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Triple oxygen isotope evidence for limited mid-Proterozoic primary productivity

Nature volume 559, pages 613–616 (2018)Cite this article

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Abstract

The global biosphere is commonly assumed to have been less productive before the rise of complex eukaryotic ecosystems than it is today1. However, direct evidence for this assertion is lacking. Here we present triple oxygen isotope measurements (∆17O) from sedimentary sulfates from the Sibley basin (Ontario, Canada) dated to about 1.4 billion years ago, which provide evidence for a less productive biosphere in the middle of the Proterozoic eon. We report what are, to our knowledge, the most-negative ∆17O values (down to −0.88‰) observed in sulfates, except for those from the terminal Cryogenian period2. This observation demonstrates that the mid-Proterozoic atmosphere was distinct from what persisted over approximately the past 0.5 billion years, directly reflecting a unique interplay among the atmospheric partial pressures of CO2 and O2 and the photosynthetic O2 flux at this time3. Oxygenic gross primary productivity is stoichiometrically related to the photosynthetic O2 flux to the atmosphere. Under current estimates of mid-Proterozoic atmospheric partial pressure of CO2 (2–30 times that of pre-anthropogenic levels), our modelling indicates that gross primary productivity was between about 6% and 41% of pre-anthropogenic levels if atmospheric O2 was between 0.1–1% or 1–10% of pre-anthropogenic levels, respectively. When compared to estimates of Archaean4,5,6 and Phanerozoic primary production7, these model solutions show that an increasingly more productive biosphere accompanied the broad secular pattern of increasing atmospheric O2 over geologic time8.

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Fig. 1: Triple oxygen isotope data over the past 1.5 billion years.
Fig. 2: Sulfur and oxygen isotope constraints on limited microbial sulfur cycling in the Sibley basin.
Fig. 3: Empirical probability densities of mid-Proterozoic GPP.

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Acknowledgements

P.W.C. acknowledges funding from a Natural Sciences and Engineering Research Council of Canada (NSERC) PGS-D grant. This research was supported by funding from NSERC, the Fonds de Recherche du Québec–Nature et Technologies, and the University of Colorado Boulder (B.A.W.). H.B. acknowledges funding from the strategic priority research program (B) of CAS (XDB18010104). We thank E. Wolf, N. Cowan, S. Becker, Y. Slichter and L. Derry for discussions on the assumptions, methods and implications of our study.

Reviewer information

Nature thanks B. Passey and the other anonymous reviewer(s) for their contribution to the peer review of this work.

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Authors and Affiliations

  1. McGill University, Montreal, Quebec, Canada

    Peter W. Crockford, Galen P. Halverson & Thi Hao Bui

  2. Weizmann Institute of Science, Rehovot, Israel

    Peter W. Crockford

  3. Princeton University, Princeton, NJ, USA

    Peter W. Crockford

  4. Rice University, Houston, TX, USA

    Justin A. Hayles

  5. Louisiana State University, Baton Rouge, LA, USA

    Justin A. Hayles, Huiming Bao & Yongbo Peng

  6. School of Earth & Space Sciences, Peking University, Beijing, China

    Huiming Bao

  7. Yale University, New Haven, CT, USA

    Noah J. Planavsky

  8. University of California Riverside, Riverside, CA, USA

    Andrey Bekker

  9. Lakehead University, Thunder Bay, Ontario, Canada

    Philip W. Fralick

  10. University of Colorado Boulder, Boulder, CO, USA

    Boswell A. Wing

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  1. Peter W. Crockford
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Contributions

P.W.C. and B.A.W. designed research. N.J.P., A.B. and P.W.F. provided samples. P.W.C., J.A.H., Y.P. and T.H.B. performed isotopic analyses. P.W.C. and B.A.W. conducted modelling. P.W.C. wrote the manuscript with contributions from B.A.W., N.J.P. and A.B., and input from all co-authors.

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Correspondence to Peter W. Crockford.

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Extended data figures and tables

Extended Data Fig. 1 Histograms of existing data for ∆17O values through Earth history.

The histograms show Phanerozoic sulfates2 (n = 51; light grey), syn-Marinoan CAS29 (n = 25; dark grey), post-Marinoan barite2,39,40,41,42 (n = 213; blue) and results from the Sibley sulfates (n = 68; red).

Extended Data Fig. 2 Compiled \({{\boldsymbol{p}}}_{{{\bf{CO}}}_{{\bf{2}}}}\) and \({{\boldsymbol{p}}}_{{{\bf{O}}}_{{\bf{2}}}}\) estimates.

a, \({p}_{{{\rm{CO}}}_{2}}\) estimates. Left y axis, percentage of PAL; right y axis, p.p.m. Grey band outlines results from 1D modelling61 based on temperatures of 273 K (bottom), 288 K (top) and changing solar luminosity. Red dotted lines represent extrapolated general circulation model (GCM) results62 from Archaean estimates. The green-shaded region represents the uncertainty envelope of palaeosol-based estimates65 with the green dotted lines interpolating between estimates at 1.8 and 1.1 Ga together. The pink-shaded region represents estimates based on the COPSE Earth system model63. The brown bar represents modelling-based estimates required to prevent a global glaciation at 1.1 Ga89. The dark-blue square is the microfossil-based estimate that sets maximum limits at 1.05 Ga90,91. Yellow arrows represent the upper (30 PAL) and lower (2 PAL) limits used in this work. Data are from previous publications61,62,63,65,89,91. b, \({p}_{{{\rm{O}}}_{2}}\) estimates. Green arrows represent biologically based estimates; blue arrows represent geochemical estimates; and in red are modelling \({p}_{{{\rm{O}}}_{2}}\) estimates. Purple lines represent the removal of S-MIF92, a proposed bistability field93, and constraints on the establishment of a modern-like ozone layer13,67. The yellow dashed line represents the suggested limits for the removal of deep ocean anoxia76, and the grey dashed line represents the appearance of charcoal. Data are from previous publications9,19,67,68,70,71,72,74,76,77,80,81,82,83,93,94.

Extended Data Fig. 3 Probability distribution functions for the control parameters of the model.

The justification for the form (Gaussian or uniform), the spread (standard deviation or range) and the mean of each distribution is given in the main text and Methods.

Extended Data Fig. 4 Realization of about 10,000 Monte Carlo calculations of GPP (PAL) relative to various control parameters in the isotope mass-balance model.

a, Unlike model calculations for the Neoproterozoic era, there is no clear strong dependence of GPP on assumed \({p}_{{{\rm{CO}}}_{2}}\). b, There is a clear log-linear dependence of the GPP estimates on \({p}_{{{\rm{O}}}_{2}}\). c, GPP responds weakly to \({f}_{{{\rm{O}}}_{2}}\), with large fractions of O2 in sulfate (which indicate smaller ∆17OO2 values) leading to higher estimates of GPP. d, The response of GPP to ∆17Osulfate is similar to the response to \({f}_{{{\rm{O}}}_{2}}\). Smaller ∆17Osulfate values indicate smaller ∆17OO2 values, which—all else being the same—requires greater GPP. e, GPP estimates seem to be largely independent of gamma.

Extended Data Fig. 5 Realization of about 20,000 Monte Carlo calculations of GPP (PAL) and \({{\boldsymbol{p}}}_{{{\bf{O}}}_{{\bf{2}}}}\).

a, Results are calculated to be consistent with the Δ17O measurements in Extended Data Table 1 and the probability distribution functions shown in Extended Data Fig. 2, with the exception of \({p}_{{{\rm{O}}}_{2}}\). These calculations assume restricted ranges of \({p}_{{{\rm{O}}}_{2}}\) between 0.1% and 1% PAL (orange histogram) and between 1% and 10% PAL (blue histogram). In both cases the bimodality seen in the full suite of Monte Carlo calculations (Fig. 3) disappears, and both sets of calculations are well-approximated by single-peaked Gaussian probability density functions. This confirms that \({p}_{{{\rm{O}}}_{2}}\) is the dominant control on the bimodal structure seen in the full suite of Monte Carlo calculations (Fig. 3), and justifies our division of those results into a pair of Gaussian probability density functions, one associated with \({p}_{{{\rm{O}}}_{2}}\) between 0.1% and 1% PAL and another associated with \({p}_{{{\rm{O}}}_{2}}\) between 1% and 10% PAL. b, Results are solutions that are consistent with the ∆17Osulfate dataset (Extended Data Table 1), the probability density functions shown in Extended Data Fig. 1 (with the exception of \({p}_{{{\rm{O}}}_{2}}\)) and the mean GPP estimates of the two inferred Gaussian probability distributions for mid-Proterozoic GPP (Fig. 3). GPP was allowed to vary in a Gaussian fashion between the 95% confidence limits on the GPP mean values.

Extended Data Fig. 6 Geological map of the Lake Nipigon–northern Lake Superior region.

This figure was adapted from a previous publication28. © 2008 Canadian Science Publishing or its licensors. Reproduced with permission.

Extended Data Fig. 7 Oxygen and sulfur isotope compositions (∆17O, δ18O, δ34S and ∆33S) for sulfates from drill hole NI-92-7 plotted against stratigraphic height.

Uncertainty on all analyses is smaller than the sizes of the data points.

Extended Data Table 1 Isotopic data and comparisons with previously published results
Full size table
Extended Data Table 2 Summary of reference parameters for model calculations
Full size table

Supplementary information

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Crockford, P.W., Hayles, J.A., Bao, H. et al. Triple oxygen isotope evidence for limited mid-Proterozoic primary productivity. Nature 559, 613–616 (2018). https://doi.org/10.1038/s41586-018-0349-y

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