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Dimensionality of consumer search space drives trophic interaction strengths

Abstract

Trophic interactions govern biomass fluxes in ecosystems, and stability in food webs. Knowledge of how trophic interaction strengths are affected by differences among habitats is crucial for understanding variation in ecological systems. Here we show how substantial variation in consumption-rate data, and hence trophic interaction strengths, arises because consumers tend to encounter resources more frequently in three dimensions (3D) (for example, arboreal and pelagic zones) than two dimensions (2D) (for example, terrestrial and benthic zones). By combining new theory with extensive data (376 species, with body masses ranging from 5.24 × 10−14 kg to 800 kg), we find that consumption rates scale sublinearly with consumer body mass (exponent of approximately 0.85) for 2D interactions, but superlinearly (exponent of approximately 1.06) for 3D interactions. These results contradict the currently widespread assumption of a single exponent (of approximately 0.75) in consumer–resource and food-web research. Further analysis of 2,929 consumer–resource interactions shows that dimensionality of consumer search space is probably a major driver of species coexistence, and the stability and abundance of populations.

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Figure 1: Consumer–resource interactions can be classified by dimensionality.
Figure 2: Model for scaling of search and consumption rate with body size.
Figure 3: Effect of interaction dimensionality on scaling of search and consumption rate.
Figure 4: Effects of interaction dimensionality on consumer–resource dynamics.

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References

  1. Cohen, J. E. & Fenchel, T. Marine and continental food webs: three paradoxes? Phil. Trans. R. Soc. Lond. B 343, 57–69 (1994)

    Article  ADS  Google Scholar 

  2. Savage, V. M., Webb, C. T. & Norberg, J. A general multi-trait-based framework for studying the effects of biodiversity on ecosystem functioning. J. Theor. Biol. 247, 213–229 (2007)

    Article  MathSciNet  PubMed  PubMed Central  Google Scholar 

  3. Ritchie, M. E. Scale, Heterogeneity, and the Structure and Diversity of Ecological Communities. Vol. 112 (Princeton Univ. Press, 2009)

    Book  Google Scholar 

  4. Briand, F. & Cohen, J. E. Environmental correlates of food-chain length. Science 238, 956–960 (1987)

    Article  ADS  CAS  PubMed  Google Scholar 

  5. Rip, J. M. K. & McCann, K. S. Cross-ecosystem differences in stability and the principle of energy flux. Ecol. Lett. 14, 733–740 (2011)

    Article  CAS  PubMed  Google Scholar 

  6. Cyr, H., Peters, R. H. & Downing, J. A. Population density and community size structure: comparison of aquatic and terrestrial systems. Oikos 80, 139–149 (1997)

    Article  Google Scholar 

  7. Farlow, J. O. A consideration of the trophic dynamics of a late Cretaceous large-dinosaur community (Oldman formation). Ecology 57, 841–857 (1976)

    Article  Google Scholar 

  8. Peters, R. H. The Ecological Implications of Body Size. (Cambridge Univ. Press, 1983)

    Book  Google Scholar 

  9. Brown, J. H., Gillooly, J. F., Allen, A. P., Savage, V. M. & West, G. B. Toward a metabolic theory of ecology. Ecology 85, 1771–1789 (2004)

    Article  Google Scholar 

  10. Otto, S. B., Rall, B. C. & Brose, U. Allometric degree distributions facilitate food-web stability. Nature 450, 1226–1229 (2007)

    Article  ADS  CAS  PubMed  Google Scholar 

  11. Berlow, E. L. et al. Simple prediction of interaction strengths in complex food webs. Proc. Natl Acad. Sci. USA 106, 187–191 (2009)

    Article  ADS  CAS  PubMed  Google Scholar 

  12. Lewis, H. M., Law, R. & McKane, A. J. Abundance–body size relationships: the roles of metabolism and population dynamics. J. Anim. Ecol. 77, 1056–1062 (2008)

    Article  PubMed  Google Scholar 

  13. Yodzis, P. & Innes, S. Body size and consumer resource dynamics. Am. Nat. 139, 1151–1175 (1992)

    Article  Google Scholar 

  14. Savage, V. M., Gillooly, J. F., Brown, J. H., West, G. B. & Charnov, E. L. Effects of body size and temperature on population growth. Am. Nat. 163, 429–441 (2004)

    Article  PubMed  Google Scholar 

  15. Brose, U., Williams, R. J. & Martinez, N. D. Allometric scaling enhances stability in complex food webs. Ecol. Lett. 9, 1228–1236 (2006)

    Article  PubMed  Google Scholar 

  16. Brose, U. Body-mass constraints on foraging behaviour determine population and food-web dynamics. Funct. Ecol. 24, 28–34 (2010)

    Article  Google Scholar 

  17. McGill, B. J. & Mittelbach, G. G. An allometric vision and motion model to predict prey encounter rates. Evol. Ecol. Res. 8, 691–701 (2006)

    Google Scholar 

  18. Alexander, R. M. Principles of Animal Locomotion. (Princeton Univ. Press, 2003)

    Book  Google Scholar 

  19. Schmidt-Nielsen, K. Scaling, Why is Animal Size so Important? (Cambridge Univ. Press, 1984)

    Book  Google Scholar 

  20. Jetz, W., Carbone, C., Fulford, J. & Brown, J. H. The scaling of animal space use. Science 306, 266–268 (2004)

    Article  ADS  CAS  PubMed  Google Scholar 

  21. Weibel, E. R., Bacigalupe, L. D., Schmitt, B. & Hoppeler, H. Allometric scaling of maximal metabolic rate in mammals: muscle aerobic capacity as determinant factor. Respir. Physiol. Neurobiol. 140, 115–132 (2004)

    Article  PubMed  Google Scholar 

  22. Holling, C. S. Cross-scale morphology, geometry, and dynamics of ecosystems. Ecol. Monogr. 62, 447–502 (1992)

    Article  Google Scholar 

  23. Whitehead, H. & Walde, S. J. Habitat dimensionality and mean search distances of top predators: implications for ecosystem structure. Theor. Popul. Biol. 42, 1–9 (1992)

    Article  MathSciNet  Google Scholar 

  24. Witting, L. The body mass allometries as evolutionarily determined by the foraging of mobile organisms. J. Theor. Biol. 177, 129–137 (1995)

    Article  Google Scholar 

  25. Milne, B. T., Turner, M. G., Wiens, J. A. & Johnson, A. R. Interactions between the fractal geometry of landscapes and allometric herbivory. Theor. Popul. Biol. 41, 337–353 (1992)

    Article  Google Scholar 

  26. Weitz, J. S. & Levin, S. A. Size and scaling of predator-prey dynamics. Ecol. Lett. 9, 548–557 (2006)

    Article  PubMed  Google Scholar 

  27. Holling, C. S. Some characteristics of simple types of predation and parasitism. Can. Entomol. 91, 385–398 (1959)

    Article  Google Scholar 

  28. Laska, M. S. & Wootton, T. J. Theoretical concepts and empirical approaches to measuring interaction strength. Ecology 79, 461–476 (1998)

    Article  Google Scholar 

  29. Pawar, S. Community assembly, stability and signatures of dynamical constraints on food web structure. J. Theor. Biol. 259, 601–612 (2009)

    Article  MathSciNet  PubMed  Google Scholar 

  30. Jeschke, J. M., Kopp, M. & Tollrian, R. Consumer-food systems: why type I functional responses are exclusive to filter feeders. Biol. Rev. Camb. Phil. Soc. 79, 337–349 (2004)

    Article  Google Scholar 

  31. Brose, U. et al. Consumer–resource body-size relationships in natural food webs. Ecology 87, 2411–2417 (2006)

    Article  PubMed  Google Scholar 

  32. Shurin, J. B., Gruner, D. S. & Hillebrand, H. All wet or dried up? Real differences between aquatic and terrestrial food webs. Proc. R. Soc. B 273, 1–9 (2006)

    Article  PubMed  Google Scholar 

  33. Chase, J. M. Are there real differences among aquatic and terrestrial food webs? Trends Ecol. Evol. 15, 408–412 (2000)

    Article  ADS  CAS  PubMed  Google Scholar 

  34. Damuth, J. Population density and body size in mammals. Nature 290, 699–700 (1981)

    Article  ADS  Google Scholar 

  35. Reuman, D. C. et al. Allometry of body size and abundance in 166 food webs. Adv. Ecol. Res. 41, 1–44 (2009)

    Article  Google Scholar 

  36. Leaper, R. & Raffaelli, D. Defining the abundance body-size constraint space: data from a real food web. Ecol. Lett. 2, 191–199 (1999)

    Article  Google Scholar 

  37. Cermeño, P., Maranon, E., Harbour, D. & Harris, R. P. Invariant scaling of phytoplankton abundance and cell size in contrasting marine environments. Ecol. Lett. 9, 1210–1215 (2006)

    Article  PubMed  Google Scholar 

  38. Belgrano, A., Allen, A. P., Enquist, B. J. & Gillooly, J. F. Allometric scaling of maximum population density: a common rule for marine phytoplankton and terrestrial plants. Ecol. Lett. 5, 611–613 (2002)

    Article  Google Scholar 

  39. Field, C. B., Behrenfeld, M. J., Randerson, J. T. & Falkowski, P. Primary production of the biosphere: integrating terrestrial and oceanic components. Science 281, 237–240 (1998)

    Article  ADS  CAS  PubMed  Google Scholar 

  40. Vucic-Pestic, O., Rall, B. C., Kalinkat, G. & Brose, U. Allometric functional response model: body masses constrain interaction strengths. J. Anim. Ecol. 79, 249–256 (2010)

    Article  PubMed  Google Scholar 

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Acknowledgements

We thank the authors who contributed data (Supplementary Tables 5–8), and P. Amarasekare, J. H. Brown, E. Economo, A. Mikheyev, C. Estrada, C. Johnson, M. Johnson and K. Lafferty for helpful discussions and comments. S.P., A.I.D. and V.M.S. were supported by University of California, Los Angeles Biomathematics start-up funds and by the US National Science Foundation Division of Environmental Biology award 1021010. The data reported in this paper are available in the Supplementary Information online.

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S.P., A.I.D. and V.M.S. contributed equally to this work. All authors discussed the results and commented on the manuscript.

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Correspondence to Samraat Pawar.

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The authors declare no competing financial interests.

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This file contains Supplementary Text and Data, Supplementary Figures 1-4 and Supplementary Tables 1-8. (PDF 4567 kb)

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Pawar, S., Dell, A. & Van M. Savage Dimensionality of consumer search space drives trophic interaction strengths. Nature 486, 485–489 (2012). https://doi.org/10.1038/nature11131

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