Oecologia

, 167:131

The modularity of seed dispersal: differences in structure and robustness between bat– and bird–fruit networks

  • Marco Aurelio Ribeiro Mello
  • Flávia Maria Darcie Marquitti
  • Paulo R. GuimarãesJr.
  • Elisabeth Klara Viktoria Kalko
  • Pedro Jordano
  • Marcus Aloizio Martinez de Aguiar
Plant-Animal interactions - Original Paper

Abstract

In networks of plant–animal mutualisms, different animal groups interact preferentially with different plants, thus forming distinct modules responsible for different parts of the service. However, what we currently know about seed dispersal networks is based only on birds. Therefore, we wished to fill this gap by studying bat–fruit networks and testing how they differ from bird–fruit networks. As dietary overlap of Neotropical bats and birds is low, they should form distinct mutualistic modules within local networks. Furthermore, since frugivory evolved only once among Neotropical bats, but several times independently among Neotropical birds, greater dietary overlap is expected among bats, and thus connectance and nestedness should be higher in bat–fruit networks. If bat–fruit networks have higher nestedness and connectance, they should be more robust to extinctions. We analyzed 1 mixed network of both bats and birds and 20 networks that consisted exclusively of either bats (11) or birds (9). As expected, the structure of the mixed network was both modular (M = 0.45) and nested (NODF = 0.31); one module contained only birds and two only bats. In 20 datasets with only one disperser group, bat–fruit networks (NODF = 0.53 ± 0.09, C = 0.30 ± 0.11) were more nested and had a higher connectance than bird–fruit networks (NODF = 0.42 ± 0.07, C = 0.22 ± 0.09). Unexpectedly, robustness to extinction of animal species was higher in bird–fruit networks (R = 0.60 ± 0.13) than in bat–fruit networks (R = 0.54 ± 0.09), and differences were explained mainly by species richness. These findings suggest that a modular structure also occurs in seed dispersal networks, similar to pollination networks. The higher nestedness and connectance observed in bat–fruit networks compared with bird–fruit networks may be explained by the monophyletic evolution of frugivory in Neotropical bats, among which the diets of specialists seem to have evolved from the pool of fruits consumed by generalists.

Keywords

Complex networks Ecosystem services Food webs Guilds Mutualisms 

Supplementary material

442_2011_1984_MOESM1_ESM.pdf (108 kb)
Supplementary material 1 (PDF 107 kb)
442_2011_1984_MOESM2_ESM.pdf (12.6 mb)
Supplementary material 2 (PDF 12944 kb)

References

  1. Almeida-Neto M, Guimarães PR, Guimarães PR Jr, Loyola RD, Ulrich W (2008) A consistent metric for nestedness analysis in ecological systems: reconciling concept and measurement. Oikos 117:1227–1239CrossRefGoogle Scholar
  2. Bascompte J (2009) Disentangling the web of life. Science 325:416–419PubMedCrossRefGoogle 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, Melian CJ, Olesen JM (2003) The nested assembly of plant–animal mutualistic networks. Proc Natl Acad Sci USA 100:9383–9387PubMedCrossRefGoogle Scholar
  5. Bastolla U, Fortuna MA, Pascual-Garcia A, Ferrera A, Luque B, Bascompte J (2009) The architecture of mutualistic networks minimizes competition and increases biodiversity. Nature 458:U1018–U1091CrossRefGoogle Scholar
  6. Batagelj V, Mrvar A (1998) Pajek–a program for large network analysis. Connections 21:47–57Google Scholar
  7. Bezerra ELS, Machado ICS, Mello MAR (2009) Pollination networks of oil-flowers: a tiny world within the smallest of all worlds. J Anim Ecol 78:1096–1101PubMedCrossRefGoogle Scholar
  8. Blondel J (2003) Guilds or functional groups: does it matter? Oikos 100:223–231CrossRefGoogle Scholar
  9. Blüthgen N, Menzel F, Blüthgen N (2006) Measuring specialization in species interaction networks. BMC Ecology 6:1–12CrossRefGoogle Scholar
  10. Blüthgen N, Menzel F, Hovestadt T, Fiala B, Bluthgen N (2007) Specialization, constraints, and conflicting interests in mutualistic networks. Curr Biol 17:341–346PubMedCrossRefGoogle Scholar
  11. Blüthgen N, Frund J, Vazquez DP, Menzel F (2008) What do interaction network metrics tell us about specialization and biological traits? Ecology 89:3387–3399PubMedCrossRefGoogle Scholar
  12. Boucher DH, James S, Keeler KH (1982) The ecology of mutualism. Annu Rev Ecol Syst 13:315–347CrossRefGoogle Scholar
  13. Burgos E, Ceva H, Perazzo RPJ, Devoto M, Medan D, Zimmermann M, MarÌa Delbue A (2007) Why nestedness in mutualistic networks? J Theor Biol 249:307–313PubMedCrossRefGoogle Scholar
  14. Cazetta E, Schaefer H, Galetti M (2009) Why are fruits colorful? The relative importance of achromatic and chromatic contrasts for detection by birds. Evol Ecol 23:233–244CrossRefGoogle Scholar
  15. Cipollini ML, Levey DJ (1997) Why are some fruits toxic? Glykoalkaloids in Solanum and fruit choice by vertebrates. Ecology 78:782–798Google Scholar
  16. Datzmann T, von Helversen O, Mayer F (2010) Evolution of nectarivory in phyllostomid bats (phyllostomidae gray, 1825, chiroptera: mammalia). BMC Evol Biol 10:165PubMedCrossRefGoogle Scholar
  17. Dormann CF, Gruber B, Fründ J (2008) Introducing the bipartite package: analyzing ecological networks. R News 8:8–11Google Scholar
  18. Dormann CF, Fründ J, Blüthgen N, Gruber B (2009) Indices, graphs and null models: analyzing bipartite ecological networks. Open Ecol J 2:7–24CrossRefGoogle Scholar
  19. Fleming TH, Sosa VJ (1994) Effects of nectarivorous and frugivorous mammals on reproductive success of plants. J Mammal 75:845–851CrossRefGoogle Scholar
  20. Fleming TH, Breitwisch R, Whitesides GH (1987) Patterns of tropical vertebrate frugivore diversity. Annu Rev Ecol Syst 18:91–109CrossRefGoogle Scholar
  21. Fonseca CR, Ganade G (1996) Asymmetries, compartments and null interactions in an Amazonian ant–plant community. J Anim Ecol 66:339–347CrossRefGoogle Scholar
  22. 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 79:811–817PubMedGoogle Scholar
  23. Galindo-Gonzáles J, Guevara S, Sosa VJ (2000) Bat and bird-generated seed rains at isolated trees in pastures in a tropical rainforest. Conserv Biol 14:1693–1703CrossRefGoogle Scholar
  24. Guimaraes PR, Rico-Gray V, Oliveira PS, Izzo TJ, dos Reis SF, Thompson JN (2007) Interaction intimacy affects structure and coevolutionary dynamics in mutualistic networks. Curr Biol 17:1797–1803PubMedCrossRefGoogle Scholar
  25. Guimarães 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 249:181–189PubMedCrossRefGoogle Scholar
  26. Guimerà R, Amaral LAN (2005) Cartography of complex networks: modules and universal roles. J Stat Mech Theory Exp P02001Google Scholar
  27. Howe HF, Smallwood J (1982) Ecology of seed dispersal. Annu Rev Ecol Syst 13:201–228CrossRefGoogle Scholar
  28. Jordano P (1987) Patterns of mutualistic interactions in pollination and seed dispersal—connectance, dependence asymmetries, and coevolution. Am Nat 129:657–677CrossRefGoogle Scholar
  29. Jordano P, Bascompte J, Olesen JM (2003) Invariant properties in coevolutionary networks of plant–animal interactions. Ecol Lett 6:69–81CrossRefGoogle Scholar
  30. Jordano P, Vázquez D, Bascompte J (2009) Redes complejas de interacciones mutualistas planta–animal. In: Medel R, Aizen M, Zamora R (eds) Ecología y evolución de interacciones planta–animal. Editorial Universitaria, Santiago, pp 17–41Google Scholar
  31. Kalko EKV, Ayasse M (2009) Study and analysis of odor involved in behavioral ecology of bats. In: Kunz TH, Parsons S (eds) Ecological and behavioral methods for the study of bats, 2nd edn. The Johns Hopkins University Press, Baltimore, pp 491–499Google Scholar
  32. Kissling WD, Gaese KB, Jetz W (2009) The global distribution of frugivory in birds. Glob Ecol Biogeogr 18:150–162CrossRefGoogle Scholar
  33. Korine C, Kalko EKV, Herre EA (2000) Fruit removal by bats and birds from a community of strangler figs in Panama. Oecologia 123:560–568CrossRefGoogle Scholar
  34. Levey DJ, Silva WR, Galetti M (2002) Seed dispersal and frugivory : ecology, evolution, and conservation. CABI Publishing, New YorkGoogle Scholar
  35. Lobova TA, Geiselman CK, Mori SA (2009) Seed dispersal by bats in the Neotropics. New York Botanical Garden Press, New YorkGoogle Scholar
  36. Melo FPL, Rodriguez-Herrera B, Chazdon RL, Medellin RA, Ceballos GG (2009) Small tent-roosting bats promote dispersal of large-seeded plants in a Neotropical forest. Biotropica 41:737–743CrossRefGoogle Scholar
  37. Mills LS, Soule ME, Doak DF (1993) The keystone-species concept in ecology and conservation. Bioscience 43:219–224CrossRefGoogle Scholar
  38. Muscarella R, Fleming TH (2007) The role of frugivorous bats in tropical forest succession. Biol Rev 82:573–590PubMedCrossRefGoogle Scholar
  39. Nogueira MR, Peracchi AL (2003) Fig-seed predation by 2 species of Chiroderma: discovery of a new feeding strategy in bats. J Mammal 84:225–233CrossRefGoogle Scholar
  40. Nooy W, Mrvar A, Batagelj V (2005) Exploratory social network analysis with Pajek. Cambridge University Press, New YorkGoogle Scholar
  41. Olesen JM, Bascompte J, Dupont YL, Jordano P (2006) The smallest of all worlds: pollination networks. J Theor Biol 240:270–276PubMedCrossRefGoogle Scholar
  42. Olesen JM, Bascompte J, Dupont YL, Jordano P (2007) The modularity of pollination networks. Proc Natl Acad Sci USA 104:19891–19896PubMedCrossRefGoogle Scholar
  43. Oliver TH, Leather SR, Cook JM (2008) Macroevolutionary patterns in the origin of mutualisms involving ants. J Evol Biol 21:1597–1608PubMedCrossRefGoogle Scholar
  44. Root RB (1967) The niche exploitation pattern of the blue-gray gnatcatcher. Ecol Monogr 37:317–350CrossRefGoogle Scholar
  45. Scheffer M, Bascompte J, Brock WA, Brovkin V, Carpenter SR, Dakos V, Held H, van Nes EH, Rietkerk M, Sugihara G (2009) Early-warning signals for critical transitions. Nature 461:53–59PubMedCrossRefGoogle Scholar
  46. Terborgh J, Pitman N, Silman M, Schichter H, Núñes VP (2002) Maintenance of tree diversity in tropical forests. In: Levey DJ, Silva WR, Galetti M (eds) Seed dispersal and frugivory : ecology, evolution, and conservation. CABI Publishing, New York, pp 1–17Google Scholar
  47. Thies W, Kalko EKV (2004) Phenology of Neotropical pepper plants (Piperaceae) and their association with their main dispersers, two short-tailed fruit bats, Carollia perspicillata and C. castanea (Phyllostomidae). Oikos 104:362–376CrossRefGoogle Scholar
  48. van der Pijl L (1972) Principles of dispersal in higher plants. Springer, BerlinGoogle Scholar
  49. Walker BH (1992) Biodiversity and ecological redundancy. Conserv Biol 6:18–23CrossRefGoogle Scholar
  50. Watts DJ, Strogatz SH (1998) Collective dynamics of small-world networks. Nature 393:440–442PubMedCrossRefGoogle Scholar
  51. Wendeln MC, Runkle JR, Kalko EKV (2000) Nutritional values of 14 fig species and bat feeding preferences in Panama. Biotropica 32:489–501Google Scholar
  52. Wilmers CC, Sinha S, Brede M (2002) Examining the effects of species richness on community stability: an assembly model approach. Oikos 99:363–367CrossRefGoogle Scholar
  53. Wright SJ (2002) Plant diversity in tropical forests: a review of mechanisms of species coexistence. Oecologia 130:1–14Google Scholar

Copyright information

© Springer-Verlag 2011

Authors and Affiliations

  • Marco Aurelio Ribeiro Mello
    • 1
  • Flávia Maria Darcie Marquitti
    • 2
  • Paulo R. GuimarãesJr.
    • 3
    • 4
  • Elisabeth Klara Viktoria Kalko
    • 1
    • 5
  • Pedro Jordano
    • 4
  • Marcus Aloizio Martinez de Aguiar
    • 6
  1. 1.Institut für Experimentelle ÖkologieUniversität UlmUlmGermany
  2. 2.Programa de Pós-graduação em EcologiaUniversidade Estadual de CampinasCampinasBrazil
  3. 3.Departamento de EcologiaUniversidade de São PauloSão PauloBrazil
  4. 4.Integrative Ecology Group, Estación Biológica de Doñana, CSICSevillaSpain
  5. 5.Smithsonian Tropical Research InstituteBalboaRepublic of Panamá
  6. 6.Instituto de Física ‘Gleb Wataghin’Universidade Estadual de CampinasCampinasBrazil

Personalised recommendations