Phase shifts and stable states on coral reefs

Marine Ecology Progress Series

Volumn 413, Issue , 2010, Pages 201-216

  Dudgeon, Steve R ^a   Aronson, Richard B ^b   Bruno, John F ^c   Precht, William F ^d  

^a CALIFORNIA STATE UNIVERSITY   (United States)

^b Florida Institute of Technology   (United States)

^c University of North Carolina at Chapel Hill   (United States)

^d NOAA EARTH SYSTEM RESEARCH LABORATORY   (United States)

Author keywords

Alternative stable states; Community state; Coral; Coral reef; Macroalgae; Multiple stable states; Phase shift

Indexed keywords

ANTHROPOGENIC EFFECT; CORAL REEF; DOMINANCE; ECOSYSTEM RESILIENCE; HYPOTHESIS TESTING; MACROALGA; RESTORATION ECOLOGY; SUCCESSION; THEORETICAL STUDY; TROPICAL ENVIRONMENT;

ANTHOZOA;

EID: 77957346796     PISSN: 01718630     EISSN: None     Source Type: Journal    
DOI: 10.3354/meps08751     Document Type: Article

References (132)

1. Abraham R, Shaw CD (1992) Dynamics: The geometry of behavior. Addison-Wesley, Reading, MA
2. Adjeroud M, Chancerelle Y, Schrimm M, Perez T, Lecchini D, Galzin R, Salvat B (2005) Detecting the effects of natural disturbances on coral assemblages in French Polynesia: A decade survey at multiple scales. Aquat Living Resour 18: 111-123 (Pubitemid 41009108)
3. Adjeroud M, Michonneau F, Edmunds PJ, Chancerelle Y and others (2009) Recurrent disturbances, recovery trajectories, and resilience of coral assemblages on a South Central Pacific reef. Coral Reefs 28:775-780
4. Aronson RB, Precht WF (2000) Herbivory and algal dynamics on the coral reef at Discovery Bay, Jamaica. Limnol Oceanogr 45:251-255
5. Aronson RB, Precht WF (2006) Conservation, precaution, and Caribbean reefs. Coral Reefs 25:441-450
6. Aronson RB, Swanson DW (1997a) Disturbance and recovery from ship groundings in the Florida Keys National Marine Sanctuary. Dauphin Island Sea Lab Tech Rep 97-1002, Dauphin Island, AL
7. Aronson RB, Swanson DW (1997b) Video surveys of coral reefs: uni- and multivariate applications. Proc 8th Int Coral Reef Symp, Panama 2:1441-1446
8. Aronson RB, Macintyre IG, Precht WF, Murdoch TJT, Wapnick CM (2002a) The expanding scale of species turnover events on coral reefs in Belize. Ecol Monogr 72:233-249
9. Aronson RB, Precht WF, Toscano MA, Koltes KH (2002b) The 1998 bleaching event and its aftermath on a coral reef in Belize. Mar Biol 141:435-447
10. Aronson RB, Macintyre IG, Lewis SA, Hilbun NL (2005) Emergent zonation and geographic convergence of coral reefs. Ecology 86:2586-2600
11. Banner AH (1974) Kaneohe Bay, Hawaii: urban pollution and a coral reef ecosystem. Proc 2nd Int Coral Reef Symp, Brisbane 2:685-702
12. Bechtel JD, Gayle P, Kaufman L (2006) The return of Diadema antillarum to Discovery Bay: Patterns of distribution and abundance. Proc 10th Int Coral Reef Symp, Okinawa 1: 367-375
13. Beisner BE, Haydon DT, Cuddington K (2003) Alternative stable states in ecology. Front Ecol Environ 1:376-382
14. Bellwood DR, Hughes TP, Folke C, Nyström M (2004) Confronting the coral reef crisis. Nature 429:827-833 (Pubitemid 38843290)
15. Bender EA, Case TJ, Gilpin ME (1984) Perturbation experiments in community ecology-theory and practice. Ecology 65:1-13
16. Berumen ML, Pratchett MS (2006) Recovery without resilience: Persistent disturbance and long-term shifts in the structure of fish and coral communities at Tiahura Reef, Moorea. Coral Reefs 25:647-653
17. Bruno JF, Bertness MD (2001) Habitat modification and facilitation in benthic marine communities. In: Bertness, MD, Gaines, SD, Hay, ME (eds) Marine community ecology. Sinauer Associates, Sunderland, MA, p 201-220
18. 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: 1478-1484
19. Carpenter RC (1986) Partitioning herbivory and its effects on coral reef algal communities. Ecol Monogr 56:345-363
20. Carpenter RC, Edmunds PJ (2006) Local and regional scale recovery of Diadema promotes recruitment of scleractinian corals. Ecol Lett 9:268-277
21. Chen CA, Dai CF (2004) Local phase shift from Acroporadominant to Condylactis-dominant community in the Tiao-Shi Reef, Kenting National Park, southern Taiwan. Coral Reefs 23:508
22. Chesher RH (1969) Destruction of Pacific corals by the sea star Acanthaster planci. Science 165:280-283
23. Cho LL, Woodley JD (2002) Recovery of reefs at Discovery Bay, Jamaica and the role of Diadema antillarum. Proc 9th Int Coral Reef Symp, Bali 1:331-338
24. Connell JH (1997) Disturbance and recovery of coral assemblages. Coral Reefs 16:S101-S113 (Pubitemid 127709597)
25. Connell JH, Slatyer RO (1977) Mechanisms of succession in natural communities and their role in community stability and organization. Am Nat 111:1119-1144
26. Connell JH, Sousa WP (1983) On the evidence needed to judge ecological stability or persistence. Am Nat 121: 789-824
27. 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 67:461-488
28. Crabbe MJC (2009) Scleractinian coral population size structures and growth rates indicate coral resilience on the fringing reefs of North Jamaica. Mar Environ Res 67: 189-198
29. Davis GE (1982) A century of natural change in coral distribution in the Dry Tortugas: A comparison of reef maps from 1881 and 1976. Bull Mar Sci 32:608-623
30. Diaz-Pulido G, McCook LJ, Dove S, Berkelmans J and others (2009) Doom and boom on a resilient reef: climate change, algal overgrowth and coral recovery. PLoS ONE 4:e5239
31. Done TJ (1992) Phase shifts in coral reef communities and their ecological significance. Hydrobiologia 247:121-132
32. Done TJ, Dayton PK, Dayton AE, Steger R (1991) Regional and local variability in recovery of shallow coral communities: Moorea, French Polynesia and central Great Barrier Reef. Coral Reefs 9:183-192
33. Eakin CM (1996) Where have all the carbonates gone? A model comparison of calcium carbonate budgets before and after the 1982-1983 El Niño. Coral Reefs 15:109-119 (Pubitemid 26262790)
34. Eakin CM (2001) A tale of two ENSO events: carbonate budgets and the influence of two warming disturbances and intervening variability, Uva Island, Panama. Bull Mar Sci 69:171-186
35. Edmunds PJ, Carpenter RC (2001) Recovery of Diadema antillarum reduces macroalgal cover and increases abundance of juvenile corals on a Caribbean reef. Proc Natl Acad Sci USA 98:5067-5071
36. Edwards AJ, Gomez ED (2007) Reef restoration concepts and guidelines: making sensible management choices in the face of uncertainty. Coral Reef Targeted Research & Capacity Building for Management Programme, St Lucia, Australia
37. Elmhirst T, Connolly SR, Hughes TP (2009) Connectivity, regime shifts and the resilience of coral reefs. Coral Reefs 28:949-957
38. Elmqvist T, Folke C, Nyström M, Peterson G, Bengtsson J, Walker B, Norberg J (2003) Response diversity, ecosystem change, and resilience. Front Ecol Environ 1:488-494
39. Emlen JM (1977) Ecology: An evolutionary approach. Addison- Wesley, Reading, MA
40. Emslie MJ, Cheal AJ, Sweatman H, Delean S (2008) Recovery from disturbance of coral and reef fish communities on the Great Barrier Reef, Australia. Mar Ecol Prog Ser 371: 177-190
41. Endean R, Stablum W (1973) The apparent extent of recovery of reefs of Australia's Great Barrier Reef devastated by the crown-of-thorns starfish. Atoll Res Bull 168:1-41
42. Fong P, Smith TB, Wartian MJ (2006) Epiphytic cyanobacteria maintain shifts to macroalgal dominance on coral reefs following ENSO disturbance. Ecology 87:1162-1168 (Pubitemid 43752556)
43. Graham MH, Dayton PK (2002) On the evolution of ecological ideas: Paradigms and scientific progress. Ecology 83: 1481-1489
44. Greenaway AM, Gordon-Smith D (2006) The effects of rainfall on the distribution of inorganic nitrogen and phos- phorus in Discovery Bay, Jamaica. Limnol Oceanogr 51: 2206-2220 (Pubitemid 44520917)
45. Greenstein BJ, Pandolfi JM (2008) Escaping the heat: Range shifts of reef coral taxa in coastal Western Australia. Glob Change Biol 14:513-528
46. Grimm V, Wissel C (1997) Babel, or the ecological stability discussions: An inventory and analysis of terminology and a guide for avoiding confusion. Oecologia 109:323-334 (Pubitemid 27114940)
47. Halpern BS, Silliman BR, Olden JD, Bruno JP, Bertness MD (2007) Incorporating positive interactions in aquatic restoration and conservation. Front Ecol Environ 5:153-160
48. Hardt MJ (2008) Lessons from the past: The collapse of Jamaican coral reefs. Fish Fish 10:1-16
49. Hare SR, Mantua NJ (2000) Empirical evidence for North Pacific regime shifts in 1977 and 1989. Prog Oceanogr 47: 103-145
50. Hatcher BG (1984) A maritime accident provides evidence for alternate stable states in benthic communities on coral reefs. Coral Reefs 3:199-204
51. Hatcher BG (1992) Kelp beds on coral reefs: Alternate stable benthic communities co-exist in high latitude reef systems (abstract). Proc 7th Int Coral Reef Symp, Guam 2:1239
52. Hawkins JP, Roberts CM (2004) Effects of artisanal fishing on Caribbean coral reefs. Conserv Biol 18:215-226 (Pubitemid 38215605)
53. Hilborn R (2004) Ecosystem-based fisheries management: The carrot or the stick? Mar Ecol Prog Ser 274:275-278 (Pubitemid 38927604)
54. Holling CS (1973) Resilience and stability of ecological systems. Annu Rev Ecol Syst 4:1-23
55. Hughes TP (1994) Catastrophes, phase shifts, and large-scale degradation of a Caribbean coral reef. Science 265: 1547-1551
56. Hughes TP, Bellwood DR, Folke C, Steneck RS, Wilson J (2005) New paradigms for supporting the resilience of marine ecosystems. Trends Ecol Evol 20:380-386 (Pubitemid 40817317)
57. Hunter CL, Evans CW (1995) Coral reefs in Kaneohe Bay, Hawaii: Two centuries of Western influence and two decades of data. Bull Mar Sci 57:501-515
58. Idjadi JA, Lee SC, Bruno JF, Precht WF, Allen-Requa L, Edmunds PJ (2006) Rapid phase-shift reversal on a Jamaican coral reef. Coral Reefs 25:209-211
59. Idjadi JA, Haring RN, Precht WF (2010) Recovery of the sea urchin Diadema antillarum promotes scleractinian coral growth and survivorship on shallow Jamaican reefs. Mar Ecol Prog Ser 403:91-100
60. Ivany LC, Brett CE, Wall HLB, Wall PD, Handley JC (2009) Relative taxonomic and ecologic stability in Devonian marine faunas of New York State: A test of coordinated stasis. Paleobiology 35:499-524
61. Jackson JBC, Johnson KG (2000) Life in the last few million years. Paleobiology 26(Suppl):221-235
62. Jackson JBC, Kirby MX, Berger WH, Bjorndal KA and others (2001) Historical overfishing and the recent collapse of coastal ecosystems. Science 293:629-638
63. Kaiser MJ, Attrill MJ, Jennings S, Thomas DN and others (2005) Marine ecology: Processes, systems, impacts. Oxford University Press, Oxford, UK
64. Knowlton N (1992) Thresholds and multiple stable states in coral reef community dynamics. Am Zool 32:674-682
65. Knowlton N (2001) The future of coral reefs. Proc Natl Acad Sci USA 98:5419-5425 (Pubitemid 32435657)
66. Knowlton N (2004) Multiple 'stable' states and the conservation of marine ecosystems. Prog Oceanogr 60:387-396 (Pubitemid 38537095)
67. Knowlton N (2006) Coral reef coda: what can we hope for? In: Côté IM, Reynolds JD (eds) Coral reef conservation. Cambridge University Press, Cambridge, UK, p 538-549
68. Lessios HA (1988) Mass mortality of Diadema antillarum in the Caribbean: what have we learned? Annu Rev Ecol Syst 19:371-393
69. Levins R (1968) Evolution in changing environments. Princeton University Press, Princeton, NJ
70. Lewontin RC (1969) The meaning of stability. In: Woodwell GM, Smith HH (eds) Diversity and stability in ecological systems, Vol 22. Brookhaven National Laboratory, Upton, NY, p 13-24
71. Liddell WD, Ohlhorst SL (1992) Ten years of disturbance and change on a Jamaican fringing reef. Proc 7th Int Coral Reef Symp, Guam 1:144-150
72. Lighty RG (1980) Fleshy-algal domination of a modern Bahamian barrier reef: example of an alternative climax reef community (abstract). Proc 4th Int Coral Reef Symp, Manila 1:722
73. Lighty RG, Macintyre IG, Stuckenrath R (1978) Submerged early Holocene barrier reef, south-east Florida shelf. Nature 276:59-60
74. Lotka AJ (1956) Elements of mathematical biology. Dover Publications, New York, NY
75. Loya Y (2004) The coral reefs of Eilat-past, present and future: Three decades of coral community structure studies. In: Rosenberg E, Loya Y (eds) Coral health and disease. Springer-Verlag, Berlin, p 1-34
76. Macia S, Robinson MP, Nalevanko A (2007) Experimental dispersal of recovering Diadema antillarum increases grazing intensity and reduces macroalgal abundance on a coral reef. Mar Ecol Prog Ser 348:173-182 (Pubitemid 350189916)
77. Maragos J, Evans C, Holthus P (1985) Reef corals in Kaneohe Bay six years before and after termination of sewage discharges (Oahu, Hawaiian Archipelago). Proc 5th Int Coral Reef Congr, Tahiti, 4:189-194
78. May RM (1977) Thresholds and breakpoints in ecosystems with a multiplicity of stable states. Nature 269:471-477
79. McManus JW, Polsenberg JF (2004) Coral-algal phase shifts on coral reefs: ecological and environmental aspects. Prog Oceanogr 60:263-279
80. Mumby PJ (2006) The impact of exploiting grazers (Scaridae) on the dynamics of Caribbean coral reefs. Ecol Appl 16: 747-769
81. Mumby PJ (2009) Phase shifts and the stability of macroalgal communities on Caribbean coral reefs. Coral Reefs 28: 761-773
82. Mumby PJ, Harborne AR (2010) Marine reserves enhance the recovery of corals on Caribbean reefs. PLoS ONE 5:e8657
83. Mumby PJ, Hastings A, Edwards HJ (2007a) Thresholds and the resilience of Caribbean coral reefs. Nature 450:98-101 (Pubitemid 350070571)
84. Mumby PJ, Harborne AR, Williams J, Kappel CV and others (2007b) Trophic cascade facilitates coral recruitment in a marine reserve. Proc Natl Acad Sci USA 104:8362-8367 (Pubitemid 47175493)
85. Ninio R, Meekan M, Done T, Sweatman H (2000) Temporal patterns in coral assemblages on the Great Barrier Reef from local to large spatial scales. Mar Ecol Prog Ser 194: 65-74 (Pubitemid 30186219)
86. Norström AV, Nyström M, Lokrantz J, Folke C (2009) Alternative states on coral reefs: Beyond coral-macroalgal phase shifts. Mar Ecol Prog Ser 376:295-306
87. Nyström M, Folke C, Moberg F (2000) Coral reef disturbance and resilience in a human-dominated environment. Trends Ecol Evol 15:413-417
88. Nyström M, Graham NAJ, Lokrantz J, Norström AV (2008) Capturing the cornerstones of coral reef resilience: linking theory to practice. Coral Reefs 27:795-809
89. Paine RT (1977) Controlled manipulations in the marine intertidal zone and their contributions to ecological theory. In: Goulden CE (ed) The changing scenes in the natural sciences, 1776-1976. Academy of Natural Sciences, Philadelphia, PA, p 245-270
90. Palumbi SR, McLeod KL, Grünbaum D (2008) Ecosystems in action: lessons from marine ecology about recovery, resis- tance, and reversibility. Bioscience 58:33-42 (Pubitemid 351185988)
91. Pandolfi JM, Bradbury RH, Sala E, Hughes TP and others (2003) Global trajectories of the long-term decline of coral reef ecosystems. Science 301:955-958 (Pubitemid 36994805)
92. Peterson CH (1984) Does a rigorous criterion for environmental identity preclude the existence of multiple stable points? Am Nat 124:127-133
93. Petraitis PS, Dudgeon SR (2004) Detection of alternative stable states in marine communities. J Exp Mar Biol Ecol 300: 343-371 (Pubitemid 38583477)
94. Petraitis PS, Dudgeon SR (2005) Divergent succession and implications for alternative states on rocky intertidal shores. J Exp Mar Biol Ecol 326:14-26
95. Petraitis PS, Hoffman CA (2010) Multiple stable states and relationship between thresholds in processes and states. Mar Ecol Prog Ser 413:189-200
96. Petraitis PS, Latham R (1999) The importance of scale in testing the origins of alternative community states. Ecology 80:429-442 (Pubitemid 29126118)
97. Petraitis PS, Latham RE, Niesenbaum RA (1989) The maintenance of species diversity by disturbance. Q Rev Biol 64: 393-418
98. Petraitis PS, Methratta ET, Rhile EC, Vidargas NA, Dudgeon SR (2009) Experimental confirmation of multiple community states in a marine ecosystem. Oecologia 161:139-148
99. Power ME, Tilman D, Estes JA, Menge BA and others (1996) Challenges in the quest for keystones. Bioscience 46: 609-620
100. Precht WF, Aronson RB (2004) Climate flickers and range shifts of reef corals. Front Ecol Environ 2:307-314
101. Precht WF, Aronson RB (2006a) Rapid range expansion of reef corals in response to climatic warming (abstract). Geol Soc America Abstr Progr 38:535
102. Precht WF, Aronson RB (2006b) Death and resurrection of Caribbean coral reefs: A palaeoecological approach. In: Côté IM, Reynolds JD (eds) Coral reef conservation. Cambridge University Press, Cambridge, UK, p 40-77
103. Precht WF, Aronson RB, Swanson DW (2001) Improving scientific decision-making in the restoration of shipgrounding sites on coral reefs. Bull Mar Sci 69:1001-1012
104. Precht WF, Aronson RB, Moody RM, Kaufman L (2010) Changing patterns of microhabitat utilization by the threespot damselfish, Stegastes planifrons, on Caribbean reefs. PLoS ONE 5:e10835
105. Quinn NJ, Kojis BL (2008) The recent collapse of a rapid phase-shift reversal on a Jamaican north coast coral reef after the 2005 bleaching event. Rev Biol Trop 56(Suppl1): 149-159
106. Ricklefs RE (1979) Ecology, 2nd edn. Chiron, New York
107. Riegl B, Bruckner A, Coles SL, Renaud P, Dodge RE (2009) Coral reefs: Threats and conservation in an era of global change. Ann N Y Acad Sci 1162:136-186
108. Rogers CS, Miller J (2006) Permanent 'phase shifts' or reversible declines in coral cover? Lack of recovery of two coral reefs in St. John, US Virgin Islands. Mar Ecol Prog Ser 306:103-114 (Pubitemid 43241565)
109. Romme WH (1982) Fire and landscape diversity in subalpine forests of Yellowstone National Park. Ecol Monogr 52: 199-221
110. Romme WH, Despain DG (1989) Historical perspective on the Yellowstone fires of 1988. Bioscience 39:695-699
111. Romme WH, Turner MG (2004) Ten years after the 1988 Yellowstone fires: Is restoration needed? In: Wallace LL (ed) After the fires: The ecology of change in Yellowstone National Park. Yale University Press, New Haven, CT, p 318-361
112. Sammarco PW (1980) Diadema and its relationship to coral spat mortality: grazing, competition, and biological disturbance. J Exp Mar Biol Ecol 45:245-272
113. Sammarco PM (1982a) Effects of grazing by Diadema antillarum Philippi (Echinodermata: Echinoidea) on algal diversity and community structure. J Exp Mar Biol Ecol 65: 83-105
114. Sammarco PW (1982b) Echinoid grazing as a structuring force in coral communities: whole-reef manipulations. J Exp Mar Biol Ecol 61:31-55
115. Scheffer M, Carpenter SR (2003) Catastrophic regime shifts in ecosystems: linking theory to observation. Trends Ecol Evol 18:648-656 (Pubitemid 37399486)
116. Scheffer M, Carpenter S, Foley JA, Folke C, Walker B (2001) Catastrophic shifts in ecosystems. Nature 413:591-596 (Pubitemid 32964052)
117. Schröder A, Perrson L, DeRoos AM (2005) Direct experimental evidence for alternative stable states: A review. Oikos 110:3-19 (Pubitemid 40802179)
118. Schroeder RE, Green AL, DeMartini EE, Kenyon JC (2008) Long-term effects of a ship-grounding on coral reef fish assemblages at Rose Atoll, American Samoa. Bull Mar Sci 82:345-364
119. Schutte VGW, Selig ER, Bruno JF (2010) Regional spatiotemporal trends in Caribbean coral reef benthic communities. Mar Ecol Prog Ser 402:115-122
120. Simberloff D (1998) Flagships, umbrellas, and keystones: Is single species management passé in the landscape era? Biol Conserv 83:247-257
121. Smale DA, Kendrick GA, Waddington KI, Van Niel KP, Meeuwig JJ, Harvey ES (2010) Benthic assemblage composition on subtidal reefs along a latitudinal gradient in Western Australia. Estuar Coast Shelf Sci 86:83-92
122. Sousa WP, Connell JH (1985) Further comments on the evidence for multiple stable points in natural communities. Am Nat 125:612-615
123. Stimson J, Conklin E (2008) Potential reversal of a phase shift: The rapid decrease in the cover of the invasive green macroalga Dictyosphaeria cavernosa Forsskål on coral reefs in K-ane'ohe Bay, Oahu, Hawai'i. Coral Reefs 27: 717-726
124. Stoddart DR (1963) Effects of Hurricane Hattie on the British Honduras reefs and cays, October 30-31, 1961. Atoll Res Bull 95:1-142
125. Stoddart DR (1969) Post-hurricane changes on the British Honduras reefs and cays: Re-survey of 1965. Atoll Res Bull 131:1-25
126. Stoddart DR (1974) Post-hurricane changes on the British Honduras reefs: Re-survey of 1972. Proc 2nd Int Coral Reef Symp, Brisbane 2:473-483
127. Turner MG, Romme WH, Tinker DB (2003) Surprises and lessons from the 1988 Yellowstone fires. Front Ecol Environ 1:351-358
128. Watson M, Munro JL (2004) Settlement and recruitment of coral reef fishes in moderately exploited and overexploited Caribbean ecosystems: Implications for marine protected areas. Fish Res 69:415-425 (Pubitemid 39301148)
129. Webber M, Edwards-Myers E, Campbell C, Webber D (2005) Phytoplankton and zooplankton as indicators of water quality in Discovery Bay, Jamaica. Hydrobiologia 545: 177-193 (Pubitemid 40924533)
130. Woodley JD (1999) Sea urchins exert top-down control on Jamaican coral reefs. Coral Reefs 18:192
131. Woodley JD, Sary Z (2000) Development of a locally managed fisheries reserve at Discovery Bay, Jamaica. Proc 9th Int Coral Reef Symp, Bali 2:627-634
132. Work TM, Aeby GS, Maragos JE (2008) Phase shift from a coral to a corallimorph-dominated reef associated with a shipwreck on Palmyra Atoll. PLoS ONE 3:e2989