Chinese Geographical Science

, Volume 25, Issue 2, pp 159–173 | Cite as

Spatial and temporal variability of thermal stress to China’s coral reefs in South China Sea

  • Xiuling Zuo
  • Fenzhen Su
  • Wenzhou Wu
  • Zhike Chen
  • Wei Shi


Coral bleaching, caused by elevated sea surface temperature (SST), is occurring more frequently and seriously worldwide. Due to the lack of field observations, we understand little about the large-scale variability of thermal stress in the South China Sea (SCS) and its effect on China’s coral reefs. This paper used 4-km high resolution gap-filled SST (FilledSST) data and thermal stress data related to coral bleaching derived from Coral Reef Temperature Anomaly Database (CoRTAD) to quantify the spatial and temporal characteristics of chronic thermal stress and acute thermal stress to China’s coral reefs in SCS from 1982 to 2009. We analyzed the trend of SST in summer and the thermal stress frequency, intensity and duration during this period. The results indicate that, as a chronic thermal stress, summer mean SST in SCS shows an average upward trend of 0.2 °C/decade and the spatial pattern is heterogeneous. Waters of Xisha Islands and Dongsha Islands of the northern SCS are warming faster through time compared to Zhongsha Islands and Nansha Islands sea areas of the southern SCS. High frequency bleaching related thermal stress events for these reefs are seen in the area to the northwest of Luzon Island. Severe anomaly thermal stress events are more likely to occur during the subsequent year of the El Niño year for these coral reefs. Besides, the duration of thermal stress varies considerably by anomaly year and by region.


coral reef sea surface temperature (SST) thermal stress El Niño-Southern Oscillation (ENSO) South China Sea (SCS) 


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  1. Aeby G S, Williams G J, Franklin E C et al., 2011. Patterns of coral disease across the Hawaiian archipelago: relating disease to environment. PLoS ONE, 6(5): e20370. doi:10.1371/journal.pone.0020370CrossRefGoogle Scholar
  2. Allen G R, Werner T B, 2002. Coral reef fish assessment in the ‘coral triangle’ of southeastern Asia. Environmental Biology of Fishes, 65: 209–214. doi:10.1023/A:1020093012502CrossRefGoogle Scholar
  3. Anthony K R N, Kline D I, Diaz-Pulido G et al., 2008. Ocean acidification causes bleaching and productivity loss in coral reef builders. Proceedings of the National Academy of Sciences of the United States of America, 105(45): 17442–17446. doi: 10.1073/pnas.0804478105CrossRefGoogle Scholar
  4. Arceo H O, Quibilan M C, Aliño P M et al., 2001. Coral bleaching in Philippine reefs: coincident evidences with mesoscale thermal anomalies. Bulletin of Marine Science, 69(2): 579–593.Google Scholar
  5. Arthur D, Vassilvitskii S, 2007. k-means++: the advantages of careful seeding. Proceedings of the 18th Annual ACM-SIAM Symposium on Discrete Algorithms. SODA 2007, 1027–1035.Google Scholar
  6. Baird A H, Marshall P A, 2002. Mortality, growth and reproduction in scleractinian corals following bleaching on the Great Barrier Reef. Marine Ecology Progress Series, 237: 133–141. doi: 10.3354/meps237133CrossRefGoogle Scholar
  7. Berkelmans R, De’ath G, Kininmonth S et al., 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-yCrossRefGoogle Scholar
  8. Burke L, Selig E, Spalding M, 2006. Reefs at Risk in Southeast Asia. Washington D C: World Resources Institute Press, 48.Google Scholar
  9. Carilli J E, Norris R D, Black B et al., 2010. Century-scale records of coral growth rates indicate that local stressors reduce coral thermal tolerance threshold. Global Change Biology, 16: 1247–1257. doi: 10.1111/j.1365-2486.2009.02043.xCrossRefGoogle Scholar
  10. Carricart-Ganivet J P, Cabanillas-Terán N, Cruz-Ortega I et al., 2012. Sensitivity of calcification to thermal stress varies among genera of massive reef-building corals. PLoS ONE, 7(3): e32859. doi: 10.1371/journal.pone.0032859CrossRefGoogle Scholar
  11. Carrigan A D, Puotinen M L, 2011. Assessing the potential for tropical cyclone induced sea surface cooling to reduce thermal stress on the world’s coral reefs. Geophysical Research Letters, 38: L23604. doi:10.1029/2011GL049722CrossRefGoogle Scholar
  12. Casey K S, Brandon T B, Cornillon P et al., 2010. The past, present and future of the AVHRR Pathfinder SST program. In: Barale V et al. (eds.). Oceanography from Space: Revisited. New York: Springer Press, 273–287.CrossRefGoogle Scholar
  13. Chang Genying, Huang Fupeng, Li Man et al., 2012. Public perception of climate change and their support of climate policy in China: based on global surveys and in comparison with USA. Scientia Geographica Sinica, 32(12): 1481–1487. (in Chinese)Google Scholar
  14. Chen T, Li S, Yu K et al., 2013. Increasing temperature anomalies reduce coral growth in the Weizhou Island, northern South China Sea. Estuarine, Coastal and Shelf Science, 130: 121–126. doi:10.1016/j.ecss.2013.05.009CrossRefGoogle Scholar
  15. Dai C F, Fan T Y, Wu C S, 1995. Coral fauna of Tungsha Tao (Pratas Islands). Acta Oceanographica Taiwanica, 34: 1–16.Google Scholar
  16. Dai Changfeng, 2010. Biotic reefs and reef biotops in Taiwan area. Journal of Palaeogeography, 12(5): 565–576. (in Chinese)Google Scholar
  17. Fan T Y, Wei C, Fang L S, 2008a. Status of coral reef communities and reef restoration efforts at Dongsha Atoll, South China Sea. Available at: Google Scholar
  18. Fan T Y, Wu B J, Fang L S, 2008b. The heterogeneity of temperature change and coral bleaching during temperature abnormally warm in summer 2007. Available at: Google Scholar
  19. Fang G, Chen H, Wei Z et al., 2006. Trends and interannual variability of the South China Sea surface winds, surface height, and surface temperature in the recent decade. Journal of Geophysical Research, 111: C11S16. doi:10.1029/2005JC003276CrossRefGoogle Scholar
  20. Ferreira B P, Costa M B S F, Coxey M S et al., 2013. The effects of sea surface temperature anomalies on oceanic coral reef systems in the southwestern tropical Atlantic. Coral Reefs, 32: 441–454. doi: 10.1007/s00338-012-0992-yCrossRefGoogle Scholar
  21. Fu Xiumei, Wang Changyun, Shao Changlun et al., 2009. Investigation of the status of coral reef resources and medicinal research in China. I. coral reef resources and ecological functions. Periodical of Ocean University of China, 39(4): 676–684. (in Chinese)Google Scholar
  22. Furby K A, Bouwmeester J, Berumen M L, 2013. Susceptibility of central Red Sea corals during a major bleaching event. Coral Reefs, 32: 505–513. doi: 10.1007/s00338-012-0998-5CrossRefGoogle Scholar
  23. Glynn P W, 1993. Coral reef bleaching: ecological perspectives. Coral Reefs, 12: 1–17. doi: 10.1007/BF00303779CrossRefGoogle Scholar
  24. Glynn P W, Cortés-Núñez J, Guzmán-Espinal H M et al., 1988. El Niño (1982-83) associated coral mortality and relationship to sea surface temperature deviations in the tropical eastern Pacific. Proceedings of the 6th International Coral Reef Symposium. Townsville, Australia, 3: 231–243.Google Scholar
  25. Goreau T J, Hayes R L, 1994. Coral bleaching and ocean ‘hot spots’. Ambio, 23: 176–180.Google Scholar
  26. Goreau T, McClanahan T, Hayes R et al., 2000. Conservation of coral reefs after the 1998 global bleaching event. Conservation Biology, 14(1): 5–15. doi: 10.1046/j.1523-1739.2000.00011.xCrossRefGoogle Scholar
  27. Guest J R, Baird A H, Maynard J A et al., 2012. Contrasting patterns of coral bleaching susceptibility in 2010 suggest an adaptive response to thermal stress. PLoS ONE, 7(3): e33353. doi: 10.1371/journal.pone.0033353CrossRefGoogle Scholar
  28. Heron S F, Willis B L, Skirving W J et al., 2010. Summer hot snaps and winter conditions: modelling white syndrome outbreaks on Great Barrier Reef corals. PLoS ONE, 5(8): e12210. doi: 10.1371/journal.pone.0012210CrossRefGoogle Scholar
  29. Hoegh-Guldberg O, 1999. Climate change, coral bleaching and the future of the world’s coral reefs. Marine Freshwater Research, 50: 839–866. doi: 10.1071/MF99078CrossRefGoogle Scholar
  30. Hongo C, Yamano H, 2013. Species-specific responses of corals to bleaching events on anthropogenically turbid reefs on Okinawa Island, Japan, over a 15-year period (1995–2009). PLoS ONE, 8(4): e60952. doi: 10.1371/journal.pone.0060952CrossRefGoogle Scholar
  31. Huang Zhuo, Xu Haiming, Du Yan et al., 2009. Two sea-surface warming events in the South China Sea during and after El Niño. Journal of Tropical Oceanography, 28(5): 49–55. (in Chinese)Google Scholar
  32. Hughes T P, Huang H, Young M A L, 2012. The wicked problem of China’s disappearing coral reefs. Conservation Biology, 27(2): 261–269. doi: 10.1111/j.1523-1739.2012.01957.xCrossRefGoogle Scholar
  33. IPCC (Intergovernmental Panel on Climate Change), 2013. Climate change 2013: the physical science basis. In: Stocker T F et al. (eds.) Contribution of Working Group I to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge: Cambridge University Press.Google Scholar
  34. Kerr R A, 1999. Big El Niños ride the back of slower climate change. Science, 283(5405): 1108–1109. doi: 10.1126/science.283.5405.1108CrossRefGoogle Scholar
  35. Klein S A, Brian J S, Ngar-Cheung L, 1999. Remote sea surface temperature variations during ENSO: evidence for a tropical atmospheric bridge. Journal of Climate, 12: 917–932. doi:10.1175/1520-0442(1999)012〈0917:RSSTVD〉2.0.CO;2CrossRefGoogle Scholar
  36. Kleypas J A, McManus J W, Menez L A B, 1999. Environmental limits to coral reef development: where do we draw the line? American Zoologist, 39(1): 146–159. doi: 10.1093/icb/39.1.146Google Scholar
  37. Langdon C, Takahashi T, Sweeney C et al., 2000. Effect of calcium carbonate saturation state on the calcification rate of an experimental coral reef. Global Biogeochemical Cycles, 14(2): 639–654. doi:10.1029/1999GB001195CrossRefGoogle Scholar
  38. Li S, Yu K F, Chen T R et al., 2011. Assessment of coral bleaching using symbiotic zooxanthellae density and satellite remote sensing data in the Nansha Islands, South China Sea. Chinese Science Bulletin, 56(10): 1031–1037. doi: 10.1007/s11434-011-4390-6CrossRefGoogle Scholar
  39. Li X, Liu S, Huang H et al., 2012. Coral bleaching caused by an abnormal water temperature rise at Luhuitou fringing reef, Sanya Bay, China. Aquatic Ecosystem Health & Management, 15(2): 227–233. doi:10.1080/14634988.2012.687651Google Scholar
  40. Liu G, Strong A E, Skirving W, 2003. Remote sensing of sea surface temperatures during 2002 Barrier Reef coral bleaching. Eos, Transactions American Geophysical Union, 84(15): 137–144. doi:10.1029/2003EO150001CrossRefGoogle Scholar
  41. Liu Y, Liu W, Peng Z et al., 2009. Instability of seawater pH in the South China Sea during the mid-late Holocene: evidence from boron isotopic composition of corals. Geochimica et Cosmochimica Acta, 73: 1264–1272. doi:10.1016/j.gca.2008.11.034CrossRefGoogle Scholar
  42. Logan C A, Dunne J P, Eakin C M et al., 2014. Incorporating adaptive responses into future projections of coral bleaching. Global Change Biology, 20(1): 125–139. doi: 10.1111/gcb.12390CrossRefGoogle Scholar
  43. Lough J M, 2000. 1997–98: unprecedented thermal stress to coral reefs? Geophysical Research Letters, 27(23): 3901–3904. doi:10.1029/2000GL011715CrossRefGoogle Scholar
  44. Lough J M, 2012. Small change, big difference: sea surface temperature distributions for tropical coral reef ecosystems, 1950–2011. Journal of Geophysical Research, 117: C09018. doi:10.1029/2012JC008199CrossRefGoogle Scholar
  45. Ma Guangren, 2012. Valuing wetlands as natural infrastructure to safeguard human development. Wetland Science, 10(4): 385–388. (in Chinese)Google Scholar
  46. McClanahan T R, Baird A H, Marshall P A et al., 2004. Comparing bleaching and mortality responses of hard corals between southern Kenya and the Great Barrier Reef, Australia. Marine Pollution Bulletin, 48: 327–335. doi:10.1016/j.marpolbul.2003.08.024CrossRefGoogle Scholar
  47. McManus J W, 1994. The Sprately Islands: a marine park? AMBIO, 23: 181–186.Google Scholar
  48. McWilliams J P, Côté I M, Gill J A et al., 2005. Accelerating impacts of temperature-induced coral bleaching in the Caribbean. Ecology, 86(8): 2055–2060. doi:10.1890/04-1657CrossRefGoogle Scholar
  49. Meissner K J, Lippmann T, Gupta A S, 2012. Large-scale stress factors affecting coral reefs: open ocean sea surface temperature and surface seawater aragonite saturation over the next 400 years. Coral Reefs, 31: 309–319. doi: 10.1007/s00338-011-0866-8CrossRefGoogle Scholar
  50. Moberg F, Folke C, 1999. Ecological goods and services of coral reef ecosystems. Ecological Economics, 29: 215–233. doi: 10.1016/S0921-8009(99)00009-9CrossRefGoogle Scholar
  51. Mora C, Ginsburg R, 2007. A clear human footprint on the Caribbean coral reefs. Proceedings of the Royal Society B, 275: 767–773. doi:10.1098/rspb.2007.1472CrossRefGoogle Scholar
  52. Morton B, Blackmore G, 2001. South China Sea. Marine Pollution Bulletin, 42(12): 1236–1263. doi: 10.1016/S0025-326X(01)00240-5CrossRefGoogle Scholar
  53. Negri A P, Flores F, Röthig T et al., 2011. Herbicides increase the vulnerability of corals to rising sea surface temperature. Limnology and Oceanography, 56(2): 471–485. doi:10.4319/lo.2011.56.2.0471CrossRefGoogle Scholar
  54. Negri A P, Hoogenboom M O, 2011. Water contamination reduces the tolerance of coral larvae to thermal stress. PLoS ONE, 6(5): e19703. doi:10.1371/journal.pone.0019703CrossRefGoogle Scholar
  55. Obura D, Mangubhai S, 2011. Coral mortality associated with thermal fluctuations in the Phoenix Islands, 2002–2005. Coral Reefs, 30: 607–619. doi: 10.1007/s00338-011-0741-7CrossRefGoogle Scholar
  56. Peñaflor E L, Skirving W J, Strong A E et al., 2009. Sea-surface temperature and thermal stress in the Coral Triangle over the past two decades. Coral Reefs, 28: 841–850. doi: 10.1007/s00338-009-0522-8CrossRefGoogle Scholar
  57. Podestá G P, Glynn P W, 2001. The 1997–98 El Niño event in Panama and Galápagos: an update of thermal stress indices relative to coral bleaching. Bulletin of Marine Science, 69(1): 43–59.Google Scholar
  58. Prada C, Weil E, Yoshioka P M, 2010. Octocoral bleaching during unusual thermal stress. Coral Reefs, 29: 41–45. doi: 10.1007/s00338-009-0547-zCrossRefGoogle Scholar
  59. Randall C J, Szmant A M, 2009. Elevated temperature affects development, survivorship, and settlement of the elkhorn coral, Acropora palmata (Lamarck 1816). The Biological Bulletin, 217(3): 269–282. doi: 10.1143/JJAP.43.5922Google Scholar
  60. Selig E R, Casey K S, Bruno J F, 2010. New insights into global patterns of ocean temperature anomalies: implications for coral reef health and management. Global Ecology and Biogeography, 19: 397–411. doi: 10.1111/j.1466-8238.2009.00522.xCrossRefGoogle Scholar
  61. Shang Erping, Bai Wanqi, 2012. A review on the studies of wetland vulnerability assessment. Wetland Science, 10(3): 378–384. (in Chinese)Google Scholar
  62. Soong K, Dai C F, Lee C P, 2002. Status of Pratas Atoll in South China Sea. Proceedings of the 4th Conference on the Protected Areas of East Asia. Taipei, 739–742.Google Scholar
  63. Toscano M A, Liu G, Guch I C et al., 2000. Improved prediction of coral bleaching using high-resolution HotSpot anomaly mapping. 9th International Coral Reef Symposium. Bali, Indonesia, 2: 1143–1147.Google Scholar
  64. Wang C, Wang W, Wang D et al., 2006. Interannual variability of the South China Sea associated with El Niño. Journal of Geophysical Research, 111: C03023. doi:10.1029/2005JC003333Google Scholar
  65. Weeks S J, Anthony K R N, Bakun A et al., 2008. Improved predictions of coral bleaching using seasonal baselines and higher spatial resolution. Limnology and Oceanography, 53(4): 1369–1375. doi:10.4319/lo.2008.53.4.1369CrossRefGoogle Scholar
  66. Wilkinson C, 1998. The 1997–1998 mass bleaching event around the world. In: Wilkinson C et al. (eds.) Status of Coral Reefs of the World: 1998. Townsville: Australian Institute of Marine Science Press, 12.Google Scholar
  67. Worum F P, Carricart-Ganivet J P, Benson L et al., 2007. Simulation and observations of annual density banding in skeletons of Montastraea (Cnidaria: Scleractinia) growing under thermal stress associated with ocean warming. Limnology and Oceanography, 52(5): 2317–2323. doi:10.4319/lo.2007.52.5.2317CrossRefGoogle Scholar
  68. Yu K F, 2012. Coral reefs in the South China Sea: their response to and records on past environmental changes. Science China Earth Sciences, 55(8): 1217–1229. doi: 10.1007/s11430-012-4449-5CrossRefGoogle Scholar
  69. Yu K F, Zhao J X, Liu T S et al., 2004. High-frequency winter cooling and reef coral mortality during the Holocene climatic optimum. Earth and Planetary Science Letters, 224: 143–155. doi:10.1016/j.epsl.2004.04.036CrossRefGoogle Scholar
  70. Yu K, Zhao J, Shi Q et al., 2012. Recent massive coral mortality events in the South China Sea: was global warming and ENSO variability responsible? Chemical Geology, 320–321: 54–65. doi:10.1016/j.chemgeo.2012.05.028CrossRefGoogle Scholar
  71. Zhang Yaoguang, Liu Kai, Liu Guichun, 2012. The evolvement of the state maritime boundary in South China Sea by maps: China’s nine-dotted maritime boundary line in South China Sea. Scientia Geographica Sinica, 32(9): 1033–1040. (in Chinese)Google Scholar
  72. Zhao M X, Yu K F, Zhang Q M et al., 2014. Age structure of massive Porites lutea corals at Luhuitou fringing reef (northern South China Sea) indicates recovery following severe anthropogenic disturbance. Coral Reefs, 33: 39–44. doi: 10.1007/s00338-013-1109-yCrossRefGoogle Scholar

Copyright information

© Science Press, Northeast Institute of Geography and Agricultural Ecology, CAS and Springer-Verlag Berlin Heidelberg 2015

Authors and Affiliations

  • Xiuling Zuo
    • 1
    • 2
  • Fenzhen Su
    • 1
  • Wenzhou Wu
    • 1
    • 2
  • Zhike Chen
    • 3
  • Wei Shi
    • 1
  1. 1.State Key Laboratory of Resources and Environmental Information System, Institute of Geographic Sciences and Natural Resources ResearchChinese Academy of SciencesBeijingChina
  2. 2.University of Chinese Academy of SciencesBeijingChina
  3. 3.Heilongjiang Agricultural Reclamation SurveyDesign and Research InstituteHarbinChina

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