Possible links between extreme oxygen perturbations and the Cambrian radiation of animals

Abstract

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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Fig. 1: Carbonate carbon and carbonate-associated sulfate sulfur isotope records from Cambrian Stage 2 to Stage 4 of sections of the Siberian Aldan and Lena rivers.
Fig. 2: Carbon and sulfur cycle model output.
Fig. 3: Animal diversity, biological events and their correlation to the isotope records and oxygenation pattern across Cambrian Stages 2–4.

Data availability

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

Code availability

The code used to generate the coupled carbon and sulfur cycle model results is available from the corresponding author on request.

References

  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).

    Article  Google Scholar 

  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).

    Article  Google Scholar 

  3. 3.

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

    Article  Google Scholar 

  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).

    Article  Google Scholar 

  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).

    Article  Google Scholar 

  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).

    Article  Google Scholar 

  7. 7.

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

    Article  Google Scholar 

  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).

    Article  Google Scholar 

  9. 9.

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

    Article  Google Scholar 

  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).

    Article  Google Scholar 

  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).

    Article  Google Scholar 

  12. 12.

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

    Article  Google Scholar 

  13. 13.

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

    Article  Google Scholar 

  14. 14.

    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 

  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).

    Article  Google Scholar 

  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).

    Article  Google Scholar 

  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).

    Article  Google Scholar 

  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).

    Article  Google Scholar 

  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).

    Article  Google Scholar 

  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).

    Article  Google Scholar 

  22. 22.

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

    Article  Google Scholar 

  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).

    Article  Google Scholar 

  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).

    Article  Google Scholar 

  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).

    Article  Google Scholar 

  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).

    Article  Google Scholar 

  27. 27.

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

    Article  Google Scholar 

  28. 28.

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

    Article  Google Scholar 

  29. 29.

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

    Article  Google Scholar 

  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).

    Article  Google Scholar 

  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).

    Article  Google Scholar 

  32. 32.

    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 

  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).

    Article  Google Scholar 

  34. 34.

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

    Article  Google Scholar 

  35. 35.

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

    Article  Google Scholar 

  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).

    Article  Google Scholar 

  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).

    Article  Google Scholar 

  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).

    Article  Google Scholar 

  40. 40.

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

    Article  Google Scholar 

  41. 41.

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

    Article  Google Scholar 

  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).

    Article  Google Scholar 

  43. 43.

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

    Article  Google Scholar 

  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).

    Article  Google Scholar 

  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).

    Article  Google Scholar 

  46. 46.

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

    Article  Google Scholar 

  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).

    Article  Google Scholar 

  48. 48.

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

    Article  Google Scholar 

  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).

    Article  Google Scholar 

  50. 50.

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

    Article  Google Scholar 

  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).

    Article  Google Scholar 

  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).

    Article  Google Scholar 

  54. 54.

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

    Article  Google Scholar 

  55. 55.

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

    Article  Google Scholar 

  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).

    Article  Google Scholar 

  57. 57.

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

    Article  Google Scholar 

  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).

    Article  Google Scholar 

  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).

    Article  Google Scholar 

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Acknowledgements

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.

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

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He, T., Zhu, M., Mills, B.J.W. et al. Possible links between extreme oxygen perturbations and the Cambrian radiation of animals. Nat. Geosci. 12, 468–474 (2019). https://doi.org/10.1038/s41561-019-0357-z

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