Oecologia

, Volume 176, Issue 3, pp 837–848 | Cite as

Functional importance of avian seed dispersers changes in response to human-induced forest edges in tropical seed-dispersal networks

  • Francisco Saavedra
  • Isabell Hensen
  • Stephan G. Beck
  • Katrin Böhning-Gaese
  • Denis Lippok
  • Till Töpfer
  • Matthias Schleuning
Community ecology - Original research

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.

Keywords

Ecosystem functioning Functional diversity Morphological traits Montane forest Plant–frugivore interactions 

Supplementary material

442_2014_3056_MOESM1_ESM.docx (129 kb)
Supplementary material 1 (DOCX 128 kb)

References

  1. 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 33:57–68Google Scholar
  2. Baayen RH, Davidson DJ, Bates DM (2008) Mixed-effects modeling with crossed random effects for subjects and items. J Mem Lang 59:390–412CrossRefGoogle Scholar
  3. Bascompte J, Jordano P (2007) Plant-animal mutualistic networks: the architecture of biodiversity. Annu Rev Ecol Evol Syst 38:567–593CrossRefGoogle Scholar
  4. Bascompte J, Jordano P, Olesen JM (2006) Asymmetric coevolutionary networks facilitate biodiversity maintenance. Science 312:431–433PubMedCrossRefGoogle Scholar
  5. Böhning-Gaese K, Caprano T, van Ewijk K, Veith M (2006) Range size: disentangling current traits and phylogenetic and biogeographic factors. Am Nat 167:555–567PubMedCrossRefGoogle Scholar
  6. 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 24:127–135PubMedCrossRefGoogle Scholar
  7. 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 168:425–437PubMedCrossRefGoogle Scholar
  8. Cadotte MW, Carscadden K, Mirotchnick N (2011) Beyond species: functional diversity and the maintenance of ecological processes and services. J Appl Ecol 48:1079–1087CrossRefGoogle Scholar
  9. Carlo TA, Yang S (2011) Network models of frugivory and seed dispersal: challenges and opportunities. Acta Oecol 37:619–624CrossRefGoogle Scholar
  10. Chapin FS III, Walker BH, Hobbs RJ, Hooper DU, Lawton JH, Sala OE, Tilman D (1997) Biotic control over the functioning of ecosystems. Science 277:500–504CrossRefGoogle Scholar
  11. Clapham AR (1936) Over-dispersion in grassland communities and the use of statistical methods in plant ecology. J Ecol 24:232–251CrossRefGoogle Scholar
  12. 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 112:137–148Google Scholar
  13. 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 91:793–801PubMedCrossRefGoogle Scholar
  14. Dormann C, Fründ J, Blüthgen N, Gruber B (2009) Indices graphs and null models: analyzing bipartite ecological networks. Open Ecol J 2:7–24CrossRefGoogle Scholar
  15. Dunning JB (2007) CRC handbook of avian body masses, 2nd edn. CRC, Boca Raton, FLCrossRefGoogle Scholar
  16. Eck S, Fiebig J, Fiedler W, Heynen BI, Nicolai T, Töpfer RV, Elzen D, Winkler R, Woog F (2011) Measuring birds. Vögelvermessen Deutsche Ornithologen, WilhelmshavenGoogle Scholar
  17. Eshiamwata GW, Berens DG, Bleher B, Dean WRJ, Böhning-Gaese K (2006) Bird assemblages in isolated Ficus trees in Kenyan farmland. J Trop Ecol 22:723–726CrossRefGoogle Scholar
  18. 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 111:269–273CrossRefGoogle Scholar
  19. 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 340:1086–1090PubMedCrossRefGoogle Scholar
  20. Gallegos CS, Hensen I, Schleuning M (2014) Secondary dispersal by ants promotes forest regeneration after deforestation. J Ecol 102:659–666CrossRefGoogle Scholar
  21. Gentry AH (1982) Patterns of Neotropical plant species diversity. Evol Biol 15:1–84CrossRefGoogle Scholar
  22. 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 46:89–120CrossRefGoogle Scholar
  23. Haskell JP, Ritchie ME, Olff H (2002) Fractal geometry predicts varying body size scaling relationships for mammal and bird home ranges. Nature 418:527–530PubMedCrossRefGoogle Scholar
  24. Hector A, Joshi J, Lawler S, Spehn EM, Wilby A (2001) Conservation implications of the link between biodiversity and ecosystem functioning. Oecologia 129:624–628PubMedCrossRefGoogle Scholar
  25. Henle K, Davies KF, Kleyer M, Margules C, Settele J (2004) Predictors of species sensitivity to fragmentation. Biodivers Conserv 13:207–251CrossRefGoogle Scholar
  26. 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 99:1100–1107CrossRefGoogle Scholar
  27. 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 40:27–40Google Scholar
  28. Howe HF, Smallwood J (1982) Ecology of seed dispersal. Annu Rev Ecol Syst 13:201–228CrossRefGoogle Scholar
  29. Jordano P (2000) Fruits and frugivory. In: Fenner M (ed) Seeds: the ecology of regeneration in plant communities, 2nd edn. CABI, Wallingford, pp 125–166Google Scholar
  30. Jordano P, García C, Godoy JA, García-Castaño JL (2007) Differential contribution of frugivores to complex seed dispersal patterns. Proc Natl Acad Sci 104:3278–3282PubMedCrossRefPubMedCentralGoogle Scholar
  31. 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 7:321–323PubMedCrossRefPubMedCentralGoogle Scholar
  32. 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 27:329–341CrossRefGoogle Scholar
  33. 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 23:9–24Google Scholar
  34. Laliberté E, Legendre P (2010) A distance-based framework for measuring functional diversity from multiple traits. Ecology 91:299–305PubMedCrossRefGoogle Scholar
  35. 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 278:2257–2264CrossRefGoogle Scholar
  36. 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 3:724–733Google Scholar
  37. 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 26:1072–1081PubMedCrossRefGoogle Scholar
  38. Mason NWH, Mouillot D, Lee WG, Wilson JB (2005) Functional richnessfunctional evenness and functional divergence : the primary components of functional diversity. Oikos 111:112–118CrossRefGoogle Scholar
  39. McGill BJ, Enquist BJ, Weiher E, Westoby M (2006) Rebuilding community ecology from functional traits. Trends Ecol Evol 21:178–185PubMedCrossRefGoogle Scholar
  40. Melo FPL, Lemire D, Tabarelli M (2007) Extirpation of large-seeded seedlings from the edge of a large Brazilian Atlantic forest fragment. Ecoscience 14:124–129CrossRefGoogle Scholar
  41. 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 121:1553–1566CrossRefGoogle Scholar
  42. 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 Google Scholar
  43. 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 24:867–876CrossRefGoogle Scholar
  44. Navarro G, Maldonado M (2002) Geografía ecológica de Bolivia: vegetación y ambientes acuáticos, 3rd edn. Centro de Ecología Difusión Simón I, PatiñoGoogle Scholar
  45. Perea R, Delibes M, Polko M, Suárez-Esteban A, Fedriani JM (2012) Context-dependent fruit-frugivore interactions: partner identities and spatio-temporal variations. Oikos 122:943–951CrossRefGoogle Scholar
  46. 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 94:1296–1306PubMedCrossRefGoogle Scholar
  47. R Development Core Team (2009) R: A language and environment for statistical computing. R Foundation for Statistical Computing, ViennaGoogle Scholar
  48. Santamaría L, Rodríguez-Gironés M (2007) Linkage rules for plant–pollinator networks: trait complementarity or exploitation barriers? PLoS Biol 5:354–362CrossRefGoogle Scholar
  49. 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 199–207Google Scholar
  50. 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 92:26–36PubMedCrossRefGoogle Scholar
  51. 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 17:454–463PubMedCrossRefGoogle Scholar
  52. Schulenberg TS, Stotz DF, Lane DF, O’Neill JP, Parker IIITA (2007) Birds of Peru. Princeton University Press, NJ, pp 5–656Google Scholar
  53. Schupp EW (1993) Quantity, quality and the effectiveness of seed dispersal by animals. Vegetatio 107(108):15–29Google Scholar
  54. Schupp EW, Jordano P, Gómez JM (2010) Seed dispersal effectiveness revisited: a conceptual review. New Phytol 188:333–353PubMedCrossRefGoogle Scholar
  55. Sodhi NS, Liow LH, Bazzaz FA (2004) Avian extinctions from tropical and subtropical forests. Annu Rev Ecol Evol Syst 35:323–345CrossRefGoogle Scholar
  56. 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 151:442–453PubMedCrossRefGoogle Scholar
  57. Tilman D (2001) Functional diversity. In: Levin SA (ed) Encyclopedia of Biodiversity. Academic Press, San Diego, CA, pp 109–120CrossRefGoogle Scholar
  58. Tylianakis JM, Tscharntke T, Lewis OT (2007) Habitat modification alters the structure of tropical host-parasitoid food webs. Nature 445:202–205PubMedCrossRefGoogle Scholar
  59. Tylianakis JM, Laliberté E, Nielsen A, Bascompte J (2010) Conservation of species interaction networks. Biol Conserv 143:2270–2279CrossRefGoogle Scholar
  60. Vanthomme H, Bellé B, Forget PM (2010) Bushmeat hunting alters recruitment of large-seeded plant species in Central Africa. Biotropica 42:672–679CrossRefGoogle Scholar
  61. Vázquez DP, Melián CJ, Williams NM, Blüthgen N, Krasnov BR, Poulin R (2007) Species abundance and asymmetric interaction strength in ecological networks. Oikos 116:1120–1127CrossRefGoogle Scholar
  62. Vázquez DP, Blüthgen N, Cagnolo L, Chacoff NP (2009) Uniting pattern and process in plant–animal mutualistic networks: a review. Ann Bot 103:1445–1457PubMedCrossRefPubMedCentralGoogle Scholar
  63. Villéger S, Mason NWH, Mouillot D (2008) New multidimensional functional diversity indices for a multifaceted framework in functional ecology. Ecology 89:2290–2301PubMedCrossRefGoogle Scholar
  64. Wang BC, Smith TB (2002) Closing the seed dispersal loop. Trends Ecol Evol 17:379–386CrossRefGoogle Scholar
  65. Wenny DG, Levey DJ (1998) Directed seed dispersal by bellbirds in a tropical cloud forest. Proc Natl Acad Sci USA 95:6204–6207PubMedCrossRefPubMedCentralGoogle Scholar
  66. Wheelwright NT (1985) Fruit size gape width and the diets of fruit eating birds. Ecology 66:808–818CrossRefGoogle Scholar
  67. Wheelwright NT (1993) Fruit size in a tropical tree species: variation, preference by birds, and heritability. Vegetatio 107:163–174Google Scholar
  68. 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 39:1973–1983CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2014

Authors and Affiliations

  • Francisco Saavedra
    • 1
    • 2
    • 3
  • Isabell Hensen
    • 1
  • Stephan G. Beck
    • 3
  • Katrin Böhning-Gaese
    • 2
    • 4
  • Denis Lippok
    • 1
  • Till Töpfer
    • 2
    • 5
    • 6
  • Matthias Schleuning
    • 2
  1. 1.Institute of Biology/Geobotany and Botanical GardenMartin Luther University Halle-WittenbergHalle (Saale)Germany
  2. 2.Biodiversity and Climate Research Centre (BiK-F) and Senckenberg Gesellschaft für NaturforschungFrankfurt (Main)Germany
  3. 3.Herbario Nacional de Bolivia, Instituto de EcologíaUniversidad Mayor de San AndresCorreo Central La PazBolivia
  4. 4.Institute for Ecology, Evolution and DiversityGoethe University FrankfurtFrankfurt (Main)Germany
  5. 5.Zoological Research Museum Alexander KoenigBonnGermany
  6. 6.Senckenberg Naturhistorische SammlungenMuseum für TierkundeDresdenGermany

Personalised recommendations