Skip to main content
SpringerLink
Log in

Specialization increases in a frugivorous bird–plant network from an isolated montane forest remnant

  • Original Article
  • Published:
Community Ecology Aims and scope Submit manuscript

An Editorial Expression of Concern to this article was published on 05 August 2021

This article has been updated

Abstract

The structure of mutualist interactions is still poorly understood in isolated remnants of montane forests. We tried to answer whether a plant–frugivore network from an isolated remnant could maintain its functional structure, despite the absence of certain species and traits. We hypothesized that a network of frugivore birds and plants from an isolated remnant would be less specialized and modular, and would show higher degree of nestedness than one from a continuous forest area. Functionally distinctive species in the networks were also identified based on analyses of the fourth-corner matrices, which cross plant and bird traits weighted by their interaction frequencies. The structure of studied networks showed a high similarity in which most interactions were performed by small generalist bird species on plant species carrying small unprotected fruits. Both networks showed similar levels of niche partitioning, although specialization and modularity increased in the isolated remnant network. Networks also showed a strong correlation between fruit weights and bird masses reflecting the functional distinctiveness of large frugivorous birds and plants with the heaviest fruits. Several large bird species were recorded in the studied networks although they contributed with a low percentage of interactions. Therefore, networks from isolated forest remnants seem resilient to the reduction of species richness due to the persistence of tolerant bird species and plant species carrying small fruits.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

Change history

Abbreviations

IBA:

Important bird area

WNOD:

Weighted nestedness metric based on overlap and decreasing fill

References

  • Albrecht, J., Berens, D. G., Blüthgen, N., Jaroszewicz, B., Selva, N., & Farwig, N. (2013). Logging and forest edges reduce redundancy in plant–frugivore networks in an old-growth European forest. Journal of Ecology, 101, 990–999.

    Google Scholar 

  • Almeida-Neto, M., & Ulrich, W. (2011). A straightforward computational approach for measuring nestedness using quantitative matrices. Environmental Modelling and Software, 26, 173–178.

    Google Scholar 

  • Bascompte, J., & Jordano, P. (2007). Plant-animal mutualistic networks: The architecture of biodiversity. Annual Review of Ecology Evolution and Systematics, 38, 567–593.

    Google Scholar 

  • Bender, I. M. A., Kissling, W. D., Böhning-Gaese, K., Hensen, I., Kühn, I., Wiegand, T., et al. (2017). Functionally specialised birds respond flexibly to seasonal changes in fruit availability. Journal of Animal Ecology, 86, 800–811.

    Google Scholar 

  • Blüthgen, N. (2010). Why network analysis is often disconnected from community ecology: A critique and an ecologist’s guide. Basic and Applied Ecology, 11, 185–195.

    Google Scholar 

  • Blüthgen, N., & Klein, A. M. (2011). Functional complementarity and specialisation: The role of biodiversity in plant-pollinator interactions. Basic and Applied Ecology, 12, 282–291.

    Google Scholar 

  • Blüthgen, N., Menzel, F., & Blüthgen, N. (2006). Measuring specialization in species interaction networks. BMC Ecology, 6, 9.

    PubMed  PubMed Central  Google Scholar 

  • Boyle, W. A. (2010). Does food abundance explain altitudinal migration in a tropical frugivorous bird? Canadian Journal of Zoology, 88, 204–213.

    Google Scholar 

  • Buitrón-Jurado, G. (2012). Diversidad de aves frugívoras y árboles, redes de interacción e identificación de árboles magnetos en dos bosques nublados de Venezuela con distintas condiciones de fragmentación. MSc thesis, Inst. Venezolano de Investigaciones Científicas, San Antonio, Venezuela.

  • Buitrón-Jurado, G., & Ramírez, N. (2014). Dispersal spectra, diaspore size and the importance of endozoochory in the equatorial Andean montane forests. Flora, 209, 299–311.

    Google Scholar 

  • Cardozo, A. (1999). Comparacion floristica y estructural entre la selva nublada baja y selva nublada superior del Parque Nacional Henri Pittier, Edo. Aragua y Carabobo. PhD.Univ. Central de Venezuela, Caracas, Venezuela.

  • Carlo, T. A., Collazo, J. A., & Groom, M. J. (2003). Avian fruit preferences across a Puerto Rican forested landscape: Pattern consistency and implications for seed removal. Oecologia, 134, 119–131.

    PubMed  Google Scholar 

  • Chapman, H., Cordeiro, N. J., Dutton, P., Wenny, D., Kitamura, S., Kaplin, B., et al. (2016). Seed-dispersal ecology of tropical montane forests. Journal of Tropical Ecology, 32, 1–18.

    Google Scholar 

  • Chaves-Campos, J. (2004). Elevational movements of large frugivorous birds and temporal variation in abundance of fruits along an elevational gradient. Ornitologia Neotropical, 15, 433–445.

    Google Scholar 

  • Cramer, J. M., Mesquita, R. C. G., & Williamson, G. B. (2007). Forest fragmentation differentially affects seed dispersal of large and small-seeded tropical trees. Biological Conservation, 137, 415–423.

    Google Scholar 

  • DeFries, R., Hansen, A., Newton, A. C., & Hansen, M. C. (2005). Increasing isolation of protected areas in tropical forests over the past twenty years. Ecological Applications, 15, 19–26.

    Google Scholar 

  • Dehling, D. M., Jordano, P., Schaefer, H. M., Böhning-Gaese, K., & Scheuling, M. (2016). Morphology predicts species’ functional roles and their degree of specialisation in plant–frugivore interactions. Proceedings of the Royal Society B: Biological Sciences, 283, 20152444.

    PubMed  PubMed Central  Google Scholar 

  • Dehling, D. M., Töpfer, T., Schaefer, H. M., Jordano, P., Böhning-Gaese, K., & Schleuning, M. (2014). Functional relationships beyond species richness patterns: Trait matching in plant–bird mutualisms across scales. Global Ecology and Biogeography, 23, 1085–1093.

    Google Scholar 

  • Dodson, C. H., & Gentry, A. H. (1991). Biological extinction in western Ecuador. Annals of the Missouri Botanical Garden, 78, 273.

    Google Scholar 

  • 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.

    PubMed  Google Scholar 

  • Dormann, C. F., Frund, J., Bluthgen, N., & Gruber, B. (2009). Indices, graphs and null models: Analyzing bipartite ecological networks. The Open Ecology Journal, 2, 7–24.

    Google Scholar 

  • Dormann, C. F., Gruber, B., & Fründ, J. (2008). Introducing the bipartite package: Analysing ecological networks. R News., 8, 8–11.

    Google Scholar 

  • Dormann, C. F., & Strauss, R. (2014). A method for detecting modules in quantitative bipartite networks. Methods in Ecology and Evolution, 5, 90–98.

    Google Scholar 

  • Dray, S., Choler, P., Dolédec, S., Peres-Neto, P. R., Thuiller, W., Pavoine, S., et al. (2014). Combining the fourth-corner and the RLQ methods for assessing trait responses to environmental variation. Ecology, 95, 14–21.

    PubMed  Google Scholar 

  • Dray, S., & Dufour, A.-B. (2007). The ade4 package: Implementing the duality diagram for ecologists. Journal of Statistical Software, 22, 1–20.

    Google Scholar 

  • Duivenvoorden, J. F., & Cuello, N. L. (2012). Functional trait state diversity of Andean forests in Venezuela changes with altitude. Journal of Vegetation Science, 23, 1105–1113.

    Google Scholar 

  • Emer, C., Galetti, M., Pizo, M. A., Guimarães, P. R., Moraes, S., Piratelli, A., et al. (2018). Seed-dispersal interactions in fragmented landscapes—A metanetwork approach. Ecology Letters, 21, 484–493.

    PubMed  Google Scholar 

  • Fahrig, L. (2003). Effects of habitat fragmentation on biodiversity. Annual Review of Ecology Evolution and Systematics, 34, 487–515.

    Google Scholar 

  • Fauth, A. J. E., Bernardo, J., Camara, M., Resetarits, W. J., & Van Buskirk, J. (1996). Simplifying the Jargon of community ecology: A conceptual approach. American Naturalist, 147, 282–286.

    Google Scholar 

  • Ferry-Graham, L. A., Bolnick, D. I., Wainwright, P. C., & Avenue, O. S. (2002). Using functional morphology to examine the ecology and evolution of specialization. Integrative and Comparative Biology, 42, 265–277.

    PubMed  Google Scholar 

  • Fortuna, M. A., Stouffer, D. B., Olesen, J. M., Jordano, P., Mouillot, D., Krasnov, B. R., et al. (2010). Nestedness versus modularity in ecological networks: Two sides of the same coin? Journal of Animal Ecology, 79, 811–817.

    Google Scholar 

  • Galetti, M., & Pizo, M. A. (1996). Fruit eating by birds in a forest fragment in southeastern Brazil. Revista Brasileira de Ornitologia, 4, 71–79.

    Google Scholar 

  • García, D., Martínez, D., Stouffer, D. B., & Tylianakis, J. M. (2014). Exotic birds increase generalization and compensate for native bird decline in plant–frugivore assemblages. Journal of Animal Ecology, 83, 1441–1450.

    Google Scholar 

  • Gotelli, N. J., & Colwell, R. K. (2001). Quantifying biodiversity: Procedures and pitfalls in the measurement and comparison of species richness. Ecology Letters, 4, 379–391.

    Google Scholar 

  • Hagen, M., Kissling, W. D., Rasmussen, C., Aguiar, M. A. M., Brown, L., Carstensen, D. W., et al. (2012). Biodiversity, species interactions and ecological networks in a fragmented world. Advances in Ecological Research, 46, 89–120.

    Google Scholar 

  • Hamann, A., & Curio, E. (1999). Interactions among frugivores and fleshy fruit trees in a Philippine submontane rainforest. Conservation Biology, 13, 766–773.

    Google Scholar 

  • Hilty, S. L. (2003). Birds of Venezuela. New Jersey: Princeton University Press.

    Google Scholar 

  • Howe, H. F. (1984). Implications of seed dispersal by animals for tropical reserve management. Biological Conservation, 30, 261–281.

    Google Scholar 

  • Huber, O. (1986). Las selvas nubladas de Rancho Grande: Observaciones sobre su fisionomia, estructura y fenología. In O. Huber (Ed.), La Selva Nublada Rancho Grande, Parque Nacional “Henri Pittier” (pp. 131–170). Caracas: Fondo Editorial Acta Científica Venezolana.

    Google Scholar 

  • Laurance, W. F., Nascimento, H. E. M., Laurance, S. G., Andrade, A., Ewers, R. M., Harms, K. E., et al. (2007). Habitat fragmentation, variable edge effects, and the landscape-divergence hypothesis. PLoS ONE, 2, e1017.

    PubMed  PubMed Central  Google Scholar 

  • Laurance, W. F., Nascimento, H. E. M., Laurance, S. G., Andrade, A., Ribeiro, J. E. L. S., Giraldo, J. P., et al. (2006). Rapid decay of tree-community composition in Amazonian forest fragments. Proceedings of the National Academy of Sciences of the United States of America, 103, 19010–19014.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Leck, C. F. (1979). Avian extinctions in an isolated tropical wet-forest preserve, Ecuador. Auk, 96, 343–352.

    Google Scholar 

  • Lentino, M., & Esclasans, D. (2009). Important bird areas: Venezuela. In C. Devenish, D. F. Díaz, R. P. Clay, I. Davidson, & I. Yépez Zábala (Eds.), Important bird areas America—Priority sites for biodiversity conservation (pp. 393–402). Quito: Birdlife International.

    Google Scholar 

  • Lord, J. (2004). Frugivore gape size and the evolution of fruit size and shape in southern hemisphere floras. Austral Ecology, 29, 430–436.

    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.

    Google Scholar 

  • Mazer, S. J., & Wheelwright, N. T. (1993). Fruit size and shape: Allometry at different taxonomic levels in bird-dispersed plants. Evolutionary Ecology, 7, 556–575.

    Google Scholar 

  • McKinney, M. L., & Lockwood, J. L. (1999). Biotic homogenization: A few winners replacing many losers in the next mass extinction. Trends in Ecology & Evolution, 14, 450–453.

    CAS  Google 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 

  • Moran, C., & Catterall, C. P. (2010). Can functional traits predict ecological interactions? A case study using rain forest frugivores and plants in Australia. Biotropica, 42, 318–326.

    Google Scholar 

  • Muñoz, M. C., Schaefer, H. M., Böhning-Gaese, K., & Schleuning, M. (2017). Importance of animal and plant traits for fruit removal and seedling recruitment in a tropical forest. Oikos, 126, 823–832.

    Google Scholar 

  • Naoki, K. (2007). Arthropod resource partitioning among omnivorous tanagers Tangara spp. in western Ecuador. Auk, 124, 197–209.

    Google Scholar 

  • Oksanen, J., Blanchet, F. G., Kindt, R., Legendre, P., Minchin, P. R., O’Hara, R. B., Simpson, G. L., Solymos, P., Stevens, M. H. H., & Wagner, H. (2013). Package ‘vegan’. R Packag. ver. 2.0–8. Retrieved June 13, 2014, from https://CRANr-project.org/package=vegan.

  • Olesen, J. M., Bascompte, J., Dupont, Y. L., & Jordano, P. (2007). The modularity of pollination networks. Proceedings of the National Academy of Sciences of the United States of America, 104, 19891–19896.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Olito, C., & Fox, J. W. (2015). Species traits and abundances predict metrics of plant-pollinator network structure, but not pairwise interactions. Oikos, 124, 428–436.

    Google Scholar 

  • Plein, M., Langsfeld, L., Neuschulz, E. L., Schulthei, C., Ingmann, L., Topfer, T., et al. (2013). Constant properties of plant–frugivore networks despite fluctuations in fruit and bird communities in space and time. Ecology, 94, 1296–1306.

    PubMed  Google Scholar 

  • R Core Team. (2017). R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/.

  • Ramos-Robles, M., Andresen, E., & Díaz-Castelazo, C. (2018). Modularity and robustness of a plant–frugivore interaction network in a disturbed tropical forest. Ecoscience, 25, 209–222.

    Google Scholar 

  • Remsen Jr., J. V., Areta, J. I., Cadena, C. D., Claramunt, S., Jaramillo, A., Pacheco, J. F., Pérez-Emán, J., Robbins, M. B., Stiles, F. G., Stotz, D. F., & Zimmer, K. J. (2017). A classification of the bird species of South America. Retrieved August 24, 2017, from http://www.museum.lsu.edu/~Remsen/SACCBaseline.htm.

  • Restrepo, C., Sargent, S., Levey, D. J., & Watson, D. M. (2002). The role of vertebrates in diversification of New World Mistletoes. In D. J. Levey, W. R. Silva, & M. Galetti (Eds.), Seed dispersal and frugivory: Ecology, evolution and conservation (pp. 83–98). Wallingford: CABI.

    Google Scholar 

  • Saavedra, F., Hensen, I., Beck, S. G., Böhning-Gaese, K., Lippok, D., Töpfer, T., et al. (2014). Functional importance of avian seed dispersers changes in response to human-induced forest edges in tropical seed-dispersal networks. Oecologia, 176, 837–848.

    PubMed  Google Scholar 

  • Schleuning, M., Böhning-Gaese, K., Dehling, D. M., & Burns, K. C. (2014a). At a loss for birds: Insularity increases asymmetry in seed-dispersal networks. Global Ecology and Biogeography, 23, 385–394.

    Google Scholar 

  • Schleuning, M., Fründ, J., Klein, A. M., Abrahamczyk, S., Alarcón, R., Albrecht, M., et al. (2012). Specialization of mutualistic interaction networks decreases toward tropical latitudes. Current Biology, 22, 1925–1931.

    CAS  PubMed  Google Scholar 

  • Schleuning, M., Ingmann, L., Strauß, R., Fritz, S. A., Dalsgaard, B., Dehling, M. D., et al. (2014b). Ecological, historical and evolutionary determinants of modularity in weighted seed-dispersal networks. Ecology Letters, 17, 454–463.

    PubMed  Google Scholar 

  • Sebastián-González, E., Dalsgaard, B., Sandel, B., & Guimaraes, P. R. (2015). Macroecological trends in nestedness and modularity of seed-dispersal networks: Human impact matters. Global Ecology and Biogeography, 24, 293–303.

    Google Scholar 

  • Sethi, P., & Howe, H. F. (2009). Recruitment of hornbill-dispersed trees in hunted and logged forests of the Indian Eastern Himalaya. Conservation Biology, 23, 710–718.

    PubMed  Google Scholar 

  • Slocum, M. G. (2001). How tree species differ as recruitment foci in a tropical pasture. Ecology, 82, 2547–2559.

    Google Scholar 

  • Stevenson, P. R., Link, A., González-Caro, S., & Torres-Jiménez, M. F. (2015). Frugivory in canopy plants in a western Amazonian forest: Dispersal systems, phylogenetic ensembles and keystone plants. PLoS ONE, 10, 1–22.

    Google Scholar 

  • Steyermark, J. A., & Huber, O. (1978). Flora del Ávila. Caracas: Sociedad Venezolana de Ciencias Naturales.

    Google Scholar 

  • Stoner, K. E., Vulinec, K., Wright, S. J., & Peres, C. A. (2007). Hunting and plant community dynamics in tropical forests: A synthesis and future directions. Biotropica, 39, 385–392.

    Google Scholar 

  • Turner, I. M. (1996). Species loss in fragments of tropical rain forest: A review of the evidence. Journal of Applied Ecology, 33, 200–209.

    Google Scholar 

  • Vázquez, D. P., Bluthgen, N., Cagnolo, L., & Chacoff, N. P. (2009). Uniting pattern and process in plant-animal mutualistic networks: A review. Annals of Botany, 103, 1445–1457.

    PubMed  PubMed Central  Google Scholar 

  • Vázquez, D. P., Morris, W. F., & Jordano, P. (2005). Interaction frequency as a surrogate for the total effect of animal mutualists on plants. Ecology Letters, 8, 1088–1094.

    Google Scholar 

  • Vidal, M. M., Hasui, E., Pizo, M. A., Tamashiro, J. Y., Silva, W. R., & Guimarães, P. R. (2014). Frugivores at higher risk of extinction are the key elements of a mutualistic network. Ecology, 95, 3440–3447.

    Google Scholar 

  • Violle, C., Thuiller, W., Mouquet, N., Munoz, F., Kraft, N. J., Cadotte, M. W., et al. (2017). Functional rarity: The ecology of outliers. Trends in Ecology & Evolution, 32, 356–367.

    Google Scholar 

  • 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.

    PubMed  PubMed Central  Google Scholar 

  • Wheelwright, N. T., Haber, W. A., Murray, K. G., & Guindon, C. (1984). Tropical fruit-eating birds and their food plants: A survey of a Costa Rican lower montane forest. Biotropica, 16, 173–192.

    Google Scholar 

Download references

Acknowledgements

We would like to thank the Regional Direction of INPARQUES Lara and M. Mendez for permission to work in Yacambú National Park. We are grateful also to L. Rodríguez, S. Peréz-Cortés and J. Grande of the Venezuelan National Herbarium (VEN) and A. Fernández and R. Gonto (IVIC) for helping us with plant species identification. To M. Lentino and M. Martínez for kindly permitted our access to Phelps Ornithological Collection. Fieldwork assistance was provided by L. Alvarado, C. Azpurúa, V. Morón, L. Cordero and A. Arias. This study has benefited of comments by J. Pérez-Emán, A. Mata and J. Vizentin-Bugoni, and it was financially supported by the IVIC, IDEAWILD and The Rufford Small Grant Foundation (No. 9163-1). This research was authorized by the Ministerio del Poder Popular para el Ambiente de Venezuela (Permit No. I-176).

Author information

Authors and Affiliations

  1. Laboratorio de Biología de Organismos, Centro de Ecología, Instituto Venezolano de Investigaciones Científicas, Km 11 Carretera Panamericana, Apartado 2032, Caracas, 1020-A, Miranda, Venezuela

    Galo Buitrón-Jurado & Virginia Sanz

Authors
  1. Galo Buitrón-Jurado
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Virginia Sanz
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

GBJ and VS conceived and designed the study, GBJ conducted fieldwork, and GBJ and VS analyzed the data and wrote the manuscript.

Corresponding author

Correspondence to Galo Buitrón-Jurado.

Ethics declarations

Ethical approval

All applicable institutional and/or national guidelines for the care and use of animals were followed.

Additional information

APG IV (Tropicos.org 2019) for plants and Remsen et al. (2017) for birds.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 372 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Buitrón-Jurado, G., Sanz, V. Specialization increases in a frugivorous bird–plant network from an isolated montane forest remnant. COMMUNITY ECOLOGY 22, 261–274 (2021). https://doi.org/10.1007/s42974-020-00010-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s42974-020-00010-x

Keywords

Search

Navigation