Devonian rise in atmospheric oxygen correlated to the radiations of terrestrial plants and large predatory fish

Abstract

The evolution of Earth's biota is intimately linked to the oxygenation of the oceans and atmosphere. We use the isotopic composition and concentration of molybdenum (Mo) in sedimentary rocks to explore this relationship. Our results indicate two episodes of global ocean oxygenation. The first coincides with the emergence of the Ediacaran fauna, including large, motile bilaterian animals, ca. 550-560 million year ago (Ma), reinforcing previous geochemical indications that Earth surface oxygenation facilitated this radiation. The second, perhaps larger, oxygenation took place around 400 Ma, well after the initial rise of animals and, therefore, suggesting that early metazoans evolved in a relatively low oxygen environment. This later oxygenation correlates with the diversification of vascular plants, which likely contributed to increased oxygenation through the enhanced burial of organic carbon in sediments. It also correlates with a pronounced radiation of large predatory fish, animals with high oxygen demand. We thereby couple the redox history of the atmosphere and oceans to major events in animal evolution.

Fig. 1.

Bulk δ⁹⁸Mo of sediments deposited in the last 1,800 million years under various redox conditions: euxinic (red circle), ferruginous (brown diamond), oxic with sulfidic sediments (sand-colored triangle), and oxic sediments with Mn-oxides (gray triangle). Data with Mo EF < 2 or Mo/Mo_crust < 2 are dominated by detrital material (not shown). Some published data have no local redox constraints (purple circle). Mildly or intermittently euxinic conditions (pink circle) are known to fractionate Mo isotopes in the modern system but cannot be distinguished from highly euxinic sediments in the past. The blue and green vertical lines mark the Ediacaran emergence of large animals including motile bilaterians and the Devonian invasion of vascular land plants, respectively. Typical error of the isotope determination is ± 0.14‰ (2sd, standard reproducibility).

Fig. 2.

Model results showing how seawater δ⁹⁸Mo responds to Mo burial into its different sinks (model details in SI Appendix). Contours show range of solutions for a given seawater δ⁹⁸Mo that represents modern seawater (2.3‰), early Devonian seawater (2.0‰), early Paleozoic seawater (1.4‰), and Mesoproterozoic seawater (1.1‰). The black circle represents modern state (Table S3). The shaded area at bottom left represents states where the sulfidic sinks are dominant, so that the ocean becomes heterogeneous in dissolved molybdenum. The faded area at top lacks the intermediate redox sink, despite the extreme end-members (OX and EUX) being substantial (top). Both regions are considered unlikely.

Fig. 3.

(A) Size maxima of vertebrates is used as a measure of maximal specific metabolic rate at a given time (42). (B) euxinic samples over the last 800 Ma with seawater value inferred from highly euxinic sediments (red circles) and mildly euxinic sediments fractionated to lower values (pink circles). Seawater values above the dashed line require a substantial oxic Mo sink. (C) Mo/TOC of black shales (new data, solid green circles; old data, gray circles; compilation summarized in SI Appendix). In B and C solid lines represent 90% percentiles for the three time periods: 800-542 Ma, 541-390 Ma, and 390-0 Ma. These three time periods are distinct from each other; see statistical analysis in SI Appendix. The Ediacaran emergence of large animals and the Devonian invasion of vascular land plants are shown by graded column bars in blue and green, respectively.