaped central anterior petal lobe (Fig. 1A), and When dissecting flowers in order to describe Eplingiella they are released explosively when visited by a potential brightoniae (Harley 2014), we noted that the flowers were pollinator (Fig. 1B). The flowers show marked protandry often, but not invariably resupinate. This prompted more and the initially short style which lies along the anterior detailed studies so as to investigate to what extend this corolla lip subsequently elongates and the stigma becomes situation might affect the pollination process and to see receptive. In such flowers, pollen is likely to be deposited on, whether the phenomenon was exclusive to this species. and picked up by the stigma from the ventral surface of the bee, such that pollination is sternotribic. However, in the three species comprising the genus Eplingiella the flowers Materials and methods differed in two important respects from this structure. Firstly, in all flowers the style was no longer found above the Previous studies of the flowers of Eplingiella brightoniae declinate stamens but rather more upright and closer to the Harley, E. cuniloides (Epling) Harley & J.F.B. Pastore and E. posterior lip of the corolla and thus occupied a more central fruticosa (Salzm. ex Benth.) Harley & J.F.B. Pastore in the position. Secondly, in the populations we studied, ca. half herbaria of the Royal Botanic Gardens, Kew (K), and at the plants had flowers as described above, with the stamens the Universidade Estadual de Feira de Santana (HUEFS), held within the anterior corolla lobe in a ventral position revealed that plants in each of these three species had one of so that pollen deposition on the vector was sternotribic, two types of flower, resupinate or non-resupinate. A detailed whilst in the remaining half of the population, the plants study of the inflorescence of E. brightoniae was carried showed resupinate (inverted) flowers so that the stamens out, with the aid of a high-powered binocular microscope, were located above the style/stigma and consequently to see whether the position of the bracteoles below the pollen deposition was nototribic. In both cases, the four flower might indicate where the axis was twisted, to produce stamens were held within the boat-shaped median lobe resupination. of the anterior corolla-lip and showed a similar explosive Complementary fieldwork was carried out in Bahia mechanism of pollen release (Figs. 1C-G, 2A-F). state, Brazil, in April 2015, to assess the floral morphs Resupination of the flower by torsion of the pedicel has distribution in individuals of E. cuniloides (Morro do Chapéu been demonstrated in other Lamiaceae, e.g. Salvia jurisicii Municipality, Cachoeira do Ferro Doido, 11°37’39.7”S, (Schmucker 1929; Turrill 1929). However, with a pedicel of 41°00’02.4”W, 900 m elev., 6-7th) and E.