Coral Reefs

, Volume 38, Issue 4, pp 713–719 | Cite as

Back-to-back coral bleaching events on isolated atolls in the Coral Sea

  • Hugo B. HarrisonEmail author
  • Mariana Álvarez-Noriega
  • Andrew H. Baird
  • Scott F. Heron
  • Chancey MacDonald
  • Terry P. Hughes


Severe bleaching events caused by marine heat waves over the past four decades have now affected almost every coral reef ecosystem in the world. These recurring events have led to major losses of coral cover, with adverse consequences for tropical reef ecosystems and the people who depend on them. Here, we document two consecutive and widespread coral bleaching events on remote atolls in the Coral Sea in 2016 and 2017. In each year, the proportion of colonies that bleached was strongly related to heat exposure (measured as degree heating weeks, DHW, °C-weeks), depth and coral assemblage structure. Bleaching was more severe at higher DHW exposure and at sites with a higher proportion of susceptible taxa. Bleaching was also lower at 6 m than at 2 m depth. Despite the severe bleaching in 2016 on reefs in the central section of the Coral Sea Marine Park, total coral cover was not significantly reduced by 2017, suggesting that most bleached corals survived. Moreover, bleaching was less severe in 2017 despite a higher exposure to heat stress. These results indicate that while the isolation of these oceanic reefs provides no refuge from bleaching, low nutrient levels, high wave energy and proximity to cooler deeper waters may make coral on these reefs more resistant to bleaching-induced mortality.


Bleaching Coral reefs Marine heat wave Coral Sea Coral Sea Marine Park 



This research was jointly funded by the Director of National Parks, Australia, an ACR Discovery Early Career Research Award to HBH (DE160101141) and the ARC Centre of Excellence for Coral Reef Studies. This research was conducted in the Coral Sea Marine Park under Permit No. CMR-16-000394 and CMR-16-000443. The authors wish to thank the relevant staff at Parks Australia, with particular mention given to Andy Warmbrunn, Jennifer Hoy, Bianca Priest, Samantha Fox and Jason Mundy. We thank Cpt Peter Sayre, Glenn Percy and the crew of the MV Phoenix for their assistance in the field. We are grateful to Thomas DeCarlo for producing Fig. 1b, c and two anonymous reviewers for their thoughtful comments. The findings and views expressed are those of the authors and do not necessarily represent the views of Parks Australia, the Director of National Parks or the Australian Government. The scientific results and conclusions, as well as any views or opinions expressed herein, are those of the authors and do not necessarily reflect the views of NOAA or the US Department of Commerce.

Authors’ contribution

M.A.-N., A.H.B., H.B.H. and C.MacD. collected the field observations and S.F.H. collated the NOAA temperature data; A.H.B. and H.B.H. planned the study, and all authors analysed the data and wrote the paper.


Funding was provided by the Director of National Parks, Parks Australia, an ACR Discovery Early Career Research Award to H.B.H. (DE160101141) and the ARC Centre of Excellence for Coral Reef Studies.

Compliance with ethical standards

Conflict of interest

On behalf of all authors, the corresponding author states that there is no conflict of interest.

Supplementary material

338_2018_1749_MOESM1_ESM.docx (7 mb)
Supplementary material 1 (DOCX 7207 kb)


  1. Ainsworth TD, Heron SF, Ortiz JC, Mumby PJ, Grech A, Ogawa D, Eakin CM, Leggat W (2016) Climate change disables coral bleaching protection on the Great Barrier Reef. Science 352:338–342CrossRefPubMedGoogle Scholar
  2. Ayling AM, Ayling AL (1985) Report on a preliminary survey of the Lihou and Caringua/Herald Nature Reserves. Australian National Parks and Wildlife ServiceGoogle Scholar
  3. Baird AH, Madin JS, Álvarez-Noriega M, Fontoura L, Kerry J, Precoda K, Torres-Pulliza D, Woods RM, Zawada K, Hughes TP (2018) A decline in bleaching suggests that depth can provide a refuge from global warming in most coral taxa. Mar Ecol Prog Ser 603:257–264CrossRefGoogle Scholar
  4. Baker AC, Glynn PW, Riegl B (2008) Climate change and coral reef bleaching: An ecological assessment of long-term impacts, recovery trends and future outlook. Estuar Coast Shelf Sci 80:435–471CrossRefGoogle Scholar
  5. Bates D, Maechler M, Bolker B, Walker S (2015) Fitting Linear Mixed-Effects Models Using lme4. J Stat Softw 67:1–48CrossRefGoogle Scholar
  6. Brown BE (1997) Coral bleaching: causes and consequences. Coral Reefs 16:S129–S138CrossRefGoogle Scholar
  7. Brown BE, Dunne RP, Goodson MS, Douglas AE (2000) Bleaching patterns in reef corals. Nature 404:142–143CrossRefPubMedGoogle Scholar
  8. Ceccarelli D, Choat JH, Ayling AM, Richards Z, van Herwerden L, Ayling A, Ewels G, Hobbs J–P, Cuff B (2008) Coringa-Herald National Nature Reserve Marine Survey—2007. Report to the Department of the Environment, Water, Heritage and the Arts by C&R Consulting and James Cook UniversityGoogle Scholar
  9. Ceccarelli D, Ayling AM, Choat JH, Ayling AL, Williamson DH, Cuff B (2009) Lihou Reef National Nature Reserve Marine Survey—October 2008. Report to the Department of the Environment, Water, Heritage and the Arts by C&R Consulting Pty Ltd.Google Scholar
  10. Ceccarelli DM, McKinnon AD, Andrefouet S, Allain V, Young J, Gledhill DC, Flynn A, Bax NJ, Beaman R, Borsa P, Brinkman R, Bustamante RH, Campbell R, Cappo M, Cravatte S, D’Agata S, Dichmont CM, Dunstan PK, Dupouy C, Edgar G, Farman R, Furnas M, Garrigue C, Hutton T, Kulbicki M, Letourneur Y, Lindsay D, Menkes C, Mouillot D, Parravicini V, Payri C, Pelletier B, de Forges BR, Ridgway K, Rodier M, Samadi S, Schoeman D, Skewes T, Swearer S, Vigliola L, Wantiez L, Williams A, Williams A, Richardson AJ (2013) The Coral Sea: Physical Environment, Ecosystem Status and Biodiversity Assets. Adv Mar Biol 66:213–290CrossRefPubMedGoogle Scholar
  11. Done T, Whetton P, Jones R, Berkelmans R, Lough JM, Skirving W, Wooldridge S (2003) Global Climate Change and Coral Bleaching on the Great Barrier Reef. Queensland Government Department of Natural Resources and MinesGoogle Scholar
  12. Fisk DA, Done TJ (1985) Taxonomic and bathymetric patterns of bleaching in corals, Myrmidon Reef (Queensland). Proc Fifth Inter Coral Reef Congress 6:149–154Google Scholar
  13. Gilmour JP, Smith LD, Heyward AJ, Baird AH, Pratchett MS (2013) Recovery of an isolated coral reef system following severe disturbance. Science 340:69–71CrossRefPubMedGoogle Scholar
  14. Gleason MG (1993) Effects of Disturbance on Coral Communities - Bleaching in Moorea, French-Polynesia. Coral Reefs 12:193–201CrossRefGoogle Scholar
  15. Glynn PW (1984) Widespread coral mortality and the 1982-83 El Nino warming event. Environ Conserv 11:133–146CrossRefGoogle Scholar
  16. Heron SF, Maynard JA, van Hooidonk R, Eakin CM (2016) Warming Trends and Bleaching Stress of the World’s Coral Reefs 1985-2012. Sci Rep 6:38402CrossRefPubMedPubMedCentralGoogle Scholar
  17. Hughes TP, Kerry JT, Álvarez-Noriega M, Álvarez-Romero JG, Anderson KD, Baird AH, Babcock RC, Beger M, Bellwood DR, Berkelmans R, Bridge TC, Butler IR, Byrne M, Cantin NE, Comeau S, Connolly SR, Cumming GS, Dalton SJ, Diaz-Pulido G, Eakin CM, Figueira WF, Gilmour JP, Harrison HB, Heron SF, Hoey AS, Hobbs J-PA, Hoogenboom MO, Kennedy EV, C-y Kuo, Lough JM, Lowe RJ, Liu G, McCulloch MT, Malcolm HA, McWilliam MJ, Pandolfi JM, Pears RJ, Pratchett MS, Schoepf V, Simpson T, Skirving WJ, Sommer B, Torda G, Wachenfeld DR, Willis BL, Wilson SK (2017) Global warming and recurrent mass bleaching of corals. Nature 543:373–377CrossRefPubMedGoogle Scholar
  18. Hughes TP, Anderson KD, Connolly SR, Heron SF, Kerry JT, Lough JM, Baird AH, Baum JK, Berumen ML, Bridge TC, Claar DC, Eakin CM, Gilmour JP, Graham NAJ, Harrison HB, Hobbs J-PA, Hoey A, Hoogenboom M, Lowe RJ, McCulloch MT, Pandolfi JM, Pratchett M, Schoepf V, Torda G, Wilson SK (2018a) Spatial and temporal patterns of mass bleaching of corals in the Anthropocene. Science 359:80–83CrossRefPubMedGoogle Scholar
  19. Hughes TP, Kerry JT, Baird AH, Connolly SR, Dietzel A, Eakin CM, Heron SF, Hoey AS, Hoogenboom MO, Liu G, McWilliam MJ, Pears RJ, Pratchett MS, Skirving WJ, Stella JS, Torda G (2018b) Global warming transforms coral reef assemblages. Nature doi:10.1038/s41586-018-0041-2Google Scholar
  20. Kennedy EV, Perry CT, Halloran PR, Iglesias-Prieto R, Schönberg CHL, Wisshak M, Form AU, Carricart-Ganivet JP, Fine M, Eakin CM, Mumby PJ (2013) Avoiding Coral Reef Functional Collapse Requires Local and Global Action. Curr Biol 23:912–918CrossRefPubMedGoogle Scholar
  21. King AD, Karoly DJ, Henley BJ (2017) Australian climate extremes at 1.5 degrees C and 2 degrees C of global warming. Nat Clim Change 7:412–416CrossRefGoogle Scholar
  22. Liu G, Heron S, Eakin CM, Muller-Karger FE, Vega-Rodriguez M, Guild LS et al (2014) Reef-Scale Thermal Stress Monitoring of Coral Ecosystems: New 5-km Global Products from NOAA Coral Reef Watch. Remote Sens 6:11579–11606CrossRefGoogle Scholar
  23. Lough JM, Anderson KD, Hughes TP (2018) Increasing thermal stress for tropical coral reefs: 1871–2017. Scientific Reports 8:6079CrossRefPubMedPubMedCentralGoogle Scholar
  24. Loya Y (1972) Community structure and species diversity of hermatypic corals at Eilat, Red Sea. Mar Biol 13:100–112CrossRefGoogle Scholar
  25. Loya Y, Sakai K, Yamazato K, Nakano Y, Sambali H, van Woesik R (2001) Coral bleaching: the winners and the losers. Ecol Lett 4:122–131CrossRefGoogle Scholar
  26. Marshall PA, Baird AH (2000) Bleaching of corals on the Great Barrier Reef: differential susceptibilities among taxa. Coral Reefs 19:155–163CrossRefGoogle Scholar
  27. McClanahan TR, Baird AH, Marshall PA, Toscano MA (2004) Comparing bleaching and mortality responses of hard corals between southern Kenya and the Great Barrier Reef, Australia. Mar Pollut Bull 48:327–335CrossRefGoogle Scholar
  28. McClanahan T, Weil E, Cortés J, Baird AH, Ateweberhan M (2009) Consequences of coral bleaching for sessile reef organisms. In: van Oppen MJH, Lough JM (eds) Ecological Studies: Coral Bleaching: Patterns, Processes, Causes and Consequences. Springer-Verlag, Berlin, pp 121–138CrossRefGoogle Scholar
  29. Mellin C, MacNeil MA, Cheal AJ, Emslie MJ, Caley JM (2016) Marine protected areas increase resilience among coral reef communities. Ecol Lett 19:629–637CrossRefPubMedGoogle Scholar
  30. Muir PR, Marshall PA, Abdulla A, Aguirre JD (2017) Species identity and depth predict bleaching severity in reef-building corals: shall the deep inherit the reef? Proc Royal Soc B 284:20171551CrossRefGoogle Scholar
  31. Mumby PJ, Chisholm JRM, Edwards AJ, Andrefouet S, Jaubert J (2001) Cloudy weather may have saved Society Island reef corals during the 1998 ENSO event. Mar Ecol Prog Ser 222:209–216CrossRefGoogle Scholar
  32. Nakamura T, van Woesik R, Yamasaki H (2005) Photoinhibition of photosynthesis is reduced by water flow in the reef-building coral Acropora digitifera. Mar Ecol Prog Ser 301:109–118CrossRefGoogle Scholar
  33. Oliver ECJ, Donat MG, Burrows MT, Moore PJ, Smale DA, Alexander LV, Benthuysen JA, Feng M, Gupta Sen A, Hobday AJ, Holbrook NJ, Perkins-Kirkpatrick SE, Scannell HA, Straub SC, Wernberg T (2018) Longer and more frequent marine heatwaves over the past century. Nat Commun 9:227CrossRefGoogle Scholar
  34. Oxley WG, Emslie M, Muir P, Thompson AA (2004) Marine surveys undertaken in the Lihou Reef Nature Reserve, March 2004. Department of the Environment and HeritageGoogle Scholar
  35. R Core Team (2016) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria.
  36. Richards CL, Boruta M, Bossdorf O, Coon CAC, Foust CM, Hughes AR, Kilvitis HJ, Liebl AL, Nicotra AB, Pigliucci M, Robertson MH, Schrey AW (2013) Epigenetic mechanisms of phenotypic plasticity. Integr Comp Biol 53:E179–E179Google Scholar
  37. Riegl B, Piller WE (2003) Possible refugia for reefs in times of environmental stress. Int J Earth Sci 92:520–531CrossRefGoogle Scholar
  38. Sandin SA, Smith JE, DeMartini EE, Dinsdale EA, Donner SD, Friedlander AM, Konotchick T, Malay M, Maragos JE, Obura D, Pantos O, Paulay G, Richie M, Rohwer F, Schroeder RE, Walsh S, Jackson JBC, Knowlton N, Sala E (2008) Baselines and Degradation of Coral Reefs in the Northern Line Islands. PLoS ONE 3:e1548CrossRefPubMedPubMedCentralGoogle Scholar
  39. van Hooidonk R, Maynard JA, Planes S (2013) Temporary refugia for coral reefs in a warming world. Nat Clim Change 3:508–511CrossRefGoogle Scholar
  40. Veron JEN (2000) Corals of the world. Australian Institute of Marine Science, TownsvilleGoogle Scholar
  41. Wiedenmann J, D’Angelo C, Smith EG, Hunt AN, Legiret F-E, Postle AD, Achterberg EP (2013) Nutrient enrichment can increase the susceptibility of reef corals to bleaching. Nat Clim Change 3:160–164CrossRefGoogle Scholar
  42. Williams GJ, Knapp IS, Maragos JE, Davy SK (2010) Modeling patterns of coral bleaching at a remote Central Pacific atoll. Mar Pollut Bull 60:1467–1476CrossRefPubMedGoogle Scholar
  43. Wooldridge SA (2009) Water quality and coral bleaching thresholds: Formalising the linkage for the inshore reefs of the Great Barrier Reef, Australia. Marine Pollution Bulletin 58:745–751CrossRefPubMedGoogle Scholar
  44. Wooldridge SA, Done TJ (2009) Improved water quality can ameliorate effects of climate change on corals. Ecol Appl 19:1492–1499CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Australian Research Council Centre of Excellence for Coral Reef StudiesJames Cook UniversityTownsvilleAustralia
  2. 2.College of Science and EngineeringJames Cook UniversityTownsvilleAustralia
  3. 3.Coral Reef WatchUS National Oceanic and Atmospheric AdministrationCollege ParkUSA
  4. 4.ReefSenseTownsvilleAustralia
  5. 5.Marine Geophysical Laboratory, College of Science, Technology and EngineeringJames Cook UniversityTownsvilleAustralia

Personalised recommendations