Ocean oxygenation in the wake of the Marinoan glaciation


Metazoans are likely to have their roots in the Cryogenian period1,2,3, but there is a marked increase in the appearance of novel animal and algae fossils shortly after the termination of the late Cryogenian (Marinoan) glaciation about 635 million years ago4,5,6. It has been suggested that an oxygenation event in the wake of the severe Marinoan glaciation was the driving factor behind this early diversification of metazoans and the shift in ecosystem complexity7,8. But there is little evidence for an increase in oceanic or atmospheric oxygen following the Marinoan glaciation, or for a direct link between early animal evolution and redox conditions in general9. Models linking trends in early biological evolution to shifts in Earth system processes thus remain controversial10. Here we report geochemical data from early Ediacaran organic-rich black shales (635–630 million years old) of the basal Doushantuo Formation in South China. High enrichments of molybdenum and vanadium and low pyrite sulphur isotope values (Δ34S values ≥65 per mil) in these shales record expansion of the oceanic inventory of redox-sensitive metals and the growth of the marine sulphate reservoir in response to a widely oxygenated ocean. The data provide evidence for an early Ediacaran oxygenation event, which pre-dates the previous estimates for post-Marinoan oxygenation11,12,13 by more than 50 million years. Our findings seem to support a link between the most severe glaciations in Earth’s history, the oxygenation of the Earth’s surface environments, and the earliest diversification of animals.

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Figure 1: Locality maps and stratigraphy.
Figure 2: Trace-metal abundances (Mo, Mo/TOC, V, V/TOC, U, U/TOC) and pyrite sulphur isotopes (δ 34 S pyrite ) from the lower Doushantuo Formation black shales.
Figure 3: Summary of redox-sensitive trace elements and evolution of the ocean–atmosphere redox state.


  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

    Love, G. D. et al. Fossil steroids record the appearance of Demospongiae during the Cryogenian period. Nature 457, 718–721 (2009)

  3. 3

    Maloof, A. C. et al. Possible animal-body fossils in pre-Marinoan limestones from South Australia. Nature Geosci. 3, 653–659 (2010)

  4. 4

    Yin, L. et al. Doushantuo embryos preserved inside diapause egg cysts. Nature 446, 661–663 (2007)

  5. 5

    McFadden, K. A. et al. Pulsed oxidation and biological evolution in the Ediacaran Doushantuo Formation. Proc. Natl Acad. Sci. USA 105, 3197–3202 (2008)

  6. 6

    Yuan, X. et al. An early Ediacaran assemblage of macroscopic and morphologically differentiated eukaryotes. Nature 470, 390–393 (2011)

  7. 7

    Hoffman, P. F. & Schrag, D. P. The snowball Earth hypothesis: testing the limits of global change. Terra Nova 14, 129–155 (2002)

  8. 8

    Planavsky, N. J. et al. The evolution of the marine phosphate reservoir. Nature 467, 1088–1090 (2010)

  9. 9

    Och, L. M. & Shields-Zhou, G. A. The Neoproterozoic oxygenation event: environmental perturbations and biogeochemical cycling. Earth Sci. Rev. 110, 26–57 (2012)

  10. 10

    Butterfield, N. J. Oxygen, animals and oceanic ventilation: an alternative view. Geobiology 7, 1–7 (2009)

  11. 11

    Fike, D. A. et al. Oxidation of the Ediacaran ocean. Nature 444, 744–747 (2006)

  12. 12

    Canfield, D. E., Poulton, S. W. & Narbonne, G. M. Late-Neoproterozoic deep-ocean oxygenation and the rise of animal life. Science 315, 92–95 (2007)

  13. 13

    Scott, C. et al. Tracing the stepwise oxygenation of the Proterozoic ocean. Nature 452, 456–459 (2008)

  14. 14

    Holland, H. D. The oxygenation of the atmosphere and oceans. Phil. Trans. R. Soc. B 361, 903–915 (2006)

  15. 15

    Canfield, D. E. The early history of atmospheric oxygen: homage to Robert A. Garrels. Annu. Rev. Earth Planet. Sci. 33, 1–36 (2005)

  16. 16

    Knoll, A. H. & Carroll, S. E. Early animal evolution: emerging views from comparative biology and geology. Science 284, 2129–2137 (1999)

  17. 17

    Peterson, K. J. & Butterfield, N. J. Origin of the Eumetazoa: testing ecological predictions of molecular clocks against the Proterozoic fossil record. Proc. Natl Acad. Sci. USA 102, 9547–9552 (2005)

  18. 18

    Emerson, S. R. & Huested, S. S. Ocean anoxia and the concentrations of molybdenum and vanadium in seawater. Mar. Chem. 34, 177–196 (1991)

  19. 19

    Hastings, D. W., Emerson, S. R. & Mix, A. C. Vanadium in foraminiferal calcite as a tracer for changes in the areal extent of reducing sediments. Paleoceanography 11, 665–678 (1996)

  20. 20

    Algeo, T. J. & Lyons, T. W. Mo-total organic carbon covariation in modern anoxic marine environments: implications for analysis of paleoredox and paleohydrographic conditions. Paleoceanography 21, PA1016, http://dx.doi.org/10.1029/2004PA001112 (2006)

  21. 21

    Wedepohl, K. H. The composition of the continental crust. Geochim. Cosmochim. Acta 59, 1217–1232 (1995)

  22. 22

    Miller, C. A., Peucker-Ehrenbrink, B., Walker, B. D. & Marcantonio, F. Re-assessing the surface cycling of molybdenum and rhenium. Geochim. Cosmochim. Acta 75, 7146–7179 (2011)

  23. 23

    Lyons, T. W. et al. Tracking euxinia in the ancient ocean: a multiproxy perspective and Proterozoic case study. Annu. Rev. Earth Planet. Sci. 37, 507–534 (2009)

  24. 24

    Li, C. et al. A stratified redox model for the Ediacaran ocean. Science 328, 80–83 (2010)

  25. 25

    Pecoits, E. et al. Bilaterian burrows and grazing behavior at >585 million years ago. Science 336, 1693–1696 (2012)

  26. 26

    Condon, D. et al. U-Pb ages from the Neoproterozoic Doushantuo Formation, China. Science 308, 95–98 (2005)

  27. 27

    Jiang, G. et al. Stratigraphy and paleogeography of the Ediacaran Doushantuo Formation (ca. 635–551 Ma) in South China. Gondwana Res. 19, 831–849 (2011)

  28. 28

    Jiang, G. et al. Organic carbon isotope constraints on the dissolved organic carbon (DOC) reservoir at the Cryogenian-Ediacaran transition. Earth Planet. Sci. Lett. 299, 159–168 (2010)

  29. 29

    Calvert, S. E. & Pedersen, T. F. Geochemistry of recent oxic and anoxic marine sediments: implications for the geological record. Mar. Geol. 113, 67–88 (1993)

  30. 30

    Sim, M. S., Bosak, T. & Ono, S. Large sulfur isotope fractionation does not require disproportionation. Science 333, 74–77 (2011)

  31. 31

    Canfield, D. E. & Raiswell, R. The evolution of the sulfur cycle. Am. J. Sci. 299, 697–723 (1999)

  32. 32

    Anbar, A. D. & Knoll, A. H. Proterozoic ocean chemistry and evolution: a bioinorganic bridge? Science 297, 1137–1142 (2002)

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This study was supported by the National Science Foundation Division of Earth Science, NASA Astrobiology programme and National Natural Science Foundation of China. We are grateful to S. Xiao for input, discussions and editing the palaeontological text. We thank C. Reinhard, G. Love, A. Mix, J. Morford, D. Adams, J. Owens, C. Li and L. Och for discussions and S. Bates, G. Gordon and J. Owens for assistance with laboratory analyses. We thank M. Wille for comments and suggestions.

Author information

The research was planned by G.J., T.W.L., A.D.A., X.S., S.K.S., N.J.P., B.K. and X.W. Samples were collected by S.K.S., X.W. and G.J. The manuscript was prepared by S.K.S., N.J.P. and G.J., with important contributions from all co-authors. Analyses were carried out by S.K.S. with contributions from N.J.P. and B.K.

Correspondence to Ganqing Jiang.

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The authors declare no competing financial interests.

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Sahoo, S., Planavsky, N., Kendall, B. et al. Ocean oxygenation in the wake of the Marinoan glaciation. Nature 489, 546–549 (2012). https://doi.org/10.1038/nature11445

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