New evidence of floral elaiophores and characterization of the oil flowers in the subtribe Oncidiinae (Orchidaceae)

Abstract

Elaiophores seems to be uncommon in Orchidaceae; however, the number of known species with floral oil glands has increased in recent years, principally in Oncidiinae. Oil rewards are used by bees of the tribes Centridini, Tapinotaspidini and Tetrapediini. Our aims were to identify the presence of elaiophores and to describe their structure in species of Gomesa, Grandiphyllum and Trichocentrum, and to compare our results with other studies of elaiophores in Oncidiinae. We selected a set of characters presumably associated with oil production in flowers of Oncidiinae, which were evaluated using a cluster analysis to identify different floral morphologies of the oil flowers. The correlation between morphological types of oil flowers and species of pollinators was examined. The cluster analysis distinguished two groups of species, one of them principally linked with pollination by bees of genus Centris and the other type associated to species of Paratetrapedia and Tetrapedia. The evaluation of these results into a phylogenetic framework of the Oncidiinae, adding more evidence that species of this subtribe with similar floral morphology associated with floral oil secretion arise in many independent clades, in parallel evolution with the oil-bee pollination.

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References

  1. Aliscioni SS, Torretta JP, Bello ME, Galati BG (2009) Elaiophores in Gomesa bifolia (Sims) M.W. Chase and N.H. Williams (Oncidiinae: Cymbidieae: Orchidaceae): structure and oil secretion. Ann Bot (Oxford) 104:1141–1149. doi:10.1093/aob/mcp199

    Article  Google Scholar 

  2. Anderson WR (1979) Floral conservatism in neotropical Malpighiaceae. Biotropica 11:219–223

    Article  Google Scholar 

  3. Blanco MA, Davies KL, Stpiczyńska M, Carlsward BS, Ionta GM, Gerlach G (2013) Floral elaiophores in Lockhartia Hook. (Orchidaceae: Oncidiinae): their distribution, diversity and anatomy. Ann Bot (Oxford) 112:1775–1791. doi:10.1093/aob/mct232

    Article  Google Scholar 

  4. Buchmann SL (1987) The ecology of oil flowers and their bees. Annual Rev Ecol Evol Syst 18:343–369. doi:10.1146/annurev.es.18.110187.002015

    Article  Google Scholar 

  5. Carmona-Díaz G, García-Franco JG (2009) Reproductive success in the Mexican rewardless Oncidium cosymbephorum (Orchidaceae) facilitated by the oil-rewarding Malpighia glabra (Malpighiaceae). Pl Ecol 203:253–261. doi:10.1007/s11258-008-9543-6

    Article  Google Scholar 

  6. Chase MW, Williams NH, Faria AD, Neubig KM, Amaral MCE, Whitten WM (2009) Floral convergence in Oncidiinae (Cymbidieae; Orchidaceae): an expanded concept of Gomesa and a new genus Nohawilliamsia. Ann Bot (Oxford) 104:387–402. doi:10.1093/aob/mcp067

    Article  Google Scholar 

  7. Chase MW, Cameron KM, Freudenstein JV, Pridgeon AM, Salazar G, Berg C, Schuiteman A (2015) An updated classification of Orchidaceae. Bot J Linn Soc 177:151–174. doi:10.1111/boj.12234

    Article  Google Scholar 

  8. Cocucci AA, Sérsic A, Roig-Alsina A (2000) Oil-collecting structures in Tapinotaspidini: their diversity, function and probable origin. Mitt Münch Entomol Ges 90:51–74

    Google Scholar 

  9. Damon AA, Cruz-López L (2006) Fragrance in relation to pollination of Oncidium sphacelatum and Trichocentrum oerstedii (Orchidaceae) in the Soconusco region of Chiapas, Mexico. Selbyana 27:186–194

    Google Scholar 

  10. Darwin C (1862) The various contrivances by which orchid are fertilized. John Murray, London

    Google Scholar 

  11. Davies KL, Stpiczyńska M (2008) The anatomical basis of floral, food-reward production in Orchidaceae. In: Teixeira da Silva J (ed) Floriculture, ornamental and biotechnology: advances and topical issues, vol 5. Global Science Books, Isleworth, pp 392–407

  12. Davies KL, Stpiczyńska M (2009) Comparative histology of floral elaiophores in the orchids Rudolfiella picta (Schltr.) Hoehne (Maxillariinae sensu lato) and Oncidium ornithorhynchum HBK (Oncidiinae sensu lato). Ann Bot (Oxford) 104:221–234. doi:10.1093/aob/mcp119

    Article  Google Scholar 

  13. Davies KL, Stpiczyńska M, Rawski M (2014) Comparative anatomy of floral elaiophores in Vitekorchis Romowicz and Szlach., Cyrtochilum Kunth and a florally dimorphic species of Oncidium Sw. (Orchidaceae: Oncidiinae). Ann Bot (Oxford) 113:1155–1173. doi:10.1093/aob/mcu045

    Article  Google Scholar 

  14. Dodson CH (1962) The importance of pollination in the evolution of the orchids of tropical America. Amer Orchid Soc Bull 31:525–534

    Google Scholar 

  15. Dressler RL (1990) The major clades of the Orchidaceae-Epidendroideae. Lindleyana 5:117–125

    Google Scholar 

  16. Dressler RL (1993) Phylogeny and classification of the orchid family. Dioscorides Press, Oregon

    Google Scholar 

  17. Gomiz NE, Torretta JP, Aliscioni SS (2013) Comparative anatomy of elaiophores and oil secretion in the genus Gomesa (Orchidaceae). Turkish J Bot 37:859–871. doi:10.3906/bot-1209-6

    Article  Google Scholar 

  18. Gomiz NE, Torretta JP, Aliscioni SS (2014) Zygostates alleniana (Orchidaceae: Epidendroideae: Cymbidieae: Oncidiinae): estructura floral relacionada a la polinización. Anales Jard Bot Madrid 7:1–9. doi:10.3989/ajbm.2378

    Google Scholar 

  19. Michener CD, Moure JC (1957) A study of the classification of the more primitive non-parasitic anthophorine bees (Hymenoptera, Apoidea). Bull Amer Mus Nat Hist 112:395–452

    Google Scholar 

  20. Neff JL, Simpson BB (1981) Oil-collecting structures in the Anthophoridae (Hymenoptera): morphology, function, and use in systematic. J Kansas Entomol Soc 54:95–123

    Google Scholar 

  21. Neubig KM, Whitten WM, Williams NH, Blanco MA, Endara L, Burleigh JG, Silvera K, Cushman JC, Chase MW (2012) Generic recircumscriptions of Oncidiinae (Orchidaceae: Cymbidieae) based on maximum likelihood analysis of combined DNA datasets. Bot J Linn Soc 168:117–146. doi:10.1111/j.1095-8339.2011.01194.x

    Article  Google Scholar 

  22. Pacek A, Stpiczyńska M (2007) The structure of elaiophores in Oncidium cheirophorum Rchb. f. and Ornithocephalus kruegeri Rchb. f. (Orchidaceae). Acta Agrobot 60:9–14. doi:10.5586/aa.2007.024

    Article  Google Scholar 

  23. Pacek A, Stpiczyńska M, Davies KL, Szymczak G (2012) Floral elaiophore structure in four representatives of the Ornithocephalus clade (Orchidaceae: Oncidiinae). Ann Bot (Oxford) 110:809–820. doi:10.1093/aob/mcs158

    CAS  Article  Google Scholar 

  24. Pansarin EM, Pansarin LM (2011) Reproductive biology of Trichocentrum pumilum: an orchid pollinated by oil-collecting bees. Pl Biol (Stuttgart) 13:576–581. doi:10.1111/j.1438-8677.2010.00420.x

    CAS  Article  Google Scholar 

  25. Pansarin LM, De Moraes Castro M, Sazima M (2009) Osmophore and elaiophores of Grobya amherstiae (Catasetinae, Orchidaceae) and their relation to pollination. Bot J Linn Soc 159:408–415. doi:10.1111/j.1095-8339.2009.00953.x

    Article  Google Scholar 

  26. Papadopulos AST, Powell MP, Pupulin F, Warner J, Hawkins JA, Salamin N, Chittka L, Williams NH, Whitten WM, Loader D, Valente LM, Chase MW, Savolainen V (2013) Convergent evolution of floral signals underlies the success of Neotropical orchids. Proc Roy Soc London Ser B Biol Sci 280:20130960. doi:10.1098/rspb.2013.0960

    Google Scholar 

  27. Parra-Tabla V, Vargas CF, Magaña-Rueda S, Navarro J (2000) Female and male pollination success of Oncidium ascendens (Orchidaceae) in two contrasting habitat patches: forest vs agricultural field. Biol Conservation 94:335–340. doi:10.1016/S0006-3207(99)00187-1

    Article  Google Scholar 

  28. Pemberton RW (2008) Pollination of the ornamental orchid Oncidium sphacelatum by the naturalized oil-collecting bee (Centris nitida) in Florida. Selbyana 29:87–91

    Google Scholar 

  29. Proctor M, Yeo P, Lack A (1996) The natural history of pollination. Timber Press, Oregon

    Google Scholar 

  30. Reis MG, de Faria AD, Bittrich V, Amaral MCE, Marsaioli AJ (2000) The chemistry of flower rewards–Oncidium (Orchidaceae). J Brazil Chem Soc 11:600–608. doi:10.1590/S0103-50532000000600008

    CAS  Article  Google Scholar 

  31. Reis MG, de Faria AD, dos Santos IA, Amaral MDE, Marsaioli AJ (2007) Byrsonic acid—the clue to floral mimicry involving oil-producing flowers and oil-collecting bees. J Chem Ecol 33:1421–1429. doi:10.1007/s10886-007-9309-y

    CAS  Article  PubMed  Google Scholar 

  32. Renner SS, Schaefer H (2010) The evolution and loss of oil-offering flowers: new insights from dated phylogenies for angiosperms and bees. Philos Trans Ser B 365:423–435. doi:10.1098/rstb.2009.0229

    CAS  Article  Google Scholar 

  33. Rohlf F (1998) NTSYS-Pc: numerical taxonomy and multivariate analysis system version 20. Department of Ecology and Evolution. State University of New York, Stony Brook. Available at: http://www.exetersoftware.com/downloads/ntsysguide21.pdf

  34. Roig-Alsina A (1997) A generic study of the bees of the tribe Tapinotaspidini, with notes on the evolution of their oil-collecting structures (Hymenoptera, Apidae). Mitt Münchner Entomol Ges 87:3–21

    Google Scholar 

  35. Silvera K (2002) Adaptive radiation of oil-reward compounds among Neotropical orchid species (Oncidiinae). MSc Thesis, University of Florida, Gainesville

  36. Singer RB, Cocucci AA (1999) Pollination mechanisms in four sympatric southern Brazilian Epidendroideae orchids. Lindleyana 14:47–56

    Google Scholar 

  37. Singer RB, Marsaioli AJ, Flach A, Reis MG (2006) The ecology and chemistry of pollination in Brazilian orchids: recent advances. In: Teixeira da Silva J (ed) Floriculture, ornamental and plant biotechnology, vol 4. Global Science Books, Isleworth, pp 569–582

    Google Scholar 

  38. Stpiczyńska M, Davies KL (2008) Elaiophore structure and oil secretion in flowers of Oncidium trulliferum Lindl. and Ornithophora radicans (Rchb.f.) Garay and Pabst (Oncidiinae: Orchidaceae). Ann Bot (Oxford) 101:375–384. doi:10.1093/aob/mcm297

    Article  Google Scholar 

  39. Stpiczyńska M, Davies KL, Gregg A (2007) Elaiophore diversity in three contrasting members of Oncidiinae (Orchidaceae). Bot J Linn Soc 155:135–148. doi:10.1111/j.1095-8339.2007.00681.x

    Article  Google Scholar 

  40. Stpiczyńska M, Davies KL, Pacek-Bieniek A, Kamińska M (2013) Comparative anatomy of the floral elaiophore in representatives of the newly re-circumscribed Gomesa and Oncidium clades (Orchidaceae: Oncidiinae). Ann Bot (Oxford) 112:839–854. doi:10.1093/aob/mcu045

    Article  Google Scholar 

  41. Thiers B (2016-continuously updated) Index herbariorum: a global directory of public herbaria and associated staff. New York Botanical Garden’s virtual herbarium, New York. http://sweetgum.nybg.org/science/ih/

  42. Torretta JP, Gomiz NE, Aliscioni SS, Bello ME (2011) Biología reproductiva de Gomesa bifolia (Orchidaceae, Cymbidieae, Oncidiinae). Darwiniana 49:16–24

    Google Scholar 

  43. Tremblay RL, Ackerman JD, Zimmerman JK, Calvo RN (2005) Variation in sexual reproduction in orchids and its evolutionary consequences: a spasmodic journey to diversification. Biol J Linn Soc 84:1–54. doi:10.1111/j.1095-8312.2004.00400.x

    Article  Google Scholar 

  44. Vale A, Navarro L, Rojas D, Álvarez JC (2011) Breeding system and pollination by mimicry of the orchid Tolumnia guibertiana in Western Cuba. Pl Spec Biol 26:163–173. doi:10.1111/j.1442-1984.2011.00322.x

    Article  Google Scholar 

  45. van der Cingel NA (2001) Atlas of orchid pollination: orchids of America, Africa, Asia and Australia. AA Balkema, Rotterdam

    Google Scholar 

  46. van der Pijl L, Dodson CH (1966) Orchid flowers: their pollination and evolution. University of Miami Press, Coral Gables

    Google Scholar 

  47. Vinson SB, Frankie GW, Williams HJ (1996) Chemical ecology of bees of the genus Centris (Hymenoptera: Apidae). Florida Entomol 79:109–129

    CAS  Article  Google Scholar 

  48. Vogel S (1969) Flowers offering fatty oil instead of nectar. In: Abstracts of the papers presented at the XI International Botanical Congress, University of Washington, Seattle, USA, 24 August–2 September, 1969, p 229

  49. Vogel S (1974) Ölblumen und ölsammelnde Bienen. Trop Subtrop Pflanzenwelt 7:285–547

    Google Scholar 

  50. Zarlavsky GE (2014) Histología Vegetal: técnicas simples y complejas. Sociedad Argentina de Botánica, Buenos Aires

    Google Scholar 

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Acknowledgements

This work was supported by FONCYT PICT 2013-1867 and CONICET PIP 2012-2014 (11220110100312). We thank to B. Galati and G. Zarlavsky for technical assistance, G. Sanchez for image processing, A. Torretta for the revision of manuscript and M. Bello and M. Lovisolo for providing plant material, and two anonymous reviewers for their constructive comments on this manuscript.

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Correspondence to Sandra S. Aliscioni.

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Handling editor: Louis P. Ronse De Craene.

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Online Resource 1. Data base used in the cluster analysis with the corresponding bibliography.

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Gomiz, N.E., Torretta, J.P. & Aliscioni, S.S. New evidence of floral elaiophores and characterization of the oil flowers in the subtribe Oncidiinae (Orchidaceae). Plant Syst Evol 303, 433–449 (2017). https://doi.org/10.1007/s00606-016-1382-7

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Keywords

  • Anatomy
  • Micromorphology
  • Oil
  • Orchidaceae
  • Secretion