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.

  • Perspective
  • Published:

Biogeochemical extremes and compound events in the ocean

Nature volume 600, pages 395–407 (2021)Cite this article

Subjects

This article has been updated

Abstract

The ocean is warming, losing oxygen and being acidified, primarily as a result of anthropogenic carbon emissions. With ocean warming, acidification and deoxygenation projected to increase for decades, extreme events, such as marine heatwaves, will intensify, occur more often, persist for longer periods of time and extend over larger regions. Nevertheless, our understanding of oceanic extreme events that are associated with warming, low oxygen concentrations or high acidity, as well as their impacts on marine ecosystems, remains limited. Compound events—that is, multiple extreme events that occur simultaneously or in close sequence—are of particular concern, as their individual effects may interact synergistically. Here we assess patterns and trends in open ocean extremes based on the existing literature as well as global and regional model simulations. Furthermore, we discuss the potential impacts of individual and compound extremes on marine organisms and ecosystems. We propose a pathway to improve the understanding of extreme events and the capacity of marine life to respond to them. The conditions exhibited by present extreme events may be a harbinger of what may become normal in the future. As a consequence, pursuing this research effort may also help us to better understand the responses of marine organisms and ecosystems to future climate change.

This is a preview of subscription content, access via your institution

Access options

Buy this article

  • Purchase on Springer Link
  • Instant access to full article PDF
Buy now

Prices may be subject to local taxes which are calculated during checkout

Fig. 1: Drivers of marine heatwaves and ocean biogeochemical extremes and their impact.
Fig. 2: Global pattern and trends of marine heatwaves and biogeochemical extremes.
Fig. 3: Idealized depictions of the mechanisms giving rise to extreme conditions in temperature, acidity and oxygen.
Fig. 4: Illustration of the temporal evolution and four-dimensional nature of ocean extremes using model simulation results for the 2013–2015 Blob.
Fig. 5: Conceptual framework to understand the impact of marine biogeochemical extremes and heatwaves on the functioning of marine life—from physiology through to ecosystems.

Similar content being viewed by others

Data availability

The model results presented in the paper are available through the ETH Research Collection (https://www.research-collection.ethz.ch, https://doi.org/10.3929/ethz-b-000501082).

Change history

  • 07 January 2022

    This Article was amended to correct the Peer review information.

References

  1. Gruber, N. Warming up, turning sour, losing breath: ocean biogeochemistry under global change. Philos. Trans. A Math. Phys. Eng. Sci. 369, 1980–1996 (2011). Identifies the potential synegistic threat to marine ecosystems resulting from ocean warming, deoxygenation and acidification.

    ADS  CAS  PubMed  Google Scholar 

  2. Gattuso, J.-P. et al. Contrasting futures for ocean and society from different anthropogenic CO2 emissions scenarios. Science 349, aac4722 (2015).

    Article  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

  4. Cheng, L. et al. Improved estimates of ocean heat content from 1960 to 2015. Sci. Adv. 3, e1601545 (2017).

    Article  ADS  PubMed  PubMed Central  Google Scholar 

  5. Friedlingstein, P. et al. Global carbon budget 2020. Earth Syst. Sci. Data 12, 3269–3340 (2020).

    Article  ADS  Google Scholar 

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

    Article  PubMed  Google Scholar 

  7. Li, G. et al. Increasing ocean stratification over the past half-century. Nat. Clim. Change 10, 1116–1123 (2020).

    Article  ADS  Google Scholar 

  8. Sallée, J. B. et al. Summertime increases in upper-ocean stratification and mixed-layer depth. Nature 591, 592–598 (2021).

    Article  ADS  PubMed  PubMed Central  Google Scholar 

  9. Sarmiento, J. L. & Gruber, N. Ocean Biogeochemical Dynamics (Princeton Univ. Press, 2006).

  10. Mikaloff Fletcher, S. E. et al. Inverse estimates of anthropogenic CO2 uptake, transport, and storage by the ocean. Glob. Biogeochem. Cycles 20, GB2002 (2006).

    Article  ADS  Google Scholar 

  11. Doney, S. C., Fabry, V. J., Feely, R. A. & Kleypas, J. A. Ocean acidification: the other CO2 problem. Ann. Rev. Mar. Sci. 1, 169–192 (2009).

    Article  PubMed  Google Scholar 

  12. Doney, S. C., Busch, D. S., Cooley, S. R. & Kroeker, K. J. The impacts of ocean acidification on marine ecosystems and reliant human communities. Annu. Rev. Environ. Resour. 45, 83–112 (2020).

    Article  Google Scholar 

  13. Kroeker, K. J., Kordas, R. L., Crim, R. N. & Singh, G. G. Meta-analysis reveals negative yet variable effects of ocean acidification on marine organisms. Ecol. Lett. 13, 1419–1434 (2010).

    Article  PubMed  Google Scholar 

  14. Mollica, N. R. et al. Ocean acidification affects coral growth by reducing skeletal density. Proc. Natl Acad. Sci. USA 115, 1754–1759 (2018).

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  ADS  Google Scholar 

  16. Kwiatkowski, L. et al. Twenty-first century ocean warming, acidification, deoxygenation, and upper-ocean nutrient and primary production decline from CMIP6 model projections. Biogeosciences 17, 3439–3470 (2020).

    Article  ADS  CAS  Google Scholar 

  17. Seneviratne, S. I. et al. in Managing the Risks of Extreme Events and Disasters to Advance Climate Change Adaptation (eds Field, C. B. et al.) 109–230 (Cambridge Univ. Press, 2012).

  18. Lavell, A. et al. in Managing the Risks of Extreme Events and Disasters to Advance Climate Change Adaptation (eds Field, C. B. et al.) 25–64 (2012).

  19. Parmesan, C., Root, T. L. & Willig, M. R. Impacts of extreme weather and climate on terrestrial biota. Bull. Am. Meteor. Soc. 81, 443–450 (2000).

    Article  ADS  Google Scholar 

  20. Smith, M. D. An ecological perspective on extreme climatic events: a synthetic definition and framework to guide future research. J. Ecol. 99, 656–663 (2011).

    Article  Google Scholar 

  21. Oliver, E. C. J. et al. Marine heatwaves. Ann. Rev. Mar. Sci. 13, 313–342 (2021).

    Article  PubMed  Google Scholar 

  22. Frölicher, T. L., Fischer, E. M. & Gruber, N. Marine heatwaves under global warming. Nature 560, 360–364 (2018). Quantifies the future evolution of marine heatwaves under different climate scenarios and their attribution to climate change.

    Article  ADS  PubMed  Google Scholar 

  23. Oliver, E. C. J. et al. Longer and more frequent marine heatwaves over the past century. Nat. Commun. 9, 1324 (2018). Highlights the strong increase in the occurrence and intensity of marine heatwaves in recent decades.

    Article  ADS  PubMed  PubMed Central  Google Scholar 

  24. Oliver, E. C. J. et al. Projected marine heatwaves in the 21st century and the potential for ecological impact. Front. Mar. Sci. 6, 734 (2019).

    Article  Google Scholar 

  25. Benedetti-Cecchi, L. Complex networks of marine heatwaves reveal abrupt transitions in the global ocean. Sci. Rep. 11, 1739 (2021).

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  26. Smale, D. A. et al. Marine heatwaves threaten global biodiversity and the provision of ecosystem services. Nat. Clim. Change 9, 306–312 (2019). Assesses the potential for global ocean ecosystem impacts of marine heatwaves.

    Article  ADS  Google Scholar 

  27. Wernberg, T. et al. An extreme climatic event alters marine ecosystem structure in a global biodiversity hotspot. Nat. Clim. Change 3, 78–82 (2012). Demonstrates marked ocean ecosystem changes in response to a heatwave.

    Article  ADS  Google Scholar 

  28. Hobday, A. J. et al. A hierarchical approach to defining marine heatwaves. Prog. Oceanogr. 141, 227–238 (2016).

    Article  ADS  Google Scholar 

  29. Holbrook, N. J. et al. A global assessment of marine heatwaves and their drivers. Nat. Commun. 10, 2624 (2019).

    Article  ADS  PubMed  PubMed Central  Google Scholar 

  30. Huang, B. et al. Extended reconstructed sea surface temperature version 4 (ERSST.v4). Part I: upgrades and intercomparisons. J. Clim. 28, 911–930 (2015).

    Article  ADS  Google Scholar 

  31. Gentemann, C. L., Fewings, M. R. & García-Reyes, M. Satellite sea surface temperatures along the west coast of the United States during the 2014–2016 northeast Pacific marine heat wave. Geophys. Res. Lett. 44, 312–319 (2017).

    Article  ADS  Google Scholar 

  32. Cavole, L. et al. Biological impacts of the 2013–2015 warm-water anomaly in the northeast Pacific: winners, losers, and the future. Oceanography 29, 273–285 (2016). A synthesis of the ecosystem impacts of the 2013–2015 Blob heatwave.

  33. Di Lorenzo, E. & Mantua, N. Multi-year persistence of the 2014/15 north Pacific marine heatwave. Nat. Clim. Change 6, 1042–1047 (2016).

    Article  ADS  Google Scholar 

  34. Brodeur, R. D., Auth, T. D. & Phillips, A. J. Major shifts in pelagic micronekton and macrozooplankton community structure in an upwelling ecosystem related to an unprecedented marine heatwave. Front. Mar. Sci. 6, 212 (2019).

    Article  Google Scholar 

  35. Cheung, W. W. L. & Frölicher, T. L. Marine heatwaves exacerbate climate change impacts for fisheries in the northeast Pacific. Sci. Rep. 10, 6678 (2020).

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  36. Laufkötter, C., Zscheischler, J. & Frölicher, T. L. High-impact marine heatwaves attributable to human-induced global warming. Science 369, 1621–1625 (2020).

    Article  ADS  PubMed  Google Scholar 

  37. Hauri, C., Gruber, N., McDonnell, A. M. P. & Vogt, M. The intensity, duration, and severity of low aragonite saturation state events on the California continental shelf. Geophys. Res. Lett. 40, 3424–3428 (2013). Models the evolution of ocean-acidification-related extremes in the California Current System.

    Article  ADS  Google Scholar 

  38. Burger, F. A., John, J. G. & Frölicher, T. L. Increase in ocean acidity variability and extremes under increasing atmospheric CO2. Biogeosciences 17, 4633–4662 (2020).

    Article  ADS  CAS  Google Scholar 

  39. Leonard, M. et al. A compound event framework for understanding extreme impacts. Wiley Interdiscip. Rev. Clim. Change 5, 113–128 (2014).

    Article  Google Scholar 

  40. Zscheischler, J. et al. Future climate risk from compound events. Nat. Clim. Change 8, 469–477 (2018).

    Google Scholar 

  41. Le Grix, N., Zscheischler, J., Laufkötter, C., Rousseaux, C. S. & Frölicher, T. L. Compound high-temperature and low-chlorophyll extremes in the ocean over the satellite period. Biogeosciences 18, 2119–2137 (2021).

    Article  ADS  Google Scholar 

  42. Boyd, P. W. & Brown, C. J. Modes of interactions between environmental drivers and marine biota. Front. Mar. Sci. 2, 9 (2015).

    Article  Google Scholar 

  43. Trisos, C. H., Merow, C. & Pigot, A. L. The projected timing of abrupt ecological disruption from climate change. Nature 580, 496–501 (2020).

  44. Limburg, K. E., Breitburg, D., Swaney, D. P. & Jacinto, G. Ocean deoxygenation: a primer. One Earth 2, 24–29 (2020).

    Article  Google Scholar 

  45. Dunne, J. P. et al. GFDL’s ESM2 global coupled climate-carbon earth system models. Part II: carbon system formulation and baseline simulation characteristics. J. Clim. 26, 2247–2267 (2013).

    Article  ADS  Google Scholar 

  46. Dunne, J. P. et al. GFDL’s ESM2 global coupled climate–carbon earth system models. Part I: physical formulation and baseline simulation characteristics. J. Clim. 25, 6646–6665 (2012).

    Article  ADS  Google Scholar 

  47. Allen, M. R. et al. An IPCC Special Report on the Impacts of Global Warming of 1.5 °C Above Pre-Industrial Levels and Related Global Greenhouse Gas Emission Pathways, in the Context of Strengthening the Global Response to the Threat of Climate Change (eds. Masson-Delmotte, V. et al.) 49–91 (IPCC, 2018).

  48. Frölicher, T. L. & Laufkötter, C. Emerging risks from marine heat waves. Nat. Commun. 9, 650 (2018).

    Article  ADS  PubMed  PubMed Central  Google Scholar 

  49. Pilo, G. S., Holbrook, N. J., Kiss, A. E. & Hogg, A. M. C. sensitivity of marine heatwave metrics to ocean model resolution. Geophys. Res. Lett. 46, 14604–14612 (2019).

    Article  ADS  Google Scholar 

  50. Schlegel, R. W., Oliver, E. C. J., Hobday, A. J. & Smit, A. J. Detecting marine heatwaves with sub-optimal data. Front. Mar. Sci. 6, 737 (2019).

    Article  Google Scholar 

  51. Hobday, A. et al. Categorizing and naming marine heatwaves. Oceanography 31, 162–173 (2018).

  52. Alexander, M. A. et al. The atmospheric bridge: the influence of ENSO teleconnections on air–sea interaction over the global oceans. J. Clim. 15, 2205–2231 (2002).

    Article  ADS  Google Scholar 

  53. Amaya, D. J., Miller, A. J., Xie, S. P. & Kosaka, Y. Physical drivers of the summer 2019 north Pacific marine heatwave. Nat. Commun. 11, 1903 (2020).

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  54. Negrete-García, G., Lovenduski, N. S., Hauri, C., Krumhardt, K. M. & Lauvset, S. K. Sudden emergence of a shallow aragonite saturation horizon in the Southern Ocean. Nat. Clim. Change 9, 313–317 (2019).

    Article  ADS  Google Scholar 

  55. Schaeffer, A. & Roughan, M. Subsurface intensification of marine heatwaves off southeastern Australia: the role of stratification and local winds. Geophys. Res. Lett. 44, 5025–5033 (2017).

    Article  ADS  Google Scholar 

  56. Jackson, J. M., Johnson, G. C., Dosser, H. V. & Ross, T. Warming from recent marine heatwave lingers in deep British Columbia fjord. Geophys. Res. Lett. 45, 9757–9764 (2018).

    Article  ADS  Google Scholar 

  57. Scannell, H. A., Johnson, G. C., Thompson, L., Lyman, J. M. & Riser, S. C. Subsurface evolution and persistence of marine heatwaves in the northeast Pacific. Geophys. Res. Lett. 47, e2020GL090548 (2020).

    Article  ADS  Google Scholar 

  58. Deutsch, C., Brix, H., Ito, T., Frenzel, H. & Thompson, L. Climate-forced variability of ocean hypoxia. Science 333, 336–339 (2011).

    Article  ADS  CAS  PubMed  Google Scholar 

  59. Frenger, I. et al. Biogeochemical role of subsurface coherent eddies in the ocean: tracer cannonballs, hypoxic storms, and microbial stewpots? Glob. Biogeochem. Cycles 32, 226–249 (2018).

    Article  ADS  CAS  Google Scholar 

  60. Schütte, F. et al. Characterization of ‘dead-zone’ eddies in the eastern tropical north Atlantic. Biogeosciences 13, 5865–5881 (2016).

    Article  ADS  Google Scholar 

  61. Lauvset, S. K. et al. Processes driving global interior ocean pH distribution. Glob. Biogeochem. Cycles 34, e2019GB006229 (2020).

    Article  ADS  CAS  Google Scholar 

  62. Gaube, P., Chelton, D. B., Strutton, P. G. & Behrenfeld, M. J. Satellite observations of chlorophyll, phytoplankton biomass, and Ekman pumping in nonlinear mesoscale eddies. J. Geophys. Res. Oceans 118, 6349–6370 (2013).

    Article  ADS  CAS  Google Scholar 

  63. Frenger, I., Münnich, M., Gruber, N. & Knutti, R. Southern Ocean eddy phenomenology. J. Geophys. Res. Oceans 120, 7413–7449 (2015).

    Article  ADS  Google Scholar 

  64. Hauss, H. et al. Dead zone or oasis in the open ocean? Zooplankton distribution and migration in low-oxygen modewater eddies. Biogeosciences 13, 1977–1989 (2016).

    Article  ADS  CAS  Google Scholar 

  65. Gruber, N. et al. Rapid progression of ocean acidification in the California Current System. Science 337, 220–223 (2012).

    Article  ADS  CAS  PubMed  Google Scholar 

  66. Santora, J. A. et al. Habitat compression and ecosystem shifts as potential links between marine heatwave and record whale entanglements. Nat. Commun. 11, 536 (2020).

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  67. Bond, N. A., Cronin, M. F., Freeland, H. & Mantua, N. Causes and impacts of the 2014 warm anomaly in the NE Pacific. Geophys. Res. Lett. 42, 3414–3420 (2015).

    Article  ADS  Google Scholar 

  68. Peterson, W. T., Bond, N. A. & Robert, M. The Blob (part three): going, going, gone? PICES Press 24, 46–48 (2016).

    Google Scholar 

  69. Frischknecht, M., Münnich, M. & Gruber, N. Local atmospheric forcing driving an unexpected California Current System response during the 2015–2016 El Niño. Geophys. Res. Lett. 44, 304–311 (2017).

    Article  ADS  Google Scholar 

  70. Pörtner, H. O. & Knust, R. Climate change affects marine fishes through the oxygen limitation of thermal tolerance. Science 315, 95–97 (2007).

    Article  ADS  PubMed  Google Scholar 

  71. Penn, 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).

  72. Dahlke, F. T., Wohlrab, S., Butzin, M. & Pörtner, H.-O. Thermal bottlenecks in the life cycle define climate vulnerability of fish. Science 369, 65–70 (2020).

    Article  ADS  CAS  PubMed  Google Scholar 

  73. Pörtner, H. O. Ecosystem effects of ocean acidification in times of ocean warming: a physiologist’s view. Mar. Ecol. Progr. Ser. 373, 203–217 (2008).

    Article  ADS  Google Scholar 

  74. Stillman, J. H. Heat waves, the new normal: summertime temperature extremes will impact animals, ecosystems, and human communities. Physiology 34, 86–100 (2019).

    Article  CAS  PubMed  Google Scholar 

  75. Straub, S. C. et al. Resistance, extinction, and everything in between—the diverse responses of seaweeds to marine heatwaves. Front. Mar. Sci. 6, 763 (2019).

    Article  Google Scholar 

  76. Hughes, T. P. et al. Spatial and temporal patterns of mass bleaching of corals in the Anthropocene. Science 359, 80–83 (2018). Demonstrates the global-scale impact of marine heatwaves on warm-water corals.

    Article  ADS  CAS  PubMed  Google Scholar 

  77. Donovan, M. K. et al. Local conditions magnify coral loss following marine heatwaves. Science 372, 977–980 (2021).

    Article  CAS  PubMed  Google Scholar 

  78. Klein, S. G. et al. Projecting coral responses to intensifying marine heatwaves under ocean acidification. Glob. Change Biol. https://doi.org/10.1111/gcb.15818 (2021).

  79. McMahon, B. R. Physiological responses to oxygen depletion in intertidal animals. Am. Zool. 28, 39–53 (1988).

    Article  Google Scholar 

  80. Kroeker, K. J. et al. Ecological change in dynamic environments: accounting for temporal environmental variability in studies of ocean change biology. Glob. Change Biol. 26, 54–67 (2020).

    Article  ADS  Google Scholar 

  81. Hofmann, G. E. et al. High-frequency dynamics of ocean pH: a multi-ecosystem comparison. PLoS ONE 6, e28983 (2011).

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  82. Spisla, C. et al. Extreme levels of ocean acidification restructure the plankton community and biogeochemistry of a temperate coastal ecosystem: a mesocosm study. Front. Mar. Sci. 7, 611157 (2021).

    Article  Google Scholar 

  83. Engström-Öst, J. et al. Eco-physiological responses of copepods and pteropods to ocean warming and acidification. Sci. Rep. 9, 4748 (2019).

    Article  ADS  PubMed  PubMed Central  Google Scholar 

  84. Bednaršek, N. et al. El Niño-related thermal stress coupled with upwelling-related ocean acidification negatively impacts cellular to population-level responses in pteropods along the California current system with implications for increased bioenergetic costs. Front. Mar. Sci. 5, 486 (2018). Shows the impact of a compound event on pteropods, a keystone zooplankton species in many marine ecosystems.

    Article  Google Scholar 

  85. Calderón-Liévanos, S. et al. Survival and respiration of green abalone (Haliotis fulgens) facing very short-term marine environmental extremes. Mar. Freshw. Behav. Physiol. 52, 1–15 (2019).

    Article  Google Scholar 

  86. Mieszkowska, N., Burrows, M. T., Hawkins, S. J. & Sugden, H. Impacts of pervasive climate change and extreme events on rocky intertidal communities: evidence from long-term data. Front. Mar. Sci. 8, 642764 (2021).

  87. Nielsen, J. M. et al. Responses of ichthyoplankton assemblages to the recent marine heatwave and previous climate fluctuations in several northeast Pacific marine ecosystems. Glob. Chang. Biol. 27, 506–520 (2020).

    Article  ADS  PubMed  Google Scholar 

  88. Wernberg, T. et al. Climate-driven regime shift of a temperate marine ecosystem. Science 353, 169–172 (2016).

    Article  ADS  CAS  PubMed  Google Scholar 

  89. Garrabou, J. et al. Mass mortality in northwestern Mediterranean rocky benthic communities: effects of the 2003 heat wave. Glob. Change Biol. 15, 1090–1103 (2009).

    Article  ADS  Google Scholar 

  90. Darling, E. S., McClanahan, T. R. & Côté, I. M. Life histories predict coral community disassembly under multiple stressors. Glob. Change Biol. 19, 1930–1940 (2013).

    Article  ADS  Google Scholar 

  91. Ateweberhan, M., McClanahan, T. R., Graham, N. A. J. & Sheppard, C. R. C. Episodic heterogeneous decline and recovery of coral cover in the Indian Ocean. Coral Reefs 30, 739–752 (2011).

    Article  ADS  Google Scholar 

  92. Weitzman, B. et al. Changes in rocky intertidal community structure during a marine heatwave in the Northern Gulf of Alaska. Front. Mar. Sci. 8, 556820 (2021).

  93. Samuels, T., Rynearson, T. A. & Collins, S. Surviving heatwaves: thermal experience predicts life and death in a Southern Ocean Diatom. Front. Mar. Sci. 8, 600343 (2021).

  94. Vajedsamiei, J., Wahl, M., Schmidt, A. L., Yazdanpanahan, M. & Pansch, C. The higher the needs, the lower the tolerance: extreme events may select ectotherm recruits with lower metabolic demand and heat sensitivity. Front. Mar. Sci. 8, 660427 (2021).

    Article  Google Scholar 

  95. Bindoff, N. L. et al. IPCC Special Report on the Ocean and Cryosphere in a Changing Climate (eds. Pörtner, H.-O. et al.) Ch. 5 (IPCC, 2021).

  96. IPCC. Climate Change 2014: Impacts, Adaptation, and Vulnerability (eds Field, C. B. et al.) Ch. 6 (Cambridge Univ. Press, 2014).

  97. Harvey, B. P., Gwynn-Jones, D. & Moore, P. J. Meta-analysis reveals complex marine biological responses to the interactive effects of ocean acidification and warming. Ecol. Evol. 3, 1016–1030 (2013).

    Article  PubMed  PubMed Central  Google Scholar 

  98. Gunderson, A. R., Armstrong, E. J. & Stillman, J. H. Multiple stressors in a changing world: the need for an improved perspective on physiological responses to the dynamic marine environment. Ann. Rev. Mar. Sci. 8, 357–378 (2016).

    Article  PubMed  Google Scholar 

  99. Seifert, M., Rost, B., Trimborn, S. & Hauck, J. Meta-analysis of multiple driver effects on marine phytoplankton highlights modulating role of pCO2. Glob. Change Biol. 26, 6787–6804 (2020).

    Article  ADS  Google Scholar 

  100. Sampaio, E. et al. Impacts of hypoxic events surpass those of future ocean warming and acidification. Nat. Ecol. Evol. 5, 311–321 (2021).

    Article  PubMed  Google Scholar 

  101. Bernhardt, J. R., O’Connor, M. I., Sunday, J. M. & Gonzalez, A. Life in fluctuating environments: adaptation to changing environments. Philos. Trans. R. Soc. B Biol. Sci. 375, 20190454 (2020).

    Article  Google Scholar 

  102. Somero, G. N. The cellular stress response and temperature: function, regulation, and evolution. J. Exp. Zool. A Ecol. Integr. Physiol. 333, 379–397 (2020).

    Article  CAS  PubMed  Google Scholar 

  103. Fordyce, A. J., Ainsworth, T. D., Heron, S. F. & Leggat, W. Marine heatwave hotspots in coral reef environments: physical drivers, ecophysiological outcomes and impact upon structural complexity. Front. Mar. Sci. 6, 498 (2019).

    Article  Google Scholar 

  104. Krueger, T. et al. Antioxidant plasticity and thermal sensitivity in four types of Symbiodinium sp. J. Phycol. 50, 1035–1047 (2014).

    Article  CAS  PubMed  Google Scholar 

  105. Reusch, T. B. H. & Boyd, P. W. Experimental evolution meets marine phytoplankton. Evolution 67, 1849–1859 (2013).

    Article  PubMed  Google Scholar 

  106. Schlüter, L., Lohbeck, K. T., Gröger, J. P., Riebesell, U. & Reusch, T. B. H. Long-term dynamics of adaptive evolution in a globally important phytoplankton species to ocean acidification. Sci. Adv. 2, e1501660 (2016).

    Article  ADS  PubMed  PubMed Central  Google Scholar 

  107. Schlüter, L. et al. Adaptation of a globally important coccolithophore to ocean warming and acidification. Nat. Clim. Change 4, 1024–1030 (2014).

    Article  ADS  Google Scholar 

  108. Aranguren-Gassis, M., Kremer, C. T., Klausmeier, C. A. & Litchman, E. Nitrogen limitation inhibits marine diatom adaptation to high temperatures. Ecol. Lett. 22, 1860–1869 (2019).

    Article  PubMed  Google Scholar 

  109. Dam, H. G. Evolutionary adaptation of marine zooplankton to global change. Ann. Rev. Mar. Sci. 5, 349–370 (2013).

    Article  PubMed  Google Scholar 

  110. Hinder, S. L. et al. Multi-decadal range changes vs. thermal adaptation for north east Atlantic oceanic copepods in the face of climate change. Glob. Change Biol. 20, 140–146 (2014).

    Article  ADS  Google Scholar 

  111. Antell, G. S., Fenton, I. S., Valdes, P. J. & Saupe, E. E. Thermal niches of planktonic foraminifera are static throughout glacial-interglacial climate change. Proc. Natl Acad. Sci. USA 118, e2017105118 (2021).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  112. Lonhart, S. I., Jeppesen, R., Beas-Luna, R., Crooks, J. A. & Lorda, J. Shifts in the distribution and abundance of coastal marine species along the eastern Pacific Ocean during marine heatwaves from 2013 to 2018. Mar. Biodivers. Rec. 12, 13 (2019).

    Article  Google Scholar 

  113. Pinsky, M. L., Selden, R. L. & Kitchel, Z. J. Climate-driven shifts in marine species ranges: scaling from organisms to communities. Ann. Rev. Mar. Sci. 12, 153–179 (2020).

    Article  PubMed  Google Scholar 

  114. Thurman, L. L. et al. Persist in place or shift in space? Evaluating the adaptive capacity of species to climate change. Front. Ecol. Environ. 18, 520–528 (2020).

    Article  Google Scholar 

  115. Gilman, S. E., Urban, M. C., Tewksbury, J., Gilchrist, G. W. & Holt, R. D. A framework for community interactions under climate change. Trends Ecol. Evol. 25, 325–331 (2010).

    Article  PubMed  Google Scholar 

  116. Dutkiewicz, S., Boyd, P. W. & Riebesell, U. Exploring biogeochemical and ecological redundancy in phytoplankton communities in the global ocean. Glob. Change Biol. 27, 1196–1213 (2021).

    Article  ADS  Google Scholar 

  117. Bernhardt, J. R. & Leslie, H. M. Resilience to climate change in coastal marine ecosystems. Ann. Rev. Mar. Sci. 5, 371–392 (2013).

    Article  PubMed  Google Scholar 

  118. Grant, P. R. et al. Evolution caused by extreme events. Philos. Trans. R. Soc. B Biol. Sci. 372, 5–8 (2017).

    Article  ADS  Google Scholar 

  119. Gonzalez, A. & Loreau, M. The causes and consequences of compensatory dynamics in ecological communities. Annu. Rev. Ecol. Evol. Syst. 40, 393–414 (2009).

    Article  Google Scholar 

  120. Vallina, S. M. & Le Quéré, C. Stability of complex food webs: resilience, resistance and the average interaction strength. J. Theor. Biol. 272, 160–173 (2011).

    Article  ADS  MathSciNet  PubMed  MATH  Google Scholar 

  121. Neutel, A. M. et al. Reconciling complexity with stability in naturally assembling food webs. Nature 449, 599–602 (2007).

    Article  ADS  CAS  PubMed  Google Scholar 

  122. Ives, A. R. & Cardinale, B. J. Food-web interactions govern the resistance of communities after non-random extinctions. Nature 429, 174–177 (2004).

    Article  ADS  CAS  PubMed  Google Scholar 

  123. Nagelkerken, I., Goldenber, S. U., Ferreir, C. M., Ullah, H. & Conne, S. D. Trophic pyramids reorganize when food web architecture fails to adjust to ocean change. Science 369, 829–832 (2020).

    Article  ADS  CAS  PubMed  Google Scholar 

  124. Carpenter, S. R. et al. Cascading trophic interactions and lake productivity. Bioscience 35, 634–639 (1985).

    Article  Google Scholar 

  125. Bideault, A. et al. Thermal mismatches in biological rates determine trophic control and biomass distribution under warming. Glob. Change Biol. 27, 257–269 (2021).

    Article  ADS  Google Scholar 

  126. Dee, L. E., Okamtoto, D., Gårdmark, A., Montoya, J. M. & Miller, S. J. Temperature variability alters the stability and thresholds for collapse of interacting species: species interactions facing variability. Philos. Trans. R. Soc. B Biol. Sci. 375, 20190457 (2020).

    Article  Google Scholar 

  127. Adjeroud, M. et al. Recovery of coral assemblages despite acute and recurrent disturbances on a south central Pacific reef. Sci. Rep. 8, 9680 (2018).

    Article  ADS  PubMed  PubMed Central  Google Scholar 

  128. Hughes, T. P. et al. Ecological memory modifies the cumulative impact of recurrent climate extremes. Nat. Clim. Change 9, 40–43 (2019).

    Article  ADS  Google Scholar 

  129. Boyd, P. W. et al. Biological responses to environmental heterogeneity under future ocean conditions. Glob. Change Biol. 22, 2633–2650 (2016).

    Article  ADS  Google Scholar 

  130. Ainsworth, T. D., Hurd, C. L., Gates, R. D. & Boyd, P. W. How do we overcome abrupt degradation of marine ecosystems and meet the challenge of heat waves and climate extremes? Glob. Change Biol. 26, 343–354 (2020).

    Article  ADS  Google Scholar 

  131. 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). Develops the concept of how other stressors can interact with each other in marine ectotherms.

    Article  PubMed  Google Scholar 

  132. Deutsch, C., Ferrel, A., Seibel, B., Portner, H.-O. & Huey, R. B. Climate change tightens a metabolic constraint on marine habitats. Science 348, 1132–1135 (2015).

    Article  ADS  CAS  PubMed  Google Scholar 

  133. Deutsch, C., Penn, J. L. & Seibel, B. Metabolic trait diversity shapes marine biogeography. Nature 585, 557–562 (2020).

    Article  ADS  CAS  PubMed  Google Scholar 

  134. Kroeker, K. J. et al. Impacts of ocean acidification on marine organisms: quantifying sensitivities and interaction with warming. Glob. Change Biol. 19, 1884–1896 (2013).

    Article  ADS  Google Scholar 

  135. Bertolini, C. & Pastres, R. Tolerance landscapes can be used to predict species-specific responses to climate change beyond the marine heatwave concept: using tolerance landscape models for an ecologically meaningful classification of extreme climate events. Estuar. Coast. Shelf Sci. 252, 107284 (2021).

    Article  Google Scholar 

  136. Le Gland, G., Vallina, S. M., Smith, S. L. & Cermeño, P. SPEAD 1.0—simulating plankton evolution with adaptive dynamics in a two-trait continuous fitness landscape applied to the Sargasso Sea. Geosci. Model Dev. 14, 1949–1985 (2021).

    Article  ADS  Google Scholar 

  137. Merico, A., Bruggeman, J. & Wirtz, K. A trait-based approach for downscaling complexity in plankton ecosystem models. Ecol. Modell. 220, 3001–3010 (2009).

    Article  CAS  Google Scholar 

  138. Walworth, N. G., Zakem, E. J., Dunne, J. P., Collins, S. & Levine, N. M. Microbial evolutionary strategies in a dynamic ocean. Proc. Natl Acad. Sci. USA 117, 5943–5948 (2020).

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  139. Toseland, A. et al. The impact of temperature on marine phytoplankton resource allocation and metabolism. Nat. Clim. Change 3, 979–984 (2013).

    Article  ADS  CAS  Google Scholar 

  140. Collins, M. et al. IPCC Special Report on the Ocean and Cryosphere in a Changing Climate (eds. Pörtner, H.-O. et al.) Ch. 6 (IPCC, 2021).

  141. Hughes, T. P. et al. Global warming and recurrent mass bleaching of corals. Nature 543, 373–377 (2017).

    Article  ADS  CAS  PubMed  Google Scholar 

  142. Cheung, W. W. L., Reygondeau, G. & Frölicher, T. L. Large benefits to marine fisheries of meeting the 1.5 °C global warming target. Science 354, 1591–1594 (2016).

    Article  ADS  CAS  PubMed  Google Scholar 

  143. Rashid Sumaila, U. et al. Benefits of the Paris Agreement to ocean life, economies, and people. Sci. Adv. 5, eaau3855 (2019).

    Article  ADS  PubMed  Google Scholar 

  144. Tilbrook, B. et al. An enhanced ocean acidification observing network: from people to technology to data synthesis and information exchange. Front. Mar. Sci. 6, 337 (2019).

    Article  Google Scholar 

  145. Claustre, H., Johnson, K. S. & Takeshita, Y. Observing the global ocean with Biogeochemical-Argo. Ann. Rev. Mar. Sci. 12, 23–48 (2020).

    Article  PubMed  Google Scholar 

  146. Chai, F. et al. Monitoring ocean biogeochemistry with autonomous platforms. Nat. Rev. Earth Environ. 1, 315–326 (2020).

    Article  ADS  Google Scholar 

  147. Fennel, K. et al. Advancing marine biogeochemical and ecosystem reanalyses and forecasts as tools for monitoring and managing ecosystem health. Front. Mar. Sci. 6, 89 (2019).

    Article  Google Scholar 

  148. Reichstein, M. et al. Deep learning and process understanding for data-driven Earth system science. Nature 566, 195–204 (2019).

    Article  ADS  CAS  PubMed  Google Scholar 

  149. Sen Gupta, A. et al. Drivers and impacts of the most extreme marine heatwaves events. Sci. Rep. 10, 19359 (2020).

    Article  ADS  PubMed  PubMed Central  Google Scholar 

  150. Holbrook, N. J. et al. Keeping pace with marine heatwaves. Nat. Rev. Earth Environ. 1, 482–493 (2020).

    Article  ADS  Google Scholar 

  151. Boyd, P. & Hutchins, D. Understanding the responses of ocean biota to a complex matrix of cumulative anthropogenic change. Mar. Ecol. Prog. Ser. 470, 125–135 (2012).

    Article  ADS  Google Scholar 

  152. Thomas, M. K. et al. Temperature–nutrient interactions exacerbate sensitivity to warming in phytoplankton. Glob. Change Biol. 23, 3269–3280 (2017).

    Article  ADS  Google Scholar 

  153. Clark, J. R., Daines, S. J., Lenton, T. M., Watson, A. J. & Williams, H. T. P. Individual-based modelling of adaptation in marine microbial populations using genetically defined physiological parameters. Ecol. Modell. 222, 3823–3837 (2011).

    Article  Google Scholar 

  154. Bruggeman, J. & Kooijman, S. A. L. M. A biodiversity-inspired approach to aquatic ecosystem modeling. Limnol. Oceanogr. 52, 1533–1544 (2007).

    Article  ADS  Google Scholar 

  155. Small-Lorenz, S. L., Culp, L. A., Ryder, T. B., Will, T. C. & Marra, P. P. A blind spot in climate change vulnerability assessments. Nat. Clim. Change 3, 91–93 (2013).

    Article  ADS  Google Scholar 

  156. Sala, E. et al. Protecting the global ocean for biodiversity, food and climate. Nature 592, 397–402 (2021).

    Article  ADS  CAS  PubMed  Google Scholar 

  157. Halpern, B. S. et al. An index to assess the health and benefits of the global ocean. Nature 488, 615–620 (2012).

    Article  ADS  CAS  PubMed  Google Scholar 

  158. Suryan, R. M. et al. Ecosystem response persists after a prolonged marine heatwave. Sci. Rep. 11, 6235 (2021).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  Google Scholar 

  160. Liquete, C. et al. Current status and future prospects for the assessment of marine and coastal ecosystem services: a systematic review. PLoS ONE 8, e67737 (2013).

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  161. Glynn, P. W. & D’Croz, L. Experimental evidence for high temperature stress as the cause of El Nino-coincident coral mortality. Coral Reefs 8, 181–191 (1990).

    Article  ADS  Google Scholar 

  162. Eakin, C. M. et al. Caribbean corals in crisis: record thermal stress, bleaching, and mortality in 2005. PLoS ONE 5, e13969 (2010).

    Article  ADS  PubMed  PubMed Central  Google Scholar 

  163. Gardner, J., Manno, C., Bakker, D. C. E., Peck, V. L. & Tarling, G. A. Southern Ocean pteropods at risk from ocean warming and acidification. Mar. Biol. 165, 8 (2018).

    Article  PubMed  Google Scholar 

Download references

Acknowledgements

N.G., M.V. and T.L.F. acknowledge support from the Swiss National Science Foundation (project XEBUS and PP00P2-198897), and from the European Union’s Horizon 2020 research and innovation programme under grant agreement no. 820989 (project COMFORT). The work reflects only the authors’ views; the European Commission and their executive agency are not responsible for any use that may be made of the information the work contains. P.W.B. was primarily supported by the Australian Research Council through a Laureate (FL160100131). P.W.B. also acknowledges support from NSF to the SCOR infrastructure project COBS (Changing Ocean Biological Systems). N.G. thanks F. Desmet, E. Köhn and J. Perreten for evaluating and analysing the regional ocean biogeochemical model simulations for the northeast Pacific Blob event. The GFDL ESM2M simulations were conducted by Friedrich Burger on the Swiss National Supercomputing Centre. We thank K. Fennel and A. Sen Gupta for their constructive reviews and inputs.

Author information

Authors and Affiliations

  1. Environmental Physics, Institute of Biogeochemistry and Pollutant Dynamics, ETH Zürich, Zürich, Switzerland

    Nicolas Gruber & Meike Vogt

  2. Institute for Marine and Antarctic Studies, University of Tasmania, Hobart, Tasmania, Australia

    Philip W. Boyd

  3. Climate and Environmental Physics, University of Bern, Bern, Switzerland

    Thomas L. Frölicher

  4. Oeschger Centre for Climate Change Research, University of Bern, Bern, Switzerland

    Thomas L. Frölicher

Authors
  1. Nicolas Gruber
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Philip W. Boyd
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Thomas L. Frölicher
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Meike Vogt
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

N.G. conceived this Perspective, visualized and wrote it with strong conceptual and editorial input by all of the co-authors. P.W.B. and M.V. led the writing of the biological impact section and T.F. led the analyses of the global model results.

Corresponding author

Correspondence to Nicolas Gruber.

Ethics declarations

Competing interests

The authors declare no competing interests.

Additional information

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

Peer review information Nature thanks Katja Fennel and Alex Sen Gupta and the other, anonymous, reviewer(s) for their contribution to the peer review of this work.

Supplementary information

Supplementary Information

Supplementary Notes and Supplementary Figs. 1–6.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Gruber, N., Boyd, P.W., Frölicher, T.L. et al. Biogeochemical extremes and compound events in the ocean. Nature 600, 395–407 (2021). https://doi.org/10.1038/s41586-021-03981-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/s41586-021-03981-7

This article is cited by

Comments

By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.

Search

Advanced search

Quick links

Nature Briefing Anthropocene

Sign up for the Nature Briefing: Anthropocene newsletter — what matters in anthropocene research, free to your inbox weekly.

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