Theoretical Ecology

, Volume 8, Issue 4, pp 399–417 | Cite as

The potential for alternative stable states in nutrient-enriched invaded grasslands

  • Ryan A. ChisholmEmail author
  • Duncan N. L. Menge
  • Tak Fung
  • Nicholas S. G. Williams
  • Simon A. Levin


Nutrient enrichment of native grasslands can promote invasion by exotic plant species, leading to reduced biodiversity and altered ecosystem function. Empirical evidence suggests that positive feedbacks may make such transitions difficult to reverse. We developed a mathematical model of grassland dynamics in which one group of species (native) is a better competitor for nitrogen (N) and another group (exotic) is a better competitor for light. We parameterized the model for a grassland community and reproduced observed transitions from a native- to an exotic-dominated state under N loading. Within known bounds of parameter values, both smooth and hysteretic transitions are plausible. The model also predicts that N loading alone is insufficient to achieve a transition to an exotic-dominated state on a timescale relevant to grassland management (a few decades), and that therefore some other disturbance (e.g., fire suppression or heaving grazing) must be present to accelerate it. The model predicts that to restore a grassland to a native-dominated state after N inputs have been reduced, fire and carbon supplements would be most effective. Further field research in N-enriched invaded grasslands is required to establish the strengths of positive feedbacks and, in turn, the consequences of anthropogenic modification of grasslands worldwide.


Grasslands Nutrient enrichment Invasion Hysteresis Bistability Alternative stable states 



RC and TF acknowledge the support of National University of Singapore grant R-154-000-551-133.

Supplementary material

12080_2015_258_MOESM1_ESM.docx (358 kb)
ESM 1 (DOCX 358 kb)


  1. Alpert P, Bone E, Holzapfel C (2000) Invasiveness, invasibility and the role of environmental stress in the spread of non-native plants. Perspect Plant Ecol Evol Syst 3:52–66. doi: 10.1078/1433-8319-00004 CrossRefGoogle Scholar
  2. Barlow TJ, Ross JR (2001) Vegetation of the Victorian volcanic plain. Proc Roy Soc Victoria 113:25–28Google Scholar
  3. Blumenthal DM, Jordan NR, Russelle MP (2003) Soil carbon addition controls weeds and facilitates prairie restoration. Ecol Appl 13:605–615. doi: 10.1890/1051-0761(2003)013[0605:scacwa];2 CrossRefGoogle Scholar
  4. Clark CM, Tilman D (2010) Recovery of plant diversity following N cessation: effects of recruitment, litter, and elevated N cycling. Ecology 91:3620–3630. doi: 10.1890/09-1268.1 CrossRefPubMedGoogle Scholar
  5. Clark CM, Morefield PE, Gilliam FS, Pardo LH (2013) Estimated losses of plant biodiversity in the United States from historical N deposition 1985–2010. Ecology 94:1441–1448CrossRefPubMedGoogle Scholar
  6. D’Antonio CM, Vitousek PM (1992) Biological invasions by exotic grasses, the grass fire cycle, and global change. Annu Rev Ecol Syst 23:63–87CrossRefGoogle Scholar
  7. Dorrough J, McIntyre S, Scroggie MP (2011) Individual plant species responses to phosphorus and livestock grazing. Aust J Bot 59:670–681CrossRefGoogle Scholar
  8. Galloway JN et al (2008) Transformation of the nitrogen cycle: recent trends, questions, and potential solutions. Science 320:889–892CrossRefPubMedGoogle Scholar
  9. Garden DL, Bolger TP (2001) Interaction of competition and management in regulating composition and sustainability of native pasture. In: Tow PG, Lazenby A (eds) Competition and succession in pasturesGoogle Scholar
  10. Groves RH, Keraitis K, Moore CWE (1973) Relative growth of Themeda australis and Poa labillardieri in pots in response to phosphorus and nitrogen. Aust J Bot 21:1–11CrossRefGoogle Scholar
  11. Hautier Y, Niklaus PA, Hector A (2009) Competition for light causes plant biodiversity loss after eutrophication. Science 324:636–638CrossRefPubMedGoogle Scholar
  12. Hobbs RJ, Norton DA (1996) Towards a conceptual framework for restoration ecology. Restor Ecol 4:93–110CrossRefGoogle Scholar
  13. Hobbs WO et al (2012) A 200-year perspective on alternative stable state theory and lake management from a biomanipulated shallow lake. Ecol Appl 22:1483–1496. doi: 10.1890/11-1485.1 CrossRefPubMedGoogle Scholar
  14. Holling CS (1973) Resilience and stability of ecological systems. Annu Rev Ecol Syst 4:1–23CrossRefGoogle Scholar
  15. Huenneke LF, Hamburg SP, Koide R, Mooney HA, Vitousek PM (1990) Effects of soil resources on plant invasion and community structure in Californian serpentine grassland. Ecology 71:478–491CrossRefGoogle Scholar
  16. Isbell F, Reich PB, Tilman D, Hobbie SE, Polasky S, Binder S (2013a) Nutrient enrichment, biodiversity loss, and consequent declines in ecosystem productivity. Proc Natl Acad Sci 110:11911–11916CrossRefPubMedPubMedCentralGoogle Scholar
  17. Isbell F, Tilman D, Polasky S, Binder S, Hawthorne P (2013b) Low biodiversity state persists two decades after cessation of nutrient enrichment. Ecol Lett 16:454–460. doi: 10.1111/ele.12066 CrossRefPubMedGoogle Scholar
  18. Jeppesen E, Søndergaard M, Meerhoff M, Lauridsen TL, Jensen JP (2007) Shallow lake restoration by nutrient loading reduction—some recent findings and challenges ahead. In: Shallow Lakes in a Changing World. Springer, pp 239–252Google Scholar
  19. Knapp A, Seastedt T (1986) Detritus accumulation limits productivity of tallgrass prairie. Bioscience 46:662–668CrossRefGoogle Scholar
  20. Knowlton N (1992) Thresholds and multiple stable states in coral-reef community dynamics. Am Zool 32:674–682CrossRefGoogle Scholar
  21. Lunt ID, Morgan JW (2002) The role of fire regimes in temperate lowland grasslands of southeastern Australia. In: Bradstock RA, Williams JE, Gill M (eds) Flammable Australia. Cambridge University Press, Cambridge, pp 177–196Google Scholar
  22. Mack RN (1989) Temperate grasslands vulnerable to plant invasions: characteristics and consequences. In: Drake JA, Mooney HA, di Castri F, Groves RH, Kruger FJ, Rejmánek M, Williamson M (eds) Biological invasions: a global perspective. Wiley, Chichester, pp 155–179Google Scholar
  23. May RM (1977) Thresholds and breakpoints in ecosystems with a multiplicity of stable states. Nature 269:471–477CrossRefGoogle Scholar
  24. Menge DNL, Levin SA, Hedin LO (2008) Evolutionary tradeoffs can select against nitrogen fixation and thereby maintain nitrogen limitation. Proc Natl Acad Sci 105:1573–1578CrossRefPubMedPubMedCentralGoogle Scholar
  25. Morgan JW (1998) Patterns of invasion of an urban remnant of a species-rich grassland in southeastern Australia by non-native plant species. J Veg Sci 9:181–190CrossRefGoogle Scholar
  26. Morgan JW, Lunt ID (1999) Effects of time-since-fire on the tussock dynamics of a dominant grass (Themeda triandra) in a temperate Australian grassland. Biol Conserv 88:379–386. doi: 10.1016/S0006-3207(98)00112-8 CrossRefGoogle Scholar
  27. Perrings C, Walker B (1997) Biodiversity, resilience and the control of ecological-economic systems: the case of fire-driven rangelands. Ecol Econ 22:73–83CrossRefGoogle Scholar
  28. Prober S, Lunt I (2009) Restoration of Themeda australis swards suppresses soil nitrate and enhances ecological resistance to invasion by exotic annuals. Biol Invasions 11:171CrossRefGoogle Scholar
  29. Prober SM, Thiele KR (2005) Restoring Australia’s temperate grasslands and grassy woodlands: integrating function and diversity. Ecol Manage Restor 6:16–27. doi: 10.1111/j.1442-8903.2005.00215.x CrossRefGoogle Scholar
  30. Prober SM, Thiele KR, Lunt ID (2002) Identifying ecological barriers to restoration in temperate grassy woodlands: soil changes associated with different degradation states. Aust J Bot 50:699–712. doi: 10.1071/bt02052 CrossRefGoogle Scholar
  31. Prober SM, Thiele KR, Lunt ID, Koen TB (2005) Restoring ecological function in temperate grassy woodlands: manipulating soil nutrients, exotic annuals and native perennial grasses through carbon supplements and spring burns. J Appl Ecol 42:1073–1085. doi: 10.1111/j.1365-2664.2005.01095.x CrossRefGoogle Scholar
  32. Prober SM, Lunt ID, Morgan JW (2008) Rapid internal plant-soil feedbacks lead to alternative stable states in temperate Australian grassy woodlands. In: Hobbs RJ, Suding KN (eds) New models for ecosystem dynamics and restoration. Island, USA, pp 156–168Google Scholar
  33. Scheffer M, Hosper SH, Meijer ML, Moss B, Jeppesen E (1993) Alternative equilibria in shallow lakes. Trends Ecol Evol 8:275–279CrossRefPubMedGoogle Scholar
  34. Scheffer M, Carpenter S, Foley JA, Folke C, Walker B (2001) Catastrophic shifts in ecosystems. Nature 413:591–596CrossRefPubMedGoogle Scholar
  35. Seabloom EW et al (2013) Predicting invasion in grassland ecosystems: is exotic dominance the real embarrassment of richness? Glob Chang Biol 19:3677–3687. doi: 10.1111/gcb.12370 CrossRefPubMedGoogle Scholar
  36. Smil V (2000) Phosphorus in the environment: natural flows and human interferences. Annu Rev Energy Environ 25:53–88CrossRefGoogle Scholar
  37. Standish RJ, Cramer VA, Wild SL, Hobbs RJ (2007) Seed dispersal and recruitment limitation are barriers to native recolonisation of old-fields in western. Aust J Appl Ecol 44:434–445Google Scholar
  38. Staver AC, Archibald S, Levin S (2011) Tree cover in sub-Saharan Africa: rainfall and fire constrain forest and savanna as alternative stable states. Ecology 92:1063–1072. doi: 10.1890/10-1684.1 CrossRefPubMedGoogle Scholar
  39. Stevens CJ, Dise NB, Mountford JO, Gowing DJ (2004) Impact of nitrogen deposition on the species richness of grasslands. Science 303:1876–1879CrossRefPubMedGoogle Scholar
  40. Suding KN, Gross KL (2006) The dynamic nature of ecological systems: multiple stable states and restoration trajectories. In: Falk D, Palmer MA, Zedler J (eds) Foundations of restoration ecology. Island, Washington, pp 190–209Google Scholar
  41. Suding KN, Gross KL, Houseman GR (2004a) Alternative states and positive feedbacks in restoration ecology. Trends Ecol Evol 19:46–53. doi: 10.1016/j.tree.2003.10.005 CrossRefPubMedGoogle Scholar
  42. Suding KN, LeJeune KD, Seastedt TR (2004b) Competitive impacts and responses of an invasive weed: dependencies on nitrogen and phosphorus availability. Oecologia 141:526–535CrossRefPubMedGoogle Scholar
  43. Tilman D (1982) Resource competition and community structure. Princeton University Press, PrincetonGoogle Scholar
  44. Tilman D, Lehman CL, Thomson KT (1997) Plant diversity and ecosystem productivity: theoretical considerations. Proc Natl Acad Sci 94:1857–1861CrossRefPubMedPubMedCentralGoogle Scholar
  45. Tilman D, Isbell F, Cowles JM (2014) Biodiversity and ecosystem functioning. Annu Rev Ecol Evol Syst 45:471–493CrossRefGoogle Scholar
  46. Vitousek PM, Mooney HA, Lubchenco J, Melillo JM (1997) Human domination of Earth’s ecosystems. Science 277:494–499CrossRefGoogle Scholar
  47. Wedin DA, Tilman D (1996) Influence of nitrogen loading and species composition on the carbon balance of grasslands. Science 274:1720–1723. doi: 10.1126/science.274.5293.1720 CrossRefPubMedGoogle Scholar
  48. Williams NSG, McDonnell MJ, Seager EJ (2005) Factors influencing the loss of an endangered ecosystem in an urbanising landscape: a case study of native grasslands from Melbourne. Aust Landsc Urban Plann 71:35–49. doi: 10.1016/j.landurbplan.2004.01.006 CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2015

Authors and Affiliations

  • Ryan A. Chisholm
    • 1
    Email author
  • Duncan N. L. Menge
    • 2
  • Tak Fung
    • 1
  • Nicholas S. G. Williams
    • 3
    • 4
  • Simon A. Levin
    • 5
  1. 1.Department of Biological SciencesNational University of SingaporeSingaporeSingapore
  2. 2.Department of Ecology, Evolution and Environmental BiologyColumbia UniversityNew YorkUSA
  3. 3.School of Ecosystem and Forest SciencesThe University of MelbourneVictoriaAustralia
  4. 4.Australian Research Centre for Urban EcologyRoyal Botanic Gardens MelbourneVictoriaAustralia
  5. 5.Department of Ecology and Evolutionary BiologyPrinceton UniversityPrincetonUSA

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