The end-Permian mass extinction (EPME) represents the largest biocrisis in Earth’s history, a result of environmental perturbations following volatiles released during Siberian Traps magmatism. A leading hypothesis links the marine mass extinction to the expansion of oceanic anoxia, although uncertainties exist as to the timing and extent. Thallium isotopes, a novel palaeoredox proxy with a rapid global response due to its short residence time in seawater, track global rates of manganese oxide burial, one of the first redox half-reactions to occur under reduced oxygen conditions. For this study, we analysed thallium isotopes from three widely distributed sites in Panthalassa, the largest ocean basin at the time. Our results provide evidence for the onset of deoxygenation considerably before the EPME, earlier by ≥1 Myr than the onset implied by other proxy records. Notably, there is a transient negative thallium isotope excursion concurrent with the EPME, which requires substantial manganese oxide burial based on the thallium isotope mass balance. This feature suggests a brief oxygenation episode before a return to more anoxic conditions, implying a more complex redox scenario, with rapid changes in oceanic (de)oxygenation leading to spatially and temporally variable biotic stresses. This oxygenation event may have been related to a transient cooling episode, based on published oxygen isotope records. These findings show that the Earth system experienced a highly fluctuating response to forcings linked to volcanogenic volatiles during the EPME.
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The datasets generated during the current study are available as supplementary files alongside the published manuscript. They are available through the Pangaea online data repository at https://doi.pangaea.de/10.1594/PANGAEA.933389.
Raup, D. M. Size of the Permo-Triassic bottleneck and its evolutionary implications. Science 206, 217–218 (1979).
Sepkoski, J. J.Jr Ten years in the library: new data confirm paleontological patterns. Paleobiology 19, 43–51 (1993).
Fan, J. et al. A high-resolution summary of Cambrian to early Triassic marine invertebrate biodiversity. Science 367, 272–277 (2020).
Erwin, D. H. The Permo–Triassic extinction. Nature 367, 231–236 (1994).
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).
Bond, D. P. G. & Grasby, S. E. On the causes of mass extinctions. Palaeogeogr. Palaeoclimatol. Palaeoecol. 478, 3–29 (2017).
Broadley, M. W., Barry, P. H., Ballentine, C. J., Taylor, L. A. & Burgess, R. End-Permian extinction amplified by plume-induced release of recycled lithospheric volatiles. Nat. Geosci. 11, 682–687 (2018).
Benton, M. J. Hyperthermal-driven mass extinctions: killing models during the Permian–Triassic mass extinction. Philos. Trans. R. Soc. A 376, 20170076 (2018).
Black, B. A. et al. Systemic swings in end-Permian climate from Siberian Traps carbon and sulfur outgassing. Nat. Geosci. 11, 949–954 (2018).
Shen, S.-Z. et al. End-Permian mass extinction and palaeoenvironmental changes in Neotethys: evidence from an oceanic carbonate section in southwestern Tibet. Glob. Planet. Change 73, 3–14 (2010).
Sun, Y. et al. Lethally hot temperatures during the Early Triassic greenhouse. Science 338, 366–370 (2012).
Chen, J. et al. High-resolution SIMS oxygen isotope analysis on conodont apatite from South China and implications for the end-Permian mass extinction. Palaeogeogr. Palaeoclimatol. Palaeoecol. 448, 26–38 (2016).
Joachimski, M. M., Alekseev, A. S., Grigoryan, A. & Gatovsky, Y. A. Siberian Trap volcanism, global warming and the Permian-Triassic mass extinction: new insights from Armenian Permian-Triassic sections. Geol. Soc. Am. Bull. 132, 427–443 (2020).
Hinojosa, J. L. et al. Evidence for end-Permian ocean acidification from calcium isotopes in biogenic apatite. Geology 40, 743–746 (2012).
Grasby, S. E. et al. Progressive environmental deterioration in northwestern Pangea leading to the latest Permian extinction. Geol. Soc. Am. Bull. 127, 1331–1347 (2015).
Sephton, M. A., Jiao, D., Engel, M. H., Looy, C. V. & Visscher, H. Terrestrial acidification during the end-Permian biosphere crisis? Geology 43, 159–162 (2015).
Bond, D. P. G. & Wignall, P. B. Pyrite framboid study of marine Permian–Triassic boundary sections: a complex anoxic event and its relationship to contemporaneous mass extinction. Geol. Soc. Am. Bull. 122, 1265–1279 (2010).
Algeo, T. J. et al. Spatial variation in sediment fluxes, redox conditions, and productivity in the Permian–Triassic Panthalassic Ocean. Palaeogeogr. Palaeoclimatol. Palaeoecol. 308, 65–83 (2011).
Schoepfer, S. D. et al. Termination of a continent-margin upwelling system at the Permian–Triassic boundary (Opal Creek, Alberta, Canada). Glob. Planet. Change 105, 21–35 (2013).
Mettam, C. et al. High-frequency fluctuations in redox conditions during the latest Permian mass extinction. Palaeogeogr. Palaeoclimatol. Palaeoecol. 485, 210–223 (2017).
Zhang, 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).
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).
Grice, K. et al. Photic zone euxinia during the Permian–Triassic superanoxic event. Science 307, 706–709 (2005).
Song, H. et al. Early Triassic seawater sulfate drawdown. Geochim. Cosmochim. Acta 128, 95–113 (2014).
Grasby, S. E., Beauchamp, B., Bond, D. P. G., Wignall, P. B. & Sanei, H. Mercury anomalies associated with three extinction events (Capitanian Crisis, Latest Permian Extinction and the Smithian/Spathian Extinction) in NW Pangea. Geol. Mag. 153, 285–297 (2016).
Visscher, H. et al. Environmental mutagenesis during the end-Permian ecological crisis. Proc. Natl Acad. Sci. USA 101, 12952–12956 (2004).
Algeo, T. J. & Twitchett, R. J. Anomalous Early Triassic sediment fluxes due to elevated weathering rates and their biological consequences. Geology 38, 1023–1026 (2010).
Algeo, T. J., Chen, Z. Q., Fraiser, M. L. & Twitchett, R. J. Terrestrial–marine teleconnections in the collapse and rebuilding of Early Triassic marine ecosystems. Palaeogeogr. Palaeoclimatol. Palaeoecol. 308, 1–11 (2011).
Lau, K. V., Romaniello, S. J. & Zhang, F. in Elements in Geochemical Tracers in Earth System Science https://doi.org/10.1017/9781108584142 (Cambridge Univ. Press, 2019).
Kendall, B., Dahl, T. W. & Anbar, A. D. The stable isotope geochemistry of molybdenum. Rev. Mineral. Geochem. 82, 683–732 (2017).
Owens, J. D., Nielsen, S. G., Horner, T. J., Ostrander, C. M. & Peterson, L. C. Thallium-isotopic compositions of euxinic sediments as a proxy for global manganese-oxide burial. Geochim. Cosmochim. Acta 213, 291–307 (2017).
Owens, J. D. in Elements in Geochemical Tracers in Earth System Science https://doi.org/10.1017/9781108688697 (Cambridge Univ. Press, 2019).
Ostrander, C. M., Owens, J. D. & Nielsen, S. G. Constraining the rate of oceanic deoxygenation leading up to a Cretaceous Oceanic Anoxic Event (OAE-2: ∼94 Ma). Sci. Adv. 3, e1701020 (2017).
Them, T. R. et al. Thallium isotopes reveal protracted anoxia during the Toarcian (Early Jurassic) associated with volcanism, carbon burial, and mass extinction. Proc. Natl Acad. Sci. USA 115, 6596–6601 (2018).
Bowman, C. N. et al. Linking the progressive expansion of reducing conditions to a stepwise mass extinction event in the late Silurian oceans. Geology 47, 968–972 (2019).
Rue, E. L., Smith, G. J., Cutter, G. A. & Bruland, K. W. The response of trace-element redox couples to suboxic conditions in the water column. Deep Sea Res. I 44, 113–134 (1997).
Nielsen, S. G., Rehkämper, M. & Prytulak, J. Investigation and application of thallium isotope fractionation. Rev. Mineral. Geochem. 82, 759–798 (2017).
Fan, H. et al. Constraining oceanic oxygenation during the Shuram excursion in South China using thallium isotopes. Geobiology 18, 348–365 (2020).
Kaiho, K. et al. Changes in depth-transect redox conditions spanning the end-Permian mass extinction and their impact on the marine extinction: evidence from biomarkers and sulfur isotopes. Glob. Planet. Change 94–95, 20–32 (2012).
Schoepfer, S. D., Henderson, C. M., Garrison, G. H. & Ward, P. D. Cessation of a productive coastal upwelling system in the Panthalassic Ocean at the Permian–Triassic Boundary. Palaeogeogr. Palaeoclimatol. Palaeoecol. 313–314, 181–188 (2012).
Nielsen, S. G., Rehkämper, M., Baker, J. & Halliday, A. N. The precise and accurate determination of thallium isotope compositions and concentrations for water samples by MC-ICPMS. Chem. Geol. 204, 109–124 (2004).
Rehkämper, M. et al. Thallium isotope variations in seawater and hydrogenetic, diagenetic, and hydrothermal ferromanganese deposits. Earth Planet. Sci. Lett. 197, 65–81 (2002).
Kiessling, W. et al. Pre-mass extinction decline of latest Permian ammonoids. Geology 46, 283–286 (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).
Shen, S.-Z. et al. A sudden end-Permian mass extinction in South China. Geol. Soc. Am. Bull. 131, 205–223 (2019).
Haq, B. U. & Schutter, S. R. A chronology of Paleozoic sea-level changes. Science 322, 64–68 (2008).
Clarkson, M. O. et al. A new high-resolution δ13C record for the Early Triassic: insights from the Arabian Platform. Gondwana Res. 24, 233–242 (2013).
Korte, C. & Kozur, H. W. Carbon-isotope stratigraphy across the Permian–Triassic boundary: a review. J. Asian Earth Sci. 39, 215–235 (2010).
Fenchel, T. & Finlay, B. J. Oxygen toxicity, respiration and behavioural responses to oxygen in free-living anaerobic ciliates. J. Gen. Microbiol. 136, 1953–1959 (1990).
Blakey, R. C. Triassic global paleogeographic map. Global Paleogeography and Tectonics in Deep Time Series (Deep Time Maps Inc., 2016); https://deeptimemaps.com/global-paleogeography-and-tectonics-in-deep-time/
Nielsen, S. G. et al. Thallium isotope composition of the upper continental crust and rivers—an investigation of the continental sources of dissolved marine thallium. Geochim. Cosmochim. Acta 69, 2007–2019 (2005).
Baker, R. G. A., Rehkämper, M., Hinkley, T. K., Nielsen, S. G. & Toutain, J. P. Investigation of thallium fluxes from subaerial volcanism—implications for the present and past mass balance of thallium in the oceans. Geochim. Cosmochim. Acta 73, 6340–6359 (2009).
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).
We thank C. Bowman, N. Kozik and A. Karl for assistance in sample processing and data collection. The FSU EOAS Winchester Fund helped fund work done by S.M.N. Grants to J.D.O. through the NASA Exobiology program (NNX16AJ60G and 80NSSC18K1532) and the Sloan Research Foundation (FG-2020–13552) funded this work. This work was performed at the National High Magnetic Field Laboratory in Tallahassee, Florida, which is supported by National Science Foundation Cooperative Agreement No. DMR-1644779 and by the State of Florida.
The authors declare no competing interests.
Peer review information Nature Geoscience thanks Matthew Clarkson and the other, anonymous, reviewer(s) for their contribution to the peer review of this work.
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Biostratigraphy, lithostratigraphy, and chemostratigraphy for Opal Creek (a), Gujo-Hachiman (b), and Ubara (c). Chemostratigraphy includes carbon isotopes (black line), manganese concentrations (red line), vanadium concentrations (purple line), molybdenum concentrations (green line), and thallium isotopes (blue line). Biostratigraphy, lithostratigraphy, and trace metal concentrations are from previous sources18,19,39,40, as well as carbon isotopes of Opal Creek40. For Opal Creek, biozones 1–4 represent Mesogondolella bitteri and M. rosenckrantzi (1), M. sheni (2), Clarkina hauschkei and C. meishanensis (3), and Hindeodus parvus (4). Lithostratigraphic columns are present on the left adjacent to height. Separate patterns are used to distinguish lithologies, including chert (rounded bricks), shale (dashed lines), and silty mudstones (dashed and dotted lines), with approximate colour of the rocks. All three trace metal concentration charts have upper continental crust concentrations marked with a dashed vertical line, with arrow pointing towards more reducing conditions. The Tl isotope plots have a dashed vertical line indicating modern seawater values, with more positive values representing greater extent of anoxia. All three sites are correlated with the EPME (red dashed line) and PTB (light blue dashed line) using both biostratigraphy and carbon isotope stratigraphy. Thallium plotted with error bars (2σ). Opal Creek features an Upper Permian19,40 unconformity near the base of the described section (wavy line), below the EPME. Opal Creek here features a more extensive section up to 43m as compared to Fig. 2. Trace metal concentrations generally indicate reducing conditions at all three sections, though each trace metal responds in a different manner for each locality due to fluctuating local redox18,19. Global similarity in thallium isotopes despite this indicates little local explanation for the excursion.
Model showing how changes in Mn oxide burial can cause the negative isotope excursion exhibited during the EPME. Parameters can be found in Extended Data Table 1. The approximate duration of the oxygenation interval (~60 kyr;18 see Supplementary Discussion) is highlighted in blue, while the approximate duration of the extinction interval (~60 kyr53) is highlighted in red, with these slightly overlapping based on average position of the negative thallium isotope excursion compared to the negative carbon isotope excursion (see Fig. 4). Various runs were conducted under the premise of decreasing Mn oxide burial between 0.20 and 1.50 Myr, representing the upper Changhsingian data found in the lower part of the Gujo-Hachiman section. As there is relatively small change at a steady rate across this interval, a gap between 0.4 and 1.4 Myr was applied for convenience of space, though this trend continues at a constant rate across this interval (represented as a dashed line in the gap). Following this, a short-term major increase in Mn oxide burial is recreated. The duration and flux of Mn oxide burial is modulated so that the minimum value of the excursion is consistent, all values near ε205Tl = ~6.0, with included table within the figure to distinguish the different runs and how the duration of the excursion compares. This can be compared to a scenario with no major isotope excursion (thick black line).
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Newby, S.M., Owens, J.D., Schoepfer, S.D. et al. Transient ocean oxygenation at end-Permian mass extinction onset shown by thallium isotopes. Nat. Geosci. 14, 678–683 (2021). https://doi.org/10.1038/s41561-021-00802-4