Abstract
Although seed-dispersal networks are increasingly used to infer the functioning of ecosystems, few studies have investigated the link between the properties of these networks and the ecosystem function of seed dispersal by animals. We investigate how frugivore communities and seed dispersal change with habitat disturbance and test whether relationships between morphological traits and functional roles of seed dispersers change in response to human-induced forest edges. We recorded interaction frequencies between fleshy fruited plants and frugivorous bird species in tropical montane forests in the Bolivian Andes and recorded functional bird traits (body mass, gape width and wing tip length) associated with quantitative (seed-removal rate) and qualitative (seed-deposition pattern) components of seed-dispersal effectiveness. We found that the abundance and richness of frugivorous birds were higher at forest edges. More fruits were removed and dispersed seeds were less clustered at edges than in the interior. Additionally, functional and interaction diversity were higher at edges than in the interior, but functional and interaction evenness did not differ. Interaction strength of bird species increased with body mass, gape width and wing tip length in the forest interior, but was not related to bird morphologies at forest edges. Our study suggests that increases in functional and interaction diversity and an even distribution of interaction strength across bird morphologies lead to enhanced quantity and tentatively enhanced quality of seed dispersal. It also suggests that the effects of species traits on ecosystem functions can vary along small-scale gradients of human disturbance.
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References
Alberti LF, Morellato LPC (2010) Variation on fruit production of Nectandra megapotamica (Lauraceae) trees on the edge and interior of a semideciduous forest—a case study. Naturalia 33:57–68
Baayen RH, Davidson DJ, Bates DM (2008) Mixed-effects modeling with crossed random effects for subjects and items. J Mem Lang 59:390–412
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, Olesen JM (2006) Asymmetric coevolutionary networks facilitate biodiversity maintenance. Science 312:431–433
Böhning-Gaese K, Caprano T, van Ewijk K, Veith M (2006) Range size: disentangling current traits and phylogenetic and biogeographic factors. Am Nat 167:555–567
Bolker BM, Brooks ME, Clark CJ, Geange SW, Poulsen JR, Stevens MH, White JS (2009) Generalized linear mixed models: a practical guide for ecology and evolution. Trends Ecol Evol 24:127–135
Breitbach N, Tillmann S, Schleuning M, Grünewald C, Laube I, Steffan-Dewenter I, Böhning-Gaese K (2012) Influence of habitat complexity and landscape configuration on pollination and seed-dispersal interactions of wild cherry trees. Oecologia 168:425–437
Cadotte MW, Carscadden K, Mirotchnick N (2011) Beyond species: functional diversity and the maintenance of ecological processes and services. J Appl Ecol 48:1079–1087
Carlo TA, Yang S (2011) Network models of frugivory and seed dispersal: challenges and opportunities. Acta Oecol 37:619–624
Chapin FS III, Walker BH, Hobbs RJ, Hooper DU, Lawton JH, Sala OE, Tilman D (1997) Biotic control over the functioning of ecosystems. Science 277:500–504
Clapham AR (1936) Over-dispersion in grassland communities and the use of statistical methods in plant ecology. J Ecol 24:232–251
de Castro ER, Cortes MC, Navarro L, Galetti M, Morellato LPC (2012) Temporal variation in the abundance of two species of thrushes in relation to fruiting phenology in the Atlantic rainforest. EMU Austral Ornithol 112:137–148
Díaz-Castelazo C, Guimarāes PR, Jordano P, Thompson JN, Marquis RJ, Rico-Gray V (2010) Changes of a mutualistic network over time: reanalysis over a 10-year period. Ecology 91:793–801
Dormann C, Fründ J, Blüthgen N, Gruber B (2009) Indices graphs and null models: analyzing bipartite ecological networks. Open Ecol J 2:7–24
Dunning JB (2007) CRC handbook of avian body masses, 2nd edn. CRC, Boca Raton, FL
Eck S, Fiebig J, Fiedler W, Heynen BI, Nicolai T, Töpfer RV, Elzen D, Winkler R, Woog F (2011) Measuring birds. Vögelvermessen Deutsche Ornithologen, Wilhelmshaven
Eshiamwata GW, Berens DG, Bleher B, Dean WRJ, Böhning-Gaese K (2006) Bird assemblages in isolated Ficus trees in Kenyan farmland. J Trop Ecol 22:723–726
Galetti M, Alves-Costa CP, Cazetta E (2003) Effects of forest fragmentation, anthropogenic edges and fruit colour on the consumption of ornithocoric fruits. Biol Conserv 111:269–273
Galetti M, Guevara R, Côrtes MC, Fadini R, Von Matter S, Leite AB, Labecca F, Ribeiro T, Carvalho CS, Collevatti RG, Pires MM, Guimaraes PR Jr, Brancalion PH, Ribeiro MC, Jordano P (2013) Functional extinction of birds drives rapid evolutionary changes in seed size. Science 340:1086–1090
Gallegos CS, Hensen I, Schleuning M (2014) Secondary dispersal by ants promotes forest regeneration after deforestation. J Ecol 102:659–666
Gentry AH (1982) Patterns of Neotropical plant species diversity. Evol Biol 15:1–84
Hagen M, Kissling WD, Rasmussen C, De Aguilar Marcus AM, Brown LL, Carstensen DW, Alves-Dos Santos I, Dupont YL, Edwards FK, Genini J, Guimarães PR, Jenkins GD, Jordano P (2012) Biodiversity species interactions and ecological networks in a fragmented world. Adv Ecol Res 46:89–120
Haskell JP, Ritchie ME, Olff H (2002) Fractal geometry predicts varying body size scaling relationships for mammal and bird home ranges. Nature 418:527–530
Hector A, Joshi J, Lawler S, Spehn EM, Wilby A (2001) Conservation implications of the link between biodiversity and ecosystem functioning. Oecologia 129:624–628
Henle K, Davies KF, Kleyer M, Margules C, Settele J (2004) Predictors of species sensitivity to fragmentation. Biodivers Conserv 13:207–251
Herrera JM, Morales JM, García D (2011) Differential effects of fruit availability and habitat cover for frugivore-mediated seed dispersal in a heterogeneous landscape. J Ecol 99:1100–1107
Herzog SK, Soria Auza RW, Hennessey B (2005) Patrones ecorregionales de riqueza, endemismo y amenaza de la avifauna boliviana: prioridades para la planificación ecorregional. Ecol Bol 40:27–40
Howe HF, Smallwood J (1982) Ecology of seed dispersal. Annu Rev Ecol Syst 13:201–228
Jordano P (2000) Fruits and frugivory. In: Fenner M (ed) Seeds: the ecology of regeneration in plant communities, 2nd edn. CABI, Wallingford, pp 125–166
Jordano P, García C, Godoy JA, García-Castaño JL (2007) Differential contribution of frugivores to complex seed dispersal patterns. Proc Natl Acad Sci 104:3278–3282
Jordano P, Forget PM, Lambert JE, Böhning-Gaese K, Traveset A, Wright SJ (2011) Frugivores and seed dispersal: mechanisms and consequences for biodiversity of a key ecological interaction. Biol Lett 7:321–323
Junker RR, Blüthgen N, Brehm T, Binkenstein J, Paulus J, Martin Schaefer H, Stang M (2013) Specialization on traits as basis for the niche-breadth of flower visitors and as structuring mechanism of ecological networks. Funct Ecol 27:329–341
Karubian J, Browne L, Bosque C, Carlo T, Galetti M, Loiselle BA, Blake JG, Cabrera D, Durães R, Labecca FM, Hobrook KM, Holland R, Jetz W, Kümmenth F, Olivo J, Ottewell K, Papadakis G, Rivas G, Steiger S, Voirin B, Wikelski M (2012) Seed dispersal by Neotropical birds: emerging patterns and underlying processes. Ornitol Neotrop 23:9–24
Laliberté E, Legendre P (2010) A distance-based framework for measuring functional diversity from multiple traits. Ecology 91:299–305
Lenz J, Fiedler W, Caprano T, Friedrichs W, Gaese BH, Wikelski M, Böhning-Gaese K (2011) Seed-dispersal distributions by trumpeter hornbills in fragmented landscapes. Proc R Soc B Biol Sci 278:2257–2264
Lippok D, Beck S, Renison D, Hensen I, Apaza A, Schleuning M (2013) Topography and edge effects are more important than elevation as drivers of vegetation patterns in a Neotropical montane forest. J Veg Sci 3:724–733
Markl JS, Schleuning M, Forget PM, Jordano P, Lambert JE, Traveset A, Wright SJ, Böhning-Gaese K (2012) Meta-analysis of the effects of human disturbance on seed dispersal by animals. Conserv Biol 26:1072–1081
Mason NWH, Mouillot D, Lee WG, Wilson JB (2005) Functional richnessfunctional evenness and functional divergence : the primary components of functional diversity. Oikos 111:112–118
McGill BJ, Enquist BJ, Weiher E, Westoby M (2006) Rebuilding community ecology from functional traits. Trends Ecol Evol 21:178–185
Melo FPL, Lemire D, Tabarelli M (2007) Extirpation of large-seeded seedlings from the edge of a large Brazilian Atlantic forest fragment. Ecoscience 14:124–129
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
Morales JM, García D, Martínez D, Rodriguez-Pérez J, Herrera JM (2013) Frugivore behavioural details matter for seed dispersal: a multi-species model for Cantabrian thrushes and trees. PLoS ONE. doi:10.1371/journal.pone.0065216
Mouchet MA, Villéger S, Mason NWH, Mouillot D (2010) Functional diversity measures: an overview of their redundancy and their ability to discriminate community assembly rules. Funct Ecol 24:867–876
Navarro G, Maldonado M (2002) Geografía ecológica de Bolivia: vegetación y ambientes acuáticos, 3rd edn. Centro de Ecología Difusión Simón I, Patiño
Perea R, Delibes M, Polko M, Suárez-Esteban A, Fedriani JM (2012) Context-dependent fruit-frugivore interactions: partner identities and spatio-temporal variations. Oikos 122:943–951
Plein M, Längsfeld L, Neuschulz EL, Schultheiß C, Ingmann L, Töpfer T, Böhning-Gaese K, Schleuning M (2013) Constant properties of plant–frugivore networks despite fluctuations in fruit and bird communities in space and time. Ecology 94:1296–1306
R Development Core Team (2009) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna
Santamaría L, Rodríguez-Gironés M (2007) Linkage rules for plant–pollinator networks: trait complementarity or exploitation barriers? PLoS Biol 5:354–362
Schawe M, Gerold G, Bach K, Gradstein S (2010) Hydrometeorological patterns in relation to montane forest types along an elevational gradient in the Yungas of Bolivia. In: Bruijnzeel LA, Scatena FN, Hamilton LS (eds) Tropical montane cloud forest: science for conservation and management. Cambridge University Press, Cambridge, pp 199–207
Schleuning M, Blüthgen N, Flörchinger M, Braun J, Schaefer HM, Böhning-Gaese K (2011) Specialization and interaction strength in a tropical plant-frugivore network differ among forest strata. Ecology 92:26–36
Schleuning M, Ingmann L, Strauß R, Fritz SA, Dalsgaard B, Dehling DM, Plein M, Saavedra F, Sandel B, Svenning JC, Böhning-Gaese K, Dormann CF (2014) Ecological, historical and evolutionary determinants of modularity in weighted seed-dispersal networks. Ecol Lett 17:454–463
Schulenberg TS, Stotz DF, Lane DF, O’Neill JP, Parker IIITA (2007) Birds of Peru. Princeton University Press, NJ, pp 5–656
Schupp EW (1993) Quantity, quality and the effectiveness of seed dispersal by animals. Vegetatio 107(108):15–29
Schupp EW, Jordano P, Gómez JM (2010) Seed dispersal effectiveness revisited: a conceptual review. New Phytol 188:333–353
Sodhi NS, Liow LH, Bazzaz FA (2004) Avian extinctions from tropical and subtropical forests. Annu Rev Ecol Evol Syst 35:323–345
Stang M, Klinkhamer P, Van der Meijden E (2007) Asymmetric specialization and extinction risk in plant-flower visitor webs: a matter of morphology or abundance? Oecologia 151:442–453
Tilman D (2001) Functional diversity. In: Levin SA (ed) Encyclopedia of Biodiversity. Academic Press, San Diego, CA, pp 109–120
Tylianakis JM, Tscharntke T, Lewis OT (2007) Habitat modification alters the structure of tropical host-parasitoid food webs. Nature 445:202–205
Tylianakis JM, Laliberté E, Nielsen A, Bascompte J (2010) Conservation of species interaction networks. Biol Conserv 143:2270–2279
Vanthomme H, Bellé B, Forget PM (2010) Bushmeat hunting alters recruitment of large-seeded plant species in Central Africa. Biotropica 42:672–679
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, Blüthgen N, Cagnolo L, Chacoff NP (2009) Uniting pattern and process in plant–animal mutualistic networks: a review. Ann Bot 103:1445–1457
Villéger S, Mason NWH, Mouillot D (2008) New multidimensional functional diversity indices for a multifaceted framework in functional ecology. Ecology 89:2290–2301
Wang BC, Smith TB (2002) Closing the seed dispersal loop. Trends Ecol Evol 17:379–386
Wenny DG, Levey DJ (1998) Directed seed dispersal by bellbirds in a tropical cloud forest. Proc Natl Acad Sci USA 95:6204–6207
Wheelwright NT (1985) Fruit size gape width and the diets of fruit eating birds. Ecology 66:808–818
Wheelwright NT (1993) Fruit size in a tropical tree species: variation, preference by birds, and heritability. Vegetatio 107:163–174
Wotton DM, Kelly D (2012) Do larger frugivores move seeds further? Body size, seed dispersal distance, and a case study of a large, sedentary pigeon. J Biogeogr 39:1973–1983
Acknowledgments
We are grateful to Rodrigo Calvimontes, Fabrizzio Peralta, and especially to Veronica Avalos, for their help during fieldwork, to the staff of the Herbario Nacional de Bolivia for their help with the identification of plant species and to R. van den Elzen (Zoologisches Forschungsmuseum Alexander Koenig, Bonn), R. Prŷs-Jones and M. P. Adams (Natural History Museum, Tring), G. Mayr (Senckenberg Museum, Frankfurt/M.) and R. Winkler (Naturhistorisches Museum, Basel) for providing access to the bird collections kept in their charge. M. Hennen, J. Bates and D. Willard [Field Museum of Natural History (FMNH), Chicago] sent specimens, and J. V. Remsen and S. W. Cardiff (Louisiana State University Museum of Natural Science, Baton Rouge) and D. Willard (FMNH, Chicago) provided additional measurements. We also thank R. Diesener, S. Frahnert, C. Bracker, P. R. Becker, J. Fjeldså, N. Krabbe and J. Mlíkovsky for information about collection holdings. The study was funded by the German Science Foundation (Deutsche Forschungsgemeinschaft) (HE2041/20-1). M. S. was also supported by the research funding program Landes-Offensive zur Entwicklung Wissenschaftlich-ökonomischer Exzellenz of Hesse’s Ministry of Higher Education, Research and the Arts. This study was done under permission and current laws of the government of Bolivia.
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Communicated by Joanna E. Lambert.
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Saavedra, F., Hensen, I., Beck, S.G. et al. Functional importance of avian seed dispersers changes in response to human-induced forest edges in tropical seed-dispersal networks. Oecologia 176, 837–848 (2014). https://doi.org/10.1007/s00442-014-3056-x
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DOI: https://doi.org/10.1007/s00442-014-3056-x