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Floral Structure of Two Species of Bulbophyllum Section Cirrhopetalum Lindl.: B

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Floral Structure of Two Species of Bulbophyllum Section Cirrhopetalum Lindl.: B Protoplasma DOI 10.1007/s00709-016-1034-3 ORIGINAL ARTICLE Floral structure of two species of Bulbophyllum section Cirrhopetalum Lindl.: B. weberi Ames and B. cumingii (Lindl.) Rchb. f. (Bulbophyllinae Schltr., Orchidaceae) Agnieszka K. Kowalkowska1 & Sławomir Turzyński1 & Małgorzata Kozieradzka-Kiszkurno1 & Natalia Wiśniewska1 Received: 22 January 2016 /Accepted: 10 October 2016 # The Author(s) 2016. This article is published with open access at Springerlink.com Abstract Flowers of Bulbophyllum weberi and B. cumingii Keywords Bulbophyllum weberi . Bulbophyllum cumingii . are characterized by fly-pollinated features. The secretory ac- Bulbophyllum . Cirrhopetalum . Nectary . Osmophore . tivity was described in dorsal sepals in both species (putative Ultrastructure osmophores), petals in B. weberi (possible osmophores) and adaxial surface of lips in both species. In the cells of dorsal sepals and petals of B. weberi proteins, dihydroxyphenols, Introduction lipids and starch grains were detected, in lateral sepals— lipids. Whereas in dorsal sepal of B. cumingii only lipids Bulbophyllum Lindl. is a large, pantropical genus, containing and starch grains were noted, in lateral sepals—proteins and about 2200 species, distributed from Continental Africa, dihydroxyphenols and in petals—proteins and starch grains. Madagascar, East Indian Islands, Asia, Australia and the trop- The lips in both species differed histochemically and ultra- ical Pacific islands to the Neotropics. Madagascar and New structurally. The epidermal cells of lip groove in B. weberi Guinea are the main centres of diversity (Pridgeon et al. 2014). contained lipids, proteins, starch grains in cytoplasm, Their flowers are dull cream or yellow-green to purple-brown, dihydroxyphenols in vacuoles and pectic acids/mucilage on frequently spotted and hirsute, with mobile labella and ap- surface. Whereas in B. cumingii—few lipids, starch grains, no pendages, emitted fruity or malodorous and carrion-like scents proteins, no dihydroxyphenols and no mucilage were noted. (Tan and Nishida 2000, 2005; Tan et al. 2002). The species Ultrastructurally, in B. weberi, the secretory material was pres- demonstrate flowers, which are primarily pollinated by flies ent on surface and vesicles building into plasmalemma, while (van der Pijl and Dodson 1966; van der Cingel 2001; Nishida in B. cumingii—cell wall ingrowths and microchannels in et al. 2004): Diptera: Calliphoridae, Sarcophagidae, cuticle. The osmiophilic irregular materials and globular, Platystomatidae and Milichiidae, species from genus osmiophilic globules in B. weberi are probably tannin-like Bactrocera from Tephritidae and Drosophila from materials. For the first time, we described the cell wall in- Drosophilidae), but also by bees, wasps and foraging beetles growths in Bulbophyllum species: in lip of B. cumingii and (Stpiczyńska et al. 2015 and references therein). petals of B. weberi. Fly pollination is understood to comprise two syndromes: myophily and sapromyophily. The set of features characterizing myophilous flowers includes simple, relatively small flowers with bright dull colour (yellow-green to brownish or purplish) and musky, slightly sweet or fruity odour. It is also known that Handling Editor: Hanns H. Kassemeyer myophilous flowers could produce secretion in open shallow nectaries which occur in longitudinal labellar groove in * Agnieszka K. Kowalkowska Bulbophyllum family (Endress 1994; Kite et al. 1998; Jürgens [email protected] et al. 2006; Johnson and Jürgens 2010;Humeauetal.2011; Davies and Stpiczyńska 2014; Stpiczyńska et al. 2015). 1 Department of Plant Cytology and Embryology, University of Whereas the sapromyiophilous pollination syndrome embraces Gdańsk, Wita Stwosza 59, 80-308 Gdańsk, Poland dark flowers (brown, purple, greenish, often with great depth), A. K. Kowalkowska et al. emitting the putrescent odour containing sulphur compounds The epidermis of the adaxial labellar groove contained isodi- (Feinstein et al. 2009; van der Pijl and Dodson 1966). In fruit ametriccells,e.g.inB. meridense (Nunes et al. 2014), fly-pollinated Bulbophyllum species, methyl eugenol (aromatic B. wendlandianum (Kowalkowska et al. 2015) or palisade-like compound) and ketones have been identified as key cells,e.g.inB. involutum (Nunes et al. 2014), B. careyanum, chemical components in plant-pollinator interaction. In B. morphologorum, B. orientale and B. wangkaense (Davies B. cheiri methyl eugenol acts as sex pheromone precur- and Stpiczyńska 2014). It is known that the secretion in sor for males of Bactrocera species during pollination Bulbophyllum flowers is produced superficially on the lip (van (Tan et al. 2002; Nishida et al. 2004). The flowers of der Pijl and Dodson 1966;Teixeiraetal.2004; Kowalkowska Malaysian Bulbophyllum vinaceum also emit methyl eu- 2009; Davies and Stpiczyńska 2014; Nunes et al. 2014; genol and attract Bactrocera dorsalis and B. unimacula Kowalkowska et al. 2015; Stpiczyńska et al. 2015). In most (Tan et al. 2006). Furthermore, raspberry ketone was representatives, this secretion was described as nectar, but there detected as the major fragrance compound in is evidence that in some species, the secretion could be oil in Bulbophyllum apertum ssp. verrucosum being attracted conjunction with sugar (Pohl 1935;vanderCingel2001;Nunes to Bactrocera species sensitive to this ketone (Tan and et al. 2014) or protein-rich mucilage (Davies and Stpiczyńska Ritsuo 2005). Zingerone, identified in Bulbophyllum 2014). The oily or resinous material has been described in the baileyi and B. patens, was also qualified as volatile Asian species of Bulbophyllum,i.e.inB. lobbii Lindl. (section component enticing Bactrocera species (Tan and Sestochilus (Breda) Benth. and Hook.f.), B. macranthum Lindl. Nishida 2000, 2007). The unpleasant urine-like odour (section Stenochilus J.J.Sm.), B. alticola Schltr. (section in sapromyiophilous Bulbophyllum variegatum could be Codonosiphon Schltr.), B. auratum (Lindl.) Rchb.f. (section ascribed to indole, p-cresol, 2-heptanone (Arctander Recurvae). Pohl (1935) recorded that the flower of B. lobbii 1994;Dobson2006) and nitrogenous and sulphur com- and B. macranthum produces oil and sugar at the base of lip, in pounds (Humeau et al. 2011). the latter also by adjacent floral parts. The glistening droplets of The labellar morphology of Bulbophyllum species has sticky fluid on lips a few hours after opening have been found in homogenous and highly conservative characters (Teixeira B. alticola from Papua New Guinea (Jongejan 1994). Flowers of et al. 2004): the linguiform mid-lobe with adaxial median B. auratum produce a huge amount of sticky fluid, which func- longitudinal groove, relatively small and forwardly pointing tions as a trap for insects. The smaller ones draw down, whereas lateral lobes and also the articulation to the column foot the bigger ones, after trying to release, are thrown against the allowed lip to balance. However, the micromorphology and column by hinged lip regaining to its original position anatomy of species from section Didactyle showed consid- (Jongejan 1994). erable variation (Nunes et al. 2014). The anatomical studies The lip of Bulbophyllum species contains adaxial secretory in up-to-date investigated species revealed the general lip tissue, which is defined in the literature as ‘nectary’.Teixeira arrangement from the transverse sections: the single layer et al. (2004) and Nunes et al. (2014) described both nectaries in of epidermis, few layers of subepidermis and ground paren- lip groove and osmophores on the lip lobes of Neotropical chyma built by the isodiametric cells with collateral vascular species of Bulbophyllum. The liquid-like nectar was present in bundles. The labellar ground parenchyma was fleshy with- the lip cavity (=groove) of the non-wind-assisted fly-pollinated out intracellular spaces, e.g. Bulbophyllum exaltatum Lindl., Bulbophyllum species: B. epiphytum (Barb. Rodr.) Cogn., B. involutum Borba, Semir and F. Barros, B. meridense B. glutinosum (Barb. Rodr.) Cogn., B. regnellii Rchb.f. and Rchb.f., B. perii Schltr., B. popayanense Kraenzl., B. rothschildianum (O’Brien) J.J. Sm., whereas the osmophores B. tripetalum Lindl., B. weddellii (Lindl.) Rchb.f. (Nunes were located as papillae on the lip lobes and in the upper surface et al. 2014), B. careyanum (Hook.) Spreng., of the lip callus in most investigated wind and non-wind- B. morphologorum Kraenzl., B. orientale Seidenf., assisted species (Teixeira et al. 2004). The labellum in B. sec- B. wangkaense Seidenf. (Davies and Stpiczyńska 2014)or tion Didactyle (Nunes et al. 2014) was clothed with trichomes with intracellular spaces, e.g. B. wendlandianum (Kraenzl.) (possible osmophores), with a secretory cavity in the callus Dammer (Kowalkowska et al. 2015), B. falcatum (Lindl.) (nectary), bound by scale-like papillae. With some differences Rchb.f., B. lupulinum Lindl., Bulbophyllum maximum between species, the epidermal papillose cells on hypochile (Lindl.) Rchb.f., B. schinzianum Kraenzl. (Stpiczyńska gave positive reaction on lipids and formed the boundary of et al. 2015). The idioblasts with raphides occurred under secretory cavity. The three to five subepidermal secretory layers the epidermal cells through the subepidermis and parenchy- with cytoplasmic proteins were described in callus cavity. The ma (Davies and Stpiczyńska 2014; Kowalkowska et al. co-occurrence of osmophores and nectaries was in highest 2015). In petals, lip epichile, gynostemium and ovary of probability
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