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Temporal dynamics in the effectiveness of seed dispersal by birds visiting a tropical tree

Published online by Cambridge University Press:  26 July 2018

Marco A. Pizo*
Affiliation:
Department of Zoology, São Paulo State University (UNESP), Institute of Biosciences, Rio Claro, Brazil
Paulo H. S. A. Camargo
Affiliation:
Graduate Program in Ecology and Biodiversity, São Paulo State University (UNESP), Institute of Biosciences, Rio Claro, Brazil
*
*Corresponding author. Email: [email protected]

Abstract:

Seed dispersal effectiveness (SDE) is related to the role of seed dispersal agents in realizing the reproductive potential of plants through seed dispersal and subsequent plant recruitment. The SDE of a given seed disperser may vary spatially and temporally, with important implications for our understanding of the mutualistic relationships involving plants and frugivores. Here we observed 22 frugivorous bird species visiting an individual tree (Cabralea canjerana) over a 9-y period in a fragment of Atlantic forest in south-eastern Brazil to document the temporal variation in SDE. The quantitative (that takes into account the frequency of feeding visits to the focal plant and the number of fruits removed per visit) and qualitative (that considers the probability of seed deposition on a suitable site for plant recruitment) components of SDE varied in two and one order of magnitude both among bird species and among years within bird species, respectively. As a result, the SDE of bird species fluctuates over the years, especially for a migratory species that is the main seed disperser of C. canjerana (Chivi vireo Vireo chivi) whose quantitative component (i.e. the product of visit and fruit intake rates) varied from 3.0 to 7.1. This study illustrates the dynamic nature of the seed-dispersal environment to which a plant is subjected to over the course of its life, which has important consequences for the plant's individual fitness.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2018 

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References

LITERATURE CITED

BLAKE, J. G. & LOISELLE, B. A. 1991. Variation in resource abundance affects capture rates of birds in three lowland habitats in Costa Rica. The Auk 108:114130.Google Scholar
BLENDINGER, P. G., GIANNINI, N. P., ZAMPINI, I. C., ORDOÑEZ, R., TORRES, S., SAYAGO, J. E., RUGERA, R. A. & ISLA, M. I. 2015. Nutrients in fruits as determinants of resource tracking by birds. Ibis 157:480495.Google Scholar
BLIGH, E. G. & DYER, W. J. 1959. A rapid method of total lipid extraction and purification. Canadian Journal of Biochemistry and Physiology 37:911917.Google Scholar
FRENCH, A. R. & SMITH, T. B. 2005. Importance of body size in determining dominance hierarchies among diverse tropical frugivores. Biotropica 37:96101.Google Scholar
GALETTI, M., GUEVARA, R., CÔRTES, M. C., FADINI, R., VON MATTER, S., LEITE, A. B., LABECCA, F., RIBEIRO, T., CARVALHO, C. S., COLLEVATTI, R. G., PIRES, M. M., GUIMARÃES, P. R., BRANCALION, P. H., RIBEIRO, M. C. & JORDANO, P. 2013. Functional extinction of birds drives rapid evolutionary changes in seed size. Science 340:10861090.Google Scholar
GROEMPING, U. 2006. Relative importance for linear regression in R: the package relaimpo. Journal of Statistical Software 17:127.Google Scholar
HERRERA, C. M. 1985. Determinants of plant-animal coevolution: the case of mutualistic dispersal of seeds by vertebrates. Oikos 44:132141.Google Scholar
HERRERA, C. M. 1998. Long-term dynamics of Mediterranean frugivorous birds and fleshy fruits: a 12-year study. Ecological Monographs 68:511538.Google Scholar
HORWITZ, W. 1975. Official methods of analysis. Association of Official Analytical Chemists/AOAC, Arlington. 1094 pp.Google Scholar
HOULE, A., CHAPMAN, C. A. & VICKERY, W. L. 2007. Intratree variation in fruit production and implications for primate foraging. International Journal of Primatology 28:11971217.Google Scholar
HOWE, H. F. & DE STEVEN, D. 1979. Fruit production, migrant bird visitation, and seed dispersal of Guarea glabra in Panama. Oecologia 39:185196.Google Scholar
JORDANO, P. 1995. Spatial and temporal variation in the avian-frugivore assemblage of Prunus mahaleb: patterns and consequences. Oikos 71:479491.Google Scholar
JORDANO, P. & SCHUPP, E. W. 2000. Determinants of seed disperser effectiveness: the quantity component and patterns of seed rain for Prunus mahaleb. Ecological Monographs 70:591615.Google Scholar
LEVEY, D. J. & MARTÍNEZ-DEL-RIO, C. 2001. It takes guts (and more) to eat fruit: lessons from avian nutritional ecology. Auk 118:819831.Google Scholar
MALE, T. D. & ROBERTS, G. E. 2002. Defense of fruiting trees by birds in an Australian forest. Biotropica 34:172176.Google Scholar
MCCONKEY, K. R., BROCKELMAN, W. Y. & SARALAMBA, C. 2014. Mammalian frugivores with different foraging behavior can show similar seed dispersal effectiveness. Biotropica 46:647651.Google Scholar
MORELLATO, L. P. C. & HADDAD, C. F. B. 2000. Introduction: the Brazilian Atlantic Forest. Biotropica 32:786792.Google Scholar
NATHAN, R. & MULLER-LANDAU, H. C. 2000. Spatial patterns of seed dispersal, their determinants and consequences for recruitment. Trends in Ecology and Evolution 15:278285.Google Scholar
PENNINGTON, T. D. 1981. Flora neotropica: monograph number 28. Meliaceae. New York Botanical Garden, New York. 472 pp.Google Scholar
PIACENTINI, V. D. Q., ALEIXO, A., AGNE, C. E., MAURIĆIO, G. N., PACHECO, J. F., BRAVO, G. A., BRITO, G. R. R., NAKA, L. N., OLMOS, F., POSSO, S., SILVEIRA, L. F., BETINI, G. S., CARRANO, E., FRANZ, I., LEES, A. C., LIMA, L.M., PIOLI, D., SCHUNCK, F., DO AMARAL, F. R., BENCKE, G. A., COHN-HAFT, M., FIGUEIREDO, L. F. A., STRAUBE, F. C. & CESARI, E. 2015. Annotated checklist of the birds of Brazil by the Brazilian Ornithological Records Committee/Lista comentada das aves do Brasil pelo Comitê Brasileiro de Registros Ornitológicos. Revista Brasileira de Ornitologia 23:90298.Google Scholar
PIZO, M. A. 1997. Seed dispersal and predation in two populations of Cabralea canjerana (Meliaceae) in the Atlantic Forest of southeast Brazil. Journal of Tropical Ecology 13:559578.Google Scholar
ROBY, G., HARBERTSON, J. F., ADAMS, D. A. & MATTHEWS, M. A. 2004. Berry size and vine water deficits as factors in winegrape composition: anthocyanins and tannins. Australian Journal of Grape and Wine Research 10:100107.Google Scholar
ROTHER, D. C., PIZO, M. A. & JORDANO, P. 2016. Variation in seed dispersal effectiveness: the redundancy of consequences in diversified tropical frugivore assemblages. Oikos 125:336342.Google Scholar
SAINO, N., AMBROSINI, R., RUBOLINI, D., VON HARDENBERG, J., PROVENZALE, A., HÜPPOP, K., HÜPPOP, O., LEHIKOINEN, A., LEHIKOINEN, E., RAINIO, K., ROMANO, M. & SOKOLOV, L. 2011. Climate warming, ecological mismatch at arrival and population decline in migratory birds. Proceedings of the Royal Society of London B: Biological Sciences 278:835842.Google Scholar
SCHAEFER, H. M., SCHMIDT, V. & BAIRLEIN, F. 2003. Discrimination abilities for nutrients: which difference matters for choosy birds and why? Animal Behaviour 65:531541.Google Scholar
SCHUPP, E. W. 1993. Quantity, quality and the effectiveness of seed dispersal by animals. Vegetatio 107:1529.Google Scholar
SCHUPP, E. W., JORDANO, P. & GÓMEZ, J. M. 2010. Seed dispersal effectiveness revisited: a conceptual review. New Phytologist 188:333353.Google Scholar
SIMMONS, B., SUTHERLAND, W. J., DICKS, L. V., ALBRECHT, J., FARWIG, N., GARCÍA, D., JORDANO, P. & GONZÁLEZ-VARO, J. P. 2018. Moving from frugivory to seed dispersal: incorporating the functional outcomes of interactions in plant-frugivore networks. Journal of Animal Ecology. In press.Google Scholar
TELLERÍA, J. L., RAMIREZ, A. & PÉREZ-TRIS, J. 2008. Fruit tracking between sites and years by birds in Mediterranean wintering grounds. Ecography 31:381388.Google Scholar
TELLERÍA, J. L., CARRASCAL, L. M. & SANTOS, T. 2014. Large-scale features affect spatial variation in seed dispersal by birds in juniper woodlands. Ecological Research 29: 1320.Google Scholar
THOMPSON, J. N. 2005. The geographic mosaic of coevolution. University of Chicago Press, Chicago. 425 pp.Google Scholar
WHEELWRIGHT, N. T. 1993. Fruit size in a tropical tree species: variation, preference by birds, and heritability. Vegetatio 107/108:163174.Google Scholar
WORMAN, C. O. D. & CHAPMAN, C. A. 2005. Seasonal variation in the quality of a tropical ripe fruit and the response of three frugivores. Journal of Tropical Ecology 21: 689697.Google Scholar
YAMAZAKI, Y., NAOE, S., MASAKI, T. & ISAGI, Y. 2016. Temporal variations in seed dispersal patterns of a bird-dispersed tree, Swida controversa (Cornaceae), in a temperate forest. Ecological Research 31:165176.Google Scholar