Abstract
During 2015–2016, an El Niño and associated warm water event caused widespread coral bleaching across the equatorial Pacific. Here, we combine 8 yr of benthic monitoring data from permanent photoquadrats with remotely sensed and in situ temperature measurements to assess the impact of the warming event on benthic communities at Palmyra Atoll. We quantified bleaching prevalence across two distinct reef habitats using the best available data. On the fore reef (~ 10 m depth), we quantified bleaching severity within 100–200 m2 large-area plots using the custom visualization and analysis software, Viscore. On the reef terrace (~ 5 m depth), we used 95 focal colonies across three species that have been monitored annually since 2014. The 2015–2016 warm water event was the most extreme such event recorded on Palmyra in the past several decades with a maximum cumulative heat stress (degree heating weeks) of 11.9 °C-weeks. On the fore reef, 90% of live coral cover exhibited some degree of bleaching (32% severe bleaching). On the shallow reef terrace, bleaching was observed in 93% of the focal colonies across all species. Overall, coral cover declined 9% on the fore reef from 2014 to 2017, whereas coral cover did not change on the terrace. These contrasting results may be associated with typical daily temperature ranges on the terrace that are three times greater than on the fore reef. Permanent photoquadrats showed that turf algae initially colonized skeletons of recently dead corals but transitioned to crustose coralline algae within a year. Collectively, our study emphasizes that comprehensive monitoring of benthic communities over time combined with in situ temperature data can provide taxonomically precise trajectories of community change during and following thermal stress.
This is a preview of subscription content,
to check access.



Similar content being viewed by others
References
Baird AH, Marshall PA (2002) Mortality, growth and reproduction in scleractinian corals following bleaching on the Great Barrier Reef. Marine Ecology Progress Series 237:133–141
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. Estuarine, Coastal and Shelf Science 80:435–471
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, 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
Barott KL, Williams GJ, Vermeij MJA, Harris J, Smith JE, Rohwer FL, Sandin SA (2012) Natural history of coral – algae competition across a gradient of human activity in the Line Islands. Marine Ecology Progress Series 460:1–12
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
Berkelmans R, van Oppen MJ (2006) The role of zooxanthellae in the thermal tolerance of corals: a ‘nugget of hope’ for coral reefs in an era of climate change. Proc Biol Sci 273:2305–2312
Brainard RE, Maragos J, Schroeder R, Kenyon J, Vroom P, Godwin S, Hoeke R, Aeby G, Moffitt R, Lammers M, Gove J, Timmers M, Holzwarth S, Kolinski S (2010) The State of Coral Reef Ecosystems of the U.S.: Pacific Remote Island Areas, NOAA
Brainard RE, Oliver T, McPhaden MJ, Cohen A, Venegas R, Heenan A, Vargas-Ángel B, Rotjan R, Mangubhai S, Flint E (2018) Ecological Impacts of the 2015/16 El Niño in the Central Equatorial Pacific. Bulletin of the American Meteorological Society 99:S21–S26
Bresnahan PJ, Martz TR, Takeshita Y, Johnson KS, LaShomb M (2014) Best practices for autonomous measurements of seawater pH with the Honeywell Durafet. Methods in Oceanography 9:44–60
Brown BE (1997) Coral bleaching: causes and consequences. Coral reefs 16:S129–S138
Buddemeier RW, Fautin DG (1993) Coral bleaching as an adaptive mechanism. Bioscience 43:320–326
Burns JHR, Delparte D, Gates RD, Takabayashi M (2015) Integrating structure-from-motion photogrammetry with geospatial software as a novel technique for quantifying 3D ecological characteristics of coral reefs. PeerJ 3:e1077
Claar DC, Szostek L, McDevitt-Irwin JM, Schanze JJ, Baum JK (2018) Global patterns and impacts of El Niño events on coral reefs: A meta-analysis. PLOS ONE 13:e0190957
Connell JH (1997) Disturbance and recovery of coral assemblages. Coral reefs 16:S101–S113
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
Cunning R, Ritson-Williams R, Gates RD (2016) Patterns of bleaching and recovery of Montipora capitata in Kāne ‘ohe Bay, Hawai ‘i, USA. Marine Ecology Progress Series 551:131–139
DeCarlo TM, Cohen AL, Wong GTF, Davis KA, Lohmann P, Soong K (2017) Mass coral mortality under local amplification of 2 °C ocean warming. Scientific Reports 7:44586
Diaz-Pulido G, McCook LJ (2002) The fate of bleached corals patterns and dynamics of algal recruitment. Marine Ecology Progress Series 232:115–128
Donner SD (2011) An evaluation of the effect of recent temperature variability on the prediction of coral bleaching events. Ecological Applications 21:1718–1730
Eakin CM, Liu G, Gomez AM, De La Cour JL, Heron SF, Skirving WJ, Geiger EF, Tirak KV, Strong AE (2016) Global coral bleaching 2014–2017: status and an appeal for observations. Reef Encounter 31:20–26
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 J-P, Marks K, Mihaly J, Miller WJ, Mueller EM, Muller EM, Orozco Toro CA, Oxenford HA, Ponce-Taylor D, Quinn N, Ritchie KB, Rodríguez S, Ramírez AR, Romano S, Samhouri JF, Sánchez JA, Schmahl GP, Shank BV, 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:e13969
Edmunds PJ, Adjeroud M, Baskett ML, Baums IB, Budd AF, Carpenter RC, Fabina NS, Fan T-Y, Franklin EC, Gross K (2014) Persistence and change in community composition of reef corals through present, past, and future climates. PLoS One 9:e107525
Edwards CB, Eynaud Y, Williams GJ, Pedersen NE, Zgliczynski BJ, Gleason ACR, Smith JE, Sandin SA (2017) Large-area imaging reveals biologically driven non-random spatial patterns of corals at a remote reef. Coral Reefs 36:1291–1305
Edwards CB, Friedlander AM, Green AG, Hardt MJ, Sala E, Sweatman HP, Williams ID, Zgliczynski B, Sandin SA, Smith JE (2014) Global assessment of the status of coral reef herbivorous fishes: evidence for fishing effects. Proc R Soc B 281
Fox MD, Williams GJ, Johnson MD, Kelly ELA, Radice VA, Zgliczynski BJ, Rohwer FL, Sandin SA, Smith JE (2018) Gradients in primary production predict trophic strategies of mixotrophic corals across spatial scales. Current Biology 28:1–9
Furby KA, Smith JE, Sandin SA (2017) Porites superfusa mortality and recovery from a bleaching event at Palmyra Atoll, USA. PeerJ 5:e3204
Gove JM, Williams GJ, McManus MA, Heron SF, Sandin SA, Vetter OJ, Foley DG (2013) Quantifying climatological ranges and anomalies for Pacific coral reef ecosystems. PLoS ONE 8:e61974
Graham NAJ, Jennings S, MacNeil MA, Mouillot D, Wilson SK (2015) Predicting climate-driven regime shifts versus rebound potential in coral reefs. Nature 518:94–97
Grottoli AG, Rodrigues LJ (2011) Bleached Porites compressa and Montipora capitata corals catabolize δ13C-enriched lipids. Coral Reefs 30:687–692
Grottoli AG, Rodrigues LJ, Palardy JE (2006) Heterotrophic plasticity and resilience in bleached corals. Nature 440:1186–1189
Grottoli AG, Warner ME, Levas SJ, Aschaffenburg MD, Schoepf V, McGinley M, Baumann J, Matsui Y (2014) The cumulative impact of annual coral bleaching can turn some coral species winners into losers. Global Change Biology 20:3823–3833
Guest JR, Baird AH, Maynard JA, Muttaqin E, Edwards AJ, Campbell SJ, Yewdall K, Affendi YA, Chou LM (2012) Contrasting Patterns of Coral Bleaching Susceptibility in 2010 Suggest an Adaptive Response to Thermal Stress. PLOS ONE 7:e33353
Guest JR, Low J, Tun K, Wilson B, Ng C, Raingeard D, Ulstrup KE, Tanzil JTI, Todd PA, Toh TC, McDougald D, Chou LM, Steinberg PD (2016) Coral community response to bleaching on a highly disturbed reef. Scientific Reports 6:20717
Hamilton SL, Smith JE, Price NN, Sandin SA (2014) Quantifying patterns of fish herbivory on Palmyra Atoll (USA), an uninhabited predator-dominated central Pacific coral reef. Marine Ecology Progress Series 501:141–155
Harrington L, Fabricius K, De’Ath G, Negri A (2004) Recognition and selection of settlement substrata determine post-settlement survival in corals. Ecology 85:3428–3437
Hedley JD, Roelfsema CM, Chollett I, Harborne AR, Heron SF, Weeks S, Skirving WJ, Strong AE, Eakin CM, Christensen TRL (2016) Remote sensing of coral reefs for monitoring and management: a review. Remote Sensing 8:118
Hoegh-Guldberg O, Salvat B (1995) Periodic mass-bleaching and elevated sea temperatures: bleaching of outer reef slope communities in Moorea, French Polynesia. Marine ecology progress series 121:181–190
Hughes TP, Graham NA, Jackson JB, Mumby PJ, Steneck RS (2010) Rising to the challenge of sustaining coral reef resilience. Trends Ecol Evol 25:633–642
Hughes TP, Kerry JT, Álvarez-Noriega M, Álvarez-Romero JG, Anderson KD, Baird AH, Babcock RC, Beger M, Bellwood DR, Berkelmans R (2017) Global warming and recurrent mass bleaching of corals. Nature 543:373–377
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 H, Hobbs J-PA, Hoey AS, 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 359:80–83
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
Hughes TP, Rodrigues MJ, Bellwood DR, Ceccarelli D, Hoegh-Guldberg O, McCook L, Moltschaniwskyj N, Pratchett MS, Steneck RS, Willis B (2007) Phase Shifts, Herbivory, and the Resilience of Coral Reefs to Climate Change. Current Biology 17:360–365
Kayanne H, Harii S, Ide Y, Akimoto F (2002) Recovery of coral populations after the 1998 bleaching on Shiraho Reef, in the southern Ryukyus, NW Pacific. Marine Ecology Progress Series 239:93–103
Kilpatrick KA, Podesta GP, Evans R (2001) Overview of the NOAA/NASA advanced very high resolution radiometer Pathfinder algorithm for sea surface temperature and associated matchup database. J Geophys Res 106:9179–9197
Liu G, Heron S, Eakin C, Muller-Karger F, Vega-Rodriguez M, Guild L, De La Cour J, Geiger E, Skirving W, Burgess T, Strong A, Harris A, Maturi E, Ignatov A, Sapper J, Li J, Lynds S (2014) Reef-Scale Thermal Stress Monitoring of Coral Ecosystems: New 5-km Global Products from NOAA Coral Reef Watch. Remote Sensing 6:11579
Logan CA, Dunne JP, Eakin CM, Donner SD (2014) Incorporating adaptive responses into future projections of coral bleaching. Global Change Biology 20:125–139
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
Magel JMT, Burns JHR, Gates RD, Baum JK (2019) Effects of bleaching-associated mass coral mortality on reef structural complexity across a gradient of local disturbance. Scientific Reports 9:2512
McClanahan TR (2017) Changes in coral sensitivity to thermal anomalies. Marine Ecology Progress Series 570:71–85
Mizerek TL, Baird AH, Madin JS (2018) Species traits as indicators of coral bleaching. Coral Reefs 37:791–800
Morse DE, Hooker N, Morse ANC, Jensen RA (1988) Control of larval metamorphosis and recruitment in sympatric agariciid corals. Journal of Experimental Marine Biology and Ecology 116:193–217
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 R Soc B 284:20171551
Mullen AD, Treibitz T, Roberts PL, Jaffe JS (2017) An Underwater Microscope for In Situ Imaging of Seafloor Organism Novel Techniques in Microscopy. Optical Society of America, p NTu1C. 1
Murfitt SL, Allan BM, Bellgrove A, Rattray A, Young MA, Ierodiaconou D (2017) Applications of unmanned aerial vehicles in intertidal reef monitoring. Scientific reports 7:10259
Naughton P, Edwards C, Petrovic V, Kastner R, F. K, Sandin S (2015) Scaling the annotation of subtidal marine habitats Proceedings of the 10th International Conference on Underwater Networks and Systems 31
Nyström M, Folke C, Moberg F (2000) Coral reef disturbance and resilience in a human-dominated environment. Trends in Ecology & Evolution 15:413–417
Obura D, Mangubhai S (2011) Coral mortality associated with thermal fluctuations in the Phoenix Islands, 2002–2005. Coral Reefs 30:607–619
Petrovic V, Vanoni D, Richter A, Levy T, Kuester F (2014) Visualizing high resolution three-dimensional and two-dimensional data of cultural heritage sites. Mediterranean Archaeology and Archaeometry 14:93–100
Pizarro O, Eustice RM, Singh H (2009) Large area 3-D reconstructions from underwater optical surveys. IEEE Journal of Oceanic Engineering 34:150–169
Rogers JS, Monismith SG, Fringer OB, Koweek DA, Dunbar RB (2017) A coupled wave-hydrodynamic model of an atoll with high friction: Mechanisms for flow, connectivity, and ecological implications. Ocean Modelling 110:66–82
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
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 JB, Knowlton N, Sala E (2008) Baselines and degradation of coral reefs in the Northern Line Islands. PLoS One 3:e1548
Smith JE, Brainard R, Carter A, Grillo S, Edwards C, Harris J, Lewis L, Obura D, Rohwer F, Sala E, Vroom P, Sandin S (2016) Re-evaluating the health of coral reef communities: baselines and evidence for human impacts across the central Pacific. Proc R Soc B 283:20151985
Smith JE, Hunter CL, Smith CM (2010) The effects of top-down versus bottom-up control on benthic coral reef community structure. Oecologia 163:497–507
Tebben J, Motti CA, Siboni N, Tapiolas DM, Negri AP, Schupp PJ, Kitamura M, Hatta M, Steinberg PD, Harder T (2015) Chemical mediation of coral larval settlement by crustose coralline algae. Scientific Reports 5:10803
Thomas L, Rose NH, Bay RA, López EH, Morikawa MK, Ruiz-Jones L, Palumbi SR (2018) Mechanisms of Thermal Tolerance in Reef-Building Corals across a Fine-Grained Environmental Mosaic: Lessons from Ofu, American Samoa. Frontiers in Marine Science 4:434
van Woesik R, Sakai K, Ganase A, Loya Y (2011) Revisiting the winners and the losers a decade after coral bleaching. Marine Ecology Progress Series 434:67–76
Wall M, Putchim L, Schmidt GM, Jantzen C, Khokiattiwong S, Richter C (2015) Large-amplitude internal waves benefit corals during thermal stress. Proceedings of the Royal Society of London B Biological Sciences 282:20140650
Wiedenmann J, D’Angelo C, Smith EG, Hunt AN, Legiret F-E, Postle AD, Achterberg EP (2012) Nutrient enrichment can increase the susceptibility of reef corals to bleaching. Nature Climate Change 3:160–164
Williams GJ, Knapp IS, Maragos JE, Davy SK (2010) Modeling patterns of coral bleaching at a remote Central Pacific atoll. Marine Pollution Bulletin 60:1467–1476
Williams GJ, Sandin SA, Zgliczynski B, Fox MD, Furby K, Gove JM, Rogers JS, Hartmann AC, Caldwell ZR, Price NN, Smith JE (2018) Biophysical drivers of coral trophic depth zonation. Marine Biology 165:60
Yeh S-W, Kug J-S, Dewitte B, Kwon M-H, Kirtman BP, Jin F-F (2009) El Niño in a changing climate. Nature 461:511–514
Acknowledgements
We thank The Nature Conservancy, the US Fish and Wildlife Service and the Palmyra Atoll Research Consortium, for logistical support and access to the refuge. This research was conducted under special use permits #12533-14016 and #12533-14012. Funding to support field work was provided by NSF CRI-OA-1316047, NFWF #0302.16.053589 and generous donations from the Scripps Family Foundation, and the Bohn and Grand families. MF was supported by a NOAA Nancy Foster Scholarship.
Author information
Authors and Affiliations
Corresponding authors
Ethics declarations
Conflict of interest
On behalf of all authors, the corresponding author states that there is no conflict of interest.
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
Fox, M.D., Carter, A.L., Edwards, C.B. et al. Limited coral mortality following acute thermal stress and widespread bleaching on Palmyra Atoll, central Pacific. Coral Reefs 38, 701–712 (2019). https://doi.org/10.1007/s00338-019-01796-7
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00338-019-01796-7