Skip to main content Accessibility help
×
Home

Modularity in ecological networks between frugivorous birds and congeneric plant species

  • Adriano M. Silva (a1) (a2), Pietro K. Maruyama (a2), Luís Pedro M. Paniago (a1) and Celine Melo (a1)

Abstract:

Ecological and evolutionary factors influence the presence of modules in species interaction networks, and these modules usually cluster functional similar species. But whether closely related species form modules is still unknown. We tested whether the interaction networks formed by frugivorous birds and Miconia plants are modular and evaluated how modules were divided. To do so, we gathered from the literature data concerning four networks of Miconia and their frugivorous birds (three from Brazilian savanna and one from a rain forest in Panama). We quantified modularity using binary and weighted algorithms and also tested the relationship between bird traits (body mass, dietary specialization, migratory behaviour and phylogeny) in relation to within- and among-module connectivity indices (c and z values). If considering only binary information, networks did not present distinct modular structure. Nevertheless, by including interaction strength, modules can be detected in all four Miconia-bird networks. None of the bird traits, however, was related with the connectivity indices. The possible fluctuation of frugivorous bird abundance coupled with the asynchronic fruiting period of Miconia might favour the formation of temporal modules comprising birds and plant species with phenological overlap, ensuring seed dispersal and facilitating the coexistence in sympatry. Bird traits had little effect on the role that each species plays within the modular network, probably because the frugivorous assemblages were dominated by small-bodied and opportunistic species.

Copyright

Corresponding author

1 Corresponding author. Email: adriano.biologia@yahoo.com.br

References

Hide All
ARIM, M., BERAZATEGUI, M., BARRENECHE, J. M., ZIEGLER, L., ZARUCKI, M. & ABADES, S. R. 2011. Determinants of density-body size scaling within food webs and tools for their detection. Advances in Ecological Research 45:139.
BARBER, M. J. 2007. Modularity and community detection in bipartite networks. Physical Review E 76:066102.
BASCOMPTE, J. 2009. Disentangling the web of life. Science 325:416419.
BASCOMPTE, J., JORDANO, P., MELIÁN, C. J. & OLESEN, J. M. 2003. The nested assembly of plant-animal mutualistic networks. Proceedings of the National Academy of Sciences USA 100:93839387.
BELTRÁN, E., VALIENTE-BANUET, A. & VERDÚ, M. 2012. Trait divergence and indirect interactions allow facilitation of congeneric species. Annals of Botany 110:13691376.
BLÜTHGEN, N., MENZEL, F., HOVESTADT, T., FIALA, B. & BLÜTHGEN, N. 2007. Specialization, constraints, and conflicting interests in mutualistic networks. Current Biology 17:341346.
BLÜTHGEN, N., FRÜND, J., VAZQUEZ, D. P. & MENZEL, F. 2008. What do interaction network metrics tell us about specialization and biological traits? Ecology 89:33873399.
BOLKER, B. M., BROOKS, M. E., CLARK, C. J., GEANGE, S. W., POULSEN, J. R., STEVENS, M. H. H. & WHITE, J. S. 2009. Generalized linear mixed models: a practical guide for ecology and evolution. Trends in Ecology and Evolution 24:127135.
BORGES, M. R. 2010. Oferta de frutos e frugivoria por aves, em espécies do gênero Miconia Ruiz and Pav. (Melastomataceae) em duas áreas do Cerrado. Universidade Federal de Uberlândia.
BORGHESIO, L. & LAIOLO, P. 2004. Seasonal foraging ecology in a forest avifauna of northern Kenya. Journal of Tropical Ecology 20:145155.
CARNICER, J., JORDANO, P. & MELIAN, C. J. 2009. The temporal dynamics of resource use by frugivorous birds: a network approach. Ecology 90:19581970.
DONATTI, C. I., GUIMARÃES, P. R., GALETTI, M., PIZO, M. A., MARQUITTI, F. M. D. & DIRZO, R. 2011. Analysis of a hyper-diverse seed dispersal network: modularity and underlying mechanisms. Ecology Letters 14:773781.
DORMANN, C. F. & STRAUSS, R. 2014. A method for detecting modules in quantitative bipartite networks. Methods in Ecology and Evolution 5:9098.
DORMANN, C. F., FRÜND, J., BLÜTHGEN, N. & GRUBER, B. 2009. Indices, graphs and null models: analyzing bipartite ecological networks. The Open Ecology Journal 2:724.
DUNNING, J. B. 2008. CRC handbook of avian body masses. (Second edition.). CRC Press, Boca Raton. 574 pp.
ELLISON, A. M., DENSLOW, J. S., LOISELLE, B. A. & BRENES, D. 1993. Seed and seedling ecology of Neotropical Melastomataceae. American Naturalist 140: 447476.
ERDŐS, P. & RÉNYI, A. 1959. On random graphs. Publicationes Mathematicae 6:290297.
FONSECA, C. R. & GANADE, G. 1996. Asymmetries, compartments and null interactions in an Amazonian ant-plant community. Journal of Animal Ecology 65:339347.
GILARRANZ, L. J., PASTOR, J. M. & GALEANO, J. 2012. The architecture of weighted mutualistic networks. Oikos 121:11541162.
GUIMERÀ, R. & AMARAL, L. N. 2005. Functional cartography of complex metabolic networks. Nature 433:895900.
HERRERA, C. 1981. Fruit variation and competition for dispersers in natural populations of Smilax aspera . Oikos 36:5158.
HOWE, H. F. 1993. Specialized and generalized dispersal systems: where does ‘the paradigm’ stand? Vegetatio 107/108:313.
HOWE, H. F. & ESTABROOK, G. F. 1977. On intraspecific competition for avian dispersers in tropical trees. American Naturalist 111:817.
HOWE, H. F. & SMALLWOOD, J. 1982. Ecology of seed dispersal. Annual Review of Ecology and Systematics 13:201228.
DEL HOYO, J., ELLIOTT, A., SARGATAL, J., CHRISTIE, D. A. & DE JUANA, E. 2015. Handbook of the birds of the world alive. Lynx Edicions, Barcelona. http://www.hbw.com/
INGS, T. C., MONTOYA, J. M., BASCOMPTE, J., BLÜTHGEN, N., BROWN, L., DORMANN, C. F., EDWARDS, F., FIGUEROA, D., JACOB, U., JONES, J. I., LAURIDSEN, R. B., LEDGER, M. E., LEWIS, H. M., OLESEN, J. M., VAN VEEN, F. J. F., WARREN, P. H. & WOODWARD, G. 2009. Ecological networks – beyond food webs. Journal of Animal Ecology 78:253269.
JORDANO, P., GODOY, J. A., GARCIA, J. L. & GARCÍA-CASTAÑO, J. L. 2007. Differential contribution of frugivores to complex. Proceedings of the National Academy of Sciences USA 104:32783282.
KISSLING, W. D., RAHBEK, C. & BÖHNING-GAESE, K. 2007. Food plant diversity as broad-scale determinant of avian frugivore richness. Proceedings of the Royal Society B: Biological Sciences 274:799808.
KRASNOV, B. R., FORTUNA, M. A., MOUILLOT, D., KHOKHLOVA, I. S., SHENBROT, G. I. & POULIN, R. 2012. Phylogenetic signal in module composition and species connectivity in compartmentalized host-parasite networks. American Naturalist 179:501511.
KRAUSE, A. E., FRANK, K. A., MASON, D. M., ULANOWICZ, R. E. & TAYLOR, W. W. 2003. Compartments revealed in food-web structure. Nature 426:282285.
LEVEY, D. J. & STILES, F. G. 1992. Evolutionary precursors of long-distance migration: resource availability and movement patterns in neotropical landbirds. American Naturalist 140:447476.
LOISELLE, B. A. & BLAKE, J. G. 1991. Temporal variation in birds and fruits along an elevational gradient in Costa Rica. Ecology 72:180193.
LOSOS, J. B. 2008. Phylogenetic niche conservatism, phylogenetic signal and the relationship between phylogenetic relatedness and ecological similarity among species. Ecology Letters 11:9951003.
MARQUITTI, F. M. D., GUIMARÃES, P. R., PIRES, M. M. & BITTENCOURT, L. F. 2014. MODULAR: software for the autonomous computation of modularity in large network sets. Ecography 37:221224.
MARTÍN GONZÁLEZ, A. M., ALLESINA, S., RODRIGO, A. & BOSCH, J. 2012. Drivers of compartmentalization in a Mediterranean pollination network. Oikos 121:20012013.
MARUYAMA, P. K., ALVES-SILVA, E. & MELO, C. 2007. Oferta qualitativa e quantitativa de frutos em espécies ornitocóricas do gênero Miconia (Melastomataceae). Revista Brasileira de Biociências 5:672674.
MARUYAMA, P. K., BORGES, M. R., SILVA, P. A., BURNS, K. C. & 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.
MARUYAMA, P. K., VIZENTIN-BUGONI, J., OLIVEIRA, G. M., OLIVEIRA, P. E. & DALSGAARD, B. 2014. Morphological and spatio-temporal mismatches shape a neotropical savanna plant-hummingbird network. Biotropica 46:740747.
MARUYAMA, P. K., VIZENTIN-BUGONI, J., DALSGAARD, B., SAZIMA, I. & SAZIMA, M. 2015. Nectar robbery by a hermit hummingbird: association to floral phenotype and its influence on flowers and network structure. Oecologia 178:783793.
MELLO, M. A. R., MARQUITTI, F. M. D., GUIMARÃES, P. R., KALKO, E. K. V., JORDANO, P. & DE AGUIAR, M. A. M. 2011. The modularity of seed dispersal: differences in structure and robustness between bat– and bird–fruit networks. Oecologia 167:131140.
MELLO, M. A. R., RODRIGUES, F. A., COSTA, L. D. F., KISSLING, W. D., ŞEKERCIOĞLU, Ç. H., MARQUITTI, F. M. D. & KALKO, E. K. V. 2015. Keystone species in seed dispersal networks are mainly determined by dietary specialization. Oikos 124:10311039.
MENKE, S., BÖHNING-GAESE, K. & SCHLEUNING, M. 2012. Plant-frugivore networks are less specialized and more robust at forest-farmland edges than in the interior of a tropical forest. Oikos 121:15531566.
NUNES, A. P. & TOMAS, W. M. 2008. Aves migratórias e nômades ocorrentes no Pantanal. Embrapa Pantanal, Corumbá. 124 pp.
OLESEN, J. M., BASCOMPTE, J., DUPONT, Y. L. & JORDANO, P. 2007. The modularity of pollination networks. Proceedings of the National Academy of Sciences USA 104:1989119896.
PANIAGO, L. P. 2014. Frugivoria por aves em Miconia sp. (Melastomataceae): potencial de dispersão em áreas de cerrado sensu stricto em regeneração. Universidade Federal de Uberlândia.
PATEFIELD, A. 1981. An efficient method of generating r × c tables with given row and column totals. Journal of the Royal Statistical Society. Series C (Applied Statistics) 30:9197.
POULIN, B., WRIGHT, S. J., LEFEBVRE, G. & CALDERÓN, O. 1999. Interspecific synchrony and asynchrony in the fruiting phenologies of congeneric bird-dispersed plants in Panama. Journal of Tropical Ecology 15:213227.
REMSEN, J. V, ARETA, J. I., CADENA, C. D., JARAMILLO, A., NORES, M., PACHECO, J. F., PÉREZ-EMÁN, J., STILES, F. G., STOTZ, D. F. & ZIMMER, K. J. 2015. A classification of the bird species of South America. American Ornithologists' Union. Available from: http://www.museum.lsu.edu/~Remsen/SACCBaseline.htm
REZENDE, E. L., ALBERT, E. M., FORTUNA, M. A. & BASCOMPTE, J. 2009. Compartments in a marine food web associated with phylogeny, body mass, and habitat structure. Ecology Letters 12:779788.
ROBBINS, C. T. 1981. Estimation of the relative protein cost of reproduction in birds. The Condor 83:177179.
ROMERO, R. & MARTINS, A. 2002. Melastomataceae from Serra da Canastra National Park, Minas Gerais, Brazil. Revista Brasileira de Botânica 25:1924.
SAAVEDRA, F., HENSEN, I., BECK, S. G., BÖHNING-GAESE, K., LIPPOK, D., TÖPFER, T. & 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.
SCHLEUNING, M., INGMANN, L., STRAUS, R., FRITZ, S., DALSGAARD, B., MATTHIAS DEHLING, D., PLEIN, M., SAAVEDRA, F., SANDEL, B., SVENNING, J. C., BÖHNING-GAESE, K. & DORMANN, C. F. 2014. Ecological, historical and evolutionary determinants of modularity in weighted seed-dispersal networks. Ecology Letters 17:454463.
SCOTTI, M., PODANI, J. & JORDÁN, F. 2007. Weighting, scale dependence and indirect effects in ecological networks: a comparative study. Ecological Complexity 4:148159.
SICK, H. 1997. Ornitologia Brasileira. (Second edition.). Editora Nova Fronteira, Rio de Janeiro, Brazil. 912 pp.
SILVA, A. M. & MELO, C. 2013. Overlap and resource sharing in coteries of fruit-eating birds. Journal of Tropical Ecology 29:409416.
SNOW, D. D. W. 1981. Tropical frugivorous birds and their food plants: a world survey. Biotropica 13:114.
STILES, F. G. & ROSSELLI, L. 1993. Consumption of fruits of the Melastomataceae by birds: how diffuse is coevolution? Advances in Vegetation Science 15:5773.
STOUFFER, D. B. & BASCOMPTE, J. 2011. Compartmentalization increases food-web persistence. Proceedings of the National Academy of Sciences USA 108:36483652.
TERBORGH, J. & DIAMOND, J. M. 1970. Niche overlap in feeding assemblages of New Guinea birds. The Wilson Bulletin 82:2952.
TUR, C., OLESEN, J. M. & TRAVESET, A. 2015. Increasing modularity when downscaling networks from species to individuals. Oikos 124:581592.
TYLIANAKIS, J. M., LALIBERTÉ, E., NIELSEN, A. & BASCOMPTE, J. 2010. Conservation of species interaction networks. Biological Conservation 143:22702279.
VÁZQUEZ, D. P., MELIÁN, C., WILLIAMS, N., BLÜTHGEN, N., KRASNOV, B. & POULIN, R. 2007. Species abundance and asymmetric interaction strength in ecological networks. Oikos 116:11201127.
VÁZQUEZ, D. P., BLUTHGEN, N., CAGNOLO, L. & CHACOFF, N. P. 2009a. Uniting pattern and process in plant-animal mutualistic networks: a review. Annals of Botany 103:14451457.
VÁZQUEZ, D. P., CHACOFF, N. P. & CAGNOLO, L. 2009b. Evaluating multiple determinants of the structure of plant-animal mutualistic networks. Ecology 90:20392046.
VIZENTIN-BUGONI, J., MARUYAMA, P. K. & SAZIMA, M. 2014. Processes entangling interactions in communities: forbidden links are more important than abundance in a hummingbird-plant network. Proceedings of the Royal Society B: Biological Sciences 281: 20132397.
WEBB, C. O., ACKERLY, D. D., MCPEEK, M. A. & DONOGHUE, M. J. 2002. Phylogenies and community ecology. Annual Review of Ecology and Systematics 33:475505.
WHEELWRIGHT, N. T. 1985. Fruit size, gape width, and the diets of fruit-eating birds. Ecology 66:808818.
WOTTON, D. M. & KELLY, D. 2012. Do larger frugivores move seeds further? Body size, seed dispersal distance, and a case study of a large, sedentary pigeon. Journal of Biogeography 39:19731983.

Keywords

Metrics

Full text views

Total number of HTML views: 0
Total number of PDF views: 0 *
Loading metrics...

Abstract views

Total abstract views: 0 *
Loading metrics...

* Views captured on Cambridge Core between <date>. This data will be updated every 24 hours.

Usage data cannot currently be displayed