Abstract
Ocean warming is negatively impacting coral reef ecosystems and considerable effort is currently invested in projecting coral reef futures under 21st century climate change. A limiting factor in these projections is lack of quantitative data on the thermal thresholds of different reef communities, due in large part to spatial and temporal gaps in bleaching observations. Here we apply a coral bleaching proxy, skeletal stress bands, to reconstruct the history of bleaching on eight coral reefs in the central equatorial Pacific (CEP) and use this information to constrain the thermal thresholds of their coral communities. First, three genera of massive corals collected on both Pacific and Caribbean reefs are used to derive a calibration between the proportion of corals that form stress bands during a bleaching event, and the total observed bleaching incidence in the community of mixed coral taxa. The correlation is highly significant, indicating that stress bands in massive corals reflect community-level bleaching severity (R2 = 0.945, p < 0.001). We applied the calibration to stress band records from eight Pacific reefs, reconstructing their bleaching histories over the period 1982 to 2015. A percentile-based method of estimating thermal stress (Degree Heating Weeks) for CEP reefs was developed and applied. Comparing the level of thermal stress experienced by each coral community during each event with the reconstructed bleaching response, we characterized the thermal sensitivities of each reef community and quantified the thermal threshold (b½) at which 50% of the coral community bleached. Our analysis reveals a unique non-linear thermal response curve for each reef. The most thermally tolerant reefs in the study (Jarvis and Kanton Islands) experienced 50% bleaching at seven to nine times more thermal stress than did the least resistant reef in the study (Maiana Island). An exploration of the potential drivers of thermal tolerance revealed a strong correlation between b½ and the history of thermal stress events in each reef system. Thermal tolerance was also correlated with concentrations of dissolved inorganic nitrate in the water column and with estimates of coral energetic reserve.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Change history
19 June 2019
Figure 2 in the original article has been updated with this figure 2 due to discrepancies related to incorrect mapping with one of the islands.
References
Alpert AE, Cohen AL, Oppo DW, Decarlo TM, Gove JM, Young CW (2016) Comparison of equatorial Pacific sea surface temperature variability and trends with Sr/Ca records from multiple corals. Paleoceanography 31:252–265
Ashok K, Behera SK, Rao SA, Weng H (2007) El Nino Modoki and its possible teleconnection. J Geophys Res 112:1–27
Barkley HC, Cohen AL (2016) Skeletal records of community-level bleaching in Porites corals from Palau. Coral Reefs 35:1407–1417
Barkley HC, Cohen AL, Brainard RE, Mollica NR, Rivera HE, Drenkard EJ, Young CW, Vargas-Ángel B, Lohmann GP, Decarlo TM, Alpert AE, Lino KC, Oliver TA, Pietro KR, Luu VH (2018) Repeat bleaching of a central Pacific coral reef over the past six decades (1960–2016). Nat Biol Commun
Barkley HC, Cohen AL, Golbuu Y, Starczak VR, Decarlo TM, Shamberger KEF (2015) Changes in coral reef communities across a natural gradient in seawater pH. Sci Adv 1–7
Barnes DJ, Lough JM (1992) Systematic variations in the depth of skeleton occupied by coral tissue in massive colonies of Porites from the Great Barrier Reef. J Exp Mar Bio Ecol 159:113–128
Beyer HL, Kennedy E V., Beger M, Chen CA, Cinner JE, Darling ES, Eakin CM, Gates RD, Heron SF, Knowlton N, Obura DO, Palumbi SR, Possingham HP, Puotinen M, Runting RK, Skirving WJ, Spalding M, Wilson KA, Wood S, Veron JE, Hoegh-Guldberg O (2018) Risk-sensitive planning for conserving coral reefs under rapid climate change. Conserv Lett e12587
Cantin NE, Cohen AL, Karnauskas KB, Tarrant AM, McCorkle DC (2010) Ocean Warming Slows Coral Growth in the Central Red Sea. Science 329:322–325
Cantin NE, Lough JM (2014) Surviving coral bleaching events: Porites growth anomalies on the great barrier reef. PLoS One 9
Carilli J, Donner SD, Hartmann AC (2012) Historical temperature variability affects coral response to heat stress. PLoS ONE 7:1–9
Carilli JE, Norris RD, Black B, Walsh SM, Mcfield M (2010) Century-scale records of coral growth rates indicate that local stressors reduce coral thermal tolerance threshold. Glob Chang Biol 16:1247–1257
Carilli JE, Norris RD, Black BA, Walsh SM, McField M (2009) Local stressors reduce coral resilience to bleaching. PLoS ONE 4:1–5
Casey KS, Brandon TB, Cornillon P, Evans R (2010) The Past, Present, and Future of the AVHRR Pathfinder SST Program. Oceanogr from Sp Revisit 1–375
Coles SL, Brown BE (2003) Coral bleaching-capacity for acclimatization and adaptation. Adv Mar Biol 46:183–223
Coles SL, Jokiel PL (1977) Effects of temperature on photosynthesis and respiration in hermatypic corals. Mar Biol 43:209–216
D’Angelo C, Wiedenmann J (2014) Impacts of nutrient enrichment on coral reefs: New perspectives and implications for coastal management and reef survival. Curr Opin Environ Sustain 7:82–93
DeCarlo TM, Cohen AL (2016) coralCT: software tool to analyze computerized tomography (CT) scans of coral skeletal cores for calcification and bioerosion rates. Zenodo
DeCarlo TM, Cohen AL (2017) Dissepiments, density bands, and signatures of thermal stress in Porites skeletons. Coral Reefs 1–13
DeCarlo TM, Cohen AL, Barkley HC, Cobban Q, Young C, Shamberger KE, Brainard RE, Golbuu Y (2015) Coral macrobioerosion is accelerated by ocean acidification and nutrients. Geology 43:7–10
DeCarlo TM, Cohen AL, Wong GTF, Davis KA, Lohmann P, Soong K (2017) Mass coral mortality under local amplification of 2 C ocean warming. Sci Rep 7:44586
Donner S (2011) An evaluation of the effect of recent temperature variability on\nthe prediction of coral. Ecol Appl 21:1718–1730
Donner SD (2009) Coping with commitment: Projected thermal stress on coral reefs under different future scenarios. PLoS One 4
Donner SD, Rickbeil GJM, Heron SF (2017) A new, high-resolution global mass coral bleaching database. PLoS ONE 12:1–17
Eakin CM, Morgan JA, Heron SF, Smith TB, Liu G, Alvarez-Filip L, Baca B, Bartels E, Bastidas C, Bouchon C, Brandt M, Bruckner AW, Bunkley-Williams L, Cameron A, Causey BD, Chiappone M, Christensen TRL, Crabbe MJC, Day O, de la Guardia E, Díaz-Pulido G, DiResta D, Gil-Agudelo DL, Gilliam DS, Ginsburg RN, Gore S, Guzmán HM, Hendee JC, Hernández-Delgado EA, Husain E, Jeffrey CFG, Jones RJ, Jordán-Dahlgren E, Kaufman LS, Kline DI, Kramer PA, Lang JC, Lirman D, Mallela J, Manfrino C, Maréchal JP, Marks K, Mihaly J, Miller WJ, Mueller EM, Muller EM, Toro CAO, Oxenford HA, Ponce-Taylor D, Quinn N, Ritchie KB, Rodríguez S, Ramírez AR, Romano S, Samhouri JF, Sánchez JA, Schmahl GP, Shank B V., Skirving WJ, Steiner SCC, Villamizar E, Walsh SM, Walter C, Weil E, Williams EH, Roberson KW, Yusuf Y (2010) Caribbean corals in crisis: Record thermal stress, bleaching, and mortality in 2005. PLoS One 5
Emiliani C, Hudson JH, Shinn EA, George RY (1978) Oxygen and Carbon Isotopic Growth Record in a Reef Coral from the Florida Keys and a Deep-Sea Coral from Blake Plateau. Science (80) 627–628
Estep A, Sandin S, Vermeij M (2017) The State of Curaçao’s Coral Reefs
Fine M, Gildor H, Genin A (2013) A coral reef refuge in the Red Sea. Glob Chang Biol 19:3640–3647
Fisk DA, Done TJ (1985) Taxonomic and Bathymetric Patterns of Bleaching in Corals, Myrmidon Reef (Queensland). Proc Fifth Int Coral Reef Congr Tahiti 6:149–154
Frieler K, Meinshausen M, Golly A, Mengel M, Lebek K, Donner SD, Hoegh-Guldberg O (2012) Limiting global warming to 2 C is unlikely to save most coral reefs. Nat Clim Chang 3:165–170
Gleeson MW, Strong AE (1995) Applying MCSST to coral reef bleaching. Adv Sp Res 16:151–154
Golbuu Y, Victor S, Penland L, Idip D, Emaurois C, Okaji K, Yukihira H, Iwase A, Van Woesik R (2007) Palau’s coral reefs show differential habitat recovery following the 1998-bleaching event. Coral Reefs 26:319–332
Grottoli G, Rodrigues LJ, Palardy JE (2006) Heterotrophic plasticity and resilience in bleached corals. Nature 440:10–13
Hendy EJ, Lough JM, Gagan MK (2003) Historical mortality in massive Porites from the central Great Barrier Reef, Australia: Evidence for past environmental stress? Coral Reefs 22:207–215
Heron SF, Liu G, Eakin CM, Skirving WJ, Muller-Karger FE, Vera-Rodriguez M, de la Cour JL, Burgess TFR, Strong AE, Geiger EF, Guild LS, Lynds S (2015) NOAA Technical Report NESDIS 145 Climatology Development for NOAA Coral Reef Watch’ s 5-km Product Suite. 30
Hoegh-Guldberg O, Smith GJ (1989) The effect of sudden changes in temperature, light and salinity on the population density and export of zooxanthellae from the reef corals Stylophora pistillata Esper and Seriatopora hystrix Dana. J Exp Mar Bio Ecol 129:279–303
Hoogenboom MO, Campbell DA, Beraud E, DeZeeuw K, Ferrier-Pagès C (2012) Effects of light, food availability and temperature stress on the function of photosystem II and photosystem I of coral symbionts. PLoS One 7
van Hooidonk R, Huber M (2009) Quantifying the quality of coral bleaching predictions. Coral Reefs 28:579–587
van Hooidonk R, Maynard J, Tamelander J, Gove J, Ahmadia G, Raymundo L, Williams G, Heron SF, Planes S (2016) Local-scale projections of coral reef futures and implications of the Paris Agreement. Sci Rep 6:39666
Hudson JH, Shinn EA, Halley RB, Lidz B (1976) Sclerochronology: A tool for interpreting past environments. Geology 4:361–364
Hughes TP, Anderson KD, Connolly SR, Heron SF, Kerry JT, Lough JM, Baird AH, Baum JK, Berumen ML, Bridge TC, Claar DC (2018) Spatial and temporal patterns of mass bleaching of corals in the Anthropocene. Science 359(80):80–83
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, Kuo C, 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 543:373–377
IPCC AR5 (2014) Climate Change 2014: Synthesis Report
Kessler WS, Kleeman R (2000) Rectification of the Madden-Julian Oscillation into the ENSO cycle. J Clim 13:3560–3575
Liu G, Strong AE, Skirving WJ, Arzayus F (2006) Overview of NOAA Coral Reef Watch Program’s Near-Real- Time Satellite Global Coral Bleaching Monitoring Activities. Proc 10th Int Coral Reef Symp 1783–1793
Logan CA, Dunne JP, Eakin CM, Donner SD (2014) Incorporating adaptive responses into future projections of coral bleaching. Glob Chang Biol 20:125–139
Lough JM, Anderson KD, Hughes TP (2018) Increasing thermal stress for tropical coral reefs: 1871–2017. Sci Rep 1–8
Mallela J, Hetzinger S, Halfar J (2015) Thermal stress markers in Colpophyllia natans provide an archive of site-specific bleaching events. Coral Reefs 35:181–186
Mangubhai S, Rotjan R, de Villiers S, Braun C, Carilli J, Cavin J, Cohen A, Coker D, Cook C, Drenkard L, Gawne P, Harper S, Koethen J, Lasley R, Nand Y, Payet S, Rivera H, Sandin S, Kiareti A, Thorrold S, Young CC, Zgliczynski B (2015) Phoenix Islands Protected Area 2015 Expedition Report
Mantel N, Haenszel W (1959) Issue Cover 22(4), April 1959 < Previous Next > Statistical Aspects of the Analysis of Data From Retrospective Studies of Disease. J Natl Cancer Inst 22:719–748
Matson EG (2011) Core Plugs. Encycl Mod Coral Reefs 294–296
Maynard JA, Anthony KRN, Marshall PA, Masiri I (2008) Major bleaching events can lead to increased thermal tolerance in corals. Mar Biol 155:173–182
McClanahan TR, Ateweberhan M, Muhando C, Maina J, Mohammed SM (2007) Climate change and spatio-temporal variation in seawater temperature effects on coral bleaching and mortality in East Africa. Ecol Monogr 77:503–525
Obura D, Mangubhai S (2011) Coral mortality associated with thermal fluctuations in the Phoenix Islands, 2002–2005. Coral Reefs 30:607–619
Oliver TA, Palumbi SR (2011) Do fluctuating temperature environments elevate coral thermal tolerance? Coral Reefs 30:429–440
Pandolfi JM, Connolly SR, Marshall DJ, Cohen AL (2011) Projecting Coral Reef Futures Under Global Warming and Ocean Acidification. Science 333(80):418–422
Pratchett M, Munday P, Wilson S, Graham N, Cinner J, Bellwood D, Jones G, Polunin N, Mcclanahan T (2008) Effects Of Climate-Induced Coral Bleaching On Coral-Reef Fishes - Ecological And Economic Consequences
Reynolds RW, Rayner NA, Smith TM, Stokes DC, Wang W (2002) An Improved In Situ and Satellite SST Analysis for Climate. J Clim 15:1609–1625
Rodrigues LJ, Grottoli AG (2006) Calcification rate and the stable carbon, oxygen, and nitrogen isotopes in the skeleton, host tissue, and zooxanthellae of bleached and recovering Hawaiian corals. Geochim Cosmochim Acta 70:2781–2789
Rowan R, Knowlton N, Baker A, Jara J (1997) Landscape ecology of algal symbionts creates variation in episodes of coral bleaching. Nature 388:265–269
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. Nat Commun 9:1–12
Smithers SG, Woodroffe CD (2001) Coral microatolls and 20th century sea level in the eastern Indian Ocean. Earth Planet Sci Lett 191:173–184
Trenberth KE (1997) The Definition of El Nino. Am Meteorol Soc
Vargas-Ángel B, Looney EE, Vetter OJ, Coccagna EF (2011) Severe, widespread El Niño-associated coral bleaching in the US Phoenix Islands. Bull Mar Sci 87:623–638
Wilkinson C (2008) Status of Coral Reefs of the World: Executive Summary. Glob Coral Reef Monit Netw 5–28
Van Woesik R, Houk P, Isechal AL, Idechong JW, Victor S, Golbuu Y (2012) Climate-change refugia in the sheltered bays of Palau: Analogs of future reefs. Ecol Evol 2:2474–2484
Van Woesik R, Sakai K, Ganase A, Loya Y (2011) Revisiting the winners and the losers a decade after coral bleaching. Mar Ecol Prog Ser 434:67–76
Wooldridge SA (2009) Water quality and coral bleaching thresholds: Formalising the linkage for the inshore reefs of the Great Barrier Reef, Australia. Mar Pollut Bull 58:745–751
Acknowledgements
We gratefully acknowledge the Government of Kiribati and the Phoenix Islands Marine Protected Area (PIPA) Trust for access to the PIPA and for permission to core corals on Maiana and in the PIPA. The US Fish and Wildlife granted permission to collect coral samples on Jarvis and Howland Islands. Fieldwork on Dongsha Atoll was conducted with the support and permission of the Dongsha Atoll Research Station. We thank the Palau International Coral Reef Center and the Palau Bureau of Marine Resources for logistical support and permission to sample corals on Palau. We thank the Coastal Zone Management Unit, Government of Barbados, the Ministry of the Environment on Martinique, and the Carmabi Foundation, Curacao for assistance with permitting and coral sampling on the Caribbean Islands. Fieldwork on Jarvis, Howland, Maiana, Martinique, Barbados and Curacao was made possible by Pangaea Exploration and their vessel Seadragon, Captain Eric Loss and his crew. We are extremely grateful for their expertise, enthusiasm and continued support of our mission. Funding was provided by the National Science Foundation (NSF OCE 1737311 and 1601365 to ALC, a WHOI Access to the Sea Award to ALC, and the Atlantic Donor Advised Fund to ALC. The National Science Foundation Graduate Research Fellowship supported AA, TD, and HB, the National Defense Science and Engineering Graduate Fellowship supported HR, the Woods Hole Oceanographic Institution Summer Student Fellowship and the Cornell Hunter R. Rawlings III Presidential Research Scholars Program supported CSB. The Prince Albert 2 of Monaco Foundation, the Akiko Shiraki Dynner Fund, the New England Aquarium, the Martin Family Society Fellowship for Sustainability, the Gates Millenium Scholarship, American Association for University Women American Dissertation Fellowship, the NOAA Coral Reef Conservation Program, and the Ocean Ventures Fund at Woods Hole Oceanographic Institution also provided support. Additional operational support was provided by the scientific staff of the NOAA’s Pacific Islands Fisheries Science Center and the officers and crew of the NOAA ship Hi'ialakai. The views expressed are the authors’ own and not necessarily those of the U.S. Government.
Author information
Authors and Affiliations
Corresponding authors
Additional information
Topic Editor Morgan S. Pratchett
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Mollica, N.R., Cohen, A.L., Alpert, A.E. et al. Skeletal records of bleaching reveal different thermal thresholds of Pacific coral reef assemblages. Coral Reefs 38, 743–757 (2019). https://doi.org/10.1007/s00338-019-01803-x
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00338-019-01803-x