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Consequences of a biological invasion reveal the importance of mutualism for plant communities

Abstract

Seed-dispersal mutualisms have a fundamental role in regenerating natural communities1,2. Interest in the importance of seed dispersal to plant communities has been heightened by worldwide declines in animal dispersers3,4,5. One view, the ‘keystone mutualist hypothesis’, predicts that these human-caused losses will trigger a cascade of linked extinctions throughout the community6. Implicitly, this view holds that mutualisms, such as seed dispersal, are crucial ecological interactions that maintain the structure and diversity of natural communities. Although many studies suggest the importance of mutualism3,7, empirical evidence for community-level impacts of mutualists has remained anecdotal8,9, and the central role of mutualism, relative to other species interactions, has long been debated in the theoretical literature10,11. Here I report the community-level consequences of a biological invasion that disrupts important seed-dispersal mutualisms. I show that invasion of South African shrublands by the Argentine ant (Linepithema humile) leads to a shift in composition of the plant community, owing to a disproportionate reduction in the densities of large-seeded plants. This study suggests that the preservation of mutualistic interactions may be essential for maintaining natural communities.

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Figure 1: Comparison of the densities of four common, native fynbos ant species and the Argentine ant in invaded and uninvaded areas.
Figure 2: Bimodal distribution of seed size found in ant-dispersed Proteaceae.
Figure 3: Probability of dispersal for large- and small-seeded Proteaceae by four native fynbos ant species and the Argentine ant.
Figure 4: The effects of the Argentine ant on seed predation of large-seeded and small-seeded species.
Figure 5: Consequences of the Argentine ant invasion for post-fire seedling recruitment of small-seeded versus large-seeded Proteaceae.

References

  1. 1

    Howe, H. F. & Smallwood, J. Ecology of seed dispersal. Ann. Rev. Eco. Syst. 13, 201–228 (1982).

    Article  Google Scholar 

  2. 2

    Chapman, C. A. Primate seed dispersal; coevolution and conservation implications. Evol. Anthropol. 4, 74–82 (1995)).

    Article  Google Scholar 

  3. 3

    Cox, P. A., Elmquist, T., Pierson, E. D. & Rainey, W. E. Flying foxes as strong interactors in South Pacific island ecosystems: a conservation hypothesis. Conserv. Biol. 5, 448–454 (1991).

    Article  Google Scholar 

  4. 4

    Chapman, C. A. & Chapman, L. J. Survival without dispersers: seedling recruitment under parents. Conserv. Biol. 9, 675–678 (1995).

    Article  Google Scholar 

  5. 5

    Aparecida Lopez, M. & Ferrari, S. F. Effects of human colonization on the abundance and diversity of mammals in eastern Brazilian Amazonia. Conserv. Biol. 14, 1658–1665 (2000).

    Article  Google Scholar 

  6. 6

    Gilbert, L. E. in Conservation Biology: An Evolutionary–Ecological Perspective (eds Soule, M. E. & Wilcox, B. A.) 11–33 (Sinauer, Sunderland, 1980).

    Google Scholar 

  7. 7

    Bond, W. J. Do mutualisms matter? Assessing the impact of pollinator and disperser disruption on plant extinction. Phil. Trans. R. Soc. Lond. B 344, 83–90 (1994).

    ADS  Article  Google Scholar 

  8. 8

    Mills, L. S., Soule, M. E. & Doak, D. F. The keystone-species concept in ecology and conservation. Bioscience 43, 219–224 (1993).

    Article  Google Scholar 

  9. 9

    Power, M. E. et al. Challenges in the quest for keystones. Bioscience 46, 609–620 (1996).

    Article  Google Scholar 

  10. 10

    May, R. M. in Theoretical Ecology, Principles and Applications (ed. May, R. M.) 49–70 (Saunders, Philadelphia, 1976).

    Google Scholar 

  11. 11

    Addicott, J. F. in A New Ecology: Novel Approaches to Interactive Systems (eds Price, P. W., Slobodchikoff, C. N. & Gaud, W. S.) 437–455 (Wiley, New York, 1984).

    Google Scholar 

  12. 12

    de Kock, A. E. & Giliomee, J. H. A survey of the Argentine ant, Iridomyrmex humilis (Mayr) (Hymenoptera: Formicidae) in South African fynbos. J. Entomol. Soc. S. Africa 52, 151–164 (1989).

    Google Scholar 

  13. 13

    Bond, W. J., Yeaton, R. & Stock, W. D. in Ant–Plant Interactions (eds Huxley, C. & Cutler, D.) 448–462 (Oxford Univ. Press, Oxford, 1991).

    Google Scholar 

  14. 14

    Bond, W. J. & Slingsby, P. Collapse of an ant–plant mutualism: the Argentine ant (Iridomyrmex humilis) and myrmecochorous Proteaceae. Ecology 65, 1031–1037 (1984).

    Article  Google Scholar 

  15. 15

    Cole, F. R., Medeiros, A. C., Loope, L. L. & Zuehlke, W. W. Effects of the Argentine ant on arthropod fauna of Hawaiian high-elevation shrubland. Ecology 73, 1313–1322 (1992).

    Article  Google Scholar 

  16. 16

    Ward, P. S. Distribution of the introduced Argentine ant (Iridomyrmex humilis) in natural habitats of the lower Sacramento Valley and its effects on the indigenous ant fauna. Hilgardia 55, 1–16 (1987).

    Article  Google Scholar 

  17. 17

    Way, M. J., Cammell, M. E., Paiva, M. R. & Collingwood, C. A. Distribution and dynamics of the Argentine ant Linepithema (Iridomyrmex) humile (Mayr) in relation to vegetation, soil conditions, topography and native ant competitor ants in Portugal. Insectes Sociaux 44, 415–433 (1997).

    Article  Google Scholar 

  18. 18

    De Kock, A. E., Giliomee, J. H., Pringle, K. L. & Majer, J. D. in Fire in South African Mountain Fynbos (eds van Wilgen, B. W., Richardson, D. M., Kruger, F. J. & van Hensbergen, H. J.) 201–215 (Springer, Berlin, 1992).

    Google Scholar 

  19. 19

    Lawton, J. H. & Brown, V. K. in Biodiversity and Ecosystem Function (eds Schulze, E.-D. & Mooney, H. A.) 255–270 (Springer, Berlin, 1993).

    Google Scholar 

  20. 20

    Cushman, J. H. in Islands: Biological Diversity and Ecosystem Function (eds Vitousik, P. M., Loope, L. L. & Adsersen, H.) 135–147 (Springer, Berlin, 1995).

    Book  Google Scholar 

  21. 21

    Brown, J. H. & Henske, E. J. Control of a desert–grassland transition by a keystone rodent guild. Science 250, 1705–1707 (1990).

    ADS  CAS  Article  Google Scholar 

  22. 22

    Howe, H. F. Specialized and generalized dispersal systems: where does the ‘the paradigm’ stand? Vegetatio 107/108, 3–13 (1993).

    Google Scholar 

  23. 23

    Hughes, L. et al. Predicting dispersal spectra: a minimal set of hypotheses based on plant attributes. J. Ecol. 82, 933–950 (1994).

    Google Scholar 

  24. 24

    Slingsby, P. & Bond, W. Ants—friends of the Fynbos: Mimetes hirtus, dispersal and storage by ants. Veld Flora 67, 39–45 (1981).

    Google Scholar 

  25. 25

    Visser, D., Wright, M. G. & Giliomee, J. H. The effect of the Argentine ant, Linepithema humile (Mayr) (Hymenoptera: Formicidae), on flower-visiting insects of Protea nitida Mill. (Proteaceae). Afr. Entomol. 4, 285–287 (1996).

    Google Scholar 

  26. 26

    Witt, A. B. R. Factors affecting Myrmecochory in Fynbos. (Thesis, Univ. Stellenbosch, 1993).

    Google Scholar 

  27. 27

    Hölldobler, B. & Wilson, E. O. The Ants (Harvard Univ. Press, Cambridge, 1990).

    Book  Google Scholar 

  28. 28

    Passera, L. in Exotic ants: Biology, Impact, and Control of Introduced Species (ed. Williams, D. H.) 23–43 (Westview, Boulder, 1994).

    Google Scholar 

  29. 29

    Slingsby, P. & Bond, W. J. The influence of ants on the dispersal distance and seedling recruitment of Leucospermum conocarpodendron (L.) Buek (Proteaceae). S. Afr. J. Bot. 51, 30–34 (1985).

    Article  Google Scholar 

  30. 30

    Bond, W. J. & Breytenbach, G. J. Ants, rodents and seed predation in Proteaceae. S. Afr. J. Zool. 20, 150–154 (1985).

    Article  Google Scholar 

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Acknowledgements

Comments from A. Agrawal, E. Baack, E. Bruna, H. Cushman, A. Pauw, J. Rudgers, M. Stanton, S. Strauss and H. Robertson improved this manuscript. I thank E. Baack, W. Bond, D. Doak, M. and A. Johns, and P. Ward for their assistance and discussions during this project. Cape Nature Conservation and the South African Museum also provided support. This work was supported by grants from the National Science Foundation, Achievement Rewards for College Scientists Foundation, and the Center for Population Biology, UC Davis.

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Correspondence to Caroline E. Christian.

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Christian, C. Consequences of a biological invasion reveal the importance of mutualism for plant communities. Nature 413, 635–639 (2001). https://doi.org/10.1038/35098093

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