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


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.

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Figure 1: Redox proxy data is consistent with decreased oxygenation of the marine environment following the early Cambrian increase in bioturbation.
Figure 2: Modelled steady-state oxygen/phosphorus reservoir sizes as a function of bioturbation.
Figure 3: Examples of the dynamic model response to the introduction of oxygen-sensitive bioturbation.
Figure 4: Net change in steady-state oxygen and phosphate reservoirs due to the introduction of dynamical oxygen-sensitive bioturbation.


  1. Liu, A. G., Mcllroy, D. & Brasier, M. D. First evidence for locomotion in the Ediacara biota from the 565 Ma Mistaken Point Formation, Newfoundland. Geology 38, 123–126 (2010).

    Article  Google Scholar 

  2. Menon, L., McIlroy, D. & Brasier, M. D. Evidence for Cnidaria-like behavior in ca. 560 Ma Ediacaran Aspidella. Geology 41, 895–898 (2013).

    Article  Google Scholar 

  3. Mangano, M & Buatois, L. A. Decoupling of body plan diversification and ecological structuring during the Ediacaran–Cambrian transition: Evolutionary and geobiological feedbacks. Proc. R. Soc. B 281, 20140038 (2014).

    Article  Google Scholar 

  4. Buatois, L. A., Narbonne, G. M., Mangano, M. G., Carmona, M. B. & Myrow, P. Ediacaran matground persisted into the earliest Cambrian. Nature Commun. 5, 3544 (2014).

    Article  Google Scholar 

  5. Tarhan, L. G. & Droser, M. L. Widespread delayed mixing in early to middle Cambrian marine shelfal settings. Palaeogeogr. Palaeoclimatol. Palaeoecol. 399, 310–322 (2014).

    Article  Google Scholar 

  6. Seilacher, A. Biomat-related lifestyles in the Precambrian. Palaios 14, 86–93 (1999).

    Article  Google Scholar 

  7. Droser, M. L. & Bottjer, D. J. Trends and patterns of Phanerozoic ichnofabrics. Ann. Rev. Earth Planet. Sci. Lett. 21, 205–225 (1993).

    Article  Google Scholar 

  8. Frei, R., Gaucher, C., Poulton, S. W. & Canfield, D. E. Fluctuations in Precambrian atmospheric oxygenation recorded by chromium isotopes. Nature 461, 250–254 (2009).

    Article  Google Scholar 

  9. Scott, C. et al. Tracing the stepwise oxidation of the Proterozoic ocean. Nature 452, 456–460 (2008).

    Article  Google Scholar 

  10. Dahl, T. W. et al. Devonian rise in atmospheric oxygen correlated to the radiations in terrestrial plants and large predatory fish. Proc. Natl Acad. Sci. USA 107, 17911–17915 (2010).

    Article  Google Scholar 

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

    Article  Google Scholar 

  12. Redfield, A. C. The biological control of chemical factors in the environment. Am. Sci. 46, 205–221 (1958).

    Google Scholar 

  13. Betts, J. N. & Holland, H. D. The oxygen content of ocean bottom waters, the burial efficiency of organic carbon, and the regulation of atmospheric oxygen. Palaeogeogr. Palaeoclimatol. Palaeoecol. 97, 5–18 (1991).

    Article  Google Scholar 

  14. Ingall, E. & Jahnke, R. Evidence for enhanced phosphorus regeneration from marine sediments overlain by oxygen depleted waters. Geochim. Cosmochim. Acta 58, 2571–2575 (1994).

    Article  Google Scholar 

  15. Ingall, E. D., Bustin, R. M. & Van Cappellen, P. Influence of water column anoxia on the burial and preservation of carbon and phosphorus in marine shales. Geochim. Cosmochim. Acta 57, 303–316 (1993).

    Article  Google Scholar 

  16. Anderson, L. D., Delaney, M. L. & Faul, K. L. Carbon to phosphorus ratios in sediments: Implications for nutrient cycling. Glob. Biogeochem. Cycles 15, 65–79 (2001).

    Article  Google Scholar 

  17. Aller, R. C. Bioturbation and remineralization of sedimentary organic matter: Effects of redox oscillation. Chem. Geol. 114, 331–345 (1994).

    Article  Google Scholar 

  18. Kerrn-Jespersen, J. P. & Henze, M. Biological phosphorus uptake under anoxic and aerobic conditions. Water Res. 27, 617–624 (1993).

    Article  Google Scholar 

  19. Droser, M. L. & Bottjer, D. J. Trends in depth and extent of bioturbation in Cambrian carbonate marine environments, western United States. Geology 16, 233–236 (1988).

    Article  Google Scholar 

  20. McIlroy, D. & Logan, G. A. The impact of bioturbation on infaunal ecology and evolution during the Proterozoic–Cambrian transition. Palaios 14, 58–72 (1999).

    Article  Google Scholar 

  21. Taylor, A., Goldring, R. & Gowland, S. Analysis and application of ichnofabrics. Earth Sci. Rev. 60, 227–259 (2003).

    Article  Google Scholar 

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

    Article  Google Scholar 

  23. Berner, R. A. Burial of organic carbon and pyrite sulphur in the modern ocean: Its Geochemical and environmental significance. Am. J. Sci. 282, 451–473 (1982).

    Article  Google Scholar 

  24. Slomp, C. P., Thomson, J. & de Lange, G. J. Controls on phosphorus regeneration and burial during formation of eastern Mediterranean sapropels. Mar. Geol. 203, 141–159 (2004).

    Article  Google Scholar 

  25. Van Cappellen, P. & Ingall, E. D. Benthic phosphorus regeneration, net primary production, and ocean anoxia: A model of the coupled marine biogeochemical cycles of carbon and phosphorus. Paleoceanography 9, 677–692 (1994).

    Article  Google Scholar 

  26. Lenton, T. M. & Watson, A. J. Redfield revisited: 2. What regulates the oxygen content of the atmosphere? Glob. Biogeochem. Cycles 14, 249–268 (2000).

    Article  Google Scholar 

  27. Gundersen, J. K. & Jorgensen, B. B. Microstructure of diffusive boundary layers and the oxygen uptake of the seafloor. Nature 345, 604–607 (1993).

    Article  Google Scholar 

  28. Papineau, D. Global biogeochemical changes at both ends of the proterozoic: Insights from phosphorites. Astrobiology 10, 165–181 (2010).

    Article  Google Scholar 

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

    Article  Google Scholar 

  30. Partin, C. A. et al. Large scale fluctuations in Precambrian atmospheric and oceanic oxygen levels from the record of U in shales. Earth. Plan. Sci. Lett. 369–370, 284–293 (2013).

    Article  Google Scholar 

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R.A.B., T.M.L. and G.A.S-Z. gratefully acknowledge funding from the National Environment Research Council (NE/I005978/1). T.W.D. was sponsored from the Inge Lehmann Scholarship and the VILLUM Foundation (VKR023127). M.Z. is funded by the National Basic Research Program of China (2013CB835000) and the National Natural Science Foundation of China (40930211). A.W.D. was supported by the SFB754, funded by the German DFG (

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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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Correspondence to R. A. Boyle.

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

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