On the coevolution of Ediacaran oceans and animals Yanan Shen*†, Tonggang Zhang*, and Paul F. Hoffman†‡ *De´partement des Sciences de la Terre et de l’Atmosphe`re, Universite´du Que´bec, Montre´al, QC, Canada H3C 3P8; and ‡Department of Earth and Planetary Sciences, Harvard University, Cambridge, MA 02138 Contributed by Paul F. Hoffman, March 4, 2008 (sent for review December 3, 2007) Fe speciation and S-isotope of pyrite data from the terminal mostly buried by younger rocks. Southwest of the Plateau Thrust Proterozoic Sheepbed Formation in Canada and Doushantuo For- system, a single transverse structural culmination exposes three mation in China reveal that ocean deep waters were anoxic after separate inliers of Ediacaran strata, the most easterly of which the global glaciations (snowball Earth) ending 635 million years (Sekwi Brook) contains a moderately diverse assemblage of ago, but that marine sulfate concentrations and inferentially at- mostly disk-shaped macrofossils, apparently representing the mospheric oxygen levels were higher than before the glaciations. bases of sessile, polypoid, and frond-like, soft-bodied organisms, This supports a long-postulated link between oxygen levels and as well as rare ovate segmented fossils, and abundant simple or the emergence of eumetazoa. Subsequent ventilation of the deep irregularly meandering burrows (28–30). The oldest fossils (five ocean, inferred from shifts in Fe speciation in Newfoundland genera of disk-shaped forms) occur in the middle Sheepbed (previously published data) and western Canada (this report), Formation (Fig. 1), a 1,050-m-thick sequence of black shales, paved the way for Ediacaran macrobiota to colonize the deep turbiditic siltstones, and contour-current sands, deposited at seafloors. estimated water depths of 1–1.5 km on an open-marine conti- nental slope subject to geostrophic currents (26). They are much atmospheric oxygen ͉ iron speciation ͉ sulfur isotopes ͉ larger and more diverse than the simple discs found between the Sheepbed Formation ͉ Doushantuo Formation two Cryogenian glacial horizons in the same area (31). The shelf–slope transition is best exposed on Stelfox Mountain pair of global glaciations (1) between 725 and 635 million years (Fig. 1), 25 km northeast of Sekwi Brook, where a major Aago (Cryogenian Period) was followed by the appearance and down-to-southwest breakaway paleoscarp (32) marks the outer diversification of (mainly nonskeletal) multicellular animals in the edge of the Keele Formation, a mixed carbonate-clastic shelf Ediacaran Period from 635 to 541 million years ago (2–7). The sequence beneath the end-Cryogenian glacial horizon (33). The oldest animal fossils include diapause egg and embryo cysts (Tian- submarine landslide responsible for the paleoscarp generated an zhushania spinosa) from the lower Doushantuo Formation (Ϸ632 enormous megabreccia, the Durkan Formation (32), carrying Ma) in South China (8) and lipid biomarkers (24-isopropyl- house-size blocks of Keele shelf lithologies. The landslide is cholestane) diagnostic of marine demosponges in late Cryogenian thought to be unrelated to the subsequent glaciation (32), the and early Ediacaran strata of Oman (9). In contrast, colonization retreat of which left a blanket (Stelfox Member) of nonstratified of the deep seafloor (below the euphotic zone) by large soft-bodied diamictite (marine till) and ice-rafted debris on both the hanging organisms was delayed until mid-Ediacaran time Ϸ579 Ma (10–14). wall and footwall of the paleoscarp (Fig. 1). Stelfox diamictite is The delayed appearance of large animals in the fossil record, Ϸ600 overlain by a well developed syn-deglacial ‘‘cap’’ dolostone million years after multicellularity arose in algae (15), inspired the (Ravensthroat Formation) with giant wave ripples and corrugate hypothesis that an increase in atmospheric oxygen catalyzed early stromatolites, overlain discontinuously by limestone (Hayhook animal evolution (6, 16–22). Formation) with seafloor cements (27). At Stelfox Mountain, Recent chemostratigraphic studies provide some evidence for the dolostone-limestone couplet tapers downslope because of progressive oxygenation of the Ediacaran ocean (23), including slump-related truncation (Fig. 1). The Ravensthroat Formation mid-Ediacaran (ca. 580 Ma) deep waters (24). The first study is widely assumed to be correlative with the Nuccaleena cap based its inference mainly on increasing sulfur isotope fraction- dolostone at the global stratotype section and point (GSSP) in ation between coexisting sulfides and carbonate-associated sul- South Australia, which defines the base of the Ediacaran Period fate (23); the second was based on the low ratios between highly (34, 35). reactive Fe and total Fe (FeHR/FeT) (24). These data purport The basal Ediacaran cap-carbonate couplet is overlain every- to ‘‘see’’ through the veil of diagenesis under the influence of where by a thick black shale, the Sheepbed Formation, which anoxic pore-waters to the redox state of ancient seawater. Here, grades into flaggy dark limestones of the overlying Gametrail we present Fe speciation and S-isotope of pyrite data from Formation on Stelfox Mountain (Fig. 1). The shale is associated deep-water ocean-margin settings in northwestern Canada and with long-term flooding of the shelf after the end-Cryogenian in South China that point to an extended early Ediacaran interval (‘‘Marinoan’’) glaciation. A stratigraphically and lithologically of sulfate-rich oceans with sulfidic deep waters, implying an homologous section of Sheepbed Formation occurs at Shale oxygen-rich atmosphere, followed by the ventilation of deep Lake, 130 km to the northwest. Like Stelfox Mountain, the Shale waters in mid-Ediacaran time. Lake section is situated on the extreme edge of the Keele shelf (26–28). The Gametrail at Shale Lake is a cliff-forming crystal- Geological Setting line dolostone. We elected to measure and sample the Sheepbed Northwest Canada. Ediacaran strata of the Windermere Super- group (25) are exposed for Ͼ500 km along the concave-to- southwest arc of the Mackenzie Mountains, the topographic Author contributions: Y.S. and P.F.H. designed research; Y.S., T.Z., and P.F.H. performed expression of the early Cenozoic foreland thrust-fold belt of the research; Y.S. analyzed data; and Y.S. and P.F.H. wrote the paper. northern Canadian Cordillera. Because of a low-angle uncon- The authors declare no conflict of interest. formity with overlying Cambrian strata, the Ediacaran is mainly Freely available online through the PNAS open access option. limited to the Plateau Thrust system, an outcrop belt less than †To whom correspondence may be addressed. E-mail: [email protected] or Ϸ30 km wide. Fortuitously, it preserves the shelf-to-slope tran- [email protected]. sition of an Ediacaran passive continental margin (25–27). To This article contains supporting information online at www.pnas.org/cgi/content/full/ the northeast (landward), Ediacaran strata were removed by 0802168105/DCSupplemental. sub-Cambrian erosion and to the southwest (seaward), they are © 2008 by The National Academy of Sciences of the USA 7376–7381 ͉ PNAS ͉ May 27, 2008 ͉ vol. 105 ͉ no. 21 www.pnas.org͞cgi͞doi͞10.1073͞pnas.0802168105 Downloaded by guest on October 2, 2021 SE G a m e t r a i l F o r m a t i o n NW 0.0 0.2 0.4 0.6 0.8 -200 20 40 d e b p e e h S r e p p U p p e r S h e e p b e d 1000 500 LITHOFACIES 660 ) )ekaL e )ekaL E Ediacaran macrofossils m( cc cc evob esab fo debpeehS mF contour-current siltstone 640 500 900 O x greyi c turbiditic S h siltstone e e p b e d 400 l black pyritic shale a 620 h limestone with crystal fans li mF S( E peloidal dolostone with giant wave ripples 800 600 dolostone with corrugate 300 a stromatolites rtemaG a glacigenic diamictite t 580 hgieh d e b p e e h S e l l e S h e e p b e d green turbiditic siltstone 400 landslide mega-breccia 700 FeHR epigenetic dolostone 200 560 cc /FeT E flaggy limestone shift 0 1 24356 o crossbedded sandstone δ13C ( /oo VPDB) d d i M i d 600 d c i x o n A A n o x i c e b p p b e 100 E cc e e h S h e e 300 E cc 500 Hayhook 0 Ravensthroat Stelfox 400 -100 Sheepbed 200 d e b p p b e d breakaway 300 paleoscarp -200 e e h h e e FeHR/FeT S r e w w e r S Stelfox k o Keele 200 o -300 shift r Delthore B o o e L c I c 100 Durkan 100 -400 Stelfox Mountain Aitken (1991) EVOLUTION 0 (this work) Ice -500 Twitya Brook Sekwi Brook Shale Lake 0 Dalrymple & Narbonne (this work) 0.0 0.2 0.4 0.6 0.8 -200 20 40 (1996) o FeHR / FeT δ34S ( /oo CDT) Fig. 1. Fe speciation and S-isotopic data from the Sheepbed Formation and C-isotope data from the Gametrail Formation in the Shale Lake section, Northwest GEOLOGY Territories, Canada. Correlative sections at Stelfox Mountain (32) and Sekwi Brook (26) are shown for reference. Note the shift in FeHR/FeT ratio between 138 and 160 m at Shale Lake. The dashed line separates anoxic deep water at Ͼ0.38 from oxic deep water at Ͻ0.38 (47). Fe speciation data of filled circles were measured by using the method in ref. 47, and the data of open circles were measured by using the method in ref. 52. Formation at two locations at Shale Lake. The first (64°31Ј40ЉN, problems related to faulting and submarine landsliding than with 129°30Ј15ЉW) exposes the basal 60 m of the Sheepbed Formation the slope section at Sekwi Brook (26).