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Impacts of the 2014–2017 global bleaching event on a protected remote atoll in the Western Indian Ocean

Abstract

The third global bleaching event caused prolonged elevated sea surface temperatures from 2014 to 2017 that heavily impacted coral reefs worldwide. This study determines changes in benthic community following this bleaching event at a remote UNESCO World Heritage Site in the Western Indian Ocean. Aldabra Atoll offers a rare opportunity to study global impacts in the absence of local anthropogenic stressors. Analysis of satellite-derived temperature data indicated that Aldabra was exposed to the highest bleaching-risk intensity of the past 20 years during this bleaching event. Bleaching-risk conditions lasted from December 2015 to June 2016 close to the 4 °C-week threshold, when bleaching is expected. Benthic cover was established pre- and post-bleaching from 21 transects across two reef locations (lagoonal reef, 2 m depth; seaward reef, 5 and 15 m depth). From a pre-bleaching benthic community in which living corals and epilithic algal matrix (EAM) predominated, Aldabra’s reefs switched to an EAM-dominated community 8 months after bleaching. Soft corals declined by 93% of their overall pre-bleaching cover to < 1%. Although overall hard-coral cover was also reduced, the decline varied among depths and might indicate local adaptations of the lagoonal reef, due to greater variability in sea surface temperature compared to the seaward reef. With the exception of Isopora palifera, all taxomorphic coral groups experienced a decline following bleaching. Overall, Rhytisma experienced a near-complete extirpation, Acroporids (excluding I. palifera) and branching Poritids declined by more than 80%, Merulinidae lost ca. 60% of their pre-bleaching cover, while massive Poritids cover slightly decreased. Aldabra’s benthic community therefore underwent substantial changes following the 2014–2017 bleaching event and showed that live coral cover declines significantly even in protected areas isolated from local anthropogenic pressures.

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References

  1. Andréfouët S, Chagnaud N, Kranenburg C (2009) Atlas of western and central Indian Ocean coral reefs. Centre IRD de Nouméa, Nouméa, Nouvelle-Calédonie

  2. Ateweberhan M, Feary DA, Keshavmurthy S, Chen A, Schleyer MH, Sheppard CR (2013) Climate change impacts on coral reefs: synergies with local effects, possibilities for acclimation, and management implications. Marine Pollution Bulletin 74:526–539

  3. Ayre D, Veron JE, Dufty S (1991) The corals Acropora palifera and Acropora cuneata are genetically and ecologically distinct. Coral Reefs 10:13–18

  4. Baird AH, Bhagooli R, Ralph PJ, Takahashi S (2009) Coral bleaching: the role of the host. Trends in Ecology & Evolution 24:16–20

  5. Barkley HC, Cohen AL, Mollica NR, Brainard RE, Rivera HE, DeCarlo TM, Lohmann GP, Drenkard EJ, Alpert AE, Young CW, Vargas-Ángel B, Lino KC, Oliver TA, Pietro KR, Luu VH (2018) Repeat bleaching of a central Pacific coral reef over the past six decades (1960–2016). Communications Biology 1:177

  6. Barshis DJ, Ladner JT, Oliver TA, Seneca FO, Traylor-Knowles N, Palumbi SR (2013) Genomic basis for coral resilience to climate change. Proceedings of the National Academy of Sciences 110:1387–1392

  7. Berkelmans R, van Oppen MJH (2006) The role of zooxanthellae in the thermal tolerance of corals: a ‘nugget of hope’ for coral reefs in an era of climate change. Proceedings Biological sciences 273:2305–2312

  8. Bolker BM, Brooks ME, Clark CJ, Geange SW, Poulsen JR, Stevens MHH, White J-SS (2009) Generalized linear mixed models: a practical guide for ecology and evolution. Trends in Ecology & Evolution 24:127–135

  9. Boyle S, De Anda V, Koenig K, O’Reilly E, Schafer M, Acoba T, Dillon A, Heenan A, Oliver TTA, Swanson DW (2017) Coral reef ecosystems of the Pacific Remote Islands Marine National Monument: a 2000-2016 overview

  10. Brown H, Kempton R (1994) The application of REML in clinical trials. Statistics in Medicine 13:1601–1617

  11. Bruno JF, Sweatman H, Precht WF, Selig ER, Schutte VG (2009) Assessing evidence of phase shifts from coral to macroalgal dominance on coral reefs. Ecology 90:1478–1484

  12. Burt JA, Paparella F, Al-Mansoori N, Al-Mansoori A, Al-Jailani H (2019) Causes and consequences of the 2017 coral bleaching event in the southern Persian/Arabian Gulf. Coral Reefs. https://doi.org/10.1007/s00338-019-01767-y

  13. Ceccarelli D, Richards Z, Pratchett MS, Cvitanovic C (2011) Rapid increase in coral cover on an isolated coral reef, the Ashmore Reef National Nature Reserve, north-western Australia. Mar Freshw Res 62:1214–1220

  14. Couch CS, Burns JHR, Liu G, Steward K, Gutlay TN, Kenyon J, Eakin CM, Kosaki RK (2017) Mass coral bleaching due to unprecedented marine heatwave in Papahānaumokuākea Marine National Monument (Northwestern Hawaiian Islands). PLOS One 12:e0185121

  15. Darling ES, Graham NA, Januchowski-Hartley FA, Nash KL, Pratchett MS, Wilson SK (2017) Relationships between structural complexity, coral traits, and reef fish assemblages. Coral Reefs 36:561–575

  16. Done TJ (1982) Patterns in the distribution of coral communities across the central Great Barrier Reef. Coral Reefs 1:95–107

  17. Done TJ (1992) Phase shifts in coral reef communities and their ecological significance. Hydrobiologia 247:121–132

  18. Drew E, Yon L, Lythgoe J (1971) Morphology and ecology of the reef front of Aldabra. Regional Variation in Indian Ocean Coral Reefs: The Proceedings of a Symposium, Organized Jointly by the Royal Society of London and the Zoological Society of London, Held at the Zoological Society of London on 28 and 29 May, 1970:87

  19. Fabricius KK, Alderslade PP (2001) Soft corals and sea fans: a comprehensive guide to the tropical shallow water genera of the central-west Pacific, the Indian Ocean and the Red Sea. Australian Institute of Marine Science (AIMS)

  20. Farrow G, Brander K (1971) Tidal studies on Aldabra. Philosophical Transactions of the Royal Society of London B: Biological Sciences 260:93–121

  21. Friedlander A, Ballesteros E, Beets J, Brown EK, Fay JM, Haupt P, Henning B, Rose P, Sala E (2015) Biodiversity and ecosystem health of the Aldabra Group, Southern Seychelles

  22. Furby KA, Bouwmeester J, Berumen ML (2013) Susceptibility of central Red Sea corals during a major bleaching event. Coral Reefs 32:505–513

  23. Gilmour AR, Gogel B, Cullis B, Thompson R, Butler D (2009) ASReml user guide release 3.0. VSN International Ltd, Hemel Hempstead, UK

  24. Gilmour JP, Smith LD, Heyward AJ, Baird AH, Pratchett MS (2013) Recovery of an isolated coral reef system following severe disturbance. Science 340:69–71

  25. Graham NA, Nash K (2013) The importance of structural complexity in coral reef ecosystems. Coral Reefs 32:315–326

  26. Graham NA, McClanahan TR, MacNeil MA, Wilson SK, Polunin NV, Jennings S, Chabanet P, Clark S, Spalding MD, Letourneur Y (2008) Climate warming, marine protected areas and the ocean-scale integrity of coral reef ecosystems. PLOS One 3:e3039

  27. Granek EF (2006) Linkages between mangrove forests and coral reefs: quantifying disturbance effects and energy flow between systems. Oregon State University, Department of Zoology, Corvallis, p p171

  28. Green RH, Lowe RJ, Buckley ML, Foster T, Gilmour JP (2019) Physical mechanisms influencing localized patterns of temperature variability and coral bleaching within a system of reef atolls. Coral Reefs. https://doi.org/10.1007/s00338-019-01771-2

  29. Gudka M, Obura D, Mwaura J, Porter S, Yahya S, Mabwa R (2018) Impact of the 3rd Global Coral Bleaching Event on the Western Indian Ocean in 2016. Global Coral Reef Monitoring Network (GCRMN)/Indian Ocean Commission

  30. Harrison HB, Álvarez-Noriega M, Baird AH, Heron SF, MacDonald C, Hughes TP (2018) Back-to-back coral bleaching events on isolated atolls in the Coral Sea. Coral Reefs. https://doi.org/10.1007/s00338-018-01749-6

  31. Head CE, Bayley DT, Rowlands G, Roche RC, Tickler DM, Rogers AD, Koldewey H, Turner JR, Andradi-Brown DA (2019) Coral bleaching impacts from back-to-back 2015–2016 thermal anomalies in the remote central Indian Ocean. Coral Reefs:1-14

  32. Heron S, Johnston L, Liu G, Geiger E, Maynard J, De La Cour J, Johnson S, Okano R, Benavente D, Burgess T (2016) Validation of reef-scale thermal stress satellite products for coral bleaching monitoring. Remote Sensing 8:59

  33. Heron SF, Eakin CM, Douvere F, Anderson KL, Day JC, Geiger E, Hoegh-Guldberg O, Van Hooidonk R, Hughes T, Marshall P, Obura D (2017) Impacts of climate change on World Heritage coral reefs : a first global scientific assessment

  34. Hoegh-Guldberg O (2011) Coral reef ecosystems and anthropogenic climate change. Regional Environmental Change 11:215–227

  35. 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:e60952

  36. Hsu C-M, Keshavmurthy S, Denis V, Kuo C-Y, Wang J-T, Meng P-J, Chen CA (2012) Temporal and spatial variations in symbiont communities of catch bowl coral Isopora palifera (Scleractinia: Acroporidae) on reefs in Kenting National Park, Taiwan. Zoological Studies 51:1343–1353

  37. Hughes TP (1994) Catastrophes, phase shifts, and large-scale degradation of a Caribbean coral reef. Science-AAAS-Weekly Paper Edition 265:1547–1551

  38. Hughes TP, Barnes ML, Bellwood DR, Cinner JE, Cumming GS, Jackson JB, Kleypas J, van de Leemput IA, Lough JM, Morrison TH (2017) Coral reefs in the Anthropocene. Nature 546:82–90

  39. Hughes TP, Anderson KD, Connolly SR, Heron SF, Kerry JT, Lough JM, Baird AH, Baum JK, Berumen ML, Bridge TC (2018a) Spatial and temporal patterns of mass bleaching of corals in the Anthropocene. Science 359:80–83

  40. Hughes TP, Kerry JT, Baird AH, Connolly SR, Dietzel A, Eakin CM, Heron SF, Hoey AS, Hoogenboom MO, Liu G (2018b) Global warming transforms coral reef assemblages. Nature 556:492

  41. Hume BC, Voolstra CR, Arif C, D’Angelo C, Burt JA, Eyal G, Loya Y, Wiedenmann J (2016) Ancestral genetic diversity associated with the rapid spread of stress-tolerant coral symbionts in response to Holocene climate change. Proceedings of the National Academy of Sciences 113:4416–4421

  42. Kohler KE, Gill SM (2006) Coral Point Count with Excel extensions (CPCe): A Visual Basic program for the determination of coral and substrate coverage using random point count methodology. Computers & Geosciences 32:1259–1269

  43. Le Nohaïc M, Ross CL, Cornwall CE, Comeau S, Lowe R, McCulloch MT, Schoepf V (2017) Marine heatwave causes unprecedented regional mass bleaching of thermally resistant corals in northwestern Australia. Scientific Reports 7:14999

  44. Liu G, Rauenzahn JL, Heron SF, Eakin CM, Skirving WJ, Christensen T, Strong AE, Li J (2013) NOAA coral reef watch 50 km satellite sea surface temperature-based decision support system for coral bleaching management

  45. Lough JM, Anderson KD, Hughes TP (2018) Increasing thermal stress for tropical coral reefs: 1871–2017. Scientific Reports 8:6079

  46. Lowe RJ, Pivan X, Falter J, Symonds G, Gruber R (2016) Rising sea levels will reduce extreme temperature variations in tide-dominated reef habitats. Science Advances 2:e1600825

  47. Loya Y, Sakai K, Yamazato K, Nakano Y, Sambali H, van Woesik R (2001) Coral bleaching: the winners and the losers. Ecology Letters 4:122–131

  48. Maida M, Sammarco PW, Coll JC (1995) Effects of soft corals on scleractinian coral recruitment. I: Directional allelopathy and inhibition of settlement. Marine Ecology Progress Series 121:191–202

  49. McClanahan TR, Ateweberhan M, Sebastian CR, Graham N, Wilson S, Bruggemann JH, Guillaume MM (2007) Predictability of coral bleaching from synoptic satellite and in situ temperature observations. Coral Reefs 26:695–701

  50. Monroe AA, Ziegler M, Roik A, Röthig T, Hardenstine RS, Emms MA, Jensen T, Voolstra CR, Berumen ML (2018) In situ observations of coral bleaching in the central Saudi Arabian Red Sea during the 2015/2016 global coral bleaching event. PLOS One 13:e0195814

  51. Mumby PJ, Steneck RS (2008) Coral reef management and conservation in light of rapidly evolving ecological paradigms. Trends in ecology & evolution 23:555–563

  52. Mumby PJ, Chisholm JR, Edwards AJ, Andrefouet S, Jaubert J (2001a) Cloudy weather may have saved Society Island reef corals during the 1998 ENSO event. Marine Ecology Progress Series 222:209–216

  53. Mumby PJ, Chisholm J, Edwards A, Clark C, Roark E, Andrefouet S, Jaubert J (2001b) Unprecedented bleaching-induced mortality in Porites spp. at Rangiroa Atoll, French Polynesia. Marine Biology 139:183–189

  54. Mumby PJ, Dahlgren CP, Harborne AR, Kappel CV, Micheli F, Brumbaugh DR, Holmes KE, Mendes JM, Broad K, Sanchirico JN (2006) Fishing, trophic cascades, and the process of grazing on coral reefs. Science 311:98–101

  55. NOAA-CRW (2000) NOAA Coral Reef Watch 50-km Satellite Virtual Station Time Series Data for Aldabra, Seychelles; Comoros; Glorieuse Island, France; Mahé, Seychelles; Maldives; and Mayotte, France (dataset accessed: 2019-04-04 at https://coralreefwatch.noaa.gov/satellite/vs/docs/list_vs_group_latlon_201103.php; please refer to the according station). Silver Spring, Maryland, USA

  56. Norström AV, Nyström M, Lokrantz J, Folke C (2009) Alternative states on coral reefs: beyond coral–macroalgal phase shifts. Marine ecology progress series 376:295–306

  57. Obura D, Gudka M, Abdou Rabi F, Bacha Gian S, Bijoux J, Freed S, Maharavo J, Mwaura J, Porter S, Sola E (2017) Coral reef status report for the western Indian Ocean. global coral reef monitoring network (GCRMN)/international coral reef initiative (ICRI) CORDIO East Africa

  58. Oliver TA, Palumbi SR (2011) Do fluctuating temperature environments elevate coral thermal tolerance? Coral Reefs 30:429–440

  59. Perry C, Morgan K (2017) Bleaching drives collapse in reef carbonate budgets and reef growth potential on southern Maldives reefs. Scientific Reports 7:40581

  60. Pratchett MS, McCowan D, Maynard JA, Heron SF (2013) Changes in bleaching susceptibility among corals subject to ocean warming and recurrent bleaching in Moorea, French Polynesia. PLOS One 8:e70443

  61. Rowan R (2004) Coral bleaching: thermal adaptation in reef coral symbionts. Nature 430:742

  62. Rukhin AL (2011) Maximum Likelihood and Restricted Likelihood Solutions in Multiple-Method Studies. Journal of research of the National Institute of Standards and Technology 116:539–556

  63. Safaie A, Silbiger NJ, McClanahan TR, Pawlak G, Barshis DJ, Hench JL, Rogers JS, Williams GJ, Davis KA (2018) High frequency temperature variability reduces the risk of coral bleaching. Nature Communications 9:1671

  64. 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:e1548

  65. Schmid B, Baruffol M, Wang Z, Niklaus PA (2017) A guide to analyzing biodiversity experiments. Journal of Plant Ecology 10:91–110

  66. Sheppard CR (1999) Coral decline and weather patterns over 20 years in the Chagos Archipelago, Central Indian Ocean. Ambio:472-478

  67. Sheppard CR, Obura D (2005) Corals and reefs of Cosmoledo and Aldabra atolls: extent of damage, assemblage shifts and recovery following the severe mortality of 1998. Journal of Natural History 39:103–121

  68. Sheppard CR, Harris A, Sheppard A (2008) Archipelago-wide coral recovery patterns since 1998 in the Chagos Archipelago, central Indian Ocean. Marine Ecology Progress Series 362:109–117

  69. Sheppard CR, Sheppard A, Mogg A, Bayley D, Dempsey AC, Roche R, Turner J, Purkis S (2017) Coral bleaching and mortality in the Chagos Archipelago. Atoll Research Bulletin 2017

  70. Skirving W, Enríquez S, Hedley J, Dove S, Eakin CM, Mason R, De La Cour J, Liu G, Hoegh-Guldberg O, Strong A (2017) Remote sensing of coral bleaching using temperature and light: progress towards an operational algorithm. Remote Sensing 10(1):18

  71. Skirving W, Heron SF, Marsh B, Liu G, De La Cour J, Geiger E, Eakin CM (2019) The relentless march of mass coral bleaching: a global perspective of changing heat stress. Coral Reefs:1-11

  72. Steneck RS, Mumby PJ, MacDonald C, Rasher DB, Stoyle G (2018) Attenuating effects of ecosystem management on coral reefs. Science Advances 4, eaao5493

  73. Stobart B, Buckley R, LeClair L, Teleki K, Downing N, Souter D, Callow M (2002) Aldabra: Monitoring the path to recovery. Coral Reef Degradation in the Indian Ocean 5:232

  74. Stobart B, Teleki K, Buckley R, Downing N, Callow M (2005) Coral recovery at Aldabra Atoll, Seychelles: five years after the 1998 bleaching event. Philosophical Transactions of the Royal Society of London A: Mathematical, Physical and Engineering Sciences 363:251–255

  75. Stoddart D (1984) Coral reefs of the Seychelles and adjacent regions. Biogeography and Ecology of the Seychelles Islands W Junk, The Hague, pp 63–81

  76. Stoddart D, Taylor J, Fosberg F, Farrow G (1971) Geomorphology of Aldabra atoll. Philosophical Transactions of the Royal Society of London B, Biological Sciences 260:31–66

  77. Stuart-Smith RD, Brown CJ, Ceccarelli D, Edgar GJ (2018) Ecosystem restructuring along the Great Barrier Reef following mass coral bleaching. Nature 560:92–96

  78. Taylor J (1971) Intertidal zonation at Aldabra atoll. Phil Trans R Soc Lond B 260:173–213

  79. Teleki K, Downing N, Stobart B, Buckley R (1999) Aldabra marine programme. Cambridge Coastal Research Unit, Department of Geography, University of Cambridge, p 31

  80. Veron JE (2000) Corals of the World, vol. 1–3. Australian Institute of Marine Science, Townsville 295

  81. Virk D, Pandit D, Sufian M, Ahmed F, Siddique M, Samad M, Rahman M, Islam M, Ortiz-Ferrara G, Joshi K (2009) REML is an effective analysis for mixed modelling of unbalanced on-farm varietal trials. Experimental Agriculture 45:77–91

  82. Wallace C (1999) Staghorn corals of the world: a revision of the genus Acropora. CSIRO publishing, Melbourne

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Acknowledgements

A special thanks goes to the Seychelles Islands Foundation (SIF) and staff for their invaluable support and help, in particular: Rowana Walton and Anna Koester for the identification of benthic data, as well as the SIF staff who helped with data collection (Daig Romain, Rebecca Filippin, Sheril De Commarmond, Jude Brice, Samuel Basset and Terence Mahoune for pre-bleaching data; Terence Mahoune, Ella Nancy, Joel Bonne, Marvin Roseline for post-bleaching data). Anna Koester is further thanked for cleaning the temperature dataset. We thank the Global Environment Facility for funding for the diving and research equipment, and the development of the ARM programme. We further thank Anthony Bernard and Nick Riddin from the South African Institute for Aquatic Biodiversity and SIF staff who assisted in the establishment of permanent benthic transects; and Rebecca Klaus for advice on benthic transect set-up and photoquadrat methodology. Prof. Gabriela Schaepman-Strub was supported by the University of Zürich Research Priority Programme on Global Change and Biodiversity. Prof. Bernhard Schmid and Prof. Pascal A. Niklaus are further thanked for their advice on the statistical analyses. Finally, we would like to thank the editor and reviewers for their constructive feedback.

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Cerutti, J.M.B., Burt, A.J., Haupt, P. et al. Impacts of the 2014–2017 global bleaching event on a protected remote atoll in the Western Indian Ocean. Coral Reefs 39, 15–26 (2020) doi:10.1007/s00338-019-01853-1

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Keywords

  • Coral bleaching
  • El Niño
  • Marine protected area
  • Aldabra Atoll
  • Seychelles
  • UNESCO World Heritage Site