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Original Articles

Modularity and robustness of a plant-frugivore interaction network in a disturbed tropical forest

ORCID Icon, ORCID Icon &
Pages 209-222 | Received 14 Aug 2017, Accepted 23 Feb 2018, Published online: 20 Mar 2018

References

  • Almazán-Núñez RC, Arizmendi MdC, Eguiarte LE, Corcuera P. 2015. Distribution of the community of frugivorous birds along a successional gradient in a tropical dry forest in south-western Mexico. J Trop Ecol. 31:57–68.
  • August PV. 1981. Fig fruit Consumption and seed dispersal by Artibeus jamaicensis in the Llanos of Venezuela. Biotropica. 13:70–76.
  • Bairey E, Kelsic ED, Kishony R. 2016. High-order species interactions shape ecosystem diversity. Nat Commun. 7:12285.
  • Bascompte J, Jordano P. 2007. Plant-animal mutualistic networks: the architecture of biodiversity. Annu Rev Ecol Evol Syst. 38:567–593.
  • Bascompte J, Jordano P, Melián CJ, Olesen JM. 2003. The nested assembly of plant–animal mutualistic networks. Proc Natl Acad Sci. 100:9383–9387.
  • Beaune D, Bretagnolle F, Bollache L, Hohmann G, Surbeck M, Fruth B. 2013. Seed dispersal strategies and the threat of defaunation in a Congo forest. Biodivers Conserv. 22:225–238.
  • Benítez-Malvido J, Dáttilo W. 2015. Interaction intimacy of pathogens and herbivores with their host plants influences the topological structure of ecological networks in different ways. Am J Bot. 102:512–519.
  • Blüthgen N, Menzel F, Hovestadt T, Fiala B, Blüthgen N. 2007. Specialization, constraints, and conflicting interests in mutualistic networks. Curr Biol. 17:341–346.
  • Brodie JF, Aslan CE. 2012. Halting regime shifts in floristically intact tropical forests deprived of their frugivores. Restor Ecol. 20:153–157.
  • Burgos E, Ceva H, Perazzo RPJ, Devoto M, Medan D, Zimmermann M, María Delbue A. 2007. Why nestedness in mutualistic networks? J Theor Biol. 249:307–313.
  • Butchart SHM, Walpole M, Collen B, van Strien A, Scharlemann JPW, Almond REA, Baillie JEM, Bomhard B, Brown C, Bruno J, et al. 2010. Global biodiversity: indicators of recent declines. Science. 328:1164.
  • Cagnolo L, Salvo A, Valladares G. 2011. Network topology: patterns and mechanisms in plant-herbivore and host-parasitoid food webs. J Anim Ecol. 80:342–351.
  • Carlo TA, Morales JM. 2016. Generalist birds promote tropical forest regeneration and increase plant diversity via rare-biased seed dispersal. Ecology. 97:1819–1831.
  • Caryl FM, Raynor R, Quine CP, Park KJ. 2012. The seasonal diet of British pine marten determined from genetically identified scats. J Zool. 288:252–259.
  • Ceballos G, Ehrlich PR, Barnosky AD, García A, Pringle RM, Palmer TM. 2015. Accelerated modern human–induced species losses: entering the sixth mass extinction. Sci Adv. 1:e1400253–e1400253.
  • Chacoff NP, Vázquez DP, Lomáscolo SB, Stevani EL, Dorado J, Padrón B. 2012. Evaluating sampling completeness in a desert plant–pollinator network. J Anim Ecol. 81:190–200.
  • Chao A. 2005. Species richness estimation. In: Balakrishnan N, Read CB, Vidakovic B, editors. Encyclopedia of statistical sciences. New York (NY): Wiley; p. 7909–7916.
  • Chao A, Colwell RK, Lin C-W, Gotelli NJ. 2009. Sufficient sampling for asymptotic minimum species richness estimators. Ecology. 90:1125–1133.
  • Christensen AF. 2000. The fifteenth-and twentieth-century colonization of the Basin of Mexico by the great-tailed grackle (Quiscalus mexicanus). Global Ecol Biogeogr. 9:415–420.
  • Colwell RK. 2013. EstimateS: statistical estimation of species richness and shared species from samples. Version 9.1.0. User’s Guide and Application. [ accessed 2016 Nov 29]. http://viceroy.eeb.uconn.edu/estimates.
  • Convention on Wetlands of International Importance especially as Waterfowl Habitat. 1971. UN Treaty Series No. 14583. Ramsar (Iran). 2 Feb.
  • Cottee-Jones HEW, Bajpai O, Chaudhary LB, Whittaker RJ. 2016. The importance of Ficus (Moraceae) trees for tropical forest restoration. Biotropica. 48:413–419.
  • D’Avila G, Gomes-Jr A, Canary AC, Bugoni L. 2010. The role of avian frugivores on germination and potential seed dispersal of the Brazilian Pepper Schinus terebinthifolius. Biota Neotrop. 10:45–51.
  • Dáttilo W, Lara-Rodríguez N, Jordano P, Guimarães PR, Thompson JN, Marquis RJ, Medeiros LP, Ortiz-Pulido R, Marcos-García MA, Rico-Gray V. 2016. Unravelling Darwin’s entangled bank: architecture and robustness of mutualistic networks with multiple interaction types. Proc R Soc Lond B Biol Sci. 283:20161564.
  • Dehling DM, Töpfer T, Schaefer HM, Jordano P, Böhning-Gaese K, Schleuning M. 2014. Functional relationships beyond species richness patterns: trait matching in plant–bird mutualisms across scales. Global Ecol Biogeogr. 23:1085–1093.
  • Dirzo R, Young HS, Galetti M, Ceballos G, Isaac NJB, Collen B. 2014. Defaunation in the Anthropocene. Science. 345:401–406.
  • Donatti CI, Guimarães PR, Galetti M, Pizo MA, Marquitti F, Dirzo R. 2011. Analysis of a hyper‐diverse seed dispersal network: modularity and underlying mechanisms. Ecol Lett. 14:773–781.
  • Donoso I, Schleuning M, García D, Fründ J. 2017. Defaunation effects on plant recruitment depend on size matching and size trade-offs in seed-dispersal networks. Proc R Soc Lond B Biol Sci. 284:1855.
  • Dormann CF, Fründ J, Blüthgen N, Gruber B. 2009. Indices, graphs and null models: analyzing Bipartite ecological networks. Open Ecol J. 2:7–24.
  • Dormann CF, Strauss R. 2014. A method for detecting modules in quantitative bipartite networks. Methods Ecol Evol. 5:90–98.
  • Dubroeucq D, Geissert D, Moreno P, Millot G. 1992. Soil evolution and plant communities in coastal dunes near Veracruz, Mexico. Cahiers-ORSTOM Pédologie. 27:237–250.
  • Evans DM, Pocock MJ, Memmott J. 2013. The robustness of a network of ecological networks to habitat loss. Ecol Lett. 16:844–852.
  • Falcão JCF, Dáttilo W, Rico-Gray V. 2016. Sampling effort differences can lead to biased conclusions on the architecture of ant–plant interaction networks. Ecol Complex. 25:44–52.
  • Farwig N, Berens DG. 2012. Imagine a world without seed dispersers: a review of threats, consequences and future directions. Basic Appl Ecol. 13:109–115.
  • Fleming TH. 1988. The short-tailed fruit bat: a study in plant-animal interactions. Chicago (IL): University of Chicago Press.
  • Fleming TH, Kress WJ. 2013. The ornaments of life: coevolution and conservation in the tropics. Chicago (IL): University of Chicago Press.
  • Fortuna MA, Stouffer DB, Olesen JM, Jordano P, Mouillot D, Krasnov BR, Poulin R, Bascompte J. 2010. Nestedness versus modularity in ecological networks: two sides of the same coin? J Anim Ecol. 79:811–817.
  • Galetti M, Dirzo R. 2013. Ecological and evolutionary consequences of living in a defaunated world. Biol Conserv. 163:1–6.
  • Galetti M, Pires AS, Brancalion PHS, Fernandez FAS. 2017. Reversing defaunation by trophic rewilding in empty forests. Biotropica. 49:5–8.
  • González-Romero A, Lara-López MS. 2006. Los anfibios, los reptiles y los mamíferos [Amphibians, reptiles and mammals]. In: Moreno-Casasola P, editor. Entornos veracruzanos: la costa de La Mancha. Xalapa (VE): Instituto de Ecología; p. 407–422.
  • Gotelli NJ, Colwell RK. 2001. Quantifying biodiversity: procedures and pitfalls in the measurement and comparison of species richness. Ecol Lett. 4:379–391.
  • Greenberg R, Foster MS, Marquez-Valdelamar L. 1995. The role of the white-eyed vireo in the dispersal of Bursera fruit on the Yucatan Peninsula. J Trop Ecol. 11:619–639.
  • Guimarães Jr PR, Machado G, de Aguiar MAM, Jordano P, Bascompte J, Pinheiro A, dos Reis SF. 2007. Build-up mechanisms determining the topology of mutualistic networks. J Theor Biol. 249:181–189.
  • Guimarães PR Jr, Jordano P, Thompson JN. 2011. Evolution and coevolution in mutualistic networks. Ecol Lett. 14:877–885.
  • Guimerà R, Nunes Amaral LA. 2005. Functional cartography of complex metabolic networks. Nature. 433:895–900.
  • Harrison RD, Tan S, Plotkin JB, Slik F, Detto M, Brenes T, Itoh A, Davies SJ. 2013. Consequences of defaunation for a tropical tree community. Ecol Lett. 16:687–694.
  • Heithaus ER. 1982. Coevolution between bats and plants. In: Kutz TH, editor. Ecology of Bats. Boston (MA): Springer; p. 327–367.
  • Henneman ML, Memmott J. 2001. Infiltration of a Hawaiian community by introduced biological control agents. Science. 293:1314–1316.
  • Hull PM, Darroch SAF, Erwin DH. 2015. Rarity in mass extinctions and the future of ecosystems. Nature. 528:345–351.
  • Inzunza ER, Hoffman SW, Goodrich L. 2005. Stopover ecology of Neotropical migrants in Central Veracruz, Mexico. USDA For Serv Gen Tech Rep. PSW-GTR-191; p. 657–672.
  • Joppa LN, Montoya JM, Solé R, Sanderson J, Pimm SL. 2010. On nestedness in ecological networks. Evol Ecol Res. 12:35–46.
  • Jordano P. 2016. Sampling networks of ecological interactions. Funct Ecol. 30:1883–1893.
  • Jordano P. 2014. Fruits and frugivory. In: Gallagher RS, editor. Seeds: the ecology of regeneration of plant communities. 3rd ed. Wallingford ((OX)): CABI; p. 18–61.
  • Kurten EL, Wright SJ, Carson WP. 2015. Hunting alters seedling functional trait composition in a Neotropical forest. Ecology. 96:1923–1932.
  • Lees AC, Peres CA. 2008. Conservation value of remnant riparian forest corridors of varying quality for amazonian birds and mammals. Conserv Biol. 22:439–449.
  • Lewis SL, Edwards DP, Galbraith D. 2015. Increasing human dominance of tropical forests. Science. 349:827–832.
  • López-Carretero A, Díaz-Castelazo C, Boege K, Rico-Gray V. 2014. Evaluating the spatio-temporal factors that structure network parameters of plant-herbivore interactions. PloS One. 9:e110430.
  • Martínez ML, García-Franco JG, Rico-Gray V. 2006. Las adaptaciones y las interacciones de especies [Species adaptations and interactions]. In: Moreno-Casasola P, editor. Entornos Veracruzanos: la costa de La Mancha. Xalapa (VE): Instituto de Ecología, A.C.; p. 273–283.
  • Martínez-Adriano CA, Aguirre-Jaimes A, Díaz-Castelazo C. 2016. Floristic survey of flowering plants in a tropical coastal ecosystem in Veracruz, Mexico. Bot Sci. 94:185–197.
  • McCauley DJ, Pinsky ML, Palumbi SR, Estes JA, Joyce FH, Warner RR. 2015. Marine defaunation: animal loss in the global ocean. Science. 347:6219.
  • McConkey KR, O’Farrill G. 2016. Loss of seed dispersal before the loss of seed dispersers. Biol Conserv. 201:38–49.
  • Mello MAR, Rodrigues FA, Costa LdF, Kissling WD, Şekercioğlu ÇH, Marquitti FMD, Kalko EKV. 2015. Keystone species in seed dispersal networks are mainly determined by dietary specialization. Oikos. 124:1031–1039.
  • Memmott J, Waser NM, Price MV. 2004. Tolerance of pollination networks to species extinctions. Proc R Soc Lond B Biol Sci. 271:2605–2611.
  • Muscarella R, Fleming TH. 2007. The role of frugivorous bats in tropical forest succession. Biol Rev. 82:573–590.
  • Oksanen J, Blanchet FG, Kindt R, Legendre P, O’Hara RB, Simpson GL, Solymos P, Henry M, Stevens H, Wagner H. 2010. Vegan: community Ecology Package. R package version 1.17-2. http://CRAN.R-project.org/package=vegan.
  • Olesen JM, Bascompte J, Dupont YL, Elberling H, Rasmussen C, Jordano P. 2010. Missing and forbidden links in mutualistic networks. Proc R Soc Lond B Biol Sci. 278:725–732.
  • Olesen JM, Bascompte J, Dupont YL, Jordano P. 2007. The modularity of pollination networks. Proc Natl Acad Sci U S A. 104:19891–19896.
  • Ortíz-Púlido R, Laborde J, Guevara S. 2000. Frugivoría por aves en un paisaje fragmentado consecuencias de la dispersión de semillas [Frugivory by birds in a fragmented landscape consequences of seed dispersal]. Biotropica. 32:473–488.
  • Patefield WM. 1981. Algorithm AS 159: an efficient method of generating r x c tables with given row and column totals. ‎J Appl Stat. 30:91–97.
  • Peredo A, Martínez D, Rodríguez-Pérez J, García D. 2013. Mammalian seed dispersal in Cantabrian woodland pastures: network structure and response to forest loss. Basic Appl Ecol. 14:378–386.
  • Peres CA, Dolman PM. 2000. Density compensation in neotropical primate communities: evidence from 56 hunted and nonhunted Amazonian forests of varying productivity. Oecologia. 122:175–189.
  • Peres CA, Palacios E. 2007. Basin-wide effects of game harvest on vertebrate population densities in Amazonian forests: implications for animal-mediated seed dispersal. Biotropica. 39:304–315.
  • Pérez-Méndez N, Jordano P, García C, Valido A. 2016. The signatures of Anthropocene defaunation: cascading effects of the seed dispersal collapse. Sci Rep. 6:24820.
  • Pérez-Méndez N, Jordano P, Valido A. 2017. Persisting in defaunated landscapes: reduced plant population connectivity after seed dispersal collapse. J Ecol. 00:1–12.
  • Pocock MJO, Evans DM, Memmott J. 2012. The robustness and restoration of a network of ecological networks. Science. 335:973–977.
  • Poisot T, Stouffer DB, Gravel D. 2015. Beyond species: why ecological interaction networks vary through space and time. Oikos. 124:243–251.
  • R Core Team. 2014. R: A language and environment for statistical computing. Vienna (Austria): R Foundation for Statistical Computing. http://www.R-project.org/.
  • Ramos-Robles M, Andresen E, Díaz-Castelazo C. 2016. Temporal changes in the structure of a plant-frugivore network are influenced by bird migration and fruit availability. PeerJ. 4:e2048.
  • Ribeiro da Silva F, Montoya D, Furtado R, Memmott J, Pizo MA, Rodrigues RR. 2015. The restoration of tropical seed dispersal networks. Restor Ecol. 23:852–860.
  • Ripple WJ, Abernethy K, Betts MG, Chapron G, Dirzo R, Galetti M, Levi T, Lindsey PA, Macdonald DW, Machovina B, et al. 2016. Bushmeat hunting and extinction risk to the world’s mammals. R Soc Open Sci. 3:160498.
  • Ripple WJ, Estes JA, Beschta RL, Wilmers CC, Ritchie EG, Hebblewhite M, Berger J, Elmhagen B, Letnic M, Nelson MP, et al. 2014. Status and ecological effects of the world’s largest carnivores. Science. 343:1241484.
  • Ruggera RA, Blendinger PG, Gomez MD, Marshak C. 2016. Linking structure and functionality in mutualistic networks: do core frugivores disperse more seeds than peripheral species? Oikos. 125:541–555.
  • Rumeu B, Devoto M, Traveset A, Olesen JM, Vargas P, Nogales M, Heleno R. 2017. Predicting the consequences of disperser extinction: richness matters the most when abundance is low. Funct Ecol. 31:1910–1920.
  • Schaefer HM, Schmidt V, Winkler H. 2003. Testing the defence trade-off hypothesis: how contents of nutrients and secondary compounds affect fruit removal. Oikos. 102:318–328.
  • Schleuning M, Böhning-Gaese K, Dehling DM, Burns KC. 2014. At a loss for birds: insularity increases asymmetry in seed-dispersal networks. Global Ecol Biogeogr. 23:385–394.
  • Schleuning M, Fründ J, García D. 2015. Predicting ecosystem functions from biodiversity and mutualistic networks: an extension of trait-based concepts to plant-animal interactions. Ecography. 38:380–392.
  • Schleuning M, Ingmann L, Strauß R, Fritz SA, Dalsgaard B, Matthias Dehling D, Plein M, Saavedra F, Sandel B, Svenning J-C, et al. 2014. Ecological, historical and evolutionary determinants of modularity in weighted seed-dispersal networks. Ecol Lett. 17:454–463.
  • Stevenson P. 2005. Potential keystone plant species for the frugivore community at Tinigua park, Colombia. In: Dew JL, Bouble JP, editors. Tropical fruits and frugivores: the search for strong interactors. Dordrecht (HO): Springer Netherlands; p. 37–57.
  • Stiles E. 1993. The influence of pulp lipids on fruit preference by birds. Vegetatio. 107:227–235.
  • Terborgh J, Nuñez-Iturri G, Pitman NCA, Valverde FHC, Alvarez P, Swamy V, Pringle EG, Paine CET. 2008. Tree recruitment in an empty forest. Ecology. 89:1757–1768.
  • Tilman D, May RM, Lehman CL, Nowak MA. 1994. Habitat destruction and the extinction debt. Nature. 371:65–66.
  • Travieso-Bello AC. 2000. Biodiversidad del paisaje costero de La Mancha, Actopan, Veracruz [Biodiversity of the coastal landscape of La Mancha, Actopan, Veracruz] [master’s thesis]. Xalapa (VE): Instituto de Ecología, A. C.
  • Tylianakis JM, Laliberté E, Nielsen A, Bascompte J. 2010. Conservation of species interaction networks. Biol Conserv. 143:2270–2279.
  • Valdovinos FS, Ramos-Jiliberto R, Flores JD, Espinoza C, López G. 2009. Structure and dynamics of pollination networks: the role of alien plants. Oikos. 118:1190–1200.
  • Valiente-Banuet A, Aizen MA, Alcántara JM, Arroyo J, Cocucci A, Galetti M, García MB, García D, Gómez JM, Jordano P, et al. 2015. Beyond species loss: the extinction of ecological interactions in a changing world. Funct Ecol. 29:299–307.
  • Van Der Pijl L. 1957. The dispersal of plants by bats (Chiropterochory). Acta Bot Neerl. 6:291–315.
  • Vázquez DP, Melián CJ, Williams NM, Blüthgen N, Krasnov BR, Poulin R. 2007. Species abundance and asymmetric interaction strength in ecological networks. Oikos. 116:1120–1127.
  • Vázquez DP, Poulin R, Krasnov BR, Shenbrot GI. 2005. Species abundance and the distribution of specialization in host–parasite interaction networks. J Anim Ecol. 74:946–955.
  • Vidal MM, Hasui E, Pizo MA, Tamashiro JY, Silva WR, Guimaraes JPR. 2014. Frugivores at higher risk of extinction are the key elements of a mutualistic network. Ecology. 95:3440–3447.
  • Vidal MM, Pires MM, Guimarães JPR. 2013. Large vertebrates as the missing components of seed-dispersal networks. Biol Conserv. 163:42–48.
  • Watson DM, Rawsthorne J. 2013. Mistletoe specialist frugivores: latterday ‘Johnny Appleseeds’ or self-serving market gardeners? Oecologia. 172:925–932.
  • Watts S, Dormann CF, Amm G, Ollerton J. 2016. The influence of floral traits on specialization and modularity of plant–pollinator networks in a biodiversity hotspot in the Peruvian Andes. Ann Bot. 118:415–429.
  • Wilkie DS, Bennett EL, Peres CA, Cunningham AA. 2011. The empty forest revisited. Ann N Y Acad Sci. 1223:120–128.

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