Late Ediacaran redox stability and metazoan evolution

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Abstract

The Neoproterozoic arrival of animals fundamentally changed Earth's biological and geochemical trajectory. Since the early description of Ediacaran and Cambrian animal fossils, a vigorous debate has emerged about the drivers underpinning their seemingly rapid radiation. Some argue for predation and ecology as central to diversification, whereas others point to a changing chemical environment as the trigger. In both cases, questions of timing and feedbacks remain unresolved. Through these debates, the last fifty years of work has largely converged on the concept that a change in atmospheric oxygen levels, perhaps manifested indirectly as an oxygenation of the deep ocean, was causally linked to the initial diversification of large animals. What has largely been absent, but is provided in this study, is a multi-proxy stratigraphic test of this hypothesis. Here, we describe a coupled geochemical and paleontological investigation of Neoproterozoic sedimentary rocks from northern Russia. In detail, we provide iron speciation data, carbon and sulfur isotope compositions, and major element abundances from a predominantly siliciclastic succession (spanning>1000 m) sampled by the Kel'tminskaya-1 drillcore. Our interpretation of these data is consistent with the hypothesis that the pO2 threshold required for diversification of animals with high metabolic oxygen demands was crossed prior to or during the Ediacaran Period. Redox stabilization of shallow marine environments was, however, also critical and only occurred about 560 million years ago (Ma), when large motile bilaterians first enter the regional stratigraphic record. In contrast, neither fossils nor geochemistry lend support to the hypothesis that ecological interactions altered the course of evolution in the absence of environmental change. Together, the geochemical and paleontological records suggest a coordinated transition from low oxygen oceans sometime before the Marinoan (∼635 Ma) ice age, through better oxygenated but still redox-unstable shelves of the early Ediacaran Period, to the fully and persistently oxygenated marine environments characteristic of later Ediacaran successions that preserve the first bilaterian macrofossils and trace fossils.

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).

References (114)

  • M.T. Hurtgen et al.

    Sulfur cycling in the aftermath of a 635-Ma snowball glaciation: evidence for a syn-glacial sulfidic deep ocean

    Earth Planet. Sci. Lett.

    (2006)
  • E. Ingall et al.

    Evidence for enhanced phosphorus regeneration from marine sediments overlain by oxygen depleted waters

    Geochim. Cosmochim. Acta

    (1994)
  • G. Jiang et al.

    Carbon isotope variability across the Ediacaran Yangtze platform in South China: implications for a large surface-to-deep ocean delta C-13 gradient

    Earth Planet. Sci. Lett.

    (2007)
  • D.T. Johnston

    Multiple sulfur isotopes and the evolution of Earth's surface sulfur cycle

    Earth-Sci. Rev.

    (2011)
  • D.T. Johnston et al.

    An emerging picture of Neoproterozoic ocean chemistry: insights from the Chuar Group, Grand Canyon, USA

    Earth Planet. Sci. Lett.

    (2010)
  • A. Kampschulte et al.

    The sulfur isotopic evolution of Phanerozoic seawater based on the analysis of structurally substituted sulfate in carbonates

    Chem. Geol.

    (2004)
  • A.J. Kaufman et al.

    Stable isotope record of the terminal Neoproterozoic Krol platform in the Lesser Himalayas of northern India

    Precambrian Res.

    (2006)
  • P. Kraal et al.

    Sedimentary organic carbon to phosphorus ratios as a redox proxy in Quaternary records from the Mediterranean

    Chem. Geol.

    (2010)
  • T.W. Lyons et al.

    A critical look at iron paleoredox proxies: new insights from modern euxinic marine basins

    Geochim. Cosmochim. Acta

    (2006)
  • T.W. Lyons et al.

    Contrasting sulfur geochemistry and Fe/Al and Mo/Al ratios across the last oxic-to-anoxic transition in the Cariaco Basin, Venezuela

    Chem. Geol.

    (2003)
  • C. Marz et al.

    Redox sensitivity of P cycling during marine black shale formation: dynamics of sulfidic and anoxic, non-sulfidic bottom waters

    Geochim. Cosmochim. Acta

    (2008)
  • H.W. Nesbitt et al.

    Preictions of some weathering trends of plutonic and volcanic rocks based on thermodynamic and kinetic considerations

    Geochim. Cosmochim. Acta

    (1984)
  • S.W. Poulton et al.

    Development of a sequential extraction procedure for iron: implications for iron partitioning in continentally derived particulates

    Chem. Geol.

    (2005)
  • S.W. Poulton et al.

    A revised scheme for the reactivity of iron (oxyhydr)oxide minerals towards dissolved sulfide

    Geochim. Cosmochim. Acta

    (2004)
  • R. Raiswell et al.

    Rates of reaction between silicate iron and dissolved sulfide in Peru Margin sediments

    Geochim. Cosmochim. Acta

    (1996)
  • R. Raiswell et al.

    A comparison of iron extraction methods for the determination of degree of pyritization and the recognition of iron limited pyrite formation

    Chem. Geol.

    (1994)
  • B. Runnegar

    Precambrian oxygen levels estimated from the biochemistry and physiology of early eukaryotes

    Palaeogeogr. Palaeoclimatol.

    (1991)
  • T.F. Anderson et al.

    Sources and mechanisms for the enrichment of highly reactive iron in euxinic Black Sea sediments

    Am. J. Sci.

    (2004)
  • S. Bengston et al.

    Early radiation of biomineralizing phyla

    Top. Geobiol.

    (1992)
  • N.M. Bergman et al.

    COPSE: a new model of biogeochemical cycling over Phanerozoic time

    Am. J. Sci.

    (2004)
  • R.A. Berner et al.

    A new model for atmospheric oxygen over Phanerozoic time

    Am. J. Sci.

    (1989)
  • B. Bingen et al.

    Timing of Late Neoproterozoic glaciation on Baltica constrained by detrital zircon geochronology in the Hedmark Group, south-east Norway

    Terra Nova

    (2005)
  • N.J. Butterfield

    Macroevolution and macroecology through deep time

    Palaeontology

    (2007)
  • N.J. Butterfield

    Oxygen, animals and oceanic ventilation: an alternative view

    Geobiology

    (2009)
  • D.E. Canfield

    Biogeochemistry of sulfur isotopes

    Stable Isot. Geochem.

    (2001)
  • D.E. Canfield et al.

    A model for iron deposition to euxinic Black Sea sediments

    Am. J. Sci.

    (1996)
  • D.E. Canfield et al.

    Ferruginous conditions dominated later neoproterozoic deep-water chemistry

    Science

    (2008)
  • D.E. Canfield et al.

    Late-Neoproterozoic deep-ocean oxygenation and the rise of animal life

    Science

    (2007)
  • D.E. Canfield et al.

    The reactvity of sedimentary iron minerals towards sulfide

    Am. J. Sci.

    (1992)
  • D.E. Canfield et al.

    Late Proterozoic rise in atmospheric oxygen concentration inferred from phylogenetic and sulphur-isotope studies

    Nature

    (1996)
  • Cloud, P.E., Drake, E.T., 1968. Pre-metazoan evolution and the origins of the Metazoa. In: Evolution and Environment: A...
  • P.A. Cohen et al.

    Large spinose microfossils in Ediacaran rocks as resting stages of early animals

    Proc. Natl. Acad. Sci. USA

    (2009)
  • T.W. Dahl et al.

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

    Proc. Natl. Acad. Sci. USA

    (2010)
  • Diaz, R.J., Rosenberg, R., 1995. Marine benthic hypoxia: a review of its ecological effects and the behavioural...
  • D.H. Erwin et al.

    The Cambrian conundrum: early divergence and later ecological success in the early history of animals

    Science

    (2011)
  • M. Fedonkin et al.

    New data on Kimberella, the Vendian mollusc-like organism (White Sea region, Russia): Palaeoecological and Evolutionary Implications

    (2007)
  • M.A. Fedonkin et al.

    The Late Precambrian fossil Kimberella is a mollusc-like bilaterian organism

    Nature

    (1997)
  • D.A. Fike et al.

    Oxidation of the Ediacaran Ocean

    Nature

    (2006)
  • R.M. Garrels et al.

    Phanerozoic cycles of sedimentary carbon and sulfur

    Proc. Natl. Acad. Sci. USA-Phys. Sci.

    (1981)
  • D.V. Grazhdankin

    Structure and depositional environment of the Vendian Complex in the southeastern White Sea area

    Stratigr. Geol. Correlation

    (2003)
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