Hostname: page-component-cd9895bd7-q99xh Total loading time: 0 Render date: 2024-12-19T03:01:37.042Z Has data issue: false hasContentIssue false

Loss of Generalist Plant Species and Functional Diversity Decreases the Robustness of a Seed Dispersal Network

Published online by Cambridge University Press:  09 November 2018

Vinicius AG Bastazini*
Affiliation:
Theoretical and Experimental Ecology Station, National Center for Scientific Research – Paul Sabatier University, 2 route du CNRS, 09200, Moulis, France Graduate Program in Ecology, Universidade Federal do Rio Grande do Sul, Porto Alegre, RS, 91501-970, Brazil
Vanderlei J Debastiani
Affiliation:
Graduate Program in Ecology, Universidade Federal do Rio Grande do Sul, Porto Alegre, RS, 91501-970, Brazil
Bethânia O Azambuja
Affiliation:
Graduate Program in Ecology, Universidade Federal do Rio Grande do Sul, Porto Alegre, RS, 91501-970, Brazil
Paulo R Guimarães Jr
Affiliation:
Departmento de Ecologia, Instituto de Biociências, Universidade de São Paulo, Rua do Matão, Travessa 14, no. 321, 05508-900, São Paulo, SP, Brazil
Valério D Pillar
Affiliation:
Department of Ecology, Universidade Federal do Rio Grande do Sul, Porto Alegre, RS, 91501-970, Brazil
*
Author for correspondence: Dr Vinicius AG Bastazini, Email: [email protected]

Summary

Understanding cascading effects of species loss is a major challenge for ecologists. Traditionally, the robustness of ecological networks has been evaluated based on simulation studies where primary extinctions occur at random or as a function of species specialization, ignoring other important biological factors. Here, we estimate the robustness of a seed dispersal network from a grassland–forest mosaic in southern Brazil, simulating distinct scenarios of woody plant species extinction, including scenarios where species are eliminated based on their evolutionary and functional distinctiveness. Our results suggest that the network is more robust when species are eliminated based on their evolutionary uniqueness, followed by random extinctions, the extinction of the most specialist species, functional distinctiveness and, at last, when the most generalist species are sequentially eliminated. Our results provide important information for grassland–forest mosaic management, as they indicate that loss of generalist species and functional diversity makes the system more likely to collapse.

Type
Non-Thematic Papers
Copyright
© Foundation for Environmental Conservation 2018 

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

Angiosperm Phylogeny Group (2009) An update of the Angiosperm Phylogeny Group classification for the orders and families of flowering plants: APG III. Botanical Journal of the Linnean Society 161: 105121.Google Scholar
Albert, R, Barabási, A (2002) Statistical mechanics of complex networks. Reviews of Modern Physics 74: 4774.Google Scholar
Astegiano, J, Massol, F, Vidal, MM, Cheptou, PO, Guimarães, PR Jr (2015) The robustness of plant–pollinator assemblages: linking plant interaction patterns and sensitivity to pollinator loss. PLoS One 10: e0117243.Google Scholar
Azambuja, BO (2009) Relações Entre Aves Dispersoras de Sementes e Manchas Florestais em Matriz Campestre na Serra do Sudeste, RS. PhD thesis. Porto Alegre, Brazil: Federal University of Rio Grande do Sul.Google Scholar
Bascompte, J, Jordano, P, Melián, CJ, Olesen, JM (2003) The nested assembly of plant–animal mutualistic networks. Proceedings of the National Academy of Sciences of the United States of America 100: 93839387.Google Scholar
Bastazini, VAG, Ferreira, PMA, Azambuja, BO, Casas, G, Debastiani, VJ, Guimaraes, PR Jr, Pillar, VD (2017) Untangling the tangled bank: a novel method for partitioning the effects of phylogenies and traits on ecological networks. Evolutionary Biology 44: 312324.Google Scholar
Bond, WJ, Parr, CL (2010) Beyond the forest edge: ecology, diversity and conservation of the grassy biomes. Biological Conservation 143: 23952404.Google Scholar
Borrett, SR, Moody, J, Edelmann, A (2014) The rise of network ecology: maps of the topic diversity and scientific collaboration. Ecological Modelling 293: 111127.Google Scholar
Bossuyt, B, Hermy, M, Deckers, J (1999) Migration of herbaceous plant species across ancient–recent forest ecotones in central Belgium. Journal of Ecology 87: 629638.Google Scholar
Bowman, DMJS, Walsh, A, Milne, DJ (2001) Forest expansion and grassland contraction within a Eucalyptus savanna matrix between 1941 and 1994 at Litchfield National Park in the Australian monsoon tropics. Global Ecology & Biogeography 10: 535548.Google Scholar
Breymeyer, AI, van Dyne, GM (1980) Grasslands, Systems Analysis and Man. Cambridge, UK: Cambridge University Press.Google Scholar
Brodie, JF, Aslan, CE, Rogers, HS, Redford, KH, Maron, JL, Bronstein, JL, Groves, CR (2014) Secondary extinctions of biodiversity. Trends in Ecology & Evolution 29: 664672.Google Scholar
Burgos, E, Ceva, H, Perazzo, RPJ, Devoto, M, Medan, D, Zimmermann, M, Delbue, AM (2007) Why nestedness in mutualistic networks? Journal of Theoretical Biology 249: 307313.Google Scholar
Cardillo, M, Mace, GM, Jones, KE, Bielby, J, Bininda-Emonds, OR, Sechrest, W, Orme, CDL, Purvis, A (2005) Multiple causes of high extinction risk in large mammal species. Science 309: 12391241.Google Scholar
Cardillo, M, Mace, GM, Gittleman, JL, Jones, KE, Bielby, J, Purvis, A (2008) The predictability of extinction: biological and external correlates of decline in mammals. Proceedings of the Royal Society of London B: Biological Sciences 275: 14411448.Google Scholar
Carlucci, MB, Duarte, LDS, Pillar, VD (2011) Nurse rocks influence forest expansion over native grassland in southern Brazil. Journal of Vegetation Science 22: 111119.Google Scholar
Ceballos, G, Ehrlich, PR, Barnosky, AD, García, A, Pringle, RM, Palmer, TM (2015) Accelerated modern human-induced species losses: entering the sixth mass extinction. Science Advances 1: e1400253.Google Scholar
Colwell, RK, Dunn, RR, Harris, NC (2012) Coextinction and persistence of dependent species in a changing world. Annual Review in Ecology, Evolution and Systematic 43: 183203.Google Scholar
Correa, SB, Costa‐Pereira, R, Fleming, T, Goulding, M, Anderson, JT (2015) Neotropical fish–fruit interactions: eco‐evolutionary dynamics and conservation. Biological Reviews 90: 12631278.Google Scholar
Costa, JM, Ramos, JA, Silva, LP, Timóteo, S, Andrade, P, Araújo, PM, Carneiro, C, Correia, E, Cortez, P, Felgueiras, M, Godinho, C, Lopes, RJ, Matos, C, Norte, AC, Pereira, PF, Rosa, A, Heleno, RH (2018) Rewiring of experimentally disturbed seed dispersal networks might lead to unexpected network configurations. Basic and Applied Ecology 30: 1122.Google Scholar
Coupland, RT (ed.) (1979) Grasslands Ecosystems of the World: Analysis of Grasslands and Their Uses. Cambridge, UK: Cambridge University Press.Google Scholar
Curtin, C, Western, D (2008) Grasslands, people, and conservation: over‐the‐horizon learning exchanges between African and American pastoralists. Conservation biology 22: 870877.Google Scholar
Curtsdotter, A, Binzer, A, Brose, U, de Castro, F, Ebenman, B, Eklöf, A, Riede, JO, Thierry, A, Rall, BC (2011) Robustness to secondary extinctions: comparing trait-based sequential deletions in static and dynamic food webs. Basic and Applied Ecology 12: 571580.Google Scholar
Danielson, BJ (1991) Communities in a landscape: the influence of habitat heterogeneity on the interactions between species. The American Naturalist 138: 11051120.Google Scholar
Dehling, D, Jordano, P, Schaefer, H, Böhning-Gaese, K, Schleuning, M (2016) Morphology predicts species’ functional roles and their degree of specialization in plant–frugivore interactions. Proceedings of the Royal Society of London B: Biological Sciences 283: 20152444.Google Scholar
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. Proceedings of the Royal Society of London B: Biological Sciences 284: 20162664.Google Scholar
Dunn, RR, Harris, NC, Colwell, RK, Koh, LP, Sodhi, NS (2009) The sixth mass coextinction: are most endangered species parasites and mutualists? Proceedings of the Royal Society of London B: Biological Sciences 276: 30373045.Google Scholar
Dunne, JA, Williams, RJ, Martinez, ND (2002) Network structure and biodiversity loss in food webs: robustness increases with connectance. Ecology Letters 5: 558567.Google Scholar
Eklöf, A, Tang, S, Allesina, S (2013) Secondary extinctions in food webs: a Bayesian network approach. Methods in Ecology and Evolution 4: 760770.Google Scholar
Fowler, M (2010) Exticntion cascades and the distribution of species interactions. Oikos 119: 864873.Google Scholar
Gaston, KJ, Fuller, RA (2008) Commonness, population depletion and conservation biology. Trends in Ecology & Evolution 23: 1419.Google Scholar
González, AMM, Dalsgaard, B, Olesen, JM (2010) Centrality measures and the importance of generalist species in pollination networks. Ecological Complexity 7: 3643.Google Scholar
Goudard, A, Loreau, M (2008) Nontrophic interactions, biodiversity, and ecosystem functioning: an interaction web model. The American Naturalist 171: 91106.Google Scholar
Hanley, TC, La Pierre, KJ, (eds). (2015) Trophic Ecology: Bottom-Up and Top-Down Interactions across Aquatic and Terrestrial Systems. Cambridge, UK: Cambridge University Press.Google Scholar
Henwood, WD (2010) Toward a strategy for the conservation and protection of the world’s temperate grasslands. Great Plains Research 20: 121134.Google Scholar
Herrera, CM (1985) Determinants of plant–animal coevolution: the case of mutualistic dispersal of seeds by vertebrates. Oikos 44: 132141.Google Scholar
Hu, S, Chapin, FS III, Firestone, MK, Field, CB, Chiariello, NR (2001) Nitrogen limitation of microbial decomposition in a grassland under elevated CO2 . Nature 409: 188191.Google Scholar
Iganci, JR, Heiden, G, Miotto, STS, Pennington, RT (2011) Campos de Cima da Serra: the Brazilian subtropical highland grasslands show an unexpected level of plant endemism. Botanical Journal of the Linnean Society 167: 378393.Google Scholar
Instituto de Pesquisas Agronômicas (1989) Atlas Agroclimático do Estado do Rio Grande do Sul. Porto Alegre, Brazil: Pallotti.Google Scholar
Jackson, JB, Kirby, MX, Berger, WH, Bjorndal, KA, Botsford, LW, Bourque, BJ, Bradbury, RH, et al. (2001) Historical overfishing and the recent collapse of coastal ecosystems. Science 293: 629637.Google Scholar
Jensen, TS, Nielsen, OF (1986) Rodents as seed dispersers in a heath–oak wood succession. Oecologia 70: 214221.Google Scholar
Jordano, P (2000) Fruits and frugivory. In: Seeds: The Ecology of Regeneration in Natural Plant Communities, ed. M Fenner, pp. 125165. Wallingford, UK: CABI Publishing.Google Scholar
Kang, S, Ma, W, Li, FY, Zhang, Q, Niu, J, Ding, Y, Han, F, et al. (2015) Functional redundancy instead of species redundancy determines community stability in a typical steppe of Inner Mongolia. PLoS One 10: e0145605.Google Scholar
Kiers, ET, Palmer, TM, Ives, AR, Bruno, JF, Bronstein, JL (2010) Mutualisms in a changing world: an evolutionary perspective. Ecology Letters 13: 14591474.Google Scholar
Lefcheck, JS, Bastazini, VAG, Griffin, JN (2015) Choosing and using multiple traits in functional diversity research. Environmental Conservation 42: 104107.Google Scholar
Legendre, P, Legendre, LF (2012) Numerical Ecology. Amsterdam, The Netherlands: Elsevier.Google Scholar
Luza, AL, Carlucci, MB, Hartz, SM, Duarte, LD (2014) Moving from forest vs. grassland perspectives to an integrated view towards the conservation of forest–grassland mosaics. Natureza & Conservação 12: 166169.Google Scholar
Luza, AL, Gonçalves, GL, Hartz, SM (2015) Phylogenetic and morphological relationships between nonvolant small mammals reveal assembly processes at different spatial scales. Ecology and Evolution 5: 889902.Google Scholar
Mello, MAR, Marquitti, FMD, Guimarães, PR Jr, Kalko, EKV, Jordano, P, de Aguiar, MM (2011a) The missing part of seed dispersal networks: structure and robustness of bat-fruit interactions. PLoS One 6: e17395.Google Scholar
Mello, MAR, Marquitti, FMD, Guimarães, PR Jr, Kalko, EKV, Jordano, P, de Aguiar, MM (2011b) The modularity of seed dispersal: differences in structure and robustness between bat– and bird–fruit networks. Oecologia 167: 131140.Google Scholar
Memmott, J, Waser, NM, Price, MV (2004) Tolerance of pollination networks to species extinctions. Proceedings of the Royal Society B 271: 26052611.Google Scholar
Moir, ML, Vesk, PA, Brennan, KEC, Keith, DA, Hughes, L, McCarthy, MA (2010) Current constraints and future directions in estimating coextinctions. Conservation Biology 24: 682690.Google Scholar
Morton, ES (1973) On the evolutionary advantages and disadvantages of fruit eating in tropical birds. The American Naturalist 107: 822.Google Scholar
Muller-Landau, HC, Hardesty, BD (2005) Seed dispersal of woody plants in tropical forests: concepts, examples and future directions. In: Biotic Interactions in the Tropics: Their Role in the Maintenance of Species Diversity, eds. DF Burslem, MA Pinard and SE Hartley, pp. 267309. Cambridge, UK: Cambridge University Press.Google Scholar
Müller, SC, Overbeck, GE, Pfadenhauer, J, Pillar, VD (2012) Woody species patterns at forest–grassland boundaries in southern Brazil. Flora – Morphology, Distribution, Functional Ecology of Plants 207: 586598.Google Scholar
Myster, RW (2012) Ecotones between Forest and Grassland. New York, NY, USA: Springer.Google Scholar
Overbeck, GE, Müller, SC, Fidelis, A, Pfadenhauer, J, Pillar, VD, Blanco, CC, Boldrini, II, Both, R, Forneck, ED (2007) Brazil’s neglected biome: the south Brazilian campos. Perspectives in Plant Ecology, Evolution and Systematics 9: 101116.Google Scholar
Overbeck, GE, Hermann, JM, Andrade, BO, Boldrini, II, Kiehl, K, Kirmer, A, Koch, C, et al. (2013) Restoration ecology in Brazil – time to step out of the forest. Natureza & Conservação 11: 9295.Google Scholar
Parr, CL, Lehmann, CER, Bond, WJ, Hoffmann, WA, Andersen, AN (2014) Tropical grassy biomes: misunderstood, neglected, and under threat. Trends in Ecology and Evolution 29: 205213.Google Scholar
Pascual, M, Dunne, JA (2006) Ecological Networks: Linking Structure to Dynamics in Food Webs. Oxford, UK: Oxford University Press.Google Scholar
Pillar, VD, Blanco, CC, Müller, SC, Sosinski, EE, Joner, F, Duarte, LDS (2013) Functional redundancy and stability in plant communities. Journal of Vegetation Science 24: 963974.Google Scholar
Pimm, SL, Jenkins, CN, Abell, R, Brooks, TM, Gittleman, JL, Joppa, LN, Raven, PH, Roberts, CM, Sexton, JO (2014) The biodiversity of species and their rates of extinction, distribution, and protection. Science 344: 1246752.Google Scholar
Pocock, MJ, Evans, DM, Memmott, J (2012) The robustness and restoration of a network of ecological networks. Science 335: 973977.Google Scholar
Poisot, T, Mouquet, N, Gravel, D (2013) Trophic complementarity drives the biodiversity–ecosystem functioning relationship in food webs. Ecology Letters 16: 853861.Google Scholar
Proulx, SR, Promislow, DE, Phillips, PC (2005) Network thinking in ecology and evolution. Trends in Ecology & Evolution 20: 345353.Google Scholar
Purvis, A, Gittleman, JL, Cowlishaw, G, Mace, GM (2000) Predicting extinction risk in declining species. Proceedings of the Royal Society of London B: Biological Sciences 267: 19471952.Google Scholar
R Core Team (2012) R: A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing, URL. http://www.R-project.org/ Google Scholar
Redding, DW, Hartmann, K, Mimoto, A, Bokal, D, DeVos, M, Mooers, (2008) Evolutionarily distinctive species often capture more phylogenetic diversity than expected. Journal of Theoretical Biology 251: 606615.Google Scholar
Rezende, EL, Lavabre, JE, Guimarães, PR, Jordano, P, Bascompte, J (2007) Non-random coextinctions in phylogenetically structured mutualistic networks. Nature 448: 925928.Google Scholar
Reynolds, JD, Dulvy, NK, Goodwin, NB, Hutchings, JA (2005) Biology of extinction risk in marine fishes. Proceedings of the Royal Society of London B: Biological Sciences 272: 23372344.Google Scholar
Richmond, CE, Breitburg, DL, Rose, KA (2005) The role of environmental generalist species in ecosystem function. Ecological Modelling 188: 279295.Google Scholar
Rosenfeld, JS (2002) Functional redundancy in ecology and conservation. Oikos 98: 156162.Google Scholar
Santamaría, L, Rodríguez-Gironés, MA (2007) Linkage rules for plant–pollinator networks: trait complementarity or exploitation barriers? PLoS Biology 5: e31.Google Scholar
Säterberg, T, Sellman, S, Ebenman, B (2013) High frequency of functional extinctions in ecological networks. Nature 499: 468470.Google Scholar
Scherber, C, Eisenhauer, N, Weisser, WW, Schmid, B, Voigt, W, Fischer, M, Schulze, E, et al. (2010) Bottom-up effects of plant diversity on multitrophic interactions in a biodiversity experiment. Nature 468: 553556.Google Scholar
Schleuning, M, Fründ, J, Schweiger, O, Welk, E, Albrecht, J, Albrecht, M, Beil, MN, et al. (2016) Ecological networks are more sensitive to plant than to animal extinction under climate change. Nature Communications 7: 13965.Google Scholar
Schwartz, D, Foresta, H, Mariotti, X, Balesdent, J, Massimba, JP, Girardin, C (1996) Present dynamics of the savanna–forest boundary in the Congolese Mayombe: a pedological, botanical and isotopic (13C and 14C) study. Oecologia 106: 516524.Google Scholar
Snow, DW (1971) Evolutionary aspects of fruit‐eating by birds. Ibis 113: 194202.Google Scholar
Solé, RV, Montoya, M (2001) Complexity and fragility in ecological networks. Proceedings of the Royal Society of London B: Biological Sciences 268: 20392045.Google Scholar
Srinivasan, UT, Dunne, JA, Harte, J, Martinez, ND (2007) Response of complex food webs to realistic extinction sequences. Ecology 88: 671682.Google Scholar
Timóteo, S, Ramos, JA, Vaughan, IP, Memmott, J (2016) High resilience of seed dispersal webs highlighted by the experimental removal of the dominant disperser. Current Biology 26: 910915.Google Scholar
Trakhtenbrot, A, Nathan, R, Perry, G, Richardson, DM (2005) The importance of long‐distance dispersal in biodiversity conservation. Diversity and Distributions 11: 173181.Google Scholar
Valiente‐Banuet, A, Aizen, MA, Alcántara, JM, Arroyo, J, Cocucci, A, Galetti, M, García, MB, et al. (2015) Beyond species loss: the extinction of ecological interactions in a changing world. Functional Ecology 29: 299307.Google Scholar
Vieira, MC, Cianciaruso, MV, Almeida-Neto, M (2013) Plant–pollinator coextinctions and the loss of plant functional and phylogenetic diversity. PLoS One 8: e81242.Google Scholar
Vieira, MC, Almeida‐Neto, M (2014) A simple stochastic model for complex coextinctions in mutualistic networks: robustness decreases with connectance. Ecology Letters 18: 144152.Google Scholar
Vizentin-Bugoni, J, Maruyama, PK, 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 of London B: Biological Sciences 281: 20132397.Google Scholar
Wheelwright, NT (1985) Fruit-size, gape width, and the diets of fruit-eating birds. Ecology 66: 808818.Google Scholar
White, R, Murray, S, Rohweder, M (2000) Pilot Analysis of Global Ecosystems: Grasslands Ecosystems. Washington, DC, USA: World Resource Institute.Google Scholar
Wunderle, JM Jr (1997) The role of animal seed dispersal in accelerating native forest regeneration on degraded tropical lands. Forest Ecology and Management 99: 223235.Google Scholar