Abstract
The relationships between frugivorous animals and plants are of vital importance particularly in tropical forests. The way species interact and how they are organized within interaction networks could be determined by their ecological and morphological characteristics. This study evaluates the hypothesis that the topological position of species within an interaction network is determined by their degree of frugivory, body size, and abundance. Thus, we constructed the frugivory network between birds and plants in a rainforest fragment in northwestern Colombia. The position of the species within the network was calculated based on three centrality measures (degree, betweenness, and closeness), and its association with relative abundance, degree of frugivory, and body size of each bird species was evaluated by means of a generalized linear model. We found that the species that were most abundant and had the smallest body size had central positions in the interaction network. This pattern is contrary to what has been observed in pristine forests, where species with large body size are more important for network stability. Our results suggest that forest fragmentation modifies the roles of species within the network structure, in part, due to changes in the makeup of the original frugivore community. The information presented may be useful to evaluate the effects of the loss of species as a result of anthropic actions, with the aim of generating ecosystem restoration strategies.
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Abbreviations
- BC:
-
Betweenness
- CC:
-
Closeness
- ND:
-
Degree
- PCA:
-
Principal Components Analysis
References
APG IV. 2016. An update of the Angiosperm Phylogeny Group classification for the orders and families of flowering plants : APG IV. Bot. J. Linn. Soc. 181:1–20.
Audubon, and Cornell Lab of Ornithology. 2018. eBird. http://ebird.org/explore.
Barthélemy, M. 2004. Betweenness centrality in large complex networks. Eur. Phys. J. B 38:163–168.
Bascompte, J. and P. Jordano. 2007. Plant-animal mutualistic networks: the architecture of biodiversity. Annu. Rev. Ecol. Evol. Syst. 38:567–593.
Bates, D., M. Mächler, B. Bolker and S. Walker. 2015. Fitting linear mixed-effects models using lme4 67. J. Stat. Softw. 67(1):1–48.
Bibby, C., M. Jones and S. Marsden. 1998. Expedition Field Techniques Bird Surveys. Expedition advisory centre of the Royal Geographical Society, London.
Buckton, S.E.B. 2001. Threatened Birds of the World. Birdlife International (2000). Barcelona and Cambridge, UK: Lynx Edicions and BirdLife International. Page Bird Conservation International. Cambridge University Press. ??
Ceballos, G., and P.R. Ehrlich. 2002. Mammal population losses and the extiction crisis. Science 296:904–907.
Chacoff, N.P., D.P. Vázquez, S.B. Lomáscolo, E.L. Stevani, J. Dorado and B. Padrón. 2012. Evaluating sampling completeness in a desert plant-pollinator network. J. Anim. Ecol. 81:190–200.
Chao, A., R.K. Colwell, C.W. Lin and N.J. Gotelli. 2009. Sufficient sampling for asymptotic minimum species richness estimators. Ecology 90:1125–1133.
Christiansen, M.B. and E. Pitter. 1997. Species loss in a forest bird community near Lagoa Santa in southeastern Brazil. Biol. Conserv. 80:23–32.
Colorado, G. de J. 2013. Landbird monitoring program at Tulenapa research station, Carepa Municipality, Northwestern Colombia. The Nature Conservancy.
Colwell, R.K. 2013. EstimateS: Biodiversity Estimation of species richness and shared species from samples. Version 9.1.0. published at: purl.oclc.org/estimates.
Dehling, D.M., P. Jordano, H.M. Schaefer, K. Böhning-Gaese and M. Schleuning. 2016. Morphology predicts species’ functional roles and their degree of specialization in plant–frugivore interactions. P. R. Soc. B: Biological Sciences 283:20152444.
Dehling, D.M., T. Töpfer, H.M. Schaefer, P. Jordano, K. Böhning-Gaese and M. Schleuning. 2014. Functional relationships beyond species richness patterns: Trait matching in plant-bird mutualisms across scales. Global Ecol. Biogeogr. 23:1085–1093.
Dirección de Regionalización Universidad de Antioquia. 2011. Propuesta académica para la creación del centro de estudios biológicos Tulenapa, Carepa, Antioquia.
Dirzo, R., H.S. Young, M. Galetti, G. Ceballos, N.J.B. Isaac and B. Collen. 2014. Defaunation in the Anthropocene. Science 345:401–406.
Donatti, C.I., P.R. Guimarães, M. Galetti, M.A. Pizo, F.M.D. Marquitti and R. Dirzo. 2011. Analysis of a hyper-diverse seed dispersal network: Modularity and underlying mechanisms. Ecol. Lett. 14:773–781.
Donoso, I., D. García, D. Martínez, J. M. Tylianakis and D.B. Stouffer. 2017a. Complementary effects of species abundances and ecological neighborhood on the occurrence of fruit-frugivore interactions. Front. Ecol. Evol. 5:133.
Donoso, I., M. Schleuning, D. García and J. Fründ. 2017b. Defaunation effects on plant recruitment depend on size matching and size trade-offs in seed-dispersal networks. P. R. Soc. B. 284:20162664.
Dormann, C. F., J. Fruend, B. Gruber, M. Devoto, J. Iriondo, R. Strauss and D. Vazquez. 2017. Package “barpartite.” online PDF.
Emer, C., M. Galetti, M. A. Pizo, P. R. J. Guimarães, S. Moraes, A. Piratelli and P. Jordano. 2018. Seed-dispersal interactions in fragmented landscapes – a metanetwork approach. Ecol. Lett. 21: 484–493.
Escobar-Cardona, O. and H. Alvarez-Lopez. 1966. Estudio ecologico prelimirar del parque nacional del río León-Antioquia. Universidad Nacional de Colombia Sede Medellín.
Escribano-Avila, G., C. Lara-romero, R. Heleno, and A. Traveset. 2018. Tropical seed dispersal networks: emerging patterns, biases, and keystone species traits. In: Rico-Gray, V. and W. Dáttilo (eds.), Ecological Networks in the Tropics. Springer, Cham. pp. 93–110.
Estrada, E. 2007. Characterization of topological keystone species. Local, global and “meso-scale” centralities in food webs. Ecol Complex. 4:48–57.
Etter, A., C. McAlpine., K. Wilson., S. Phinn and H. Possingham. 2006. Regional patterns of agricultural land use and deforestation in Colombia. Agr. Ecosyst. Environ. 114: 369–386.
Feeley K.J. and J.W. Terborgh. 2008. Direct vs. indirect effects of habitat reduction on the loss of avian species from tropical forest fragments. Anim. Conserv. 11: 353–360.
Fox, J. 2015. Applied Regression Analysis and Generalized Linear Models. SAGE Publications, USA.
Gard, T.C. 1984. Persistence in food webs. In: S. Levin and T. Hallam (eds.), Mathematical Ecology. Springer, Berlin. pp. 208–219.
Henle, K., K.F. Davies, M. Kleyer, C. Margules and J. Settele. 2004. Predictors of species sensitivity to fragmentation. Biodivers. Conserv. 13:207–251.
Howe, H.F. and J. Smallwood. 1982. Ecology of seed dispersal. Annu. Rev. Ecol. Syst. 13:201–228.
Jordán, F., W. Liu, A. J. Davis, J. Memmott, F. Jordan, W. Liu and A. J. Davis. 2006. Topological keystone species : measures of positional importance in food webs. Oikos 112:535–546.
Jordano, P. 2000. Fruits and frugivory. In: M. Fenner (ed.), Seeds: The Ecology of Regeneration in Plant Communities. 2nd edition. CABI Publ., Wallingford. pp. 125–165.
Jordano, P. 2016. Sampling networks of ecological interactions. Funct. Ecol. 30:1883–1893.
Jordano, P., D. Vazquez and J. Bascompte. 2009. Redes complejas de interacciones mutualistas planta-animal. In: Medel, R, Aizen, M. A. and R. Zamora (eds.), Ecología y evolucion de interacciones planta-animal. Editorial Universitaria, Santiago de Chile. pp. 17–41.
Karr, J.R. 1976. Seasonality, resource availability , and community diversity in tropical bird communities. Am. Nat. 110:973–994.
Kattan, G. H., H. Alvarez-Lopez and M. Giraldo. 1994. Forest fragmentation and bird extinctions. San Antonio eight years later. Conserv. Biol. 8:138–146.
Kays, R., P. A. Jansen, E. M. H. Knecht, R. Vohwinkel and M. Wikelski. 2011. The effect of feeding time on dispersal of Virola seeds by toucans determined from GPS tracking and accelerometers. Acta Oecol. 37:625–631.
Markl, J.S., M. Schleuning, P.M. Forget, P. Jordano, J.E. Lambert, A. Traveset, S. J. Wright and K. Böhning-Gaese. 2012. Metaanalysis of the effects of human disturbance on seed dispersal by animals. Conserv. Biol. 26:1072–1081.
Martín González, A.M., B. Dalsgaard and J.M. Olesen. 2010. Centrality measures and the importance of generalist species in pollination networks. Ecol Complex. 7:36–43.
Mello, M.A.R., F.A. Rodrigues, L. da F. Costa, W.D. Kissling, Ç. H. Şekercioğlu, F.M.D. Marquitti and E.K.V. Kalko. 2014. Keystone species in seed dispersal networks are mainly determined by dietary specialization. Oikos 124:1031–1039.
Mueller, T, J. Lenz, T. Caprano, W. Fiedler and K. Böhning-Gaese. 2014. Large frugivorous birds facilitate functional connectivity of fragmented landscapes. J. Appl. Ecol. 51:684–692.
Muñoz, M.C, H.M. Schaefer, K. Böhning-Gaese and M. Schleuning. 2016. Importance of animal and plant traits for fruit removal and seedling recruitment in a tropical forest. Oikos 126:823–832.
Newman, M.E.J. 2003. The structure and function of complex networks. Soc. Ins. Appl. Math. 45(2):167–256.
Olesen, J.M., J. Bascompte, Y.L. Dupont, H. Elberling, C. Rasmussen and P. Jordano. 2011. Missing and forbidden links in mutualistic networks. P. R. Soc. B- Biol. Sci. 278:725–732.
Palacio, R.D., C. Valderrama-Ardila, and G.H. Kattan. 2016. Generalist species have a central role in a highly diverse plant – frugivore network. Biotropica 43:349–355.
Peres, C. and E. Palacios. 2007. Basin wide effects of game harvest on vertebrate population densities in amazonian forests: implications for animal mediated seed dispersal. Biotropica 39:304–315.
Pimm, S., P. Raven, A. Peterson, Ç.H. Şekercioğlu and PR. Ehrlich. 2006. Human impacts on the rates of recent, present, and future bird extinctions. P. Natl. Acad. Sci. USA 103:10941–10946.
R Develoment Core Team. 2017. R: The R Project for Statistical Computing.
Redford, K.H. 1992. The Empty Forest. BioScience 42:412–422.
Remsen, J.V.J., CD. Cadena, S. Claramunt, A. Jaramillo, J.F. Pachecho, J. Pérez-Emán, M.B. Robbins, F.G. Stiles, D.F. Stotz and K.J. Zimmer. 2018. South American Classification Committee. http://www.museum.lsu.edu/~Remsen/SACCBaseline.htm.
Renjifo, L.M. 1999. Composition changes in a subandean avifauna after long-term forest fragmentation. Conserv. Biol. 13:1124–1139.
Saavedra, S., D.B. Stouffer, B. Uzzi and J. Bascompte. 2011. Strong contributors to network persistence are the most vulnerable to extinction. Nature 478:233–235.
Sanchez-Cuervo, A.M., and T.M. Aide. 2013. Identifying hotspots of deforestation and reforestation in Colombia (2001–2010): implications for protected areas. Ecosphere 4(11): 1–21.
Sarmento, R., C.P. Alves-Costa, A. Ayub, and M.A.R. Mello. 2014. Partitioning of seed dispersal services between birds and bats in a fragment of the Brazilian Atlantic Forest. Zoologia-Curitiba 31:245–255.
Sazima, C., P.R. Guimarães, S.F. dos Reis, and I. Sazima. 2010. What makes a species central in a cleaning mutualism network? Oikos 119:1319–1325.
Sebastián-González, E. 2017. Drivers of species’ role in avian seed-dispersal mutualistic networks. J. Anim. Ecol. 86:878–887.
Tylianakis, J.M., E. Laliberté, A. Nielsen and J. Bascompte. 2010. Conservation of species interaction networks. Biol. Conserv. 143:2270–2279.
Vázquez, D.P., C.J. Melián, N.M. Williams, N. Blüthgen, B.R. Krasnov and R. Poulin. 2007. Species abundance and asymmetric interaction strength in ecological networks. Oikos 116:1120–1127.
Vidal, M.M., E. Hasui, M., Pizo, J.Y. Tamashiro, W.R. Silva and P. R. Guimarães. 2014. Frugivores at higher risk of extinction are the key elements of a mutualistic network. Ecology 95:3440–3447.
Vidal, M.M., M.M. Pires and P.R. Guimarães, Jr. 2013. Large vertebrates as the missing components of seed-dispersal networks. Biol. Conserv. 163:42–48.
Willis, E.O. 1979. The Composition of avian communities in remanescent woodlots in Southern Brazil. Pap. Avulsos de Zool. (São Paulo) 33(1):1–26.
Wilman, H., J. Belmaker, J. Simpson, C. de la Rosa, M.M. Rivadeneira, and W. Jetz. 2014. EltonTraits 1.0: Species-level foraging attributes of the world’s birds and mammals. Ecology 95:2027.
Acknowledgements
SMA was supported by the Alejandro Ángel Escobar Foundation through the Colombia Biodiversa Grant. JFAQ was supported by a National Doctoral scholarship from COLCIENCIAS (647, 2015-II). We also would like to thank IDEA WILD for the support with equipment for field sampling. We are grateful with the herbarium at the Universidad de Antioquia (HUA) for kindly providing the data for the plant plots and with the Sede de Estudios Ecol-gicos y Agroambientales Tulenapa administration for logistical support. We thank the students and colleagues who helped us during field sampling and to M. C. Vargas, A. Idárraga and S. Murillo Serna for the help with botanical identifications. We appreciate the contributions from C. López Gallego, J. Gastón Zamora, the Vertebrate Ecology and Evolution Research Group at the Universidad de Antioquia, two anonymous reviewers and the editor that helped us improve this manuscript.
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Montoya-Arango, S., Acevedo-Quintero, J.F. & Parra, J.L. Abundance and size of birds determine the position of the species in plant-frugivore interaction networks in fragmented forests. COMMUNITY ECOLOGY 20, 75–82 (2019). https://doi.org/10.1556/168.2019.20.1.8
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DOI: https://doi.org/10.1556/168.2019.20.1.8