Hostname: page-component-586b7cd67f-t8hqh Total loading time: 0 Render date: 2024-11-27T22:26:43.540Z Has data issue: false hasContentIssue false

Detecting the effects of natural disturbances on coral assemblages in French Polynesia: A decade survey at multiple scales

Published online by Cambridge University Press:  15 July 2005

Mehdi Adjeroud
Affiliation:
Centre de Recherches Insulaires et Observatoire de l'Environnement (CRIOBE), BP 1013, 98729 Papetoai, Moorea, French Polynesia, and École Pratique des Hautes Études, UMR 8046 CNRS, Université de Perpignan, 66860 Perpignan Cedex, France
Yannick Chancerelle
Affiliation:
Centre de Recherches Insulaires et Observatoire de l'Environnement (CRIOBE), BP 1013, 98729 Papetoai, Moorea, French Polynesia, and École Pratique des Hautes Études, UMR 8046 CNRS, Université de Perpignan, 66860 Perpignan Cedex, France
Muriel Schrimm
Affiliation:
Centre de Recherches Insulaires et Observatoire de l'Environnement (CRIOBE), BP 1013, 98729 Papetoai, Moorea, French Polynesia, and École Pratique des Hautes Études, UMR 8046 CNRS, Université de Perpignan, 66860 Perpignan Cedex, France
Thierry Perez
Affiliation:
Centre Océanologique de Marseille, UMR 6540, DIMAR, rue de la batterie des lions, 13007 Marseille, France
David Lecchini
Affiliation:
Centre de Recherches Insulaires et Observatoire de l'Environnement (CRIOBE), BP 1013, 98729 Papetoai, Moorea, French Polynesia, and École Pratique des Hautes Études, UMR 8046 CNRS, Université de Perpignan, 66860 Perpignan Cedex, France
René Galzin
Affiliation:
Centre de Recherches Insulaires et Observatoire de l'Environnement (CRIOBE), BP 1013, 98729 Papetoai, Moorea, French Polynesia, and École Pratique des Hautes Études, UMR 8046 CNRS, Université de Perpignan, 66860 Perpignan Cedex, France
Bernard Salvat
Affiliation:
Centre de Recherches Insulaires et Observatoire de l'Environnement (CRIOBE), BP 1013, 98729 Papetoai, Moorea, French Polynesia, and École Pratique des Hautes Études, UMR 8046 CNRS, Université de Perpignan, 66860 Perpignan Cedex, France
Get access

Abstract

Coral reefs in French Polynesia, just like many others throughout the world, have been subjected to several natural disturbances including 15 cyclones, seven major bleaching events, and several Acanthaster planci outbreaks since the 1980s. In order to document the effects of these perturbations on coral assemblages, we initiated a long-term monitoring program that extended over both local and regional scales. Coral cover was quantified at 20 sites situated on the outer reef slope of 13 islands. The results from the first decade (1992-2002) are analyzed and the adequacy of our approach is discussed in the context of identifying potential indicators of coral reef health. Among 13 islands in French Polynesia, only two were unaffected by natural disturbances. We found important local and regional variation in the impacts of coral bleaching and cyclones, and three major temporal trends were distinguished: 1) 10 sites where coral cover decreased in relation to the occurrence of major disturbances; 2) nine sites where coral cover increased, despite the occurrence of disturbances affecting seven of them; and 3) a site where no significant variation in coral cover was found. The responses to perturbations were different among coral genera: Acropora species were particularly susceptible to bleaching events, whereas physical damages induced by cyclones concerned mainly branching species of Acropora and Pocillopora. Thus, monitoring surveys could be improved by selecting different and complementary indicators (one on the variation in diversity, one estimating changes in the abundance/cover, and one estimating the potential for recovery), by integrating several spatial scales, and by including at least the most informative species. High frequency recordings of environmental parameters (e.g. sea surface temperature) may be also a complementary tools for identifying causal relationships between changes in coral reef community structure and the factors causing the changes.

Type
Research Article
Copyright
© EDP Sciences, IFREMER, IRD, 2005

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Adjeroud, M., 1997a, Factors influencing spatial patterns on coral reefs around Moorea, French Polynesia. Mar. Ecol. Prog. Ser. 159, 105-119. CrossRef
Adjeroud, M., 1997b, Long-term changes of epibenthic macrofauna communities in a closed lagoon (Taiaro Atoll, French Polynesia): 1972-1994. Hydrobiologia 356, 11-19. CrossRef
Adjeroud, M., Andréfouët, S., Payri, C., 2001, Mass mortality of macrobenthic communities in the lagoon of Hikueru atoll (French Polynesia). Coral Reefs 19, 287-291. CrossRef
Adjeroud, M., Augustin, D., Galzin, R., Salvat, B., 2002, Natural disturbances and interannual variability of coral reef communities on the outer slope of Tiahura (Moorea, French Polynesia): 1991 to 1997. Mar. Ecol. Prog. Ser. 237, 121-131. CrossRef
Ammenberg, P., Lindell, L.T., Kramer, P., 2002, Detection of coral bleaching using high spatial resolution satellite images. Proc. 9th Int. Coral Reef Symp. 2, 997-1000.
Andréfouët, S., Berkelmans, R., Odriozola, L., Done, T., Oliver, J., Müller-Karger, F., 2002, Choosing the appropriate spatial resolution for monitoring coral bleaching events using remote sensing. Coral Reefs 21, 147-154. CrossRef
Andres, N.G., Witman, J.D., 1995, Trends in community structure on a Jamaican reef. Mar. Ecol. Prog. Ser. 118, 305-310. CrossRef
Aronson, R.B., Edmunds, P.J., Precht, W.F., Swanson, D.W., Levitan, D.R., 1994, Large-scale, long-term monitoring of Caribbean coral reefs: Simple, quick, inexpensive techniques. Atoll Res. Bull. 421, 1-19. CrossRef
Atkinson, M.J., Carlson, B., Crow, G.L., 1995, Coral growth in high nutrient, low-pH seawater: A case study of corals cultured at the Waikiki Aquarium, Honolulu, Hawaii. Coral Reefs 14, 215-233. CrossRef
Augustin, D., Galzin, R., Legendre, P., Salvat, B., 1997, Variation interannuelle des peuplements récifaux du récif-barrière de Tiahura (île de Moorea, Polynésie française). Oceanol. Acta 20, 743-756.
Bak, R.P.M., Meesters, E.H., 1998, Coral population structure: The hidden information of colony-size frequency distribution. Mar. Ecol. Prog. Ser. 162, 301-306. CrossRef
Bak, R.P.M., Meesters, E.H., 1999, Population structure as a response of coral communities to global change. Am. Zool. 39, 56-65. CrossRef
Barnes, D.J., Lough, J.M., 1992, Systematic variations in the depth of skeleton occupied by coral tissue in massive colonies of Porites from the Great Barrier Reef. J. Exp. Mar. Biol. Ecol. 159, 113-128. CrossRef
Ben-Tzvi, O., Loya, Y., Abelson, A., 2004, Deterioration Index (DI): A suggested criterion for assessing the health of coral communities. Mar. Pollut. Bull. 48, 954-960. CrossRef
Black, N.A., Voellmy, R., Szmant, A.M., 1995, Heat shock Protein induction in Montastraea faveolata and Aiptasia pallida exposed to elevated temperatures. Biol. Bull. 188, 234-240. CrossRef
Bouchon, C., 1985, Quantitative study of scleractinian coral communities of Tiahura Reef (Moorea Island, French Polynesia). Proc. 5th Int. Coral Reef Congr. 6, 279-284.
Bouchon, C., Bouchon-Navaro, Y., Louis, M., 2004, Critères d'évaluation de la dégradation des communautés coralliennes dans la région Caraïbe. Rev. Ecol. 59, 113-121.
Brown, B.E., 1987, World wide death of corals – natural cyclical events or man-made pollution? Mar. Pollut. Bull. 18, 9-13. CrossRef
Brown, B.E., 1988, Assessing environmental impacts on coral reefs. Proc. 8th Int. Coral Reef Symp. 1, 71-80.
Brown, B.E., Le Tissier, M.D.A., Scoffin, T.P., Tudhope, A.W., 1990, Evaluation of the environmental impact of dredging on intertidal coral reefs at Ko Phuket, Thailand, using ecological and physiological parameters. Mar. Ecol. Prog. Ser. 65, 273-281. CrossRef
Brown, E., Cox, E., Jokiel, P., Rodgers, K., Smith, W., Tissot, B., Coles, S.L., Hultquist, J., 2004, Developement of benthic sampling methods for the Coral Reef Assessment and Monitoring Program (CRAMP) in Hawai'i. Pac. Sci. 58, 145-158. CrossRef
Bythell, J.C., Byhtell, M., Gladfelter, E.H., 1993, Initial results of a long-term coral reef monitoring program: Impact of cyclone Hugo at Buck Island Reef National Monument, St. Croix, US Virgin Islands. J. Exp. Mar. Biol. Ecol. 172, 171-183. CrossRef
Chabanet, P., Dufour, V., Galzin, R., 1995, Disturbances impact on reef fish communities in Reunion Island (Indian Ocean). J. Exp. Mar. Biol. Ecol. 188, 29-45. CrossRef
Chabanet, P., Bigot, L., Naim, O., Garnier, R., Tessier, E., Moyne-Picard, M., 2002, Coral reef monitoring at Reunion island (Western Indian Ocean) using the GCRMN method. Proc. 9th Int. Coral Reef Symp. 2, 873-878.
Chou, L.M., Sudara, S., Manthachitra, V., Moredee, R., Snidvongs, A., Yeemin, T., 1991, Temporal variation in a coral reef community at Pattaya Bay, Gulf of Thailand. Environ. Monit. Assess. 19, 295-307. CrossRef
Coles, S.L., Brown, B.E., 2003, Coral bleaching – Capacity for acclimatization and adaptation. Adv. Mar. Biol. 46, 183-223. CrossRef
Conand C., Chabanet P., Quod J-P., Bigot L., 1999, Guidelines: Coral reef monitoring in the South-West region of the Indian Ocean. Indian Ocean Commission and the Regional Environmental Programme, Mauritius.
Connell, J., 1978, Diversity in tropical rain forest and coral reefs. Science 199, 1302-1310. CrossRef
Connell J.H., 1997, Disturbance and recovery of coral assemblages. Proc. 8th Int. Coral Reef Symp., Panama 1, 9-22.
Connell, J.H., Hughes, T.P., Wallace, C.C., 1997, A 30-year study of coral abundance, recruitment, and disturbance at several scales in space and time. Ecol. Monogr. 67, 461-488. CrossRef
Cortés, J.N., Risk, M.J., 1985, A reef under siltation stress: Cahuita, Costa Rica. Bull. Mar. Sci. 36, 339-356.
Dale, V.H., Beyeler, S.C., 2001, Challenges in the development and use of ecological indicators. Ecol. Indic. 1, 3-10. CrossRef
Delesalle, B., Gattuso, J.P., Frankignoulle, M., 1993, Changes in the coral reef phytoplankton biomass primary production and composition induced by the passage of the cyclone Wasa near the island of Moorea, French Polynesia. J. Plankton Res. 15, 1413-1423. CrossRef
DeVantier, L.M., De'ath, G., Done, T.J., Turak, E., 1998, Ecological assessment of a complex natural system: A case study from the Great Barrier Reef. Ecol. Appl. 8, 480-496. CrossRef
Diamant, A., von Westernhagen, H., 2003, MARS: Biological indicators of natural and man-made changes in marine and coastal waters: Scientific coordinators' introduction. Helgol. Mar. Res. 57, 146-156. CrossRef
Dodge, R.E., Jickells, T.D., Knap, A.H., Boyd, S., Bak, R.P.M., 1984, Reef-building coral skeletons as chemical pollution (phosphorus) indicators. Mar. Pollut. Bull. 15, 178-187. CrossRef
Dollar, S.J., Tribble, G.W., 1993, Recurrent storm disturbance and recovery: A long-term study of coral communities in Hawaii. Coral Reefs 12, 223-233. CrossRef
Done, T.J., 1992a, Phase shifts in coral reef communities and their ecological significance. Hydrobiologia 247, 121-132. CrossRef
Done, T.J., 1992b, Constancy and change in some Great Barrier Reef coral communities: 1980-1990. Am. Zool. 32, 655-662. CrossRef
Done, T.J., 1995, Ecological criteria for evaluating coral reefs and their implications for managers and researchers. Coral Reefs 14, 183-192. CrossRef
Downs, C.A., Mueller, E., Phillips, S., Fauth, J.E., Woodley, C.M., 2000, A molecular biomarker system for assessing the health of coral (Monstastraea faveolata) during heat stress. Mar. Biotechnol. 2, 533-544. CrossRef
Drollet, J.H., Faucon, M., Maritorena, S., Martin, P.M.V., 1994, A survey of environmental physico-chemical parameters during a minor coral mass bleaching event in Tahiti in 1993. Aust. J. Mar. Freshwater Res. 45, 1149-1156. CrossRef
Eakin, C.M., Glynn, P.W., 1996, Low tidal exposure and reef mortalities in the eastern Pacific. Coral Reefs 15, 120.
Edinger, E.N., Limmon, G.V., Jompa, J., Widjatmoko, W., Heikoop, J.M., Risk, M.J., 2000, Normal coral growth rates on dying reefs: Are coral growth rates good indicators of reef health? Mar. Pollut. Bull. 40, 404-425. CrossRef
Edmunds, P.J., 2002, Long-term dynamics of coral reefs in St. John, US Virgin Islands. Coral Reefs 21, 357-367.
Edmunds, P.J., Bruno, J.F., 1996, The importance of sampling scale in ecology: Kilometer-wide variation in coral reef communities. Mar. Ecol. Prog. Ser. 143, 165-171. CrossRef
Endean R., Cameron A.M., 1990, Acanthaster planci populations outbreaks. In: Dubinsky Z. (Ed.), Ecosystems of the world 25, Coral reefs. Elsevier, Amsterdam, pp 469-492.
Fagerstrom, J.A., 1992, Reef flat community dynamics, Tiahura, Moorea Island, French Polynesia: I. Degradation 1971-1987. Proc. 7th Int. Coral Reef Symp. 2, 762-768.
Fagerstrom, J.A., Rougerie, F., 1994, 1994 coral bleaching event, Society Island, French Polynesia. Mar. Pollut. Bull. 29, 34-35. CrossRef
Fang, L.S., Chen, Y.W.J., Soong, K.Y., 1997, Methodology and measurement of ATP in coral. Bull. Mar. Sci. 41, 605-610.
Faure, G., 1989, Degradation of coral reefs at Moorea Island (French Polynesia) by Acanthaster planci. J. Coast. Res. 5, 295-305.
Fujioka, Y., 1999, Mass destruction of the hermatypic corals during a bleaching event in Ishigaki Islands, southwestern Japan. Galaxea 1, 41-50. CrossRef
Galzin, R., Marfin, J.P., Salvat, B., 1993, Long-term coral reef monitoring program: Heterogeneity of the Tiahura Barrier Reef (Moorea, French Polynesia). Galaxea 11, 73-91.
Galzin R., Morize E., Stein A., Conte E., 1989, Dégradations naturelles et/ou anthropiques en zones côtières intertropicales et répercussions possibles sur l'économie des pêches : le cas des récifs coralliens. Action Cordet, Rep. EPHE/Museum RA 32.
Ginsburg, R.N., Bak, R.P.M., Kiene, W.E., Gischler, E., Kosmynin, V., 1996, Rapid assessment of reef condition using coral vitality. Reef Encounter 19, 12-14.
Ginsburg, R.N., Gischler, E., Kiene, W.E., 2001, Partial mortality of massive reef-building corals: An index of patch reef condition, Florida Reef Tract. Bull. Mar. Sci. 69, 1149-1173.
Gleason, M.G., 1993, Effects of disturbance on coral communities: Bleaching in Moorea, French Polynesia. Coral Reefs 12, 193-201. CrossRef
Glynn, P.W., 1984, Widespread coral mortality and the 1982-1983 El Niño warming event. Environ. Conserv. 11, 133-146. CrossRef
Glynn, P.W., 1991, Coral reef bleaching in the 1980s and possible connections with global warming. Trends Ecol. Evol. 6, 175-179. CrossRef
Gomez, E.D., Alino, P.M., Yap, H.T., Licuanan, W.Y., 1994, A review of the status of Phillipine reefs. Mar. Pollut. Bull. 29, 62-68. CrossRef
Grigg, R.W., 1995, Coral reef in an urban embayment in Hawaii: A complex case history controlled by natural and anthropogenic stress. Coral Reefs 14, 253-266. CrossRef
Grigg R.W., Dollar S.J., 1990, Natural and anthropogenic disturbance on coral reef ecology. In: Dubinsky Z. (Ed.), Ecosystems of the world 25, Coral reefs. Elsevier, Amsterdam, pp. 439-452.
Guzman, H.M., Cortes, J., Glynn, P.W., Richmond, R.H., 1990, Coral mortality associated with dinoflagellate blooms in the eastern Pacific (Costa Rica and Panama). Mar. Ecol. Prog. Ser. 60, 299-303. CrossRef
Guzman, H.M., Burns, K.A., Jackson, J.B.C., 1994, Injury, regeneration and growth of Caribbean reef corals after a major oil spill in Panama. Mar. Ecol. Prog. Ser. 105, 231-241. CrossRef
Hanna, R.G., Muir, G.L., 1990, Red Sea corals as biomonitors of trace metal pollution. Environ. Monogr. Assess. 14, 211-222. CrossRef
Hallock, P., Barnes, K., Fisher, E.M., 2004, Coral-reef risk assessment from satellites to molecules: A multi-scale approach to environmental monitoring and risk assessment of coral reefs. Environ. Micropaleontol. Microbiol. Meiobenthol. 1, 11-39.
Harmelin-Vivien, M.L., 1985, Tikehau Atoll, Tuamotu Archipelago. Proc. 5th Int. Coral Reef Congr. 1, 211-268.
Harmelin-Vivien, M.L., 1994, The effects of storms and cyclones on coral reefs: A review. J. Coast. Res. 12, 211-231.
Harmelin-Vivien, M.L., Laboute, P., 1986, Catastrophic impact of hurricanes on outer reef slope in the Tuamotu (French Polynesia). Coral Reefs 5, 55-62. CrossRef
Harriott, V.J., 1993, Coral lipids and environmental stress. Environ. Monit. Assess. 25, 131-139. CrossRef
Harvell, C.D., Kim, K., Burkholder, J.M., Colwell, R.R., Epstein, P.R., Grimes, D.J., Hofmann, E.E., Lipp, E.K., Osterhaus, A.D.M.E., Overstreet, R.M., Porter, J.W., Smith, G.W., Vasta, G.R., 1999, Emerging marine diseases – Climate links and anthropogenic factors. Science 285, 1505-1510. CrossRef
Heikoop, J.M., Risk, M.J., Lazier, A.V., Edinger, E.N., Jompa, J., Limmon, G.V., Dunn, J.J., Browne, D.R., Schwarcz, H.P., 2000, Nitrogen-15 signals of anthropogenic nutrient loading in reef corals. Mar. Pollut. Bull. 40, 628-636. CrossRef
Highsmith, R., Riggs, A., D'Antonio, C., 1980, Survival of hurricane-generated coral fragments and a disturbance model of reef calcification/growth rates. Oecologia 46, 322-329. CrossRef
Hodgson, G., 1999, A global assessment of human effects on coral reefs. Mar. Pollut. Bull. 38, 345-355. CrossRef
Hodgson, G., 2000, Coral reef monitoring and management using Reef Check. Integrated Coast. Zone Manage. 1, 169-179.
Hoegh-Guldberg, O., 1999, Climate change, coral bleaching and the future of the world's coral reefs. Mar. Freshwater Res. 50, 839-866. CrossRef
Hoegh-Guldberg, O., 2002, The future of coral reefs: Integrating climate model projections and the recent behavior of corals and their dinoflagellates. Proc. 9th Int. Coral Reef Symp. 2, 1105-1110.
Hoegh-Guldberg, O., Salvat, B., 1995, Periodic mass-bleaching and elevated sea temperatures: Bleaching of outer reef slope communities in Moorea, French Polynesia. Mar. Ecol. Prog. Ser. 121, 181-190. CrossRef
Holmes, K.E., 1997, Eutrophication and its effect on bioeroding sponge communities. Proc. 8th Int. Coral Reef Symp. 2, 1411-1416.
Hughes, T.P., 1989, Community structure and diversity of coral reefs: The role of history. Ecology 70, 275-279. CrossRef
Hughes, T.P., 1994, Catastrophes, phase shifts and large scale degradation of a Caribbean coral reef. Science 265, 1547-1551. CrossRef
Hughes, T.P., Connell, J.H., 1999, Multiple stressors on coral reefs: A long-term perspective. Limnol. Oceanogr. 44, 932-940. CrossRef
Hughes, 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., Lough, J.M., Marshall, P., Nyström, M., Palumbi, S.R., Pandolfi, J.M., Rosen, B., Roughgarden, J., 2003, Climate change, human impacts, and the resilience of coral reefs. Science 301, 929-933. CrossRef
Hunte, W., Wittemberg, M., 1992, Effects of eutrophication and sedimentation on juvenile corals. II Settlement. Mar. Biol. 114, 625-631. CrossRef
Hutchings, P., Payri, C., Gabrié, C., 1994, The current status of coral reef management in French Polynesia. Mar. Pollut. Bull. 29, 26-33. CrossRef
Jameson, S.C., Erdmann, M.V., Karr, J.R., Potts, K.W., 2001, Charting a course toward diagnostic monitoring: A continuing review of coral reef attributes and a research strategy for creating coral reef indexes of biotic integrity. Bull. Mar. Sci. 69, 701-744.
Jokiel, P.L., Brown, E.K., Friedlander, A., Rodgers, S.K., Smith, W.R., 2004, Hawai'i Coral Reef Assessment and Monitoring Program: Spatial patterns and temporal dynamics in reef coral communities. Pac. Sci. 58, 159-174. CrossRef
Jones, R.J., 1997, Zooxanthellae loss as a bioassay for assessing stress in corals. Mar. Ecol. Progr. Ser. 149, 163-171. CrossRef
Karlson, R.H., Hurd, L.E., 1993, Disturbances, coral reef communities, and changing ecological paradigms. Coral Reefs 12, 117-125. CrossRef
Kaufman, L.S., 1983, Effects of Hurricane Allen on reef fish assemblages near Discovery Bay, Jamaica. Coral Reefs 2, 43-47. CrossRef
Kendall, J.J., Powell, E.N., Connor, S.J., Bright, T.J., Zastrow, C.E., 1985, Effects of turbidity on calcification rates, protein concentration and the free amino acid pool of the coral Acropora cervicornis. Mar. Biol. 87, 33-46. CrossRef
Kinzi, R.A. III, Takayama, M., Santos, S.C., Coffroth, M.A., 2001, The adaptive bleaching hypothesis: Experimental tests of critical assumptions. Biol. Bull. 200, 51-58. CrossRef
Kramer, P.A., Kramer, P.R., 2002, Transient and lethal effects of the 1998 coral bleaching event on the Mesoamerican reef system. Proc. 9th Int. Coral Reef Symp. 2, 1175-1180.
Laboute, P., 1985, Evaluation des dégâts causés par les passages des cyclones de 1982-1983 en Polynésie française sur les pentes etxernes des atolls de Tikehau et de Takapoto (Archipel des Tuamotu). Proc. 5th Int. Coral Reef Congr. 3, 323-329.
Ledesma, M.C., Mejia, M., 2002, Coral reef monitoring in Tubbataha Reef National Marine Park, Sulu Sea, Philippines. Proc. 9th Int. Coral Reef Symp. 2, 879-881.
Lessios, H.A., Robertson, D.R., Cubit, J.D., 1984, Spread of Diadema mass mortality through the Caribbean? Science 226, 335-337. CrossRef
Lewis, A.R., 1998, Effects of experimental coral disturbance on the population dynamics of fishes on large patch reefs. J. Exp. Mar. Biol. Ecol. 230, 91-110. CrossRef
Lindahl, U.F.L., Öhman, M.C., Shelten, C.K., 2001, The 1997/1998 Mass Mortality of Corals: Effects on Fish Communities on a Tanzanian Coral Reef. Mar. Pollut. Bull. 42, 127-131. CrossRef
McClanahan, T.R., 2000, Bleaching damage and recovery potential of Maldivian coral reefs. Mar. Pollut. Bull. 40, 587-597. CrossRef
Meesters, E.H., Bak, R.P.M., 1993, Effects of coral bleaching on tissue regeneration potential and colony survival. Mar. Ecol. Prog. Ser. 96, 189-198. CrossRef
Meesters, E.H., Hilterman, M., Kardinaal, E., Keetman, M., de Vries, M., Bak, R.P.M., 2001, Colony-size frequency distributions of scleractinian coral populations: Spatial and interspecific variation. Mar. Ecol. Prog. Ser. 209, 43-54. CrossRef
Meesters, E.H., Nieuwland, G., Duineveld, G.C.A., Kok, A., Bak, R.P.M., 2002, RNA/DNA ratios of scleractinian corals suggest acclimatisation/adaptation in relation to light gradients and turbidity regimes. Mar. Ecol. Prog. Ser. 227, 233-239. CrossRef
Mendes, J.M., Risk, M.J., Schwarcz, H.P., Woodley, J.D., 1997, Stable isotopes of nitrogen as measures of marine pollution: A preliminary assay of coral tissue from Jamaica. Proc. 8th Int. Coral Reef Symp. 2, 1869-1872.
Miller, M.W., Barimo, J., 2002, Assessment of juvenile coral populations at two reef restoration sites in the Florida Keys National Marine Sanctuary: Indicators of success? Bull. Mar. Sci. 69, 395-405.
Miller, S.L., Swanson, D.W., Chiappone, M., 2002, Multiple spatial scale assessment of coral reef and hard-bottom community structure in the Florida Keys National Marine Sanctuary. Proc. 9th Int. Coral Reef Symp. 1, 69-74.
Moran, P.J., 1986, The Acanthaster phenomenon. Oceanogr. Mar. Biol. Ann. Rev. 24, 379-480.
Mumby, P.J., Hedley, J.D., Chisholm, J.R.M., Clark, C.D., Ripley, H., Jaubert, J., 2004, The cover of living and dead corals from airborne remote sensing. Coral Reefs 23, 171-183. CrossRef
Mumby, P.J., Chisholm, J.R.M., Edwards, A.J., Andréfouët, S., Jaubert, J., 2001a, Cloudy weather may have saved Society Island reef corals during the 1998 ENSO event. Mar. Ecol. Prog. Ser. 222, 209-216. CrossRef
Mumby, P.J., Chisholm, J.R.M., Edwards, A.J., Clark, C.D., Roark, E.B., Andréfouët, S., Jaubert, J., 2001b, Unprecedented bleaching-induced mortality in Porites spp. at Rangiroa Atoll, French Polynesia. Mar. Biol. 139, 183-189.
Naim, O., Progent, W., Boucher, N., 2001, Utilisation de la croissance de transplants du scléractiniaires hermatypique Acropora muricata (Linnée, 1758) comme bioindicateur (île de La Réunion, océan Indien). Rev. Ecol. 56, 201-211.
Niemi, G.J., McDonald, M.E., 2004, Application of ecological indicators. Ann. Rev. Ecol. Evol. Syst. 35, 89-111. CrossRef
Ninio, R., Meekan, M.G., 2002, Spatial patterns in benthic communities and the dynamics of a mosaic ecosystem on the Great Barrier Reef, Australia. Coral Reefs 21, 95-103. CrossRef
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. CrossRef
Nugues, M.M., 2002, Impact of a coral disease outbreak on coral communities in St. Lucia: What and how much has been lost? Mar. Ecol. Prog. Ser. 229, 61-71.
Obura, D.O., 2001, Can differential bleaching and mortality among coral species offer useful indicators for assessment and management of reefs under stress? Bull. Mar. Sci. 69, 421-442.
Pandolfi, J.M., Bradbury, R.H., Sala, E., Hughes, T.H., Bjorndal, K.A., Cooke, R.G., McArdle, D., McClenachan, L., Newman, M.J.H., Paredes, G., Warner, R.R., Jackson, J.B.C., 2003, Global trajectories of the long-term decline of coral reef ecosystems. Science 301, 955-958. CrossRef
Pearson, R.G., 1981, Recovery and recolonization of coral reefs. Mar. Ecol. Prog. Ser. 4, 105-122. CrossRef
Poli, G., Salvat, B., 1976, Étude bionomique d'un lagon d'atoll totalement fermé: Taiaro. Cah. Pac. 19, 227-251.
Porter, J.W., Dustan, P., Jaap, W.C., Patterson, K.L., Kosmynin, V., Meier, O.W., Patterson, M.E., Parsons, M., 2001, Patterns of spread of coral disease in the Florida Keys. Hydrobiologia 460, 1-24. CrossRef
Randall, R.H., Eldredge, L.G., 1977, Effects of typhoon Pamela on the coral reefs of Guam. Proc. 3rd Int. Coral Reef Symp. 2, 526-531.
Ridgway, T., Hoegh-Guldberg, O., 2002, Reef recovery in disturbed coral reef ecosystems. Proc. 9th Int. Coral Reef Symp. 2, 1117-1121.
Risk M.J., Dunn J.J., Allison W.P., Horrill C., 1994, Reef monitoring in Maldives and Zanzibar: Low-tech and high-tech science. In: Ginsburg R.N. (Ed.), Proc. Colloq. Global Aspects of Coral Reefs: Health, hazards and history. Rosenstiel School of Marine and Atmospheric Science, University of Miami, pp. 66-72.
Rogers, C.S., 1993, Cyclones and coral reefs: The intermediate disturbance hypothesis revisited. Coral Reefs 12, 127-137. CrossRef
Rossi, S., Snyder, M.J., 2001, Competition for space among sessile marine invertebrates: Changes in HSP70 expression in two Pacific cnidarians. Biol. Bull. 201, 385-393. CrossRef
Rougerie, F, Wauthy, B., 1983, Anomalies de l'hydroclimat et cyclogenèse en Polynésie en 1982 et 1983. Met. Mar. 121, 27-40.
Rowan, R., Knowlton, N., Baker, A., Jara, A., 1997, Landscape ecology of algal symbionts creates variation in episodes of coral bleaching. Nature 388, 265-269. CrossRef
Salvat, B., 1992, Blanchissement et mortalité des scléractiniaires sur les récifs de Moorea (archipel de la Société) en 1991. C.R. Acad. Sci. Paris 314, 105-111.
Salvat B., 2000, Status of South East and Central Pacific Coral Reefs “Polynesia Mana Node”: Cook Islands, French Polynesia, Kiribati, Niue, Tokelau, Tonga, Wallis and Futuna. In: Wilkinson, C. (Ed.), Status of Coral Reefs of the World 2000. Global Coral Reef Monitoring Network, Australian Institute of Marine Science, Townsville, pp. 181-198.
Salvat B., 2002, Status of Southeast and Central Coral Reefs “Polynesia Mana Node” 2002: Cook Islands, French Polynesia, Kiribati, Niue, Tokelau, Tonga, Wallis and Futuna. In: Wilkinson C. (Ed.), Status of Coral Reefs of the World 2002. Global Coral Reef Monitoring Network, Australian Institute of Marine Science, Townsville, pp. 203-215.
Salvat, B., Aubanel, A., 2002, La gestion des récifs coralliens de Polynésie francaise. Rev. Ecol. 57, 193-251.
Salvat B., Hutchings P., Aubanel A., Tatarata M., Dauphin C., 2001, French Polynesia Coral Reefs Status and Resources Report. In: Salvat B. (Ed.), Status of Coral Reefs 2000 in Southeast and Central Pacific – Polynesia Mana Network. Fondation Naturalia Polynesia, Papeete, Tahiti, pp. 31-60.
Salvat, B., Chancerelle, Y., Schrimm, M., Morancy, R., Porcher, M., Aubanel, A., 2002, Restauration d'une zone corallienne dégradée et implantation d'un jardin corallien à Bora Bora, Polynésie française. Rev. Ecol. (Terre Vie) suppl. 9, 81-96.
Salvat, B., Vergonzanne, G., Galzin, R., Richard, G., Chevalier, J.P., Ricard, M., Renaud-Mornant, J., 1979, Conséquences écologiques des activités d'une zone d'extraction de sable corallien dans le lagon de Moorea (île de la Société, Polynésie française). Cah. Indo-Pacif. 1, 83-126.
Santavy, D.L., Peters, E.C., 1997, Microbial pests: Coral disease in the western Atlantic. Proc. 8th Int. Coral Reef Symp. 1, 607-612.
Santavy, D.L., Mueller, E., Peters, E.C., MacLaughlin, L., Porter, J.W., Patterson, K.L., Campbell, J., 2001, Quantitative assessment of coral diseases in the Florida Keys: Strategy and methodology. Hydrobiologia 460, 39-52. CrossRef
Scherrer B., 1984, Biostatistiques. Morin G., Chicoutimi, Québec.
Schönberg, C.H.L., 2001, Small-scale distribution of great barrier reef bioeroding sponges in shallow water. Ophelia 55, 39-54. CrossRef
Schönberg, C.H.L., Wilkinson, C.R., 2001, Induced colonization of corals by a clionid bioeroding sponge. Coral Reefs 20, 69-76.
Sharp, V.A., Brown, B.E., Miller, D., 1997, Heat Shock Protein (HSP 70) expression in the tropical reef coral Goniopora djiboutiensis. J. Therm. Biol. 22, 11-19. CrossRef
Shulman, M.J., Robertson, D.R., 1996, Changes in the coral reefs of San Blas, Caribbean Panama: 1983-1990. Coral Reefs 15, 231-236. CrossRef
Sousa, W.P., 1984, The role of disturbance in natural communities. Ann. Rev. Ecol. Syst. 15, 353-391. CrossRef
Steven, A.D.L., Broadbent, A.D., 1997, Growth and metabolic responses of Acropora palifera to long term nutrient enrichment. Proc. 8th Int. Coral Reef Symp. 1, 867-872.
Sugihara, K., Iryu, Y., Nakamori, T., 1999, Coral bleaching, geological ranges, and adaptation to high sea surface temperatures. Galaxea 1, 89-95. CrossRef
Tom, M., Douek, J., Yankelevich, I., Bosch, T.C.G., Rinkevich, B., 1999, Molecular characterization of the first Heat Shock Protein 70 from a reef coral. Biochem. Biophys. Res. Co. 262, 103-108. CrossRef
Van Woesik, R., 1994, Contemporary disturbances to coral communities of the Great Barrier Reef. J. Coast. Res. 12, 233-252.
Ward, S., Harrison, P., 2000, Changes in gametogenesis and fecundity of acroporid corals that were exposed to elevated nitrogen and phosphorus during the ENCORE experiment. J. Exp. Mar. Biol. Ecol. 246, 179-221. CrossRef
Wilkinson C., 1998, Status of coral reefs of the world: 1998. Townsville, Australia, Australian Institute of Marine Science and the Global Coral Reef Monitoring Network.
Wilkinson, C.R., Lindén, O., Cesar, H., Hodgson, G., Rubens, J., Strong, A.E., 1999, Ecological and socio-economic impacts of 1998 coral mortality in the Indian Ocean: An ENSO impact and a warning of future change? Ambio 28, 188-196.
Williams, D.Mc.B., 1986, Temporal variation in the structure of reef slope fish communities (central Great Barrier Reef): Short-term effects of Acanthaster planci infestation. Mar. Ecol. Prog. Ser. 28, 157-164. CrossRef
Williams, E.H., Bunkley-Williams, L., 1990, The worldwide coral reef bleaching cycle and related sources of coral mortality. Atoll Res. Bull. 335, 1-71. CrossRef
Witman, J.D., 1992, Physical disturbance and community structure of exposed and protected reefs: A case study from St. John, U.S. Virgin Islands. Am. Zool. 32, 641-654. CrossRef
Woodley, C.M., Downs, C.A., Fauth, J.E., Mueller, E., Halas, J.C., Bemiss, J., Ben-Haim, Y., Rosenberg, E., 2002, A novel diagnostic system to assess the physiological status of corals. Proc. 9th Int. Coral Reef Symp. 2, 1267-1272.
Yamano, H., Tamura, M., 2002, Can satellite sensors detect coral reef bleaching? A feasability study using radiative transfer models in air and water. Proc. 9th Int. Coral Reef Symp. 2, 1025-1031.
Yamano, H., Tamura, M., Kunii, Y., Hidaka, M., 2002, Hyperspectral remote sensing and radiative transfer simulation as a tool for monitoring coral reef health. Mar. Tech. Sci. J. 36, 4-13. CrossRef
Zea, S., Geister, J., Garzon-Ferreira, J., Diaz, J.M., 1998, Biotic changes in the reef complex of San Andres Island (southwestern Caribbean Sea, Colombia) occurring over nearly three decades. Atoll Res. Bull. 456, 1-30. CrossRef