Hostname: page-component-586b7cd67f-tf8b9 Total loading time: 0 Render date: 2024-11-20T17:31:42.087Z Has data issue: false hasContentIssue false

Frugivory and seed dispersal effectiveness in two Miconia (Melastomataceae) species from ferruginous campo rupestre

Published online by Cambridge University Press:  28 March 2017

Alessandra M. O. Santos
Affiliation:
Departamento de Biologia Geral, Instituto de Ciências Biológicas, UFMG – Universidade Federal de Minas Gerais, CP 486, 31270-901, Belo Horizonte, Brazil
Claudia M. Jacobi
Affiliation:
Departamento de Biologia Geral, Instituto de Ciências Biológicas, UFMG – Universidade Federal de Minas Gerais, CP 486, 31270-901, Belo Horizonte, Brazil
Fernando A. O. Silveira*
Affiliation:
Departamento de Botânica, Instituto de Ciências Biológicas, UFMG – Universidade Federal de Minas Gerais, CP 486, 31270-901, Belo Horizonte, Brazil
*
*Correspondence Email: [email protected]

Abstract

Seed dispersal effectiveness (SDE) is a useful framework to explore the evolutionary and ecological consequences of seed dispersal to plant fitness. However, SDE is poorly studied in tropical open grasslands. Here, we studied both quantitative and qualitative components of SDE in two species of Miconia (Melastomataceae) from ferruginous campo rupestre, a vegetation highly threatened by mining activities. We determined fruit traits and fruit availability and found that fruits of both species are produced in times of resource scarcity at the study site. Based on the number of visits and the number of fruits removed per visit, we calculated the quantitative component of SDE for both species. Finally, we explored the qualitative component of SDE by means of a controlled experiment that simulated the effects of gut passage on seed germination. Bird species differed strongly in the quantitative component of SDE. Gut passage did not affect germination compared with hand-extracted seeds, except for a minor negative effect on germination time in M. pepericarpa. However, seeds within intact fruits showed lower germination percentages compared with hand-extracted seeds. Our data indicate that Miconia species from ferruginous campo rupestre are visited by a diverse assemblage of generalist birds that differ in quantitative, but not qualitative, seed dispersal effectiveness. We argue that planting Miconia species can overcome seed limitation in degraded areas and thus assist ecological restoration after mining abandonment.

Type
Research Papers
Copyright
Copyright © Cambridge University Press 2017 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Allenspach, N. and Dias, M.M. (2012) Frugivory by birds on Miconia albicans (Melastomataceae), in a fragment of cerrado in São Carlos, south-eastern Brazil. Brazilian Journal of Biology 72, 407413.Google Scholar
Allenspach, N., Telles, M. and Dias, M.M. (2012) Phenology and frugivory by birds on Miconia ligustroides (Melastomataceae) in a fragment of cerrado, south-eastern Brazil. Brazilian Journal of Biology 72, 859864.Google Scholar
Baldwin, S.P., Oberholser, H.C. and Worley, L.G. (1931) Measurements of birds. Scientific Publications of the Cleveland Museum of Natural History 2, 1165.Google Scholar
Comitê Brasileiro de Registros Ornitológicos (CBRO) (2014) Lista das aves do Brasil. Comitê Brasileiro de Registros Ornitológicos, Sociedade Brasileira de Ornitologia. Available at: http://www4.museu-goeldi.br/revistabrornito/revista/index.php/BJO/article/view/1263/pdf_905 (last accessed 9 March 2017).Google Scholar
Cestari, C. and Pizo, M.A. (2013) Context dependence in seed removal by lekking and non-lekking frugivorous birds in Atlantic forest. Wilson Journal of Ornithology 125, 546551.Google Scholar
Dehling, D.M., Jordano, P., Schaefer, H.M., Böhning-Gaese, K. and Schleuning, M. (2016) Morphology predicts species’ functional roles and their degree of specialisation in plant–frugivore interactions. Proceedings of the Royal Society B 283, 20152444.Google Scholar
Fleming, T.H. and Kress, W.J. (2011) A brief history of fruits and frugivores. Acta Oecologica 37, 521530.CrossRefGoogle Scholar
Duarte, G.T., Ribeiro, M.C. and Paglia, A.P. (2016) Ecosystem services modeling as a tool for defining priority areas for conservation. PLoS ONE e0154573.Google Scholar
Eriksson, O. (2016) Evolution of angiosperm seed disperser mutualisms: the timing of origins and their consequences for coevolutionary interactions between angiosperms and frugivores. Biological Reviews 91, 168186.Google Scholar
Ferreira, J., Aragão, L.E.O.C., Barlow, J., Barreto, P., Berenguer, E., Bustamante, M., Gardner, T.A., Lees, A.C., Lima, A., Louzada, J., Pardini, R., Parry, L., Peres, C. A., Pompeu, P.S., Tabarelli, M. and Zuanon, J. (2014) Brazil's environmental leadership at risk. Science 346, 706707.Google Scholar
Goldenberg, R., Almeda, F., Meirelles, J., Caddah, M.K., Michelangeli, F.A., Martins, A.B. and Weiss, M. (2013) Nomenclator botanicus for the neotropical genus Miconia (Melastomataceae: Miconieae). Phytotaxa 106, 1171.Google Scholar
Graham, C.H., Moermond, T.C., Kristensen, K.A. and Mvukiyumwami, J. (1995) Seed dispersal effectiveness by two bulbuls on Maesa lanceolata, an African montane forest tree. Biotropica 27, 479486.CrossRefGoogle Scholar
Guerra, T.J. and Pizo, M.A. (2014) Asymmetrical dependence between a neotropical mistletoe and its avian seed disperser. Biotropica 46, 285293.CrossRefGoogle Scholar
Guidetti, B.Y., Amico, G.C., Dardanelli, S. and Rodriguez-Cabral, M.A. (2016) Artificial perches promote vegetation restoration. Plant Ecology 217, 935942.CrossRefGoogle Scholar
Gwynne, J.A., Ridgely, R.S., Tudor, G. and Argel, M. (2010) Aves do Brasil: Pantanal e Cerrado. São Paulo: Editora Horizonte.Google Scholar
Howe, H.F. (1993) Specialized and generalized dispersal systems: where does ‘the paradigm’ stand? Vegetatio 107/108, 313.Google Scholar
Howe, H.F. and Smallwood, J. (1982) Ecology of seed dispersal. Annual Review of Ecology and Systematics 13, 201228.CrossRefGoogle Scholar
Jacobi, C. M. and Carmo, F. F. (2012) Diversidade florística nas cangas do Quadrilátero Ferrífero. Belo Horizonte, IDM. 240 pp.Google Scholar
Jacobi, C. M., Carmo, F. F., Vincent, R. C. and Stehmann, J.R. (2007) Plant communities on ironstone outcrops: a diverse and endangered Brazilian ecosystem. Biodiversity and Conservation 16, 21852200.Google Scholar
Jacobi, C.M., Carmo, F.F. and Vincent, R.C. (2008) Estudo fitossociológico de uma comunidade vegetal sobre canga como subsídio para a reabilitação de áreas mineradas no Quadrilátero Ferrífero, MG. Revista Árvore 32, 345353.CrossRefGoogle Scholar
Jacomassa, F.A.F. and Pizo, M.A. (2010) Birds and bats diverge in the qualitative and quantitative components of seed dispersal of a pioneer tree. Acta Oecologica 36, 493496.Google Scholar
Jordano, P. and Schupp, E.W. (2000) Seed disperser effectiveness: the quantity component and patterns of seed rain for Prunus mahaleb . Ecological Monographs 70, 591615.CrossRefGoogle Scholar
Kessler-Rios, M.M. and Kattan, G.H. (2012) Fruits of Melastomataceae: phenology in Andean forest and role as food sources for birds. Journal of Tropical Ecology 28, 1121.Google Scholar
Levey, D.J. (1987) Seed size and fruit-handling techniques of avian frugivores. The American Naturalist 129, 471485.Google Scholar
Levey, D.J. (1990) Habitat-dependent fruiting behaviour of an understorey tree, Miconia centrodesma, and tropical treefall gaps as keystone habitats for frugivores in Costa Rica. Journal of Tropical Ecology 6, 409420.Google Scholar
Levin, S.A., Muller-Landau, H.C., Nathan, R. and Chave, J. (2003) The ecology and evolution of seed dispersal: a theoretical perspective. Annual Review of Ecology, Evolution, and Systematics 34, 575604.Google Scholar
Loiselle, B.A. and Blake, J.G. (1999) Dispersal of melastome seeds by fruit-eating birds of tropical forest understory. Ecology 80, 330336.CrossRefGoogle Scholar
Manhães, M.A., Assis, L.C.S. and Castro, R.M. (2003) Frugivoria e dispersão de sementes de Miconia urophylla (Melastomataceae) por aves em um fragmento de Mata Atlântica secundária em Juiz de Fora, Minas Gerais, Brasil. Ararajuba 11, 173180.Google Scholar
Maruyama, P.K., Borges, M.R., Silva, P.A., Burns, K.C. and Melo, C. (2013) Avian frugivory in Miconia (Melastomataceae): contrasting fruiting times promote habitat complementarity between savanna and palm swamp. Journal of Tropical Ecology 29, 99109.Google Scholar
McKey, D. (1975) The ecology of coevolved seed dispersal systems. In Gilbert, L.E. and Raven, P.H. (eds), Coevolution of Animals and Plants, pp. 159191. Austin: University of Texas Press.Google Scholar
Pizo, M.A. and Galetti, M. (2010) Métodos e perspectivas da frugivoria e dispersão de sementes por aves. In Von Matter, S., Straube, F.C., Accordi, I., Piacentini, V. and Cândido, J.F. Jr (eds), Ornitologia e Conservação: Ciência Aplicada, Técnicas de Pesquisa e Levantamento, pp. 493506. Rio de Janeiro: Technical Books Editora.Google Scholar
Poulin, B., Wright, S.J., Lefebvre, G. and Calderón, O. (1999) Interspecific synchrony and asynchrony in the fruiting phenologies of congeneric bird-dispersed plants in Panamá. Journal of Tropical Ecology 15, 213227.CrossRefGoogle Scholar
R Core Team (2014) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. Available at: http://www.R-project.org/ (last accessed 28 February 2017).Google Scholar
Ruggera, R.A., Gomez, M.D. and Blendinger, P.G. (2016) Frugivory and seed dispersal role of the Yellow-striped Brush-Finch (Atlapetes citrinellus), an endemic emberizid of Argentina. Emu 114, 343351.Google Scholar
Saavedra, F., Hensen, I., Beck, S.G., Böhning-Gaese, K., Lippok, D., Töpfer, T. and Schleuning, M. (2014) Functional importance of avian seed dispersers changes in response to human-induced forest edges in tropical seed-dispersal networks. Oecologia 176, 837848.CrossRefGoogle ScholarPubMed
Samuels, I.A. and Levey, D.J. (2005) Effects of gut passage on seed germination: do experiments answer the questions they ask? Functional Ecology 19, 365368.CrossRefGoogle Scholar
Schupp, E.W., Jordano, P. and Gomez, J.M. (2010) Seed dispersal effectiveness revisited: a conceptual review. New Phytologist 188, 333353.Google Scholar
Sigrist, T. (2009) Guia de Campo Avis Brasilis: Avifauna Brasileira. Avis Brasilis, São Paulo. 480 pp.Google Scholar
Sileshi, G.W. (2012) A critique of current trends in the statistical analysis of seed germination and viability data. Seed Science Research 22, 145159.Google Scholar
Silveira, F.A.O., Fernandes, G.W. and Lemos-Filho, J.P. (2013a) Seed and seedling ecophysiology of Neotropical Melastomataceae: implications for conservation and restoration of savannas and rainforests. Annals of the Missouri Botanical Garden 99, 8299.Google Scholar
Silveira, F.A.O., Ribeiro, R.C., Soares, S., Rocha, D. and Moura, C.O. (2013b) Physiological dormancy and seed germination inhibitors in Melastomataceae. Plant Ecology and Evolution 146, 290294.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
Snow, D.W. (1965) A possible selective factor in the evolution of fruiting seasons in tropical Forest. Oikos 15, 274281.Google Scholar
Straube, F.C. (2013) Um incômodo consenso: estudo de caso sobre Elaenia . Atualidades Ornitológicas 172, 3748.Google Scholar
Stiles, F.G. and Rosselli, L. (1993) Consumption of fruits of the Melastomataceae by birds: how diffuse is coevolution? Vegetatio 108, 5773.CrossRefGoogle Scholar
Traveset, A., Robertson, A.W. and Rodríguez-Pérez, J. (2007) A review on the role of endozoochory in seed germination. In Dennis, A.J., Schupp, E.W., Green, R.J. and Westcott, D.A. (eds), Seed Dispersal: Theory and its Application in a Changing World, pp. 78103. CAB International, Wallingford, United Kingdom.Google Scholar
Traveset, A. and Verdú, M. (2002) A meta-analysis of the effect of gut treatment on seed germination. In Levey, D.J., Silva, W.R. and Galetti, M. (eds), Seed Dispersal and Frugivory: Ecology, Evolution and Conservation, pp. 339350. CAB International, Wallingford, United Kingdom.Google Scholar
Vasconcelos, M.F. and Hoffmann, D. (2015) Avifauna das vegetações abertas e semiabertas associadas a geossistemas ferruginosos do Brasil: levantamento, conservação e perspectivas para futuros estudos. In Carmo, F.F. and Kamino, L.H.Y. (eds), Geossistemas ferruginosos do Brasil: áreas prioritárias para conservação da diversidade geológica e biológica, patrimônio cultural e serviços ambientais, pp. 259287. Belo Horizonte, 3i Editora.Google Scholar
Wischhoff, U., Marques-Santos, F. and Rodrigues, M. (2014) Foraging behavior and diet of the vulnerable Cinereous Warbling-finch Poospiza cinerea (Aves, Emberizidae). Brazilian Journal of Biology 74, 821827.Google Scholar
Supplementary material: File

Santos supplementary material

Supplementary Tables and Figures

Download Santos supplementary material(File)
File 26.9 MB