Historical thermal regimes define limits to coral acclimatization

Ecology

Volumn 94, Issue 5, 2013, Pages 1078-1088

  Howells, Emily J ^a,b,c   Berkelmans, Ray ^b   Van Oppen, Madeleine J H ^a,b   Willis, Bette L ^a   Bay, Line K ^a,b  

^a JAMES COOK UNIVERSITY   (Australia)

^b AUSTRALIAN INSTITUTE OF MARINE SCIENCE   (Australia)

^c NEW YORK UNIVERSITY ABU DHABI   (United Arab Emirates)

Author keywords

Acclimatization; Acropora millepora; Assisted migration; Australia; Coral; Coral bleaching; Coral mortality; Great Barrier Reef; Local adaptation; Sea temperature rise; Symbiodinium; Thermal tolerance; Zooxanthellae

Indexed keywords

ACCLIMATION; ADAPTATION; BIOMASS ALLOCATION; COLONY; CONSERVATION MANAGEMENT; CORAL BLEACHING; CORAL REEF; LOCAL ADAPTATION; MIGRATION; MORTALITY; PHYSIOLOGICAL RESPONSE; SURVIVAL; TEMPERATURE TOLERANCE; THERMAL REGIME; TRANSPLANTATION; ZOOXANTHELLA;

ACCLIMATIZATION; ANIMAL; ANTHOZOA; ARTICLE; CORAL REEF; HEAT; PHYSIOLOGY; TIME;

ACCLIMATIZATION; ANIMALS; ANTHOZOA; CORAL REEFS; HOT TEMPERATURE; TIME FACTORS;

AUSTRALIA; CORAL SEA; GREAT BARRIER REEF; PACIFIC OCEAN; QUEENSLAND;

EID: 84878081041     PISSN: 00129658     EISSN: None     Source Type: Journal    
DOI: 10.1890/12-1257.1     Document Type: Article

References (58)

1. Ainsworth, T. D., O. Hoegh-Guldberg, S. F. Heron, W. J. Skirving, and W. Leggat. 2008. Early cellular changes are indicators of pre-bleaching thermal stress in the coral host. Journal of Experimental Marine Biology and Ecology 364: 63-71.
2. Anthony, K. R. N. 2000. Enhanced particle-feeding capacity of corals on turbid reefs (Great Barrier Reef, Australia). Coral Reefs 19:59-67.
3. Baird, A. H., R. Bhagooli, P. J. Ralph, and S. Takahashi. 2009. Coral bleaching: the role of the host. Trends in Ecology and Evolution 24:16-20.
4. Berkelmans, R. 2002. Time-integrated thermal bleaching thresholds of reefs and their variation on the Great Barrier Reef. Marine Ecology Progress Series 229:73-82.
5. Berkelmans, R., and M. J. H. van Oppen. 2006. The role of zooxanthellae in the thermal tolerance of corals: a 'nugget of hopé for coral reefs in an era of climate change. Proceedings of the Royal Society B 273:2305-2312.
6. Cantin, N. E., M. J. H. van Oppen, B. L. Willis, J. C. Mieog, and A. P. Negri. 2009. Juvenile corals can acquire more carbon from high-performance algal symbionts. Coral Reefs 28:405-414.
7. Chen, C. A., J.-T. Wang, L. S. Fang, and Y.-W. Yang. 2005. Fluctuating algal symbiont communities in Acropora palifera (Scleractinia: Acroporidae) from Taiwan. Marine Ecology Progress Series 295:113-121.
8. Coles, S. L., and Y. H. Fadlallah. 1991. Reef coral survival and mortality at low temperatures in the Arabian Gulf: new species-specific lower temperature limits. Coral Reefs 9:231-237.
9. Coles, S. L., and P. L. Jokiel. 1978. Synergistic effects of temperature, salinity and light on the hermatypic coral Montipora verrucosa. Marine Biology (Berlin) 49:187-196.
10. Coles, S. L., P. L. Jokiel, and C. R. Lewis. 1976. Thermal tolerance in tropical vs. subtropical reef corals. Pacific Science 30:159-166.
11. Csá szá r, N. B. M., P. J. Ralph, R. Frankham, R. Berkelmans, and M. J. H. van Oppen. 2010. Estimating the potential for adaptation of corals to climate warming. PLoS ONE 5930: e9751.
12. Devlin, M., J. Waterhouse, L. McKinna, and S. Lewis. 2010. Terrestrial runoff in the Great Barrier Reef, Marine Monitoring Program (3.7.2b) Tully and Burdekin case studies. Australian Centre for Tropical Freshwater Research, James Cook University. Australian Government, Department of the Environment, Water, Heritage, and the Arts, Canberra, ACT, Australia.
13. Dizon, R. T., and H. T. Yap. 2006. Effects of coral transplantation in sites of varying distances and environmental conditions. Marine Biology (Berlin) 148:933-943.
14. Donelson, J. M., P. L. Mundy, M. I. McCormick, and R. C. Pitcher. 2011. Rapid transgenerational acclimation of a tropical reef fish to climate change. Nature Climate Change 2:30-32.
15. Downs, C. A., J. E. Fauth, J. C. Halas, P. Dustan, J. Bemiss, and C. M. Woodley. 2002. Oxidative stress and seasonal coral bleaching. Free Radical Biology and Medicine 33:533-543.
16. Edwards, A. J., S. Job, and S. Wells. 2010. Learning lessons from past reef-rehabilitation projects. Pages 129-166 in A. J. Edwards, editor. Reef rehabilitation manual. Coral Reef Targeted Research and Capacity Building for Management Program, Global Change Institute, University of Queensland, St. Lucia, Queensland, Australia.
17. Falkowski, P. G., and Z. Dubinsky. 1981. Light-shade adaptation of Stylophora pistillata, a hermatypic coral from the Gulf of Eilat, Aqaba, Red Sea. Nature (London) 289: 172-174.
18. Fan, T.-Y., and C.-F. Dai. 1999. Reproductive plasticity in the reef coral Echinopora lamellosa. Marine Ecology Progress Series 190:297-301.
19. Fitt, W. K., F. K. McFarland, M. E. Warner, and G. C. Chilcoat. 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.
20. Frascaria-Lacoste, N., and J. Ferná ndez-Manjarré s. 2012. Assisted colonization of foundation species: lack of consideration of the extended phenotype concept -response to Kreyling et al. (2011). Restoration Ecology 20:296-298.
21. Harrison, P. L. 2011. Sexual reproduction of scleractinian corals. Pages 59-85 in Z. Dubinsky and N. Stambler, editors. Coral reefs: an ecosystem in transition. Springer, Dordrecht, Germany.
22. Hoegh-Guldberg, O., L. Hughes, S. McIntyre, D. Lindenmayer, C. Parmesan, H. Possingham, and C. Thomas. 2008. Assisted colonization and rapid climate change. Science 321: 345-346.
23. Howells, E. J., V. H. Beltran, N. W. Larsen, L. K. Bay, B. L. Willis, and M. J. H. van Oppen. 2012. Coral thermal tolerance shaped by local adaptation of photosymbionts. Nature Climate Change 2:116-120.
24. Howells, E. J., M. J. H. van Oppen, and B. L. Willis. 2009. High genetic differentiation and cross-shelf patterns of genetic diversity among Great Barrier Reef populations of Symbiodinium. Coral Reefs 28:215-225.
25. Iglesias-Prieto, R., J. L. Matta, W. A. Robins, and R. K. Trench. 1992. Photosynthetic response to elevated temperature in the symbiotic dinoflagellate Symbiodinium microadriaticum in culture. Proceedings of the National Academy of Sciences USA 89:10302-10305.
26. Jokiel, P. L. 2004. Temperature stress and coral bleaching. Pages 401-425 in E. Rosenberg and Y. Loya, editors. Coral health and disease. Springer-Verlag, New York, New York, USA.
27. Jones, A. M., and R. Berkelmans. 2011. Tradoffs to thermal acclimation: Energetics and reproduction of a reef coral with heat tolerant Symbiodinium type D. Journal of Marine Biology 2011:185890.
28. Jones, A. M., R. Berkelmans, M. J. H. van Oppen, J. C. Mieog, and W. Sinclair. 2008. A community change in the algal endosymbionts of a scleractinian coral following a natural bleaching event: field evidence of acclimatization. Proceedings of the Royal Society B 275:1359-1365.
29. Jones, R. J. 2008. Coral bleaching, bleaching-induced mortality, and the adaptive significance of the bleaching response. Marine Biology (Berlin) 154:65-80.
30. Kemp, D. W., C. Oakley, D. J. Thornhill, L. Newcomb, G. W. Schmidt, and W. K. Fitt. 2011. Catastrophic mortality on inshore coral reefs of the Florida Keys due to severe lowtemperature stress. Global Change Biology 17:3468-3477.
31. Kreyling, J., T. Bittner, A. Jaeschke, A. Jentsch, M. J. Steinbauer, D. Thiel, and C. Beierkuhnlein. 2011. Assisted colonization: a question of focal units and recipient localities. Restoration Ecology 19:433-440.
32. LaJeunesse, T. C., R. Smith, et al. 2010. Host-symbiont recombination versus natural selection in the response of coral-dinoflagellate symbioses to environmental disturbance. Proceedings of the Royal Society B 277:2925-2934.
33. Lesser, M. P. 2006. Oxidative stress in marine environments. Biochemistry and physiological ecology. Annual Review of Physiology 68:253-278.
34. Linä́ n-Cabello, M. A., L. A. Flores-Ramírez, T. Zenteno-Savin, N. O. Olguín-Monroy, R. Sosa-Avalos, M. Patinö-Barragan, and A. Olivos-Ortiz. 2010. Seasonal changes of antioxidant and oxidative parameters in the coral Pocillopora capitata on the Pacific coast of Mexico. Marine Ecology 31:407-417.
35. Marshall, P. A., and A. H. Baird. 2000. Bleaching of corals on the Great Barrier Reef: Differential susceptibilities among taxa. Coral Reefs 19:155-163.
36. Meehl, G., et al. 2007. Global Climate Projections. Pages 747-845 in S. Solomon, D. Qin, M. Manning, Z. Chen, M. Marquis, K. Averyt, M. Tignor, and H. Miller, editors. Climate change 2007: the physical science basis. Contribution of Working Group I to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge University Press, Cambridge, UK.
37. Meyer, E., S. Davies, S. Wang, B. L. Willis, D. Abrego, T. E. Juenger, and M. V. Matz. 2009. Genetic variation in responses to a settlement cue and elevated temperature in the reef-building coral Acropora millepora. Marine Ecology Progress Series 392:81-92.
38. Mieog, J. C., M. J. H. van Oppen, N. E. Cantin, W. T. Stam, and J. L. Olsen. 2007. Real-time PCR reveals a high incidence of Symbiodinium clade D at low levels in four scleractinian corals across the Great Barrier Reef: implications for symbiont shuffling. Coral Reefs 26:449-457.
39. Mousseau, T. A., and C. W. Fox. 1998. The adaptive significance of maternal effects. Trends in Ecology and Evolution 13:403-407.
40. Mumby, P. J., I. A. Elliott, C. M. Eakin, W. Skirving, C. B. Paris, H. J. Edwards, S. Enríquez, R. Iglesias-Prieto, L. M. Cherubin, and J. R. Stevens. 2011. Reserve design for uncertain responses of coral reefs to climate change. Ecology Letters 14:132-140.
41. Omori, M. 2011. Degradation and restoration of coral reefs: experience in Okinawa, Japan. Marine Biology Research 7:3-12.
42. Padilla-Gaminö, J. L., et al. 2012. Are all eggs created equal? A case study from the Hawaiian reef-building coral Montipora capitata. Coral Reefs 2. http://dx.doi.org/10.1007/s00338-012-0957-1
43. Pandolfi, J. M., S. R. Connolly, D. J. Marshall, and A. L. Cohen. 2011. projecting coral reef futures under global warming and ocean acidification. Science 333:418-422.
44. Polato, N. R., C. R. Voolstra, J. Schnetzer, M. K. DeSalvo, C. J. Randall, A. M. Szmant, M. Medina, and I. B. Baums. 2010. Location-specific responses to thermal stress in larvae of the reef-building coral Montastraea faveolata. PLoS ONE 5:e11221.
45. Robbart, M. L., P. Peckol, S. P. Scordilis, H. A. Curran, and J. Brown-Saracino. 2004. Population recovery and differential heat shock protein expression for the corals Agaricia agaricites and A. tenuifolia in Belize. Marine Ecology Progress Series 283:151-160.
46. Robison, J. D., and M. E. Warner. 2006. Differential impacts of photoacclimation and thermal stress on the photobiology of four different phylotypes of Symbiodinium (Pyrrhophyta). Journal of Phycology 42:568-579.
47. Sanford, E., and M. W. Kelly. 2011. Local adaptation in marine invertebrates. Annual Review of Marine Science 3: 509-535.
48. Saxby, T., W. C. Dennison, and O. Hoegh-Guldberg. 2003. Photosynthetic responses of the coral Montipora digitata to cold temperature stress. Marine Ecology Progress Series 248: 85-97.
49. Sharp, V. A., B. E. Brown, and D. Miller. 1997. Heat shock protein (hsp 70) expression in the tropical reef coral Goniopora djiboutiensis. Journal of Thermal Biology 22:11-19.
50. StatSoft. 2011. Statistica version 10. StatSoft, Tulsa, Oklahoma, USA.
51. Tchernov, D., H. Kvitt, L. Haramaty, T. Bibby, M. Y. Gorbunov, H. Rosenfeld, and P. G. Falkowski. 2011. Apoptosis and the selective survival of host animals following thermal bleaching in zooxanthellate corals. Proceedings of the National Academy of Sciences USA 108:9905-9909.
52. Thornhill, D. J., D. W. Kemp, B. U. Bruns, W. K. Fitt, and G. W. Schmidt. 2008. Correspondence between cold tolerance and temperate biogeography in a western atlantic Symbiodinium (Dinophyta) lineage. Journal of Phycology 44: 1126-1135.
53. Ulstrup, K. E., R. Berkelmans, P. J. Ralph, and M. J. H. van Oppen. 2006. Variation in bleaching sensitivity of two coral species across a latitudinal gradient on the Great Barrier Reef: the role of zooxanthellae. Marine Ecology Progress Series 314:135-148.
54. van Oppen, M. J. H., and R. D. Gates. 2006. Conservation genetics and the resilience of reef-building corals. Molecular Ecology 15:3863-3883.
55. van Oppen, M. J. H., F. P. Palstra, A. M. T. Piquet, and D. J. Miller. 2001. Patterns of coral-dinoflagellate associations in Acropora: significance of local availability and physiology of Symbiodinium strains and host-symbiont selectivity. Proceedings of the Royal Society B 268:1759-1767.
56. van Oppen, M. J. H., L. M. Peplow, S. Kininmonth, and R. Berkelmans. 2011. Historical and contemporary factors shape the population genetic structure of the broadcast spawning coral, Acropora millepora, on the Great Barrier Reef. Molecular Ecology 23:4899-4914.
57. Walther, G., E. Post, P. Convey, A. Menzel, C. Parmesan, T. J. C. Beebee, J. Fromentin, O. Hoegh-Guldberg, and F. Bairlein. 2002. Ecological responses to recent climate change. Nature 416:389-395.
58. Willis, B. L., R. C. Babcock, P. L. Harrison, and J. K. Oliver. 1985. Patterns in the mass spawning of corals on the Great Barrier Reef from 1981 to 1984. Pages 343-348 in C. Gabrie and B. Salvat, editors. Proceedings of the Fifth International Coral Reef Congress, Tahiti 4. Antenne Museum-Ephe, Mooré a, French Polynesia.