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Does seed coat structure modulate gut-passage effects on seed germination? Examples from Miconieae DC. (Melastomataceae)

Published online by Cambridge University Press:  04 April 2016

Rafaella C. Ribeiro
Affiliation:
Departamento de Botânica, Instituto de Ciências Biológicas, Universidade Federal de Minas Gerais, 31270-901, Belo Horizonte, Minas Gerais, Brazil
Maria Letícia N. Figueiredo
Affiliation:
Departamento de Botânica, Instituto de Ciências Biológicas, Universidade Federal de Minas Gerais, 31270-901, Belo Horizonte, Minas Gerais, Brazil
Agnello Picorelli
Affiliation:
Departamento de Botânica, Instituto de Ciências Biológicas, Universidade Federal de Minas Gerais, 31270-901, Belo Horizonte, Minas Gerais, Brazil
Denise M.T. Oliveira
Affiliation:
Departamento de Botânica, Instituto de Ciências Biológicas, Universidade Federal de Minas Gerais, 31270-901, Belo Horizonte, Minas Gerais, Brazil
Fernando A.O. Silveira*
Affiliation:
Departamento de Botânica, Instituto de Ciências Biológicas, Universidade Federal de Minas Gerais, 31270-901, Belo Horizonte, Minas Gerais, Brazil
*
*Correspondence Email: [email protected]

Abstract

Fruits of Melastomataceae constitute a key resource for Neotropical frugivores. However, the mechanisms determining gut-passage effects on seed germination are poorly known. Here, we determine how bird gut-passage affects seed germination in three species of Miconieae by running germination experiments, examining changes in seed coat structure and determining germination inhibition by fruit extracts. Mature fruits of Clidemia urceolata, Leandra aurea and Miconia rubiginosa were sampled in south-eastern Brazil and seeds were submitted to treatments evaluating gut-passage effects and different concentrations of fruit extracts. Light and scanning electron microscopy were used to compare seed coat structure and thickness of control and gut-passed seeds. We found minor effects of gut passage on seed germination. However, changes in seed coat structure of gut-passed seeds of L. aurea may have been related to a decrease in germination. Our data also support the idea that germination inhibitors in fruit pulp may contribute to the inhibition effect. Our study corroborates the idea that changes in the seed coat following gut passage modulate the complex fruit–frugivore interactions, especially between plants and generalist dispersers, and that seed cleaning is a key factor determining seedling establishment in Neotropical Melastomataceae.

Type
Research Papers
Copyright
Copyright © Cambridge University Press 2016 

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References

Alves, M.A.S., Ritter, P.D., Antonini, R.D. and Almeida, E.M. (2008) Two thrush species as dispersers of Miconia prasina (Sw.) DC. (Melastomataceae): an experimental approach. Brazilian Journal of Biology 68, 631637.CrossRefGoogle Scholar
Amaral, L.I.V. and Paulilo, M.T.S. (1992) Efeito da luz, temperatura, reguladores de crescimento e nitrato de potássio na germinação de Miconia cinnamomifolia (DC) Naudim. Insula 21, 5986.Google Scholar
Baskin, C.C. and Baskin, J.M. (1998) Seeds. Ecology, biogeography, and evolution of dormancy and germination. San Diego, Academic Press.Google Scholar
Bravo, C., Velilla, S., Bautista, L.M. and Peco, B. (2014) Effects of great bustard (Otis tarda) gut passage on black nightshade (Solanum nigrum) seed germination. Seed Science Research 24, 265271.Google Scholar
Briggs, C.L., Morris, E.C. and Ashford, A.E. (2005) Investigations into seed dormancy in Grevillea linearifolia, G. buxifolia and G. sericea: anatomy and histochemistry of the seed coat. Annals of Botany 96, 965980.Google Scholar
Carreira, R.C. and Zaidan, L.B.P. (2007) Germinação de sementes de espécies de Melastomataceae de Cerrado sob condições controladas de luz e temperatura. Hoehnea 34, 261269.Google Scholar
Charalambidou, I., Santamaría, L., Jansen, C. and Nolet, B.A. (2005) Digestive plasticity in Mallard ducks modulates dispersal probabilities of aquatic plants and crustaceans. Functional Ecology 19, 513519.CrossRefGoogle Scholar
Corner, E.J.H. (1976) The seeds of dicotyledons, vol. 1. Cambridge, Cambridge University Press.Google Scholar
Ellison, A.M., Denslow, A.M., Loiselle, B.A. and Brenes, D.M. (1993) Seed and seedling ecology of neotropical Melastomataceae. Ecology 74, 17371749.Google Scholar
Goldenberg, R., Almeda, F., Caddah, M.K., Martins, A.B., Meirelles, J., Michelangeli, F.A. and Weiss, M. (2013) Nomenclator botanicus for the neotropical genus Miconia (Melastomataceae: Miconieae). Phytotaxa 106, 1171.Google Scholar
Gomes, V.S.M., Correia, M.C.R., Lima, H.A. and Alves, M.A.S. (2008) Potential role of frugivorous birds (Passeriformes) on seed dispersal of six plant species of a restinga habitat, southeastern Brazil. Revista de Biología Tropical 56, 205216.Google ScholarPubMed
Jensen, W.A. (1962) Botanical histochemistry: principles and pratice. San Francisco, W.H. Freeman.Google Scholar
Johansen, D.A. (1940) Plant microtechnique. New York, McGraw-Hill.Google Scholar
Jordano, P. (2000) Fruits and frugivory. pp. 125166 in Fenner, M. (Ed.) Seeds: the ecology of regeneration in plant communities. Wallingford, CAB International.Google Scholar
Karasov, W. and Levey, D.J. (1990) Digestive system trade-offs and adaptations of frugivorous passerine birds. Physiological Zoology 63, 12481270.Google Scholar
Karnovsky, M.J. (1965) A formaldehyde-glutaraldehyde fixative of high osmolality for use in electron microscopy. Journal of Cell Biology 27, 137A138A.Google Scholar
Levey, D.J. and Martínez del Rio, C.M. (2001) It takes guts (and more) to eat fruit: lessons from avian nutritional ecology. The Auk 118, 819831.CrossRefGoogle Scholar
Madeira, J.A. and Fernandes, G.W. (1999) Reproductive phenology of sympatric species of Chamaecrista (Leguminosae) in Serra do Cipó, Brazil. Journal of Tropical Ecology 15, 463479.CrossRefGoogle Scholar
McKey, D. (1975) The ecology of coevolved seed dispersal systems. pp. 159191 in Gilbert, L.E.; Raven, P.H. (Eds) Coevolution of animals and plants. Austin, University of Texas Press.Google Scholar
Murray, K.G., Russell, S., Picone, C.M., Winnett-Murray, K., Sherwood, W. and Kuhlmann, M.L. (1994) Fruit laxatives and seed passage rates in frugivores: consequences for plant reproductive success. Ecology 75, 989994.Google Scholar
O'Brien, T.P., Feder, N. and McCully, M.E. (1964) Polychromatic staining of plant cell walls by toluidine blue O. Protoplasma 59, 368373.Google Scholar
Ocampo, G. and Almeda, F. (2013) Seed diversity in the Miconieae (Melastomataceae): morphological characterization and phenetic relationships. Phytotaxa 80, 1129.Google Scholar
Paiva, E.A.S., Pinho, S.Z. and Oliveira, D.M.T. (2011) Large plant samples: how to process for GMA embedding? pp. 3749 in Chiarini-Garcia, H.; Melo, R.C.N. (Eds) Light microscopy: methods and protocols. New York, Springer/Humana Press.Google Scholar
Pollux, B.J.A., Santamaria, L. and Ouborg, N.J. (2005) Differences in endozoochorous dispersal between aquatic plant species, with reference to plant population persistence in rivers. Freshwater Biology 50, 232242.Google Scholar
Ranal, M.A. and Santana, D.G. (2006) How and why to measure the germination process? Revista Brasileira de Botânica 29, 111.Google Scholar
Renner, S.S., Clausing, G. and Meyer, K. (2001) Historical biogeography of Melastomataceae: the role of Tertiary migration and long-distance dispersal. American Journal of Botany 88, 12901300.Google Scholar
Ribeiro, R.C. and Oliveira, D.M.T. (2014) Small and hard seeds: a practical and inexpensive method to improve embedding techniques for light microscopy. Acta Botanica Brasilica 28, 624630.Google Scholar
Samuels, A. and Levey, D.J. (2005) Effects of gut passage on seed germination: do experiments answer the questions they ask? Functional Ecology 19, 365368.Google Scholar
Santamaría, L., Charalambidou, I., Figuerola, J. and Green, A.J. (2002) Effect of passage through duck gut on germination of fennel pondweed seeds. Archiv für Hydrobiologie 156, 1122.Google Scholar
Schupp, E.W., Jordano, P. and Gómez, J.M. (2010) Seed dispersal effectiveness revisited: a conceptual review. New Phytologist 188, 333353.Google Scholar
Sick, H. (1997) Ornitologia brasileira, edição revista e ampliada por José Fernando Pacheco. Rio de Janeiro, Nova Fronteira.Google Scholar
Silveira, F.A.O., Mafia, P.O., Lemos-Filho, J.P. and Fernandes, G.W. (2012) Species-specific outcomes of avian gut passage on germination of Melastomataceae seeds. Plant Ecology and Evolution 145, 350355.Google Scholar
Silveira, F.A.O., Fernandes, G.W. and Lemos-Filho, J.P. (2013) Seed and seedling ecophysiology of neotropical Melastomataceae: implications for conservation and restoration of savannas and rain forests. Annals of the Missouri Botanical Garden 99, 8299.Google Scholar
Silveira, F.A.O., Negreiros, D., Barbosa, N.P.U., Buisson, E., Carmo, F.F., Carstensen, D.W., Conceicao, A.A., Cornelissen, T.G., Echternacht, L., Fernandes, G.W., Garcia, Q.S., Guerra, T.J., Jacobi, C.M., Lemos-Filho, J.P., Le Stradic, S., Morellato, L.P.C., Neves, F.S., Oliveira, R.S., Schaefer, C.E., Viana, P.L. and Lambers, H. (2016) Ecology and evolution of plant diversity in the endangered campo rupestre: a neglected conservation priority. Plant and Soil doi:10.1007/s11104-015-2637-8.CrossRefGoogle Scholar
Stiles, F.G. and Rosselli, L. (1993) Consumption of fruits of the Melastomataceae by birds: how diffuse is coevolution? Vegetation 107/108, 5773.Google Scholar
Tewksbury, J.J., Levey, D.J., Huizinga, M., Haak, D.C. and Traveset, A. (2008) Costs and benefits of capsaicin-mediated control of gut retention in dispersers of wild chilies. Ecology 89, 107117.Google Scholar
Traveset, A. (1998) Effect of seed passage through vertebrate frugivores’ guts on germination: a review. Perspectives Plant Ecology Evolution Systematics 12, 151190.Google Scholar
Traveset, A., Riera, N. and Mas, R.E. (2001a) Passage through bird guts causes interspecific differences in seed germination characteristics. Functional Ecology 15, 669675.Google Scholar
Traveset, A., Riera, N. and Mas, R.E. (2001b) Ecology of fruit colour polymorphism in Myrtus communis and differential effects of birds and mammals on seed germination and seedling growth. Journal of Ecology 89, 749760.Google Scholar
Traveset, A., Roberstson, A. and Rodríguez-Pérez, J. (2007) A review on the role of endozoochory on seed germination. pp. 78103 in Dennis, A.J.; Schupp, E.W.; Green, R.J.; Westcott, D.A. (Eds) Seed dispersal: theory and its application in a changing world. Wallingford, CAB International.Google Scholar
Traveset, A., Rodríguez, R. and Pías, B. (2008) Seed traits changes in dispersers’ gut and consequences for germination and seedling growth. Ecology 89, 95106.Google Scholar
Verdú, M. and Traveset, A. (2004) Bridging meta-analysis with the comparative method: a test of seed size effect on germination after frugivores’ gut passage. Oecologia 138, 414418.Google Scholar
Werker, E. (1997) Seed anatomy. Berlin, Gebrüder Borntraeger.Google Scholar