Stabilization of the coupled oxygen and phosphorus cycles by the evolution of bioturbation

Journal name:
Nature Geoscience
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Animal burrowing and sediment-mixing (bioturbation) began during the run up to the Ediacaran/Cambrian boundary1, 2, 3, initiating a transition4, 5 between the stratified Precambrian6 and more well-mixed Phanerozoic7 sedimentary records, against the backdrop of a variable8, 9 global oxygen reservoir probably smaller in size than present10, 11. Phosphorus is the long-term12 limiting nutrient for oxygen production via burial of organic carbon13, and its retention (relative to carbon) within organic matter in marine sediments is enhanced by bioturbation14, 15, 16, 17, 18. Here we explore the biogeochemical implications of a bioturbation-induced organic phosphorus sink in a simple model. We show that increased bioturbation robustly triggers a net decrease in the size of the global oxygen reservoir—the magnitude of which is contingent upon the prescribed difference in carbon to phosphorus ratios between bioturbated and laminated sediments. Bioturbation also reduces steady-state marine phosphate levels, but this effect is offset by the decline in iron-adsorbed phosphate burial that results from a decrease in oxygen concentrations. The introduction of oxygen-sensitive bioturbation to dynamical model runs is sufficient to trigger a negative feedback loop: the intensity of bioturbation is limited by the oxygen decrease it initially causes. The onset of this feedback is consistent with redox variations observed during the early Cambrian rise of bioturbation, leading us to suggest that bioturbation helped to regulate early oxygen and phosphorus cycles.

At a glance


  1. Redox proxy data is consistent with decreased oxygenation of the marine environment following the early Cambrian increase in bioturbation.
    Figure 1: Redox proxy data is consistent with decreased oxygenation of the marine environment following the early Cambrian increase in bioturbation.

    a,b, Bioturbation data from ref. 3. Bioturbation index3, 22 refers to the percentage of the original sediment fabric exhibiting disturbance by bioturbation: 0 = 0%, 1 = 1–4%, 2 = 5–30%, 3 = 31–60%, 4 = 61–90%, 5 = 91–99%, 6 = 100%. c, Molybdenum isotope compositions δ98Mo= [(98Mo/95Mo)sample /(98Mo/95Mo)NIST−SRM3134 − 1] ⋅ 1,000 [‰]. Seawater δ98Mo scales positively with ocean oxygenation. The maximum δ98Mo value (rather than the mean) is the strongest indicator of the extent of ocean oxygenation, because mildly euxinic shales have a lower δ98Mo than ambient seawater. df, Mo/TOC (d), U/TOC (e) and sedimentary Mo and U contents (f). Both Mo and U are soluble in oxic waters and more efficiently removed under anoxic and sulphidic conditions. Normalization to TOC scales out the dependence of trace metal enrichment on TOC content. Anoxic settings identified by Fe:Al > 0.5, euxinic settings by Fe(highly reactive/total) > 0.38 and Fe(pyritized/highly reactive) > 0.7 (see Supplementary Table 3 for further details and full references). Arrows mark intervals of the proposed relative oxygen decline.

  2. Modelled steady-state oxygen/phosphorus reservoir sizes as a function of bioturbation.
    Figure 2: Modelled steady-state oxygen/phosphorus reservoir sizes as a function of bioturbation.

    Steady-state size of the atmosphere/surface oxygen (blue, left) and marine phosphorus (green, right) reservoirs for different bulk weathering forcings W = 0.5 (a), W = 1.0 (b), W = 1.5 (c) relative to the present and with different values for the organic carbon to phosphorus ratio for bioturbated C : Pbiot and laminated C : Plam sediments (as indicated by the different linestyles on each plot).

  3. Examples of the dynamic model response to the introduction of oxygen-sensitive bioturbation.
    Figure 3: Examples of the dynamic model response to the introduction of oxygen-sensitive bioturbation.

    Model initialized at a steady state with negligible bioturbation, fbiot = 0.01, then dynamic bioturbation fbiot = 1 − anox (where anox is the ocean anoxic fraction) is introduced 25 million years into each 100-million-year simulation. For each model run the upper panel in the subfigure shows the marine reservoirs (relative to their modern values) and relevant fluxes, while the lower panel in the subfigure shows the fluxes affecting the phosphorus reservoir (in absolute values of 1010 mol yr−1). ac, Moderate difference in prescribed C:P burial ratios C:Pbiot = 150, C:Plam = 300. df, Larger difference in prescribed C:P burial ratios C:Pbiot = 200, C:Plam = 700. Columns show different bulk weathering values W = 0.5 (a,d), W = 1.0 (b,e), W = 1.5 (c,f). Abbreviations: PO4, marine phosphate reservoir; O2, atmosphere/surface ocean oxygen reservoir; fbiot, bioturbated fraction of buried organic matter; newp, new production; anox, ocean anoxic fraction; mocb, marine organic carbon burial; mopb, marine organic phosphorus burial; capb, calcium-bound phosphate burial; fepb, iron adsorbed phosphate burial; phosw, phosphorus weathering.

  4. Net change in steady-state oxygen and phosphate reservoirs due to the introduction of dynamical oxygen-sensitive bioturbation.
    Figure 4: Net change in steady-state oxygen and phosphate reservoirs due to the introduction of dynamical oxygen-sensitive bioturbation.

    The model was allowed to reach steady state with negligible bioturbation, then dynamical bioturbation was introduced leading to a new steady state (that is, every point in Fig. 4 corresponds to a dynamical run equivalent to Fig. 3). Pre-bioturbation reservoir sizes were subtracted from their respective post-bioturbation values and the difference is expressed relative to the present-day reservoir size—that is, (O2(after) − O2(before))/O20 and(PO4(after) − PO4(before))/PO40. Results are shown as a function of bulk weathering rate (x-axis) with different C:P burial ratio parameter choices (as indicated by the linestyles in the legend). a, Change in atmosphere–surface–ocean oxygen reservoir. b, Change in marine phosphate reservoir.


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  1. Institute of Biology and Nordic Centre for Earth Evolution, University of Southern Denmark, Campusvej 55, 5230 Odense M, Odense, Denmark

    • R. A. Boyle,
    • T. W. Dahl &
    • D. E. Canfield
  2. Laver Building, College of Life and Environmental Sciences, University of Exeter, North Park Road, Exeter EX4 4QE, UK

    • R. A. Boyle &
    • T. M. Lenton
  3. Natural History Museum of Denmark, University of Copenhagen, Øster Voldgade 5-7, 1350 København K, Denmark

    • T. W. Dahl
  4. GEOMAR Helmholtz Centre for Ocean Research Kiel, Wischhofstrasse 1-3, 24148 Kiel, Germany

    • A. W. Dale
  5. Department of Earth Sciences, University College London, Gower Street, London WC1E 6BT, UK

    • G. A. Shields-Zhou
  6. Nanjing Institute of Geology and Palaeontology, Chinese Academy of Sciences, 39 East Beijing Road, Nanjing 210008, China

    • M. Zhu
  7. Department of Earth Sciences, University of Oxford, South Parks Road, Oxford OX1 3AN, UK

    • M. D. Brasier


R.A.B., T.M.L., G.A.S-Z. and M.Z. developed the hypothesis, including ideas from all co-authors. T.W.D. provided data. R.A.B. modified the original model of T.M.L. R.A.B. wrote the paper with input from all co-authors.

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