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Rise to Modern Levels of Ocean Oxygenation Coincided with the Cambrian Radiation of Animals

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Rise to Modern Levels of Ocean Oxygenation Coincided with the Cambrian Radiation of Animals ARTICLE Received 8 Dec 2014 | Accepted 9 Apr 2015 | Published 18 May 2015 DOI: 10.1038/ncomms8142 OPEN Rise to modern levels of ocean oxygenation coincided with the Cambrian radiation of animals Xi Chen1, Hong-Fei Ling1, Derek Vance2, Graham A. Shields-Zhou3,4, Maoyan Zhu4, Simon W. Poulton5, Lawrence M. Och3, Shao-Yong Jiang1,6,DaLi1, Lorenzo Cremonese3 & Corey Archer2 The early diversification of animals (B630 Ma), and their development into both motile and macroscopic forms (B575–565 Ma), has been linked to stepwise increases in the oxygenation of Earth’s surface environment. However, establishing such a linkage between oxygen and evolution for the later Cambrian ‘explosion’ (540–520 Ma) of new, energy- sapping body plans and behaviours has proved more elusive. Here we present new molybdenum isotope data, which demonstrate that the areal extent of oxygenated bottom waters increased in step with the early Cambrian bioradiation of animals and eukaryotic phytoplankton. Modern-like oxygen levels characterized the ocean at B521 Ma for the first time in Earth history. This marks the first establishment of a key environmental factor in modern-like ecosystems, where animals benefit from, and also contribute to, the ‘homeostasis’ of marine redox conditions. 1 State Key Laboratory for Mineral Deposits Research, Department of Earth Sciences, School of Earth Sciences and Engineering, Nanjing University, 163 Xianlin Avenue, Nanjing 210023, China. 2 Department of Earth Sciences, Institute of Geochemistry and Petrology, ETH, Zu¨rich CH-8092, Switzerland. 3 Department of Earth Sciences, University College London, Gower Street, London WC1E 6BT, UK. 4 State Key Laboratory of Palaeobiology and Stratigraphy, Nanjing Institute of Geology and Palaeontology, Chinese Academy of Sciences, 39 East Beijing Road, Nanjing 210008, China. 5 School of Earth and Environment, University of Leeds, Leeds LS2 9JT, UK. 6 State Key Laboratory of Geological Processes and Mineral Resources, Department of Resource Science and Engineering, Faculty of Earth Resources, China University of Geosciences, Wuhan 430074, China. Correspondence and requests for materials should be addressed to H.-F.L. (email: hfl[email protected]) or to D.V. (email: [email protected]). NATURE COMMUNICATIONS | 6:7142 | DOI: 10.1038/ncomms8142 | www.nature.com/naturecommunications 1 & 2015 Macmillan Publishers Limited. All rights reserved. ARTICLE NATURE COMMUNICATIONS | DOI: 10.1038/ncomms8142 he delay between the origin of animals (B800 Ma, as isotope compositions (see Methods) of well-preserved organic-rich inferred from molecular clocks)1 and their early marine sediments of Cryogenian to early Cambrian age. We also Tdiversification in the Ediacaran Period (635–541 Ma)2 has assess local water column redox conditions using iron speciation been suggested to be due to sluggish oxygenation of the Earth (see Methods) in the same sediments. We find that the tempo of surface3,4. After the ‘Great Oxidation Event’ (GOE5) in the early ocean oxygenation, as reconstructed by the Mo isotope and B Proterozoic ( 2,400–2,100 Ma), atmospheric PO2 stayed within concentration profiles, was in step with the early Cambrian B0.01 and B10% of the present atmospheric level during the bioradiation. mid-Proterozoic (B2,100–800 Ma (refs 6,7)). It was only after the B termination of the Cryogenian glaciations ( 635 Ma) that Results oxygen levels in Earth’s surface environment began to increase 8,9 Geologic setting and samples. Late Neoproterozoic to Cambrian significantly again . Although the lower estimate of Ediacaran successions are well developed in South China. They are fossili- atmospheric PO2 may surpass the minimum oxygen requirement ferous, with several unique biotas in various environments of animals (o0.1% present atmospheric level)4, the deeper ocean 10–12 (Supplementary Note 1) and provide one of the best candidates likely remained predominantly anoxic . As a consequence, O2 13 14 for constraining the co-evolution of marine oxygenation and deficiency ,H2S toxicity and a scarcity of trace metal life9,14,40. We collected black shales and organic-rich cherts from micronutrients (such as Mo, Cu and Zn (ref. 15)) may have shallow-to-deep water successions on the south-eastern margin of continued to limit the ecological distribution of eukaryotes. the Yangtze platform (Supplementary Figs 1 and 2). The ages of Eukaryotes, especially animals and planktonic algae, only our samples span the mid-Cryogenian to the early Cambrian began to dominate the marine ecosystem during the ‘Cambrian (B660–520 Ma). Ediacaran and early Cambrian successions in B 12,16,17 explosion’ of biological diversity ( 520 Ma) . Many the Yangtze Gorges area represent shallow-water facies, while essential aspects of this biotic event, such as increased animal 18 19,20 deeper water facies occur in northwestern Hunan and southern body size , active locomotion, bioturbation , carbonate Anhui provinces (see Supplementary Note 1). biomineralization21, carnivory13,22 and cropping17,23,24, have been linked to a rise in atmospheric oxygen beyond the minimum requirement of animals, and/or widespread ocean Mo isotopes. Our Mo concentration and isotopic data, together oxygenation. However, redox conditions in the early Cambrian with published data from the late Archaean to early Cambrian, oceans, especially the deep ocean, are still controversial. Some are compiled in Supplementary Data 1 and shown in Fig. 1 and studies suggest widespread oxygenation13,25,26, while others Supplementary Fig. 2. After several moderate peaks ( þ 1.5% to propose a ferruginous (Fe2 þ -rich) or even euxinic (H S-rich) þ 1.7%) without a distinct increase in Mo abundance in the late 2 B 41–44 98/95 deep marine environment10,27. Moreover, it has been suggested Archaean ( 2,500–2,750 Ma) , presaging the GOE, d Mo that oceanic oxygen remained at levels much lower than the remained at low levels (o þ 1.3%) from the late B modern until the Devonian28. Palaeoproterozoic ( 2,300 Ma) to the mid-Neoproterozoic (B750 Ma)28,30,41,45–48. In the late Neoproterozoic, higher Here we use sedimentary molybdenum (Mo) isotope composi- 98/95 tions to trace the evolution of global ocean redox state over this d Mo values (up to þ 1.6%) are tied to increased Mo critical period for animal evolution. Global marine redox abundance in the aftermath of the three major glaciations conditions can be inferred from the sedimentary Mo record (Sturtian, Marinoan and Gaskiers), possibly linked to oxygenation events driven by high nutrient inputs from enhanced terrestrial because of its redox-sensitive deposition and isotope fractionation 6,8 98/95 mechanisms9,29–32. In the modern oxic openÀÁ oceans, Mo is present weathering . d Mo values approached 4 þ 1.5% around as the conservative oxyanion molybdate MoO2 À at relatively 550 Ma, and then reached þ 2% for the first time in Earth 4 B high concentrations (its salinity-normalized concentration is history during the earliest Cambrian ( 535 Ma, mid-Fortunian B107 nmol kg À 1)33. The modern open-ocean seawater (OSW) Stage). After that, coinciding with the first occurrence of trilobites Mo reservoir is enriched in heavy isotopes (modern and nearly all animal clades in the major phase of the ‘Cambrian 98/95 explosion’, both high d98/95Mo values (near þ 2.3%) and high d MoOSW ¼þ2.34%, relative to NIST-SRM-3134 (ref. 34)) 98/95 Mo concentrations (4100 p.p.m.) are found in samples from relative to the dominant input from rivers (d MoRivers ¼ þ 0.7% (ref. 35)). This arises because a major sink for Mo in the different locations, and cluster around the Cambrian Stage 2/3 modern oceans is the slow adsorption on particulate manganese boundary (521 Ma). There are four sulphidic samples out of eight 98/95 B oxides under widespread oxic conditions, and because this process samples having high d Mo values (4 þ 1.9%) between 525 and B520 Ma. Although the other half of these eight samples is accompanied by a À 3% isotopic fractionation DSediment–OSW, that is, d98/95Mo À d98/95Mo ¼À3% (refs 29,36)). were deposited under Fe-rich conditions (note that these samples Sediment OSW B still contain appreciable pyrite, with FePy/FeHR40.3 to 0.5), we When bottom-water dissolved oxygen is low or absent, H2Smay 98/95 be present in pore waters of organic-rich reducing sediments (on emphasise that the sediments analysed likely record d Mo some continental margins) or in the water column (for example, close to that of contemporaneous seawater (for the sulphidic Black Sea and regions of intense upwelling). Under these black shales) or a minimum value for seawater (for the conditions, Mo deposition can be accelerated by one to two ferruginous black shales). orders of magnitude37,38, leading to smaller isotopic fractionations DSediment–OSW ¼ 0to À 0.7% (ref. 39)) due to more quantitative Discussion sequestration from the dissolved phase in these settings. An Our data provide an estimate for the lower limit of coeval expansion of such sulphidic conditions will therefore cause seawater Mo isotopic composition and document the fact that 98/95 98/95 the d Mo value of seawater to decrease towards the riverine d MoOSW rose to a level higher than ever before during the input value. Seawater d98/95Mo will most likely be recorded in early Cambrian, peaking at modern levels (B þ 2.3%)at sediments deposited under euxinic conditions because of B520 Ma. The rarity of black shales deposited under fully quantitative removal of aqueous Mo. However, importantly, euxinic conditions makes a continuous record of the precise measured d98/95Mo values of sediments provide a minimum d98/95Mo of seawater difficult to obtain. However, where constraint on contemporaneous seawater isotopic composition sulphidic black shale data (or phosphatic data, which have been because all known sedimentary Mo sinks record suggested also to record seawater values25) are available, their d98/95Morseawater28.
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