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Morphoanatomy of the Leaflets of the Hymenaea Clade (Fabaceae: Detarioideae) Reveals Their Potential for Taxonomic and Phylogenetic Studies

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Morphoanatomy of the Leaflets of the Hymenaea Clade (Fabaceae: Detarioideae) Reveals Their Potential for Taxonomic and Phylogenetic Studies Botanical Journal of the Linnean Society, 2018, 187, 87–98. With 4 figures. Morphoanatomy of the leaflets of the Hymenaea clade (Fabaceae: Detarioideae) reveals their potential for taxonomic and phylogenetic studies RAFAEL B. PINTO1,2*, MAKELI G. LUSA2,3, VIDAL DE F. MANSANO4, Downloaded from https://academic.oup.com/botlinnean/article/187/1/87/4965893 by guest on 25 September 2021 ANA MARIA G. DE AZEVEDO TOZZI2 and JULIANA LISCHKA SAMPAIO MAYER2 1Universidade Federal de Goiás, Instituto de Ciências Biológicas, Departamento de Botânica, Programa de Pós-Graduação em Biodiversidade Vegetal, Campus Samambaia, CEP 74690-900, Goiânia, GO, Brazil 2Universidade Estadual de Campinas, Instituto de Biologia, Departamento de Biologia Vegetal, Programa de Pós-Graduação em Biologia Vegetal, Rua Monteiro Lobato 255, CEP 13083-862, Cidade Universitária Zeferino Vaz, Campinas, SP, Brazil 3Universidade Federal de Santa Catarina, Departamento de Botânica, CEP 88040–900, Campus Universitário Prof. João David Ferreira Lima, Bairro Trindade, Florianópolis, SC, Brazil 4Instituto de Pesquisa Jardim Botânico do Rio de Janeiro, DIPEQ, Rua Pacheco Leão, 915, CEP 22460- 030, Jardim Botânico, Rio de Janeiro, RJ, Brazil Received 16 January 2017; revised 29 August 2017; accepted for publication 9 February 2018 The Hymenaea clade is part of the resin-producing clade of Fabaceae subfamily Detarioideae and is composed of three genera distributed mainly in tropical regions of Africa and South America. Anatomical characteristics of the leaflets are known for just a few representatives of this clade. This study aimed to improve this knowledge with morphoanatomical and histochemical characterizations of several species of Guibourtia, Hymenaea and Peltogyne. Our results support previous findings related to the presence of glandular cavities in Hymenaea and also add new evidence of the presence of these cavities in Guibourtia and Peltogyne. Absence of cavities was verified for H. velutina and P. catingae. Morphoanatomical characterization of the internerval region and histochemical analyses of the epidermis proved useful in delimiting species in the three genera. The position of the cavities in the leaflet lamina was also relevant in differentiating the three genera of this clade from other representatives of the subfamily. Our results contribute to the process of searching for features with phylogenetic signals and will be included in further phylogenetic analyses. ADDITIONAL KEYWORDS: Detarieae – glands – jatobá – Leguminosae – morphology – phylogeny – resin – systematics. INTRODUCTION and one in Africa; and Peltogyne Vogel with c. 21 Neotropical species. These genera share the tree habit The Hymenaea clade belongs to the recently recognized (although a few species of Hymenaea are predominately Fabaceae subfamily Detarioideae [Legume Phylogeny shrubs: H. eriogyne Benth., H. rubriflora Ducke and Working Group (LPWG), 2017], which has been H. travassii Kuhlmann ex Paes) and bifoliolate leaves, strongly supported as monophyletic (Fougère-Danezan, but they differ morphologically, mainly by the corolla Maumont & Bruneau, 2007; Bruneau et al., 2008). The (absent in Guibourtia), stamen length (heteromorphic clade is currently composed of three genera: Guibourtia in Peltogyne) and fruit dehiscence (indehiscent in Benn. with c. 15 species, two in the Neotropics and 13 in Hymenaea). Africa; Hymenaea L. with c. 16 species in the Neotropics The detarioids are known mainly for their resin production and the resin of several representatives, *Corresponding author. E-mail: [email protected] including the Hymenaea clade, is used in medicines, © 2018 The Linnean Society of London, Botanical Journal of the Linnean Society, 2018, 187, 87–98 87 88 R. B. PINTO ET AL. jewelry and artefacts (Langenheim, 2003). Studies of The occurrence of mucilage in the vegetative organs ancient trading of artefacts indicate resins of Hymenaea is usually associated with carbohydrate storage, water as one of the main products of the commercial route storage and reduction of transpiration, protection from between East Africa and Arabia during the Middle Ages intensive radiation by light scattering or reflection, and (Regert, Devièse & Le Hô, 2008; Crowther et al., 2015). protection against herbivory (Gregory & Baas, 1989). In Brazil, its exploitation reached c. 85 tons per year The species of the three genera of the Hymenaea during the 1940s (Serviço de Estatística e Economia clade are distributed in different environments of the Brasileira, 1954). Amber from Hymenaea spp. is also tropics in Africa and South America. For example, associated with palaeontological research because it most Guibourtia spp. are distributed in humid forests occasionally preserves structures of plants or animals of the African continent, but some also occur in open (especially invertebrates) over millions of years due to vegetation of the South American continent (chaco Downloaded from https://academic.oup.com/botlinnean/article/187/1/87/4965893 by guest on 25 September 2021 its hardness and fossilization capability (Poinar, 1991; and Brazilian cerrado) and near the sea in Cuba Poinar & Brown, 2002; Calvillo-Canadell, Cevallos- (Léonard, 1949, 1950). Similarly, species of Hymenaea Ferriz & Rico-Arce, 2010). and Peltogyne are distributed mainly in ombrophilous The resins usually have an ecological function vegetation of South America (Amazonian and Atlantic in providing protection against dehydration and/ forests) and in open vegetation (e.g. cerrado and or herbivory, favouring colonization of areas with caatinga) (Lee & Langenheim, 1975; Silva, 1976). high insolation and high incidence of insects, such Besides the different geography, in each genus the as in tropical vegetation (Langenheim, 1994, 2003). species can vary regarding leaflet shape, thickness, Arrhenius & Langenheim (1983) also found a brightness, pubescence and colour; however, there is fungal growth inhibitory property when studying little knowledge of the anatomy of the leaves of this this effect in resins of Hymenaea and Copaifera group, especially from a comparative standpoint. In L. Structures associated with oil/resin exudation addition to this gap in the knowledge on morphology have also been explored in a taxonomic context in of the Hymenaea clade, Guibourtia is probably not several groups of plants, including Asteraceae (Lusa, monophyletic (R. B. Pinto et al., unpublished data). Costa & Glória, 2016a), Calophyllaceae (Caddah Thus, our goal was to indicate anatomical features et al., 2011), Malpighiaceae (Araújo & Meira, 2016) that could help to better delimit the taxa and also be and Velloziaceae (Mello-Silva, 1995). In Fabaceae, used as an indication of the lineages present in the secretory structures are distributed along different Hymenaea clade. lineages and have been taxonomically explored in some genera, such as Lonchocarpus Kunth (Teixeira, Castro & Tozzi, 2000), Copaifera (Cascon & Gilbert, MATERIAL AND METHODS 2000), Myrocarpus Allemão, Myroxylon L.f. and Myrospermum Jacq. (Sartori & Tozzi 2002), Zornia Samples of leaflets of adult plants from representatives J.F.Gmel. (Fortuna-Perez, Castro & Tozzi, 2012) of the Hymenaea clade were collected in several and genera from tribe Cercideae (Duarte-Almeida locations in Brazil and for some species fragments et al., 2015). Usually referred to as translucent dots from herbarium collections were also used. When in the leaflet lamina, the secretory cavities of the possible, different individuals from each taxon were leaflets have been used as a diagnostic character in observed and the most representative picture was identification keys (Polhill, 1981). selected. Table 1 includes the vouchers with more Resin secretory cavities have been studied in a precise locality information. few Hymenaea spp. by Langenheim et al. (1982), who Fragments taken from the middle third of the leaflet suggested that the number and the position of resin blade were fixed in Karnovsky’s solution (Karnovsky, pockets may have taxonomic value. However, the 1965; modified to incorporate phosphate buffer of pH authors attribute the organization of the cavities to 7.2), subjected to vacuum and dehydrated using ethyl ecological factors, such as herbivory pressure. Paiva alcohol at different concentrations. They were then & Machado (2007) studied the secretory cavities infiltrated with hydroxyethyl methacrylate plastic resin in leaflets of H. stigonocarpa Mart. ex Hayne and (Leica Historesin; Heraeus Kulzer, Hanau, Germany), concluded that, at least in this species, the cavities are according to the manufacturer’s instructions. organized randomly; thus, neither the number nor the The samples were sectioned to a thickness of 5–7 mm position of the cavities seems to have taxonomic value. using a rotary microtome (Model RM 2245; Leica Besides oil/resin, the presence of mucilage in the leaf Microsystems Nussloch GmbH, Nussloch, Germany), tissue restricted to idioblasts or accumulated between in transverse and longitudinal sections to observe the parenchymatous and epidermal cells of the epidermis structure of the glands. These materials were stained can also help in the systematics for genera of tribe with 0.05% toluidine blue in citrate-phosphate buffer, Crotalarieae (Boatwright, Tilney & Van Wyk, 2009). pH 4.5 (Sakai, 1973), and mounted in Entellan synthetic © 2018 The Linnean Society of London, Botanical Journal of the Linnean Society, 2018, 187, 87–98 LEAFLET ANATOMY IN THE HYMENAEA CLADE 89 Table 1. Species, general localities
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