Late Ediacaran redox stability and metazoan evolution
Highlights
► Redox stability, in addition to O2, is critical for animal evolution. ► We explain Ediacaran global asynchroneity in sedimentary proxy and animals records. ► We revisit the importance of dysoxia for biological evolution. ► The data reinforce that Ediacaran acritarchs are resting stages of early animals.
Introduction
The hypothesis that increased oxygen availability facilitated Ediacaran (635–542 Ma) metazoan evolution dates back more than half a century (Cloud and Drake, 1968, Nursall, 1959). This hypothesis posits that an increase in the oxygen content of shallow-marine environments was physiologically necessary for the emergence of large, highly energetic animals (Raff and Raff, 1970, Rhoads and Morse, 1971). Ecological and physiological observations place lower dissolved oxygen (DO) limits for ocean waters in which different types of animals can live (e.g., (Diaz and Rosenberg, 1995; Levin, 2003)). They further make predictions about body shape in early animals, based on diffusion length-scales for organisms that lack a circulatory system for bulk oxygen transport (Knoll, 2011, Payne et al., 2011, Raff and Raff, 1970, Runnegar, 1991). Together, then, these physiological requirements for oxygen predict that geochemical evidence for well-oxygenated marine waters should coincide with or slightly antedate fossil records of animals with high oxygen demand.
A growing suite of redox-related geochemical tools is now available to test the oxygen-facilitation hypothesis. For instance, reconstructions of the iron and sulfur cycles in Ediacaran strata of Newfoundland suggest a broad consistency between oxygenation and animal diversification (Canfield et al., 2007). There, deep-water axial turbidites with low overall organic carbon contents preserve a shift in the distribution of iron minerals that bespeaks increased DO. This inferred change in redox structure is placed atop the ∼580 Ma glacial deposit of the Gaskiers Formation and is followed by the appearance of Ediacaran macrofossils through the overlying Drook, Briscal and Mistaken Point formations. A similar geochemical formula was applied to fossil-bearing sections from South China and the Yukon (McFadden et al., 2008, Narbonne and Aitken, 1990), however the relationship between the fossil record and redox transitions in these basins, especially as they relate to Newfoundland (Canfield et al., 2007), is less clear cut. Correlations among these basins and their stratigraphic successions are challenging, and the postulated role of sulfide as a key toxin in basins developed along the continental margin of the South China craton further complicates physiological interpretations (Li et al., 2010).
Thus, the lack of first-order geochemical coherence among these localities, perhaps due in part to locally variable biogeochemical fluxes (Johnston et al., 2010, Kah and Bartley, 2011), means that the direct role that oxygen played in the timing of both local and global animal diversification remains to be fully elucidated. Given this, it is important to acknowledge models of eumetazoan innovation that bypass oxygen entirely and call upon ecology as the primary driver (Butterfield, 2009, Peterson and Butterfield, 2005, Stanley, 1973). In addressing the role of oxygen through the application of robust geochemical techniques, both hypotheses can ultimately be tested.
Environmental and ecological hypotheses make distinct predictions about the sequence of biological and geochemical changes, which can be tested through detailed geochemical analyses of fossil-bearing Ediacaran strata. This forms the premise for our current study of Ediacaran marine sediments from the Eastern European Platform (EEP). This succession hosts some of the most exquisite examples of early animal life (Fedonkin et al., 2007, Fedonkin and Waggoner, 1997, Martin et al., 2000) and offers a prime opportunity to reconstruct oceanic redox conditions through the application of a range of geochemical methods. Here, we thus revisit both the oxygen facilitation and ecology hypotheses through the application of iron, sulfur, and carbon geochemistry, bulk elemental data, and rigorous statistical analysis.
Section snippets
Geological setting
The Kel'tminskaya-1 drillhole, located near the Dzhezhim–Parma uplift in northern Russia records ∼5000 m of upper Neoproterozoic and Paleozoic strata that accumulated along the northeast margin of the East European Platform (Fig. 1). The lowermost 2000 m of the core contains a mixed carbonate and siliciclastic succession deposited in a shallow-marine setting, correlated bio- and chemo-stratigraphically to the Cryogenian (850–635 Ma) Karatau Group in the Ural Mountains (Raaben and Oparenkova, 1997,
Methods
Iron speciation was performed following a calibrated extraction technique (Poulton and Canfield, 2005). This method targets operationally defined iron pools, such as iron carbonate (Fecarb: ankerite and siderite), Fe3+ oxides (Feox: goethite and hematite) and mixed valence iron minerals (Femag: magnetite). Pyrite iron (Fepy) and sulfur, as well as acid volatile sulfur (AVS; below detection in these samples) were extracted via traditional distillation techniques (Canfield et al., 1986).
Results and discussion
We used iron speciation chemistry, major element abundances, and stable carbon and sulfur isotopic ratios to characterize oceanic redox conditions and biogeochemical cycling during deposition of the Kel'tminskaya-1 succession (Fig. 2). The distribution of reactive iron minerals in marine sediment has been calibrated in order to differentiate between oxic and anoxic water column conditions (Canfield et al., 1996, Lyons et al., 2003, Poulton and Canfield, 2011, Raiswell et al., 1988, Raiswell et
Conclusions
Geochemical reconstructions of Cryogenian and Ediacaran successions on the margin of the Eastern European Platform preserve a history of Earth surface evolution that can be related to similar reconstructions from other continents (Canfield et al., 2007, Johnston et al., 2010, McFadden et al., 2008, Shen et al., 2008), and, more importantly, extends our understanding of how atmospheric oxygen may have influenced the early diversification of metazoans. Previous geochemical models have
Acknowledgments
We appreciate early and ongoing discussions with P. Cohen, N. Tosca, B. Gill and E. Sperling. D. Schrag and G. Eischeid are thanked for laboratory assistance. This work was funded by the Harvard Microbial Sciences Initiative (DTJ), NASA Exobiology (DTJ, AHK) and the Astrobiology Institute, MIT node (DJ and AHK), NERC (SWP), RBBR grant 10-05-00294 (VNS and NGV), and NSERC Discovery (AB).
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