The role of zooxanthellae in the thermal tolerance of corals: A 'nugget of hope' for coral reefs in an era of climate change

Proceedings of the Royal Society B: Biological Sciences

Volumn 273, Issue 1599, 2006, Pages 2305-2312

  Berkelmans, Ray ^a,b   Van Oppen, Madeleine J H ^a  

^a AUSTRALIAN INSTITUTE OF MARINE SCIENCE   (Australia)

^b Department of Civil and Environmental Engineering   (Australia)

Author keywords

Acclimatization; Climate change; Coral bleaching; Zooxanthellae

Indexed keywords

ACCLIMATION; CLIMATE CHANGE; CORAL BLEACHING; CORAL REEF; GLOBAL WARMING; TEMPERATURE TOLERANCE; TRANSPLANTATION; ZOOXANTHELLA;

ALGA; ARTICLE; CLIMATE CHANGE; CONTROLLED STUDY; CORAL; CORAL REEF; EVOLUTIONARY ADAPTATION; GREENHOUSE EFFECT; HEAT ACCLIMATIZATION; HEAT TOLERANCE; NONHUMAN; PRIORITY JOURNAL; SYMBIONT;

ACROPORA MILLEPORA; ALGAE; ANTHOZOA; SYMBIODINIUM;

EID: 33748641529     PISSN: 09628452     EISSN: 14712970     Source Type: Journal    
DOI: 10.1098/rspb.2006.3567     Document Type: Article

References (37)

1. Anthony, K. R. N. & Hoegh-Guldberg, O. 2003 Kinetics of photoacclimation in corals. Oecologia 134, 23-31. (doi:10.1007/s00442-002-1095- 1)
2. Baker, A. C. 2001 Reef corals bleach to survive change. Nature 411, 765-766. (doi:10.1038/35081151)
3. Baker, A. C. 2003 Flexibility and specificity in coral-algal symbiosis: diversity, ecology, and biogeography of Symbiodinium. Annu. Rev. Ecol. Syst. 34, 661-689. (doi:10.1146/annurev.ecolsys.34.011802.132417)
4. Baker, A. C., Starger, C. J., McClanahan, T. R. & Glynn, P. W. 2004 Corals' adaptive response to climate. Nature 430, 741. (doi:10.1038/430741a)
5. 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. (doi:10.1007/s00338-003-0353-y)
6. Buddemeier, R. W. & Fautin, D. G. 1993 Coral bleaching as an adaptive mechanism. Bioscience 43, 320-326. (doi:10.2307/1312064)
7. Buddemeier, R. W., Baker, A. C., Fautin, D. G. & Jacobs, J. R. 2004 The adaptive hypothesis of bleaching. In Coral health and disease (ed. E. Rosenberg & Y. Loya). Berlin, Germany: Springer-Verlag.
8. Coffroth, M. A. & Santos, S. R. 2005 Genetic diversity of symbiotic dinoflagellates in the genus Symbiodinium. Protist 156, 19-34. (doi:10.1016/j.protis.2005.02.004)
9. Done, T., Whetton, P., Jones, R., Berkelmans, R., Lough, J., Skirving, W. & Wooldridge, S. 2003 Global climate and coral bleaching on the Great Barrier Reef. Final report to the State of Queensland Greenhouse Taskforce. Brisbane, Australia: Queensland government Department of Natural Resources and Mines. (http://www.nrm.qld.gov.au/science/pdf/barrier_reef_report_1.pdf)
10. Elvidge, C. D., Dietz, J. B., Berkelmans, R., Andréfouët, S., Skirving, W., Strong, A. E. & Tuttle, B. T. 2004 Satellite observation of Keppel Islands (Great Barrier Reef) 2002 coral bleaching using IKONOS data. Coral Reefs 23, 123-132.
11. Enríquez, S., Méndez, E. R. & Iglesias-Prieto, R. 2005 Multiple scattering on coral skeletons enhances light absorbtion by symbiotic algae. Limnol. Oceanogr. 50, 1025-1032.
12. Fabricius, K. E., Mieog, J. C., Colin, P. L., Idip, D. & van Oppen, M. J. H. 2004 Identity and diversity of coral endosymbionts (zooxanthellae) from three Palauan reefs with contrasting bleaching, temperature and shading histories. Mol. Ecol. 13, 2445-2458. (doi:10.1111/j.1365-294X.2004.02230.x)
13. Glynn, P. W., Maté, J. L., Baker, A. C. & Calderón, M. O. 2001 Coral bleaching and mortality in Panama and Ecuador during the 1997-98 El Niño-Southern Oscillation event: spatial/temporal patterns and comparisons with the 1982-1983 event. Bull. Mar. Sci. 69, 79-109.
14. Hoegh-Guldberg, O. 1999 Climate change, coral bleaching and the future of the world's coral reefs. Mar. Freshwater Res. 50, 839-866. (doi:10.1071/ MF99078)
15. Hoegh-Guldberg, O., Jones, R. J., Ward, S. & Loh, W. 2002 Is coral bleaching really adaptive? Nature 415, 601-602. (doi:10.1038/415601a)
16. IPCC 2001 Technical summary. Climate change 2001: Working Group I: the scientific basis: IPCC Third Assessment Report. Geneva, Switzerland: Intergovernmental Panel on Climate Change. (http://www.grida.no/climate/ ipcc_tar/)
17. 2 fixation mechanism in zooxanthllae. Plant, Cell Environ. 21, 1219-1230. (doi:10.1046/j.1365-3040.1998.00345.x)
18. LaJeunesse, T. C. 2001 Investigating the biodiversity, ecology, and phylogeny of endosymbiotic dinoflagellates in the genus Symbiodinium using the ITS region: in search of a species level marker. J. Phycol. 37, 866-880. (doi:10.1046/j.1529-8817.2001.01031.x)
19. Lewis, C. L. & Coffroth, M. A. 2004 The acquisition of exogenous algal symbionts by an octocoral after bleaching. Science 304, 1490-1492. (doi:10.1126/science.1097323)
20. Little, A., van Oppen, M. J. H. & Willis, B. L. 2004 Flexibility in algal endosymbioses shapes growth in reef corals. Science 302, 1492-1494. (doi:10.1126/science.1095733)
21. Lough, J. M. 2000 1997-98: unprecedented thermal stress to coral reefs? Geophys. Res. Lett. 27, 3901-3904. (doi:10.1029/2000GL011715)
22. Mieog, J. C., van Oppen, M. J. H., Cantin, N. C., Stam, W. T. & Olsen, J. L. In preparation. Large potential for algal symbiont shuffling in reef corals.
23. Muscatine, L. & Porter, J. W. 1977 Reef corals-mutualistic symbioses adapted to nutrient-poor environments. Bioscience 27, 454-460. (doi:10.2307/1297526)
24. Pochon, X., LaJeunesse, T. C. & Pawlowski, J. 2004 Biogeographic partitioning and host specialization among foraminiferan dinoflagellate symbionts (Symbiodinium; Dinophyta). Mar. Biol. 146, 17-27.
25. Quinn, G. & Keough, M. J. 2002 Experimental designs and data analysis for biologists. Cambridge, UK: Cambridge University Press.
26. Rowan, R. 2004 Thermal adaptation in reef coral symbionts. Nature 430, 742. (doi:10.1038/430742a)
27. Rowan, R. & Knowlton, N. 1995 Intraspecific diversity and ecological zonation in coral-algal symbiosis. Proc. Natl Acad. Sci. 92, 2850-2853.
28. Spalding, M. D., Ravilious, C. & Green, E. P. 2001 World atlas of coral reefs. Berkley, CA: University of California Press.
29. Stimson, J. & Kinzie III, R. A. 1991 The temporal pattern and rate of release of zooxanthellae from the reef coral Pocillopora damicornis (Linnaeus) under nitrogen enrichment and control conditions. J. Exp. Mar. Biol. Ecol. 153, 63-74. (doi:10.1016/S0022-0981(05)80006-1)
30. Tchernov, D., Gorbunov, M. Y., de Vargas, C., Yadav, S. W., Milligan, A. J., Häggblom, M. & Falkowski, P. G. 2004 Membrane lipids of symbiotic algae are diagnostic of sensitivity to thermal bleaching in corals. Proc. Natl Acad. Sci. 101, 13 531-13 535. (doi:10.1073/pnas.0402907101)
31. Thornhill, D., LaJeunesse, T. C., Kemp, D. W., Fitt, W. K. & Schmidt, G. W. 2005 Multi-year, seasonal genotypic surveys of coral-algal symbioses reveal prevalent stability or post-bleaching reversion. Mar. Biol. 148, 711-722. (doi:10.1007/s00227-005-0114-2)
32. Turner, P., Berkelmans, R. & Brodie, M. 2002 Precise set-point control of temperature for coral bleaching experiments. Mar. Technol. Soc. J. 36, 70-75.
33. Ulstrup, K. E. & van Oppen, M. J. H. 2003 Geographic and habitat partitioning of genetically distinct zooxanthellae (Symbiodinium) in Acropora corals on the Great Barrier Reef. Mol. Ecol. 12, 3477-3484. (doi:10.1046/j.1365- 294X.2003.01988.x)
34. van Oppen, M. J. H., Palstra, F. P., Piquet, A. M.-T. & Miller, D. J. 2001 Patterns of coral-dinoflagellate associations in Acropora: significance of local availability and physiology of Symbiodinium strains and host-symbiont selectivity. Proc. R. Soc. B. 268, 1759-1767. (doi:10.1098/rspb.2001.1733)
35. van Oppen, M. J. H., Mahiny, A. & Done, T. 2005 Geographic patterns of zooxanthella types in three coral species on the Great Barrier Reef sampled after the 2002 bleaching event. Coral Reefs 24, 482-487.
36. Veron, J. E. N. 1995 Corals in space and time: the biogeography and evolution of the scleractinia. Ithaca, NY: Cornell University Press.
37. Ware, J. R. 1997 The effect of global warming on coral reefs: acclimate or die. In Proc. 8th Int. Coral Reef Symp., Panama, 24-29 June 1996, pp. 527-532. Panamá: Smithsonian Tropical Research Institute.