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(Malpighiaceae), a Neotropical Species Flora 211 (2015) 26–39 Contents lists available at ScienceDirect Flora j ournal homepage: www.elsevier.com/locate/flora Structure and secretion mechanisms of floral glands in Diplopterys pubipetala (Malpighiaceae), a neotropical species ∗ Clivia Carolina Fiorilo Possobom, Elza Guimarães, Silvia Rodrigues Machado São Paulo State University, UNESP, Institute of Biosciences of Botucatu, Department of Botany, 18618-970 Botucatu, São Paulo, Brazil a r t i c l e i n f o a b s t r a c t Article history: Detailed studies on the distribution, structure, and secretion activity of floral glands are important to Received 15 July 2014 understand the relationship of flowers with oil-collecting bees in Malpighiaceae. Here, we characterised Received in revised form the floral biology and the glands in sepals, petals and connective tissues of Diplopterys pubipetala. The 10 December 2014 data on the floral biology were obtained under field conditions. The samples from functional flowers Accepted 9 January 2015 were prepared for anatomical, histochemical and ultrastructural studies. The bees of the genera Monoeca Edited by Shahin Zarre. and Centris were the most frequent visitors. While both insects searched for oil, the former also collected Available online 14 January 2015 pollen and connective tissue secretions. The conspicuous and subsessile sepal glands are arranged in pairs Keywords: on the abaxial surface, presenting structural and cellular machinery typical of epithelial elaiophores. The oil is accumulated in the subcuticular space and released when the bee scraps the cuticle, causing its rup- Floral glands Histochemistry ture. The petal glands, observed at the fimbriate edges, are diminutive, comprising secretory epithelium Oil-collecting bees surrounding a central core of parenchymal cells supplied with vascular tissues. The petal glands are typ- Pollination ically osmophores, and secretion occurs via diffusion through the thin cuticle. The glandular connective Ultrastructure comprises large globular secretory epithelial cells, which produce a bright and viscous secretion, mim- icking pollen grains. This predominantly hydrophilic secretion is released to the surface of the connective tissue traversing the thin cell wall and intact cuticle in regions with protruding protoplasts. In addition, the sticky secretion produced from the glandular connectives might also increase the efficiency of trans- port and pollen transfer. Taken together, these results show that each gland has a peculiar mechanism and type of secretion, suggesting additional levels of floral specialisation for interactions with pollinators. © 2015 Elsevier GmbH. All rights reserved. Introduction 1967; Anderson, 2004; Judd et al., 2007), which are frequently associated with extrafloral nectar secretion and ants that protect Malpighiaceae is a pantropically distributed family, represented plants against herbivores (Lobreau-Callen, 1989; Possobom et al., by approximately 1300 species which mostly occur in neotropical 2010; Aguirre et al., 2013). Nevertheless, this ant-plant interaction region (Davis and Anderson, 2010). It is one of the most impor- may take part in a multitrophic interaction involving pollinators tant plant families that secrete floral oil as a reward to pollinators with consequences on plant reproductive success, as showed by and amongst the oldest clades to have acquired elaiophores (Vogel, Assunc¸ ão et al. (2014). 1974; Renner and Schaefer, 2010). These oil glands occur in approx- Neotropical species of Malpighiaceae are pollinated principally imately 90% of the neotropical species, and when they occur in by specialized oil-collecting bees belonging to the tribes Centridini, the paleotropical species, they seems to be related with extranup- Tapinotaspidini and Tetrapediini that are restricted to American tial nectar secretion and not with oil secretion (Vogel, 1974, continent and are especially diverse in the tropical region (Alves- 1990a). These glands are morphologically very similar to those dos-Santos et al., 2007). These bees gathered the oil produced on the petiole, abaxial surface or margins of leaves (Hutchinson, by elaiophores and use it for larval provisioning (Vogel, 1974; Vinson et al., 1997; Reis et al., 2007) and cell lining (Neff and Simpson, 1981; Simpson and Neff, 1981; Buchmann, 1987; Vogel, ∗ 1990a). The majority of Malpighiaceae species are hermaphroditic, Corresponding author at: São Paulo State University, UNESP, Institute of Bio- sciences of Botucatu, Department of Botany, Rubião Jr District s/n, PO Box 510, predominantly allogamous and highly dependent on pollen vec- 18618-970, Botucatu, São Paulo, Brazil. Tel.: +55 14 3880 0122; tors for reproduction (Teixeira and Machado, 2000; Sigrist and fax: +55 14 3815 3744. Sazima, 2004; Costa et al., 2006; Cappellari et al., 2011). The close E-mail address: [email protected] (S.R. Machado). http://dx.doi.org/10.1016/j.flora.2015.01.002 0367-2530/© 2015 Elsevier GmbH. All rights reserved. C.C.F. Possobom et al. / Flora 211 (2015) 26–39 27 interactions between Malpighiaceae and their specific pollinators glandular tissues, a set of buds was isolated in voile bags throughout have influenced the diversification rates in Malpighiaceae since its floral development. During anthesis, some flowers were exposed to origin (Renner and Schaefer, 2010; Davis et al., 2014). bees (Monoeca sp.), and subsequently these bees and non-visited, In addition to the sepal elaiophores, in more than 10 Malpighi- bagged flowers were collected for analysis using a scanning elec- aceae genera, at least one species possesses diminutive petal glands tron microscope (SEM). and/or glandular connectives on the anthers (Anderson, 1975, 1982, Voucher samples were deposited in the “Irina Delanova 1987, 1995; Gates, 1982; Johnson, 1986; Simpson, 1989; Anderson Gemtchujnicov” Herbarium (BOTU) of the Biosciences Institute, and Davis, 2007). According to Vogel (1974), the petal glands of São Paulo State University (UNESP) at Botucatu, São Paulo, Brazil Heteropterys chrysophylla produce non-polar lipids, different from (numbers 25,306–25,310). those observed in sepal gland secretion. Lobreau-Callen (1989) also detected lipids in the secretion from the petal glands of Burdachia Floral biology primatocarpa and Glandonia macrocarpa, but no ecological function has been suggested. Concerning the glandular anther connectives, The floral anthesis, longevity, time of opening and percentage Gates (1982) suggested that the location of this tissue on the flower of flowers in anthesis in 12 D. pubipetala individuals were observed favours contact with the ventral portion of the visitor, and secre- daily. The floral scents were examined using organoleptic tests, and tion could thereby increase the adhesion of the pollen grains onto the osmophores were macroscopically detected through neutral the body of the visitor. red staining (Vogel, 1990b). We also assessed the secretory activity Detailed studies correlating the structure and function of floral of the floral glands during floral development. Focal observations glands in Malpighiaceae have been limited to only a few species, of the floral visitors were conducted between 06:00 and 20:00 h, and these studies primarily focused on sepal elaiophores (Vogel, and the time, duration, and frequency of visits, behaviour, resource 1974; Subramanian et al., 1990; Cocucci et al., 1996; Castro et al., collected, and site of body contact with the anthers and stigmas 2001). Thus, our current knowledge of petal glands and glandular were recorded according to Dafni et al. (2005). The behaviour of the connectives is scarce (Vogel, 1974; Lobreau-Callen, 1989; Cocucci visitors was described based on field observations and photograph et al., 1996), and many aspects remain unknown, such as the and film analyses. The specimens collected from each visitor species structural organisation and secretion mechanisms. A comparative were analysed under a stereomicroscope to assess the presence and analysis of the different glandular tissues associated with data on location of the pollen grains and the oil on the body. the behaviour of visitors could provide insights into the role of floral exudates in plant-pollinator interactions. Anatomical analysis In the present study, we characterised the anatomy, histochem- istry and ultrastructure of the sepal, petal and connective glands For general histology, the samples were fixed in Karnovsky’s of Diplopterys pubipetala (A. Juss.) W.R. Anderson & C. Davis, as it solution (Karnovsky, 1965) for 24 h, dehydrated in an ethanol relates to interactions with pollinators. series, and embedded in 2-hydroxyethyl-methacrylate resin (His- toresin, Leica, Heidelberg, Germany). Serial cross and longitudinal sections (5–8 ␮m thickness) were obtained using a rotatory micro- Materials and methods tome. Subsequently, the sections were stained with 0.05% toluidine blue, pH 4.3 (O’Brien et al., 1964), and mounted in synthetic resin. Study site and plant material The images were obtained using a light microscope equipped with a camera. To examine the vascularisation of the petal glands, the The cerrado, or the Brazilian savannah, covers nearly fimbriate petal fragments were cleared according to Fuchs (1963). 2 2 million km , approximately 22% of the country’s land sur- face. The cerrado is extremely variable in terms of physiognomy, Histochemical analysis ranging from open grasslands to forests with discontinuous grass layers. A continuum of savanna formations between these two Hand-cut sections of fresh material were
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