Thermal refugia against coral bleaching throughout the northern Red Sea

Tropical reefs have been impacted by thermal anomalies caused by global warming that induced coral bleaching and mortality events globally. However, there have only been very few recordings of bleaching within the Red Sea despite covering a latitudinal range of 15° and consequently it has been considered a region that is less sensitive to thermal anomalies. We therefore examined historical patterns of sea surface temperature (SST) and associated anomalies (1982-2012) and compared warming trends with a unique compilation of corresponding coral bleaching records from throughout the region. These data indicated that the northern Red Sea has not experienced mass bleaching despite intensive Degree Heating Weeks (DHW) of >15°C-weeks. Severe bleaching was restricted to the central and southern Red Sea where DHWs have been more frequent, but far less intense (DHWs <4°C-weeks). A similar pattern was observed during the 2015-2016 El Niño event during which time corals in the northern Red Sea did not bleach despite high thermal stress (i.e. DHWs >8°C-weeks), and bleaching was restricted to the central and southern Red Sea despite the lower thermal stress (DHWs < 8°C-weeks). Heat stress assays carried out in the northern (Hurghada) and central (Thuwal) Red Sea on four key reef-building species confirmed different regional thermal susceptibility, and that central Red Sea corals are more sensitive to thermal anomalies as compared to those from the north. Together, our data demonstrate that corals in the northern Red Sea have a much higher heat tolerance than their prevailing temperature regime would suggest. In contrast, corals from the central Red Sea are close to their thermal limits, which closely match the maximum annual water temperatures. The northern Red Sea harbours reef-building corals that live well below their bleaching thresholds and thus we propose that the region represents a thermal refuge of global importance.

[1]  W. Johns,et al.  Direct observations of seasonal exchange through the Bab el Mandab Strait , 1997 .

[2]  Y. Loya,et al.  Ancestral genetic diversity associated with the rapid spread of stress-tolerant coral symbionts in response to Holocene climate change , 2016, Proceedings of the National Academy of Sciences.

[3]  M. Kučera,et al.  Millennial‐scale variability in Red Sea circulation in response to Holocene insolation forcing , 2010 .

[4]  C. Voolstra,et al.  Spatio-Temporal Analyses of Symbiodinium Physiology of the Coral Pocillopora verrucosa along Large-Scale Nutrient and Temperature Gradients in the Red Sea , 2014, PloS one.

[5]  M. Pratchett,et al.  Changes in Bleaching Susceptibility among Corals Subject to Ocean Warming and Recurrent Bleaching in Moorea, French Polynesia , 2013, PloS one.

[6]  David J. Smith,et al.  Photoacclimation, growth and distribution of massive coral species in clear and turbid waters , 2008 .

[7]  S. Palumbi,et al.  Bacterial community dynamics are linked to patterns of coral heat tolerance , 2017, Nature Communications.

[8]  Ibrahim Hoteit,et al.  Abrupt warming of the Red Sea , 2011 .

[9]  M. Matz,et al.  Genomic determinants of coral heat tolerance across latitudes , 2015, Science.

[10]  O. Hoegh‐Guldberg.  Climate change, coral bleaching and the future of the world's coral reefs , 1999 .

[11]  Yohei Matsui,et al.  The cumulative impact of annual coral bleaching can turn some coral species winners into losers , 2014, Global change biology.

[12]  C. Voolstra,et al.  Niche acclimatization in Red Sea corals is dependent on flexibility of host-symbiont association , 2015 .

[13]  L. Devantier,et al.  THE STATUS OF CORAL REEFS IN YEMEN - 2000 , 2000 .

[14]  C. Wilkinson,et al.  Status of coral reefs in the Red Sea and Gulf of Aden in 2004 , 2004 .

[15]  Kenneth S. Casey,et al.  New insights into global patterns of ocean temperature anomalies: implications for coral reef health and management , 2010 .

[16]  R. Steneck,et al.  Coral Reefs Under Rapid Climate Change and Ocean Acidification , 2007, Science.

[17]  Clive Wilkinson,et al.  Status of Coral Reefs of the World: 2020 , 2000 .

[18]  Edward G. Smith,et al.  Nutrient enrichment can increase the susceptibility of reef corals to bleaching , 2013 .

[19]  Tim R. McClanahan,et al.  Effects of geography, taxa, water flow, and temperature variation on coral bleaching intensity in Mauritius , 2005 .

[20]  David J. Smith,et al.  Interpreting the sign of coral bleaching as friend vs. foe , 2011 .

[21]  C. Braithwaite.  CHAPTER 2 – Geology and Palaeogeography of the Red Sea Region , 1987 .

[22]  R. van Woesik,et al.  Corals escape bleaching in regions that recently and historically experienced frequent thermal stress , 2009, Proceedings of the Royal Society B: Biological Sciences.

[23]  B. Brown,et al.  Coral bleaching--capacity for acclimatization and adaptation. , 2003, Advances in marine biology.

[24]  Scott F. Heron,et al.  Caribbean Corals in Crisis: Record Thermal Stress, Bleaching, and Mortality in 2005 , 2010, PloS one.

[25]  O. Hoegh‐Guldberg,et al.  Bleaching, energetics, and coral mortality risk: Effects of temperature, light, and sediment regime , 2007 .

[26]  K. Anthony,et al.  Improved predictions of coral bleaching using seasonal baselines and higher spatial resolution , 2008 .

[27]  A. Meibom,et al.  Common reef-building coral in the Northern Red Sea resistant to elevated temperature and acidification , 2017, Royal Society Open Science.

[28]  A. Eladawy,et al.  Characterization of the northern Red Sea's oceanic features with remote sensing data and outputs from a global circulation model , 2017 .

[29]  S. Palumbi,et al.  Mechanisms of reef coral resistance to future climate change , 2014, Science.

[30]  T. Oliver,et al.  Many corals host thermally resistant symbionts in high-temperature habitat , 2011, Coral Reefs.

[31]  P. Glynn,et al.  Climate change and coral reef bleaching: An ecological assessment of long-term impacts, recovery trends and future outlook , 2008 .

[32]  R. Salm,et al.  Coral reef resilience and resistance to bleaching , 2005 .

[33]  M. Stat,et al.  Limits to the thermal tolerance of corals adapted to a highly fluctuating, naturally extreme temperature environment , 2015, Scientific Reports.

[34]  William E. Johns,et al.  An Oceanic General Circulation Model (OGCM) investigation of the Red Sea circulation: 2. Three‐dimensional circulation in the Red Sea , 2003 .

[35]  S. Donner.  An evaluation of the effect of recent temperature variability on the prediction of coral bleaching events. , 2011, Ecological applications : a publication of the Ecological Society of America.

[36]  T. Oliver,et al.  Do fluctuating temperature environments elevate coral thermal tolerance? , 2011, Coral Reefs.

[37]  T. Oliver,et al.  Genomic basis for coral resilience to climate change , 2013, Proceedings of the National Academy of Sciences.

[38]  R Core Team,et al.  R: A language and environment for statistical computing. , 2014 .

[39]  Edward G. Smith,et al.  Local adaptation constrains the distribution potential of heat-tolerant Symbiodinium from the Persian/Arabian Gulf , 2015, The ISME Journal.

[40]  Y. Loya,et al.  Repeated bleaching events may result in high tolerance and notable gametogenesis in stony corals: Oculina patagonica as a model , 2011 .

[41]  A. Genin,et al.  A coral reef refuge in the Red Sea , 2013, Global change biology.

[42]  J. Wiedenmann,et al.  Symbiodinium thermophilum sp. nov., a thermotolerant symbiotic alga prevalent in corals of the world's hottest sea, the Persian/Arabian Gulf , 2015, Scientific Reports.

[43]  A. Bower,et al.  Formation and spreading of Red Sea Outflow Water in the Red Sea , 2015 .

[44]  D. McDougald,et al.  Sex, Scavengers, and Chaperones: Transcriptome Secrets of Divergent Symbiodinium Thermal Tolerances , 2016, Molecular biology and evolution.

[45]  Takashi Nakamura.  Importance of water-flow on the physiological responses of reef-building corals , 2010 .

[46]  Christian R. Voolstra,et al.  Absence of genetic differentiation in the coral Pocillopora verrucosa along environmental gradients of the Saudi Arabian Red Sea , 2015, Front. Mar. Sci..

[47]  P. Glynn,et al.  Coral reef bleaching in the 1980s and possible connections with global warming. , 1991, Trends in ecology & evolution.

[48]  J. Burt,et al.  Biogeography and molecular diversity of coral symbionts in the genus Symbiodinium around the Arabian Peninsula , 2017, Journal of biogeography.

[49]  J. Verreth,et al.  Interactive effects of oxygen, carbon dioxide and flow on photosynthesis and respiration in the scleractinian coral Galaxea fascicularis , 2017, Journal of Experimental Biology.

[50]  C. Wilkinson.  Status of coral reefs of the world , 2000 .

[51]  S. Purkis,et al.  Red Sea Coral Reef Trajectories over 2 Decades Suggest Increasing Community Homogenization and Decline in Coral Size , 2012, PloS one.

[52]  William E. Johns,et al.  Observations of the summer Red Sea circulation , 2007 .

[53]  M. Fine,et al.  Beyond peak summer temperatures, branching corals in the Gulf of Aqaba are resilient to thermal stress but sensitive to high light , 2017, Coral Reefs.

[54]  I. Hoteit,et al.  Decadal trends in Red Sea maximum surface temperature , 2017, Scientific Reports.

[55]  J. Wiedenmann,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. , 2013, Marine pollution bulletin.

[56]  A. Timmermann,et al.  Increasing frequency of extreme El Niño events due to greenhouse warming , 2014 .

[57]  U. Sommer,et al.  Influence of environmental gradients on C and N stable isotope ratios in coral reef biota of the Red Sea, Saudi Arabia , 2014 .

[58]  E. Howells,et al.  Host adaptation and unexpected symbiont partners enable reef‐building corals to tolerate extreme temperatures , 2016, Global change biology.

[59]  G. De’ath,et al.  The 27–year decline of coral cover on the Great Barrier Reef and its causes , 2012, Proceedings of the National Academy of Sciences.

[60]  Susceptibility of central Red Sea corals during a major bleaching event , 2013, Coral Reefs.

[61]  Raymond L. Hayes,et al.  Coral Bleaching and Ocean "Hot Spots" , 1994 .

[62]  Scott F. Heron,et al.  Warming Trends and Bleaching Stress of the World’s Coral Reefs 1985–2012 , 2016, Scientific Reports.