Marine and Freshwater Research Marine and Freshwater Research Society
Advances in the aquatic sciences
RESEARCH ARTICLE

Susceptibility of coral assemblages to successive bleaching events at Moorea, French Polynesia

A. G. Carroll A C , P. L. Harrison A and M. Adjeroud B

A Marine Ecology Research Centre, School of Environment, Science and Engineering, Southern Cross University, PO Box 157, Lismore, NSW 2480, Australia.

B Institut de Recherche pour le Développement, UMR 9220 ENTROPIE & Laboratoire d’Excellence ‘CORAIL’, UPVD 52 avenue Paul Alduy, 66860 Perpignan, France.

C Corresponding author. Email: acarroll.marine@gmail.com

Marine and Freshwater Research - http://dx.doi.org/10.1071/MF15134
Submitted: 8 April 2015  Accepted: 8 April 2016   Published online: 7 July 2016

Abstract

In 2002, bleaching was reported throughout many Indo-Pacific coral-reef regions, including French Polynesia. Bleaching occurred again in French Polynesia in 2003, providing an opportunity to compare the effects of successive bleaching events on coral susceptibility. During 2002 and 2003, underwater video surveys were completed in stations at four depths (lagoon: 0–2, 2–4 m; outer reef slope: 6–8, 12–14 m) at two locations on the northern and north-western coast of Moorea (Society Archipelago) to compare the cover of healthy-appearing, the cover of partially bleached and the cover of fully bleached coral. Bleaching patterns were genus specific and differences in susceptibility among major genera were generally consistent between 2002 and 2003, with Acropora showing the greatest susceptibility. Some genera exhibited substantial spatial variability in bleaching susceptibility between years (e.g. Pocillopora, Montipora); however, this variability was significant only for fully bleached and partially bleached Acropora. Multivariate analyses showed that spatial patterns in the proportion of healthy-appearing coral were similar over time within the assemblages, whereas the cover of partially bleached and the cover of fully bleached coral were more variable among depths and locations. This variability has important implications for assessing changes to coral community structure over time and for estimating coral-reef resistance and resilience to future bleaching disturbance.

Additional keywords: community change, coral bleaching, disturbance, scleractinian corals, spatial patterns, thermal stress.


References

Adjeroud, M., Chancerelle, Y., Schrimm, M., Perez, T., Lecchini, D., Galzin, R., and Salvat, B. (2005). Detecting the effects of natural disturbances on coral assemblages in French Polynesia: a decade survey at multiple scales. Aquatic Living Resources 18, 111–123.
Detecting the effects of natural disturbances on coral assemblages in French Polynesia: a decade survey at multiple scales.CrossRef | open url image1

Adjeroud, M., Penin, L., and Carroll, A. (2007). Spatio-temporal heterogeneity in coral recruitment around Moorea, French Polynesia: implications for population maintenance. Journal of Experimental Marine Biology and Ecology 341, 204–218.
Spatio-temporal heterogeneity in coral recruitment around Moorea, French Polynesia: implications for population maintenance.CrossRef | open url image1

Adjeroud, M., Michonneau, F., Edmunds, P. J., Chancerelle, Y., Penin, L., Vidal-Dupiol, J., Salvat, B., and Galzin, R. (2009). Recurrent disturbances, recovery trajectories, and resilience of coral assemblages on a south central Pacific reef. Coral Reefs 28, 775–780.
Recurrent disturbances, recovery trajectories, and resilience of coral assemblages on a south central Pacific reef.CrossRef | open url image1

Anderson, M. J. (2001). A new method for non-parametric multivariate analysis of variance. Austral Ecology 26, 32–46. open url image1

Anderson, M. J. (2005). ‘PERMANOVA: a FORTRAN computer program for permutational multivariate analysis of variance.’ (Department of Statistics, University of Auckland: Auckland.)

Aronson, R., Precht, W., Toscano, M., and Koltes, K. (2002). The 1998 bleaching event and its aftermath on a coral reef in Belize. Marine Biology 141, 435–447.
The 1998 bleaching event and its aftermath on a coral reef in Belize.CrossRef | open url image1

Baird, A. H., and Marshall, P. A. (2002). Mortality, growth and reproduction in scleractinian coral following bleaching on the Great Barrier Reef. Marine Ecology Progress Series 237, 133–141.
Mortality, growth and reproduction in scleractinian coral following bleaching on the Great Barrier Reef.CrossRef | open url image1

Baker, A. C. (2003). Flexibility and specificity in coral-algal symbiosis: diversity, ecology, and biogeography of Symbiodinium. Annual Review of Ecology Evolution and Systematics 34, 661–689.
Flexibility and specificity in coral-algal symbiosis: diversity, ecology, and biogeography of Symbiodinium.CrossRef | open url image1

Baker, A. C., Starger, C. J., McClanahan, T. R., and Glynn, P. W. (2004). Coral reefs: corals’ adaptive response to climate change. Nature 430, 741.
Coral reefs: corals’ adaptive response to climate change.CrossRef | 1:CAS:528:DC%2BD2cXmsVGlsr8%3D&md5=e65a4ef3936e8953318e362a2ace8131CAS | 15306799PubMed | open url image1

Baker, A. C., Glynn, P. W., and 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, 435–471.
Climate change and coral reef bleaching: an ecological assessment of long-term impacts, recovery trends and future outlook.CrossRef | open url image1

Berkelmans, R., and Oliver, J. K. (1999). Large-scale bleaching of corals on the Great Barrier Reef. Coral Reefs 18, 55–60.
Large-scale bleaching of corals on the Great Barrier Reef.CrossRef | open url image1

Berkelmans, R., and van Oppen, M. J. H. (2006). The role of zooxanthellae in the thermal tolerance of corals: a ‘nugget of hope’ for coral reefs in an era of climate change. Proceedings. Biological Sciences 273, 2305–2312.
The role of zooxanthellae in the thermal tolerance of corals: a ‘nugget of hope’ for coral reefs in an era of climate change.CrossRef | open url image1

Berkelmans, R., and Willis, B. L. (1999). Seasonal and local spatial patterns in the upper thermal limits of corals on the inshore central Great Barrier Reef. Coral Reefs 18, 219–228.
Seasonal and local spatial patterns in the upper thermal limits of corals on the inshore central Great Barrier Reef.CrossRef | open url image1

Berkelmans, R., De’ath, G., Kininmonth, S., and 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.
A comparison of the 1998 and 2002 coral bleaching events on the Great Barrier Reef: spatial correlation, patterns, and predictions.CrossRef | open url image1

Berumen, M. L., and 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, 647–653.
Recovery without resilience: persistent disturbance and long-term shifts in the structure of fish and coral communities at Tiahura Reef, Moorea.CrossRef | open url image1

Brown, B. E. (1997). Coral bleaching: causes and consequences. Coral Reefs 16, S129–S138.
Coral bleaching: causes and consequences.CrossRef | open url image1

Brown, B. E., Dunne, R. P., Scoffin, T. P., and Le Tissier, M. D. A. (1994). Solar damage in intertidal corals. Marine Ecology Progress Series 105, 219–230.
Solar damage in intertidal corals.CrossRef | open url image1

Brown, B. E., Dunne, R. P., Goodson, M. S., and Douglas, A. E. (2000). Marine ecology: bleaching patterns in reef corals. Nature 404, 142–143.
Marine ecology: bleaching patterns in reef corals.CrossRef | 1:CAS:528:DC%2BD3cXhvFKgsLw%3D&md5=47e3f85e54f14ec0902b31460f2aed9dCAS | 10724156PubMed | open url image1

Brown, B. E., Dunne, R. P., Goodson, M. S., and Douglas, A. E. (2002). Experience shapes the susceptibility of a reef coral to bleaching. Coral Reefs 21, 119–126. open url image1

Carroll, A. G., Harrison, P. L., and Adjeroud, M. (2006). Sexual reproduction of Acropora reef corals at Moorea, French Polynesia. Coral Reefs 25, 93–97.
Sexual reproduction of Acropora reef corals at Moorea, French Polynesia.CrossRef | open url image1

Clarke, K. R. (1993). Non-parametric multivariate analysis of changes in community structure. Australian Journal of Ecology 18, 117–143.
Non-parametric multivariate analysis of changes in community structure.CrossRef | open url image1

Clarke, K. R., and Gorley, R. N. (2001). ‘PRIMER v5: User Annual/tutorial.’ (PRIMER-E: Plymouth, UK.)

Clarke, K. R., and Warwick, R. M. (2001). ‘Changes in Marine Communities: an Approach to Statistical Analysis and Interpretation’, 2nd edn. (Plymouth Marine Laboratory: Plymouth, UK.)

Connell, J. H., Hughes, T. P., and Wallace, C. C. (1997). A 30-year study of coral abundance, recruitment, and disturbance at several scales in space and time. Ecological Monographs 67, 461–488.
A 30-year study of coral abundance, recruitment, and disturbance at several scales in space and time.CrossRef | open url image1

Drollet, J. H., Faucon, M., and Martin, P. M. V. (1995). Elevated sea-water temperature and solar UV-B flux associated with two successive coral mass bleaching events in Tahiti. Australian Journal of Marine and Freshwater Research 46, 1153–1157.
Elevated sea-water temperature and solar UV-B flux associated with two successive coral mass bleaching events in Tahiti.CrossRef | open url image1

Dunne, R. P., and 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, 201–210. open url image1

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, 137–142.
Evidence that reef-wide patterns of coral bleaching may be the result of the distribution of bleaching-susceptible clones.CrossRef | open url image1

Faure, G. (1989). Degradation of coral reefs at Moorea Island (French Polynesia) by Acanthaster planci. Journal of Coastal Research 5, 295–305. open url image1

Fitt, W. K., and Warner, M. E. (1995). Bleaching patterns of four species of Caribbean Reef corals. The Biological Bulletin 189, 298–307.
Bleaching patterns of four species of Caribbean Reef corals.CrossRef | open url image1

Fitt, W. K., Spero, H. J., Halas, J., White, M. W., and Porter, J. W. (1993). Recovery of the coral Montastrea annularis in the Florida Keys after the 1987 Caribbean ‘bleaching event’. Coral Reefs 12, 57–64.
Recovery of the coral Montastrea annularis in the Florida Keys after the 1987 Caribbean ‘bleaching event’.CrossRef | open url image1

Fitt, W. K., McFarland, F. K., Warner, M. E., and Chilcoat, G. C. (2000). Seasonal patterns of tissue biomass and densities of symbiotic dinoflagellates in reef corals and relation to coral bleaching. Limnology and Oceanography 45, 677–685.
Seasonal patterns of tissue biomass and densities of symbiotic dinoflagellates in reef corals and relation to coral bleaching.CrossRef | 1:CAS:528:DC%2BD3cXjsV2ltbg%3D&md5=90b8eab93f379d18d762c698585c915fCAS | open url image1

Frieler, K., Meinshausen, M., Golly, A., Mengel, M., Lebek, K., Donner, S. D., and Hoegh-Guldberg, O. (2013). Limiting global warming to 2°C is unlikely to save most coral reefs. Nature Climate Change 3, 165–170.
Limiting global warming to 2°C is unlikely to save most coral reefs.CrossRef | open url image1

Furby, K. A., Bouwmeester, J., and Berumen, M. L. (2013). Susceptibility of central Red Sea corals during a major bleaching event. Coral Reefs 32, 505–513.
Susceptibility of central Red Sea corals during a major bleaching event.CrossRef | open url image1

Gleason, M. G. (1993). Effects of disturbance on coral communities: bleaching in Moorea, French Polynesia. Coral Reefs 12, 193–201.
Effects of disturbance on coral communities: bleaching in Moorea, French Polynesia.CrossRef | open url image1

Glynn, P. W. (1993). Coral reef bleaching: ecological perspectives. Coral Reefs 12, 1–17.
Coral reef bleaching: ecological perspectives.CrossRef | open url image1

Glynn, P. W., and D’Croz, L. D. (1990). Experimental evidence for high temperature stress as the cause of El Nino-coincident coral mortality. Coral Reefs 8, 181–191.
Experimental evidence for high temperature stress as the cause of El Nino-coincident coral mortality.CrossRef | open url image1

Glynn, P. W., Maté, J. L., Baker, A. C., and Calderón, M. O. (2001). Coral bleaching and mortality in Panamá and Ecuador during the 1997–1998 El Niño–Southern Oscillation event: spatial/temporal patterns and comparisons with the 1982–1983 event. Bulletin of Marine Science 69, 79–101. open url image1

Golbuu, Y., Victor, S., Penland, L., Idip, D., Emaurois, C., Okaji, K., Yukihira, H., Iwase, A., and van Woesik, R. (2007). Palau’s coral reefs show differential habitat recovery following the 1998-bleaching event. Coral Reefs 26, 319–332.
Palau’s coral reefs show differential habitat recovery following the 1998-bleaching event.CrossRef | open url image1

Goreau, T. J., and Hayes, R. (1994). Coral bleaching and ocean ‘hot spots’. Ambio 23, 176–181. open url image1

Grigg, R. W. (1995). Coral reefs in an urban embayment in Hawaii: a complex case history controlled by natural and anthropogenic stress. Coral Reefs 14, 253–266.
Coral reefs in an urban embayment in Hawaii: a complex case history controlled by natural and anthropogenic stress.CrossRef | open url image1

Grottoli, A. G., Warner, M. E., Levas, S. J., Aschaffenburg, M. D., Schoepf, V., McGinley, M., Baumann, J., and Matsui, Y. (2014). The cumulative impact of annual coral bleaching can turn some coral species winners into losers. Global Change Biology 20, 3823–3833.
The cumulative impact of annual coral bleaching can turn some coral species winners into losers.CrossRef | 25044878PubMed | open url image1

Guest, J. R., Baird, A. H., Maynard, J. A., Muttaqin, E., Edwards, A. J., Campbell, S. J., Yewdall, K., Affendi, Y. A., and Chou, L. M. (2012). Contrasting patterns of coral bleaching susceptibility in 2010 suggest an adaptive response to thermal stress. PLoS One 7, e33353.
Contrasting patterns of coral bleaching susceptibility in 2010 suggest an adaptive response to thermal stress.CrossRef | 1:CAS:528:DC%2BC38XksVGitbw%3D&md5=5991fbc00dfa66c21e758e4041547099CAS | 22428027PubMed | open url image1

Hardman, E. R., Sabrina Meunier, M., Turner, J. R., Lynch, T. L., Taylor, M., and Klaus, R. (2004). The extent of coral bleaching in Rodrigues, 2002. Journal of Natural History 38, 3077–3089.
The extent of coral bleaching in Rodrigues, 2002.CrossRef | open url image1

Harriott, V. J., Harrison, P. L., and Banks, S. A. (1995). The coral communities of Lord Howe Island. Australian Journal of Marine and Freshwater Research 46, 457–465.
The coral communities of Lord Howe Island.CrossRef | open url image1

Harrison, P. L., and Booth, D. J. (2007). Coral reefs: naturally dynamic and increasingly disturbed ecosystems. In ‘Marine Ecology’. (Eds S. D. Connell and B. M. Gillanders.) pp. 316–377. (Oxford University Press: Melbourne.)

Hill, R., Frankart, C., and Ralph, P. J. (2005). Impact of bleaching conditions on the components of non-photochemical quenching in the zooxanthellae of a coral. Journal of Experimental Marine Biology and Ecology 322, 83–92.
Impact of bleaching conditions on the components of non-photochemical quenching in the zooxanthellae of a coral.CrossRef | 1:CAS:528:DC%2BD2MXmsVOrtr4%3D&md5=88e579e906d2834730e0097badfec2c3CAS | open url image1

Hoegh-Guldberg, O. (1999). Climate change, coral bleaching and the future of the world’s coral reefs. Australian Journal of Marine and Freshwater Research 50, 839–866.
Climate change, coral bleaching and the future of the world’s coral reefs.CrossRef | open url image1

Hoegh-Guldberg, O., and Salvat, B. (1995). Periodic mass bleaching and elevated sea temperatures: bleaching of outer reef slope communities in Moorea, French Polynesia. Marine Ecology Progress Series 121, 181–190.
Periodic mass bleaching and elevated sea temperatures: bleaching of outer reef slope communities in Moorea, French Polynesia.CrossRef | open url image1

Hoegh-Guldberg, O., and Smith, G. J. (1989). The effect of sudden changes in temperature, light and salinity on the population density and export of zooxanthellae from the reef corals Stylophora pistillata and Seriatopora hystrix Dana. Journal of Experimental Marine Biology and Ecology 129, 279–303.
The effect of sudden changes in temperature, light and salinity on the population density and export of zooxanthellae from the reef corals Stylophora pistillata and Seriatopora hystrix Dana.CrossRef | open url image1

Hoegh-Guldberg, O., Mumby, P. J., Hooten, A. J., Steneck, R. S., Greenfield, P., Gomez, E., Harvell, C. D., Sale, P. F., Edwards, A. J., Caldeira, K., Knowlton, N., Eakin, C. M., Iglesias-Prieto, R., Muthiga, N., Bradbury, R. H., Dubi, A., and Hatziolos, M. E. (2007). Coral reefs under rapid climate change and ocean acidification. Science 318, 1737–1742.
Coral reefs under rapid climate change and ocean acidification.CrossRef | 1:CAS:528:DC%2BD2sXhsVWhu7fN&md5=816b71ba5058ceb964513e2fc635e0cdCAS | 18079392PubMed | open url image1

Hughes, T. P. (1994). Catastrophes, phase shifts and large-scale degradation of a Caribbean coral reef. Science 265, 1547–1551.
Catastrophes, phase shifts and large-scale degradation of a Caribbean coral reef.CrossRef | 1:STN:280:DC%2BC3cvjs1OjsA%3D%3D&md5=cfcf13a4fcbfda5bc8b768c546aabb31CAS | 17801530PubMed | open url image1

Hughes, T. P. (1996). Demographic approaches to community dynamics: a coral reef example. Ecology 77, 2256–2260.
Demographic approaches to community dynamics: a coral reef example.CrossRef | open url image1

Hughes, T. P., and Connell, J. H. (1999). Multiple stressors on coral reef: a long-term perspective. Limnology and Oceanography 44, 932–940.
Multiple stressors on coral reef: a long-term perspective.CrossRef | open url image1

Karlson, R. H., and Hurd, L. E. (1993). Disturbance, coral reef communities, and changing ecological paradigms. Coral Reefs 12, 117–125.
Disturbance, coral reef communities, and changing ecological paradigms.CrossRef | open url image1

Kayal, M., Vercelloni, J., Lison de Loma, T., Bosserelle, P., Chancerelle, Y., Geoffroy, S., Stievenart, C., Michonneau, F., Penin, L., Planes, S., and Adjeroud, M. (2012). Predator crown-of-thorns starfish (Acanthaster planci) outbreak, mass mortality of corals, and cascading effects on reef fish and benthic communities. PLoS One 7, e47363.
Predator crown-of-thorns starfish (Acanthaster planci) outbreak, mass mortality of corals, and cascading effects on reef fish and benthic communities.CrossRef | 1:CAS:528:DC%2BC38XhsFKjt7vM&md5=9aa6f0843ad67a79d4fd5ecd5c033638CAS | 23056635PubMed | open url image1

Kleppel, G. S., Dodge, R. E., and Reese, C. J. (1989). Changes in pigment associated with the bleaching of stony corals. Limnology and Oceanography 34, 1331–1335.
Changes in pigment associated with the bleaching of stony corals.CrossRef | 1:CAS:528:DyaK3cXpsFOrtw%3D%3D&md5=ab72ada5dc84f8e0a6058e2eaf27b389CAS | open url image1

Kohler, K. E., and Gill, S. M. (2006). Coral Point Count with Excel extensions (CPCe): a Visual Basic program for the determination of coral and substrate coverage using random point count methodology. Computers & Geosciences 32, 1259–1269.
Coral Point Count with Excel extensions (CPCe): a Visual Basic program for the determination of coral and substrate coverage using random point count methodology.CrossRef | open url image1

Lenihan, H. S., Adjeroud, M., Kotchen, M. J., Hench, J. L., and Nakamura, T. (2008). Reef structure regulates small-scale spatial variation in coral bleaching. Marine Ecology Progress Series 370, 127–141.
Reef structure regulates small-scale spatial variation in coral bleaching.CrossRef | open url image1

Lesser, M. P., and Lewis, S. (1996). Action spectrum for the effects of UV radiation on photosynthesis in the hermatypic coral Pocillopora damicornis. Marine Ecology Progress Series 134, 171–177.
Action spectrum for the effects of UV radiation on photosynthesis in the hermatypic coral Pocillopora damicornis.CrossRef | open url image1

Lesser, M. P., Stochaj, W. R., Tapley, D. W., and Shick, J. M. (1990). Bleaching in coral reef anthozoans: effects of irradiance, ultraviolet radiation, and temperature on the activities of protective enzymes against active oxygen. Coral Reefs 8, 225–232.
Bleaching in coral reef anthozoans: effects of irradiance, ultraviolet radiation, and temperature on the activities of protective enzymes against active oxygen.CrossRef | open url image1

Levas, S. J., Grottoli, A. G., Hughes, A., Osburn, C. L., and Matsui, Y. (2013). Physiological and biogeochemical traits of bleaching and recovery in the mounding species of coral Porites lobata: implications for resilience in mounding corals. PLoS One 8, e63267.
Physiological and biogeochemical traits of bleaching and recovery in the mounding species of coral Porites lobata: implications for resilience in mounding corals.CrossRef | 1:CAS:528:DC%2BC3sXnsFajsr4%3D&md5=c3fb0e173307273c1eabae3f89af1340CAS | 23658817PubMed | open url image1

Levin, S. A. (1992). The problem of patterns and scale in ecology. Ecology 73, 1943–1967.
The problem of patterns and scale in ecology.CrossRef | open url image1

Loch, K., Loch, W., Schuhmacher, H., and See, W. R. (2002). Coral recruitment and regeneration on a Maldivian reef 21 months after the coral bleaching event of 1998. Marine Ecology (Berlin) 23, 219–236.
Coral recruitment and regeneration on a Maldivian reef 21 months after the coral bleaching event of 1998.CrossRef | open url image1

Loya, Y., Sakai, K., Yamazato, K., Nakano, Y., Sambali, H., and van Woesik, R. (2001). Coral bleaching: the winners and the losers. Ecology Letters 4, 122–131.
Coral bleaching: the winners and the losers.CrossRef | open url image1

Marshall, P. A., and Baird, A. H. (2000). Bleaching of corals on the Great Barrier Reef: differential susceptibilities among taxa. Coral Reefs 19, 155–163.
Bleaching of corals on the Great Barrier Reef: differential susceptibilities among taxa.CrossRef | open url image1

McClanahan, T. R. (2000). Bleaching damage and recovery potential of Maldivian coral reefs. Marine Pollution Bulletin 40, 587–597.
Bleaching damage and recovery potential of Maldivian coral reefs.CrossRef | 1:CAS:528:DC%2BD3cXlsFOqt7Y%3D&md5=e621a8cb7241574b090a9f1e9e061630CAS | open url image1

McClanahan, T. R., and Muthiga, N. A. (2014). Community change and evidence for variable warm-water temperature adaptation of corals in northern Male Atoll, Maldives. Marine Pollution Bulletin 80, 107–113.
Community change and evidence for variable warm-water temperature adaptation of corals in northern Male Atoll, Maldives.CrossRef | 1:CAS:528:DC%2BC2cXhs12is7s%3D&md5=f5adf8fb536822cc3986805e5104cbcdCAS | 24486038PubMed | open url image1

McClanahan, T. R., Maina, J., Moothien-Pillay, R., and Baker, A. C. (2005). Effects of geography, taxa, water flow, and temperature variation on coral bleaching intensity in Mauritius. Marine Ecology Progress Series 298, 131–142.
Effects of geography, taxa, water flow, and temperature variation on coral bleaching intensity in Mauritius.CrossRef | open url image1

Middlebrook, R., Hoegh-Guldberg, O., and Leggat, W. (2008). The effect of thermal history on the susceptibility of reef-building corals to thermal stress. The Journal of Experimental Biology 211, 1050–1056.
The effect of thermal history on the susceptibility of reef-building corals to thermal stress.CrossRef | 18344478PubMed | open url image1

Mumby, P. J., Chisholm, J. R. M., Edwards, A. J., Clark, C., Roark, E., Andrefouet, S., and Jaubert, J. (2001). Unprecedented bleaching-induced mortality in Porites spp. at Rangiroa Atoll, French Polynesia. Marine Biology 139, 183–189.
Unprecedented bleaching-induced mortality in Porites spp. at Rangiroa Atoll, French Polynesia.CrossRef | open url image1

Nakamura, T., and 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.
Water-flow rates and passive diffusion partially explain differential survival of corals during the 1998 bleaching event.CrossRef | open url image1

Nakamura, T., van Woesik, R., and 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.
Photoinhibition of photosynthesis is reduced by water flow in the reef-building coral Acropora digitifera.CrossRef | open url image1

Omori, M., Fukami, H., Kobinata, H., and Hatta, M. (2001). Significant drop of fertilisation of Acropora corals in 1999: the after-affects of heavy coral bleaching? Limnology and Oceanography 46, 704–706.
Significant drop of fertilisation of Acropora corals in 1999: the after-affects of heavy coral bleaching?CrossRef | open url image1

Ostrander, G. K., Armstrong, K. M., Knobbe, E. T., Gerace, D., and Scully, E. P. (2000). Rapid transition in the structure of a coral reef community: the effects of coral bleaching and physical disturbance. Proceedings of the National Academy of Sciences of the United States of America 97, 5297–5302.
Rapid transition in the structure of a coral reef community: the effects of coral bleaching and physical disturbance.CrossRef | 1:CAS:528:DC%2BD3cXjsVWntbs%3D&md5=d0075222ec2ff7f39ef6eb2ea61efffdCAS | 10792043PubMed | open url image1

Palumbi, S. R., Barshis, D. J., Traylor-Knowles, N., and Bay, R. A. (2014). Mechanisms of reef coral resistance to future climate change. Science 344, 895–898.
Mechanisms of reef coral resistance to future climate change.CrossRef | 1:CAS:528:DC%2BC2cXotlWht7k%3D&md5=1b408ec75a0cb24afec56de48ae5966eCAS | 24762535PubMed | open url image1

Pandolfi, J. (2002). Coral community dynamics at multiple scales. Coral Reefs 21, 13–23.
Coral community dynamics at multiple scales.CrossRef | open url image1

Penin, L., Adjeroud, M., Schrimm, M., and Lenihan, H. (2007). High spatial variability in coral bleaching around Moorea, French Polynesia: patterns across reefs, locations, and water depths. Comptes Rendus Biologies 330, 171–181.
High spatial variability in coral bleaching around Moorea, French Polynesia: patterns across reefs, locations, and water depths.CrossRef | 17303544PubMed | open url image1

Penin, L., Vidal-Dupiol, J., and Adjeroud, M. (2013). Response of coral assemblages to thermal stress: are bleaching intensity and spatial patterns consistent between events? Environmental Monitoring and Assessment 185, 5031–5042.
Response of coral assemblages to thermal stress: are bleaching intensity and spatial patterns consistent between events?CrossRef | 23054287PubMed | open url image1

Pratchett, M. S., McCowan, D., Maynard, J. A., and Heron, S. F. (2013). Changes in bleaching susceptibility among corals subject to ocean warming and recurrent bleaching in Moorea, French Polynesia. PLoS One 8, e70443.
Changes in bleaching susceptibility among corals subject to ocean warming and recurrent bleaching in Moorea, French Polynesia.CrossRef | 1:CAS:528:DC%2BC3sXht1OntLvF&md5=9476ab19c4c549092e60fb8dec617d11CAS | 23922992PubMed | open url image1

Rodrigues, L. J., and Grottoli, A. G. (2007). Energy reserves and metabolism as indicators of coral recovery from bleaching. Limnology and Oceanography 52, 1874–1882.
Energy reserves and metabolism as indicators of coral recovery from bleaching.CrossRef | open url image1

Salih, A., Larkum, A., Cox, G., Kühl, M., and Hoegh-Guldberg, O. (2000). Fluorescent pigments in corals are photoprotective. Nature 408, 850–853.
Fluorescent pigments in corals are photoprotective.CrossRef | 1:CAS:528:DC%2BD3MXhtlaisA%3D%3D&md5=e3ce1373ab93a36367cab542092d559cCAS | 11130722PubMed | open url image1

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 314, 105–111. open url image1

Sampayo, E. M., Ridgway, T., Bongaerts, P., and Hoegh-Guldberg, O. (2008). Bleaching susceptibility and mortality of corals are determined by fine-scale differences in symbiont type. Proceedings of the National Academy of Sciences of the United States of America 105, 10444–10449.
Bleaching susceptibility and mortality of corals are determined by fine-scale differences in symbiont type.CrossRef | 1:CAS:528:DC%2BD1cXpsFKktbk%3D&md5=f710eec2d3163174c96b61e9a6ff31dcCAS | 18645181PubMed | open url image1

Spalding, M. (2009). Detecting and monitoring coral bleaching events. In ‘Coral Bleaching: Patterns, Processes, Causes and Consequences’. (Eds M. J. H. van Oppen and J. M. Lough.) pp. 69–82. (Springer: Heidelberg, Germany.)

Stimson, J., Sakai, K., and Sembali, H. (2002). Interspecific comparison of the symbiotic relationship in corals with high and low rates of bleaching-induced mortality. Coral Reefs 21, 409–421. open url image1

Szmant, A. M., and Gassman, N. J. (1990). The effects of prolonged ‘bleaching’ on the tissue biomass and reproduction of the reef coral Montastrea anularis. Coral Reefs 8, 217–224.
The effects of prolonged ‘bleaching’ on the tissue biomass and reproduction of the reef coral Montastrea anularis.CrossRef | open url image1

Ward, S., Harrison, P., and Hoegh-Guldberg, O. (2002). Coral bleaching reduces reproduction of scleractinian corals and increases susceptibility to future stress. In ‘Proceedings of the Ninth International Coral Reef Symposium’, 23–27 October 2000, Bali, Indonesia. (Eds M. K. Moosa, S. Soemodihardo, A. Soegiarto, K. Romimohtarto, A. Nontji, Soekarno and Suharsono.) Vol. 2, pp. 1123–1128. (Ministry of Environment, Indonesian Institute of Sciences, International Society for Reef Studies.)

Wilkinson, C. (2000). ‘Status of Coral Reefs of the World: 2000.’ (Australian Institute of Marine Science: Cape Ferguson, Qld, Australia.)

Wilkinson, C. (2008). ‘Status of Coral Reefs of the World: 2008.’ (Global Coral Reef Monitoring Network and Reef and Rainforest Research Centre: Townsville, Qld, Australia.)



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