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Coral Reefs

, Volume 35, Issue 3, pp 857–865 | Cite as

Multiple feedbacks and the prevalence of alternate stable states on coral reefs

  • Ingrid A. van de LeemputEmail author
  • Terry P. Hughes
  • Egbert H. van Nes
  • Marten Scheffer
Report

Abstract

The prevalence of alternate stable states on coral reefs has been disputed, although there is universal agreement that many reefs have experienced substantial losses of coral cover. Alternate stable states require a strong positive feedback that causes self-reinforcing runaway change when a threshold is passed. Here we use a simple model of the dynamics of corals, macroalgae and herbivores to illustrate that even weak positive feedbacks that individually cannot lead to alternate stable states can nonetheless do so if they act in concert and reinforce each other. Since the strength of feedbacks varies over time and space, our results imply that we should not reject or accept the general hypothesis that alternate stable states occur in coral reefs. Instead, it is plausible that shifts between alternate stable states can occur sporadically, or on some reefs but not others depending on local conditions. Therefore, we should aim at a better mechanistic understanding of when and why alternate stable states may occur. Our modelling results point to an urgent need to recognize, quantify, and understand feedbacks, and to reorient management interventions to focus more on the mechanisms that cause abrupt transitions between alternate states.

Keywords

Positive feedback Hysteresis Critical transitions Resilience Alternate stable states Coral reefs 

Notes

Acknowledgments

This research was funded by the Australian Research Council (ARC) Centre of Excellence Program, and by European Research Council grants. IL is supported by Ecoshape Building with Nature, and by a visiting fellowship from the ARC Centre of Excellence for Coral Reef Studies. We thank D. Bellwood, N. Graham, and B. Walker for their positive feedback on the manuscript, and M. Young for technical assistance.

Supplementary material

338_2016_1439_MOESM1_ESM.docx (996 kb)
Supplementary material 1 (DOCX 996 kb)

References

  1. Ayre DJ, Hughes TP (2004) Climate change, genotypic diversity and gene flow in reef-building corals. Ecol Lett 7:273–278CrossRefGoogle Scholar
  2. Bellwood DR, Hughes TP, Folke C, Nyström M (2004) Confronting the coral reef crisis. Nature 429:827–833CrossRefPubMedGoogle Scholar
  3. Blackwood JC, Hastings A, Mumby PJ (2010) The effect of fishing on hysteresis in Caribbean coral reefs. Theor Ecol 5:105–114CrossRefGoogle Scholar
  4. Blackwood JC, Hastings A, Mumby PJ (2011) A model-based approach to determine the long-term effects of multiple interacting stressors on coral reefs. Ecol Appl 21:2722–2733CrossRefPubMedGoogle Scholar
  5. Bruno JF, Sweatman H, Precht WF, Selig ER, Schutte VGW (2009) Assessing evidence of phase shifts from coral to macroalgal dominance on coral reefs. Ecology 90:1478–1484CrossRefGoogle Scholar
  6. Connell JH (1997) Disturbance and recovery of coral assemblages. Coral Reefs 16:S101–S113CrossRefGoogle Scholar
  7. Connell JH, Hughes TP, Wallace CC (1997) A 30-year study of coral abundance, recruitment, and disturbance at several scales in space and time. Ecol Monogr 67:461–488CrossRefGoogle Scholar
  8. Dakos V, Carpenter SR, Brock WA, Ellison AM, Guttal V, Ives AR, Kéfi S, Livina V, Seekell DA, van Nes EH, Scheffer M (2012) Methods for detecting early warnings of critical transitions in time series illustrated using simulated ecological data. PLoS ONE 7:e41010CrossRefPubMedPubMedCentralGoogle Scholar
  9. DeAngelis DL, Post WM, Travis CC (1986) Positive feedback in natural systems. Springer, BerlinCrossRefGoogle Scholar
  10. Diaz-Pulido G, McCook LJ (2003) Relative roles of herbivory and nutrients in the recruitment of coral-reef seaweeds. Ecology 84:2026–2033CrossRefGoogle Scholar
  11. Done TJ (1992) Phase shifts in coral reef communities and their ecological significance. Hydrobiologia 247:121–132CrossRefGoogle Scholar
  12. Dudgeon SR, Aronson RB, Bruno JF, Precht WF (2010) Phase shifts and stable states on coral reefs. Mar Ecol Prog Ser 413:201–216CrossRefGoogle Scholar
  13. Friedlander AM, Parrish JD (1998) Habitat characteristics affecting fish assemblages on a Hawaiian coral reef. J Exp Mar Bio Ecol 224:1–30CrossRefGoogle Scholar
  14. Fung T, Seymour R, Johnson C (2011) Alternative stable states and phase shifts in coral reefs under anthropogenic stress. Ecology 92:967–982CrossRefPubMedGoogle Scholar
  15. Graham NAJ, Nash KL, Kool JT (2011) Coral reef recovery dynamics in a changing world. Coral Reefs 30:283–294CrossRefGoogle Scholar
  16. Graham NAJ, Wilson SK, Jennings S, Polunin NVC, Bijoux JP, Robinson J (2006) Dynamic fragility of oceanic coral reef ecosystems. Proc Natl Acad Sci U S A 103:8425–8429CrossRefPubMedPubMedCentralGoogle Scholar
  17. Graham NAJ, Bellwood DR, Cinner JE, Hughes TP, Norström AV, Nyström M (2013) Managing resilience to reverse phase shifts in coral reefs. Front Ecol Environ 11:541–548CrossRefGoogle Scholar
  18. Halford AR, Caley MJ (2009) Towards an understanding of resilience in isolated coral reefs. Glob Chang Biol 15:3031–3045CrossRefGoogle Scholar
  19. Hirota M, Holmgren M, Van Nes EH, Scheffer M (2011) Global resilience of tropical forest and savanna to critical transitions. Science 334:232–235CrossRefPubMedGoogle Scholar
  20. Hoey AS, Bellwood DR (2011) Suppression of herbivory by macroalgal density: a critical feedback on coral reefs? Ecol Lett 14:267–273CrossRefPubMedGoogle Scholar
  21. Hughes TP (1994) Catastrophes, phase shifts, and large-scale degradation of a Caribbean coral reef. Science 265:1547–1551CrossRefPubMedGoogle Scholar
  22. Hughes TP, Tanner JE (2000) Recruitment failure, life histories, and long-term decline of Caribbean corals. Ecology 81:2250–2263CrossRefGoogle Scholar
  23. Hughes TP, Graham NAJ, Jackson JBC, Mumby PJ, Steneck RS (2010) Rising to the challenge of sustaining coral reef resilience. Trends Ecol Evol 25:633–642CrossRefPubMedGoogle Scholar
  24. Lee SC (2006) Habitat complexity and consumer-mediated positive feedbacks on a Caribbean coral reef. Oikos 112:442–447CrossRefGoogle Scholar
  25. Lirman D (2001) Competition between macroalgae and corals: effects of herbivore exclusion and increased algal biomass on coral survivorship and growth. Coral Reefs 19:392–399CrossRefGoogle Scholar
  26. Lotka AJ (1932) The growth of mixed populations: two species competing for a common food supply. J Wash Acad Sci 22:461–469Google Scholar
  27. Melbourne-Thomas J, Johnson CR, Fung T, Seymour RM, Chérubin LM, Arias-González JE, Fulton EA (2011) Regional-scale scenario modeling for coral reefs: a decision support tool to inform management of a complex system. Ecol Appl 21:1380–1398CrossRefPubMedGoogle Scholar
  28. Mackinson S, Sumaila UR, Pitcher TJ (1997) Bioeconomics and catchability: fish and fishers behaviour during stock collapse. Fish Res 31:11–17CrossRefGoogle Scholar
  29. McClanahan TR, Uku JN, Machano H (2002) Effect of macroalgal reduction on coral-reef fish in the Watamu Marine National Park, Kenya. Mar Freshw Res 53:223–231CrossRefGoogle Scholar
  30. McCook LJ, Price IR (1997) Macroalgal distributions on the Great Barrier Reef: a review of patterns and causes. The Great Barrier Reef: science, use and management: a national conference, 25–29 November 1996, Proceedings, vol 2. Great Barrier Reef Marine Park Authority and CRC Reef Research, Townsville, Australia, pp 37–46Google Scholar
  31. Mumby PJ (2009) Phase shifts and the stability of macroalgal communities on Caribbean coral reefs. Coral Reefs 28:761–773CrossRefGoogle Scholar
  32. Mumby PJ, Steneck RS (2008) Coral reef management and conservation in light of rapidly evolving ecological paradigms. Trends Ecol Evol 23:555–563CrossRefPubMedGoogle Scholar
  33. Mumby PJ, Hastings A, Edwards HJ (2007) Thresholds and the resilience of Caribbean coral reefs. Nature 450:98–101CrossRefPubMedGoogle Scholar
  34. Mumby PJ, Steneck RS, Hastings A (2013) Evidence for and against the existence of alternate attractors on coral reefs. Oikos 122:481–491CrossRefGoogle Scholar
  35. Nyström M, Norström AV, Blenckner T, de la Torre-Castro M, Eklöf JS, Folke C, Österblom H, Steneck RS, Thyresson M, Troell M (2012) Confronting feedbacks of degraded marine ecosystems. Ecosystems 15:695–710CrossRefGoogle Scholar
  36. Oreskes N, Shrader-Frechette K, Belitz K (1994) Verification, validation, and confirmation of numerical models in the Earth sciences. Science 263:641–646CrossRefPubMedGoogle Scholar
  37. Scheffer M (1998) Ecology of shallow lakes. Chapman and Hall, LondonGoogle Scholar
  38. Scheffer M, van Nes EH, Holmgren M, Hughes T (2008) Pulse-driven loss of top-down control: the critical-rate hypothesis. Ecosystems 11:226–237CrossRefGoogle Scholar
  39. Scheffer M, Carpenter SR, Lenton TM, Bascompte J, Brock W, Dakos V, van de Koppel J, van de Leemput IA, Levin SA, van Nes EH, Pascual M, Vandermeer J (2012) Anticipating critical transitions. Science 338:344–348CrossRefPubMedGoogle Scholar
  40. Scheffer M, Barrett S, Carpenter SR, Folke C, Green AJ, Holmgren TP, Hughes TP, Kosten S, van de Leemput IA, Nepstad DC, van Nes EH, Peeters ETHM, Walker B (2015) Creating a safe operating space for iconic ecosystems. Science 347:1317–1319CrossRefPubMedGoogle Scholar
  41. Schröder A, Persson L, De Roos DAM (2005) Direct experimental evidence for alternative stable states: a review. Oikos 110:3–19CrossRefGoogle Scholar
  42. Staver AC, Archibald S, Levin SA (2011) The global extent and determinants of savanna and forest as alternative biome states. Science 334:230–232CrossRefPubMedGoogle Scholar
  43. Steneck RS, Graham MH, Bourque BJ, Corbett D, Erlandson JM, Estes JA, Tegner MJ (2002) Kelp forest ecosystems: biodiversity, stability, resilience and future. Environ Conserv 29:426–459CrossRefGoogle Scholar
  44. Thomas R (1981) On the relation between the logical structure of systems and their ability to generate multiple steady states or sustained oscillations. In: Demongeot J, Lacolle B (eds) Della Dora J. Numerical methods in the study of critical phenomena. Springer, Berlin Heidelberg, pp 180–193Google Scholar
  45. Volterra V (1926) Fluctuations in the abundance of a species considered mathematically. Nature 118:558–560CrossRefGoogle Scholar
  46. Watson J, Estes JA (2011) Stability, resilience, and phase shifts in rocky subtidal communities along the west coast of Vancouver Island, Canada. Ecol Monogr 81:215–239CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  • Ingrid A. van de Leemput
    • 1
    Email author
  • Terry P. Hughes
    • 2
  • Egbert H. van Nes
    • 1
  • Marten Scheffer
    • 1
  1. 1.Department of Environmental SciencesWageningen UniversityWageningenThe Netherlands
  2. 2.Australian Research Council Centre of Excellence for Coral Reef StudiesJames Cook UniversityTownsvilleAustralia

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