Conservation management approaches to protecting the capacity for corals to respond to climate change: A theoretical comparison

Global Change Biology

Volumn 16, Issue 4, 2010, Pages 1229-1246

  Baskett, Marissa L ^a,d   Nisbet, Roger M ^b   Kappel, Carrie V ^a   Mumby, Peter J ^c   Gaines, Steven D ^b  

^a NATIONAL CENTER FOR ECOLOGICAL ANALYSIS AND SYNTHESIS   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF EXETER   (United Kingdom)

^d UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Coral bleaching; Coral reefs; Global climate change; Quantitative genetic model; Size structured matrix model

Indexed keywords

ANTHROPOGENIC EFFECT; CLIMATE CHANGE; CLIMATE EFFECT; CONSERVATION MANAGEMENT; CORAL BLEACHING; CORAL REEF; ENVIRONMENTAL PROTECTION; ENVIRONMENTAL STRESS; GLOBAL CHANGE; GLOBAL CLIMATE; LIFE HISTORY; NUMERICAL MODEL; SURVIVORSHIP; THEORETICAL STUDY;

ANTHOZOA;

EID: 77950303222     PISSN: 13541013     EISSN: 13652486     Source Type: Journal    
DOI: 10.1111/j.1365-2486.2009.02062.x     Document Type: Article

References (100)

1. Alleaume-Benharira M, Pen IR, Ronce O. Geographical patterns of adaptation within a species' range: interactions between drift and gene flow. Journal of Evolutionary Biology 2006, 19:203-215.
2. Anthony KRN, Connolly SR, Hoegh-Guldberg O. Bleaching, energetics, and coral mortality risk: effects of temperature, light, and sediment regime. Limnology and Oceanography 2007, 52:716-726.
3. Baghdasarian G, Muscatine L. Preferential expulsion of dividing algal cells as a mechanism for regulating algal-cnidarian symbiosis. Biological Bulletin 2000, 199:278-286.
4. Baird AH, Cumbo VR, Leggat W, Rodriguez-Lanetty M. Fidelity and flexibility in coral symbioses. Marine Ecology Progress Series 2007, 347:307-309.
5. Bak RP, Nieuwland G, Meesters EH. Coral reef crisis in deep and shallow reefs: 30 years of constancy and change in reefs of Curaçao and Bonaire. Coral Reefs 2005, 24:475-479.
6. Bak RPM, Meesters EH. Population structure as a response of coral communities to global change. American Zoologist 1999, 39:56-65.
7. Baker A. Symbiont diversity on coral reefs and its relationship to bleaching resistance and resilience. Coral health and Disease 2004, 177-194. Rosenberg ELoya Y. In, eds, pp, Springer-Verlag, Berlin, New York
8. Baker AC. Flexibility and specificity in coral-algal symbiosis: diversity, ecology, and biogeography of Symbiodinium. Annual Review of Ecology, Evolution, and Systematics 2003, 34:661-689.
9. Baskett ML, Gaines SD, Nisbet RM. Symbiont diversity may help coral reefs survive moderate climate change. Ecological Applications 2009, 19:3-17.
10. Bellwood DR, Hughes TP, Folke C, Nyström M. Confronting the coral reef crisis. Nature 2004, 429:827-833.
11. Bhagooli R, Yakovleva I. Differential bleaching susceptibility and mortality patterns among four corals in response to thermal stress. Symbiosis 2004, 37:121-136.
12. Brown BE. Adaptations of reef corals to physical environmental stress. Advances in Marine Biology 1997a, 31:221-299.
13. Brown BE. Coral bleaching: causes and consequences. Coral Reefs 1997b, 16:S129-S138.
14. Brown BE, Clarke KR, Warwick RM. Serial patterns of biodiversity change in corals across shallow reef flats in Ko Phuket, Thailand, due to the effects of local (sedimentation) and regional (climatic) perturbations. Marine Biology 2002, 141:21-29.
15. Bruno JF, Petes LE, Harvell CD, Hettinger A. Nutrient enrichment can increase the severity of coral diseases. Ecology Letters 2003, 6:1056-1061.
16. Burger R. Evolution of genetic variability and the advantage of sex and recombination in changing environments. Genetics 1999, 153:1055-1069.
17. Chancerelle Y. Methods to estimate actual surface areas of scleractinian coral at the colony- and community-scale. Oceanologica Acta 2000, 23:211-219.
18. Connell JH, Hughes TP, Wallace CC. A 30-year study of coral abundance, recruitment, and disturbance at several scales in space and time. Ecological Monographs 1997, 67:461-488.
19. Cook CB, Logan A, Ward J, Luckhurst B, Berg Jr CJ. Elevated temperatures and bleaching on a high latitude coral reef: the 1988 Bermuda event. Coral Reefs 1990, 9:45-49.
20. Day T, Nagel L, van Oppen MJH, Caley MJ. Factors affecting the evolution of bleaching resistance in corals. American Naturalist 2008, 171:E72-E88.
21. de Kroon H, Plaisier A, van Groenendael J, Caswell H. Elasticity: the relative contribution of demographic parameters to population-growth rate. Ecology 1986, 67:1427-1431.
22. Done TJ. Coral community adaptability to environmental change at the scales of regions, reefs and reef zones. American Zoologist 1999, 39:66-79.
23. Done TJ. Scientific Principles for Establishing MPAs to Alleviate Coral Bleaching and Promote Recovery. Coral Bleaching and Marine Protected Areas. Proceedings of the Workshop on Mitigating Coral Bleaching Impact Through MPA Design, Bishop Museum, Honolulu, Hawaii, 29-31 May 2001. Asia Pacific Coastal Marine Program Report 0102 2001, 53-59. Salm RVColes SL. In, eds, pp, The Nature Conservancy, Honolulu, Hawaii, USA
24. Donner SD, Knutson TR, Oppenheimer M. Model-based assessment of the role of human-induced climate change in the 2005 Caribbean coral bleaching event. Proceedings of the National Academy of Sciences USA 2007, 104:5483-5488.
25. Donner SD, Skirving WJ, Little CM, Oppenheimer M, Hoegh-Guldberg O. Global assessment of coral bleaching and required rates of adaptation under climate change. Global Change Biology 2005, 11:2251-2265.
26. Edmunds PJ. The effect of sub-lethal increases in temperature on the growth and population trajectories of three scleractinian corals on the southern Great Barrier Reef. Oecologia 2005, 146:350-364.
27. Edmunds PJ, Elahi R. The demographics of a 15-year decline in cover of the Caribbean reef coral Montastraea annularis. Ecological Monographs 2007, 77:3-18.
28. Eppley RW. Temperature and phytoplankton growth in the sea. Fishery Bulletin 1972, 70:1063-1085.
29. Fabricius KE. Effects of terrestrial runoff on the ecology of corals and coral reefs: review and synthesis. Marine Pollution Bulletin 2005, 50:125-146.
30. Fernandes L, Day J, Lewis A. Establishing representative no-take areas in the Great Barrier Reef: large-scale implementation of theory on marine protected areas. Conservation Biology 2005, 19:1733-1744.
31. Fitt WK, McFarland FK, Warner ME, Chilcoat GC. Seasonal patterns of tissue biomass and densities of symbiotic dinoflagellates in reef corals and relation to coral bleaching. Limnology and Oceanography 2000, 45:677-685.
32. Fong P, Glynn PW. A regional model to predict coral population dynamics in response to El Niño-Southern Oscillation. Ecological Applications 2000, 10:842-854.
33. Game ET, McDonald-Madden E, Puotinen ML, Possingham HP. Should we protect the strong or the weak? Risk, resilience, and the selection of Marine Protected Areas. Conservation Biology 2008, 22:1619-1629.
34. Gandon S, Michalakis Y. Local adaptation, evolutionary potential and host-parasite coevolution: interactions between migration, mutation, population size and generation time. Journal of Evolutionary Biology 2002, 15:451-462.
35. Garant D, Forde SE, Hendry AP. The multifarious effects of dispersal and gene flow on contemporary adaptation. Functional Ecology 2007, 21:434-443.
36. Gattuso JP, Allemand D, Frankignoulle M. Photosynthesis and calcification at cellular, organismal and community levels in coral reefs: a review on interactions and control by carbonate chemistry. American Zoologist 1999, 39:160-183.
37. Gomulkiewicz R, Holt RD, Barfield M. The effects of density dependence and immigration on local adaptation and niche evolution in a black-hole sink environment. Theoretical Population Biology 1999, 55:283-296.
38. Grottoli AG, Rodrigues LJ, Palardy JE. Heterotrophic plasticity and resilience in bleached corals. Nature 2006, 440:1186-1189.
39. Heller NE, Zavaleta ES. Biodiversity management in the face of climate change: a review of 22 years of recommendations. Biological Conservation 2009, 142:14-32.
40. Hoegh-Guldberg O. Climate change, coral bleaching and the future of the world's coral reefs. Marine and Freshwater Research 1999, 50:839-866.
41. Hoegh-Guldberg O, Mumby PJ, Hooten AJ. Coral reefs under rapid climate change and ocean acidification. Science 2007, 318:1737-1742.
42. Holling CS. Resilience and stability of ecological systems. Annual Review of Ecology and Systematics 1973, 4:1-23.
43. Holt RD, Gomulkiewicz R. How does immigration influence local adaptation? A reexamination of a familiar paradigm. American Naturalist 1997, 149:563-572.
44. Hughes TP, Baird AH, Bellwood DR. Climate change, human impacts, and the resilience of coral reefs. Science 2003, 301:929-933.
45. Hughes TP, Rodrigues MJ, Bellwood DR. Phase shifts, herbivory, and the resilience of coral reefs to climate change. Current Biology 2007, 17:360-365.
46. Hughes TP, Tanner JE. Recruitment failure, life histories, and long-term decline of Caribbean corals. Ecology 2000, 81:2250-2263.
47. Huppert A, Stone L. Chaos in the Pacific's coral reef bleaching cycle. American Naturalist 1998, 152:447-459.
48. Jacques TG, Marshall N, Pilson MEQ. Experimental ecology of the temperate scleractinian coral Astrangia danae II. Effect of temperature, light-intensity and symbiosis with zooxanthellae on metabolic-rate and calcification. Marine Biology 1983, 76:135-148.
49. Jokiel PL, Coles SL. Response of Hawaiian and other Indo-Pacific reef corals to elevated-temperature. Coral Reefs 1990, 8:155-162.
50. Kawecki TJ, Ebert D. Conceptual issues in local adaptation. Ecology Letters 2004, 7:1225-1241.
51. Kleypas JA, Feely RA, Fabry VJ, Langdon C, Sabine CL, Robbins LL. 2006, Tech. rep., Report of a workshop held 18-20 April 2005, St. Petersberg, FL, sponsored by NSF, NOAA and the US Geological Survey. 88 pp
52. Knowlton N. The future of coral reefs. Proceedings of the National Academy of Sciences U. S. A 2001, 98:5419-5425.
53. Kuffner IB, Walters LJ, Becerro MA, Paul VJ, Ritson-Williams R, Beach KS. Inhibition of coral recruitment by macroalgae and cyanobacteria. Marine Ecology Progress Series 2006, 323:107-117.
54. LaJeunesse TC. Investigating the biodiversity, ecology, and phylogeny of endosymbiotic dinoflagellates in the genus Symbiodinium using the its region: in search of a " species" level marker. Journal of Phycology 2001, 37:866-880.
55. Lasker HR. Population-growth of a gorgonian coral: equilibrium and nonequilibrium sensitivity to changes in life-history variables. Oecologia 1991, 86:503-509.
56. Leichter JJ, Genovese SJ. Intermittent upwelling and subsidized growth of the scleractinian coral Madracis mirabilis on the deep fore-reef slope of Discovery Bay, Jamaica. Marine Ecology Progress Series 2006, 316:95-103.
57. Lenormand T. Gene flow and the limits to natural selection. Trends in Ecology and Evolution 2002, 17:183-189.
58. Loya Y, Sakai K, Yamazato K, Nakano Y, Sambali H, van Woesik R. Coral bleaching: the winners and the losers. Ecology Letters 2001, 4:122-131.
59. Lynch M. The rate of polygenic mutation. Genetical Research 1988, 51:137-148.
60. Lynch M, Gabriel W, Wood AM. Adaptive and demographic responses of plankton populations to environmental-change. Limnology and Oceanography 1991, 36:1301-1312.
61. Lynch M, Lande R. Evolution and extinction in response to environmental change. Biotic Interactions and Global Change 1993, 234-250. Kareiva PM, Kingsolver JGHuey RB. In, eds, pp, Sinauer Associates Inc., Sunderland, MA
62. Maina J, Venus V, McClanahan TR, Ateweberhan M. Modelling susceptibility of coral reefs to environmental stress using remote sensing data and GIS models. Ecological Modelling 2008, 212:180-199.
63. Marshall P, Schuttenberg H. Adapting coral reef management in the face of climate change. Coral Reefs and Climate Change: Science and Management, vol. 61 of Coastal and Estuarine Studies 2006, 223-241. Phinney JT, Heogh-Guldberg OKleypas JSkirving WStrong A. In, eds, pp, American Geophysical Union, Washington, DC
64. McCarty JP. Ecological consequences of recent climate change. Conservation Biology 2001, 15:320-331.
65. McClanahan TR, Cinner JE, Maina J. Conservation action in a changing climate. Conservation Letters 2008, 1:53-59.
66. McCook LJ, Jompa J, Diaz-Pulido G. Competition between corals and algae on coral reefs: a review of evidence and mechanisms. Coral Reefs 2001, 19:400-417.
67. Mousseau TA, Roff DA. Natural-selection and the heritability of fitness components. Heredity 1987, 59:181-197.
68. Mumby PJ. The impact of exploiting grazers (Scaridae) on the dynamics of Caribbean coral reefs. Ecological Applications 2006, 16:747-769.
69. Mumby PJ, Chisholm JRM, Edwards AJ, Clark CD, Roark EB, Andrefouet S, Jaubert J. Unprecedented bleaching-induced mortality in Porites spp. at Rangiroa Atoll, French Polynesia. Marine Biology 2001, 139:183-189.
70. Mumby PJ, Foster NL, Fahy EAG. Patch dynamics of coral reef macroalgae under chronic and acute disturbance. Coral Reefs 2005, 24:681-692.
71. Mumby PJ, Hastings A, Edwards HJ. Thresholds and the resilience of Caribbean coral reefs. Nature 2007, 450:98-101.
72. Muscatine L, Falkowski PG, Porter JW, Dubinsky Z. Fate of photosynthetic fixed carbon in light-adapted and shade-adapted colonies of the symbiotic coral Stylophora pistillata. Proceedings of the Royal Society of London Series B Biological Sciences 1984, 222:181-202.
73. Noordeloos M, Tupper M, Yusuf Y, Tan MK, Tan SL, Teoh SJ, Ikbal S. 2007, http://www.reefbase.org, ReefBase: A global information system on coral reefs. Online. Available from, (accessed 9 January 2008)
74. Norberg J. Biodiversity and ecosystem functioning: a complex adaptive systems approach. Limnology and Oceanography 2004, 49:1269-1277.
75. Nyström M, Folke C. Spatial resilience of coral reefs. Ecosystems 2001, 4:406-417.
76. Nyström M, Folke C, Moberg F. Coral reef disturbance and resilience in a human-dominated environment. Trends in Ecology and Evolution 2000, 15:413-417.
77. Obura DO. Resilience and climate change: lessons from coral reefs and bleaching in the Western Indian Ocean. Estuaruarine, Coastal Shelf Science 2005, 63:353-372.
78. Pandolfi JM, Bradbury RH, Sala E. Global trajectories of the long-term decline of coral reef ecosystems. Science 2003, 301:955-958.
79. Parmesan C. Ecological and evolutionary responses to recent climate change. Annual Review of Ecology, Evolution, and Systematics 2006, 37:637.
80. Potts DC, Swart PK. Water temperature as an indicator of environmental variability on a coral-reef. Limnology and Oceanography 1984, 29:504-516.
81. Rayner NA, Parker DE, Horton EB. Global analyses of sea surface temperature, sea ice, and night marine air temperature since the late nineteenth century. Journal of Geophysical Research 2003, 108:4407.
82. Richmond RH, Hunter CL. Reproduction and recruitment of corals: comparisons among the Caribbean, the Tropical Pacific, and the Red Sea. Marine Ecology Progress Series 1990, 60:185-203.
83. Riegl BM, Purkis SJ. Model of coral population response to accelerated bleaching and mass mortality in a changing climate. Ecological Modelling 2009, 220:192-208.
84. Ronce O, Kirkpatrick M. When sources become sinks: Migrational meltdown in heterogeneous habitats. Evolution 2001, 55:1520-1531.
85. Salm RV, Done T, McLeod E. Marine protected area planning in a changing climate. Coral Reefs and Climate Change: Science and Management, vol. 61 of Coastal and Estuarine Studies 2006, 207-221. Phinney JT, Heogh-Guldberg O, Kleypas JSkirving WStrong A. In, eds, pp, American Geophysical Union, Washington, DC
86. Santos SR, Coffroth MA. Molecular genetic evidence that dinoflagellates belonging to the genus Symbiodinium freudenthal are haploid. Biological Bulletin 2003, 204:10-20.
87. Sheppard CRC. Predicted recurrences of mass coral mortality in the Indian Ocean. Nature 2003, 425:294-297.
88. Smith SV, Buddemeier RW. Global change and coral-reef ecosystems. Annual Review of Ecology and Systematics 1992, 23:89-118.
89. Sotka EE, Thacker RW. Do some corals like it hot? Trends in Ecology and Evolution 2005, 20:59-62.
90. Stat M, Carter D, Hoegh-Guldberg O. The evolutionary history of Symbiodinium and scleractinian hosts - Symbiosis, diversity, and the effect of climate change. Perspectives in Plant Ecology Evolution and Systematics 2006, 8:23-43.
91. Stimson J, Sakai K, Sembali H. Interspecific comparison of the symbiotic relationship in corals with high and low rates of bleaching-induced mortality. Coral Reefs 2002, 21:409-421.
92. Sutherland KP, Porter JW, Torres C. Disease and immunity in Caribbean and Indo-Pacific zooxanthellate corals. Marine Ecology Progress Series 2004, 266:273-302.
93. Szmant AM, Gassman NJ. The effects of prolonged " bleaching" on the tissue biomass and reproduction of the reef coral Montastrea annularis. Coral Reefs 1990, 8:217-224.
94. van Oppen MJH, Gates RD. Conservation genetics and the resilience of reef-building corals. Molecular Ecology 2006, 15:3863-3883.
95. Walther GR, Post E, Convey P. Ecological responses to recent climate change. Nature 2002, 416:389-395.
96. Ware JR. The effect of global warming on coral reefs: acclimate or die. Proceedings of the 8th International Coral Reef Symposium 1997, 1:527-532.
97. West JM, Salm RV. Resistance and resilience to coral bleaching: implications for coral reef conservation and management. Conservation Biology 2003, 17:956-967.
98. Wilkinson CR. Global and local threats to coral reef functioning and existence: review and predictions. Marine and Freshwater Research 1999, 50:867-878.
99. Wolanski E, Richmond RH, McCook L. A model of the effects of land-based, human activities on the health of coral reefs in the Great Barrier Reef and in Fouha Bay, Guam, Micronesia. Journal of Marine Systems 2004, 46:133-144.
100. Wooldridge S, Done T, Berkelmans R, Jones R, Marshall P. Precursors for resilience in coral communities in a warming climate: a belief network approach. Marine Ecology Progress Series 2005, 295:157-169.