Abstract
Two representatives of section Lepidorhiza, previously sometimes considered conspecific, Bulbophyllum levanae and Bulbophyllum nymphopolitanum, demonstrated both similarities and differences in floral features. There were significant differences in the length of sepals and micromorphological features of the labellum. In both species, osmophores are located on the extended apices of sepals and possibly on petals. An abundance of proteins in tepals is probably associated with the unpleasant scent of the flowers, whereas the thin wax layers on the epidermis are probably involved in the maintenance of the brilliance of floral tepals, which strongly attracts flies. In all tepals of both species, we noted the presence of dihydroxyphenolic globules in the cytoplasm after staining with FeCl3. Comparison with ultrastructure results revealed that they were associated with plastids containing plastoglobuli. The most remarkable feature was the presence of a prominent periplasmic space in the epidermal cells of both investigated species. Furthermore, in the labellum of B. levanae, the cuticle contained microchannels. The combination of periplasmic space and microchannels has not previously been recorded.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Antoń S, Kamińska M, Stpiczyńska M (2012) Comparative structure of the osmophores in the flowers of Stanhopea graveolens Lindley and Cycnoches chlorochilon Klotzsch (Orchidaceae). Acta Agrobot 65:11–22. https://doi.org/10.5586/aa.2012.054
Borba EL, Semir J (1998) Wind-assisted fly pollination in three Bulbophyllum (Orchidaceae) species occurring in the Brazilian campos rupestres. Lindleyana 13:203–218
Brillouet J-M, Romieu C, Schoefs B, Solymosi K, Cheynier V, Fulcrand H, Verdeil J-L, Conéjéro (2013) The tannosome is an organelle forming condensed tannins in the chlorophyllous organs of Tracheophyta. Ann Bot. https://doi.org/10.1093/aob/mct168mct168
Bronner R (1975) Simultaneous demonstration of lipid and starch in plant tissues. Stain Technol 50(1):1–4
Curry KJ, Stern WL, McDowell LM (1988) Osmophore development in Stanhopea anfracta and S. pulla (Orchidaceae). Lindleyana 3:212
Davies KL, Stpiczyńska M (2012) Comparative labellar anatomy of resin-secreting and putative resin-mimic species of Maxillaria s.l. (Orchidaceae: Maxillariinae). Bot J Linn Soc 170:405–435. https://doi.org/10.1111/j.1095-8339.2012.01278.x
Davies KL, Stpiczyńska M (2014) Labellar anatomy and secretion in Bulbophyllum Thouars (Orchidaceae: Bulbophyllinae) sect. Racemosae Benth. & Hook. F. Ann Bot. https://doi.org/10.1093/aob/mcu153
De Melo MC, Borba EL, Paiva EAS (2010) Morphological and histological characterization of the osmophores and nectaries of four species of Acianthera (Orchidaceae: Pleurothallidinae). Lankesteriana 9:3–6
Endress PK (1994) Diversity and evolutionary biology of tropical flowers. Cambridge University Press, Cambridge
Fahn A (1979) Ultrastructure of nectaries in relation to nectar secretion. Am J Bot. 1979; 66: 977. https://doi.org/10.2307/2442240
Feder N, O’Brien TP (1968) Plant microtechnique: some principles and new methods. Am J Bot 55:123–142. https://doi.org/10.2307/2440500
Gahan PB (1984) Plant histochemistry and cytochemistry: an introduction. Academic Press, London
García AMT, Galati BG, Hoc PS (2007) Ultrastructure of the corona of scented and scentless flowers of Passiflora spp. (Passifloraceae). Flora 202:302–315. https://doi.org/10.1016/j.flora.2006.08.003
Heslop-Harrison Y (1977) The pollen stigma interaction: pollen tube penetration in Crocus. Ann Bot 41:913–922
Jensen W (1962) Botanical histochemistry. Freeman, San Francisco
Johansen DA (1940) Plant microtechnique. McGraw-Hill Book Company, New York
Johnson SD, Jürgens A (2010) Convergent evolution of carrion and faecal scent mimicry in fly-pollinated angiosperm flowers and a stinkhorn fungus. S Afr J Bot 76:796–807. https://doi.org/10.1016/j.sajb.2010.07.012
Jürgens A, Dötterl S, Meve U (2006) The chemical nature of fetid floral odours in stapeliads (Apocynaceae-Asclepiadoideae-Ceropegieae). New Phytol 172:452–468. https://doi.org/10.1111/j.1469-8137.2006.01845.x
Kowalkowska AK (2009) Analiza porównawcza struktur kwiatowych wabiących owady u wybranych gatunków Bulbophyllinae Schltr. i Pleurothallidinae Lindl. (Orchidaceae)/Comparative analysis of floral structures attracting insects in selected species of Bulbophyllinae Schltr. and Pleurothallidinae Lindl. (Orchidaceae). PhD dissertation, the University of Gdańsk, Gdańsk
Kowalkowska AK, Margońska HB, Kozieradzka-Kiszkurno M, Bohdanowicz J (2012) Studies on the ultrastructure of a three- spurred fumeauxiana form of Anacamptis pyramidalis. Plant Syst Evol 298:1025–1035. https://doi.org/10.1007/s00606-012-0611-y
Kowalkowska AK, Kostelecka J, Bohdanowicz J et al (2014a) Studies on floral nectary, tepals’ structure, and gynostemium morphology of Epipactis palustris (L.) Crantz (Orchidaceae). Protoplasma 252:321–333. https://doi.org/10.1007/s00709-014-0668-2
Kowalkowska AK, Kozieradzka-Kiszkurno M, Turzyński S (2014b) Morphological, histological and ultrastructural features of osmophores and nectary of Bulbophyllum wendlandianum (Kraenzl.) Dammer (B. section Cirrhopetalum Lindl., Bulbophyllinae Schltr., Orchidaceae). Plant Syst Evol 301:609–622. https://doi.org/10.1007/s00606-014-1100-2
Kowalkowska AK, Turzyński S, Kozieradzka-Kiszkurno M, Wiśniewska N (2016) Floral structure of two species of Bulbophyllum section Cirrhopetalum Lindl.: B. weberi Ames and B. cumingii (Lindl.) Rchb. f. (Bulbophyllinae Schltr., Orchidaceae). Protoplasma. https://doi.org/10.1007/s00709-016-1034-3
Machado SR, Gregório EA, Guimarães E (2006) Ovary peltate trichomes of Zeyheria montana (Bignoniaceae): developmental ultrastructure and secretion in relation to function. Ann Bot. https://doi.org/10.1093/aob/mcj042
Merino G, Doucette A, Pupulin F (2010) New species of Porroglossum (Orchidaceae: Pleurothallidinae) from Ecuador. Lankesteriana 9:3–6
Meve U, Liede S (1994) Floral biology and pollination in stapeliads—new results and a literature review. Plant Syst Evol 192:99–116. https://doi.org/10.1007/BF00985911
Miller RH (1985) The prevalence of pores and canals in leaf cuticular membranes. Ann Bot 55: 459–471. https://doi.org/10.1093/oxfordjournals.aob.a086924
Nepi M (2007) Nectary structure and ultrastructure. In: Nicolson SW, Nepi M, Pacini E (eds) Nectaries and nectar. Springer, Rotterdam, pp 129–166. https://doi.org/10.1007/978-1-4020-5937-7_3
Nunes ELP, Smidt EC, Stützel T, Coan AI (2014) What do floral anatomy and micromorphology tell us about Neotropical Bulbophyllum section Didactyle (Orchidaceae: Bulbophyllinae)? Bot J Linn Soc 175:438–452. https://doi.org/10.1111/boj.12176
Nunes ELP, Smidt EC, Stützel T, Coan AI (2015) Comparative floral micromorphology and anatomy of species of Bulbophyllum section Napelli (Orchidaceae), a Neotropical section widely distributed in forest habitats. Bot J Linn Soc 177:378–394. https://doi.org/10.1111/boj.12253
Pacini E, Nepi M (2007) Nectar production and presentation. In: Nicolson SW, Nepi M, Pacini E (eds) Nectaries and nectar. Springer, Rotterdam, pp 167–214. https://doi.org/10.1007/978-1-4020-5937-7
Pais M, Figueiredo ACS (1994) Floral nectaries from Limodorum abortivum (L.) Sw. and Epipactis atropurpurea Rafin. (Orchidaceae): ultrastructural changes in plastids during the secretory process. Apidologie 25:615–626
Paiva EAS (2016) How do secretory products cross the plant cell wall to be released? A new hypothesis involving cyclic mechanical actions of the protoplast. Ann Bot 117:533–540. https://doi.org/10.1093/aob/mcw012
Płachno BJ, Światek P, Szymczak G (2010) Can a stench be beautiful?—osmophores in stem-succulent stapeliads (Apocynaceae-Asclepiadoideae-Ceropegieae-Stapeliinae). Flora Morphol Distrib Funct Ecol Plants 205:101–105. https://doi.org/10.1016/j.flora.2009.01.002
Pridgeon AM, Stern WL (1985) Osmophores of Scaphosepalum (Orchidaceae). Bot Gaz 146:115–123
Pridgeon AM, Cribb PJ, Rasmussen FN, Chase MW (2014) Genera Orchidacearum: Epidendroideae. Oxford University Press, Oxford
Reynolds ES (1963) The use of lead citrate at high pH as an electron-opaque stain in electron microscopy. J Cell Biol 17:208–212
Ruzin S (1999) Plant microtechnique and microscopy. Oxford University Press, New York
Spurr AR (1969) A low-viscosity epoxy resin embedding medium for electron microscopy. J Ultrastruct Res 26:31–43. https://doi.org/10.1016/S0022-5320(69)90033-1
Statheropoulos M, Spiliopoulou C, Agapiou A (2005) A study of volatile organic compounds evolved from the decaying human body. Forensic Sci Int 153:147–155. https://doi.org/10.1016/j.forsciint.2004.08.015
Stern WL, Curry KJ, Pridgeon AM (1987) Osmophores of Stanhopea (Orchidaceae). Amer J Bot 74:1323–1331. https://doi.org/10.2307/2444310
Stpiczyńska M, Davies KL (2008) Elaiophore structure and oil secretion in flowers of Oncidium trulliferum Lindl. and Ornithophora radicans (Rchb.f.) Garay & Pabst (Oncidiinae: Orchidaceae). Ann Bot 101:375–384. https://doi.org/10.1093/aob/mcm297
Stpiczyńska M, Davies KL (2016) Evidence for the dual role of floral secretory cells in Bulbophyllum. Acta Biol Cracov Ser Bot 58:57–69. https://doi.org/10.1515/abcsb-2016-0013
Stpiczyńska M, Davies KL, Gregg A (2004) Nectary structure and nectar secretion in Maxillaria coccinea (Jacq.) L.O. Williams ex Hodge (Orchidaceae). Ann Bot 93:87–95. https://doi.org/10.1093/aob/mch00
Stpiczyńska M, Milanesi C, Faleri C, Cresti M (2005) Ultrastructure of the nectary spur of Platanthera chlorantha (Custer) Rchb. (Orchidaceae) during successive stages of nectar secretion. Acta Biol Cracov Ser Bot 47:111–119
Stpiczyńska M, Davies KL, Kamińska M (2015) Diverse labellar secretions in African Bulbophyllum (Orchidaceae: Bulbophyllinae) sections Ptiloglossum, Oreonastes and Megaclinium. Bot J Linn Soc 179(2):266–287
Teixeira SDP, Borba EL, Semir J (2004) Lip anatomy and its implications for the pollination mechanisms of Bulbophyllum species (Orchidaceae). Ann Bot 93:499–505. https://doi.org/10.1093/aob/mch072
Van Der Niet T, Hansen DM, Johnson SD (2011) Carrion mimicry in a South African orchid: flowers attract a narrow subset of the fly assemblage on animal carcasses. Ann Bot 107:981–992. https://doi.org/10.1093/aob/mcr048
Vogel S (1990) The role of scent glands in pollination: on the structure and function of osmophores. Amerind, New Delhi
Wist JT, Davis AR (2005) Floral nectar production and nectary anatomy and ultrastructure of Echinacea purpurea (Asteraceae). Ann Bot 97:177–193. https://doi.org/10.1093/aob/mcj027
Acknowledgements
The authors are very grateful to Univ.-Prof. Dr. Michael Kiehn and Anton Sieder from Botanischer Garten der Universität Wien, Christopher Ryan and Bala Kompalli from Royal Botanic Gardens - Kew, as well as to the Botanical Garden of the Jagiellonian University and Prague Botanical Garden for making specimens available. We thank Rudolf Hromniak and Paolo Rossoni (www.bulbophyllum.at) for providing the photos for this article and dr. hab. Bartosz Płachno for helpful hand with these research. We also thank the anonymous reviewers for valuable commentary on the manuscript.
Funding
This work was supported by the National Science Centre in Poland (5804/B/PO1/2010/39) and by the University of Gdansk, Faculty of Biology (538-L160-B947-15).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Additional information
Handling Editor: Hanns H. Kassemeyer
Rights and permissions
About this article
Cite this article
Wiśniewska, N., Kowalkowska, A.K., Kozieradzka-Kiszkurno, M. et al. Floral features of two species of Bulbophyllum section Lepidorhiza Schltr.: B. levanae Ames and B. nymphopolitanum Kraenzl. (Bulbophyllinae Schltr., Orchidaceae). Protoplasma 255, 485–499 (2018). https://doi.org/10.1007/s00709-017-1156-2
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00709-017-1156-2