Food Webs pp 371-395 | Cite as

The Role of Indirect Effects in Food Webs

  • Peter A. Abrams
  • Bruce A. Menge
  • Gary G. Mittelbach
  • David A. Spiller
  • Peter Yodzis

Abstract

Consider the following questions: (1) If we manipulate one species in a food web will this change the population of species that neither eat nor are eaten by the manipulated species? (2) If removing species A in food web 1 causes a 20% decrease in species B, can we assume that a similar decrease of B will occur if we remove species A in web 2, which contains a number of species not found in web 1? The answer to these sorts of questions depend a great deal on the importance of indirect interactions in food webs. If the effect of one species on the density of another tends to diminish with their separation in the food web (measured by number of feeding links in the shortest path connecting the two species), then it may be possible to ignore at least some indirect effects. Under this scenario where affects are attenuated by distance in the food web, we would expect either prey or predators of the focal species to be most affected by a change in the rate of harvest of the focal species.

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Abrams, P. A. 1984. Foraging time optimization and interactions in food webs. American Naturalist 124: 80–96.CrossRefGoogle Scholar
  2. Abrams, P. A. 1986. Character displacement and niche shift analyzed using consumer-resource models of competition. Theoretical Population Biology 29: 107–160.PubMedCrossRefGoogle Scholar
  3. Abrams, P. A. 1987a. On classifying interactions between populations. Oecologia (Berlin) 73: 272–281.CrossRefGoogle Scholar
  4. Abrams, P. A. 1987b. The functional responses of adaptive consumers of two resources. Theoretical Population Biology 32: 262–288.CrossRefGoogle Scholar
  5. Abrams, P. A. 1987c. Indirect interactions between species that share a predator: Varieties of indirect effects. In Predation: Direct and Indirect Impacts on Aquatic Communities, eds. W. C. Kerfoot and A. Sih, pp. 38–54. University Press of New England, Dartmouth, NH.Google Scholar
  6. Abrams, P. A. 1991. Strengths of indirect effects generated by optimal foraging. Oikos 62: 167-176.Google Scholar
  7. Abrams, P. A. 1992. Predators that benefit prey and prey that harm predators. Unusual effects of interacting foraging adaptations. American Naturalist 140: 573–600.CrossRefGoogle Scholar
  8. Abrams, P. A. 1993. Indirect effects arising from optimal foraging. In Mutualism and Community Organization: Behavioral, Theoretical and Food Web Approaches, ed. H. Kawanabe, J. E. Cohen, and K. Iwasaki, pp. 255–279. Oxford University Press, Oxford, U.K.Google Scholar
  9. Abrams, P. A. and H. Matsuda. 1993. Effects of adaptive predatory and anti-predator behavior in a two prey-one predator system Evolutionary Ecology 7: 312–326.CrossRefGoogle Scholar
  10. Bender, E. A., T. J. Case, and M. E. Gilpin. 1984. Perturbation experiments in community ecology: Theory and practice. Ecology 65: 113.CrossRefGoogle Scholar
  11. Brooks, J. L. and S. I. Dodson. 1965. Predation, body size, and composition of plankton. Science 150: 28–35.PubMedCrossRefGoogle Scholar
  12. Brown, C. J. D. and R. C. Ball. 1942. A fish population study of Third Sister lake. Transactions of the American Fisheries Society 72: 177186.Google Scholar
  13. Carpenter, S. R. and J. F. Kitchell. 1993. Aquatic Trophic Cascades. Cambridge University Press, Cambridge, U.K.CrossRefGoogle Scholar
  14. Carpenter, S. R., J. F. Kitchell, and J. R. Hodgson. 1985. Cascading trophic interactions and lake productivity. BioScience 35: 634–639.Google Scholar
  15. Carpenter, S. R., J. F. Kitchell, J. R. Hodgson, P. A. Cochran, J. J. Elser, M. M. Elser, D. M. Lodge, D. Kretchmer, X. He, and C. N. von Ende. 1987. Regulation of lake primary productivity by food-web structure. Ecology 68: 1863–1876.CrossRefGoogle Scholar
  16. Chesson, P. L. 1990. MacArthur’s consumer-resource model. Theoretical Population Biology 37: 26–38.CrossRefGoogle Scholar
  17. Clark, C. W. and D. A. Levy. 1988. Diel vertical migration by juvenile sockeye salmon and the antipredation window. American Naturalist 131: 271–290.CrossRefGoogle Scholar
  18. Cohen, J. E., F. Briand, and C. M. Newman. 1990. Community Food Webs: Data and Theory. Springer-Verlag, Berlin.CrossRefGoogle Scholar
  19. Connell, J. H. 1983. On the prevalence and importance of interspecific competition: Evidence from field experiments. American Naturalist 122: 661–696.CrossRefGoogle Scholar
  20. Davidson, D. W., R. S. Inouye, and J. H. Brown. 1984. Granivory in a desert ecosystem: Experimental evidence for indirect facilitation of ants by rodents. Ecology 65: 1780–1786.CrossRefGoogle Scholar
  21. Davidson, D. W., D. A. Samson, and R. S. Inouye. 1985. Granivory in the Chihuahuan Desert: Interactions within and between trophic levels. Ecology 66: 486–502.CrossRefGoogle Scholar
  22. Dayton, P. K. 1971. Competition, disturbance, and community organization: The provision and subsequent utilization of space in a rocky intertidal community. Ecological Monographs 45: 137–159.CrossRefGoogle Scholar
  23. DeAngelis, D. L. 1992. Dynamics of Nutrient Cycling and Food Webs. Chapman and Hall, New York.CrossRefGoogle Scholar
  24. Dethier, M. N. and D. O. Duggins. 1984. An “indirect commensalism” between marine herbivores and the importance of competitive hierarchies. American Naturalist 124: 205–219.CrossRefGoogle Scholar
  25. Diehl, S. 1994. Implication of omnivory and habitat complexity for aquatic community structure. Ph.D. Dissertation. Department of Animal Ecology, University of Umeä, Umeä, Sweden.Google Scholar
  26. Dungan, M. L. 1986. Three-way interactions: Barnacles, limpets, and algae in a Sonoran Desert rocky intertidal zone. American Naturalist 127: 292–316.CrossRefGoogle Scholar
  27. Dungan, M. L. 1987. Indirect mutualism: Complementary effects of grazing and predation in a rocky intertidal community. In Predation: Direct and Indirect Impacts on Aquatic Communities, eds. W. C. Kerfoot and A. Sih, pp. 188–200. University Press of New England, Hanover, NH.Google Scholar
  28. Endler, J. A. 1986. Natural Selection in the wild. Princeton University Press, Princeton, NJ.Google Scholar
  29. Field, J. G., R. J. M. Crawford, P. A. Wickens, C. L. Moloney, K. L. Cochrane, and C. A. Villacastin-Herrero. 1991. Network analysis of Benguela pelagic foodwebs. Benguela Ecology Programme, Workshop on Seal-Fishery Biological Interactions. University of Cape Town, Cape Town, South Africa.Google Scholar
  30. Fraser, D. F. and J. F. Gilliam. 1992. Nonlethal impacts of predator invasion: Facultative suppression of growth and reproduction. Ecology 73: 959–970.CrossRefGoogle Scholar
  31. Goldwasser, L. and J. Roughgarden. 1993. Construction and analysis of a large Caribbean food web. Ecology 74: 1216–1233.CrossRefGoogle Scholar
  32. Hall, D., W. Cooper, and E. E. Werner. 1970. An experimental approach to the production dynamics and structure of freshwater animal communities. Limnology and Oceanography 15: 839–928.CrossRefGoogle Scholar
  33. Helfman, G. S. 1993. Fish behavior by day, night, and twilight. In Behaviour of Teleost Fishes, 2nd Ed., ed. T. J. Pitcher, pp. 285–305. Chapman and Hall, New York.Google Scholar
  34. Hixon, M. A. 1991. Predation as a process structuring coral reef communities. In The Ecology of Fishes on Coral Reefs, ed. P. F. Sale, pp. 475–508. Academic Press, New York.Google Scholar
  35. Holt, R. D. 1977. Predation, apparent competition, and the structure of prey communities. Theoretical Population Biology 12: 197–229.PubMedCrossRefGoogle Scholar
  36. Holt, R. D. and B. P. Kotler. 1987. Short-term apparent competition. American Naturalist 130: 412–430.CrossRefGoogle Scholar
  37. Holt, R. D. and J. H. Lawton. 1994. The ecological consequences of shared natural enemies. Annual Review of Ecology and Systematics 25: 495–520.CrossRefGoogle Scholar
  38. Hsu, S. B. and S. P. Hubbell. 1979. Two predators competing for two prey species: An analysis of MacArthur’s model. Mathematical Biosciences 47: 143–171.CrossRefGoogle Scholar
  39. Kerfoot, W. C. and A. Sih, eds. 1987. Predation: Direct and Indirect Impacts on Aquatic Communities. University Press of New England, Dartmouth, NH.Google Scholar
  40. Kotler, B. P., L. Blaustein, and J. S. Brown. 1992. Predator facilitation: The combined effect of snakes and owls on the foraging behavior of gerbils. Annales Zoologi Fennici 29: 199–206.Google Scholar
  41. Kotler, B. P., J. S. Brown, R. Slotow, W. Good-friend, and M. Strauss. 1993. The influence of snakes on the foraging behavior of gerbils. Oikos 67: 309–316.CrossRefGoogle Scholar
  42. Levine, S. H. 1976. Competitive interactions in ecosystems. American Naturalist 110: 903–910.CrossRefGoogle Scholar
  43. Levins, R. 1974. Qualitative analysis of partially specified systems. Annals of the New York Academy of Science. 231: 123–138.CrossRefGoogle Scholar
  44. Levins, R. 1975. Evolution of communities near equilibrium. In Ecology and Evolution of Communities, eds. M. L. Cody and J. Diamond, pp. 16–50. Belknap, Cambridge, MA.Google Scholar
  45. Lima, S. L. and L. M. Dill. 1990. Behavioral decisions made under the risk of predation: A review and prospectus. Canadian Journal of Zoology 68: 619–640.CrossRefGoogle Scholar
  46. Lubchenco, J. and B. A. Menge. 1978. Community development and persistence in a low rocky intertidal zone. Ecological Monographs 48: 67–94.CrossRefGoogle Scholar
  47. MacArthur, R. H. 1970. Species packing and competitive equilibrium for many species. Theoretical Population Biology 1: 1–11.PubMedCrossRefGoogle Scholar
  48. MacArthur, R. H. 1972. Geographical Ecology. Harper and Row, New York.Google Scholar
  49. Matsuda, H., P. A. Abrams, and M. Hori. 1993. The effect of adaptive anti-predator behavior on exploitative competition and mutualism between predators. Oikos 68: 549–559.CrossRefGoogle Scholar
  50. Matsuda, H., M. Hori, and P. Abrams. 1994. Effects of predator-specific defense on community complexity. Evolutionary Ecology 8: 628–638.CrossRefGoogle Scholar
  51. Menge, B. A. 1976. Organization of the New England rocky intertidal community: Role of predation, competition and environmental heterogeneity. Ecological Monographs 46: 355–393.CrossRefGoogle Scholar
  52. Menge, B. A. 1995. Indirect effects in marine rocky intertidal interaction webs: Patterns and importance. Ecological Monographs 65: 21–74.CrossRefGoogle Scholar
  53. Miller, T. E. and W. C. Kerfoot. 1987. Redefining indirect effects. In Predation: Direct and Indirect Impacts on Aquatic Communities, eds. W. C. Kerfoot and A. Sih, pp. 33–37. University Press of New England, Dartmouth, NH.Google Scholar
  54. Mittelbach, G. G. 1981. Foraging efficiency and body size: A study of optimal diet and habitat use by bluegill. Ecology 62: 1370–1386.CrossRefGoogle Scholar
  55. Mittelbach, G. G. 1984. Predation and resource portioning in two sunfishes (Centrarchidae). Ecology 65: 499–513.CrossRefGoogle Scholar
  56. Mittelbach, G. G. 1986. Predator-mediated habitat use: Some consequences for species interactions. Environmental Biology of Fishes 16: 159–169.CrossRefGoogle Scholar
  57. Mittelbach, G. G. 1988. Competition among refuging sunfishes and effects of fish density on littoral zone invertebrates. Ecology 69: 614–623.CrossRefGoogle Scholar
  58. Mittelbach, G. G. and C. W. Osenberg. 1993. Stage-structured interactions in bluegill: Consequences of adult resource variation. Ecology 74: 2381–2394.Google Scholar
  59. Mittelbach, G. G., C. W. Osenberg, and M. A. Leibold. 1988. Trophic relations and ontogenetic niche shifts in aquatic ecosystems. In Size Structured Populations, eds. B. Ebenman and L. Persson, pp. 219–235. Springer Verlag, Berlin.CrossRefGoogle Scholar
  60. Neill, W. E. 1978. Experimental studies on factors limiting colonization by Daphnia pulex Leydig of coastal montane lakes in British Columbia. Canadian Journal of Zoology 56: 2498–2507.CrossRefGoogle Scholar
  61. Neill, W. E. 1988. Community responses to experimental nutrient perturbations in oligotrophic lakes: The importance of bottlenecks in size-structured populations. In Size-Structured Populations: Ecology and Evolution, eds. B. Eben-man and L. Persson, pp. 236–255. Springer-Verlag, Berlin.CrossRefGoogle Scholar
  62. Oksanen, L., S. D. Fretwell, J. Arruda, and P. Niemelä. 1981. Exploitation ecosystems in gradients of primary productivity. American Naturalist 118: 240–262.CrossRefGoogle Scholar
  63. Olson, M. A., G. G. Mittelbach, and C. W. Osenberg. 1995. Competition between predator and prey: resource-based mechanisms and implications for stage-structured dynamics Ecology. In press.Google Scholar
  64. Osenberg, C. W. 1989. Resource limitation, competition and the influence of life history in a freshwater snail community. Oecologia (Berlin) 79: 512–519.Google Scholar
  65. Osenberg, C. W., M. A. Olson, and G. G. Mittelbach 1994. Stage-structure in fishes: Resource productivity and competition gradients. In Theory and Application of Fish Feeding Ecology, eds. D. J. Stouder, K. L. Fresh, and R. J. Feller, University of South Carolina Press, Columbia, SC.Google Scholar
  66. Paine, R. T. 1966. Food web complexity and species diversity. American Naturalist 100: 6575.Google Scholar
  67. Paine, R. T. 1971. A short-term experimental investigation of resource partitioning in a New Zealand rocky intertical habitat. Ecology 52: 1096–1106.CrossRefGoogle Scholar
  68. Paine, R. T. 1980. Food webs: Linkage, interaction strength and community infrastructure. Journal of Animal Ecology 49: 667–685.CrossRefGoogle Scholar
  69. Paine, R. T. 1992. Food-web analysis through field measurement of per capita interaction strength. Nature 355: 73–75.CrossRefGoogle Scholar
  70. Persson, L. 1988. Asymmetries in competitive and predatory interactions in fish populations. In Size-Structured Populations: Ecology and Evolution, eds. B. Ebenman and L. Persson, pp. 203–218. Springer-Verlag, Berlin.CrossRefGoogle Scholar
  71. Persson, L. 1991. Behavioral response to predators reverses the outcome of competition between prey species. Behavioral Ecology and Sociobiology 28: 101–105.CrossRefGoogle Scholar
  72. Persson, L. 1993. Predator-mediated competition in prey refuges: The importance of habitat dependent prey resources. Oikos 68: 12–22.CrossRefGoogle Scholar
  73. Polis, G. A., C. A. Myers, and R. D. Holt. 1989. The ecology and evolution of intraguild predation: Potential competitors that eat each other. Annual Review of Ecology and Systematics 20: 297–330.CrossRefGoogle Scholar
  74. Power, M. E. 1990. Effects of fish in river food webs. Science 250: 811–814.Google Scholar
  75. Power, M. E., T. L. Dudley, and S. C. Cooper. 1989. Grazing catfish, fishing birds, and attached algae in a Panamanian stream. Environmental Biology of Fishes 26: 285–294.CrossRefGoogle Scholar
  76. Rahel, F. J. and Stein, R. A. 1988. Complex predator-prey interactions and predator intimidation among crayfish, piscivorous fish, and small benthic fish. Oecologia 75: 94–98.CrossRefGoogle Scholar
  77. Rosenheim, J. A., L. R. Wilhot, and C. A. Armer. 1993. Influence of intraguild predation among generalist predators on suppression of an herbivore population. Oecologia 96: 439–449.CrossRefGoogle Scholar
  78. Samson, D. A., T. E. Philippi, and D. W. Davidson. 1992. Granivory and competition as determinants of annual plant diversity in the Chihuahuan Desert. Oikos 65: 61–80.CrossRefGoogle Scholar
  79. Schaffer, W. S. 1981. Ecological abstraction: The consequences of reduced dimensionality in ecological models. Ecological Monographs 51: 383–401.CrossRefGoogle Scholar
  80. Schmitt, R. J. 1987. Indirect interactions between prey: Apparent competition, predator aggregation, and habitat segregation. Ecology 68: 1887 1897.Google Scholar
  81. Schoener, T. W. 1983. Field experiments on inter-specific competition. American Naturalist 122: 240–285.CrossRefGoogle Scholar
  82. Schoener, T. W. 1989. Food webs from the small to the large. Ecology 70: 1559–1589.CrossRefGoogle Scholar
  83. Schoener, T. W. 1993. On the relative importance of direct versus indirect effects in ecological communities. In Mutualism and Community Organization: Behavioral, Theoretical and Food Web Approaches, eds. H. Kawanabe, J. E. Cohen, and K. Iwasaki, pp. 365–411. Oxford University Press, Oxford, U.K.Google Scholar
  84. Seaburg, K. C. and J. B. Moyle. 1964. Feeding habits, digestion rates, and growth of some Minnesota warm water fishes. Transactions of the American Fisheries Society 93: 269–285.CrossRefGoogle Scholar
  85. Sih, A. 1987. Predator and prey lifestyles: An evolutionary and ecological overview. In Predation: Direct and Indirect Impacts in Aquatic Communities, eds. W. C. Kerfoot and A. Sih, pp. 203–224. University Press of New England, Hanover, NH.Google Scholar
  86. Sih, A., P. Crowley, M. McPeek, J. Petranka, and K. Strohmeier. 1985. Predation, competition and prey communities: A review of field experiments. Annual Review of Ecology and Systematics. 16: 269–311.CrossRefGoogle Scholar
  87. Skelly, D. K. and E. E. Werner. 1990. Behavioral and life-historical responses of larval American toads to an odonate predator. Ecology 71: 23132322.Google Scholar
  88. Spiller, D. A. and T. W. Schoener. 1988. An experimental study of the effect of lizards on web-spider communities. Ecological Monographs 58: 57–77.CrossRefGoogle Scholar
  89. Spiller, D. A. and T. W. Schoener. 1990a. Lizards reduce food consumption by spiders: Mechanisms and consequences. Oecologia 83: 150–161.PubMedCrossRefGoogle Scholar
  90. Spiller, D. A. and T. W. Schoener. 1990b. A terrestrial field experiment showing the impact of eliminating top predators on foliage damage. Nature 347: 469–472.CrossRefGoogle Scholar
  91. Spiller, D. A. and T. W. Schoener. 1994. Effects of top and intermediate predators in a terrestrial food web. Ecology 75: 182–196.CrossRefGoogle Scholar
  92. Strauss, S. Y. 1991. Indirect effects in community ecology: Their definition, study, and importance. Trends in Ecology and Evolution 6: 206–209.PubMedCrossRefGoogle Scholar
  93. Strong, D. R. 1992. Are trophic cascades all wet? Differentiation and donor-control in speciose ecosystems. Ecology 73: 747–754.CrossRefGoogle Scholar
  94. Tilman, D. 1987. The importance of interspecific competition. American Naturalist 129: 769–774.CrossRefGoogle Scholar
  95. Turner, A. and G. G. Mittelbach. 1990. Predator avoidance and community structure: Interactions among piscivores, planktivores, and plankton. Ecology 71: 2241–2254.CrossRefGoogle Scholar
  96. Vandermeer, J. 1980. Indirect mutualism: Variations on a theme by Stephen Levine. American Naturalist 116: 441–448.CrossRefGoogle Scholar
  97. Walters, C. J. and F. Juanes. 1993. Recruitment limitation as a consequence of natural selection for use of restricted feeding habitats and predation risk taking by juvenile fishes. Canadian Journal of Fisheries and Aquatic Science 50: 2058–2070.CrossRefGoogle Scholar
  98. Werner, E. E. 1991. Nonlethal effects of a predator on competitive interactions between two anuran larvae. Ecology 72: 1709–1720.CrossRefGoogle Scholar
  99. Werner, E. E. 1992. Individual behavior and higher-order species interactions. American Naturalist 140: S5 - S32.CrossRefGoogle Scholar
  100. Werner, E. E., and B. R. Anholt. 1993. Ecological consequences of the trade-off between growth and mortality rates mediated by foraging activity. American Naturalist 142: 242–272.PubMedCrossRefGoogle Scholar
  101. Werner, E. E., J. F. Gilliam, D. J. Hall, and G. G. Mittelbach. 1983a. An experimental test of the effects of predation risk on habitat use in fish. Ecology 64: 1540–1548.CrossRefGoogle Scholar
  102. Werner, E. E. and D. J. Hall. 1988. Ontogenetic habitat shifts in bluegill: The foraging rate-predation risk trade-off. Ecology 69: 1352–1366.CrossRefGoogle Scholar
  103. Werner, E. E., D. J. Hall, D. R. Laughlin, D. J. Wagner, L. A. Wilsmann, and F. C. Funk. 1977. Habitat partitioning in a freshwater fish community. Journal of the Fisheries Research Board of Canada 34: 360–370.CrossRefGoogle Scholar
  104. Werner, E. E., G. G. Mittelbach, D. J. Hall, and J. F. Gilliam. 1983b. Experimental tests of optimal habitat use in fish: The role of relative habitat profitability. Ecology 64: 1525–1539.CrossRefGoogle Scholar
  105. Wilson, D. S. 1986. Adaptive indirect effects. In Community Ecology, eds. J. Diamond and T. J. Case, pp. 437–444. Harper and Row, New York.Google Scholar
  106. Wootton, J. T. 1992. Indirect effects, prey susceptibility, and habitat selection: Impacts of birds on limpets and algae. Ecology 73: 981–991.CrossRefGoogle Scholar
  107. Wootton, J. T. 1993. Indirect effects and habitat use in an intertidal community: Interaction chains and interaction modifications. American Naturalist 141: 71–89.CrossRefGoogle Scholar
  108. Wootton, J. T. 1994. Predicting direct and indirect effects: An integrated approach using experiments and path analysis. Ecology 75: 151–165.CrossRefGoogle Scholar
  109. Wootton, T. and M. E. Power. 1993. Productivity, consumers, and the structure of a river food chain. Proceedings of the National Academy of Science, USA 90: 1384–1387.Google Scholar
  110. Worthen, W. B. and J. T. Moore. 1991. Higher-order interactions and indirect effects: A resolution using laboratory Drosophila communities. American Naturalist 138: 1092–1104.CrossRefGoogle Scholar
  111. Yodzis, P. 1988. The indeterminancy of ecological interactions. Ecology 69: 508–515.CrossRefGoogle Scholar
  112. Yodzis, P. 1989. An introduction to theoretical ecology. Harper and Row, New York.Google Scholar
  113. Yodzis, P. and S. Innis. 1992. Body size and consumer-resource dynamics. American Naturalist 139: 1151–1175.CrossRefGoogle Scholar
  114. Zaret, T. M. 1980. Predation and Freshwater Communities. Yale University Press, New Haven, CT.Google Scholar

Copyright information

© Springer Science+Business Media Dordrecht 1996

Authors and Affiliations

  • Peter A. Abrams
  • Bruce A. Menge
  • Gary G. Mittelbach
  • David A. Spiller
  • Peter Yodzis

There are no affiliations available

Personalised recommendations