The paradox of enrichment in metaecosystems

American Naturalist

Volumn 184, Issue 6, 2014, Pages 752-763

  Gounand, Isabelle ^a,b   Mouquet, Nicolas ^a   Canard, Elsa ^a   Guichard, Frédéric ^c   Hauzy, Céline ^d   Gravel, Dominique ^b  

^a INSTITUT DES SCIENCES DE L EVOLUTION   (France)

^b UNIVERSITÉ DU QUÉBEC À RIMOUSKI   (Canada)

^c MCGILL UNIVERSITY   (Canada)

^d SORBONNE UNIVERSITÉ   (France)

Author keywords

Alternative stable states; Dispersal; Fertility; Source sink dynamics; Spatial heterogeneity; Stability

Indexed keywords

DETRITUS; ECOSYSTEM; NUTRIENT ENRICHMENT; PRODUCER-SCROUNGER INTERACTION; SPATIAL ANALYSIS;

AQUATIC SPECIES; ECOSYSTEM; FOOD CHAIN; POPULATION DYNAMICS; THEORETICAL MODEL;

AQUATIC ORGANISMS; ECOSYSTEM; FOOD CHAIN; MODELS, THEORETICAL; POPULATION DYNAMICS;

EID: 84914154932     PISSN: 00030147     EISSN: None     Source Type: Journal    
DOI: 10.1086/678406     Document Type: Article

References (113)

1. Abbas, F., J. Merlet, N. Morellet, H. Verheyden, A. J. M. Hewison, B. Cargnelutti, J. M. Angibault, et al. 2012. Roe deer may markedly alter forest nitrogen and phosphorus budgets across Europe. Oikos 121:1271-1278.
2. Abbott, K. C. 2011. A dispersal-induced paradox: synchrony and stability in stochastic metapopulations. Ecology Letters 14:1158-1169.
3. Abrams, P. A., and L. Ruokolainen. 2011. How does adaptive consumer movement affect population dynamics in consumerresource metacommunities with homogeneous patches? Journal of Theoretical Biology 277:99-110.
4. Abrams, P. A., L. Ruokolainen, B. J. Shuter, and K. S. McCann. 2012. Harvesting creates ecological traps: consequences of invisible mortality risks in predator-prey metacommunities. Ecology 93:281-293.
5. Amarasekare, P. 2007. Spatial dynamics of communities with intraguild predation: the role of dispersal strategies. American Naturalist 170:819-831.
6. Amarasekare, P. 2008. Spatial dynamics of foodwebs. Annual Review of Ecology, Evolution, and Systematics 39:479-500.
7. Amezcua, A., and M. Holyoak. 2000. Empirical evidence for predatorprey source-sink dynamics. Ecology 81:3078-3098.
8. Attayde, J. L., and J. Ripa. 2008. The coupling between grazing and detritus food chains and the strength of trophic cascades across a gradient of nutrient enrichment. Ecosystems 11:980-990.
9. Auger, P., B. W. Kooi, R. Bravo de la Parra, and J.-C. Poggiale. 2006. Bifurcation analysis of a predator-prey model with predators using hawk and dove tactics. Journal of Theoretical Biology 238:597-607.
10. Becks, L., F. M. Hilker, H. Malchow, K. Jürgens, and H. Arndt. 2005. Experimental demonstration of chaos in a microbial food web. Nature 435:1226-9.
11. Bjornsen, P., B. Riemann, S. Horsted, T. Nielsen, and J. Pock-Sten. 1988. Trophic interactions between heterotrophic nanoflagellates and bacterioplankton in manipulated seawater enclosures. Limnology and Oceanography 33:409-420.
12. Blanchard, J. L., R. Law, M. D. Castle, and S. Jennings. 2010. Coupled energy pathways and the resilience of size-structured food webs. Theoretical Ecology 4:289-300.
13. Briggs, C. J., and M. F. Hoopes. 2004. Stabilizing effects in spatial parasitoid-host and predator-prey models: a review. Theoretical Population Biology 65:299-315.
14. Brockhurst, M. A., A. Buckling, and P. B. Rainey. 2006. Spatial heterogeneity and the stability of host-parasite coexistence. Journal of Evolutionary Biology 19:374-379.
15. Brunsting, A., and G. Heil. 1985. The role of nutrients in the interactions between a herbivorous beetle and some competing plant species in heathlands. Oikos 44:23-26.
16. Cabrera, F. M. I. 2011. Deterministic approach to the study of the interaction predator-prey in a chemostat with predator mutual interference: implications for the paradox of enrichment. Ecological Modelling 222:598-605.
17. Carpenter, A. S. R., N. F. Caraco, D. L. Correll, R. W. Howarth, A. N. Sharpley, and V. H. Smith. 1998. Nonpoint pollution of surface waters with phosphorus and nitrogen. Ecological Applications 8: 559-568.
18. Carpenter, S. R. 2005. Eutrophication of aquatic ecosystems: bistability and soil phosphorus. Proceedings of the National Academy of Sciences of the USA 102:10002-10005.
19. Casini, M., T. Blenckner, C. Möllmann, A. Gårdmark, M. Lindegren, M. Llope, G. Kornilovs, et al. 2012. Predator transitory spillover induces trophic cascades in ecological sinks. Proceedings of the National Academy of Sciences of the USA 109:8185-8189.
20. Chakraborty, S., and J. Chattopadhyay. 2011. Effect of cannibalism on a predator-prey system with nutritional value: a model based study. Dynamical Systems 26:13-22.
21. Cross, W. F., J. B. Wallace, A. D. Rosemond, and S. L. Eggert. 2006. Whole-system nutrient enrichment increases secondary production in a detritus-based ecosystem. Ecology 87:1556-1565.
22. Daugherty, M. P. 2011. Host plant quality, spatial heterogeneity, and the stability of mite predator-prey dynamics. Experimental and Applied Acarology 53:311-22.
23. Davic, R. D., and H. H. Welsh. 2004. On the ecological roles of salamanders. Annual Review of Ecology, Evolution, and Systematics 35:405-434.
24. De Roos, A. M., E. McCauley, and W. G. Wilson. 1991. Mobility versus density-limited predator-prey dynamics on different spatial scales. Proceedings of the Royal Society B: Biological Sciences 246: 117-122.
25. De Roos, A. M., E. McCauley, and W. G. Wilson. 1998. Pattern formation and the spatial scale of interaction between predators and their prey. Theoretical Ecology 53:108-130.
26. Duce, R. A., J. LaRoche, K. Altieri, K. R. Arrigo, A. R. Baker, D. G. Capone, S. Cornell, et al. 2008. Impacts of atmospheric anthropogenic nitrogen on the open ocean. Science 320:893-897.
27. Earn, D. J. D. 2000. Coherence and conservation. Science 290:1360-1364.
28. Edwards, A. 2001. Adding detritus to a nutrient-phytoplankton-zooplankton model: a dynamical-systems approach. Journal of Plankton Research 23:389-413.
29. Ellner, S. P., E. McCauley, B. E. Kendall, C. J. Briggs, P. R. Hosseini, S. N. Wood, A. Janssen, et al. 2001. Habitat structure and population persistence in an experimental community. Nature 412: 538-543.
30. Elser, J. J., M. Kyle, L. Steger, K. R. Nydick, and J. S. Baron. 2009. Nutrient availability and phytoplankton nutrient limitation across a gradient of atmospheric nitrogen deposition. Ecology 90:3062-3073.
31. Fisher, D., J. Steiner, D. Endale, J. Stuedemann, H. Schomberg, A. Franzluebbers, and S. Wilkinson. 2000. The relationship of land use practices to surface water quality in the Upper Oconee Watershed of Georgia. Forest Ecology and Management 128:39-48.
32. Fukami, T., D. A Wardle, P. J. Bellingham, C. P. H. Mulder, D. R. Towns, G. W. Yeates, K. I. Bonner, et al. 2006. Above- and belowground impacts of introduced predators in seabird-dominated island ecosystems. Ecology Letters 9:1299-307.
33. Fussmann, G. F. 2000. Crossing the Hopf bifurcation in a live predator- prey system. Science 290:1358-1360.
34. Genkai-Kato, M., and N. Yamamura. 1999. Unpalatable prey resolves the paradox of enrichment. Proceedings of the Royal Society B: Biological Sciences 266:1215-1219.
35. Goldwyn, E. E., and A. Hastings. 2008. When can dispersal synchronize populations? Theoretical Population Biology 73:395-402.
36. Goldwyn, E. E., and A. Hastings. 2009. Small heterogeneity has large effects on synchronization of ecological oscillators. Bulletin of Mathematical Biology 71:130-44.
37. Gratton, C., J. Donaldson, and M. J. Vander Zanden. 2008. Ecosystem linkages between lakes and the surrounding terrestrial landscape in northeast Iceland. Ecosystems 11:764-774.
38. Gravel, D., F. Guichard, M. Loreau, and N. Mouquet. 2010a. Source and sink dynamics in meta-ecosystems. Ecology 91:2172-2184.
39. Gravel, D., N. Mouquet, M. Loreau, and F. Guichard. 2010b. Patch dynamics, persistence, and species coexistence in metaecosystems. American Naturalist 176:289-302.
40. Greaver, T. L., T. J. Sullivan, J. D. Herrick, M. C. Barber, J. S. Baron, B. J. Cosby, M. E. Deerhake, et al. 2012. Ecological effects of nitrogen and sulfur air pollution in the US: what do we know? Frontiers in Ecology and the Environment 10:365-372.
41. Griffiths, J. R., D. E. Schindler, and L. W. Seeb. 2013. How stock of origin affects performance of individuals across a meta-ecosystem: an example from sockeye salmon. PLoS ONE 8:e58584.
42. Halpern, B. S., K. A. Selkoe, F. Micheli, and C. V. Kappel. 2007. Evaluating and ranking the vulnerability of global marine ecosystems to anthropogenic threats. Conservation Biology 21:1301-1315.
43. Hauzy, C., M. Gauduchon, F. Hulot, and M. Loreau. 2010a. Densitydependent dispersal and relative dispersal affect the stability of predator-prey metacommunities. Journal of Theoretical Biology 266:458-469.
44. Hauzy, C., G. Nadin, E. Canard, I. Gounand, N. Mouquet, and B. Ebenman. 2013. Confronting the paradox of enrichment to the metacommunity perspective. PLoS ONE 8:e82969.
45. Hauzy, C., T. Tully, T. Spataro, G. Paul, and R. Arditi. 2010b. Spatial heterogeneity and functional response: an experiment in microcosms with varying obstacle densities. Oecologia (Berlin) 163:625-636.
46. Herbert, R. A. 1999. Nitrogen cycling in coastal marine ecosystems. FEMS Microbiology Reviews 23:563-590.
47. Hilker, F. M., and K. Schmitz. 2008. Disease-induced stabilization of predator-prey oscillations. Journal of Theoretical Biology 255:299-306.
48. Holling, C. S. 1959. Some characteristics of simple types of predation and parasitism. Canadian Entomologist 91:385-398.
49. Holyoak, M. 2000. Effects of nutrient enrichment on predator-prey metapopulation dynamics. Journal of Animal Ecology 69:985-997.
50. Holyoak, M., and S. Lawler. 1996. Persistence of an extinction-prone predator-prey interaction through metapopulation dynamics. Ecology 77:1867-1879.
51. Howeth, J. G., and M. A. Leibold. 2013. Predation inhibits the positive effect of dispersal on intraspecific and interspecific synchrony in pond metacommunities. Ecology 94:2220-2228.
52. Huffaker, C. 1958. Experimental studies on predation: dispersion factors and predator-prey oscillations. Hilgardia 27:795-835.
53. Jansen, V. 1995. Regulation of predator-prey systems through spatial interactions: a possible solution to the paradox of enrichment. Oikos 74:384-390.
54. Jansen, V. 1999. Phase locking: another cause of synchronicity in predator- prey systems. Trends in Ecology and Evolution 14:278-279.
55. Jansen, V. 2001. The dynamics of two diffusively coupled predatorprey populations. Theoretical Population Biology 59:119-131.
56. Jefferies, R. L., R. F. Rockwell, and K. F. Abraham. 2004. Agricultural food subsidies, migratory connectivity and large-scale disturbance in Arctic coastal systems: a case study. Integrative and Comparative Biology 44:130-139.
57. Kiørboe, T. 2001. Formation and fate of marine snow: small-scale processes with large-scale implications. Scientia Marina 65:57-71.
58. Klepac, P., M. G. Neubert, and P. van den Driessche. 2007. Dispersal delays, predator-prey stability, and the paradox of enrichment. Theoretical Population Biology 71:436-444.
59. Koelle, K., and J. Vandermeer. 2005. Dispersal-induced desynchronization: from metapopulations to metacommunities. Ecology Letters 8:167-175.
60. Krupa, S. 2003. Effects of atmospheric ammonia (NH3) on terrestrial vegetation: a review. Environmental Pollution 124:179-221.
61. Lavery, T. J., B. Roudnew, P. Gill, J. Seymour, L. Seuront, G. Johnson, J. G. Mitchell, et al. 2010. Iron defecation by sperm whales stimulates carbon export in the Southern Ocean. Proceedings of the Royal Society B: Biological Sciences 277:3527-3531.
62. Lecomte, J., K. Boudjemadi, F. Sarrazin, K. Cally, and J. Clobert. 2004. Connectivity and homogenisation of population sizes: an experimental approach in Lacerta vivipara. Journal of Animal Ecology 73:179-189.
63. Liebhold, A., W. D. Koenig, and O. N. Bjørnstad. 2004. Spatial synchrony in population dynamics. Annual Review of Ecology, Evolution, and Systematics 35:467-490.
64. Loreau, M., T. Daufresne, A. Gonzalez, D. Gravel, F. Guichard, S. J. Leroux, N. Loeuille, et al. 2012. Unifying sources and sinks in ecology and Earth sciences. Biological Reviews of the Cambridge Philosophical Society 88:365-379.
65. Loreau, M., N. Mouquet, and R. D. Holt. 2003. Meta-ecosystems: a theoretical framework for a spatial ecosystem ecology. Ecology Letters 6:673-679.
66. Luckinbill, L. S. 1973. Coexistence in laboratory populations of Paramecium aurelia and its predator Didinium nasutum. Ecology 54: 1320-1327.
67. Marleau, J. N., F. Guichard, F. Mallard, and M. Loreau. 2010. Nutrient flows between ecosystems can destabilize simple food chains. Journal of Theoretical Biology 266:162-174.
68. Maron, J., J. Estes, D. Croll, E. Danner, S. Elmendorf, and S. Buckelew. 2006. An introduced predator alters Aleutian Island plant communities by thwarting nutrient subsidies. Ecological Monographs 76:3-24.
69. Maser, G. L., F. Guichard, and K. S. McCann. 2007. Weak trophic interactions and the balance of enriched metacommunities. Journal of Theoretical Biology 247:337-345.
70. Massol, F., D. Gravel, N. Mouquet, M. W. Cadotte, T. Fukami, and M. A. Leibold. 2011. Linking community and ecosystem dynamics through spatial ecology. Ecology Letters 14:313-323.
71. May, R. M., G. R. Conway, M. P. Hassell, and T. R. Southwood. 1974. Time delays, density-dependence and single-species oscillations. Journal of Animal Ecology 43:747-770.
72. McAllister, C., R. LeBrasseur, and M. Rosenzweig. 1972. Stability of enriched aquatic Ecosystems. Science 175:562-565.
73. Meyer, K. M., M. Vos, W. M. Mooij, W. H. G. Hol, A. J. Termorshuizen, and W. H. van der Putten. 2012. Testing the paradox of enrichment along a land use gradient in a multitrophic aboveground and belowground community. PLoS ONE 7:e49034.
74. Moore, J. C., E. L. Berlow, D. C. Coleman, P. C. Ruiter, Q. Dong, A. Hastings, N. C. Johnson, et al. 2004. Detritus, trophic dynamics and biodiversity. Ecology Letters 7:584-600.
75. Morozov, A., E. Arashkevich, A. Nikishina, and K. Solovyev. 2011. Nutrient-rich plankton communities stabilized via predator-prey interactions: revisiting the role of vertical heterogeneity. Mathematical Medicine and Biology 28:185-215.
76. Murdoch, W. W., C. J. Briggs, and R. M. Nisbet. 2003. Consumerresource dynamics. Princeton University Press, Princeton, NJ.
77. Murdoch, W. W., R. Nisbet, E. McCauley, and W. S. C. Gurneyk. 1998. Plankton abundance and dynamics across nutrient levels: tests of hypotheses. Ecology 79:1339-1356.
78. Myers, J., and B. Post. 1981. Plant nitrogen and fluctuations of insect populations : a test with the cinnabar moth-tansy ragwort system. Oecologia (Berlin) 48:151-156.
79. Neubert, M. G., P. Klepac, and P. van den Driessche. 2002. Stabilizing dispersal delays in predator-prey metapopulation models. Theoretical Population Biology 61:339-347.
80. Nisbet, R. M., A. M. de Roos, W. G. Wilson, and R. E. Snyder. 1998. Discrete consumers, small scale resource heterogeneity, and population stability. Ecology Letters 1:34-37.
81. Otto, S. B., B. C. Rall, and U. Brose. 2007. Allometric degree distributions facilitate food-web stability. Nature 450:1226-1229.
82. Paetzold, A., M. Smith, P. Warren, and L. Maltby. 2011. Environmental impact propagated by cross-system subsidy: chronic stream pollution controls riparian spider populations. Ecology 92:1711-1716.
83. Poggiale, J., M. Gauduchon, and P. Auger. 2008. Enrichment paradox induced by spatial heterogeneity in a phytoplankton-zooplankton system. Mathematical Modelling of Natural Phenomenon 3:87-102.
84. Polis, G., W. Anderson, and R. D. Holt. 1997. Toward an integration of landscape and food web ecology: the dynamics of spatially subsidized food webs. Annual Review of Ecology and Systematics 28: 289-316.
85. Rip, J. M. K., and K. S. McCann. 2011. Cross-ecosystem differences in stability and the principle of energy flux. Ecology Letters 14: 733-740.
86. Roman, J., and J. J. McCarthy. 2010. The whale pump: marine mammals enhance primary productivity in a coastal basin. PLoS ONE 5:e13255.
87. Rooney, N., K. McCann, G. Gellner, and J. C. Moore. 2006. Structural asymmetry and the stability of diverse food webs. Nature 442:265-269.
88. Rösel, S., A. Rychła, C. Wurzbacher, and H.-P. Grossart. 2012. Effects of pollen leaching and microbial degradation on organic carbon and nutrient availability in lake water. Aquatic Sciences 74:87-99.
89. Rosenzweig, M. 1971. Paradox of enrichment: destabilization of exploitation ecosystems in ecological time. Science 171:385-387.
90. Roy, S., and J. Chattopadhyay. 2007. The stability of ecosystems: a brief overview of the paradox of enrichment. Journal of Biosciences 32:421-428.
91. Ruokolainen, L., P. A. Abrams, K. S. McCann, and B. J. Shuter. 2011. The roles of spatial heterogeneity and adaptive movement in stabilizing (or destabilizing) simple metacommunities. Journal of Theoretical Biology 291:76-87.
92. Ryabov, A. B., and B. Blasius. 2011. A graphical theory of competition on spatial resource gradients. Ecology Letters 14:220-228.
93. Schindler, D. E., and M. D. Scheuerell. 2002. Habitat coupling in lake ecosystems. Oikos 98:177-189.
94. Shen, W., Y. Lin, G. D. Jenerette, and J. Wu. 2011. Blowing litter across a landscape: effects on ecosystem nutrient flux and implications for landscape management. Landscape Ecology 26:629-644.
95. Simon, M., H. Grossart, B. Schweitzer, and H. Ploug. 2002. Microbial ecology of organic aggregates in aquatic ecosystems. Aquatic Microbial Ecology 28:175-211.
96. Soetaert, K., and P. M. J. Herman. 2009. A practical guide to ecological modelling: using R as a simulation platform. Springer, New York.
97. Sugie, J., and Y. Saito. 2012. Uniqueness of limit cycles in a Rosenzweig- MacArthur model with prey immigration. SIAM Journal on Applied Mathematics 72:299-316.
98. Suzuki, K., and T. Yoshida. 2012. Non-random spatial coupling induces desynchronization, chaos and multistability in a predatorprey- resource system. Journal of Theoretical Biology 300:81-90.
99. Trzcinski, M., S. Walde, and P. Taylor. 2005. Stability of pitcher-plant microfaunal populations depends on food web structure. Oikos 110:146-154.
100. Urabe, J., and R. W. Sterner. 1996. Regulation of herbivore growth by the balance of light and nutrients. Proceedings of the National Academy of Sciences of the USA 93:8465-8469.
101. Van Baalen, M., V. Krivan, P. C. van Rijn, and M. W. Sabelis. 2001. Alternative food, switching predators, and the persistence of predator- prey systems. American Naturalist 157:512-524.
102. Van der Heijden, M. G., R. D. Bardgett, and N. M. van Straalen. 2008. The unseen majority: soil microbes as drivers of plant diversity and productivity in terrestrial ecosystems. Ecology Letters 11:296-310.
103. Vandermeer, J. 2004. Coupled oscillations in food webs: balancing competition and mutualism in simple ecological models. American Naturalist 163:857-867.
104. Van der Stap, I., M. Vos, B. W. Kooi, B. T. M. Mulling, E. Donk, and W. M. Mooij. 2009. Algal defenses, population stability, and the risk of herbivore extinctions: a chemostat model and experiment. Ecological Research 24:1145-1153.
105. Varpe, O., O. Fiksen, and A. Slotte. 2005. Meta-ecosystems and biological energy transport from ocean to coast: the ecological importance of herring migration. Oecologia (Berlin) 146:443-451.
106. Vasseur, D. A., and J.W. Fox. 2009. Phase-locking and environmental fluctuations generate synchrony in a predator-prey community. Nature 460:1007-1010.
107. Verschoor, A. M., M. Vos, and I. van der Stap. 2004. Inducible defences prevent strong population fluctuations in bi- and tritrophic food chains. Ecology Letters 7:1143-1148.
108. Vogwill, T., A. Fenton, and M. A. Brockhurst. 2009. Dispersal and natural enemies interact to drive spatial synchrony and decrease stability in patchy populations. Ecology Letters 12:1194-1200.
109. Vos, M., B. Kooi, D. L. DeAngelis, and W. M. Mooij. 2004. Inducible defences and the paradox of enrichment. Oikos 105:471-480.
110. Wetzel, P., A. van der Valk, S. Newman, C. Coronado, T. Troxler-Gann, D. Childers, W. Orem, et al. 2009. Heterogeneity of phosphorus distribution in a patterned landscape, the Florida Everglades. Plant Ecology 200:83-90.
111. Wilson, E. E., and E. M.Wolkovich. 2011. Scavenging: howcarnivores and carrion structure communities. Trends in Ecology and Evolution 26:129-135.
112. Wilson, W., A. M. de Roos, and E. McCauley. 1993. Spatial instabilities within the diffusive Lotka-Volterra system: individual-based simulation results. Theoretical Population Biology 43:91-127.
113. Wolf, A., C. E. Doughty, and Y. Malhi. 2013. Lateral diffusion of nutrients by mammalian herbivores in terrestrial ecosystems. PLoS ONE 8:e71352.