Abstract

The world's coral reefs are in decline, with many exhibiting a phase shift from coral to macroalgal dominance [1Wilkinson C. Status of Coral Reefs of the World. Australian Institute of Marine Sciences, Townsville, Queensland2002Google Scholar, 2McClanahan T. Polunin N. Done T. Resilience of coral reefs.in: Gunderson L.H. Pritchard Jr., L. Resilience and Behavior of Large-Scale Systems. Island Press, Washington2002: 111-164Google Scholar, 3Gardner T.A. Cote I.M. Gill J.A. Grant A. Watkinson A.R. Long-term region-wide declines in Caribbean corals.Science. 2003; 301: 958-960Crossref PubMed Scopus (1506) Google Scholar, 4Hughes T.P. Baird A.H. Bellwood D.R. Card M. Connolly S.R. Folke C. Grosberg R. Hoegh-Guldberg O. Jackson J.B.C. Kleypas J. et al.Climate change, human impacts, and the resilience of coral reefs.Science. 2003; 301: 929-933Crossref PubMed Scopus (2750) Google Scholar, 5Pandolfi J.M. Bradbury R.H. Sala E. Hughes T.P. Bjorndal K.A. Cooke R.G. McArdle D. McClenachan L. Newman M.J.H. Paredes G. et al.Global trajectories of the long-term decline of coral reef ecosystems.Science. 2003; 301: 955-958Crossref PubMed Scopus (1455) Google Scholar, 6Bellwood D.R. Hughes T.P. Folke C. Nystrom M. Confronting the coral reef crisis.Nature. 2004; 429: 827-833Crossref PubMed Scopus (2315) Google Scholar]. This change is often associated with habitat loss and overharvesting of herbivorous fishes, particularly parrotfishes and surgeonfishes [6Bellwood D.R. Hughes T.P. Folke C. Nystrom M. Confronting the coral reef crisis.Nature. 2004; 429: 827-833Crossref PubMed Scopus (2315) Google Scholar, 7Hughes T.P. Catastrophes, phase shifts, and large-scale degradation of a Caribbean coral reef.Science. 1994; 265: 1547-1551Crossref PubMed Scopus (2209) Google Scholar, 8Jackson J.B.C. Kirby M.X. Berger W.H. Bjorndal K.A. Botsford L.W. Bourque B.J. Bradbury R.H. Cooke R. Erlandson J. Estes J.A. et al.Historical overfishing and the recent collapse of coastal ecosystems.Science. 2001; 293: 629-638Crossref PubMed Scopus (4742) Google Scholar, 9Mumby P.J. Dahlgren C.P. Harborne A.R. Kappel C.V. Micheli F. Brumbaugh D.R. Holmes K.E. Mendes J.M. Broad K. Sanchirico J.N. et al.Fishing, trophic cascades, and the process of grazing on coral reefs.Science. 2006; 311: 98-101Crossref PubMed Scopus (665) Google Scholar]. The challenge is to reverse this decline and enhance the resilience of coral-reef ecosystems [10Scheffer M. Carpenter S. Foley J.A. Folke C. Walker B. Catastrophic shifts in ecosystems.Nature. 2001; 413: 591-596Crossref PubMed Scopus (4968) Google Scholar, 11Folke C. Carpenter S. Walker B. Scheffer M. Elmqvist T. Gunderson L. Holling C.S. Regime shifts, resilience, and biodiversity in ecosystem management.Annu. Rev. Ecol. Syst. 2004; 35: 557-581Crossref Scopus (2458) Google Scholar]. We demonstrate, by using a large-scale experimentally induced phase shift, that the rapid reversal from a macroalgal-dominated to a coral- and epilithic algal-dominated state was not a result of herbivory by parrotfishes or surgeonfishes. Surprisingly, phase-shift reversal was primarily driven by a single batfish species (Platax pinnatus), a fish previously regarded as an invertebrate feeder. The 43 herbivorous fishes in the local fauna played only a minor role, suggesting that biodiversity may not offer the protection we hoped for in complex ecosystems. Our findings highlight the dangers faced by coral reefs and other threatened complex ecosystems: Species or functional groups that prevent phase shifts may not be able to reverse phase shifts once they occur. Nevertheless, reversal is possible. The critical issue is to identify and protect those groups that underpin the resilience and regeneration of complex ecosystems.