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Reconciling complexity with stability in naturally assembling food webs

Nature volume 449, pages 599602 (04 October 2007) | Download Citation

  • An Addendum to this article was published on 05 March 2009

Abstract

Understanding how complex food webs assemble through time is fundamental both for ecological theory and for the development of sustainable strategies of ecosystem conservation and restoration. The build-up of complexity in communities is theoretically difficult, because in random-pattern models complexity leads to instability1. There is growing evidence, however, that nonrandom patterns in the strengths of the interactions between predators and prey strongly enhance system stability2,3,4. Here we show how such patterns explain stability in naturally assembling communities. We present two series of below-ground food webs along natural productivity gradients in vegetation successions5,6. The complexity of the food webs increased along the gradients. The stability of the food webs was captured by measuring the weight of feedback loops7 of three interacting ‘species’ locked in omnivory. Low predator–prey biomass ratios in these omnivorous loops were shown to have a crucial role in preserving stability as productivity and complexity increased during succession. Our results show the build-up of food-web complexity in natural productivity gradients and pin down the feedback loops that govern the stability of whole webs. They show that it is the heaviest three-link feedback loop in a network of predator–prey effects that limits its stability. Because the weight of these feedback loops is kept relatively low by the biomass build-up in the successional process, complexity does not lead to instability.

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References

  1. 1.

    Will a large complex system be stable? Nature 238, 413–414 (1972)

  2. 2.

    , & Energetics, patterns of interaction strengths, and stability in real ecosystems. Science 269, 1257–1260 (1995)

  3. 3.

    , & Weak trophic interactions and the balance of nature. Nature 395, 794–798 (1998)

  4. 4.

    , , & Structural asymmetry and the stability of diverse food webs. Nature 442, 265–269 (2006)

  5. 5.

    , & Species dynamics and nutrient accumulation during early primary succession in coastal sand dunes. J. Ecol. 81, 693–702 (1993)

  6. 6.

    & in Perspectives on Plant Competition (eds Grace, J. B. & Tilman, D.) 94–116 (Academic, New York, 1990)

  7. 7.

    , & Stability in real food webs: weak links in long loops. Science 296, 1120–1123 (2002)

  8. 8.

    Plant Strategies and Vegetation Processes (Wiley, Chichester, 1979)

  9. 9.

    The trophic-dynamic aspect of ecology. Ecology 23, 399–418 (1942)

  10. 10.

    , , & Exploitation ecosystems in gradients of primary productivity. Am. Nat. 118, 240–261 (1981)

  11. 11.

    & Productivity controls food-chain properties in microbial communities. Nature 395, 495–497 (1998)

  12. 12.

    , & Ecosystem size determines food-chain length in lakes. Nature 405, 1047–1049 (2000)

  13. 13.

    & Number of trophic levels in ecological communities. Nature 268, 329–331 (1977)

  14. 14.

    , & Arthropod regulation of micro- and mesobiota in belowground food webs. Annu. Rev. Entomol. 33, 419–439 (1988)

  15. 15.

    , , , & Calculation of nitrogen mineralisation in soil food webs. Plant Soil 157, 263–273 (1993)

  16. 16.

    & Connectance of large dynamic (cybernetic) systems: critical values for stability. Nature 228, 784 (1970)

  17. 17.

    et al. The detrital food web in a shortgrass prairie. Biol. Fertil. Soils 3, 57–68 (1987)

  18. 18.

    & in The Theory of Evolution and Dynamical Systems 204–206 (Cambridge Univ. Press, Cambridge, 1988)

  19. 19.

    , & Community Food Webs: Data and Theory (Springer, Berlin, 1990)

  20. 20.

    & Terrestrial trophic cascades: how much do they trickle? Am. Nat. 157, 262–281 (2001)

  21. 21.

    & Predator diversity dampens trophic cascades. Nature 429, 407–410 (2004)

  22. 22.

    , & Community structure, population control, and competition. Am. Nat. 142, 379–411 (1960)

  23. 23.

    , & Influence of productivity on the stability of real and model ecosystems. Science 261, 906–908 (1993)

  24. 24.

    & A theoretical framework for intraguild predation. Am. Nat. 149, 745–764 (1997)

  25. 25.

    & Self-organized similarity, the evolutionary emergence of groups of similar species. Proc. Natl Acad. Sci. USA 103, 6230–6235 (2006)

  26. 26.

    , & Asymmetric coevolutionary networks facilitate biodiversity maintenance. Science 312, 431–433 (2006)

  27. 27.

    , , , & Biomass, composition and temporal dynamics of soil organisms of a silt loam soil under conventional and integrated management. Neth. J. Agr. Sci. 38, 283–302 (1990)

  28. 28.

    , & Microbial biomass and activity of a reclaimed polder soil under a conventional or a reduced-input farming system. Soil Biol. Biochem. 23, 515–524 (1991)

  29. 29.

    , & Fully automatic determination of soil bacterium numbers, cell volumes, and frequencies of dividing cells by confocal laser scanning microscopy and image analysis. Appl. Environ. Microb. 61, 926–936 (1995)

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Acknowledgements

We thank E. Biewenga, P. Bolhuis, B. van der Boom, K. Kampen, M. Veninga and W. Willems for assistance in collecting and analysing the soil samples. We thank S. Burgers, J. Krumins and P. Morin for comments on the manuscript.

Author information

Author notes

    • Anje-Margriet Neutel

    Present address: British Antarctic Survey, High Cross, Madingley Road, Cambridge CB3 0ET, UK.

Affiliations

  1. Environment Department, University of York, Heslington, York YO10 5DD, UK

    • Anje-Margriet Neutel
  2. Faculty of Veterinary Medicine, Theoretical Epidemiology, Utrecht University, 3508 TD Utrecht, The Netherlands

    • Johan A. P. Heesterbeek
  3. Spatial Ecology Department, Centre for Estuarine and Marine Ecology, Netherlands Institute of Ecology (NIOO-KNAW), 4400 AC Yerseke, The Netherlands

    • Johan van de Koppel
  4. Department ICT, Wageningen University and Research Centre, 6700 AB Wageningen, The Netherlands

    • Guido Hoenderboom
  5. Alterra, Soil Science Centre, Wageningen University and Research Centre, 6700 AA Wageningen, The Netherlands

    • An Vos
    • , Coen Kaldeway
    •  & Peter C. de Ruiter
  6. Nature Conservation and Plant Ecology Group, Wageningen University, 6708 PB Wageningen, The Netherlands

    • Frank Berendse
  7. Department of Environmental Sciences, Copernicus Institute for Sustainable Development and Innovation, Utrecht University, 3508 TC Utrecht, The Netherlands

    • Peter C. de Ruiter

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Competing interests

The authors declare no competing financial interests.

Corresponding author

Correspondence to Anje-Margriet Neutel.

Supplementary information

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  1. 1.

    Supplementary Information

    The file contains Supplementary Tables 1-2 (of observed biomass densities and complexity characteristics), additional information on the methods used (determining intraspecific interaction, expressing stability, deriving biomass dependencies, explaining details of calculating s), and Supplementary Figures S1-S4 with Legends containing sensitivity analyses (Figures S1 to S3) and the biomass-complexity relation (Figure S4).

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https://doi.org/10.1038/nature06154

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