Network structure embracing mutualism–antagonism continuums increases community robustness

Abstract

Theory predicts that contrasting properties of mutualistic and antagonistic networks differentially promote community resilience to species loss. However, the outcome of most ecological interactions falls within a continuum between mutualism and antagonism, and we ignore the extent to which this interactions’ continuum might influence community stability. Using a large data set of interactions, we compared co-extinction cascades that either consider or ignore the mix of beneficial and detrimental actions that parrots exert on plants. When the antagonism–mutualism continuum was considered, a combination of the properties that separately enhance community stability in ecological networks emerged. This combination of properties led to an overall increase of the parrot community robustness to face plant species loss. Our results highlight that the conditional outcomes of interactions can influence the structure of ecological networks, thus affecting our predictions of community stability against eventual changes.

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Fig. 1: Trophic network of parrot species feeding on plant species.
Fig. 2: Odds ratio estimates and confidence intervals (95%) extracted from the generalized linear models that assess the plant functional traits explaining each module.
Fig. 3: Simulations of parrot co-extinction rates triggered by plant species removal based on the observed trophic network.
Fig. 4: Simulations of parrot co-extinction rates triggered by plant species removal.
Fig. 5: Pictures of various antagonistic and mutualistic interactions recorded during fieldwork.

References

  1. 1.

    Bronstein, J. L. Conditional outcomes in mutualistic interactions. Trends Ecol. Evol. 9, 214–217 (1994).

  2. 2.

    Thompson, J. N. The Coevolutionary Process (Univ. Chicago Press, Chicago, 1994).

  3. 3.

    Thompson, J. N. The Geographic Mosaic of Coevolution (Univ. Chicago Press, Chicago, 2005).

  4. 4.

    Bascompte, J. & Jordano, P. Mutualistic Networks (Princeton Univ. Press, Princeton, 2014).

  5. 5.

    Shantz, A., Lemoine, N. & Burkepile, D. Nutrient loading alters the performance of key nutrient exchange mutualisms. Ecol. Lett. 19, 20–28 (2016).

  6. 6.

    Morris, W. F. et al. Direct and interactive effects of enemies and mutualists on plant performance: a meta-analysis. Ecology 88, 1021–1029 (2007).

  7. 7.

    Larimer, A. L., Bever, J. D. & Clay, K. The interactive effects of plant microbial symbionts: a review and meta-analysis. Symbiosis 51, 139–148 (2010).

  8. 8.

    Chamberlain, S. A., Bronstein, J. L. & Rudgers, J. A. How context dependent are species interactions? Ecol. Lett. 17, 881–890 (2014).

  9. 9.

    Blanco, G., Tella, J. L., Potti, J. & Baz, A. Feather mites on birds: costs of parasitism or conditional outcomes? J. Avian Biol. 32, 271–274 (2001).

  10. 10.

    Maruyama, P. K., Vizentin-Bugoni, J., Dalsgaard, B., Sazima, I. & Sazima, M. Nectar robbery by a hermit hummingbird: association to floral phenotype and its influence on flowers and network structure. Oecologia 178, 783–793 (2015).

  11. 11.

    Mougi, A. & Kondoh, M. Diversity of interaction types and ecological community stability. Science 337, 349–351 (2012).

  12. 12.

    Yoshikawa, T. & Isagi, Y. Determination of temperate bird-flower interactions as entangled mutualistic and antagonistic sub-networks: characterization at the network and species levels. J. Anim. Ecol. 83, 651–660 (2014).

  13. 13.

    Fleming, T. H. & Kress, W. J. The Ornaments of Life: Coevolution and Conservation in the Tropics (Univ. Chicago Press, Chicago, 2013).

  14. 14.

    Heleno, R. H., Olesen, J. M., Nogales, M., Vargas, P. & Traveset, A. Seed dispersal networks in the Galápagos and the consequences of alien plant invasions. Proc. R. Soc. B 280, 20122112 (2013).

  15. 15.

    Bronstein, J. L. in Insect–Plant Interactions Vol. IV (ed. Bernays, E. A.) 1–44 (CRC Press, Boca Raton, 1992).

  16. 16.

    Norconk, M. A., Grafton, B. W. & Conklin-Brittain, N. L. Seed dispersal by neotropical seed predators. Am. J. Primatol. 45, 103–126 (1998).

  17. 17.

    Vander Wall, S. B., Kuhn, K. M. & Beck, M. J. Seed removal, seed predation, and secondary dispersal. Ecology 86, 801–806 (2005).

  18. 18.

    Pilosof, S., Porter, M. A., Pascual, M. & Kéfi, S. The multilayer nature of ecological networks. Nat. Ecol. Evol. 1, 0101 (2017).

  19. 19.

    Bascompte, J. & Jordano, P. Plant-animal mutualistic networks: the architecture of biodiversity. Annu. Rev. Ecol. Evol. S. 38, 567–593 (2007).

  20. 20.

    Montesinos-Navarro, A., Segarra-Moragues, J. G., Valiente-Banuet, A. & Verdú, M. The network structure of plant-arbuscular mycorrhizal fungi. New Phytol. 194, 536–547 (2012).

  21. 21.

    Donatti, C. I. et al. Analysis of a hyper-diverse seed dispersal network: modularity and underlying mechanisms. Ecol. Lett. 14, 773–781 (2011).

  22. 22.

    Bascompte, J., Jordano, P., Melián, C. J. & Olesen, J. M. The nested assembly of plant-animal mutualistic networks. Proc. Natl Acad. Sci. USA 100, 9383–9387 (2003).

  23. 23.

    Olesen, J. M., Bascompte, J., Dupont, Y. L. & Jordano, P. The modularity of pollination networks. Proc. Natl Acad. Sci. USA 104, 19891–19896 (2007).

  24. 24.

    Sinclair, A., Mduma, S. & Brashares, J. S. Patterns of predation in a diverse predator-prey system. Nature 425, 288–290 (2003).

  25. 25.

    Lewinsohn, T. M., Inácio Prado, P., Jordano, P., Bascompte, J. & Olesen, J. M. Structure in plant–animal interaction assemblages. Oikos 113, 174–184 (2006).

  26. 26.

    Memmott, J., Waser, N. M. & Price, M. V. Tolerance of pollination networks to species extinctions. Proc. R. Soc. Lond. B 271, 2605–2611 (2004).

  27. 27.

    Burgos, E. et al. Why nestedness in mutualistic networks? J. Theor. Biol. 249, 307–313 (2007).

  28. 28.

    Okuyama, T. & Holland, J. N. Network structural properties mediate the stability of mutualistic communities. Ecol. Lett. 11, 208–216 (2008).

  29. 29.

    Krause, A. E., Frank, K. A., Mason, D. M., Ulanowicz, R. E. & Taylor, W. W. Compartments revealed in food-web structure. Nature 426, 282–285 (2003).

  30. 30.

    Teng, J. & McCann, K. S. Dynamics of compartmented and reticulate food webs in relation to energetic flows. Am. Nat. 164, 85–100 (2004).

  31. 31.

    Thébault, E. & Fontaine, C. Stability of ecological communities and the architecture of mutualistic and trophic networks. Science 329, 853–856 (2010).

  32. 32.

    Genrich, C. M., Mello, M. A., Silveira, F. A., Bronstein, J. L. & Paglia, A. P. Duality of interaction outcomes in a plant-frugivore multilayer network. Oikos 126, 361–368 (2017).

  33. 33.

    Young, L. M., Kelly, D. & Nelson, X. J. Alpine flora may depend on declining frugivorous parrot for seed dispersal. Biol. Conserv. 147, 133–142 (2012).

  34. 34.

    Blanco, G., Hiraldo, F., Rojas, A., Dénes, F. V. & Tella, J. L. Parrots as key multilinkers in ecosystem structure and functioning. Ecol. Evol. 5, 4141–4160 (2015).

  35. 35.

    Blanco, G. et al. Internal seed dispersal by parrots: an overview of a neglected mutualism. PeerJ 4, e1688 (2016).

  36. 36.

    Tella, J. L. et al. Parrots as overlooked seed dispersers. Front. Ecol. Environ. 13, 338–339 (2015).

  37. 37.

    Baños-Villalba, A. et al. Seed dispersal by macaws shapes the landscape of an Amazonian ecosystem. Sci. Rep. 7, 7373 (2017).

  38. 38.

    Fontaine, C. et al. The ecological and evolutionary implications of merging different types of networks. Ecol. Lett. 14, 1170–1181 (2011).

  39. 39.

    Johnson, N., Graham, J. & Smith, F. Functioning of mycorrhizal associations along the mutualism-parasitism continuum. New Phytol. 135, 575–585 (1997).

  40. 40.

    Hoover, S. E. et al. Warming, CO2, and nitrogen deposition interactively affect a plant-pollinator mutualism. Ecol. Lett. 15, 227–234 (2012).

  41. 41.

    Koide, R. The nature of growth depressions in sunflower caused by vesicular-arbuscular mycorrhizal infection. New Phytol. 99, 449–462 (1985).

  42. 42.

    Ragusa-Netto, J. & Fecchio, A. Plant food resources and the diet of a parrot community in a gallery forest of the southern Pantanal (Brazil). Braz. J. Biol. 66, 1021–32 (2006).

  43. 43.

    Gleiser, G. et al. The southernmost parakeet might be enhancing pollination of a dioecious ancient conifer. Ecology http://dx.doi.org/10.1002/ecy.1938 (2017).

  44. 44.

    Lee, A. T. et al. Diet and geophagy across a western Amazonian parrot assemblage. Biotropica 46, 322–330 (2014).

  45. 45.

    Tella, J. L. et al. Endangered plant-parrot mutualisms: seed tolerance to predation makes parrots pervasive dispersers of the Parana pine. Sci. Rep. 6, 31709 (2016).

  46. 46.

    Toft, C. A. & Wright, T. F. Parrots of the Wild: A Natural History of the World’s Most Captivating Birds (Univ. California Press, Berkeley, 2015).

  47. 47.

    Navarro, G. & Maldonado, M. Geografía ecológica de Bolivia: Vegetación y ambientes acuáticos (Centro de Ecología Simón I. Patiño, Cochabamba, 2002).

  48. 48.

    Tella, J. L., Rojas, A., Carrete, M. & Hiraldo, F. Simple assessments of age and spatial population structure can aid conservation of poorly known species. Biol. Conserv. 167, 425–434 (2013).

  49. 49.

    Forshaw, J. M. Parrots of the World: An Identification Guide (Princeton Univ. Press, Princeton, 2006).

  50. 50.

    The Plant List Version 1.1. (accessed 1 January 2013); http://www.theplantlist.org/

  51. 51.

    López, R. P. Diversidad florística y endemismo de los valles secos bolivianos. Ecol. Bolivia 38, 27–60 (2003).

  52. 52.

    Atahuachi-Burgos, M. et al. La guía“Darwin” de las flores de los valles bolivianos (Darwin Initiative, Le Paz, 2005).

  53. 53.

    Juniper, A. & Parr, M. Parrots: A Guide to the Parrots of the World (Christopher Helm, London, 2010).

  54. 54.

    Anderson, S. H., Kelly, D., Ladley, J. J., Molloy, S. & Terry, J. Cascading effects of bird functional extinction reduce pollination and plant density. Science 331, 1068–1071 (2011).

  55. 55.

    Atmar, W. & Patterson, B. D. The measure of order and disorder in the distribution of species in fragmented habitat. Oecologia 96, 373–382 (1993).

  56. 56.

    Almeida-Neto, M., Guimaraes, P., Guimarães, P. R., Loyola, R. D. & Ulrich, W. A consistent metric for nestedness analysis in ecological systems: reconciling concept and measurement. Oikos 117, 1227–1239 (2008).

  57. 57.

    Vacher, C., Piou, D. & Desprez-Loustau, M.-L. Architecture of an antagonistic tree/fungus network: the asymmetric influence of past evolutionary history. PLoS ONE 3, e1740 (2008).

  58. 58.

    Guimarães, P. R. & Guimarães, P. Improving the analyses of nestedness for large sets of matrices. Environ. Modell. Softw. 21, 1512–1513 (2006).

  59. 59.

    Joppa, L. N. & Williams, R. The influence of single elements on nested community structure. Methods Ecol. Evol. 2, 541–549 (2011).

  60. 60.

    Danon, L., Diaz-Guilera, A., Duch, J. & Arenas, A. Comparing community structure identification. J. Stat. Mech. Theory Exp. 2005, P09008 (2005).

  61. 61.

    Guimerà, R. & Amaral, L. A. N. Cartography of complex networks: modules and universal roles. J. Stat. Mech. Theory Exp. 2005, P02001 (2005).

  62. 62.

    Guimerà, R., Sales-Pardo, M. & Amaral, L. A. N. Modularity from fluctuations in random graphs and complex networks. Phys. Rev. E 70, 025101 (2004).

  63. 63.

    Guimerà, R., Sales-Pardo, M. & Amaral, L. A. N. Module identification in bipartite and directed networks. Phys. Rev. E 76, 036102 (2007).

  64. 64.

    Fortuna, M. A. et al. Nestedness versus modularity in ecological networks: two sides of the same coin? J. Anim. Ecol. 79, 811–817 (2010).

  65. 65.

    Guimerà, R. & Amaral, L. A. N. Functional cartography of complex metabolic networks. Nature 433, 895–900 (2005).

  66. 66.

    Nakagawa, S. & Cuthill, I. C. Effect size, confidence interval and statistical significance: a practical guide for biologists. Biol. Rev. 82, 591–605 (2007).

  67. 67.

    R Core Team R: A Language and Environment for Statistical Computing (R Foundation for Statistical Computing, Vienna, 2014).

  68. 68.

    Amarasekare, P. Spatial dynamics of mutualistic interactions. J. Anim. Ecol. 73, 128–142 (2004).

  69. 69.

    Bascompte, J., Jordano, P. & Olesen, J. M. Asymmetric coevolutionary networks facilitate biodiversity maintenance. Science 312, 431–433 (2006).

  70. 70.

    Valiente-Banuet, A. & Verdú, M. Human impacts on multiple ecological networks act synergistically to drive ecosystem collapse. Front. Ecol. Environ. 11, 408–413 (2013).

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Acknowledgements

We thank M. de la Riva, A. Rojas, E. Pacifico, H. Garrido, A. Requejo, I. Vera, R. Rojas, J. Paca, G. Flores, S. Huici, E. Yucra and D. Alberto for fieldwork assistance, and A. Toledo for making the parrot drawings. M. de la Riva gave permission to publish his photographs in this article. M. Verdú greatly helped to improve the manuscript. Funding was provided by Zoo de Barcelona and Biorena (January 2011), Junta de Andalucía (PAI RNM107 to J.L.T. and F.H., April–September 2011), Fundación Biodiversidad (2012–2013), and a Severo Ochoa ‘microproyecto’ award (to F.H.). A.M.-N. was supported by a Juan de la Cierva-Incorporación postdoctoral contract from the Spanish Ministerio de Economía y Competitividad (IJCI-2015-23498).

Author information

G.B., J.L.T., F.H. and A.M.-N. designed the study. G.B., J.L.T. and F.H. compiled the data, A.M.-N. performed the analyses, G.B. and A.M.N. wrote the first draft of the manuscript and all the authors contributed substantially to improving the manuscript.

Correspondence to Alicia Montesinos-Navarro.

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Supplementary Information

Supplementary Fig 1, Supplementary Table 1

Supplementary Data 1

File with 6 sheets: 1) Plant traits. Each plant taxa assignment to growth form, dominance, endemicity, and module. 2) Quant. plant–parrot interaction. Number of flocks of each parrot species observed on each plant species. 3) Quali. multilayer network. Presence/absence of plant–parrot interaction, without distinguishing between mutualistic and antagonistic interactions. 4) Quali. mutual. sub-network. Presence/absence of a mutualistic interaction. 5) Quali. antag. subnetwork. Presence/absence of an antagonistic interaction. 6) Weights. Weights used in co-extinction cascades simulations

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Montesinos-Navarro, A., Hiraldo, F., Tella, J.L. et al. Network structure embracing mutualism–antagonism continuums increases community robustness. Nat Ecol Evol 1, 1661–1669 (2017). https://doi.org/10.1038/s41559-017-0320-6

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