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.

  • Article
  • Published:

Marine organic carbon burial increased forest fire frequency during Oceanic Anoxic Event 2

Nature Geoscience volume 13, pages 693–698 (2020)Cite this article

Subjects

Abstract

Volcanic-driven nutrient flux to the oceans stimulated marine productivity and organic matter burial during Oceanic Anoxic Event 2 (OAE2; ~94 million years ago). While the preferential burial of 13C-depleted organic matter led to a general 13C enrichment of sediments during the event, a 2‰ 13C depletion punctuated the first half of the event (known as the Plenus), raising questions about carbon cycle feedbacks during OAE2. Here we present organic geochemical evidence (for example, pyrogenic polycyclic aromatic hydrocarbons) from the Western Interior Seaway that indicates increased forest fire frequency in the western United States during the Plenus. Carbon mass balance equations, which account for the amount and carbon isotopic composition of atmospheric CO2 and forest biomass during OAE2, potentiate fires in the western United States as part of a widespread increase in forest fires that could have alone caused the global 2‰ 13C depletion during the Plenus. Plant biomarkers suggest that local precipitation and plant type did not change significantly, indicating that elevated atmospheric oxygen levels from widespread organic carbon burial increased the frequency of fires in wet forest ecosystems that were extensive during OAE2. Plant biomarkers also indicate that forest fires amplified the flux of terrestrial organic matter and nutrients to the oceans, which may have enhanced marine productivity, organic carbon burial and the return to 13C-enriched sediments at the end of the Plenus. The extent that this feedback impacted global biogeochemistry during the Plenus and the rest of OAE2, as well as other events in Earth history, warrants further investigation.

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: Palaeogeography of the study area.
Fig. 2: Bulk organic carbon and biomarkers from the SH#1 core.
Fig. 3: Carbon mass balance equations show the potential that forest fires were widespread during the Plenus.

Similar content being viewed by others

Data availability

The data supporting the findings of this study are available within the paper, its Supplementary Information, and on Pangaea74.

Code availability

The carbon mass balance equation R markdown is available on Pangaea74.

References

  1. Freeman, K. H. & Hayes, J. M. Fractionation of carbon isotopes by phytoplankton and estimates of ancient CO2 levels. Glob. Biogeochem. Cycles 6, 185–198 (1992).

    Google Scholar 

  2. Pancost, R. D. et al. Further evidence for the development of photic-zone euxinic conditions during Mesozoic oceanic anoxic events. J. Geol. Soc. London 161, 353–364 (2004).

    Google Scholar 

  3. Monteiro, F. M., Pancost, R. D., Ridgwell, A. & Donnadieu, Y. Nutrients as the dominant control on the spread of anoxia and euxinia across the Cenomanian-Turonian oceanic anoxic event (OAE2): model-data comparison. Paleoceanography 27, PA4209 (2012).

    Google Scholar 

  4. Schlanger, S. O. & Jenkyns, H. C. Cretaceous oceanic anoxic events: causes and consequences. Geol. Mijnbouw 55, 179–184 (1976).

    Google Scholar 

  5. Jones, M. M. et al. Astronomical pacing of relative sea level during Oceanic Anoxic Event 2: preliminary studies of the expanded SH#1 Core, Utah. Geol. Soc. Am. Bull. 131, 1702–1722 (2019).

    Google Scholar 

  6. Gale, A. S. & Christenson, W. K. Occurrence of the belemnite Actinocamax plenus in the Cenomanian of SE France and its significance. Bull. Geol. Soc. Den. 43, 68–77 (1996).

    Google Scholar 

  7. O’Connor, L. K. et al. A re-evaluation of the Plenus Cold Event, and the links between CO2, temperature, and seawater chemistry during OAE 2. Paleoceanogr. Paleoclimatol. 35, e2019PA003631 (2019).

    Google Scholar 

  8. Kuhnt, W. et al. Unravelling the onset of Cretaceous Oceanic Anoxic Event 2 in an extended sediment archive from the Tarfaya-Laayoune Basin, Morocco. Paleoceanogr. Paleoclimatol. 32, 923–946 (2017).

    Google Scholar 

  9. Kuroda, J. & Ohkouchi, N. Implications of spatiotemporal distribution of black shales deposited during the Cretaceous oceanic anoxic event-2. Paleontol. Res. 10, 345–358 (2006).

    Google Scholar 

  10. Owens, J. D., Lyons, T. W. & Lowery, C. M. Quantifying the missing sink for global organic carbon burial during a Cretaceous oceanic anoxic event. Earth Planet. Sci. Lett. 499, 83–94 (2018).

    Google Scholar 

  11. Berner, R. A. Phanerozoic atmospheric oxygen: new results using the GEOCARBSULF model. Am. J. Sci. 309, 603–606 (2009).

    Google Scholar 

  12. Baker, S. J., Hesselbo, S. P., Lenton, T. M., Duarte, L. V. & Belcher, C. M. Charcoal evidence that rising atmospheric oxygen terminated Early Jurassic ocean anoxia. Nat. Commun. 8, 15018 (2017).

    Google Scholar 

  13. Kump, L. R. Terrestrial feedback in atmosphere oxygen regulation by fire and phosphorus. Nature 335, 152–154 (1988).

    Google Scholar 

  14. Watson, A., Lovelock, J. E. & Margulis, L. Methanogenesis, fires and the regulation of atmospheric oxygen. Biosystems 10, 293–298 (1978).

    Google Scholar 

  15. Bond, W. J. & Scott, A. C. Fire and the spread of flowering plants in the Cretaceous. New Phytol. 188, 1137–1150 (2010).

    Google Scholar 

  16. Brown, S. A. E., Scott, A. C., Glasspool, I. J. & Collinson, W. E. Cretaceous wildfires and their impact on the Earth system. Cretac. Res. 36, 162–190 (2012).

    Google Scholar 

  17. Glasspool, I. J. & Scott, A. C. Phanerozoic concentrations of atmospheric oxygen reconstructed from sedimentary charcoal. Nat. Geosci. 3, 627–630 (2010).

    Google Scholar 

  18. Baker, S. J. et al. CO2-induced climate forcing on the fire record during the initiation of Cretaceous oceanic anoxic event 2. Geol. Soc. Am. Bull. 132, 321–333 (2019).

    Google Scholar 

  19. Zhang, M., Dai, S., Du, B., Ji, L. & Hu, S. Mid-Cretaceous hothouse climate and the expansion of early angiosperms. Acta Geol. Sin. Engl. 92, 2004–2025 (2018).

    Google Scholar 

  20. Blumer, M. Polycyclic aromatic compounds in nature. Sci. Am. 234, 35–45 (1976).

    Google Scholar 

  21. Lima, A. L. C., Farrington, J. W. & Reddy, C. M. Combustion-derived polycyclic aromatic hydrocarbons in the environment—a review. Environ. Forensics 6, 109–113 (2005).

    Google Scholar 

  22. Youngblood, W. W. & Blumer, M. Polycyclic aromatic hydrocarbons in the environment: homologous series in soils and recent marine sediments. Geochim. Cosmochim. Acta 39, 1303–1314 (1975).

    Google Scholar 

  23. Killops, S. D. & Massoud, M. S. Polycyclic aromatic hydrocarbons of pyrolytic origin in ancient sediments: evidence for Jurassic vegetation fires. Org. Geochem. 18, 1–7 (1992).

    Google Scholar 

  24. Finkelstein, D. B., Pratt, L. M., Curtin, T. M. & Brassell, S. C. Wildfires and seasonal aridity recorded in Late Cretaceous strata from south-eastern Arizona, USA. Sedimentology 52, 587–599 (2005).

    Google Scholar 

  25. Belcher, C. M., Finch, P., Collinson, M. E., Scott, A. C. & Grassineau, N. V. Geochemical evidence for combustion of hydrocarbons during the K-T impact event. Proc. Natl Acad. Sci. USA 106, 4112–4117 (2009).

    Google Scholar 

  26. Tsikos, H. et al. Carbon-isotope stratigraphy recorded by the Cenomanian-Turonian Oceanic Anoxic Event: correlation and implications based on three key localities. J. Geol. Soc. London 161, 711–719 (2004).

    Google Scholar 

  27. Jarvis, I., Lignum, J. S., Grocke, D. R., Jenkyns, H. C. & Pearce, M. A. Black shale deposition, atmospheric CO2 drawdown, and cooling during the Cenomanian-Turonian Oceanic Anoxic Event. Paleoceanography 26, PA3201 (2011).

    Google Scholar 

  28. Joo, Y. J. & Sageman, B. B. Cenomanian to Campanian carbon isotope chemostratigraphy from the western interior basin, USA. J. Sediment. Res. 84, 529–542 (2014).

    Google Scholar 

  29. Jenkyns, H. C., Dickson, A. J., Ruhl, M. & van den Boorn, S. H. J. M. Basalt-seawater interaction, the Plenus Cold Event, enhanced weathering and geochemical change: deconstructing Oceanic Anoxic Event 2 (Cenomanian-Turonian, Late Cretaceous). Sedimentology 64, 16–43 (2017).

    Google Scholar 

  30. Heimhofer, U. et al. Vegetation response to exceptional global warmth during Oceanic Anoxic Event 2. Nat. Commun. 9, 3832 (2018).

    Google Scholar 

  31. Elder, W. P. Geometry of Upper Cretaceous bentonite beds: implications about volcanic source areas and paleowind patterns, western interior, United States. Geology 16, 835–838 (1988).

    Google Scholar 

  32. He, T., Pausas, J. G., Belcher, C. M., Schwilk, D. W. & Lamont, B. B. Fire-adapted traits of Pinus arose in the fiery Cretaceous. New Phytol. 194, 751–759 (2012).

    Google Scholar 

  33. Belcher, C. M. & Hudspith, V. A. Changes to Cretaceous surface fire behavior influenced the spread of the early angiosperms. New Phytol. 213, 1521–1532 (2016).

    Google Scholar 

  34. Chumakov, N. M. et al. Climate belts of the mid-Cretaceous time. Stratigr. Geol. Correl. 3, 241–260 (1995).

    Google Scholar 

  35. Hasegawa, H. et al. Drastic shrinking of the Hadley circulation during the mid-Cretaceous Supergreenhouse. Clim. Past 8, 1323–1337 (2012).

    Google Scholar 

  36. Hay, W. W. Possible solutions to several enigmas of Cretaceous climate. Int. J. Earth Sci. 108, 587–620 (2018).

    Google Scholar 

  37. Hay, W. W. & Floegel, S. New thoughts about the Cretaceous climate and oceans. Earth Sci. Rev. 115, 262–272 (2012).

    Google Scholar 

  38. Scopelliti, G. et al. High-resolution geochemical and biotic records of the Tethyan ‘Bonarelli Level’ (OAE2, latest Cenomanian) from the Calabianca-Guidaloca composite section, northwestern Sicily, Italy. Palaeogeogr. Palaeoclimatol. Palaeoecol. 208, 293–317 (2004).

    Google Scholar 

  39. Charbonnier, G. et al. Obliquity pacing of the hydrological cycle during the Oceanic Anoxic Event 2. Earth Planet. Sci. Lett. 499, 266–277 (2018).

    Google Scholar 

  40. Van Helmond, N. A. G. M. et al. A perturbed hydrological cycle during Oceanic Anoxic Event 2. Geology 42, 123–126 (2014).

    Google Scholar 

  41. Carr, A. S. et al. Leaf wax n-alkane distributions in arid zone South African flora: environmental controls, chemotaxonomy and palaeoecological implications. Org. Geochem. 67, 72–84 (2014).

    Google Scholar 

  42. Denis, E. H., Pedentchouk, N., Schouten, S., Pagani, M. & Freeman, K. H. Fire and ecosystem change in the Arctic across the Paleocene-Eocene Thermal Maximum. Earth Planet. Sci. Lett. 467, 149–156 (2017).

    Google Scholar 

  43. Mills, B. J. E., Belcher, C. M., Lenton, T. M. & Newton, R. J. A modeling case for high atmospheric oxygen concentrations during the Mesozoic and Cenozoic. Geology 22, 1023–1026 (2016).

    Google Scholar 

  44. Bergman, N. M., Lenton, T. M. & Watson, A. J. COPSE: a new model of biogeochemical cycling over Phanerozoic time. Am. J. Sci. 304, 397–437 (2004).

    Google Scholar 

  45. Kump, L. Chemical stability of the atmosphere and ocean. Palaeogeogr. Palaeoclimatol. Palaeoecol. 75, 123–136 (1989).

    Google Scholar 

  46. Saltzman, M. R. et al. Pulse of atmospheric oxygen during the late Cambrian. Proc. Natl Acad. Sci. USA 108, 3876–3881 (2011).

    Google Scholar 

  47. Huang, J. et al. The global oxygen budget and its future projection. Sci. Bull. 63, 1180–1186 (2018).

    Google Scholar 

  48. Klages, J. P. et al. Temperature rainforests near the South Pole during peak Cretaceous warmth. Nature 580, 81–86 (2020).

    Google Scholar 

  49. Turgeon, S. C. & Creaser, R. A. Cretaceous oceanic anoxic event 2 triggered by a massive magmatic episode. Nature 454, 323–326 (2008).

    Google Scholar 

  50. Jones, M. M., Sageman, B. B. & Selby, D. Stratigraphic record of OAE2 from the Western Interior Basin (N. America): new insights from osmium isotopes (OSi) and the expanded Big Water, UT site. In Society for Sedimentary Geology (SEPM) Research Conference on Oceanic Anoxic Events (Oral Presentation) (2016).

  51. Arinobu, T., Ishiwatari, R., Kaiho, K. & Lamolda, M. A. Spike of pyrosynthetic polycyclic aromatic hydrocarbons associated with an abrupt decrease in δ13C of a terrestrial biomarker at the Cretaceous-Tertiary boundary at Caravaca, Spain. Geology 27, 723–726 (1999).

    Google Scholar 

  52. Finkelstein, D. B., Pratt, L. M. & Brassell, S. C. Can biomass burning produce a globally significant carbon-isotope excursion in the sedimentary record? Earth Planet. Sci. Lett. 250, 501–510 (2006).

    Google Scholar 

  53. Barclay, R. S., McElwain, J. C. & Sageman, B. B. Carbon sequestration activated by a volcanic CO2 pulse during Ocean Anoxic Event 2. Nat. Geosci. 3, 205–208 (2010).

    Google Scholar 

  54. van Bentum, E. C., Reichart, G.-J., Forster, A. & Sinninghe Damsté, J. S. Latitudinal differences in the amplitude of the OAE-2 carbon isotopic excursion: pCO2 and paleo productivity. Biogeosciences 9, 717–731 (2012).

    Google Scholar 

  55. Abatzoglou, J. T. & Williams, A. P. Impact of anthropogenic climate change on wildfire across western US forests. Proc. Natl Acad. Sci. USA 113, 11770–11775 (2016).

    Google Scholar 

  56. Shen, W., Sun, Y., Lin, Y., Liu, D. & Chai, P. Evidence for wildfire in the Meishan section and implications for Permian-Triassic events. Geochim. Cosmochim. Acta 75, 1992–2006 (2011).

    Google Scholar 

  57. Raison, R. J. Modification of the soil environment by vegetation fires, with particular reference to nitrogen transformations: a review. Plant Soil 51, 73–108 (1979).

    Google Scholar 

  58. Spencer, C. N. & Hauer, F. R. Phosphorus and nitrogen dynamics in streams during a wildfire. J. North Am. Benthol. Soc. 10, 24–30 (1991).

    Google Scholar 

  59. Moody, J. A. & Martin, D. A. Initial hydrologic and geomorphic response following a wildfire in the Colorado Front Range. Earth Surf. Process. Landf. 26, 1049–1070 (2001).

    Google Scholar 

  60. Guieu, C., Bonnet, S., Wagener, T. & Loye-Piot, M.-D. Biomass burning as a source of dissolved iron to the open ocean? Geophys. Res. Lett. 32, L19608 (2005).

    Google Scholar 

  61. Shakesby, R. A. & Doerr, S. H. Wildfire as a hydrological and geomorphological agent. Earth Sci. Rev. 74, 269–307 (2006).

    Google Scholar 

  62. Kaiho, K. et al. A forest fire and soil erosion event during the Late Devonian mass extinction. Palaeogeogr. Palaeoclimatol. Palaeoecol. 392, 272–280 (2013).

    Google Scholar 

  63. Barkley, A. E. et al. African biomass burning is a substantial source of phosphorus deposition to the Amazon, tropical Atlantic Ocean, and Southern Ocean. Proc. Natl Acad. Sci. USA 116, 16216–16221 (2019).

    Google Scholar 

  64. Leckie, R. M., Yuretich, R. F., West, O. L. O., Finkelstein, D. & Schmidt, M. in Stratigraphy and Paleoenvironments of the Cretaceous Western Interior Seaway, USA Vol. 6 (eds Dean, W. E. & Arthur, M. A.) 101–126 (Society for Sedimentary Geology, 1998).

  65. Pogge von Strandmann, P. A. E., Jenkyns, H. C. & Woodfine, R. G. Lithium isotope evidence for enhanced weathering during Oceanic Anoxic Event 2. Nat. Geosci. 6, 668–672 (2013).

    Google Scholar 

  66. Blättler, C. L., Jenkyns, H. C., Reynard, L. M. & Henderson, G. H. Significant increases in global weathering during Oceanic Anoxic Events 1a and 2 indicated by calcium isotopes. Earth Planet. Sci. Lett. 309, 77–88 (2011).

    Google Scholar 

  67. Knoll, M. A. & James, W. C. Effect of the advent and diversification of vascular land plants on mineral weathering through geologic time. Geology 15, 1099–1102 (1987).

    Google Scholar 

  68. Lenton, T. M. & Watson, A. J. Redfield revisited: what regulates the oxygen content of the atmosphere? Glob. Biogeochem. Cycles 14, 149–168 (2000).

    Google Scholar 

  69. Likens, G. E., Bormann, F. H. & Johnson, N. M. in Some Perspectives of the Major Biogeochemical Cycles (ed. Likens, G. E.) 93–112 (John Wiley & Sons, 1981).

  70. Boudinot, F. G. et al. Neritic ecosystem response to Oceanic Anoxic Event 2 in the Cretaceous Western Interior Seaway, USA. Palaeogeogr. Palaeoclimaol. Palaeoecol. 546, 109673 (2020).

    Google Scholar 

  71. Sinninghe Damsté, J. S., van Bentum, E. C., Reichart, G.-J., Pross, J. & Schouten, S. A CO2 decrease-driven cooling and increased latitudinal temperature gradient during the mid-Cretaceous Oceanic Anoxic Event 2. Earth Planet. Sci. Lett. 293, 97–103 (2010).

    Google Scholar 

  72. Van Helmond, N. A. G. M. et al. Equatorward phytoplankton migration during a cold spell within the Late Cretaceous super-greenhouse. Biogeosciences 13, 2856–2872 (2016).

    Google Scholar 

  73. Forster, A., Schouten, S., Moriya, K., Wilson, P. A. & Sinninghe Damsté, J. S. Tropical warming and intermittent cooling during the Cenomanian/Turonian oceanic anoxic event 2: sea surface temperature records from the equatorial Atlantic. Paleoceanogr. 22, PA1219 (2007).

    Google Scholar 

  74. Boudinot, F. G. and Sepúlveda, J. Organic geochemistry of SH#1 core: fires. PANGAEA https://doi.pangaea.de/10.1594/PANGAEA.921198 (2020).

Download references

Acknowledgements

We thank members of the Organic Geochemistry Lab at The University of Colorado Boulder N. Dildar, J. van Oosten, T. Bond, S. Gandhi-Besbes, J. Straight, S. Tostanoski, A. Mcquade, H. Nguyen and J. Lopez for laboratory assistance, B. Davidheiser-Kroll and K. Snell for help with the organic carbon analysis, members of the NSF-funded Collaborative Research: Perturbation of the Marine Food Web and Extinction During the Oceanic Anoxic Event at the Cenomanian/Turonian B. Sageman, M. Jones, T. Bralower, R. L. Oakes, M. Leckie and A. L. Parker for field activities, sample collection and fruitful discussions, A. Titus (Bureau of Land Management, Grand Staircase-Escalante National Monument) for prospecting coring sites and obtaining collecting permits, J. Spencer (US National Park Service Glen Canyon Recreational Area) for accessing outcrop sections, J. Parlett, S. Crawford, the western US Geological Survey drilling crew, C. Lowery, S. Karduck, Q. Li, M. Wnuk and L. Victoria for sample collection during fieldwork, and J. van Dijk, T. Marchitto and F. D. Boudinot for helpful comments on the manuscript. This study was funded by the NSF Division of Earth Sciences, Earth-Life Transitions (ELT) programme grant number 1338318, and by the American Chemical Society Petroleum Research Fund (ACS-PRF) – Doctoral New Investigator Award number 58815-DNI2. F.G.B. acknowledges support from the Department of Geological Sciences at the University of Colorado Boulder.

Author information

Authors and Affiliations

  1. Department of Geological Sciences, University of Colorado Boulder, Boulder, CO, USA

    F. Garrett Boudinot & Julio Sepúlveda

  2. Institute of Arctic and Alpine Research (INSTAAR), University of Colorado Boulder, Boulder, CO, USA

    F. Garrett Boudinot & Julio Sepúlveda

Authors
  1. F. Garrett Boudinot
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Julio Sepúlveda
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

F.G.B. and J.S. designed the study. F.G.B. carried out the sample preparation, developed GC-MS analytical methods, performed biomarker and TOC analysis, processed the data and set up and ran carbon mass balance equations. F.G.B. and J.S. interpreted results and wrote the manuscript.

Corresponding author

Correspondence to F. Garrett Boudinot.

Ethics declarations

Competing interests

The authors declare no competing interests.

Additional information

Peer review information Primary Handling Editor: James Super.

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

Extended data

Extended Data Fig. 1 SH#1 core pyroPAH concentrations that indicate enhanced forest fire frequency during the Plenus interval of OAE2.

Shading scheme is the same as in Fig.2.

Extended Data Fig. 2 Other pyroPAH concentrations in the SH#1 core that do not increase during the Plenus compared to pre-and post-Plenus intervals.

Shading scheme is the same as in Fig.2.

Extended Data Fig. 3 The effect of different atmospheric δ13CCO2 values on forest fire area estimates.

Axes and blue shading same as in Fig. 3 main text. Line types indicate different δ13CCO2 values (solid = 2‰, dashed = 4‰) used to test sensitivity of carbon mass balance equation to starting CO2 carbon isotopic composition. Minimum estimate (900 ppm CO2, δ13CCO2 = 4‰, total forest size of 1000 Gt C) is 28%, maximum estimate (1100 ppm CO2, δ13CCO2 = 2‰, total forest size of 900 Gt C) is 41%.

Extended Data Fig. 4 The effect of different terrestrial biomass δ13C values on forest fire area estimates.

Axes and blue shading same as in Fig. 3 main text. Line types indicate different forest biomass δ13C values (solid = −28‰, dashed = -24‰) used to test sensitivity of carbon mass balance equation to starting forest biomass carbon isotopic composition. Minimum estimate (900 ppm CO2, δ13Cforest = −28, total forest size of 1000 Gt C) is 26%, maximum estimate (1100 ppm CO2, δ13Cforest = −24, total forest size of 900 Gt C) is 40%.

Extended Data Table 1 Changes in δ13Corg during the Plenus from sections around the world
Full size table
Extended Data Table 2 Reported changes in total organic carbon content (ΔTOC) during the Plenus from sections around the world
Full size table
Extended Data Table 3 OAE2-relevant values used in the carbon mass balance equation to estimate percentage of global forest fires during the Plenus
Full size table

Supplementary information

Supplementary Information

Supplementary Discussion and references for Supplementary Discussion

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Boudinot, F.G., Sepúlveda, J. Marine organic carbon burial increased forest fire frequency during Oceanic Anoxic Event 2. Nat. Geosci. 13, 693–698 (2020). https://doi.org/10.1038/s41561-020-0633-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/s41561-020-0633-y

This article is cited by

Search

Advanced 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