Limits to the thermal tolerance of corals adapted to a highly fluctuating, naturally extreme temperature environment

Scientific Reports

Volumn 5, Issue , 2015, Pages

  Schoepf, Verena ^a,b   Stat, Michael ^c   Falter, James L ^a,b   McCulloch, Malcolm T ^a,b  

^a UNIVERSITY OF WESTERN AUSTRALIA   (Australia)

^b Australia   (Australia)

^c CURTIN UNIVERSITY   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

ACROPORA; AUSTRALIA; BLEACHING; CIRCADIAN RHYTHM; CLADISTICS; CORAL; ENVIRONMENTAL TEMPERATURE; EXPOSURE; HEAT STRESS; HEAT TOLERANCE; HEATING; HUMAN; IMMUNITY; MORTALITY; SYMBIODINIUM; ACCLIMATIZATION; ANIMAL; ANTHOZOA; PHYSIOLOGY;

ACCLIMATIZATION; ANIMALS; ANTHOZOA; AUSTRALIA;

EID: 84948845072     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep17639     Document Type: Article

References (65)

1. Hoegh-Guldberg, O. et al. Coral reefs under rapid climate change and ocean acidification. Science 318, 1737-1742 (2007).
2. Glynn, P. W. Coral reef bleaching: facts, hypotheses and implications. Global Change Biol. 2, 495-509 (1996).
3. Hoegh-Guldberg, O. & Smith, G. J. The effect of sudden changes in temperature, light, and salinity on the population density and export of zooxanthellae from the reef coral Stylophora pistillata Esper and Seriatopora hystrix Dana. J. Exp. Mar. Biol. Ecol. 129, 279-303 (1989).
4. Muscatine, L., McCloskey, L. R. & Marian, R. E. Estimating the daily contribution of carbon from zooxanthellae to coral animal respiration. Limnol. Oceanogr. 26, 601-611 (1981).
5. IPCC, Climate Change 2013: The Physical Science Basis. Summary for Policy Makers. (2013) Available at: www.ipcc.ch. (Accessed: 23rd May 2014).
6. Teneva, L. et al. Predicting coral bleaching hotspots: the role of regional variability in thermal stress and potential adaptation rates. Coral Reefs 31, 1-12 (2012).
7. Frieler, K. et al. Limiting global warming to 2 °C is unlikely to save most coral reefs. Nat. Clim. Change 3, 165-170 (2013).
8. Kleypas, J. A., McManus, J. W. & Menez, L. A. B. Environmental limits to coral reef development: where do we draw the line Am. Zool. 39, 146-159 (1999).
9. Riegl, B. et al. In Coral Reefs of the Gulf: Adaptation to Climatic Extremes (eds Riegl, B. & Purkis, S. J.) Ch. 6, 95-105 (Springer, 2012).
10. Coles, S. L., Jokiel, P. L. & Lewis, C. R. Thermal tolerance in tropical versus subtropical Pacific reef corals. Pac. Sci. 30, 159-166 (1976).
11. Hume, B. et al. Corals from the Persian/Arabian Gulf as models for thermotolerant reef-builders: Prevalence of clade C3 Symbiodinium, host fluorescence and ex situ temperature tolerance. Mar. Poll. Bull. 72, 313-322 (2013).
12. Palumbi, S. R., Barshis, D. J., Traylor-Knowles, N. & Bay, R. A. Mechanisms of reef coral resistance to future climate change. Science 344, 895-898 (2014).
13. Castillo, K. D., Ries, J. B., Weiss, J. M. & Lima, F. P. Decline of forereef corals in response to recent warming linked to history of thermal exposure. Nat. Clim. Change 2, 756-760 (2012).
14. Goreau, T. J. & Macfarlane, A. H. Reduced growth rate of Montastrea annularis following the 1987-1988 coral-bleaching event. Coral Reefs 8, 211-215 (1990).
15. Oliver, T. A. & Palumbi, S. R. Do fluctuating temperature environments elevate coral thermal tolerance Coral Reefs 30, 429-440 (2011).
16. Berkelmans, R. & Willis, B. L. Seasonal and local spatial patterns in the upper thermal limits of corals on the inshore Central Great Barrier Reef. Coral Reefs 18, 219-228 (1999).
17. Donner, S. D. An evaluation of the effect of recent temperature variability on the prediction of coral bleaching events. Ecol. Appl. 21, 1718-1730 (2011).
18. Loya, Y. et al. Coral bleaching: the winners and the losers. Ecol. Lett. 4, 122-131 (2001).
19. Marshall, P. A. & Baird, A. H. Bleaching of corals on the Great Barrier Reef: differential susceptibilities among taxa. Coral Reefs 19, 155-163 (2000).
20. Berkelmans, R. & van Oppen, M. J. H. The role of zooxanthellae in the thermal tolerance of corals: a "nugget of hope" for coral reefs in an era of climate change. Proc. R. Soc. B 273, 2305-2312 (2006).
21. Stat, M. & Gates, R. D. Clade D Symbiodinium in scleractinian corals: A "nugget" of hope, a selfish opportunist, an ominous sign, or all of the above J. Mar. Biol. 2011, 9 (2011).
22. Thornhill, D. J. et al. A connection between colony biomass and death in Caribbean reef-building corals. PLoS One 6, e29535, doi: 29510.21371/journal.pone.0029535 (2011).
23. Grottoli, A. G. et al. The cumulative impact of annual coral bleaching can turn some coral species winners into losers. Global Change Biol. 20, 3823-3833 (2014).
24. Grottoli, A. G., Rodrigues, L. J. & Palardy, J. E. Heterotrophic plasticity and resilience in bleached corals. Nature 440, 1186-1189 (2006).
25. Bessell-Browne, P., Stat, M., Thomson, D. & Clode, P. L. Coscinaraea marshae corals that have survived prolonged bleaching exhibit signs of increased heterotrophic feeding. Coral Reefs 33, 795-804 (2014).
26. Rosser, N. L. & Veron, J. E. N. Australian corals thriving out of water in an extreme environment. Coral Reefs 30, 21-21 (2011).
27. Dandan, S. S., Falter, J. L., Lowe, R. J. & McCulloch, M. T. Resilience of coral calcification to extreme temperature variations in the Kimberley region, northwest Australia. Coral Reefs, doi: 10.1007/s00338-015-1335-6 (2015).
28. Richards, Z. T., Garcia, R. A., Wallace, C. C., Rosser, N. L. & Muir, P. R. A diverse asemblage of reef corals thriving in a dynamic intertidal reef setting (Bonaparte Archipelago, Kimberley, Australia).PLoS One 10, e0117791 (2015).
29. Purcell, S. Intertidal reefs under extreme tidal flux in Buccaneer Archipelago, Western Australia. Coral Reefs 21, 191-192 (2002).
30. Craig, P., Birkeland, C. & Belliveau, S. High temperatures tolerated by a diverse assemblage of shallow-water corals in American Samoa. Coral Reefs 20, 185-189 (2001).
31. Budd, A. F., Fukami, H., Smith, N. D. & Knowlton, N. Taxonomic classification of the reef coral family Mussidae (Cnidaria: Anthozoa: Scleractinia).Zool. J. Linn. Soc. 166, 465-529 (2012).
32. Warner, M. E., Fitt, W. K. & Schmidt, G. W. Damage to photosystem II in symbiotic dinoflagellates: A determinant of coral bleaching. Proc. Natl. Acad. Sci. USA 96, 8007-8012 (1999).
33. Stat, M., Pochon, X., Cowie, R. O. M. & Gates, R. D. Specificity in communities of Symbiodinium in corals from Johnston Atoll. Mar. Ecol. Prog. Ser. 386, 83-96 (2009).
34. Luna, G. M., Biavasco, F. & Danovaro, R. Bacteria associated with the rapid tissue necrosis of stony corals. Environ. Microbiol. 9, 1851-1857 (2007).
35. Riegl, B. M., Purkis, S. J., Al-Cibahy, A. S., Abdel-Moati, M. A. & Hoegh-Guldberg, O. Present limits to heat-adaptability in corals and population-level responses to climate extremes. PLoS One 6, e24802 (2011).
36. Coles, S. L. & Riegl, B. M. Thermal tolerances of reef corals in the Gulf: A review of the potential for increasing coral survival and adaptation to climate change through assisted translocation. Mar. Poll. Bull. 72, 323-332 (2013).
37. Burt, J., Al-Harthi, S. & Al-Cibahy, A. Long-term impacts of coral bleaching events on the world's warmest reefs. Mar. Environ. Res. 72, 225-229 (2011).
38. Berkelmans, R. Time-integrated thermal bleaching thresholds of reefs and their variation on the Great Barrier Reef. Mar. Ecol. Prog. Ser. 229, 73-82 (2002).
39. Warner, M. E., Fitt, W. K. & Schmidt, G. W. The effects of elevated temperature on the photosynthetic efficiency of zooxanthellae in hospite from four different species of reef coral: a novel approach. Plant Cell Environ. 19, 291-299 (1996).
40. Schoepf, V. et al. Coral energy reserves and calcification in a high-CO2 world at two temperatures. PLoS One 8, e75049 (2013).
41. Brown, B. E., Downs, C. A., Dunne, R. P. & Gibb, S. W. Exploring the basis of thermotolerance in the reef coral Goniastrea aspera. Mar. Ecol. Prog. Ser. 242, 119-129 (2002).
42. Barshis, D. J. et al. Protein expression and genetic structure of the coral Porites lobata in an environmentally extreme Samoan back reef: does host genotype limit phenotypic plasticity Mol. Ecol. 19, 1705-1720 (2010).
43. Bay, Rachael A. & Palumbi, Stephen R. Multilocus adaptation associated with heat resistance in reef-building corals. Curr. Biol. 24, 2952-2956 (2014).
44. Barshis, D. J. et al. Genomic basis for coral resilience to climate change. Proc. Natl. Acad. Sci. USA 110, 1387-1392 (2013).
45. LaJeunesse, T. C. et al. Ecologically differentiated stress-tolerant endosymbionts in the dinoflagellate genus Symbiodinium (Dinophyceae) Clade D are different species. Phycologia 53, 305-319 (2014).
46. Jones, A. & Berkelmans, R. Potential costs of acclimatization to a warmer climate: Growth of a reef coral with heat tolerant vs. sensitive symbiont types. PLoS One 5, e10437 (2010).
47. Thomas, L., Kendrick, G. A., Kennington, W. J., Richards, Z. T. & Stat, M. Exploring Symbiodinium diversity and host specificity in Acropora corals from geographical extremes of Western Australia with 454 amplicon pyrosequencing. Mol. Ecol. 23, 3113-3126 (2014).
48. Silverstein, R. N., Correa, A. M. S., LaJeunesse, T. C. & Baker, A. C. Novel algal symbiont (Symbiodinium spp.) diversity in reef corals of Western Australia. Mar. Ecol. Prog. Ser. 422, 63-75 (2011).
49. LaJeunesse, T. C. et al. Low symbiont diversity in southern Great Barrier Reef corals, relative to those of the Caribbean. Limnol. Oceanogr. 48, 2046-2054 (2003).
50. Fisher, P. L., Malme, M. K. & Dove, S. The effect of temperature stress on coral-Symbiodinium associations containing distinct symbiont types. Coral Reefs 31, 473-485 (2012).
51. Hume, B. et al. Symbiodinium thermophilum sp. nov., a thermotolerant symbiotic alga prevalent in corals of the world's hottest sea, the Persian/Arabian Gulf. Sci. Rep. 5, 8562 (2015).
52. Howells, J. E. et al. Coral thermal tolerance shaped by local adaptation of photosymbionts. Nat. Clim. Change 2, 116-120 (2011).
53. Bellantuono, A. J., Hoegh-Guldberg, O. & Rodriguez-Lanetty, M. Resistance to thermal stress in corals without changes in symbiont composition. Proc. R. Soc. B 279, 1100-1107 (2012).
54. Mayfield, A. B. et al. The physiological response of the reef coral Pocillopora damicornis to elevated temperature: results from coral reef mesocosm experiments in Southern Taiwan. Mar. Environ. Res. 86, 1-11 (2013).
55. Nakamura, T., Van Woesik, R. & Yamasaki, H. Photoinhibition of photosynthesis is reduced by water flow in the reef-building coral Acropora digitifera. Mar. Ecol. Prog. Ser. 301, 109-118 (2005).
56. Guest, J. R. et al. Contrasting patterns of coral bleaching susceptibility in 2010 suggest an adaptive response to thermal stress. PLoS One 7, e33353 (2012).
57. Riegl, B. Climate change and coral reefs: different effects in two high-latitude areas (Arabian Gulf, South Africa). Coral Reefs 22, 433-446 (2003).
58. Yao, W. & Byrne, R. H. Simplified seawater alkalinity analysis: Use of linear array spectrometers. Deep-Sea Res. Pt. I 45, 1383-1392 (1998).
59. Lewis, E. & Wallace, D. Program developed for CO2 system calculations. ORNL/CDIAC-105, Carbon Dioxide Information Analysis Center, Oak Ridge National Laboratory, U.S. Department of Energy (1998).
60. Maynard, J. A. et al. ReefTemp: An interactive monitoring system for coral bleaching using high-resolution SST and improved stress predictors. Geophys. Res. Lett. 35, L05603 (2008).
61. Zhang, Z., Green, B. R. & Cavalier-Smith, T. Phylogeny of ultra-rapidly evolving dinoflagellate chloroplast genes: a possible common origin for sporozoan and dinoflagellate plastids. J. Mol. Evol. 51, 26-40 (2000).
62. Iglesias-Prieto, R., Beltran, V. H., LaJeunesse, T. C., Reyes-Bonilla, H. & Thome, P. E. Different algal symbionts explain the vertical distribution of dominant reef corals in the eastern Pacific. Proc. R. Soc. B 271, 1757-1763 (2004).
63. Fitt, W. K., McFarland, F. K., Warner, M. E. & Chilcoat, G. C. Seasonal patterns of tissue biomass and densities of symbiotic dinoflagellates in reef corals and relation to coral bleaching. Limnol. Oceanogr. 45, 677-685 (2000).
64. Marsh, J. A. Primary productivity of reef-building calcareous red algae. Ecology 51, 255-263 (1970).
65. Jeffrey, S. W. & Humphrey, G. F. New spectrophotometric equations for determining chlorophylls a, b, c1, and c2 in higher plants, algae, and natural phytoplankton. Biochem. Physiol. Pflanzen 167, 191-194 (1975).