Artigo Acesso aberto Revisado por pares

First evidence for multimodal animal seed dispersal in orchids

2022; Elsevier BV; Volume: 33; Issue: 2 Linguagem: Inglês

10.1016/j.cub.2022.11.041

ISSN

1879-0445

Autores

Adam P. Karremans, Diego Bogarín, Mauricio Fernández Otárola, Jyotsna Sharma, Charlotte Watteyn, Jorge Warner, Bernal Herrera, Isler F. Chinchilla, Ernesto Carman, Emmanuel Rojas Valerio, Ruthmery Pillco Huarcaya, Andy Whitworth,

Tópico(s)

Plant Parasitism and Resistance

Resumo

Identifying the mechanisms for seed dispersal and persistence of species is a central aim of ecology. Seed dispersal by animals is an essential form of dissemination in many plant communities, including seeds of over 66% of neotropical canopy tree species. 1 Howe H.F. Smallwood J. Ecology of seed dispersal. Annu. Rev. Ecol. Syst. 1982; 13: 201-228 Crossref Scopus (2333) Google Scholar ,2 Wunderle Jr., J.M. The role of animal seed dispersal in accelerating native forest regeneration on degraded tropical lands. For. Ecol. Manag. 1997; 99: 223-235 Crossref Scopus (382) Google Scholar Besides physical dispersal, animals influence seed germination probabilities through scarification, breaking dormancy, and preventing rotting, so plants often invest important resources in attracting them. Orchids are predominantly adapted to wind dispersal, having dust-like seeds that are easily uplifted. Exceptions include bird-, 3 Suetsugu K. Kawakita A. Kato M. 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Kings Park Research Notes No. 9. Kings Park and Botanic Gardens, 1984 Google Scholar species, featuring fleshy fruits with hard seeds that germinate after passing the animal's digestive system. Given the similarity in fruit and seed morphology, zoochory has also been suggested in Vanilla, 8 Madison M. Vanilla beans and bees. Bull. Marie Selby Bot. Gard.. 8. 1981: 8 Google Scholar ,9 Arditti J. Ghani A.K.A. Numerical and physical properties of orchid seeds and their biological implications. New Phytol. 2000; 145: 367-421 Crossref PubMed Scopus (453) Google Scholar ,10 Lubinsky P. Van Dam M. Van Dam A. Pollination of Vanilla and evolution in Orchidaceae. Lindleyana. 2006; 75: 926-929 Google Scholar ,11 Householder E. Janovec J. Balarezo Mozambite A. Huinga Maceda J. Wells J. Valega R. Diversity, natural history, and conservation of Vanilla (Orchidaceae) in Amazonian wetlands of Madre de Dios, Peru. J. Bot. Res. Inst. Tex. 2010; 4: 227-243 Google Scholar ,12 Arenas M.A.S. Dressler R.L. A revision of the Mexican and Central American species of Vanilla Plumier ex Miller with a characterization of their ITS region of the nuclear ribosomal DNA. Lankesteriana. 2010; 9: 285-354 Google Scholar ,13 Pansarin E.R. Unravelling the enigma of seed dispersal in Vanilla. Plant Biol. 2021; 23: 974-980 Crossref PubMed Scopus (4) Google Scholar ,14 Lozano Rodríguez M.Á. Rodríguez M.L. Canché J.M.P. García R.A.M. Cabrera C.R.C. Visit frequency of Euglossine bees (Hymenoptera: Apidae) to mature fruits of Vanilla planifolia (Orchidaceae). Acta Bot. Mex. 2022; 129: e2001 Google Scholar ,15 Pansarin E.R. Suetsugu K. Mammal-mediated seed dispersal in Vanilla: its rewards and clues to the evolution of fleshy fruits in orchids. Ecology. 2022; 103: e3701https://doi.org/10.1002/ecy.3701 Crossref PubMed Scopus (3) Google Scholar a pantropical genus of 118 species with vine-like growth. 16 Cameron K.M. Vanilla. in: Pridgeon A.P. Cribb P.J. Chase M.W. Rasmussen F.N. Genera Orchidacearum, Volume 3. Orchidoideae (Part two) Vanilloideae. Oxford University Press, 2003: 281-334 Google Scholar ,17 Chambers A. Cibrián-Jaramillo A. Karremans A.P. Moreno Martinez D. Hernandez-Hernandez J. Brym M. Resende M.F.R. Moloney R. Sierra S.N. Hasing T. et al. Genotyping-by-sequencing diversity analysis of international Vanilla collections uncovers hidden diversity and enables plant improvement. Plant Sci. 2021; 311: 111019 Crossref PubMed Scopus (10) Google Scholar ,18 Karremans A.P. Chinchilla I.F. Rojas-Alvarado G. Cedeño-Fonseca M. Damián A. Léotard G. A reappraisal of Neotropical Vanilla. With a note on taxonomic inflation and the importance of alpha taxonomy in biological studies. Lankesteriana. 2020; 20: 395-497 Google Scholar We test this prediction through in situ and ex situ experimentation using fruits of Vanilla planifolia, and wild relatives, from which vanillin—a widely used natural aroma and flavoring—is obtained. Seeds from dehiscent fruits are removed by male Euglossini collecting fragrances, a unique case in plants, and female Meliponini bees gathering nest-building materials, a first among monocots. By contrast, mammals, mostly rodents, consume the nutritious indehiscent fruits, passing the seeds up to 18 h after consumption. Protocorm formation in digested and undigested seeds proves that scarification in the gut is not strictly required for germination. Multimodal seed dispersal mechanisms are proven for the first time in Orchidaceae, with ectozoochory and endozoochory playing crucial roles in the unusually broad distribution of Vanilla.

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