Skip to main content

Thank you for visiting 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.

Permian–Triassic mass extinction pulses driven by major marine carbon cycle perturbations


The Permian/Triassic boundary approximately 251.9 million years ago marked the most severe environmental crisis identified in the geological record, which dictated the onwards course for the evolution of life. Magmatism from Siberian Traps is thought to have played an important role, but the causational trigger and its feedbacks are yet to be fully understood. Here we present a new boron-isotope-derived seawater pH record from fossil brachiopod shells deposited on the Tethys shelf that demonstrates a substantial decline in seawater pH coeval with the onset of the mass extinction in the latest Permian. Combined with carbon isotope data, our results are integrated in a geochemical model that resolves the carbon cycle dynamics as well as the ocean redox conditions and nitrogen isotope turnover. We find that the initial ocean acidification was intimately linked to a large pulse of carbon degassing from the Siberian sill intrusions. We unravel the consequences of the greenhouse effect on the marine environment, and show how elevated sea surface temperatures, export production and nutrient input driven by increased rates of chemical weathering gave rise to widespread deoxygenation and sporadic sulfide poisoning of the oceans in the earliest Triassic. Our findings enable us to assemble a consistent biogeochemical reconstruction of the mechanisms that resulted in the largest Phanerozoic mass extinction.

Access options

Rent or Buy article

Get time limited or full article access on ReadCube.


All prices are NET prices.

Fig. 1: Brachiopod-based stable isotope data from Italy and China.
Fig. 2: Modelled marine carbonate system and climate change.
Fig. 3: Modelled redox state of the ocean, dissolved nutrient concentrations and nitrogen cycling.

Data availability

We have chosen not to deposit the data in a repository at this time, but all the geochemical data analysed during this study are accessible in the Supplementary Data file.

Code availability

Computer code is available upon reasonable request from K.W. (


  1. 1.

    Burgess, S. D., Bowring, S. & Shen, S.-Z. High-precision timeline for Earth’s most severe extinction. Proc. Natl Acad. Sci. USA 111, 3316–3321 (2014).

    Google Scholar 

  2. 2.

    Svensen, H. et al. Siberian gas venting and the end-Permian environmental crisis. Earth Planet. Sci. Lett. 277, 490–500 (2009).

    Google Scholar 

  3. 3.

    Burgess, S. D. & Bowring, S. A. High-precision geochronology confirms voluminous magmatism before, during, and after Earth’s most severe extinction. Sci. Adv. 1, e1500470 (2015).

    Google Scholar 

  4. 4.

    Saunders, A. D. Two LIPs and two Earth-system crises: the impact of the North Atlantic igneous province and the Siberian Traps on the Earth-surface carbon cycle. Geol. Mag. 153, 201–222 (2016).

    Google Scholar 

  5. 5.

    Cui, Y. & Kump, L. R. Global warming and the end-Permian extinction event: proxy and modeling perspectives. Earth Sci. Rev. 149, 5–22 (2015).

    Google Scholar 

  6. 6.

    Sun, Y. et al. Lethally hot temperatures during the early Triassic greenhouse. Science 338, 366–370 (2012).

    Google Scholar 

  7. 7.

    Brand, U. et al. The end-Permian mass extinction: a rapid volcanic CO2 and CH4-climatic catastrophe. Chem. Geol. 323, 121–144 (2012).

    Google Scholar 

  8. 8.

    Winguth, A. M. E., Shields, C. A. & Winguth, C. Transition into a hothouse world at the Permian–Triassic boundary—a model study. Palaeogeogr. Palaeoclimatol. Palaeoecol. 440, 316–327 (2015).

    Google Scholar 

  9. 9.

    Garbelli, C. et al. Neotethys seawater chemistry and temperature at the dawn of the end-Permian mass extinction. Gondwana Res. 35, 272–272 (2016).

    Google Scholar 

  10. 10.

    Wang, W. et al. A high-resolution middle to late Permian paleotemperature curve reconstructed using oxygen isotopes of well-preserved brachiopod shells. Earth Planet. Sci. Lett. 540, 116245 (2020).

    Google Scholar 

  11. 11.

    Lau, K. V. et al. Marine anoxia and delayed Earth system recovery after the end-Permian extinction. Proc. Natl Acad. Sci. USA 113, 2360–2365 (2016).

    Google Scholar 

  12. 12.

    Elrick, M. et al. Global-ocean redox variation during the middle-late Permian through Early Triassic based on uranium isotope and Th/U trends of marine carbonates. Geology 45, 163–166 (2017).

    Google Scholar 

  13. 13.

    Zhang, F. F. et al. Congruent Permian–Triassic δ238U records at Panthalassic and Tethyan sites: confirmation of global-oceanic anoxia and validation of the U-isotope paleoredox proxy. Geology 46, 327–330 (2018).

    Google Scholar 

  14. 14.

    Korte, C. et al. Carbon, sulfur, oxygen and strontium isotope records, organic geochemistry and biostratigraphy across the Permian/Triassic boundary in Abadeh, Iran. Int. J. Earth Sci. 93, 565–581 (2004).

    Google Scholar 

  15. 15.

    Grice, K. et al. Photic zone euxinia during the Permian–Triassic superanoxic event. Science 307, 706–709 (2005).

    Google Scholar 

  16. 16.

    Payne, J. L. et al. Calcium isotope constraints on the end-Permian mass extinction. Proc. Natl Acad. Sci. USA 107, 8543–8548 (2010).

    Google Scholar 

  17. 17.

    Clarkson, M. O. et al. Ocean acidification and the Permo-Triassic mass extinction. Science 348, 229–232 (2015).

    Google Scholar 

  18. 18.

    Garbelli, C., Angiolini, L. & Shen, S.-Z. Biomineralization and global change: a new perspective for understanding the end-Permian extinction. Geology 45, 19–22 (2017).

    Google Scholar 

  19. 19.

    Hönisch, B., Hemming, N. G., Archer, D., Siddall, M. & McManus, J. F. Atmospheric carbon dioxide concentration across the mid-Pleistocene transition. Science 324, 1551–1554 (2009).

    Google Scholar 

  20. 20.

    Rae, J. W. B. et al. CO2 storage and release in the deep Southern Ocean on millennial to centennial timescales. Nature 562, 569–573 (2018).

    Google Scholar 

  21. 21.

    Gutjahr, M. et al. Very larger release of mostly volcanic carbon during the Palaeocene–Eocene thermal maximum. Nature 548, 573–577 (2017).

    Google Scholar 

  22. 22.

    Henehan, M. et al. Rapid ocean acidification and protracted Earth system recovery followed the end-Cretaceous Chicxulub impact. Proc. Natl Acad. Sci. USA 116, 22500–22504 (2019).

    Google Scholar 

  23. 23.

    Müller, T. et al. Ocean acidification during the early Toarcian extinction event: Evidence from boron isotopes in brachiopods. Geology (2020).

  24. 24.

    Posenato, R. Survival patterns of microbenthic marine assemblages during the end-Permian mass extinction in the western Tethys (Dolomites, Italy). Palaeogeogr. Palaeoclimatol. Palaeoecol. 280, 150–167 (2019).

    Google Scholar 

  25. 25.

    Wallmann, K. et al. Periodic changes in the Cretaceous ocean and climate caused by marine redox see-saw. Nat. Geosci. 12, 456–462 (2019).

    Google Scholar 

  26. 26.

    Retallack, G. J. A 300-million-year record of atmospheric carbon dioxide from fossil plant cuticles. Nature 411, 287–290 (2001).

    Google Scholar 

  27. 27.

    Goddéris, Y. et al. Causal or casual link between the rise of nannoplankton calcification and a tectonically-driven massive decrease in Late Triassic atmospheric CO2? Earth Planet. Sci. Lett. 267, 247–255 (2008).

    Google Scholar 

  28. 28.

    McElwain, J. C., Wagner, P. J. & Hesselbo, S. P. Fossil plant relative abundances indicate sudden loss of Late Triassic biodiversity in East Greenland. Science 324, 1554–1556 (2009).

    Google Scholar 

  29. 29.

    Witkowski, C. R., Weijers, J. W. H., Blais, B., Schouten, S. & Damste, J. S. S. Molecular fossils from phytoplankton reveal secular \(p_{{\rm{CO}}_2}\) trend over the Phanerozoic. Sci. Adv. 4, eaat4556 (2018).

  30. 30.

    Joachimski, M. M. et al. Climate warming in the latest Permian and the Permian–Triassic mass extinction. Geology 40, 195–198 (2012).

    Google Scholar 

  31. 31.

    Schobben, M., Joachimski, M. M., Korn, D., Leda, L. & Korte, C. Palaeotethys seawater temperature rise and an intensified hydrological cycle following the end-Permian mass extinction. Gondwana Res. 26, 675–683 (2014).

    Google Scholar 

  32. 32.

    Algeo, T. J. et al. Plankton and productivity during the Permian–Triassic boundary crisis: an analysis of organic carbon fluxes. Glob. Planet. Change 105, 52–67 (2013).

    Google Scholar 

  33. 33.

    Saitoh, M. et al. Nitrogen isotope chemostratigraphy across the Permian–Triassic boundary at Chaotian, Sichuan, South China. J. Asian Earth Sci. 93, 113–128 (2014).

    Google Scholar 

  34. 34.

    Sun, Y. D. et al. Ammonium ocean following the end-Permian mass extinction. Earth Planet. Sci. Lett. 518, 211–222 (2019).

    Google Scholar 

  35. 35.

    Shen, J. et al. Marine productivity changes during the end-Permian crisis and Early Triassic recovery. Earth Sci. Rev. 149, 136–162 (2015).

    Google Scholar 

  36. 36.

    Canfield, D. E. Models of oxic respiration, denitrification and sulfate reduction in zones of coastal upwelling. Geochim. Cosmochim. Acta 70, 5753–5765 (2006).

    Google Scholar 

  37. 37.

    Anderson, R. F. et al. Deep-sea oxygen depletion and ocean carbon sequestration during the last ice age. Glob. Biogeochem. Cycles 33, 301–317 (2019).

    Google Scholar 

  38. 38.

    Zeebe, R. & Westbroek, P. A simple model for the CaCO3 saturation state of the ocean: The ‘Strangelove’, the ‘Neritan’, and the ‘Cretan’ Ocean. Geochem. Geophys. Geosyst. 4, 1104 (2003).

    Google Scholar 

  39. 39.

    Vollstaedt, H. et al. The Phanerozoic δ88/86Sr record of seawater: new constraints on past changes in oceanic carbonate fluxes. Geochim. Cosmochim. Acta 128, 249–265 (2014).

    Google Scholar 

  40. 40.

    Silva-Tamayo, J. C. et al. Global perturbation of the marine calcium cycle during the Permian–Triassic transition. Geol. Soc. Am. Bull. 130, 1323–1338 (2018).

    Google Scholar 

  41. 41.

    Woods, A. Assessing Early Triassic paleoceanographic conditions via unusual sedimentary fabrics and features. Earth Sci. Rev. 137, 6–18 (2014).

    Google Scholar 

  42. 42.

    Burgess, S. D., Muirhead, J. D. & Bowring, S. A. Initial pulse of Siberian Traps sills as the trigger of the end-Permian mass extinction. Nat. Commun. 8, 164 (2017).

    Google Scholar 

  43. 43.

    Song, H. J., Wignall, P. B., Tong, J. N. & Yin, H. F. Two pulses of extinction during the Permian–Triassic crisis. Nat. Geosci. 6, 52–56 (2013).

    Google Scholar 

  44. 44.

    Brayard, A. et al. Transient metazoan reefs in the aftermath of the end-Permian mass extinction. Nat. Geosci. 4, 693–697 (2011).

    Google Scholar 

  45. 45.

    Martindale, R. C., Foster, W. J. & Velledits, F. The survival, recovery, and diversification of Metazoan reef ecosystems following the end-Permian mass extinction event. Palaeogeogr. Palaeoclimatol. Palaeoecol. 513, 100–115 (2019).

    Google Scholar 

  46. 46.

    Reynard, S. et al. Interacting effects of CO2 partial pressure and temperature on photosynthesis and calcification in a scleractinian coral. Glob. Change Biol. 9, 1660–1668 (2003).

    Google Scholar 

  47. 47.

    Beatty, T. W., Zonneveld, J.-P. & Henderson, C. M. Anomalously diverse Early Triassic ichnofossil assemblages in northwest Pangea: a case for shallow-marine habitable zone. Geology 36, 771–774 (2008).

    Google Scholar 

  48. 48.

    Le Quéré, C. et al. Global carbon budget 2018. Earth Syst. Sci. Data 10, 2141–2194 (2018).

    Google Scholar 

  49. 49.

    Orr, J. C. et al. Anthropogenic ocean acidification over the twenty-first century and its impact on calcifying organisms. Nature 437, 681–686 (2005).

    Google Scholar 

  50. 50.

    Schmidtko, S., Stramma, L. & Visbeck, M. Decline in global oxygen content during the past five decades. Nature 542, 335–339 (2017).

    Google Scholar 

  51. 51.

    Posenato, R. Marine biotic events in the Lopingian succession and latest Permian extinction in the Southern Alps (Italy). Geol. J. 45, 195–215 (2010).

    Google Scholar 

  52. 52.

    Broglio Loriga, C., Neri, C., Pasini, M. & Posenato, R. in Permian and Permian–Triassic Boundary in the South-Alpine segment of the western Tethys, and Additional Reports (ed. Cassinis, G.) 5–44 (Societa Geologica Italiana, 1988).

  53. 53.

    Posenato, R. The athyridoids of the transitional beds between Bellerophon and Werfen formations (uppermost Permian, Southern Alps, Italy). Riv. Ital. Paleontol. Soc. 1071, 197–226 (2001).

    Google Scholar 

  54. 54.

    Kearsey, T., Twichett, R. J., Price, G. D. & Grimes, S. T. Isotope excursion and palaeotemperature estimates from the Permian/Triassic boundary in the Southern Alps (Italy). Palaeogeogr. Palaeoclimatol. Palaeoecol. 279, 29–40 (2009).

    Google Scholar 

  55. 55.

    Muttoni, G. et al. Opening of the neo-Tethys ocean and the Pangea B to Pangea A transformation during the Permian. GeoArabia 14, 17–48 (2009).

    Google Scholar 

  56. 56.

    Reichow, M. K. et al. The timing and extent of the eruption of the Siberian Traps large igneous province: implications for the end-Permian environmental crisis. Earth Planet. Sci. Lett. 277, 9–20 (2009).

    Google Scholar 

  57. 57.

    Brand, U., Logan, A., Hiller, N. & Richardson, J. Geochemistry of modern brachiopods: applications and implications for oceanography and paleoceanography. Chem. Geol. 198, 305–334 (2003).

    Google Scholar 

  58. 58.

    Rollion-Bard, C. et al. Assessing the biomineralisation processes in the shell layers of modern brachiopods from oxygen isotopic composition and elemental ratios: implications for their use as paleoenvironmental proxies. Chem. Geol. 524, 49–66 (2019).

    Google Scholar 

  59. 59.

    Jurikova, H. et al. Boron isotope systematics of cultured brachiopods: response to acidification, vital effects and implications for palaeo-pH reconstruction. Geochim. Cosmochim. Acta 248, 370–386 (2019).

    Google Scholar 

  60. 60.

    Jurikova, H. et al. Incorporation of minor and trace elements into cultured brachiopods: implications for proxy application with new insights from a biomineralisation model. Geochim. Cosmochim. Acta 286, 418–440 (2020).

    Google Scholar 

  61. 61.

    Jurikova, H. et al. Boron isotope composition of the cold-water coral Lophelia pertusa along the Norwegian margin: zooming into a potential pH-proxy by combining bulk and high-resolution approaches. Chem. Geol. 513, 143–152 (2019).

    Google Scholar 

  62. 62.

    Kasemann, S. A., Schmidt, D. N., Bijima, J. & Foster, G. L. In situ boron isotope analyses in marine carbonates and its application for foraminifera and palaeo-pH. Chem. Geol. 260, 138–147 (2009).

    Google Scholar 

  63. 63.

    Lemarchand, D., Gaillardet, J., Lewin, É. & Allègre, C. J. The influence of rivers on marine boron isotopes and implications for reconstructing past ocean pH. Nature 408, 951–954 (2000).

    Google Scholar 

  64. 64.

    Joachimski, M. M., Simon, L., van Geldern, R. & Lécuyer, C. Boron isotope geochemistry of Paleozoic brachiopod calcite: implications for a secular change in the boron isotope geochemistry of seawater over the Phanerozoic. Geochim. Cosmochim. Acta 69, 4035–4044 (2005).

    Google Scholar 

  65. 65.

    Klochko, K., Kaufman, A. J., Wengsheng, Y., Byrne, R. H. & Tossell, J. A. Experimental measurement of boron isotope fractionation in seawater. Earth Planet. Sci. Lett. 248, 276–285 (2006).

    Google Scholar 

  66. 66.

    Lécuyer, C., Grandjean, P., Reynard, B., Albarède, F. & Telouk, P. 11B/10B analysis of geological materials by ICP-MS Plasma 54: application to the boron fractionation between brachiopod calcite and seawater. Chem. Geol. 186, 45–55 (2002).

    Google Scholar 

  67. 67.

    Ridgwell, A. A mid Mesozoic revolution in the regulation of ocean chemistry. Mar. Chem. 217, 339–357 (2005).

    Google Scholar 

  68. 68.

    Penman, D. E., Hönisch, B., Rasbury, E. T., Hemming, N. G. & Spero, H. J. Boron, carbon, and oxygen isotopic composition of brachiopod shells: intra-shell variability, controls, and potential as a paleo-pH recorder. Chem. Geol. 340, 32–39 (2013).

    Google Scholar 

  69. 69.

    Garbelli, C., Angiolini, L., Brand, U. & Jadoul, F. Brachiopod fabric, classes and biogeochemistry: implications for the reconstruction and interpretation of seawater carbon-isotope curves and records. Chem. Geol. 371, 60–67 (2014).

    Google Scholar 

  70. 70.

    Khiel, J. T. & Shields, C. A. Climate simulations of the latest Permian: implications for mass extinction. Geology 33, 757–760 (2005).

    Google Scholar 

  71. 71.

    Lowenstein, T. K., Timofeeff, M. N., Brennan, S. T., Hardie, L. A. & Demicco, R. V. Oscillations in Phanerozoic seawater chemistry: evidence from fluid inclusions. Science 294, 1086–1088 (2001).

    Google Scholar 

  72. 72.

    Berner, R. A. & Kothavala, Z. GEOCARB III: A revised model of atmospheric CO2 over Phanerozoic time. Am. J. Sci. 301, 182–204 (2001).

    Google Scholar 

  73. 73.

    Royer, D. L., Donnadieu, Y., Park, J., Kowalczyk, J. & Godderis, Y. Error analysis of CO2 and O2 estimates from the long-term geochemical model GEOCARBSULF. Am. J. Sci. 314, 1259–1283 (2014).

    Google Scholar 

  74. 74.

    Wallmann, K., Schneider, B. & Sarnthein, M. Effects of eustatic sea-level change, ocean dynamics, and nutrient utilization on atmospheric \(p_{{\rm{CO}}_2}\) and seawater composition over the last 130,000 years. Clim. Past 12, 339–375 (2016).

    Google Scholar 

  75. 75.

    Berner, R. A. GEOCARB II: a revised model of atmospheric CO2 over Phanerozoic time. Am. J. Sci. 294, 56–91 (1994).

    Google Scholar 

Download references


This project has received funding from the European Union’s Horizon 2020 research and innovation programme under the Marie Sklodowska-Curie grant agreement no. 643084 (BASE-LiNE Earth). K.W. was supported by the HGF (ESM project) and S.F. by the DFG (SFB 754, subproject A7). L.A. and R.P. were supported by the MURST (PRIN 2017RX9XXXY, project ‘Biota resilience to global change: biomineralization of planktic and benthic calcifiers in the past, present and future’). We thank D. Nürnberg for help with the carbon and oxygen isotope analyses, and A. Kolevica and T. Goepfert for laboratory support (at the GEOMAR Helmholtz Centre for Ocean Research in Kiel). We are grateful to F. Couffignal and A. Rocholl for assistance with the SIMS analyses, U. Dittmann for sample preparation and I. Schäpan for scanning electron microscopy imaging (at the GFZ German Research Centre for Geosciences—Helmholtz Centre Potsdam). Special thanks to A. Winguth (at the University of Texas Arlington) for providing us the model output.

Author information




H.J., M.G., V.L. and A.E. developed the concept and designed the study. H.J. carried out the chemical sample preparation, as well as elemental and isotopic analyses. M.W. provided isotopic microanalyses. U.B., R.P., L.A. and C.G. provided and screened the samples. R.P., L.A., C.G. and H.J. developed the age model. K.W. and S.F. devised the box model and performed the analyses. H.J. wrote the manuscript, and all the authors discussed the results, contributed to the interpretation of the data and to the final manuscript.

Corresponding author

Correspondence to Hana Jurikova.

Ethics declarations

Competing interests

The authors declare no competing interests.

Additional information

Peer review information Primary Handling Editor: Rebecca Neely.

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

Extended data

Extended Data Fig. 1 Stable isotope and Element-to-Ca ratio cross-plots for PTB brachiopods.

Grey symbols show data from solution-based analyses of PTB brachiopods. Panel a additionally shows the Al/Ca and B/Ca composition of matrix (void cement) material (n = 3, ±2 s.d.) and modern brachiopods (n = 3, ±2 s.d.; based on measured values for Magellania venosa, Liothyrella neozelandica and Pajaudina atlantica) for comparison. Matrix is highly depleted in B/Ca, with variable Al/Ca. Recent brachiopods are highly variable in both B/Ca and Al/Ca. Elemental ranges (Sr, Mn, Mg and Fe) for modern brachiopods shown in panels g and h are based on data from ref. 57.

Extended Data Fig. 2 Criteria-based boron isotope record shown relative to carbon isotope excursion (CIE; in kyr).

a Boron isotope trends when solely based on samples with low Al/Ca ratios (Al/Ca <1000 μmol/mol); b boron isotope trends when solely based on one brachiopod class (Rhynchonellata) from one site (Southern Alps, northern Italy).

Extended Data Fig. 3 Boron isotope and pH record shown relative to carbon isotope excursion (CIE; in kyr).

Red dashed rectangle in panels b and d indicates the enlarged areas shown in a and c, respectively. Boron-derived pH values (c, d) are provided for each data point together with best fit model curve. Our preferred standard case scenario (in grey) is shown along with an alternative borate ion scenario (in blue) for comparison. Error bars for solution-based δ11B values indicate the analytical uncertainty (2 s.d. = 0.2 ‰) and for SIMS δ11B the s.d. between multiple ion spots measurements within a single sample (panels a, b). Error bars for pH are based on the given δ11B envelope.

Extended Data Fig. 4 Isotopic and model-based constraints on carbon cycle dynamics across the PTB.

a Carbon isotope composition of carbonates deposited on Tethys shelf; and b carbon isotope composition of organic carbon in sediments deposited on Panthalassa seafloor based on a comprehensive compilation of literature data (sources are provided in the Supplement) and as modelled; c δ11B-based and modelled surface ocean pH (standard case scenario); d resulting global atmospheric partial pressure CO2 projected by our carbon cycle model.

Extended Data Fig. 5 Our box model setup.

The global ocean is represented by 6 boxes: surface water (0–100 m water depth), intermediate water (100–1,300 m), and deep water (>1,300) for both, Tethys and Panthalassa oceans. Water fluxes across the box boundaries are given in Sv.

Supplementary information

Supplementary Information

Supplementary discussion consisting of five sections (1–5) and integrated figures.

Supplementary Data

Containing geochemical data analysed during this study.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Jurikova, H., Gutjahr, M., Wallmann, K. et al. Permian–Triassic mass extinction pulses driven by major marine carbon cycle perturbations. Nat. Geosci. 13, 745–750 (2020).

Download citation

Further reading


Quick links