Coral reef resilience persisted for a millennium but has declined rapidly in recent decades

The lack of long-term records of coral community composition restricts our understanding of the contemporary ecological states of tropical reefs. Here we integrated paleo-ecological reconstruction, historical mortality evidence, and ecological survey data to determine the temporal variability in reef resilience of the Nansha atolls in the tropical western Pacific. Subfossil coral assemblages extracted from the reef cores exhibited no evidence of community shifts attributable to centennial-scale changes in El Niño variability during the last millennium, suggesting long-term stability in community structure and persistence of reef resilience. By contrast, ecological surveys revealed a major collapse in the reef ecosystem, and high-precision U-series dating of dead Acropora fragments indicated that this collapse occurred in recent decades and was especially relevant to several strong/extreme El Niño episodes. Frequent and intensive El Niño−Southern Oscillation and marine heatwaves have overwhelmed the reefs’ resistive and recovery capacity, thereby impairing reef resilience.

[1]  David L. Smith,et al.  A roadmap to integrating resilience into the practice of coral reef restoration , 2022, Global change biology.

[2]  T. Quinn,et al.  Unraveling forced responses of extreme El Niño variability over the Holocene , 2022, Science advances.

[3]  Tianran Chen,et al.  Marine heatwaves impair the thermal refugia potential of marginal reefs in the northern South China Sea. , 2022, The Science of the total environment.

[4]  H. Lenihan,et al.  Size‐dependent mortality of corals during marine heatwave erodes recovery capacity of a coral reef , 2021, Global change biology.

[5]  P. Mumby,et al.  Cumulative bleaching undermines systemic resilience of the Great Barrier Reef , 2021, Current Biology.

[6]  D. Bellwood,et al.  Dangerous demographics in post-bleach corals reveal boom-bust versus protracted declines , 2021, Scientific Reports.

[7]  S. Sandin,et al.  Increasing Coral Reef Resilience Through Successive Marine Heatwaves , 2021, Geophysical Research Letters.

[8]  S. Donner,et al.  Coral reefs in the Gilbert Islands of Kiribati: Resistance, resilience, and recovery after more than a decade of multiple stressors , 2021, PloS one.

[9]  J. H. Hudson,et al.  Climate and the latitudinal limits of subtropical reef development , 2021, Scientific Reports.

[10]  Jian-xin Zhao,et al.  Uranium-thorium dating of coral mortality and community shift in a highly disturbed inshore reef (Weizhou Island, northern South China Sea). , 2020, The Science of the total environment.

[11]  K. S. Tkachenko,et al.  Ecological status of coral reefs in the Spratly Islands, South China Sea (East sea) and its relation to thermal anomalies , 2020, Estuarine, Coastal and Shelf Science.

[12]  E. Treml,et al.  Coral reef resilience to thermal stress in the Eastern Tropical Pacific , 2020, Global change biology.

[13]  J. Southon,et al.  Enhanced El Niño–Southern Oscillation Variability in Recent Decades , 2020, Geophysical Research Letters.

[14]  Chaolun Allen Chen,et al.  Thermal Stress and Resilience of Corals in a Climate-Changing World , 2019, Journal of Marine Science and Engineering.

[15]  Bin Wang,et al.  Historical change of El Niño properties sheds light on future changes of extreme El Niño , 2019, Proceedings of the National Academy of Sciences.

[16]  J. Pandolfi,et al.  Defining variation in pre-human ecosystems can guide conservation: An example from a Caribbean coral reef , 2019, Scientific Reports.

[17]  G. Roff,et al.  Tropical Sand Cays as Natural Paleocyclone Archives , 2019, Geophysical Research Letters.

[18]  C. Eakin,et al.  The 2014–2017 global-scale coral bleaching event: insights and impacts , 2019, Coral Reefs.

[19]  I. B. Kuffner,et al.  The unprecedented loss of Florida's reef‐building corals and the emergence of a novel coral‐reef assemblage , 2019, Ecology.

[20]  Joshua S Madin,et al.  Global warming impairs stock–recruitment dynamics of corals , 2019, Nature.

[21]  M. McCulloch,et al.  Acclimatization of massive reef-building corals to consecutive heatwaves , 2019, Proceedings of the Royal Society B.

[22]  S. Donner,et al.  Resilience of Central Pacific reefs subject to frequent heat stress and human disturbance , 2019, Scientific Reports.

[23]  T. Alcoverro,et al.  Coral reefs respond to repeated ENSO events with increasing resistance but reduced recovery capacities in the Lakshadweep archipelago , 2018, Coral Reefs.

[24]  E. Fischer,et al.  Marine heatwaves under global warming , 2018, Nature.

[25]  Robert William Schlegel,et al.  heatwaveR: A central algorithm for the detection of heatwaves and cold-spells , 2018, J. Open Source Softw..

[26]  T. Hughes,et al.  Global warming transforms coral reef assemblages , 2018, Nature.

[27]  Michael T Burrows,et al.  Longer and more frequent marine heatwaves over the past century , 2018, Nature Communications.

[28]  Ryan J. Lowe,et al.  Spatial and temporal patterns of mass bleaching of corals in the Anthropocene , 2018, Science.

[29]  T. Done,et al.  U-Th dating reveals regional-scale decline of branching Acropora corals on the Great Barrier Reef over the past century , 2017, Proceedings of the National Academy of Sciences.

[30]  M. Scheffer,et al.  Coral reefs in the Anthropocene , 2017, Nature.

[31]  Weijian Zhou,et al.  Recent enhancement of central Pacific El Niño variability relative to last eight centuries , 2017, Nature Communications.

[32]  Alistair J. Hobday,et al.  A hierarchical approach to defining marine heatwaves , 2016 .

[33]  T. Done,et al.  Testing the precision and accuracy of the U–Th chronometer for dating coral mortality events in the last 100 years , 2014 .

[34]  Q. Shi,et al.  Coral communities of the remote atoll reefs in the Nansha Islands, southern South China Sea , 2013, Environmental Monitoring and Assessment.

[35]  T. Done,et al.  Palaeoecological evidence of a historical collapse of corals at Pelorus Island, inshore Great Barrier Reef, following European settlement , 2013, Proceedings of the Royal Society B: Biological Sciences.

[36]  R. Aronson,et al.  ENSO Drove 2500-Year Collapse of Eastern Pacific Coral Reefs , 2012, Science.

[37]  P. Mumby,et al.  Global disparity in the resilience of coral reefs. , 2012, Trends in ecology & evolution.

[38]  C. Linares,et al.  Recolonisation of Acropora hyacinthus following climate-induced coral bleaching on the Great Barrier Reef , 2011 .

[39]  Kefu Yu,et al.  Assessment of coral bleaching using symbiotic zooxanthellae density and satellite remote sensing data in the Nansha Islands, South China Sea , 2011 .

[40]  R. Steneck,et al.  Rising to the challenge of sustaining coral reef resilience. , 2010, Trends in ecology & evolution.

[41]  Y. Rosenthal,et al.  2,000-year-long temperature and hydrology reconstructions from the Indo-Pacific warm pool , 2009, Nature.

[42]  Ray Berkelmans,et al.  Doom and Boom on a Resilient Reef: Climate Change, Algal Overgrowth and Coral Recovery , 2009, PloS one.

[43]  Kefu Yu,et al.  Reconstruction of storm/tsunami records over the last 4000 years using transported coral blocks and lagoon sediments in the southern South China Sea , 2009 .

[44]  J. Overpeck,et al.  Holocene changes in eastern tropical Pacific climate inferred from a Galápagos lake sediment record , 2008 .

[45]  David M. Anderson,et al.  Variability of El Niño/Southern Oscillation activity at millennial timescales during the Holocene epoch , 2002, Nature.

[46]  Thomas M. Smith,et al.  An Improved In Situ and Satellite SST Analysis for Climate , 2002 .

[47]  K. Yamazato,et al.  Coral bleaching: the winners and the losers , 2001 .

[48]  C. Folke,et al.  Ecological goods and services of coral reef ecosystems , 1999 .

[49]  Ben P. Harvey,et al.  Marine heatwaves threaten global biodiversity and the provision of ecosystem services , 2019 .

[50]  O Hammer-Muntz,et al.  PAST: paleontological statistics software package for education and data analysis version 2.09 , 2001 .

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

[52]  Clive Wilkinson,et al.  Survey Manual for Tropical Marine Resources (2nd Edition) , 1997 .

[53]  C. Wilkinson,et al.  Survey manual for tropical marine resources , 1994 .