Abstract
The response of coral-reef ecosystems to contemporary thermal stress may be in part a consequence of recent or historical sea-surface temperature (SST) variability. To test this hypothesis, we examined whether: (i) there was a relationship between the historical frequency of SST variability and stress experienced during the most recent thermal-stress events (in 1998 and 2005–2006) and (ii) coral reefs that historically experienced frequent thermal anomalies were less likely to experience coral bleaching during these recent thermal-stress events. Examination of nine detrended coral δ18O and Sr/Ca anomaly records revealed a high- (5.7-year) and low-frequency (>54-year) mode of SST variability. There was a positive relationship between the historical frequency of SST anomalies and recent thermal stress; sites historically dominated by the high-frequency mode experienced greater thermal stress than other sites during both events, and showed extensive coral bleaching in 1998. Nonetheless, in 2005–2006, corals at sites dominated by high-frequency variability showed reduced bleaching, despite experiencing high thermal stress. This bleaching resistance was most likely a consequence of rapid directional selection that followed the extreme thermal event of 1998. However, the benefits of regional resistance could come at the considerable cost of shifts in coral species composition.
References
Anthony K. R. N., Connolly S. R.& Hoegh-Guldberg O. . 2007Bleaching, energetics, and coral mortality risk: Effects of temperature, light, and sediment regime. Limnol. Oceanogr. 52, 716–726. Crossref, ISI, Google ScholarAnthony K. R. N., Hoogenboom M. O., Maynard J. A., Grottoli A. G.& Middlebrook R. In pressEnergetics approach to predicting mortality risk from environmental stress: a case study of coral bleaching. Funct. Ecol.(doi:10.1111/j.1365-2435.2008.01531.x). ISI, Google ScholarBaird A. H.& Marshall P. A. . 2002Mortality, growth and reproduction in scleractinian corals following bleaching on the Great Barrier Reef. Mar. Ecol. Prog. Ser. 237, 133–141. (doi:10.3354/meps237133). Crossref, ISI, Google ScholarBaird A. H., Bhagooli R., Ralph P. J.& Takahashi S. . 2008Coral bleaching: the role of the host. Trends Ecol. Evol. 24, 16–20. (doi:10.1016/j.tree.2008.09.005). Crossref, PubMed, ISI, Google ScholarBaker A. C. . 2001Reef corals bleach to survive change. Nature 411, 765–766. (doi:10.1038/35081151). Crossref, PubMed, ISI, Google ScholarBaker A. C., Starger C. J., McClanahan T. R.& Glynn P. W. . 2004Corals' adaptive response to climate change. Nature 430, 741. (doi:10.1038/430741a). Crossref, PubMed, ISI, Google ScholarBates J. J.& Jackson D. L. . 2001Trends in upper-tropospheric humidity. Geophys. Res. Lett. 28, 1695–1698. (doi:10.1029/2000GL012544). Crossref, ISI, Google ScholarBerkelmans R.& van Oppen M. J. H. . 2006The 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. Link, ISI, Google ScholarBrown B. E. . 1997aAdaptations of reef corals to physical environmental stress. Advances in Marine Biology 31, 221–299. (doi:10.1016/S0065-2881(08)60224-2). Crossref, ISI, Google ScholarBrown B. E. . 1997bCoral bleaching: causes and consequences. Coral Reefs 16, S129–S138. (doi:10.1007/s003380050249). Crossref, ISI, Google ScholarBrown B. E., Dunne R. P., Scoffin T. P.& Le Tissier M. D. A. . 1994Solar damage in intertidal corals. Mar. Ecol. Prog. Ser. 105, 219–230. (doi:10.3354/meps105219). Crossref, ISI, Google ScholarBrown B. E., Dunne R. P., Goodson M. S.& Douglas A. E. . 2002Experience shapes the susceptibility of a reef coral to bleaching. Coral Reefs 21, 119–126. Crossref, ISI, Google ScholarBuddemeier R. W.& Fautin D. G. . 1993Coral bleaching as an adaptive mechanism. Bioscience 43, 320–326. (doi:10.2307/1312064). Crossref, ISI, Google ScholarCarroll S. P., Hendry A. P., Reznick D. N.& Fox C. W. . 2007Evolution on ecological time-scales. Funct. Ecol. 21, 387–393. (doi:10.1111/j.1365-2435.2007.01289.x). Crossref, ISI, Google ScholarDonner S. D., Knutson T. R.& Oppenheimer M. . 2007Model-based assessment of the role of human-induced climate change in the 2005 Caribbean coral bleaching event. Proc. Natl Acad. Sci. USA 104, 5483–5488. (doi:10.1073/pnas.0610122104). Crossref, PubMed, ISI, Google ScholarDunne R. P. . 2008The use of remotely sensed solar radiation data in modelling susceptibility of coral reefs to environmental stress: Comment on Maina et al. [Ecol. Model.212 (2008) 180–199]. Ecol. Model. 218, 188–191. (doi:10.1016/j.ecolmodel.2008.04.004). Crossref, ISI, Google ScholarDunne R. P.& Brown B. E. . 2001The influence of solar radiation on bleaching of shallow water reef corals in the Andaman Sea, 1993–1998. Coral Reefs 20, 201–210. Crossref, ISI, Google ScholarEdmunds P. J.& Gates R. D. . 2008Acclimatization in tropical reef corals. Mar. Ecol. Prog. Ser. 361, 307–310. (doi:10.3354/meps07556). Crossref, ISI, Google ScholarEndler J. A. . 1986Natural selection in the wild. Princeton, NJ: Princeton University Press. Google ScholarGhil M., 2002Advanced spectral methods for climatic time series. Rev. Geophys. 40, 1–41. (doi:10.1029/2000RG000092). Crossref, ISI, Google ScholarGleeson M. W.& Strong A. E. . 1995Applying MCSST to coral reef bleaching. Adv. Space Res. 16, (10)151–(10)154. Crossref, ISI, Google ScholarGlynn P. W. . 1993Coral reef bleaching: ecological perspectives. Coral Reefs 12, 1–17. (doi:10.1007/BF00303779). Crossref, ISI, Google ScholarGlynn P. W., Maté J. L., Baker A. C.& Calderón M. O. . 2001Coral bleaching and mortality in Panama and Ecuador during the 1997–1998 El Niño-Southern Oscillation event: spatial/temporal patterns and comparisons with the 1982–1983 event. Bull. Mar. Sci. 69, 79–109. ISI, Google ScholarGrottoli A. G., Rodrigues L. J.& Juarez C. . 2004Lipids and stable carbon isotopes in two species of Hawaiian corals, Porites compressa and Montipora verrucosa, following a bleaching event. Mar. Biol. 145, 621–631. Crossref, ISI, Google ScholarGrottoli A. G., Rodrigues L. J.& Palardy J. E. . 2006Heterotrophic plasticity and resilience in bleached corals. Nature 440, 1186–1189. (doi:10.1038/nature04565). Crossref, PubMed, ISI, Google ScholarHoegh-Guldberg O. . 1999Climate change, coral bleaching and the future of the world's coral reefs. Mar. Fresh. Res. 50, 839–866. (doi:10.1071/MF99078). Crossref, ISI, Google ScholarHoegh-Guldberg O., Jones R. J., Ward S.& Loh W. K. . 2002Is coral bleaching really adaptive?Nature 415, 601–602. (doi:10.1038/415601a). Crossref, PubMed, ISI, Google Scholar- IPCC (Intergovernmental Panel on Climate Change). 2007The fourth assessment report of the IPCC. Cambridge, UK: Cambridge University Press. Google Scholar
Jones R. J. . 2008Coral bleaching, bleaching-induced mortality, and the adaptive significance of the bleaching response. Mar. Biol. 154, 65–80. (doi:10.1007/s00227-007-0900-0). Crossref, ISI, Google ScholarKleypas J. A., Danabasoglu G.& Lough J. M. . 2008Potential role of the ocean thermostat in determining regional differences in coral reef bleaching events. Geophys. Res. Lett. 35, L03613. (doi:10.1029/2007GL032257). Crossref, ISI, Google ScholarLau K. M.& Wu H. T. . 2003Warm rain processes over tropical oceans and climate implications. Geophys. Res. Lett. 30, 2290. (doi:10.1029/2003GL018567). Crossref, ISI, Google ScholarLau K. M., Wu H. T., Sud Y. C.& Walker G. K. . 2005Effects of cloud microphysics on tropical atmospheric hydrologic processes and intraseasonal variability. J. Clim. 18, 4731–4751. (doi:10.1175/JCLI3561.1). Crossref, ISI, Google ScholarLoya Y., Sakai K., Yamazato K., Nakano Y., Sambali H.& van Woesik R. . 2001Coral bleaching: the winners and the losers. Ecol. Lett. 4, 122–131. (doi:10.1046/j.1461-0248.2001.00203.x). Crossref, ISI, Google ScholarMaina J., Venus V., McClanahan T. R.& Ateweberhan M. . 2008Modelling susceptibility of coral reefs to environmental stress using remote sensing data and GIS models. Ecol. Model. 212, 180–199. (doi:10.1016/j.ecolmodel.2007.10.033). Crossref, ISI, Google ScholarMantua N. J., Hare S. R., Zhang Y., Wallace J. M.& Francis R. C. . 1997A Pacific interdecadal climate oscillation with impacts on salmon production. Bull. Am. Met. Soc. 78, 1069–1079. Crossref, ISI, Google ScholarMaynard J. A., Anthony K. R. N., Marshall P. A.& Masiri I. . 2008Major bleaching events can lead to increased thermal tolerance in corals. Mar. Biol. 155, 173–182. (doi:10.1007/s00227-008-1015-y). Crossref, ISI, Google ScholarMumby P. J., Chisholm J. R. M., Edwards A. J., Andrefouet S.& Jaubert J. . 2001Cloudy weather may have saved Society Island reef corals during the 1998 ENSO event. Mar. Ecol. Prog. Ser 222, 209–216. (doi:10.3354/meps222209). Crossref, ISI, Google ScholarPenland L., Kloulechad J., Idip D.& van Woesik R. . 2004Coral spawning in the western Pacific Ocean is related to solar insolation: evidence of multiple spawning events in Palau. Coral Reefs 23, 133–140. Crossref, ISI, Google ScholarPodestá G. P.& Glynn P. W. . 1997Sea surface temperature variability in Panamá and Galápagos: Extreme temperatures causing coral bleaching. J. Geophys. Res. 102, 15 749–15 759. (doi:10.1029/96JC03557). Crossref, ISI, Google ScholarPower S., Casey T., Folland C., Colman A.& Mehta V. . 1999Inter-decadal modulation of the impact of ENSO on Australia. Climate Dyn. 15, 319–324. Crossref, ISI, Google ScholarRayner N. A., Parker D. E.& Horton E. B. . 2003Global analyses of sea surface temperature, sea ice, and night marine air temperature since the late nineteenth century. J. Geophys. Res. 108, 4407. (doi:10.1029/2002JD002670). Crossref, ISI, Google ScholarSampayo E. M., Ridgway T., Bongaerts P.& Hoegh-Guldberg O. . 2008Bleaching susceptibility and mortality of corals are determined by fine-scale differences in symbiont type. Proc. Natl Acad. Sci. 105, 10 444–10 449. (doi:10.1073/pnas.0708049105). Crossref, ISI, Google ScholarSchroeder S. R.& McGuirk J. P. . 1998Widespread tropical atmospheric drying from 1979 to 1995. Geophys. Res. Lett. 25, 1301–1304. (doi:10.1029/98GL01029). Crossref, ISI, Google ScholarSud Y. C., Walker G. K., Zhou Y. P., Schmidt G. A., Lau M.& Cahalan R. F. . 2008Effects of doubled CO2 on tropical sea surface temperatures (SSTs) for onset of deep convection and maximum SST: Simulations based inferences. Geophys. Res. Lett. 35, L12707. (doi:10.1029/2008GL033872). ISI, Google ScholarTakahashi S., Nakamura T., Sakamizu M., van Woesik R.& Yamasaki H. . 2004Repair machinery of symbiotic photosynthesis as the primary target of heat stress for reef-building corals. Plant Cell Physiol. 45, 251–255. (doi:10.1093/pcp/pch028). Crossref, PubMed, ISI, Google ScholarThompson J. N. . 1998Rapid evolution as an ecological process. Trends Ecol. Evol. 13, 329–332. (doi:10.1016/S0169-5347(98)01378-0). Crossref, PubMed, ISI, Google Scholarvan Woesik R. . 2001Coral bleaching: transcending spatial and temporal scales. Trends Ecol. Evol. 16, 119–121. (doi:10.1016/S0169-5347(00)02083-8). Crossref, Google ScholarVecchi G. A., Clement A.& Soden B. J. . 2008Examining the tropical Pacific's response to global warming. Eos Trans. AGU 89, 81–83. (doi:10.1029/2008EO090002). Crossref, Google ScholarWallace C. C. . 1985Reproduction, recruitment and fragmentation in nine sympatric species of the coral genus. Acropora. Marine Biol. 88, 217–233. (doi:10.1007/BF00392585). Crossref, ISI, Google ScholarWilkinson C. (ed.) 1998Status of coral reefs of the world. Townsville, Australia: Australian Institute of Marine Sciences. Google ScholarWinter A., Appeldoorn R. S., Bruckner A., Williams E. H.& Goenaga C. . 1998Sea surface temperatures and coral reef bleaching off La Parguera, Puerto Rico (northeastern Caribbean Sea). Coral Reefs 17, 377–382. (doi:10.1007/s003380050143). Crossref, ISI, Google ScholarZhang X., Sheng J.& Shabbar A. . 1998Modes of interannual and interdecadal variability of Pacific SST. J. Clim. 11, 2556–2569. Crossref, ISI, Google ScholarZhang Y., Wallace J. M.& Battisti D. S. . 1997ENSO-like interdecadal variability: 1900–1993. J. Clim. 10, 1004–1020. Crossref, ISI, Google Scholar



