Hostname: page-component-78c5997874-8bhkd Total loading time: 0 Render date: 2024-11-15T08:05:41.279Z Has data issue: false hasContentIssue false
  • English
  • Français

Modularity in ecological networks between frugivorous birds and congeneric plant species

Published online by Cambridge University Press:  31 August 2016

Adriano M. Silva ,
Pietro K. Maruyama ,
Luís Pedro M. Paniago  and
Celine Melo
Adriano M. Silva*
Affiliation:
Instituto de Biologia, Universidade Federal de Uberlândia, Bl. 2D Campus Umuarama, CEP 38400–902, Uberlândia, MG, Brazil Instituto de Biologia, Universidade Estadual de Campinas, Cx. Postal 6109, CEP: 13083–865, Campinas, SP, Brazil
Pietro K. Maruyama
Affiliation:
Instituto de Biologia, Universidade Estadual de Campinas, Cx. Postal 6109, CEP: 13083–865, Campinas, SP, Brazil
Luís Pedro M. Paniago
Affiliation:
Instituto de Biologia, Universidade Federal de Uberlândia, Bl. 2D Campus Umuarama, CEP 38400–902, Uberlândia, MG, Brazil
Celine Melo
Affiliation:
Instituto de Biologia, Universidade Federal de Uberlândia, Bl. 2D Campus Umuarama, CEP 38400–902, Uberlândia, MG, Brazil
*
1 Corresponding author. Email: [email protected]
Get access Rights & Permissions [Opens in a new window]

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.

Keywords

frugivoryMiconiamutualistic networksQuanBiMoseed dispersal
Type
Research Article
Information
Journal of Tropical Ecology , Volume 32 , Issue 6 , November 2016 , pp. 526 - 535
Copyright
Copyright © Cambridge University Press 2016 

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

LITERATURE CITED

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 45:1–39.CrossRefGoogle Scholar
BARBER, M. J. 2007. Modularity and community detection in bipartite networks. Physical Review E 76:066102.Google Scholar
BASCOMPTE, J. 2009. Disentangling the web of life. Science 325:416–419.Google Scholar
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 100:9383–9387.CrossRefGoogle ScholarPubMed
BELTRÁN, E., VALIENTE-BANUET, A. & VERDÚ, M. 2012. Trait divergence and indirect interactions allow facilitation of congeneric species. Annals of Botany 110:1369–1376.Google Scholar
BLÜTHGEN, N., MENZEL, F., HOVESTADT, T., FIALA, B. & BLÜTHGEN, N. 2007. Specialization, constraints, and conflicting interests in mutualistic networks. Current Biology 17:341–346.Google Scholar
BLÜTHGEN, N., FRÜND, J., VAZQUEZ, D. P. & MENZEL, F. 2008. What do interaction network metrics tell us about specialization and biological traits? Ecology 89:3387–3399.CrossRefGoogle ScholarPubMed
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 24:127–135.CrossRefGoogle ScholarPubMed
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.Google Scholar
BORGHESIO, L. & LAIOLO, P. 2004. Seasonal foraging ecology in a forest avifauna of northern Kenya. Journal of Tropical Ecology 20:145–155.Google Scholar
CARNICER, J., JORDANO, P. & MELIAN, C. J. 2009. The temporal dynamics of resource use by frugivorous birds: a network approach. Ecology 90:1958–1970.CrossRefGoogle ScholarPubMed
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 14:773–781.CrossRefGoogle ScholarPubMed
DORMANN, C. F. & STRAUSS, R. 2014. A method for detecting modules in quantitative bipartite networks. Methods in Ecology and Evolution 5:90–98.CrossRefGoogle Scholar
DORMANN, C. F., FRÜND, J., BLÜTHGEN, N. & GRUBER, B. 2009. Indices, graphs and null models: analyzing bipartite ecological networks. The Open Ecology Journal 2:7–24.Google Scholar
DUNNING, J. B. 2008. CRC handbook of avian body masses. (Second edition.). CRC Press, Boca Raton. 574 pp.Google Scholar
ELLISON, A. M., DENSLOW, J. S., LOISELLE, B. A. & BRENES, D. 1993. Seed and seedling ecology of Neotropical Melastomataceae. American Naturalist 140: 447–476.Google Scholar
ERDŐS, P. & RÉNYI, A. 1959. On random graphs. Publicationes Mathematicae 6:290–297.Google Scholar
FONSECA, C. R. & GANADE, G. 1996. Asymmetries, compartments and null interactions in an Amazonian ant-plant community. Journal of Animal Ecology 65:339–347.CrossRefGoogle Scholar
GILARRANZ, L. J., PASTOR, J. M. & GALEANO, J. 2012. The architecture of weighted mutualistic networks. Oikos 121:1154–1162.Google Scholar
GUIMERÀ, R. & AMARAL, L. N. 2005. Functional cartography of complex metabolic networks. Nature 433:895–900.CrossRefGoogle ScholarPubMed
HERRERA, C. 1981. Fruit variation and competition for dispersers in natural populations of Smilax aspera . Oikos 36:51–58.Google Scholar
HOWE, H. F. 1993. Specialized and generalized dispersal systems: where does ‘the paradigm’ stand? Vegetatio 107/108:3–13.CrossRefGoogle Scholar
HOWE, H. F. & ESTABROOK, G. F. 1977. On intraspecific competition for avian dispersers in tropical trees. American Naturalist 111:817.Google Scholar
HOWE, H. F. & SMALLWOOD, J. 1982. Ecology of seed dispersal. Annual Review of Ecology and Systematics 13:201–228.Google Scholar
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/ Google Scholar
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 78:253–269.Google Scholar
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 104:3278–3282.CrossRefGoogle ScholarPubMed
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 274:799–808.Google Scholar
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 179:501–511.CrossRefGoogle ScholarPubMed
KRAUSE, A. E., FRANK, K. A., MASON, D. M., ULANOWICZ, R. E. & TAYLOR, W. W. 2003. Compartments revealed in food-web structure. Nature 426:282–285.Google Scholar
LEVEY, D. J. & STILES, F. G. 1992. Evolutionary precursors of long-distance migration: resource availability and movement patterns in neotropical landbirds. American Naturalist 140:447–476.CrossRefGoogle Scholar
LOISELLE, B. A. & BLAKE, J. G. 1991. Temporal variation in birds and fruits along an elevational gradient in Costa Rica. Ecology 72:180–193.Google Scholar
LOSOS, J. B. 2008. Phylogenetic niche conservatism, phylogenetic signal and the relationship between phylogenetic relatedness and ecological similarity among species. Ecology Letters 11:995–1003.Google Scholar
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 37:221–224.CrossRefGoogle Scholar
MARTÍN GONZÁLEZ, A. M., ALLESINA, S., RODRIGO, A. & BOSCH, J. 2012. Drivers of compartmentalization in a Mediterranean pollination network. Oikos 121:2001–2013.CrossRefGoogle Scholar
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 5:672–674.Google Scholar
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 29:99–109.Google Scholar
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 46:740–747.CrossRefGoogle Scholar
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 178:783–793.CrossRefGoogle ScholarPubMed
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 167:131–140.Google Scholar
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 124:1031–1039.CrossRefGoogle Scholar
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 121:1553–1566.Google Scholar
NUNES, A. P. & TOMAS, W. M. 2008. Aves migratórias e nômades ocorrentes no Pantanal. Embrapa Pantanal, Corumbá. 124 pp.Google Scholar
OLESEN, J. M., BASCOMPTE, J., DUPONT, Y. L. & JORDANO, P. 2007. The modularity of pollination networks. Proceedings of the National Academy of Sciences USA 104:19891–19896.Google Scholar
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.Google Scholar
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) 30:91–97.Google Scholar
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 15:213–227.Google Scholar
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 Google Scholar
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 12:779–788.Google Scholar
ROBBINS, C. T. 1981. Estimation of the relative protein cost of reproduction in birds. The Condor 83:177–179.Google Scholar
ROMERO, R. & MARTINS, A. 2002. Melastomataceae from Serra da Canastra National Park, Minas Gerais, Brazil. Revista Brasileira de Botânica 25:19–24.Google Scholar
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 176:837–848.CrossRefGoogle ScholarPubMed
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 17:454–463.Google Scholar
SCOTTI, M., PODANI, J. & JORDÁN, F. 2007. Weighting, scale dependence and indirect effects in ecological networks: a comparative study. Ecological Complexity 4:148–159.Google Scholar
SICK, H. 1997. Ornitologia Brasileira. (Second edition.). Editora Nova Fronteira, Rio de Janeiro, Brazil. 912 pp.Google Scholar
SILVA, A. M. & MELO, C. 2013. Overlap and resource sharing in coteries of fruit-eating birds. Journal of Tropical Ecology 29:409–416.CrossRefGoogle Scholar
SNOW, D. D. W. 1981. Tropical frugivorous birds and their food plants: a world survey. Biotropica 13:1–14.Google Scholar
STILES, F. G. & ROSSELLI, L. 1993. Consumption of fruits of the Melastomataceae by birds: how diffuse is coevolution? Advances in Vegetation Science 15:57–73.Google Scholar
STOUFFER, D. B. & BASCOMPTE, J. 2011. Compartmentalization increases food-web persistence. Proceedings of the National Academy of Sciences USA 108:3648–3652.Google Scholar
TERBORGH, J. & DIAMOND, J. M. 1970. Niche overlap in feeding assemblages of New Guinea birds. The Wilson Bulletin 82:29–52.Google Scholar
TUR, C., OLESEN, J. M. & TRAVESET, A. 2015. Increasing modularity when downscaling networks from species to individuals. Oikos 124:581–592.CrossRefGoogle Scholar
TYLIANAKIS, J. M., LALIBERTÉ, E., NIELSEN, A. & BASCOMPTE, J. 2010. Conservation of species interaction networks. Biological Conservation 143:2270–2279.Google Scholar
VÁZQUEZ, D. P., MELIÁN, C., WILLIAMS, N., BLÜTHGEN, N., KRASNOV, B. & POULIN, R. 2007. Species abundance and asymmetric interaction strength in ecological networks. Oikos 116:1120–1127.Google Scholar
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 103:1445–1457.Google Scholar
VÁZQUEZ, D. P., CHACOFF, N. P. & CAGNOLO, L. 2009b. Evaluating multiple determinants of the structure of plant-animal mutualistic networks. Ecology 90:2039–2046.CrossRefGoogle ScholarPubMed
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.Google Scholar
WEBB, C. O., ACKERLY, D. D., MCPEEK, M. A. & DONOGHUE, M. J. 2002. Phylogenies and community ecology. Annual Review of Ecology and Systematics 33:475–505.Google Scholar
WHEELWRIGHT, N. T. 1985. Fruit size, gape width, and the diets of fruit-eating birds. Ecology 66:808–818.Google Scholar
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 39:1973–1983.Google Scholar