Volume 13 Issue 1
Mar.  2022
Turn off MathJax
Article Contents
Omar A. Hernández-Dávila, Javier Laborde, Vinicio J. Sosa, Cecilia Díaz-Castelazo. 2022: Interaction network between frugivorous birds and zoochorous plants in cloud forest riparian strips immersed in anthropic landscapes. Avian Research, 13(1): 100046. doi: 10.1016/j.avrs.2022.100046
Citation: Omar A. Hernández-Dávila, Javier Laborde, Vinicio J. Sosa, Cecilia Díaz-Castelazo. 2022: Interaction network between frugivorous birds and zoochorous plants in cloud forest riparian strips immersed in anthropic landscapes. Avian Research, 13(1): 100046. doi: 10.1016/j.avrs.2022.100046

Interaction network between frugivorous birds and zoochorous plants in cloud forest riparian strips immersed in anthropic landscapes

doi: 10.1016/j.avrs.2022.100046
More Information
  • Corresponding author: E-mail address: javier.laborde@inecol.mx (J. Laborde); E-mail address: vinicio.sosa@inecol.mx (V.J. Sosa)
  • Received Date: 24 Jul 2021
  • Accepted Date: 22 Jun 2022
  • Available Online: 11 Oct 2022
  • Publish Date: 30 Jun 2022
  • Worldwide, tropical montane cloud forest is one of the most important and biodiverse ecosystems; however, it is also one of those most threatened by anthropic activities. These activities lead to a fragmented, deforested landscape with narrow riparian forest strips immersed in an agricultural matrix dominated by pastures. Here, we characterize the interaction network between frugivorous birds and zoochorous plants in riparian strips of cloud forest in deforested landscapes of Central Veracruz, Mexico. To characterize the network of this mutualistic interaction, we estimated network- and species-level metrics using the Bipartite R package. Nestedness, modularity and robustness were used to describe network structure. Centrality measures of degree, closeness, betweenness centrality and their relative contribution to nestedness were used to determine the importance of each bird/plant species to the network's structure. This interaction network has 24 species of birds and 30 species of plants, with low connectance (0.11), low nestedness (11.53), and intermediate but not significant modularity (0.49). The bird species most important to network stability were Chlorospingus flavopectus, Myadestes occidentalis, and Catharus mexicanus. The most important plants were Conostegia xalapensis, C. arborea, and Rubus ulmifolius. Network robustness varied from 0.36 to 0.86 and its stability is compromised when species of birds or plants with the highest values of centrality are removed, with plant removal more detrimental. Riparian strips of cloud forest crossing deforested areas maintain a relatively rich set of birds that disperse the seeds of many forest plants, thus they are crucial to the preservation of this mutualistic network in anthropic landscapes. Network stability is severely undermined by the loss of any of the few species — whether birds or plants — with high centrality values. The most important plants for this stability are pioneer tree and shrub species that provide food for several bird species, and they are also crucial to cloud forest regeneration. A worrisome finding is that some of the bird species most important to network stability are also among the most sought-after as ornamental birds by illegal collectors in the region.


  • loading
  • Aguilar-Rodríguez, S.H., 1992. El comercio de aves silvestres vivas en Xalapa, Veracruz, México. La Ciencia y el Hombre 11, 47-60.
    Almeida-Neto, M., Guimarães, P., Guimarães Jr., P.R., Loyola, R.D., Ulrich, W., 2008. A consistent metric for nestedness analysis in ecological systems: reconciling concept and measurement. Oikos 117, 1227-1239. doi: 10.1111/j.0030-1299.2008.16644.x
    Baltazar, H.S., 2014. La importancia de la dispersión de semillas en la recuperación del bosque mesófilo de montaña del centro de Veracruz, México. Master's Thesis. Instituto de Ecología, A. C., Xalapa.
    Barber, M.J., 2007. Modularity and community detection in bipartite networks. Phys. Rev. E 76, 066102. doi: 10.1103/PhysRevE.76.066102
    Bascompte, J., Jordano, P., 2007. Plant-animal mutualistic networks: the architecture of biodiversity. Annu. Rev. Ecol. Evol. Syst. 38, 567-593. doi: 10.1146/annurev.ecolsys.38.091206.095818
    Bascompte, J., Jordano, P., Melián, C.J., Olesen, J.M., 2003. The nested assembly of plantanimal mutualistic networks. Proc. Natl. Acad. Sci. USA 100, 9383-9387. doi: 10.1073/pnas.1633576100
    Bello, C., Galetti, M., Pizo, M.A., Magnago, L.F.S., Rocha, M.F., Lima, R.A.F., et al., 2015. Defaunation affects carbon storage in tropical forests. Sci. Adv. 1, e1501105. doi: 10.1126/sciadv.1501105
    Blüthgen, N., Klein, A.M., 2011. Functional complementarity and specialisation: the role of biodiversity in plant-pollinator interactions. Basic Appl. Ecol. 12, 282-291. doi: 10.1016/j.baae.2010.11.001
    Bruijnzeel, L.A., Scatena, F.N., Hamilton, L.S., 2011. Tropical Montane Cloud Forests: Science for Conservation and Management. Cambridge University Press, Cambridge.
    Burgos, E., Ceva, H., Perazzo, R.P., Devoto, M., Medan, D., Zimmermann, M., et al., 2007. Why nestedness in mutualistic networks? J. Theor. Biol. 249, 307-313. doi: 10.1016/j.jtbi.2007.07.030
    Carrasco-Rueda, F., Loiselle, B.A., 2019. Do riparian forest strips in modified forest landscapes aid in conserving bat diversity? Ecol. Evol. 9, 4192-4209. doi: 10.1002/ece3.5048
    Castaño, J.H., Carranza, J.A., Pérez-Torres, J., 2018. Diet and trophic structure in assemblages of montane frugivorous phyllostomid bats. Acta Oecol. 91, 81-90. doi: 10.1016/j.actao.2018.06.005
    Chesser, R.T., Billerman, S.M., Burns, K.J., Cicero, C., Dunn, J.L., Hernández-Baños, B.E., et al., 2021. Check-list of North American Birds. American Ornithological Society. http://checklist.aou.org/taxa.
    Cruz-Angón, A., Greenberg, R., 2005. Are epiphytes important for birds in coffee plantations? An experimental assessment. J. Appl. Ecol. 42, 150-159. doi: 10.1111/j.1365-2664.2004.00983.x
    Dehling, D.M., 2018. The structure of ecological networks. In: Dáttilo, W., Rico-Gray, V. (Eds. ), Ecological Networks in the Tropics. Springer Nature, Cham, pp. 29-42.
    Delmas, E., Besson, M., Brice, M.H., et al., 2019. Analysing ecological networks of species interactions. Biol. Rev. 94, 16-36. doi: 10.1111/brv.12433
    Dormann, C.F., Gruber, B., Fründ, J., 2008. Introducing the bipartite package: analysing ecological networks. R. News 8, 8-11.
    Emer, C., Jordano, P., Pizo, M.A., Ribeiro, M.C., da Silva, F.R., Galetti, M., 2020. Seed dispersal networks in tropical forest fragments: area effects, remnant species, and interaction diversity. Biotropica 52, 81-89. doi: 10.1111/btp.12738
    Escribano-Avila, G., Lara-Romero, C., Heleno, R., Traveset, A., 2018. Tropical seed dispersal networks: emerging patterns, biases, and keystone species traits. In: Dáttilo, W., Rico-Gray, V. (Eds. ), Ecological Networks in the Tropics. Springer Nature, Cham, pp. 93-110.
    Freeman, L.C., 1977. A set of measures of centrality based on betweenness. Sociometry 40, 35-41. doi: 10.2307/3033543
    Freeman, L.C., 1978. Centrality in social networks conceptual clarification. Soc. Netw. 1, 215-239. doi: 10.1016/0378-8733(78)90021-7
    Galindo-González, J., Guevara, S., Sosa, V.J., 2000. Bat- and bird-generated seed rains at isolated trees in pastures in a tropical rainforest. Conserv. Biol. 14, 11693-11703.
    Gallina, S., González-Romero, A., Manson, R.H., 2008. Mamíferos pequeños y medianos. In: Manson, R.H., Hernández-Ortiz, V., Gallina, S., Mehltreter, K. (Eds. ), Agroecosistemas Cafetaleros de Veracruz. Instituto de Ecología, A. C. (INECOL). e Instituto Nacional de Ecología (INE-SEMARNAT), México, pp. 161-178.
    García, D., 2016. Birds in ecological networks: insights from bird-plant mutualistic interactions. ARDEOLA 63, 151-180. doi: 10.13157/arla.63.1.2016.rp7
    García, D., Zamora, R., Amico, G.C., 2010. Birds as suppliers of seed dispersal in temperate ecosystems: conservation guidelines from real-world landscapes. Conserv. Biol. 24, 1070-1079. doi: 10.1111/j.1523-1739.2009.01440.x
    Gentry, A.H., 1982. Patterns of neotropical plant species diversity. In: Hecht, M.K., Bruce, W., Prance, G.T. (Eds. ), Evolutionary Biology, vol. 15. Springer, New York, pp. 1-84.
    González-Espinosa, M., Meave, J., Lorea-Hernández, F.G., Ibarra-Manríquez, G., Newton, A.C., 2011. The Red List of Mexican Cloud Forest Trees. Fauna and Flora International, Cambridge.
    González-Salazar, C., Martínez-Meyer, E., López-Santiago, G., 2014. A hierarchical classification of trophic guilds for North American birds and mammals. Rev. Mex. Biodivers. 85, 931-941. doi: 10.7550/rmb.38023
    Gorchov, D.L., Cornejo, F., Ascorra, C., Jaramillo, M., 1993. The role of seed dispersal in the natural regeneration of rain forest after strip-cutting in the Peruvian Amazon. Vegetatio 107, 339-349.
    Graham, C., Martínez-Leyva, J.E., Cruz-Paredes, L., 2002. Use of fruiting trees by birds in continuous forest and riparian forest remnants in Los Tuxtlas, Veracruz, Mexico. Biotropica 34, 589-597. doi: 10.1111/j.1744-7429.2002.tb00578.x
    Hagen, M., Kissling, W.D., Rasmussen, C., De Aguiar, M.A.M., Brown, L.E., Carstensen, D.W., et al., 2012. Biodiversity, species interactions and ecological network in a fragmented world. Adv. Ecol. Res. 46, 89-120. doi: 10.1016/B978-0-12-396992-7.00002-2
    Hernández-Dávila, O.A., 2013. Dispersión de semillas por aves en ambientes ribereños y su importancia en la regeneración de bosque mesófilo de montaña en un paisaje fragmentado de Veracruz. Master's Thesis. Instituto de Ecología, A. C., Xalapa.
    Hernández-Dávila, O.A., Galindo-González, J., Castro-Luna, A.A., Sosa, V.J., 2015. Plastic sheets: a new method for collecting faecal samples with seeds dispersed by birds. J. Trop. Ecol. 31, 187-190. doi: 10.1017/S0266467414000716
    Hernández-Dávila, O.A., Laborde, J., Sosa, V.J., Gallardo-Hernández, C., DíazCastelazo, C., 2020. Forested riparian belts as reservoirs of plant species in fragmented landscapes of tropical mountain cloud forest. Bot. Sci. 98, 288-304. doi: 10.17129/botsci.2497
    Hernández-Ladrón De Guevara, I., Rojas-Soto, O.R., López-Barrera, F., Puebla-Olivares, F., Díaz-Castelazo, C., 2012. Dispersión de semillas por aves en un paisaje de bosque mesófilo en el centro de Veracruz, México: su papel en la restauración pasiva. Rev. Chil. Hist. Nat. 85, 89-100. doi: 10.4067/S0716-078X2012000100007
    Hernández-Montero, J.R., Saldaña-Vázquez, R.A., Galindo-González, J., Sosa, V.J., 2015. Bat-fruit interactions are more specialized in shaded-coffee plantations than in tropical mountain cloud forest fragments. PLoS One 10, e0126084. doi: 10.1371/journal.pone.0126084
    Hernández-Pérez, E., García-Franco, J.G., Vázquez, G., Cantellano de Rosas, E., 2022. Cambio de uso de suelo y fragmentación del paisaje en el centro de Veracruz, México (1989-2015). Madera Bosques 28, e2812294. doi: 10.21829/myb.2022.2812294
    Howe, H., Smallwood, J., 1982. Ecology of seed dispersal. Annu. Rev. Ecol. 13, 201-228. doi: 10.1146/annurev.es.13.110182.001221
    Howell, S.N., Webb, S., 1995. A Guide to the Birds of Mexico and Northern Central America. Oxford University Press, Oxford.
    Hsieh, T.C., Ma, K.H., Chao, A., 2016. iNEXT: an R package for rarefaction and extrapolation of species diversity (Hill numbers). Methods Ecol. Evol. 7, 1451-1456. doi: 10.1111/2041-210X.12613
    Ibarra-Manríquez, G., Martínez-Morales, M., Cornejo-Tenorio, G., 2015. Frutos y Semillas del Bosque Tropical Perennifolio: Región de Los Tuxtlas, Veracruz. CONABIO, México.
    Jordano, P., 1987. Patterns of mutualistic interactions in pollination and seed dispersal: connectance, dependence asymmetries, and coevolution. Am. Nat. 129, 657-677. doi: 10.1086/284665
    Jordano, P., 2000. Fruits and frugivory. In: Fenner, M. (Ed. ), Seeds: the Ecology of Regeneration in Plant Communities, second ed. CABI Publ., Wallingford, pp. 125-166.
    Jordano, P., Vázquez, D., Bascompte, J., 2009. Redes complejas de interacciones mutualistas planta-animal. In: Medel, R., Aizen, M.A., Zamora, R. (Eds. ), Ecología y Evolución de Interacciones Planta-Animal. Editorial Universitaria S. A., Santiago de Chile, pp. 17-41.
    Jordano, P., Forget, P.M., Lambert, J.E., Böhning-Gaese, K., Traveset, A., Wright, S.J., 2010. Frugivores and seed dispersal: mechanisms and consequences for biodiversity of a key ecological interaction. Biol. Lett. 7, 321-323.
    Karger, D.N., Kessler, M., Lehnert, M., Jetz, W., 2021. Limited protection and ongoing loss of tropical cloud forest biodiversity and ecosystems worldwide. Nat. Ecol. Evol. 5, 854-862. doi: 10.1038/s41559-021-01450-y
    Laurance, W.F., Camargo, J.L.C., Luizão, R.C.C., Laurance, S.G., Pimm, S.L., Bruna, E.M., et al., 2011. The fate of Amazonian forest fragments: a 32-year investigation. Biol. Conserv. 144, 56-67. doi: 10.1016/j.biocon.2010.09.021
    Lees, A.C., Peres, C.A., 2008. Conservation value of remnant riparian forest corridors of varying quality for Amazonian birds and mammals. Conserv. Biol. 22, 439-449. doi: 10.1111/j.1523-1739.2007.00870.x
    Martín-González, A.M., Dalsgaard, B., Olesen, J.M., 2010. Centrality measures and the importance of generalist species in pollination networks. Ecol. Complex. 7, 36-43. doi: 10.1016/j.ecocom.2009.03.008
    Mello, M.A., Rodrigues, F.A., da Fontoura Costa, L., Kissling, W.D., Şekercioğlu, Ç. H., Marquitti, F.M.D., et al., 2014. Keystone species in seed dispersal networks are mainly determined by dietary specialization. Oikos 124, 1031-1039. doi: 10.1590/S1517-83822014000300036
    Memmott, J., Waser, N.M., Price, M.V., 2004. Tolerance of pollination networks to species extinctions. Proc. R. Soc. B. 271, 2605-2611. doi: 10.1098/rspb.2004.2909
    Messeder, J.V.S., Guerra, T.J., Dáttilo, W., Silveira, F.A.O., 2020. Searching for keystone plant resources in fruit-frugivore interaction networks across the Neotropics. Biotropica 52, 857-870. doi: 10.1111/btp.12804
    Messeder, J.V.S., Silveira, F.A.O., Cornelissen, T.G., Fuzessy, L.F., Guerra, T.J., 2021. Frugivory and seed dispersal in a hyperdiverse plant clade and its role as a keystone resource for the Neotropical fauna. Ann. Bot. 127, 577-595. doi: 10.1093/aob/mcaa189
    Missouri Botanical Garden, 2020. Tropicos v3.3.2. http://www.tropicos.org. (Accessed 15 April 2020).
    Morán-López, T., Espíndola, W.D., Vizzachero, B.S., Fontanella, A., Salinas, L., Arana, C., et al., 2020. Can network metrics predict vulnerability and species roles in birddispersed plant communities? Not without behaviour. Ecol. Lett. 23, 348-358. doi: 10.1111/ele.13439
    Muñiz-Castro, M.A., Williams-Linera, G., Martínez-Ramos, M., 2012. Dispersal mode, shade tolerance, and phytogeographical affinity of tree species during secondary succession in tropical montane cloud forest. Plant Ecol. 213, 339-353. doi: 10.1007/s11258-011-9980-5
    Muñoz-Villers, L.E., López-Blanco, J., 2008. Land use/cover changes using Landsat TM/ETM images in a tropical and biodiverse mountainous area of central-eastern Mexico. Int. J. Remote Sens. 29, 71-93. doi: 10.1080/01431160701280967
    Navarro-Sigüenza, A.G., Lira-Noriega, A., Peterson, A.T., Oliveras De Ita, A., GordilloMartínez, A., 2007. Diversidad, endemismo y conservación de las aves. In: Luna, I., Morrone, J.J., Espinosa, D. (Eds. ), Biodiversidad de la Faja Volcánica Transmexicana. Universidad Nacional Autonoma de México, México, pp. 461-483.
    Palacio, R., 2014. Estructura de la red de interacciones mutualistas entre plantas y aves frugívoras en el bosque nublado de San Antonio -km 18, Valle del Cauca. Bachelor Thesis. Universidad ICESI, Santiago de Cali.
    Palacio, R., Valderrama-Ardila, C., Kattan, G.H., 2016. Generalist species have a central role in a highly diverse plant-frugivore network. Biotropica 43, 349-355. doi: 10.1111/btp.12290
    Peres, C.A., Emilio, T., Schietti, J., Desmoulière, S.J.M., Levi, T., 2016. Dispersal limitation induces long-term biomass collapse in overhunted Amazonian forests. Proc. Natl. Acad. Sci. U.S.A. 113, 892-897. doi: 10.1073/pnas.1516525113
    Pérez-Cadavid, A., Rojas-Soto, O.R., Bonilla-Moheno, M., 2018. Effect of seed ingestion by birds on the germination of understorey species in cloud forest. Rev. Mex. Biodivers. 89, 1167-1175.
    Peters, V., Carlo, T.A., Mello, M.A.R., Rice, R.A., Tallamy, D.W., Caudill, S.A., et al., 2016. Using plant-animal interactions to inform tree selection in tree-based agroecosystems for enhanced biodiversity. Bioscience 66, 1046-1056. doi: 10.1093/biosci/biw140
    Pizo, M.A., Morales, J.M., Ovaskainen, O., Carloet, T.A., 2021. Frugivory specialization in birds and fruit chemistry structure mutualistic networks across the Neotropics. Am. Nat. 197, 236-249. doi: 10.1086/712381
    Ponce-Reyes, R., Reynoso-Rosales, V.H., Watson, J.E.M., VanDerWal, J., Fuller, R.A., Pressey, R.L., et al., 2012. Vulnerability of cloud forest reserves in Mexico to climate change. Nat. Clim. Change 2, 448-452. doi: 10.1038/nclimate1453
    Ramos-Robles, M., Dáttilo, W., Díaz-Castelazo, C., Andresen, E., 2018. Fruit traits and temporal abundance shape plant-frugivore interaction networks in a seasonal tropical forest. Sci. Nat. 105, 29. doi: 10.1007/s00114-018-1556-y
    Roldán-Clarà, B., López-Medellín, X., Espejel, I., Arellano, E., 2014. Literature review of the use of birds as pets in Latin-America, with a detailed perspective on Mexico. Ethnobiol. Conserv. 3, 5.
    Roldán-Clará, B., Toledo, V.M., Espejel, I., 2017. The use of birds as pets in Mexico. J. Ethnobiol. Ethnomed. 13, 35. doi: 10.1186/s13002-017-0161-z
    Ruiz-Jiménez, C.A., Téllez-Valdés, O., Luna-Vega, I., 2012. Clasificación de los bosques mesófilos de montaña de México: afinidades de la flora. Rev. Mex. Biodivers. 83, 1110-1144.
    Saavedra, S., Stouffer, D.B., Uzzi, B., Bascompte, J., 2011. Strong contributors to network persistence are the most vulnerable to extinction. Nature 478, 233-235. doi: 10.1038/nature10433
    Salazar-Rivera, G.I., Dáttilo, W., Castillo-Campos, G., Flores-Estévez, N., García, B.R., Inzunza, E.R., 2020. The frugivory network properties of a simplified ecosystem: birds and plants in a Neotropical periurban park. Ecol. Evol. 10, 8579-8591. doi: 10.1002/ece3.6481
    Saldaña-Vázquez, R.A., Sosa, V.J., Hernández-Montero, J.R., López-Barrera, F., 2010. Abundance responses of frugivorous bats (Stenodermatinae) to coffee cultivation and selective logging practices in mountainous central Veracruz, Mexico. Biodivers. Conserv. 19, 2111-2124. doi: 10.1007/s10531-010-9829-6
    SEMARNAT (Secretaría del Medio Ambiente y Recursos Naturales), 2010. Norma Oficial Mexicana NOM-059-Semarnat-2010, Protección Ambiental-especies nativas de México de flora y fauna silvestres-categorías de riesgo y especificaciones para su inclusión, exclusión o cambio-lista de especies en riesgo. Diario Oficial de la Federación. 2da Sección, 30 de diciembre de 2010. http://www.iacseaturtle.org/docs/marco/mexico/Mexico%20-%20NORMA%20Oficial%20Mexicana%20NOM-059-SEMARNAT-2010.pdf.
    Sibley, D.A., 2014. The Sibley Guide to Birds, second ed. Alfred A. Knopf, New York.
    Skagen, S.K., Melcher, C.P., Howe, W.H., Knopf, F.L., 1998. Comparative use of riparian corridors and oases by migrating birds in Southeast Arizona. Conserv. Biol. 12, 896-909. doi: 10.1046/j.1523-1739.1998.96384.x
    Snow, D.W., 1981. Tropical frugivorous birds and their food plants: a world survey. Biotropica 13, 1-14. doi: 10.2307/2387865
    Toledo-Aceves, T., García-Franco, J., Williams-Linera, G., et al., 2014. Significance of remnant cloud forest fragments as reservoirs of tree and epiphytic bromeliad diversity. Trop. Conserv. Sci. 7, 230-243. doi: 10.1177/194008291400700205
    Vidal, M.M., Hasul, E., Pizo, M.A., Tamashiro, J.Y., Silva, W.R., Guimarães Jr., P.R., 2014. Frugivores at higher risk of extinction are the key elements of a mutualistic network. Ecology 95, 3440-3447. doi: 10.1890/13-1584.1
    Williams-Linera, G., Toledo-Garibaldi, M., Gallardo-Hernández, C., 2013. How heterogeneous are the cloud forest communities in the mountains of central Veracruz, Mexico? Plant Ecol. 214, 685-701. doi: 10.1007/s11258-013-0199-5
  • 加载中


    通讯作者: 陈斌, bchen63@163.com
    • 1. 

      沈阳化工大学材料科学与工程学院 沈阳 110142

    1. 本站搜索
    2. 百度学术搜索
    3. 万方数据库搜索
    4. CNKI搜索

    Figures(3)  / Tables(2)

    Article Metrics

    Article views (148) PDF downloads(6) Cited by()
    Proportional views


    DownLoad:  Full-Size Img  PowerPoint