The role of oxygen as a driver for early animal evolution is widely debated. During the Cambrian explosion, episodic radiations of major animal phyla occurred coincident with repeated carbon isotope fluctuations. However, the driver of these isotope fluctuations and potential links to environmental oxygenation are unclear. Here we report high-resolution carbon and sulfur isotope data for marine carbonates from the southeastern Siberian Platform that document the canonical explosive phase of the Cambrian radiation from ~524 to ~514 Myr ago. These analyses demonstrate a strong positive covariation between carbonate δ13C and carbonate-associated sulfate δ34S through five isotope cycles. Biogeochemical modelling suggests that this isotopic coupling reflects periodic oscillations in the atmospheric O2 and the extent of shallow-ocean oxygenation. Episodic maxima in the biodiversity of animal phyla directly coincided with these extreme oxygen perturbations. Conversely, the subsequent Botoman–Toyonian animal extinction events (~514 to ~512 Myr ago) coincided with decoupled isotope records that suggest a shrinking marine sulfate reservoir and expanded shallow marine anoxia. We suggest that fluctuations in oxygen availability in the shallow marine realm exerted a primary control on the timing and tempo of biodiversity radiations at a crucial phase in the early history of animal life.

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The authors declare that data supporting the findings of this study are available within the article and Supplementary Tables 15.

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  1. 1.

    Erwin, D. H. et al. The Cambrian conundrum: early divergence and later ecological success in the early history of animals. Science 334, 1091–1097 (2011).

  2. 2.

    Zhuravlev, A. Yu & Naimark, E. B. Alpha, beta, or gamma: numerical view on the Early Cambrian world. Palaeogeogr. Palaeoclimatol. Palaeoecol. 220, 207–225 (2005).

  3. 3.

    Na, L. & Kiessling, W. Diversity partitioning during the Cambrian radiation. Proc. Natl Acad. Sci. USA 112, 4702–4706 (2015).

  4. 4.

    Boyle, R. A. et al. Stabilization of the coupled oxygen and phosphorus cycles by the evolution of bioturbation. Nat. Geosci. 7, 671–676 (2014).

  5. 5.

    Lenton, T. M., Boyle, R. A., Poulton, S. W., Shields-Zhou, G. A. & Butterfield, N. J. Co-evolution of eukaryotes and ocean oxygenation in the Neoproterozoic era. Nat. Geosci. 7, 257–265 (2014).

  6. 6.

    Chen, X. et al. Rise to modern levels of ocean oxygenation coincided with the Cambrian radiation of animals. Nat. Commun. 6, 7142 (2015).

  7. 7.

    Mills, D. B. et al. Oxygen requirements of the earliest animals. Proc. Natl Acad. Sci. USA 111, 4168–4172 (2014).

  8. 8.

    Zhang, S. et al. Sufficient oxygen for animal respiration 1,400 million years ago. Proc. Natl Acad. Sci. USA 113, 1731–1736 (2016).

  9. 9.

    Sperling, E. A. et al. Oxygen, ecology, and the Cambrian radiation of animals. Proc. Natl Acad. Sci. USA 110, 13446–13451 (2013).

  10. 10.

    Levin, L. A., Gage, J. D., Martin, C. & Lamont, P. A. Macrobenthic community structure within and beneath the oxygen minimum zone, NW Arabian Sea. Deep Sea Res. Part II 47, 189–226 (2000).

  11. 11.

    Zhu, M.-Y., Babcock, L. E. & Peng, S.-C. Advances in Cambrian stratigraphy and paleontology: Integrating correlation techniques, paleobiology, taphonomy and paleoenvironmental reconstruction. Palaeoworld 15, 217–222 (2006).

  12. 12.

    Berner, R. A. GEOCARBSULF: a combined model for Phanerozoic atmospheric O2 and CO2. Geochim. Cosmochim. Acta 70, 5653–5664 (2006).

  13. 13.

    Kump, L. R. & Garrels, R. M. Modeling atmospheric O2 in the global sedimentary redox cycle. Am. J. Sci. 286, 337–360 (1986).

  14. 14.

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

  15. 15.

    Brasier, M. D., Corfield, R. M., Derry, L. A., Rozanov, A. Yu. & Zhuravlev, A. Yu. Multiple δ13C excursions spanning the Cambrian explosion to the Botomian crisis in Siberia. Geology 22, 455–458 (1994).

  16. 16.

    Dahl, T. W. et al. Reorganisation of Earth’s biogeochemical cycles briefly oxygenated the oceans 520 Myr ago. Geochem. Perspect. Lett. 3, 210–220 (2017).

  17. 17.

    Maloof, A. C. et al. The earliest Cambrian record of animals and ocean geochemical change. Geol. Soc. Am. Bull. 122, 1731–1774 (2010).

  18. 18.

    Peng, S., Babcock, L. E. & Cooper, R. A. in The Geologic Time Scale 2012 (eds Gradstein, F. M., Ogg, J. G., Schmitz, M. D. & Ogg, G. M.) 437–488 (Elsevier Science Limited, 2012)..

  19. 19.

    Tostevin, R. et al. Constraints on the late Ediacaran sulfur cycle from carbonate associated sulfate. Precambrian Res. 290, 113–125 (2017).

  20. 20.

    Cui, H. et al. Redox-dependent distribution of early macro-organisms: evidence from the terminal Ediacaran Khatyspyt formation in Arctic Siberia. Palaeogeogr. Palaeoclimatol. Palaeoecol. 461, 122–139 (2016).

  21. 21.

    Zhuravlev, A. Yu. & Wood, R. A. Anoxia as the cause of the mid-Early Cambrian (Botomian) extinction event. Geology 24, 311–314 (1996).

  22. 22.

    Bambach, R. K. Phanerozoic biodiversity mass extinctions. Annu. Rev. Earth Planet. Sci. 34, 127–155 (2006).

  23. 23.

    Gill, B. C., Lyons, T. W. & Saltzman, M. R. Parallel, high-resolution carbon and sulfur isotope records of the evolving Paleozoic marine sulfur reservoir. Palaeogeogr. Palaeoclimatol. Palaeoecol. 256, 156–173 (2007).

  24. 24.

    Veizer, J., Holser, W. T. & Wilgus, C. K. Correlation of 13C/12C and 34S/32S secular variations. Geochim. Cosmochim. Acta 44, 579–587 (1980).

  25. 25.

    Algeo, T. J., Luo, G. M., Song, H. Y., Lyons, T. W. & Canfield, D. E. Reconstruction of secular variation in seawater sulfate concentrations. Biogeosciences 12, 2131–2151 (2015).

  26. 26.

    Kah, L. C., Lyons, T. W. & Frank, T. D. Low marine sulphate and protracted oxygenation of the Proterozoic biosphere. Nature 431, 834–838 (2004).

  27. 27.

    Brennan, S. T., Lowenstein, T. K. & Horita, J. Seawater chemistry and the advent of biocalcification. Geology 32, 473–476 (2004).

  28. 28.

    Berner, R. A. Sedimentary pyrite formation: an update. Geochim. Cosmochim. Acta 48, 605–615 (1984).

  29. 29.

    Gill, B. C. et al. Geochemical evidence for widespread euxinia in the Later Cambrian ocean. Nature 469, 80–83 (2011).

  30. 30.

    Garrels, R. M. & Lerman, A. Coupling of the sedimentary sulfur and carbon cycles; an improved model. Am. J. Sci. 284, 989–1007 (1984).

  31. 31.

    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).

  32. 32.

    Algeo, T. J. & Ingall, E. Sedimentary Corg:P ratios, paleocean ventilation, and Phanerozoic atmospheric pO2. Palaeogeogr. Palaeoclimatol. Palaeoecol. 256, 130–155 (2007).

  33. 33.

    Handoh, I. C. & Lenton, T. M. Periodic mid-Cretaceous oceanic anoxic events linked by oscillations of the phosphorus and oxygen biogeochemical cycles. Global Biogeochem. Cycles 17, 1–11 (2003).

  34. 34.

    Boulila, S. et al. On the origin of Cenozoic and Mesozoic ‘third-order’ eustatic sequences. Earth Sci. Rev 109, 94–112 (2011).

  35. 35.

    Haq, B. U. & Schutter, S. R. A chronology of Paleozoic sea-level changes. Science. 322, 64–68 (2008).

  36. 36.

    Zhuravlev, A. Yu. Outlines of the Siberian platform sequence stratigraphy in the Lower and lower Middle Cambrian (Lena–Aldan area). Rev. Esp. Paleontol. Suppl., 105–114 (1998)..

  37. 37.

    Shields, G. A. & Mills, B. J. W. Tectonic controls on the long-term carbon isotope mass balance. Proc. Natl Acad. Sci. USA 114, 4318–4323 (2017).

  38. 38.

    Derry, L. A., Brasier, M. D., Corfield, R. M., Rozanov, A. Yu. & Zhuravlev, A. Yu. Sr and C isotopes in Lower Cambrian carbonates from the Siberian craton: a paleoenvironmental record during the ‘Cambrian explosion’. Earth Planet. Sci. Lett. 128, 671–681 (1994).

  39. 39.

    Feng, L., Li, C., Huang, J., Chang, H. & Chu, X. A sulfate control on marine mid-depth euxinia on the early Cambrian (ca. 529–521 Ma) Yangtze platform, South China. Precambrian Res. 246, 123–133 (2014).

  40. 40.

    Guilbaud, R. et al. Oxygen minimum zones in the early Cambrian ocean. Geochem. Perspect. Lett. 6, 33–38 (2018).

  41. 41.

    Butterfield, N. J. Oxygen, animals and aquatic bioturbation: an updated account. Geobiology 16, 3–16 (2018).

  42. 42.

    Jablonski, D., Sepkoski, J. J., Bottjer, D. J. & Sheehan, P. M. Onshore-offshore patterns in the evolution of Phanerozoic shelf communities. Science 222, 1123–1125 (1983).

  43. 43.

    Zhuravlev, A. Yu. & Wood, R. A. The two phases of the Cambrian explosion. Sci. Rep. 8, 16656 (2018).

  44. 44.

    Kiessling, W., Simpson, C. & Foote, M. Reefs as cradles of evolution and sources of biodiversity in the Phanerozoic. Science. 327, 196–198 (2010).

  45. 45.

    Bicknell, R. D. C. & Paterson, J. R. Reappraising the early evidence of durophagy and drilling predation in the fossil record: implications for escalation and the Cambrian explosion. Biol. Rev. 93, 754–784 (2018).

  46. 46.

    Wang, D. et al. Coupling of ocean redox and animal evolution during the Ediacaran–Cambrian transition. Nat. Commun. 9, 2575 (2018).

  47. 47.

    Jin, C. et al. A highly redox-heterogeneous ocean in South China during the early Cambrian (529–514 Ma): implications for biota–environment co-evolution. Earth Planet. Sci. Lett. 441, 38–51 (2016).

  48. 48.

    Zhang, J. et al. Heterogenous oceanic redox conditions through the Ediacaran–Cambrian boundary limited the metazoan zonation. Sci. Rep. 7, 8550 (2017).

  49. 49.

    Zhang, L. et al. The link between Metazoan diversity and paleo-oxygenation in the early Cambrian: an integrated palaeontological and geochemical record from the eastern Three Gorges Region of South China. Palaeogeogr. Palaeoclimatol. Palaeoecol. 495, 24–41 (2018).

  50. 50.

    Wei, G.-Y. et al. Marine redox fluctuation as a potential trigger for the Cambrian explosion. Geology 46, 587–590 (2018).

  51. 51.

    Kovalevych, V., Marshall, T., Peryt, T., Petrychenko, O. & Zhukova, S. Chemical composition of seawater in Neoproterozoic: results of fluid inclusion study of halite from Salt Range (Pakistan) and Amadeus Basin (Australia). Precambrian Res. 144, 39–51 (2006).

  52. 52.

    Astashkin, V. A. et al. The Cambrian System on the Siberian Platform. Correlation Chart and Explanatory Notes. Publication No. 27 (International Union of Geological Sciences, 1991)..

  53. 53.

    Parfenova, T. M., Korovnikov, I. V., Eder, V. G. & Melenevskii, V. N. Organic geochemistry of the Lower Cambrian Sinyaya formation (northern slope of the Aldan anteclise). Russ. Geol. Geophys. 58, 586–599 (2017).

  54. 54.

    Tostevin, R. et al. Low-oxygen waters limited habitable space for early animals. Nat. Commun. 7, 12818 (2016).

  55. 55.

    Payne, J. L. et al. The evolutionary consequences of oxygenic photosynthesis: a body size perspective. Photosynth. Res. 107, 37–57 (2011).

  56. 56.

    Edwards, C. T., Saltzman, M. R., Royer, D. L. & Fike, D. A. Oxygenation as a driver of the Great Ordovician Biodiversification Event. Nat. Geosci. 10, 925–929 (2017).

  57. 57.

    Krause, A. J. et al. Stepwise oxygenation of the Paleozoic atmosphere. Nat. Commun. 9, 4081 (2018).

  58. 58.

    Wotte, T., Shields-Zhou, G. A. & Strauss, H. Carbonate-associated sulfate: experimental comparisons of common extraction methods and recommendations toward a standard analytical protocol. Chem. Geol. 326–327, 132–144 (2012).

  59. 59.

    Wynn, P. M., Fairchild, I. J., Baker, A., Baldini, J. U. L. & McDermott, F. Isotopic archives of sulphate in speleothems. Geochim. Cosmochim. Acta 72, 2465–2477 (2008).

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This work was supported by the National Natural Science Foundation of China (41661134048) and Strategic Priority Research Program (B) of the Chinese Academy of Sciences (XDB18000000 and XDB26000000) to M.Z. and A.Y. NERC (NE/1005978/1 and NE/P013643/1) to G.A.S., University of Leeds Academic Fellowship to B.J.W.M., ERC Consolidator grant 682760 (CONTROLPASTCO2) to P.A.E.PvS. and NERC (NE/N018559/1) to S.W.P. T.H. was supported by University College London Overseas Research Scholarship, China Scholarship Council and the National Natural Science Foundation of China (41888101). We acknowledge G. Tarbuck and D. Hughes for assistance in the geochemical analysis. We thank T. W. Dahl, B. S. Wade, R. Newton, C. Yang and L. Yao for valuable discussions. We thank T. Algeo, B. Gill and M. Gomes for constructive comments.

Author information


  1. London Geochemistry and Isotope Centre (LOGIC), Institute of Earth and Planetary Sciences, University College London and Birkbeck, University of London, London, UK

    • Tianchen He
    • , Philip A. E. Pogge von Strandmann
    •  & Graham A. Shields
  2. School of Earth and Environment, University of Leeds, Leeds, UK

    • Tianchen He
    • , Benjamin J. W. Mills
    •  & Simon W. Poulton
  3. State Key Laboratory of Palaeobiology and Stratigraphy & Center for Excellence in Life and Paleoenvironment, Nanjing Institute of Geology and Palaeontology, Chinese Academy of Sciences, Nanjing, China

    • Maoyan Zhu
  4. College of Earth Sciences, University of Chinese Academy of Sciences, Beijing, China

    • Maoyan Zhu
  5. Lancaster Environment Centre, Lancaster University, Lancaster, UK

    • Peter M. Wynn
  6. Department of Biological Evolution, Faculty of Biology, Lomonosov Moscow State University, Moscow, Russia

    • Andrey Yu. Zhuravlev
  7. Department of Earth Sciences, University of Oxford, Oxford, UK

    • Rosalie Tostevin
  8. State Key Laboratory for Mineral Deposits Research, School of Earth Sciences and Engineering, Nanjing University, Nanjing, China

    • Aihua Yang


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T.H., M.Z. and G.A.S. conceived the project. G.A.S., P.A.E.PvS., B.J.W.M. and M.Z. supervised the project. M.Z., A.Y. and A.Yu.Z. collected the samples. T.H. and P.M.W. analysed the samples. A.Yu.Z. provided the fossil data. B.J.W.M. and T.H. created the models. All the authors contributed to the data interpretation and the writing of the manuscript.

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The authors declare no competing interests.

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Correspondence to Tianchen He or Maoyan Zhu or Graham A. Shields.

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