Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

Coral reef survival under accelerating ocean deoxygenation

Abstract

Global warming and local eutrophication simultaneously lower oxygen (O2) saturation and increase biological O2 demands to cause deoxygenation. Tropical shallow waters, and their coral reefs, are particularly vulnerable to extreme low O2 (hypoxia) events. These events can drive mass mortality of reef biota; however, they currently remain unaccounted for when considering coral reef persistence under local environmental alterations and global climatic change. In this Perspective, we integrate existing biological, ecological and geochemical evidence to consider how O2 availability and hypoxia affect reef biota, with particular focus on the ecosystem architects, reef-building corals, that operate as both O2 consumers and producers. We pinpoint fundamental knowledge gaps and highlight the need to understand sub-lethal hypoxia effects that are likely already in play.

Access options

Rent or Buy article

Get time limited or full article access on ReadCube.

from$8.99

All prices are NET prices.

Fig. 1: Geological reconstructed atmospheric O2, CO2 and global mean temperatures, and recent and projected oceanic dissolved O2, sea surface pH and temperature.
Fig. 2: Hypoxia thresholds and diurnal-dissolved O2 changes.
Fig. 3: Important biotic and abiotic processes affecting hypoxia exposure in tropical reefs from the ecosystem to molecular level.

References

  1. 1.

    Costanza, R. et al. Changes in the global value of ecosystem services. Glob. Environ. Chang. 26, 152–158 (2014).

    Google Scholar 

  2. 2.

    LaJeunesse, T. C. et al. Systematic revision of Symbiodiniaceae highlights the antiquity and diversity of coral endosymbionts. Curr. Biol. 28, 2570–2580 (2018).

    CAS  Google Scholar 

  3. 3.

    Hughes, T. P. et al. Coral reefs in the Anthropocene. Nature 546, 82–90 (2017).

    CAS  Google Scholar 

  4. 4.

    Breitburg, D. et al. Declining oxygen in the global ocean and coastal waters. Science 359, eaam7240 (2018).

    Google Scholar 

  5. 5.

    D. Laffoley, D. & Baxter, J. M. (eds) Ocean Deoxygenation: Everyone’s Problem. Causes, Impacts, Consequences and Solutions (IUCN, 2019).

  6. 6.

    Altieri, A. H. et al. Tropical dead zones and mass mortalities on coral reefs. Proc. Natl Acad. Sci. USA 114, 3660–3665 (2017).

    CAS  Google Scholar 

  7. 7.

    Johnson, M. D., Rodriguez, L. M. & Altieri, A. H. Shallow-water hypoxia and mass mortality on a Caribbean coral reef. B. Mar. Sci. 94, 143–144 (2018).

    Google Scholar 

  8. 8.

    Falkowski, P. G., Fenchel, T. & Delong, E. F. The microbial engines that drive Earth’s biogeochemical cycles. Science 320, 1034–1039 (2008).

    CAS  Google Scholar 

  9. 9.

    Bopp, L. et al. Multiple stressors of ocean ecosystems in the 21st century: projections with CMIP5 models. Biogeosciences 10, 6225–6245 (2013).

    Google Scholar 

  10. 10.

    Vaquer-Sunyer, R. & Duarte, C. M. Thresholds of hypoxia for marine biodiversity. Proc. Natl Acad. Sci. USA 105, 15452–15457 (2008).

    CAS  Google Scholar 

  11. 11.

    Diaz, R. & Rosenberg, R. Marine benthic hypoxia: a review of its ecological effects and the behavioural responses of benthic macrofauna. Oceanogr. Mar. Biol. An Annu. Rev. 33, 245–303 (1995).

    Google Scholar 

  12. 12.

    Nilsson, H. C. & Rosenberg, R. Succession in marine benthic habitats and fauna in response to oxygen deficiency: analysed by sediment profile-imaging and by grab samples. Mar. Ecol. Prog. Ser. 197, 139–149 (2000).

    Google Scholar 

  13. 13.

    Hobbs, J.-P. P. A. & Mcdonald, C. A. Increased seawater temperature and decreased dissolved oxygen triggers fish kill at the Cocos (Keeling) Islands, Indian Ocean. J. Fish Biol. 77, 1219–1229 (2010).

    Google Scholar 

  14. 14.

    Rabalais, N. N. et al. Dynamics and distribution of natural and human-caused hypoxia. Biogeosciences 7, 585–619 (2010).

    CAS  Google Scholar 

  15. 15.

    Levin, L. A. & Breitburg, D. L. Linking coasts and seas to address ocean deoxygenation. Nat. Clim. Change 5, 401–403 (2015).

    Google Scholar 

  16. 16.

    Hoegh-Guldberg, O., Poloczanska, E. S., Skirving, W. & Dove, S. Coral reef ecosystems under climate change and ocean acidification. Front. Mar. Sci. 4, 158 (2017).

    Google Scholar 

  17. 17.

    Hughes, T. P. et al. Global warming transforms coral reef assemblages. Nature 556, 492–496 (2018).

    CAS  Google Scholar 

  18. 18.

    Keeling, R. F., Körtzinger, A. & Gruber, N. Ocean deoxygenation in a warming world. Ann. Rev. Mar. Sci. 2, 199–229 (2010).

    Google Scholar 

  19. 19.

    Falkowski, P. G. et al. Ocean deoxygenation: past, present, and future. Eos (November 2011).

  20. 20.

    Clapham, M. E. & Payne, J. L. Acidification, anoxia, and extinction: a multiple logistic regression analysis of extinction selectivity during the Middle and Late Permian. Geology 39, 1059–1062 (2011).

    CAS  Google Scholar 

  21. 21.

    Clapham, M. E. & Renne, P. R. Flood basalts and mass extinctions. Annu. Rev. Earth Planet. Sci. 47, 275–303 (2019).

    CAS  Google Scholar 

  22. 22.

    Weidlich, O., Kiessling, W. & Flügel, E. Permian-Triassic boundary interval as a model for forcing marine ecosystem collapse by long-term atmospheric oxygen drop. Geology 31, 961–964 (2003).

    CAS  Google Scholar 

  23. 23.

    Pruss, S. B. & Bottjer, D. J. Late Early Triassic microbial reefs of the western United States: a description and model for their deposition in the aftermath of the end-Permian mass extinction. Palaeogeogr. Palaeocl. 211, 127–137 (2004).

    Google Scholar 

  24. 24.

    Penn, A. J. L., Deutsch, C., Payne, J. L. & Sperling, E. A. Temperature-dependent hypoxia explains biogeography and severity of end-Permian marine mass extinction. Science 362, eaat1327 (2018).

  25. 25.

    Payne, J. L. & Clapham, M. E. End-Permian mass extinction in the oceans: an ancient analog for the twenty-first century? Annu. Rev. Earth Planet. Sci. 40, 89–111 (2012).

    CAS  Google Scholar 

  26. 26.

    Dixon, G. B. et al. Genomic determinants of coral heat tolerance across latitudes. Science 348, 1460–1462 (2015).

    CAS  Google Scholar 

  27. 27.

    Kenkel, C. D., Moya, A., Strahl, J., Humphrey, C. & Bay, L. K. Functional genomic analysis of corals from natural CO2-seeps reveals core molecular responses involved in acclimatization to ocean acidification. Glob. Chang. Biol. 24, 158–171 (2017).

    Google Scholar 

  28. 28.

    Okazaki, R. R. et al. Species-specific responses to climate change and community composition determine future calcification rates of Florida Keys reefs. Glob. Chang. Biol. 23, 1023–1035 (2017).

    Google Scholar 

  29. 29.

    Hobbs, J. P. A. & Macrae, H. Unusual weather and trapped coral spawn lead to fish kill at a remote coral atoll. Coral Reefs 31, 961 (2012).

    Google Scholar 

  30. 30.

    Lapointe, B. E. & Matzie, W. R. Effects of stormwater nutrient discharges on eutrophication processes in nearshore waters of the Florida Keys. Estuaries 19, 422 (1996).

    CAS  Google Scholar 

  31. 31.

    Andréfouët, S., Dutheil, C., Menkes, C. E., Bador, M. & Lengaigne, M. Mass mortality events in atoll lagoons: environmental control and increased future vulnerability. Glob. Chang. Biol. 21, 195–205 (2015).

    Google Scholar 

  32. 32.

    Baird, A. H., Keith, S. A., Woolsey, E., Yoshida, R. & Naruse, T. Rapid coral mortality following unusually calm and hot conditions on Iriomote, Japan. F1000Res. 6, 1728 (2017).

    Google Scholar 

  33. 33.

    Lagos, M. E., Barneche, D. R., White, C. R. & Marshall, D. J. Do low oxygen environments facilitate marine invasions? Relative tolerance of native and invasive species to low oxygen conditions. Glob. Chang. Biol. 23, 2321–2330 (2017).

    Google Scholar 

  34. 34.

    Diaz, R. J. & Rosenberg, R. Spreading dead zones and consequences for marine ecosystems. Science 321, 926–929 (2008).

    CAS  Google Scholar 

  35. 35.

    Altieri, A. H. & Gedan, K. B. Climate change and dead zones. Glob. Chang. Biol. 21, 1395–1406 (2015).

    Google Scholar 

  36. 36.

    Mee, L. D., Friedrich, J. & Gomoiu, M. T. Restoring the Black Sea in times of uncertainty. Oceanography 18, 100–111 (2005).

    Google Scholar 

  37. 37.

    Norström, A. V., Nyström, M., Lokrantz, J. & Folke, C. Alternative states on coral reefs: Beyond coral-macroalgal phase shifts. Mar. Ecol. Prog. Ser. 376, 293–306 (2009).

    Google Scholar 

  38. 38.

    van de Leemput, I. A., Hughes, T. P., van Nes, E. H. & Scheffer, M. Multiple feedbacks and the prevalence of alternate stable states on coral reefs. Coral Reefs 35, 857–865 (2016).

    Google Scholar 

  39. 39.

    Nilsson, G. E. & Östlund-Nilsson, S. Hypoxia in paradise: widespread hypoxia tolerance in coral reef fishes. Proc. R. Soc. B Biol. Sci. 271, S30–S33 (2004).

    Google Scholar 

  40. 40.

    Scofield, V., Jacques, S. M. S., Guimarães, J. R. D. & Farjalla, V. F. Potential changes in bacterial metabolism associated with increased water temperature and nutrient inputs in tropical humic lagoons. Front. Microbiol. 6, 310 (2015).

    Google Scholar 

  41. 41.

    Roik, A. et al. Year-long monitoring of physico-chemical and biological variables provide a comparative baseline of coral reef functioning in the central Red Sea. PLoS ONE 11, e0163939 (2016).

    Google Scholar 

  42. 42.

    Camp, E. F. et al. Reef-building corals thrive within hot-acidified and deoxygenated waters. Sci. Rep. 7, 2434 (2017).

    Google Scholar 

  43. 43.

    Guadayol, Ò., Silbiger, N. J., Donahue, M. J. & Thomas, F. I. M. Patterns in temporal variability of temperature, oxygen and pH along an environmental gradient in a coral reef. PLoS ONE 9, e85213 (2014).

    Google Scholar 

  44. 44.

    Ruiz-Jones, L. J. & Palumbi, S. R. Transcriptome-wide changes in coral gene expression at noon and midnight under field conditions. Biol. Bull. 228, 227–241 (2015).

    CAS  Google Scholar 

  45. 45.

    Meire, L., Soetaert, K. E. R. & Meysman, F. J. R. Impact of global change on coastal oxygen dynamics and risk of hypoxia. Biogeosciences 10, 2633–2653 (2013).

    CAS  Google Scholar 

  46. 46.

    Camp, E. F. et al. Acclimatization to high-variance habitats does not enhance physiological tolerance of two key Caribbean corals to future temperature and pH. Proc. R. Soc. B Biol. Sci. 283, 20160442 (2016).

    Google Scholar 

  47. 47.

    Haas, A. F. et al. Global microbialization of coral reefs. Nat. Microbiol. 1, 16042 (2016).

    CAS  Google Scholar 

  48. 48.

    Wild, C., Niggl, W., Naumann, M. S. & Haas, A. F. Organic matter release by Red Sea coral reef organisms-potential effects on microbial activity and in situ O2 availability. Mar. Ecol. Prog. Ser. 411, 61–71 (2010).

    CAS  Google Scholar 

  49. 49.

    Bessell-Browne, P. et al. Impacts of turbidity on corals: the relative importance of light limitation and suspended sediments. Mar. Pollut. Bull. 117, 161–170 (2017).

    CAS  Google Scholar 

  50. 50.

    Guihen, D., White, M. & Lundälv, T. Zooplankton drive diurnal changes in oxygen concentration at Tisler cold-water coral reef. Coral Reefs 37, 1013–1025 (2018).

    Google Scholar 

  51. 51.

    Bridge, T. C. L., Hughes, T. P., Guinotte, J. M. & Bongaerts, P. Call to protect all coral reefs. Nat. Clim. Change 3, 528–530 (2013).

    Google Scholar 

  52. 52.

    Nilsson, G. E. & Östlund-Nilsson, S. Does size matter for hypoxia tolerance in fish? Biol. Rev. 83, 173–189 (2008).

    Google Scholar 

  53. 53.

    Haas, A. F., Smith, J. E., Thompson, M. & Deheyn, D. D. Effects of reduced dissolved oxygen concentrations on physiology and fluorescence of hermatypic corals and benthic algae. PeerJ 2, e235 (2014).

    Google Scholar 

  54. 54.

    Guzmán, H. M., Cortés, J., Glynn, P. W. & Richmond, R. H. Coral mortality associated with dinoflagellate blooms in the eastern Pacific (Costa Rica and Panama). Mar. Ecol. Prog. Ser. 60, 299–303

  55. 55.

    Adjeroud, M., Andréfouët, S. & Payri, C. Mass mortality of macrobenthic communities in the lagoon of Hikueru atoll (French Polynesia). Coral Reefs 19, 287–291 (2001).

    Google Scholar 

  56. 56.

    Laboy-Nieves, E. N. et al. Mass mortality of tropical marine communities in Morrocoy, Venezuela. B. Mar. Sci. 68, 163–179 (2001).

    Google Scholar 

  57. 57.

    Roder, C. et al. First biological measurements of deep-sea corals from the Red Sea. Sci. Rep. 3, 2802 (2013).

    CAS  Google Scholar 

  58. 58.

    Graham, N. A. J. & Nash, K. L. The importance of structural complexity in coral reef ecosystems. Coral Reefs 32, 315–326 (2013).

    Google Scholar 

  59. 59.

    Harrington, L., Fabricius, K., De’Ath, G. & Negri, A. Recognition and selection of settlement substrata determine post-settlement survival in corals. Ecology 85, 3428–3437 (2004).

    Google Scholar 

  60. 60.

    Mccoy, S. J. & Kamenos, N. A. Coralline algae (Rhodophyta) in a changing world: integrating ecological, physiological, and geochemical responses to global change. J. Phycol. 51, 6–24 (2015).

    Google Scholar 

  61. 61.

    Nilsson, G. E. & Östlund-Nilsson, S. Hypoxia tolerance in coral reef fishes. Fish Physiol. 21, 583–596 (2005).

    Google Scholar 

  62. 62.

    Wood, C. M. The fallacy of the Pcrit - are there more useful alternatives? J. Exp. Biol. 221, jeb163717 (2018).

    Google Scholar 

  63. 63.

    Regan, M. D. et al. Don’t throw the fish out with the respirometry water. J. Exp. Biol. 222, jeb200253 (2019).

    Google Scholar 

  64. 64.

    Grieshaber, M. K., Hardewig, I., Kreutzer, U. & Pörtner, H. O. in Reviews of Physiology, Biochemistry and Pharmacology Vol. 125 43–147 (Springer, 1993).

  65. 65.

    Speers-Roesch, B., Mandic, M., Groom, D. J. E. & Richards, J. G. Critical oxygen tensions as predictors of hypoxia tolerance and tissue metabolic responses during hypoxia exposure in fishes. J. Exp. Mar. Bio. Ecol. 449, 239–249 (2013).

    CAS  Google Scholar 

  66. 66.

    Herbert, N. A., Skjæraasen, J. E., Nilsen, T., Salvanes, A. G. V. & Steffensen, J. F. The hypoxia avoidance behaviour of juvenile Atlantic cod (Gadus morhua L.) depends on the provision and pressure level of an O2 refuge. Mar. Biol. 158, 737–746 (2011).

    Google Scholar 

  67. 67.

    Pichavant, K. et al. Comparative effects of long-term hypoxia on growth, feeding and oxygen consumption in juvenile turbot and European sea bass. J. Fish Biol. 59, 875–883 (2001).

    Google Scholar 

  68. 68.

    Kramer, D. L. Dissolved oxygen and fish behavior. Environ. Biol. Fishes 18, 81–92 (1987).

    Google Scholar 

  69. 69.

    Levin, L. A. et al. Effects of natural and human-induced hypoxia on coastal benthos. Biogeosciences 6, 2063–2098 (2009).

    CAS  Google Scholar 

  70. 70.

    Vaquer-Sunyer, R. & Duarte, C. M. Temperature effects on oxygen thresholds for hypoxia in marine benthic organisms. Glob. Chang. Biol. 17, 1788–1797 (2011).

    Google Scholar 

  71. 71.

    Patterson, M. R. A mass transfer explanation of metabolic scaling relations in some aquatic invertebrates and algae. Science 255, 1421–1423 (1992).

    CAS  Google Scholar 

  72. 72.

    Shapiro, O. H. et al. Vortical ciliary flows actively enhance mass transport in reef corals. Proc. Natl Acad. Sci. USA 111, 13391–13396 (2014).

    CAS  Google Scholar 

  73. 73.

    Yum, L. K. et al. Transcriptomes and expression profiling of deep-sea corals from the Red Sea provide insight into the biology of azooxanthellate corals. Sci. Rep. 7, 6442 (2017).

    Google Scholar 

  74. 74.

    Lunden, J. J., McNicholl, C. G., Sears, C. R., Morrison, C. L. & Cordes, E. E. Acute survivorship of the deep-sea coral Lophelia pertusa from the Gulf of Mexico under acidification, warming, and deoxygenation. Front. Mar. Sci. 1, 78 (2014).

    Google Scholar 

  75. 75.

    Dodds, L. A., Roberts, J. M., Taylor, A. C. & Marubini, F. Metabolic tolerance of the cold-water coral Lophelia pertusa (Scleractinia) to temperature and dissolved oxygen change. J. Exp. Mar. Biol. Ecol. 349, 205–214 (2007).

    CAS  Google Scholar 

  76. 76.

    Kremien, M., Shavit, U., Mass, T. & Genin, A. Benefit of pulsation in soft corals. Proc. Natl Acad. Sci. USA 110, 8978–8983 (2013).

    CAS  Google Scholar 

  77. 77.

    Shick, J. M., Malcolm, J. & Shick, J. M. Diffusion limitation and hyperoxic enhancement of oxygen consumption in zooxanthellate sea anemones, zoanthids, and corals. Biol. Bull. 179, 148–158 (1990).

    CAS  Google Scholar 

  78. 78.

    Jørgensen, B. B. & Revsbech, N. P. Diffusive boundary layers and the oxygen uptake of sediments and detritus. Limnol. Oceanogr. 30, 111–122 (1985).

    Google Scholar 

  79. 79.

    Kühl, M., Cohen, Y., Dalsgaard, T., Jørgensen, B. B. & Revsbech, N. P. Microenvironment and photosynthesis of zooxanthellae in scleractinian corals studied with microsensors for O2, pH and light. Mar. Ecol. Prog. Ser. 117, 159–177 (1995).

    Google Scholar 

  80. 80.

    Jørgensen, B. B. & Des Marais, D. J. The diffusive boundary layer of sediments: oxygen microgradients over a microbial mat. Limnol. Oceanogr. 35, 1343–1355 (1990).

    Google Scholar 

  81. 81.

    De Beer, D., Kühl, M., Stambler, N. & Vaki, L. A microsensor study of light enhanced Ca2+ uptake and photosynthesis in the reef-building hermatypic coral Favia sp. Mar. Ecol. Prog. Ser. 194, 75–85 (2000).

    Google Scholar 

  82. 82.

    Nelson, H. R. & Altieri, A. H. Oxygen: the universal currency on coral reefs. Coral Reefs 38, 177–198 (2019).

    Google Scholar 

  83. 83.

    Chindapol, N., Kaandorp, J. A., Cronemberger, C., Mass, T. & Genin, A. Modelling growth and form of the scleractinian coral Pocillopora verrucosa and the influence of hydrodynamics. PLoS Comput. Biol. 9, e1002849 (2013).

    CAS  Google Scholar 

  84. 84.

    Ong, R. H., King, A. J. C., Kaandorp, J. A., Mullins, B. J. & Caley, M. J. The effect of allometric scaling in coral thermal microenvironments. PLoS ONE 12, e0184214 (2017).

    Google Scholar 

  85. 85.

    Ferguson, N., White, C. R. & Marshall, D. J. Competition in benthic marine invertebrates: the unrecognized role of exploitative competition for oxygen. Ecology 94, 126–135 (2013).

    Google Scholar 

  86. 86.

    Suggett, D. J., Warner, M. E. & Leggat, W. Symbiotic dinoflagellate functional diversity mediates coral survival under ecological crisis. Trends Ecol. Evol. 32, 735–745 (2017).

    Google Scholar 

  87. 87.

    Hadaidi, G. et al. Stable mucus-associated bacterial communities in bleached and healthy corals of Porites lobata from the Arabian Seas. Sci. Rep. 7, 45362 (2017).

    CAS  Google Scholar 

  88. 88.

    Sunagawa, S. et al. Bacterial diversity and White Plague Disease-associated community changes in the Caribbean coral Montastraea faveolata. ISME J. 3, 512–521 (2009).

    CAS  Google Scholar 

  89. 89.

    Roder, C. et al. Bacterial profiling of White Plague Disease in a comparative coral species framework. ISME J. 8, 31–39 (2014).

    CAS  Google Scholar 

  90. 90.

    Jessen, C. et al. In-situ effects of eutrophication and overfishing on physiology and bacterial diversity of the Red Sea coral Acropora hemprichii. PLoS ONE 8, e62091 (2013).

    CAS  Google Scholar 

  91. 91.

    Bourne, D., Iida, Y., Uthicke, S. & Smith-Keune, C. Changes in coral-associated microbial communities during a bleaching event. ISME J. 2, 350–363 (2008).

    CAS  Google Scholar 

  92. 92.

    Ziegler, M., Seneca, F. O., Yum, L. K., Palumbi, S. R. & Voolstra, C. R. Bacterial community dynamics are linked to patterns of coral heat tolerance. Nat. Commun. 8, 14213 (2017).

    CAS  Google Scholar 

  93. 93.

    Ray, P. D., Huang, B. W. & Tsuji, Y. Reactive oxygen species (ROS) homeostasis and redox regulation in cellular signaling. Cell. Signal. 24, 981–990 (2012).

    CAS  Google Scholar 

  94. 94.

    Taabazuing, C. Y., Hangasky, J. A. & Knapp, M. J. Oxygen sensing strategies in mammals and bacteria. J. Inorg. Biochem. 133, 63–72 (2014).

    CAS  Google Scholar 

  95. 95.

    Kaelin, W. G. & Ratcliffe, P. J. Oxygen sensing by metazoans: the central role of the HIF hydroxylase pathway. Mol. Cell 30, 393–402 (2008).

    CAS  Google Scholar 

  96. 96.

    Loenarz, C. et al. The hypoxia-inducible transcription factor pathway regulates oxygen sensing in the simplest animal, Trichoplax adhaerens. EMBO Rep. 12, 63–70 (2011).

    CAS  Google Scholar 

  97. 97.

    Rytkönen, K. T., Williams, T. A., Renshaw, G. M., Primmer, C. R. & Nikinmaa, M. Molecular evolution of the metazoan PHD-HIF oxygen-sensing system. Mol. Biol. Evol. 28, 1913–1926 (2011).

    Google Scholar 

  98. 98.

    Semenza, G. L. Oxygen sensing, homeostasis, and disease. N. Engl. J. Med. 365, 537–547 (2011).

    CAS  Google Scholar 

  99. 99.

    Chandel, N. S. et al. Reactive oxygen species generated at mitochondrial complex III stabilize hypoxia-inducible factor-1alpha during hypoxia: a mechanism of O2 sensing. J. Biol. Chem. 275, 25130–25138 (2000).

    CAS  Google Scholar 

  100. 100.

    Mansfield, K. D. et al. Mitochondrial dysfunction resulting from loss of cytochrome c impairs cellular oxygen sensing and hypoxic HIF-α activation. Cell Metab. 1, 393–399 (2005).

    CAS  Google Scholar 

  101. 101.

    Mills, D. B. et al. The last common ancestor of animals lacked the HIF pathway and respired in low-oxygen environments. eLife 7, e31176 (2018).

  102. 102.

    Levy, O. et al. Complex Diel cycles of gene expression in coral-algal symbiosis. Science 331, 175 (2011).

  103. 103.

    DeSalvo, M. K., Estrada, A., Sunagawa, S. & Medina, M. Transcriptomic responses to darkness stress point to common coral bleaching mechanisms. Coral Reefs 31, 215–228 (2012).

    Google Scholar 

  104. 104.

    Zoccola, D. et al. Structural and functional analysis of coral hypoxia inducible factor. PLoS ONE 12, e0186262 (2017).

    Google Scholar 

  105. 105.

    Kumar, H. & Choi, D.-K. Hypoxia inducible factor pathway and physiological adaptation: a cell survival pathway? Mediat. Inflamm. 2015, 584758 (2015).

    Google Scholar 

  106. 106.

    Pelster, B. & Egg, M. Multiplicity of hypoxia-inducible transcription factors and their connection to the circadian clock in the Zebrafish. Physiol. Biochem. Zool. 88, 146–157 (2015).

    Google Scholar 

  107. 107.

    Suggett, D. J. et al. Photosynthesis and production of hydrogen peroxide by Symbiodinium (Pyrrhophyta) phylotypes with different thermal tolerances. J. Phycol. 44, 948–956 (2008).

    CAS  Google Scholar 

  108. 108.

    Hawkins, T. D. & Davy, S. K. Nitric oxide production and tolerance differ among symbiodinium types exposed to heat stress. Plant Cell Physiol. 53, 1889–1898 (2012).

    CAS  Google Scholar 

  109. 109.

    Yoshida, R., Naruse, T., Baird, A. H., Keith, S. A. & Woolsey, E. Rapid coral mortality following doldrums-like conditions on Iriomote, Japan. F1000Res. 6, 1728 (2017).

    Google Scholar 

  110. 110.

    Osman, E. O. et al. Thermal refugia against coral bleaching throughout the northern Red Sea. Glob. Chang. Biol. 24, e474–e484 (2018).

    Google Scholar 

  111. 111.

    Torda, G. et al. Rapid adaptive responses to climate change in corals. Nat. Clim. Change 7, 627–636 (2017).

    Google Scholar 

  112. 112.

    van Oppen, M. J. H. et al. Shifting paradigms in restoration of the world’s coral reefs. Glob. Change Biol. 23, 3437–3448 (2017).

    Google Scholar 

  113. 113.

    Ho, D. H. & Burggren, W. W. Parental hypoxic exposure confers offspring hypoxia resistance in zebrafish (Danio rerio). J. Exp. Biol. 215, 4208–4216 (2012).

    CAS  Google Scholar 

  114. 114.

    Robertson, C. E., Wright, P. A., Köblitz, L. & Bernier, N. J. Hypoxia-inducible factor-1 mediates adaptive developmental plasticity of hypoxia tolerance in zebrafish, Danio rerio. Proc. R. Soc. B Biol. Sci. 281, 20140637 (2014).

    Google Scholar 

  115. 115.

    Ryu, T., Veilleux, H. D., Donelson, J. M., Munday, P. L. & Ravasi, T. The epigenetic landscape of transgenerational acclimation to ocean warming. Nat. Clim. Change 8, 504–509 (2018).

    Google Scholar 

  116. 116.

    Pörtner, H.-O. Oxygen- and capacity-limitation of thermal tolerance: a matrix for integrating climate-related stressor effects in marine ecosystems. J. Exp. Biol. 213, 881–893 (2010).

    Google Scholar 

  117. 117.

    McBryan, T. L., Anttila, K., Healy, T. M. & Schulte, P. M. Responses to temperature and hypoxia as interacting stressors in fish: implications for adaptation to environmental change. Integr. Comp. Biol. 53, 648–659 (2013).

    CAS  Google Scholar 

  118. 118.

    Nilsson, G. E., Östlund-Nilsson, S. & Munday, P. L. Effects of elevated temperature on coral reef fishes: Loss of hypoxia tolerance and inability to acclimate. Comp. Biochem. Phys. A 156, 389–393 (2010).

    Google Scholar 

  119. 119.

    Camp, E. F. et al. The future of coral reefs subject to rapid climate change: lessons from natural extreme environments. Front. Mar. Sci. 5, 4 (2018).

    Google Scholar 

  120. 120.

    Gallo, N. D., Victor, D. G. & Levin, L. A. Ocean commitments under the Paris Agreement. Nat. Clim. Change 7, 833–838 (2017).

    Google Scholar 

  121. 121.

    Pörtner, H. O., Langenbuch, M. & Michaelidis, B. Synergistic effects of temperature extremes, hypoxia, and increases in CO2 on marine animals: from Earth history to global change. J. Geophys. Res.-Oceans 110, C09S10 (2005).

    Google Scholar 

  122. 122.

    Veron, J. E. N. Mass extinctions and ocean acidification: biological constraints on geological dilemmas. Coral Reefs 27, 459–472 (2008).

    Google Scholar 

  123. 123.

    Rutherford, L. D. & Thuesen, E. V. Metabolic performance and survival of medusae in estuarine hypoxia. Mar. Ecol. Prog. Ser. 294, 189–200 (2005).

    Google Scholar 

  124. 124.

    Carey, N. et al. Variation in oxygen consumption among ‘living fossils’ (Mollusca: Polyplacophora). J. Mar. Biol. Assoc. UK 93, 197–207 (2013).

    CAS  Google Scholar 

  125. 125.

    Auel, H. & Verheye, H. M. Hypoxia tolerance in the copepod Calanoides carinatus and the effect of an intermediate oxygen minimum layer on copepod vertical distribution in the northern Benguela Current upwelling system and the Angola–Benguela Front. J. Exp. Mar. Bio. Ecol. 352, 234–243 (2007).

    Google Scholar 

  126. 126.

    Low, N. H. N. & Micheli, F. Lethal and functional thresholds of hypoxia in two key benthic grazers. Mar. Ecol. Prog. Ser. 594, 165–173 (2018).

    CAS  Google Scholar 

  127. 127.

    Shashar, N., Kinane, S., Jokiel, P. L. & Patterson, M. R. Hydromechanical boundary layers over a coral reef. J. Exp. Mar. Bio. Ecol. 199, 17–28 (1996).

    Google Scholar 

  128. 128.

    Klein, S. G., Steckbauer, A. & Duarte, C. M. Defining CO2 and O2 syndromes of marine biomes in the Anthropocene. Glob. Chang. Biol. https://doi.org/10.1111/gcb.14879 (2019).

  129. 129.

    Solaini, G., Baracca, A., Lenaz, G. & Sgarbi, G. Hypoxia and mitochondrial oxidative metabolism. BBA-Bioenergetics 1797, 1171–1177 (2010).

    CAS  Google Scholar 

  130. 130.

    Gooday, A. J. et al. Faunal responses to oxygen gradients on the Pakistan margin: a comparison of foraminiferans, macrofauna and megafauna. Deep Sea Res. Part II Top. Stud. Oceanogr. 56, 488–502 (2009).

    CAS  Google Scholar 

  131. 131.

    López-Barneo, J., del Toro, R., Levitsky, K. L., Chiara, M. D. & Ortega-Sáenz, P. Regulation of oxygen sensing by ion channels. J. Appl. Physiol. 96, 1187–1195 (2004).

    Google Scholar 

  132. 132.

    Viollet, B. AMPK: lessons from transgenic and knockout animals. Front. Biosci. 1, 19–44 (2009).

    Google Scholar 

  133. 133.

    Wang, F., Chen, Z.-H. & Shabala, S. Hypoxia sensing in plants: on a quest for ion channels as putative oxygen sensors. Plant Cell Physiol. 58, 1126–1142 (2017).

    CAS  Google Scholar 

  134. 134.

    Olson, K. R. et al. Hydrogen sulfide as an oxygen sensor/transducer in vertebrate hypoxic vasoconstriction and hypoxic vasodilation. J. Exp. Biol. 209, 4011–4023 (2006).

    CAS  Google Scholar 

  135. 135.

    Epstein, A. C. et al. C. elegans EGL-9 and mammalian homologs define a family of dioxygenases that regulate HIF by prolyl hydroxylation. Cell 107, 43–54 (2001).

    CAS  Google Scholar 

  136. 136.

    Kallio, P. J. et al. Signal transduction in hypoxic cells: inducible nuclear translocation and recruitment of the CBP/p300 coactivator by the hypoxia-inducible factor-1alpha. EMBO J. 17, 6573–6586 (1998).

    CAS  Google Scholar 

  137. 137.

    Semenza, G. L. Involvement of oxygen-sensing pathways in physiologic and pathologic erythropoiesis. Blood 114, 2015–2019 (2009).

    CAS  Google Scholar 

  138. 138.

    Ney, P. A. Mitochondrial autophagy: origins, significance, and role of BNIP3 and NIX. BBA-Mol. Cell Res. 1853, 2775–2783 (2015).

    CAS  Google Scholar 

  139. 139.

    Youle, R. J. & Narendra, D. P. Mechanisms of mitophagy. Nat. Rev. Mol. Cell Biol. 12, 9–14 (2011).

    CAS  Google Scholar 

  140. 140.

    Narendra, D. P. & Youle, R. J. Targeting mitochondrial dysfunction: role for PINK1 and Parkin in mitochondrial quality control. Antioxid. Redox Sign. 14, 1929–1938 (2011).

    CAS  Google Scholar 

  141. 141.

    Zhang, J. & Ney, P. A. Role of BNIP3 and NIX in cell death, autophagy and mitophagy. Cell Death Differ. 16, 939–946 (2009).

    CAS  Google Scholar 

  142. 142.

    Srivastava, M. et al. The Trichoplax genome and the nature of placozoans. Nature 454, 955–960 (2008).

    CAS  Google Scholar 

Download references

Acknowledgements

Funding for this Perspective was provided by the Australian Research Council (ARC) discovery grant (grant no. DP180100074) to D.J.S, M.P, M.K and C.R.V.

Author information

Affiliations

Authors

Contributions

All authors contributed significantly with their respective expertise to the formulation, writing and editing. D.J.H performed digitization and analysis of peer-reviewed data.

Corresponding authors

Correspondence to David J. Hughes or David J. Suggett.

Ethics declarations

Competing interests

The authors declare no competing interests.

Additional information

Peer review information Nature Climate Change thanks Andi Haas and the other, anonymous, reviewer(s) for their contribution to the peer review of this work.

Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Hughes, D.J., Alderdice, R., Cooney, C. et al. Coral reef survival under accelerating ocean deoxygenation. Nat. Clim. Chang. 10, 296–307 (2020). https://doi.org/10.1038/s41558-020-0737-9

Download citation

Further reading

Search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing