Life histories predict coral community disassembly under multiple stressors

Global Change Biology

Volumn 19, Issue 6, 2013, Pages 1930-1940

  Darling, Emily S ^a   McClanahan, Timothy R ^b   Côté, Isabelle M ^a  

^a SIMON FRASER UNIVERSITY   (Canada)

^b WILDLIFE CONSERVATION SOCIETY   (United States)

Author keywords

Climate change; Cumulative effects; Fishing; Kenya; Marine reserves; Scleractinian corals; Stressor interactions; Synergy

Indexed keywords

BLEACHING; CLIMATE CHANGE; COMMUNITY DYNAMICS; COMMUNITY RESPONSE; CORAL REEF; ENVIRONMENTAL STRESS; FISHING; LIFE HISTORY; MARINE PARK; SPECIES DIVERSITY; SPECIES RICHNESS; SYNERGISM;

ANIMAL; ANTHOZOA; ARTICLE; CORAL REEF; PHYSIOLOGICAL STRESS; PHYSIOLOGY;

ANIMALS; ANTHOZOA; CORAL REEFS; STRESS, PHYSIOLOGICAL;

KENYA;

ANTHOZOA; SCLERACTINIA;

EID: 84877020899     PISSN: 13541013     EISSN: 13652486     Source Type: Journal    
DOI: 10.1111/gcb.12191     Document Type: Article

References (87)

1. Alvarez-Filip L, Dulvy NK, Gill JA, Côté IM, Watkinson AR (2009) Flattening of Caribbean coral reefs: region-wide declines in architectural complexity. Proceedings of the Royal Society B: Biological Sciences, 276, 3019-3025.
2. Ateweberhan M, McClanahan TR, Graham NAJ, Sheppard CRC (2011) Episodic heterogeneous decline and recovery of coral cover in the Indian Ocean. Coral Reefs, 30, 739-752.
3. Ayre DJ, Miller KJ (2004) Where do clonal coral larvae go? Adult genotypic diversity conflicts with reproductive effort in the brooding coral, Pocillopora damicornis. Marine Ecology Progress Series, 277, 95-105.
4. Baird AH, Morse AN (2004) Induction of metamorphosis in larvae of the brooding corals Acropora palifera and Stylophora pistillata. Marine and Freshwater Research, 55, 469-472.
5. Bellwood DR, Hughes TP, Folke C, Nyström M (2004) Confronting the coral reef crisis. Nature, 429, 827-833.
6. Bruno JF, Selig ER (2007) Regional decline of coral cover in the Indo-Pacific: timing, extent, and subregional comparisons. PLoS ONE, 2, e711.
7. Canty A, Ripley B (2012) Boot: Bootstrap R (S-Plus) Functions. R package version 1.3-7. Available at: http://cran.r-project.org/web/packages/boot/citation.html (accessed 15 March 2013).
8. Carreiro-Silva M, McClanahan TR (2012) Macrobioerosion of dead branching Porites, 4 and 6 years after coral mass mortality. Marine Ecology Progress Series, 458, 103-122.
9. Casella G, Berger RL (2001) Statistical Inference. Duxbury Press, Pacific Grove.
10. Chapin F III, Zavaleta E, Eviner V et al. (2000) Consequences of changing biodiversity. Nature, 405, 234-242.
11. Chong-Seng KM, Mannering TD, Pratchett MS, Bellwood DR, Graham NAJ (2012) The influence of coral reef benthic condition on associated fish assemblages. PLoS ONE, 7, e42167.
12. Côté IM, Darling ES (2010) Rethinking ecosystem resilience in the face of climate change. PLoS Biology, 8, e1000438.
13. Côté IM, Gill JA, Gardner TA, Watkinson AR (2005) Measuring coral reef decline through meta-analyses. Philosophical Transactions of the Royal Society of London Series B Biological Sciences, 360, 385-395.
14. Cover W (2011) Species Interactions Affecting Corals and Recruitment on a Protected, High-Latitude Reefs: Herbivory, Predation, and Competition by Fishes, Urchins, Macroalgae and Cyanobacteria. University of California, Santa Cruz. PhD dissertation.
15. Cowpertwait PSP, Metcalfe AV (2009) Introductory Time Series With R. Springer, New York, NY.
16. Cros A, McClanahan TR (2003) Coral transplant damage under various management conditions in the Mombasa Marine National Park, Kenya. Western Indian Ocean Journal of Marine Science, 2, 127-136.
17. Cumming RL (2002) Tissue injury predicts colony decline in reef-building corals. Marine Ecology Progress Series, 242, 131-141.
18. Darling ES, Côté IM (2013). Vulnerability of coral reefs to climate change and multiple stressors. In: Climate Vulnerability, Volume 4: Ecosystem Function (eds Seastedt T, Suding K). Elsevier, New York, NY. in press.
19. Darling ES, McClanahan TR, Côté IM (2010) Combined effects of two stressors on Kenyan coral reefs are additive or antagonistic, not synergistic. Conservation Letters, 3, 122-130.
20. Darling ES, Alvarez-Filip L, Oliver TA, McClanahan TR, Côté IM (2012) Evaluating life-history strategies of reef corals from species traits. Ecology Letters, 15, 1378-1386.
21. Dulvy NK, Freckleton RP, Polunin NVC (2004) Coral reef cascades and the indirect effects of predator removal by exploitation. Ecology Letters, 7, 410-416.
22. Gardner TA, Côté IM, Gill JA, Grant A, Watkinson AR (2003) Long-term region-wide declines in Caribbean corals. Science, 301, 958-960.
23. Gaston KJ, Fuller R (2008) Commonness, population depletion and conservation biology. Trends in Ecology and Evolution, 23, 14-19.
24. Graham RW, Grimm EC (1990) Effects of global climate change on the patterns of terrestrial biological communities. Trends in Ecology and Evolution, 5, 289-292.
25. Graham NAJ, Wilson SK, Jennings S, Polunin NVC, Bijoux JP, Robinson J (2006) Dynamic fragility of oceanic coral reef ecosystems. Proceedings of the National Academy of Sciences of the United States of America, 103, 8425-8429.
26. Graham NAJ, McClanahan TR, MacNeil MA et al. (2008) Climate warming, marine protected areas and the ocean-scale integrity of coral reef ecosystems. PLoS ONE, 3, e3039.
27. Graham NAJ, Chabanet P, Evans RD et al. (2011) Extinction vulnerability of coral reef fishes. Ecology Letters, 14, 341-348.
28. Grime JP, Pierce S (2012) The Evolutionary Strategies That Shape Ecosystems. Wiley-Blackwell, Oxford, UK.
29. Halpern BS, Walbridge S, Selkoe KA et al. (2008) A global map of human impact on marine ecosystems. Science, 319, 948-952.
30. Highsmith R (1982) Reproduction by fragmentation in corals. Marine Ecology Progress Series, 7, 207-226.
31. Hillebrand H, Bennett DM, Cadotte MW (2008) Consequences of dominance: a review of evenness effects on local and regional ecosystem processes. Ecology, 89, 1510-1520.
32. Hoegh-Guldberg O, Mumby PJ, Hooten AJ et al. (2007) Coral reefs under rapid climate change and ocean acidification. Science, 318, 1737-1742.
33. Hughes TP, Baird AH, Bellwood DR et al. (2003) Climate change, human impacts and the resilience of coral reefs. Science, 301, 929-933.
34. Hughes TP, Graham NAJ, Jackson JBC, Mumby PJ, Steneck RS (2010) Rising to the challenge of sustaining coral reef resilience. Trends in Ecology and Evolution, 25, 633-642.
35. Hughes TP, Baird AH, Dinsdale EA, Moltschaniwskyj NA, Pratchett MS, Tanner JE, Willis BL (2012) Assembly rules of reef corals are flexible along a steep climatic gradient. Current Biology, 22, 736-741.
36. Ives AR, Zhu J (2006) Statistics for correlated data: phylogenies, space, and time. Ecological Applications, 16, 20-32.
37. Jackson JBC, Kirby MX, Berger WH et al. (2001) Historical overfishing and the recent collapse of coastal ecosystems. Science, 293, 629-637.
38. Jennings S, Kaiser MJ (1998) The effects of fishing on marine ecosystems. Advances in Marine Biology, 34, 201-352.
39. Kaiser MJ, Clarke KR, Hinz H, Austen MCV, Somerfield PJ, Karakassis I (2006) Global analysis of response and recovery of benthic biota to fishing. Marine Ecology Progress Series, 311, 1-14.
40. Kordas RL, Harley CD, O'Connor MI (2011) Community ecology in a warming world: The influence of temperature on interspecific interactions in marine systems. Journal of Experimental Marine Biology and Ecology, 400, 218-226.
41. Loya Y, Sakai K, Yamazato K, Nakano Y (2001) Coral bleaching: the winners and the losers. Ecology Letters, 4, 122-131.
42. Maina J, Venus V, McClanahan TR, Ateweberhan M (2008) Modelling susceptibility of coral reefs to environmental stress using remote sensing data and GIS models. Ecological Modelling, 212, 180-199.
43. Mangi SC, Roberts CM (2006) Quantifying the environmental impacts of artisanal fishing gear on Kenya's coral reef ecosystems. Marine Pollution Bulletin, 52, 1646-1660.
44. Marshall P (2000) Skeletal damage in reef corals: relating resistance to colony morphology. Marine Ecology Progress Series, 200, 177-189.
45. McClanahan TR (2004) The relationship between bleaching and mortality of common corals. Marine Biology, 144, 1239-1245.
46. McClanahan TR, Shafir SH (1990) Causes and consequences of sea urchin abundance and diversity in Kenyan coral reef lagoons. Oecologia, 83, 362-370.
47. McClanahan TR, Maina J (2003) Response of coral assemblages to the interaction between natural temperature variation and rare warm-water events. Ecosystems, 6, 551-563.
48. McClanahan TR, Graham NAJ (2005) Recovery trajectories of coral reef fish assemblages within Kenyan marine protected areas. Marine Ecology Progress Series, 294, 241-248.
49. McClanahan TR, Muthiga NA, Mangi S (2001) Coral and algal changes after the 1998 coral bleaching: interaction with reef management and herbivores on Kenyan reefs. Coral Reefs, 19, 380-391.
50. McClanahan TR, Polunin NVC, Done T (2002) Ecological states and the resilience of coral reefs. Ecology and Society, 6, 18.
51. McClanahan TR, Mwaguni S, Muthiga NA (2005a) Management of the Kenyan coast. Ocean and Coastal Management, 48, 901-931.
52. McClanahan TR, Maina J, Starger CJ, Herron-Perez P, Dusek E (2005b) Detriments to postbleaching recovery of corals. Coral Reefs, 24, 230-246.
53. McClanahan TR, Ateweberhan M, Muhando CA, Maina J, Mohammed MS (2007a) Effects of climate and seawater temperature variation on coral bleaching and mortality. Ecological Monographs, 77, 503-525.
54. McClanahan TR, Atewerbehan M, Graham NAJ, Wilson SK, Ruiz-Sebastian C, Guillaume MMM, Bruggemann JH (2007b) Western Indian Ocean coral communities: bleaching responses and susceptibility to extinction. Marine Ecology Progress Series, 337, 1-13.
55. McClanahan TR, Ateweberhan M, Omukoto J (2008) Long-term changes in coral colony size distributions on Kenyan reefs under different management regimes and across the 1998 bleaching event. Marine Biology, 153, 755-768.
56. McClanahan TR, Weil E, Maina J (2009) Strong relationship between coral bleaching and growth anomalies in massive Porites. Global Change Biology, 15, 1804-1816.
57. McClanahan TR, Maina J, Muthiga N (2011a) Associations between climate stress and coral reef diversity in the Western Indian Ocean. Global Change Biology, 17, 2023-2032.
58. McClanahan TR, Graham NAJ, MacNeil MA, Muthiga NA, Cinner JE, Bruggemann JH, Wilson SK (2011b) Critical thresholds and tangible targets for ecosystem-based management of coral reef fisheries. Proceedings of the National Academy of Sciences of the United States of America, 108, 17230-17233.
59. McCook LJ, Jompa J, Diaz-Pulido G (2001) Competition between corals and algae on coral reefs: a review of evidence and mechanisms. Coral Reefs, 19, 400-417.
60. Mumby PJ (2009) Herbivory versus corallivory: are parrotfish good or bad for Caribbean coral reefs? Coral Reefs, 28, 683-690.
61. Mumby PJ, Harborne AR, Williams J et al. (2007) Trophic cascade facilitates coral recruitment in a marine reserve. Proceedings of the National Academy of Sciences of the United States of America, 104, 8362-8367.
62. Newton K, Côté IM, Pilling GM, Jennings S, Dulvy NK (2007) Current and future sustainability of island coral reef fisheries. Current Biology, 17, 655-658.
63. Norström AV, Nyström M, Lokrantz J, Folke C (2009) Alternative states on coral reefs: beyond coral-macroalgal phase shifts. Marine Ecology Progress Series, 376, 295-306.
64. Obura D (2001) Kenya. Marine Pollution Bulletin, 42, 1264-1278.
65. Oehlert GW (1992) A note on the delta method. American Statistician, 46, 27-29.
66. O'Leary JK, McClanahan TR (2010) Trophic cascades result in large-scale coralline algae loss through differential grazer effects. Ecology, 91, 3584-3597.
67. O'Leary JK, Potts DC, Braga JC, McClanahan TR (2012) Indirect consequences of fishing: reduction of coralline algae suppresses juvenile coral abundance. Coral Reefs, 31, 557-559.
68. Pandolfi JM, Jackson JBC, Baron N et al. (2005) Are U.S. coral reefs on the slippery slope to slime? Science, 307, 1725-1726.
69. Parmesan C, Yohe G (2003) A globally coherent fingerprint of climate change impacts across natural systems. Nature, 421, 37-42.
70. Pratchett MS, Munday PL, Wilson SK et al. (2008) Effects of climate-induced coral bleaching on coral-reef fishes: ecological and economic consequences. Oceanography and Marine Biology: an Annual Review, 46, 251-296.
71. R Development Core Team (2012). R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria. Available at: http://www.R-project.org (accessed 1 January 2012).
72. Riegl BM, Bruckner AW, Rowlands GP, Purkis SJ, Renaud P (2012) Red Sea coral reef trajectories over 2 decades suggest increasing community homogenization and decline in coral size. PLoS ONE, 7, e38396.
73. Roberts CM (1995) Effects of fishing on the ecosystem structure of coral reefs. Conservation Biology, 9, 988-995.
74. Schabenberger O, Pierce FJ (2002) Contemporary Statistical Models for the Plant and Soil Sciences. CRC Press, New York, NY.
75. Selig ER, Bruno JF (2010) A global analysis of the effectiveness of marine protected areas in preventing coral loss. PLoS ONE, 5, e9278.
76. Selig ER, Casey KS, Bruno JF (2012) Temperature-driven coral decline: the role of marine protected areas. Global Change Biology, 18, 1561-1570.
77. Soong K (1993) Colony size as a species character in massive reef corals. Coral Reefs, 12, 77-83.
78. Tanner JE, Hughes TP, Connell JH (2009) Community-level density dependence: an example from a shallow coral assemblage. Ecology, 90, 506-516.
79. Veron JEN (2000) Corals of the World. Australian Institute of Marine Science and CRR Qld Pty Ltd, Townsville, Australia.
80. Vinebrooke RD, Cottingham KL, Norberg J, Scheffer M, Dodson SI, Maberly SC, Sommer U (2004) Impacts of multiple stressors on biodiversity and ecosystem functioning: the role of species cotolerance. Oikos, 104, 451-457.
81. Wells S, Burgess N, Ngusaru A (2007) Towards the 2012 marine protected area targets in Eastern Africa. Ocean and Coastal Management, 50, 67-83.
82. Williams JW, Jackson ST (2007) Novel climates, no-analog communities, and ecological surprises. Frontiers in Ecology and the Environment, 5, 475-482.
83. van Woesik R, Sakai K, Ganase A, Loya Y (2011) Revisiting the winners and the losers a decade after coral bleaching. Marine Ecology Progress Series, 434, 67-76.
84. Yakob L, Mumby PJ (2011) Climate change induces demographic resistance to disease in novel coral assemblages. Proceedings of the National Academy of Sciences of the United States of America, 108, 1967-1969.
85. Zar JH (1998) Biostatistical Analysis. Prentice Hall, Upper Saddle River NJ.
86. Zavaleta E, Pasari J, Moore J, Hernandez D, Suttle KB, Wilmers CC (2009) Ecosystem responses to community disassembly. Annals of the New York Academy of Sciences, 1162, 311-333.
87. Zuur AF, Ieno EM, Walker N, Saviliev AA, Smith GM (2009) Mixed Effects Models and Extensions in Ecology with R. Springer, New York, NY.