Abstract
Mass bleaching events resulting in coral mortality are among the greatest threats to coral reefs, and are projected to increase in frequency and intensity with global warming. Achieving a better understanding of the consistency of the response of coral assemblages to thermal stress, both spatially and temporally, is essential to determine which reefs are more able to tolerate climate change. We compared variations in spatial and taxonomic patterns between two bleaching events at the scale of an island (Moorea Island, French Polynesia). Despite similar thermal stress and light conditions, bleaching intensity was significantly lower in 2007 (approximately 37 % of colonies showed signs of bleaching) than in 2002, when 55 % of the colonies bleached. Variations in the spatial patterns of bleaching intensity were consistent between the two events. Among nine sampling stations at three locations and three depths, the stations at which the bleaching response was lowest in 2002 were those that showed the lowest levels of bleaching in 2007. The taxonomic patterns of susceptibility to bleaching were also consistent between the two events. These findings have important implications for conservation because they indicate that corals are capable of acclimatization and/or adaptation and that, even at small spatial scales, some areas are consistently more susceptible to bleaching than others.
Similar content being viewed by others
References
Adjeroud, M., Augustin, D., Galzin, R., & Salvat, B. (2002). Natural disturbances and interannual variability on coral reef communities on the outer slope of Tiahura (Moorea, French Polynesia): 1991 to 1997. Marine Ecology Progress Series, 237, 121–131.
Adjeroud, M., Michonneau, F., Edmunds, P. J., Chancerelle, Y., Lison de Loma, T., Penin, L., et al. (2009). Recurrent disturbances, recovery trajectories, and resilience of coral assemblages on a South Central Pacific reef. Coral Reefs, 28(3), 775–780.
Anthony, K. R. N., & Hoegh-Guldberg, O. (2003a). Kinetics of photoacclimation in corals. Oecologia, 134, 23–31.
Anthony, K. R. N., & Hoegh-Guldberg, O. (2003b). Variation in coral photosynthesis, respiration and growth characteristics in contrasting light microhabitats: an analogue to plants in forest gaps and understoreys? Functional Ecology, 17, 246–259.
Baker, A. C. (2003). Flexibility and specifity in coral–algal symbiosis: diversity, ecology, and biogeography of Symbiodinium. Annual Review of Ecology, Evolution, and Systematic, 34, 661–689.
Baker, A. C., Glynn, P. W., & Riegl, B. (2008). Climate change and coral reef bleaching: an ecological assessment of long-term impacts, recovery trends and future outlook. Estuarine, Coastal and Shelf Science, 80(4), 435–471.
Bellwood, D. R., Hughes, T. P., Folke, C., & Nyström, M. (2004). Confronting the coral reef crisis. Nature, 429, 827–833.
Berkelmans, R. (2009). Bleaching and mortality thresholds: How much is too much? In M. J. H. van Oppen & J. M. Lough (Eds.), Coral bleaching (pp. 103–119). Berlin: Springer-Verlag. Ecological Studies.
Berkelmans, R., De'ath, G., Kininmonth, S., & Skirving, W. J. (2004). A comparison of the 1998 and 2002 coral bleaching events on the Great Barrier Reef: spatial correlation, patterns and predictions. Coral Reefs, 23, 74–83.
Berumen, M. L., & Pratchett, M. S. (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(4), 647–653.
Brown, B. E., Ambarsari, I., Warner, M. E., Fitt, W. K., Dunne, R. P., Gibb, S. W., et al. (1999). Diurnal changes in photochemical efficiency and xanthophyll concentrations in shallow water reef corals: evidence for photoinhibition and photoprotection. Coral Reefs, 18, 99–105.
Brown, B. E., Dunne, R. P., Goodson, M. S., & Douglas, A. E. (2000). Marine ecology: bleaching patterns in reef corals. Nature, 404(6774), 142–143.
Brown, B. E., Downs, C. A., Dunne, R. P., & Gibb, S. W. (2002a). Exploring the basis of thermotolerance in the reef coral Goniastrea aspera. Marine Ecology Progress Series, 242, 119–129.
Brown, B. E., Dunne, R. P., Goodson, M. S., & Douglas, A. E. (2002b). Experience shapes the susceptibility of a reef coral to bleaching. Coral Reefs, 21(2), 119–126.
Carilli, J. E., Norris, R. D., Black, B. A., Walsh, S. M., & McField, M. (2009). Local stressors reduce coral resilience to bleaching. PloS One, 4(7), e6324.
Coles, S. L., & Brown, B. E. (2003). Coral bleaching—capacity for acclimatization and adaptation. Advances in Marine Biology, 46, 184–206.
Douglas, A. E. (2003). Coral bleaching—how and why? Marine Pollution Bulletin, 46, 385–392.
Dunne, R. P., & Brown, B. E. (2001). The influence of solar radiation on bleaching of shallow water reef corals in the Andaman Sea, 1993–1998. Coral Reefs, 20(3), 201–210.
Edmunds, P. J. (1994). Evidence that reef-wide patterns of coral bleaching may be the result of the distribution of bleaching-susceptible clones. Marine Biology, 121(1), 137–142.
Gardner, T., Côté, I., Gill, J., Grant, A., & Watkinson, A. (2003). Long-term region-wide declines in Caribbean corals. Science, 301, 958–960.
Gleason, M. G. (1993). Effects of disturbance on coral communities: bleaching in Moorea, French Polynesia. Coral Reefs, 12, 193–201.
Gleason, D., & Wellington, G. (1993). Ultraviolet radiation and coral bleaching. Nature, 365(6449), 836–837.
Glynn, P. W., Maté, J. L., Baker, A. C., & Calderón, M. O. (2001). Coral bleaching and mortality in Panama and Ecuador during the 1997–1998 El Nino Southern Oscillation Event: spatial/temporal patterns and comparisons with the 1982–1983 event. Bulletin of Marine Science, 69(1), 79–109.
Goulet, T., LaJeunesse, T., & Fabricius, K. (2008). Symbiont specificity and bleaching susceptibility among soft corals in the 1998 Great Barrier Reef mass coral bleaching event. Marine Biology, 154(5), 795–804.
Graham, N., Ainsworth, T., Baird, A., Ban, N., Bay, L., Cinner, J., et al. (2011). From microbes to people: tractable benefits of no-take areas for coral reefs. Oceanography and Marine Biology: An Annual Review, 49, 117–148.
Hoegh-Guldberg, O. (1999). Climate change, coral bleaching and the future of the world's coral reefs. Marine and Freshwater Research, 50(8), 839–866.
Hoegh-Guldberg, O., & Salvat, B. (1995). Periodic mass-bleaching and elevated sea surface temperatures: bleaching of outer slope communities in Moorea, French Polynesia. Marine Ecology Progress Series, 121, 181–190.
Hughes, T. P., Baird, A. H., Bellwood, D. R., Card, M., Connolly, S. R., Folke, C. S., et al. (2003). Climate change, human impacts, and the resilience of coral reefs. Science, 301, 929–933.
Iglesias-Prieto, R., & Trench, R. K. (1997). Acclimation and adaptation to irradiance in symbiotic dinoflagellates. II. Response of chlorophyll-protein complexes to different photon-flux densities. Marine Biology, 130(1), 23–33.
Jackson, J. B. C., Kirby, M. X., Berger, W. H., Bjorndal, K. A., Botsford, L. W., Bourque, B. J., et al. (2001). Historical overfishing and the recent collapse of coastal ecosystems. Science, 293(5530), 629–637.
Jiménez, C., Cortés, J., León, A., & Ruíz, E. (2001). Coral bleaching and mortality associated with the 1997–98 El Nino in an upwelling environment in the eastern Pacific (Gulf of Papagayo, Costa Rica). Bulletin of Marine Science, 69(1), 151–169.
Karlson, R., & Hurd, L. (1993). Disturbance, coral reef communities, and changing ecological paradigms. Coral Reefs, 12, 117–125.
Laurent, V., Maamaatuaiahutapu, K., Maiau, J., & Varney, P. (2004). Atlas climatologique de la Polynésie française. Météo France: Papeete, Polynésie Française.
Lenihan, H. S., Adjeroud, M., Kotchen, M. J., Hench, J. L., & Nakamura, T. (2008). Reef structure regulates small-scale spatial variation in coral bleaching. Marine Ecology Progress Series, 370, 127–141.
Lesser, M. P., & Farrell, J. H. (2004). Exposure to solar radiation increases damage to both host tissues and algal symbionts of corals during thermal stress. Coral Reefs, 23(3), 367–377.
Liu, G., Strong, A. E., Skirving, W., & Arzayus, L. F. Overview of NOAA Coral Reef Watch Program’s near-real-time satellite global coral bleaching monitoring activities. In Proceedings of the 10th International Coral Reef Symposium, Okinawa, Japan, 2004 (Vol. 1, pp. 1783–1793)
Loya, Y., Sakai, K., Yamazato, K., Nakano, Y., Sambali, H., & van Woesik, R. (2001). Coral bleaching: the winners and the losers. Ecology Letters, 4(2), 122–131.
Marshall, P. A., & Baird, A. H. (2000). Bleaching of corals on the Great Barrier Reef: differential susceptibilities among taxa. Coral Reefs, 19(2), 155–163.
Maynard, J. A., Anthony, K. R. N., Marshall, P. A., & Masiri, I. (2008a). Major bleaching events can lead to increased thermal tolerance in corals. Marine Biology, 155(2), 173–182.
Maynard, J. A., Turner, P. J., Anthony, K. R. N., Baird, A. H., Berkelmans, R., Eakin, C. M., et al. (2008b). ReefTemp: an interactive monitoring system for coral bleaching using high-resolution SST and improved stress predictors. Geophysical Research Letters, 35, L05603.
McClanahan, T. R., Ateweberhan, M., Muhando, C. A., Maina, J., & Mohammed, M. S. (2007). Effects of climate and seawater temperature variation on coral bleaching and mortality. Ecological Monographs, 77(4), 503–525.
McClanahan, T. R., Weil, E., Cortés, J., Baird, A. H., & Ateweberhan, M. (2009). Consequences of coral bleaching for sessile reef organisms. In M. J. H. van Oppen & J. M. Lough (Eds.), Coral bleaching (pp. 121–138). Berlin: Springer-Verlag. Ecological studies.
McClanahan, T. R., Donner, S. D., Maynard, J. A., MacNeil, M. A., Graham, N. A. J., Maina, J., et al. (2012). Prioritizing key resilience indicators to support coral reef management in a changing climate. PloS One, 7(8), e42884.
Middlebrook, R., Hoegh-Guldberg, O., & Leggat, W. (2008). The effect of thermal history on the susceptibility of reef-building corals to thermal stress. Journal of Experimental Biology, 211(7), 1050–1056.
Mumby, P. J., Harborne, A. R., Williams, J., Kappel, C. V., Brumbaugh, D. R., Micheli, F., 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(20), 8362–8367.
Mumby, P. J., Elliott, I. A., Eakin, C. M., Skirving, W., Paris, C. B., Edwards, H. J., et al. (2011). Reserve design for uncertain responses of coral reefs to climate change. Ecology Letters, 14(2), 132–140.
Nakamura, T., & van Woesik, R. (2001). Water-flow rates and passive diffusion partially explain differential survival of corals during the 1998 bleaching event. Marine Ecology Progress Series, 212, 301–304.
Nakamura, T., van Woesik, R., & Yamasaki, H. (2005). Photoinhibition of photosynthesis is reduced by water flow in the reef-building coral Acropora digitifera. Marine Ecology Progress Series, 301, 109–118.
Obura, D. O., & Grimsdith, G. (2009). Resilience assessment of coral reefs - Assessment protocol for coral reefs, focusing on coral bleaching and thermal stress. IUCN working group on Climate Change and Coral Reefs (Vol. 5, pp. 70). Gland, Switzerland: IUCN.
Oliver, J. K., Berkelmans, R., & Eakin, C. M. (2009). Coral bleaching in space and time. In M. J. H. van Oppen & J. M. Lough (Eds.), Coral bleaching (pp. 21–39). Berlin: Springer-Verlag. Ecological studies.
Penin, L., Adjeroud, M., Pratchett, M. S., & Hughes, T. P. (2007a). Spatial distribution of juvenile and adult corals around Moorea (French Polynesia): implications for population regulation. Bulletin of Marine Science, 80, 379–389.
Penin, L., Adjeroud, M., Schrimm, M., & Lenihan, H. (2007b). High spatial variability in coral bleaching around Moorea (French Polynesia): patterns across locations and water depths. Comptes Rendus Biologies, 330, 171–181.
Penin, L., Michonneau, F., Baird, A. H., Connolly, S. R., Pratchett, M. S., Kayal, M., et al. (2010). Early post-settlement mortality and the structure of coral assemblages. Marine Ecology Progress Series, 408, 55–64.
Podesta, G. P., & Glynn, P. W. (2001). The 1997–98 El Nino event in Panama and Galapagos: an update of thermal stress indices relative to coral bleaching. Bulletin of Marine Science, 69(1), 43–59.
Rosenberg, E., Koren, O., Reshef, L., Efrony, R., & Zilber-Rosenberg, I. (2007). The role of microorganisms in coral health, disease and evolution. Nature Reviews Microbiology, 5(5), 355–362.
Salih, A., Larkum, A., Cox, G., Kuhl, M., & Hoegh-Guldberg, O. (2000). Fluorescent pigments in corals are photoprotective. Nature, 408, 850–853.
Salvat, B. (1992). Blanchissement et mortalité des scléractiniaires sur les récifs de Moorea (archipel de la Société) en 1991. Comptes Rendus de l'Académie des Sciences, Paris III, 314, 105–111.
Schrimm, M., Buscail, R., & Adjeroud, M. (2004). Spatial variability of the biogeochemical composition of surface sediments in an insular coral reef ecosystem: Moorea, French Polynesia. Estuarine, Coastal and Shelf Science, 60(3), 515–528.
Sheppard, C. (2009). Large temperature plunges recorded by data loggers at different depths on an Indian Ocean atoll: comparison with satellite data and relevance to coral refuges. Coral Reefs, 28(2), 399–403.
Stat, M., Carter, D., & Hoegh-Guldberg, O. (2006). The evolutionary history of Symbiodinium and scleractinian hosts—symbiosis, diversity, and the effect of climate change. Perspectives in Plant Ecology, Evolution and Systematics, 8(1), 23–43.
van Oppen, M. J. H., Baker, A. C., Coffroth, M. A., & Willis, B. L. (2009). Bleaching resistance and the role of algal endosymbionts. In M. J. H. van Oppen & J. M. Lough (Eds.), Coral bleaching (pp. 83–101). Berlin: Springer-Verlag. Ecological Studies 205.
Venn, A. A., Loram, J. E., & Douglas, A. E. (2008). Photosynthetic symbioses in animals. Journal of Experimental Botany, 59(5), 1069–1080.
Weis, V. M. (2008). Cellular mechanisms of Cnidarian bleaching: stress causes the collapse of symbiosis. Journal of Experimental Biology, 211(19), 3059–3066.
West, J. M., & Salm, R. V. (2003). Resistance and resilience to coral bleaching: implication for coral reef conservation and management. Conservation Biology, 17(4), 956–967.
Wooldridge, S., & Done, T. (2004). Learning to predict large-scale coral bleaching from past events: a Bayesian approach using remotely sensed data, in-situ data, and environmental proxies. Coral Reefs, 23(1), 96–108.
Wooldridge, S. A., & Done, T. J. (2009). Improved water quality can ameliorate effects of climate change on corals. Ecological Applications, 19(6), 1492–1499.
Acknowledgments
We thank the logistic support from CRIOBE station (Centre de Recherches Insulaires et Observatoire de l’Environnement-USR CNRS-EPHE 3278, Moorea), Pascal Ung, Yannick Chancerelle, Franck Lerouvreur and many students for diving assistance, and Rebecca Weeks for proofreading. Insolation data were obtained from the NASA Langley Research Center POWER Project.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Penin, L., Vidal-Dupiol, J. & Adjeroud, M. Response of coral assemblages to thermal stress: are bleaching intensity and spatial patterns consistent between events?. Environ Monit Assess 185, 5031–5042 (2013). https://doi.org/10.1007/s10661-012-2923-3
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10661-012-2923-3