Pollination in Epidendrum densiflorum Hook. (Orchidaceae: Laeliinae): Fraudulent Trap-Flowers, Self-Incompatibility, and a Possible New Type of Mimicry
Abstract
:1. Introduction
2. Results
2.1. Flower Features
2.2. Breeding System and Fruiting Success under Natural Conditions
2.3. Pollinators, Pollinator Activity, and the Pollination Process
3. Discussion
3.1. Flower Features
3.2. Breeding System and Fruiting Success under Natural Conditions
3.3. Pollinators and Pollinator Behavior
4. Materials and Methods
4.1. Study Place
4.2. Study Species and Flower Features
4.3. Fieldwork Observations
4.4. Breeding System
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Hágsater, E.; Soto Arenas, M.A. Epidendrum. In Genera Orchidacearum: Epidendroideae (Part One); Pridgeon, A., Cribb, P., Chase, M., Eds.; Oxford University Press: Oxford, UK, 2005; Volume 4, pp. 236–251. [Google Scholar]
- Dressler, R.L. Phylogeny and Classification of the Orchid Family; Cambridge University Press: Cambridge, MA, USA, 1993. [Google Scholar]
- Darwin, C. On the Various Contrivances by Which British and Foreign Orchids Are Fertilized by Insects and on the Good Effects of Intercrossing, 1st ed.; John Murray: London, UK, 1862; 360p. [Google Scholar]
- Van der Pijl, L.; Dodson, C.H. Orchid Flowers: Their Pollination and Evolution; University of Miami Press: Coral Gables, FL, USA, 1996. [Google Scholar]
- Adams, P.; Lawson, S. Pollination in Australian Orchids: A Critical-Assessment of the Literature 1882–1992. Aust. J. Bot. 1993, 41, 553–575. [Google Scholar] [CrossRef]
- Fuhro, D.A.M.; Irgang, B.E. Are there evidences of a complex mimicry system among Asclepias curassavica (Apocynaceae), Epidendrum fulgens (Orchidaceae), and Lantana camara (Verbenaceae) in Southern Brazil? Rev. Bras. Bot. 2010, 33, 589–598. [Google Scholar] [CrossRef]
- Pansarin, E.R. Biologia reprodutiva e polinização em Epidendrum paniculatum Ruiz & Pavón (Orchidaceae). Rev. Bras. Bot. 2003, 26, 203–211. [Google Scholar] [CrossRef]
- Pansarin, E.R.; Amaral, M.C.E. Reproductive biology and pollination mechanisms of Epidendrum secundum (Orchidaceae). Floral variation: A consequence of natural hybridization? Plant Biol. 2008, 10, 211–219. [Google Scholar] [CrossRef] [PubMed]
- Pansarin, E.R.; Pansarin, L.M. Reproductive biology of Epidendrum tridactylum (Orchidaceae: Epidendroideae): A reward-producing species and its deceptive flowers. Plant Syst. Evol. 2013, 300, 321–328. [Google Scholar] [CrossRef]
- Pansarin, E.R.; Pansarin, L.M. Crane flies and microlepidoptera also function as pollinators in Epidendrum (Orchidaceae: Laeliinae): The reproductive biology of E. avicula. Plant Species Biol. 2016, 32, 200–209. [Google Scholar] [CrossRef]
- Pessoa, E.M. Epidendrum in Flora do Brasil 2020. Jardim Botânico do Rio de Janeiro. 2020. Available online: https://floradobrasil2020.jbrj.gov.br/FB37584 (accessed on 26 July 2022).
- Stancik, J.F.; Goldenberg, R.; De Barros, F. O gênero Epidendrum L. (Orchidaceae) no Estado do Paraná, Brasil. Acta Bot. Bras. 2009, 23, 864–880. [Google Scholar] [CrossRef]
- Smidt, E.C.; Silva-Pereira, V.; Borba, E.L. Reproductive biology of two Cattleya (Orchidaceae) species endemic to north-eastern Brazil. Plant Species Biol. 2006, 21, 85–91. [Google Scholar] [CrossRef]
- Caballero-Villalobos, L.; Silva-Arias, G.A.; Buzatto, C.R.; Nervo, M.H.; Singer, R.B. Generalized food-deceptive pollination in four Cattleya (Orchidaceae: Laeliinae) species from Southern Brazil. Flora 2017, 234, 195–206. [Google Scholar] [CrossRef]
- Cardoso-Gustavson, P.; Saka, M.N.; Pessoa, E.M.; Palma-Silva, C.; Pinheiro, F. Unidirectional transitions in nectar gain and loss suggest food deception is a stable evolutionary strategy in Epidendrum (Orchidaceae): Insights from anatomical and molecular evidence. BMC Plant Biol. 2018, 18, 179. [Google Scholar] [CrossRef]
- Tremblay, R.L.; Ackerman, J.D.; Zimmerman, J.K.; Calvo, R.N. Variation in sexual reproduction in orchids and its evolutionary consequences: A spasmodic journey to diversification. Biol. J. Linn. Soc. 2004, 84, 1–54. [Google Scholar] [CrossRef]
- Neiland, M.R.M.; Wilcock, C.C. Fruit set, nectar reward, and rarity in the Orchidaceae. Am. J. Bot. 1998, 85, 1657–1671. [Google Scholar] [CrossRef]
- Pedron, M.; Buzatto, C.R.; Singer, R.B.; Batista, J.A.N.; Moser, A. Pollination biology of four sympatric species of Habenaria (Orchidaceae: Orchidinae) from southern Brazil. Bot. J. Linn. Soc. 2012, 170, 141–156. [Google Scholar] [CrossRef]
- Buzatto, C.R.; Nervo, M.H.; Sanguinetti, A.; Berg, C.V.D.; Singer, R.B. Efficient pollination and high reproductive success in two Brazilian Spiranthinae orchids: Insights on the evolutionary history of pollination within the Pelexia clade. Plant Species Biol. 2022, 37, 182–196. [Google Scholar] [CrossRef]
- Adams, R.M.; Goss, G.L. The reproductive biology of the epiphytic orchids of Florida III—Epidendrum anceps Jacquin. Am. Orchid. Soc. Bull. 1976, 45, 488–492. [Google Scholar]
- Goss, G.J. The reproductive biology of the epiphytic orchids of Florida V—Epidendrum difforme Jacquin. Am. Orchid. Soc. Bull. 1977, 46, 630–636. [Google Scholar]
- Stort, M.N.S.; Galdino, G.L. Self- and cross-pollination in some species of the genus Laelia Lindl. (Orchidaceae). Rev. Bras. Genét. 1984, 7, 671–676. [Google Scholar]
- Iannotti, M.A.; Stort, M.N.S.; Morales, M.A.M. O sistema reprodutivo de Epidendrum rigidum Jacq. (Orchidaceae). Ciênc. Cult. 1987, 39, 641–644. [Google Scholar]
- Matias, L.Q.; Braga, P.; Freire, A. Biologia reprodutiva de Constantia cipoensis Porto & Brade (Orchidaceae), endêmica da Serra do Cipó, Minas Gerais. Rev. Bras. Bot. 1996, 19, 119–125. [Google Scholar]
- Brown Junior, K.S. Chemistry at the Solanaceae/Ithomiinae interface. Ann. Mo. Bot. Gard. 1987, 74, 359–397. [Google Scholar] [CrossRef]
- Singer, R.B.; Koehler, S. Notes on the pollination biology of Notylia nemorosa (Orchidaceae): Do pollinators necessarily promote cross pollination? J. Plant Res. 2003, 116, 19–25. [Google Scholar] [CrossRef] [PubMed]
- Castro, J.B.; Perdomo, O.; Singer, R.B. Pollination biology and reproductive success in four Brazilian species of Gomesa (Orchidaceae: Oncidiinae): Specific pollinators, but high pollen loss and low fruit set. Plant Species Biol. 2022, 37, 132–147. [Google Scholar] [CrossRef]
- De Vries, P.J.; Stiles, F.G. Attraction of pyrrolizidine alkaloid seeking lepidoptera to Epidendrum paniculatum orchids. Biotropica 1990, 22, 290–297. [Google Scholar] [CrossRef]
- Luning, B. Studies on Orchidaceae alkaloids I. Acta Chem. Scand. 1964, 18, 1507–1516. [Google Scholar] [CrossRef]
- Pliske, T.E. Attraction of Lepidoptera to Plants Containing Pyrrolizidine Alkaloids. Environ. Èntomol. 1975, 4, 455–473. [Google Scholar] [CrossRef]
- Bohman, B.; Flematti, G.R.; Barrow, R.A.; Pichersky, E.; Peakall, R. Pollination by sexual deception—It takes chemistry to work. Curr. Opin. Plant Biol. 2016, 32, 37–46. [Google Scholar] [CrossRef] [PubMed]
- Coombs, G.; Peter, C.I. The invasive ‘mothcatcher’ (Araujia sericifera Brot.; Asclepiadoideae) co-opts native honeybees as its primary pollinator in South Africa. AoB Plants 2010, 2010, plq021. [Google Scholar] [CrossRef]
- Pemberton, R.W. Pollination of slipper orchids (Cypripedioideae): A review. Lankesteriana Int. J. Orchid. 2013, 13, 65–74. [Google Scholar] [CrossRef]
- Phillips, R.D.; Scaccabarozzi, D.; Retter, B.A.; Hayes, C.; Brown, G.R.; Dixon, K.W.; Peakall, R. Caught in the act: Pollination of sexually deceptive trap-flowers by fungus gnats in Pterostylis (Orchidaceae). Ann. Bot. 2014, 113, 629–641. [Google Scholar] [CrossRef]
- Singer, R.B.S. The Pollination Mechanism in Trigonidium obtusum Lindl (Orchidaceae: Maxillariinae): Sexual Mimicry and Trap-flowers. Ann. Bot. 2002, 89, 157–163. [Google Scholar] [CrossRef]
- INMET 2020. Instituto Brasileiro de Meteorologia (INMET). Available online: Inmet.gov.br (accessed on 15 July 2022).
- Dinno, A. Nonparametric Pairwise Multiple Comparisons in Independent Groups using Dunn′s Test. Stata J. Promot. Commun. Stat. Stata 2015, 15, 292–300. [Google Scholar] [CrossRef]
- R Core Team. “R”: A language and Environment for Statistical Computing; R Foundation for Statistical Computing: Vienna, Austria, 2021; Available online: https://www.rproject.org/ (accessed on 18 July 2022).
- Nilsson, L.A.; Rabakonandrianina, E.; Razananaivo, R.; Randriamanindry, J.-J. Long pollinia on eyes: Hawk-moth pollination of Cynorkis uniflora Lindley (Orchidaceae) in Madagascar. Bot. J. Linn. Soc. 1992, 109, 145–160. [Google Scholar] [CrossRef]
Treatments N = 50 Flowers/Treatment | Fruits | |||
---|---|---|---|---|
Total | Average | SE | SD | |
Cross-pollination | 48 | 0.96 a | 0.028 | 0.198 |
Self-pollination | 1 | 0.02 ᵇ | 0.020 | 0.141 |
Emasculation | 0 | 0 ᵇ | 0.0 | 0.00 |
Intact flowers | 0 | 0 ᵇ | 0.0 | 0.00 |
Pollination Success (Open Pollination) N = 969 Flowers | Number/Percentage |
---|---|
Pollinaria removed | 158 (16.30%) |
Pollinaria deposited | 41 (4.23%) |
Nilsson’s male efficiency factor | 0.259% |
Fructification | 28 (2.88%) |
Family/Subfamily Species | Visits | Gender | Pollinaria Removed | Average Time in Flower (min) | SD | SE |
---|---|---|---|---|---|---|
Erebidae: Arctiinae | ||||||
Antichloris eriphia Fabricius, 1776 | 13 | male | 9 | 47 ᵃ | 13.9 | 4.55 |
Calodesma collaris Drury, 1782 | 9 | male | 7 | 62 ᵃ | 8.3 | 10.1 |
Cyanopepla jucunda Walker, 1854 | 2 | male | 1 | 38 ᵃ | 6.7 | 4.00 |
Philoros rubriceps Walker, 1854 | 11 | male | 8 | 59 ᵃ | 10.4 | 8.63 |
Phoenicoprocta teda Walker, 1845 | 17 | male | 14 | 73 ᵃ | 16.5 | 10.4 |
Nymphalidae: Ithomiinae | ||||||
Episcada hymenaea Prittwitz, 1865 | 4 | male | 2 | 15 ᵇ | 7.1 | 3.15 |
Hypothyris euclea Doubleday, 1847 | 2 | male | 1 | 4 ᵇ | 2.4 | 1.00 |
Methona themisto Hübner, 1818 | 5 | male | 3 | 6 ᵇ | 5.2 | 0.70 |
Placidina euryanassa C. & R. Felder, 1860 | 1 | male | 1 | 5 ᵇ | 0 | 0 |
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Silveira, R.S.; Singer, R.B.; Ferro, V.G. Pollination in Epidendrum densiflorum Hook. (Orchidaceae: Laeliinae): Fraudulent Trap-Flowers, Self-Incompatibility, and a Possible New Type of Mimicry. Plants 2023, 12, 679. https://doi.org/10.3390/plants12030679
Silveira RS, Singer RB, Ferro VG. Pollination in Epidendrum densiflorum Hook. (Orchidaceae: Laeliinae): Fraudulent Trap-Flowers, Self-Incompatibility, and a Possible New Type of Mimicry. Plants. 2023; 12(3):679. https://doi.org/10.3390/plants12030679
Chicago/Turabian StyleSilveira, Rodrigo Santtanna, Rodrigo Bustos Singer, and Viviane Gianluppi Ferro. 2023. "Pollination in Epidendrum densiflorum Hook. (Orchidaceae: Laeliinae): Fraudulent Trap-Flowers, Self-Incompatibility, and a Possible New Type of Mimicry" Plants 12, no. 3: 679. https://doi.org/10.3390/plants12030679