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.
This is a preview of subscription content, access via your institution
Open Access articles citing this article.
Microbiomes of a disease-resistant genotype of Acropora cervicornis are resistant to acute, but not chronic, nutrient enrichment
Scientific Reports Open Access 03 March 2023
Scientific Reports Open Access 31 October 2022
Coral Reefs Open Access 12 November 2021
Access Nature and 54 other Nature Portfolio journals
Get Nature+, our best-value online-access subscription
$29.99 / 30 days
cancel any time
Subscribe to this journal
Receive 12 print issues and online access
$209.00 per year
only $17.42 per issue
Rent or buy this article
Prices vary by article type
Prices may be subject to local taxes which are calculated during checkout
Costanza, R. et al. Changes in the global value of ecosystem services. Glob. Environ. Chang. 26, 152–158 (2014).
LaJeunesse, T. C. et al. Systematic revision of Symbiodiniaceae highlights the antiquity and diversity of coral endosymbionts. Curr. Biol. 28, 2570–2580 (2018).
Hughes, T. P. et al. Coral reefs in the Anthropocene. Nature 546, 82–90 (2017).
Breitburg, D. et al. Declining oxygen in the global ocean and coastal waters. Science 359, eaam7240 (2018).
D. Laffoley, D. & Baxter, J. M. (eds) Ocean Deoxygenation: Everyone’s Problem. Causes, Impacts, Consequences and Solutions (IUCN, 2019).
Altieri, A. H. et al. Tropical dead zones and mass mortalities on coral reefs. Proc. Natl Acad. Sci. USA 114, 3660–3665 (2017).
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).
Falkowski, P. G., Fenchel, T. & Delong, E. F. The microbial engines that drive Earth’s biogeochemical cycles. Science 320, 1034–1039 (2008).
Bopp, L. et al. Multiple stressors of ocean ecosystems in the 21st century: projections with CMIP5 models. Biogeosciences 10, 6225–6245 (2013).
Vaquer-Sunyer, R. & Duarte, C. M. Thresholds of hypoxia for marine biodiversity. Proc. Natl Acad. Sci. USA 105, 15452–15457 (2008).
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).
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).
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).
Rabalais, N. N. et al. Dynamics and distribution of natural and human-caused hypoxia. Biogeosciences 7, 585–619 (2010).
Levin, L. A. & Breitburg, D. L. Linking coasts and seas to address ocean deoxygenation. Nat. Clim. Change 5, 401–403 (2015).
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).
Hughes, T. P. et al. Global warming transforms coral reef assemblages. Nature 556, 492–496 (2018).
Keeling, R. F., Körtzinger, A. & Gruber, N. Ocean deoxygenation in a warming world. Ann. Rev. Mar. Sci. 2, 199–229 (2010).
Falkowski, P. G. et al. Ocean deoxygenation: past, present, and future. Eos (November 2011).
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).
Clapham, M. E. & Renne, P. R. Flood basalts and mass extinctions. Annu. Rev. Earth Planet. Sci. 47, 275–303 (2019).
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).
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).
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).
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).
Dixon, G. B. et al. Genomic determinants of coral heat tolerance across latitudes. Science 348, 1460–1462 (2015).
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).
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).
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).
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).
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).
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).
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).
Diaz, R. J. & Rosenberg, R. Spreading dead zones and consequences for marine ecosystems. Science 321, 926–929 (2008).
Altieri, A. H. & Gedan, K. B. Climate change and dead zones. Glob. Chang. Biol. 21, 1395–1406 (2015).
Mee, L. D., Friedrich, J. & Gomoiu, M. T. Restoring the Black Sea in times of uncertainty. Oceanography 18, 100–111 (2005).
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).
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).
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).
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).
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).
Camp, E. F. et al. Reef-building corals thrive within hot-acidified and deoxygenated waters. Sci. Rep. 7, 2434 (2017).
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).
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).
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).
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).
Haas, A. F. et al. Global microbialization of coral reefs. Nat. Microbiol. 1, 16042 (2016).
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).
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).
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).
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).
Nilsson, G. E. & Östlund-Nilsson, S. Does size matter for hypoxia tolerance in fish? Biol. Rev. 83, 173–189 (2008).
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).
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
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).
Laboy-Nieves, E. N. et al. Mass mortality of tropical marine communities in Morrocoy, Venezuela. B. Mar. Sci. 68, 163–179 (2001).
Roder, C. et al. First biological measurements of deep-sea corals from the Red Sea. Sci. Rep. 3, 2802 (2013).
Graham, N. A. J. & Nash, K. L. The importance of structural complexity in coral reef ecosystems. Coral Reefs 32, 315–326 (2013).
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).
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).
Nilsson, G. E. & Östlund-Nilsson, S. Hypoxia tolerance in coral reef fishes. Fish Physiol. 21, 583–596 (2005).
Wood, C. M. The fallacy of the Pcrit - are there more useful alternatives? J. Exp. Biol. 221, jeb163717 (2018).
Regan, M. D. et al. Don’t throw the fish out with the respirometry water. J. Exp. Biol. 222, jeb200253 (2019).
Grieshaber, M. K., Hardewig, I., Kreutzer, U. & Pörtner, H. O. in Reviews of Physiology, Biochemistry and Pharmacology Vol. 125 43–147 (Springer, 1993).
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).
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).
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).
Kramer, D. L. Dissolved oxygen and fish behavior. Environ. Biol. Fishes 18, 81–92 (1987).
Levin, L. A. et al. Effects of natural and human-induced hypoxia on coastal benthos. Biogeosciences 6, 2063–2098 (2009).
Vaquer-Sunyer, R. & Duarte, C. M. Temperature effects on oxygen thresholds for hypoxia in marine benthic organisms. Glob. Chang. Biol. 17, 1788–1797 (2011).
Patterson, M. R. A mass transfer explanation of metabolic scaling relations in some aquatic invertebrates and algae. Science 255, 1421–1423 (1992).
Shapiro, O. H. et al. Vortical ciliary flows actively enhance mass transport in reef corals. Proc. Natl Acad. Sci. USA 111, 13391–13396 (2014).
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).
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).
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).
Kremien, M., Shavit, U., Mass, T. & Genin, A. Benefit of pulsation in soft corals. Proc. Natl Acad. Sci. USA 110, 8978–8983 (2013).
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).
Jørgensen, B. B. & Revsbech, N. P. Diffusive boundary layers and the oxygen uptake of sediments and detritus. Limnol. Oceanogr. 30, 111–122 (1985).
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).
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).
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).
Nelson, H. R. & Altieri, A. H. Oxygen: the universal currency on coral reefs. Coral Reefs 38, 177–198 (2019).
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).
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).
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).
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).
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).
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).
Roder, C. et al. Bacterial profiling of White Plague Disease in a comparative coral species framework. ISME J. 8, 31–39 (2014).
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).
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).
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).
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).
Taabazuing, C. Y., Hangasky, J. A. & Knapp, M. J. Oxygen sensing strategies in mammals and bacteria. J. Inorg. Biochem. 133, 63–72 (2014).
Kaelin, W. G. & Ratcliffe, P. J. Oxygen sensing by metazoans: the central role of the HIF hydroxylase pathway. Mol. Cell 30, 393–402 (2008).
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).
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).
Semenza, G. L. Oxygen sensing, homeostasis, and disease. N. Engl. J. Med. 365, 537–547 (2011).
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).
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).
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).
Levy, O. et al. Complex Diel cycles of gene expression in coral-algal symbiosis. Science 331, 175 (2011).
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).
Zoccola, D. et al. Structural and functional analysis of coral hypoxia inducible factor. PLoS ONE 12, e0186262 (2017).
Kumar, H. & Choi, D.-K. Hypoxia inducible factor pathway and physiological adaptation: a cell survival pathway? Mediat. Inflamm. 2015, 584758 (2015).
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).
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).
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).
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).
Osman, E. O. et al. Thermal refugia against coral bleaching throughout the northern Red Sea. Glob. Chang. Biol. 24, e474–e484 (2018).
Torda, G. et al. Rapid adaptive responses to climate change in corals. Nat. Clim. Change 7, 627–636 (2017).
van Oppen, M. J. H. et al. Shifting paradigms in restoration of the world’s coral reefs. Glob. Change Biol. 23, 3437–3448 (2017).
Ho, D. H. & Burggren, W. W. Parental hypoxic exposure confers offspring hypoxia resistance in zebrafish (Danio rerio). J. Exp. Biol. 215, 4208–4216 (2012).
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).
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).
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).
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).
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).
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).
Gallo, N. D., Victor, D. G. & Levin, L. A. Ocean commitments under the Paris Agreement. Nat. Clim. Change 7, 833–838 (2017).
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).
Veron, J. E. N. Mass extinctions and ocean acidification: biological constraints on geological dilemmas. Coral Reefs 27, 459–472 (2008).
Rutherford, L. D. & Thuesen, E. V. Metabolic performance and survival of medusae in estuarine hypoxia. Mar. Ecol. Prog. Ser. 294, 189–200 (2005).
Carey, N. et al. Variation in oxygen consumption among ‘living fossils’ (Mollusca: Polyplacophora). J. Mar. Biol. Assoc. UK 93, 197–207 (2013).
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).
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).
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).
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).
Solaini, G., Baracca, A., Lenaz, G. & Sgarbi, G. Hypoxia and mitochondrial oxidative metabolism. BBA-Bioenergetics 1797, 1171–1177 (2010).
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).
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).
Viollet, B. AMPK: lessons from transgenic and knockout animals. Front. Biosci. 1, 19–44 (2009).
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).
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).
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).
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).
Semenza, G. L. Involvement of oxygen-sensing pathways in physiologic and pathologic erythropoiesis. Blood 114, 2015–2019 (2009).
Ney, P. A. Mitochondrial autophagy: origins, significance, and role of BNIP3 and NIX. BBA-Mol. Cell Res. 1853, 2775–2783 (2015).
Youle, R. J. & Narendra, D. P. Mechanisms of mitophagy. Nat. Rev. Mol. Cell Biol. 12, 9–14 (2011).
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).
Zhang, J. & Ney, P. A. Role of BNIP3 and NIX in cell death, autophagy and mitophagy. Cell Death Differ. 16, 939–946 (2009).
Srivastava, M. et al. The Trichoplax genome and the nature of placozoans. Nature 454, 955–960 (2008).
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.
The authors declare no competing interests.
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.
About this article
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
This article is cited by
Microbiomes of a disease-resistant genotype of Acropora cervicornis are resistant to acute, but not chronic, nutrient enrichment
Scientific Reports (2023)
Nature Geoscience (2023)
The genome of Symbiodiniaceae-associated Stutzerimonas frequens CAM01 reveals a broad spectrum of antibiotic resistance genes indicating anthropogenic drift in the Palk Bay coral reef of south-eastern India
Archives of Microbiology (2023)
Patterns of coral diseases linked to the impact of climate change: a case study of scleractinia corals in Southeast Sulawesi, Indonesia’s coral triangle
Modeling Earth Systems and Environment (2023)
Nature Climate Change (2023)