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Calibrating the Coevolution of Ediacaran Life and Environment Calibrating the coevolution of Ediacaran life and environment Alan D. Rooneya,1, Marjorie D. Cantineb,1, Kristin D. Bergmannb, Irene Gómez-Pérezc, Badar Al Baloushic, Thomas H. Boagd, James F. Busche, Erik A. Sperlingd, and Justin V. Strausse aDepartment of Earth and Planetary Sciences, Yale University, New Haven, CT 06520; bDepartment of Earth, Atmospheric, and Planetary Sciences, Massachusetts Institute of Technology, Cambridge, MA 02139; cPetroleum Development Oman, Exploration Directorate, Muscat 100, Oman; dDepartment of Geological Sciences, Stanford University, Stanford, CA 94305; and eDepartment of Earth Sciences, Dartmouth College, Hanover, NH 03755 Edited by Paul F. Hoffman, University of Victoria, Victoria, BC, Canada, and approved June 1, 2020 (received for review February 15, 2020) The rise of animals occurred during an interval of Earth history that White Sea assemblage includes more complex and mobile taxa such as witnessed dynamic marine redox conditions, potentially rapid plate Dickinsonia and the bilaterian Kimberella and largely occurs in marine motions, and uniquely large perturbations to global biogeochemical subtidal to intertidal shelf settings (26). Finally, the terminal Ediacaran cycles. The largest of these perturbations, the Shuram carbon Nama assemblage is highly depauperate and dominated by early bilat- isotope excursion, has been invoked as a driving mechanism for erian trace fossils, tubiculous fauna, and the earliest biomineralizing Ediacaran environmental change, possibly linked with evolutionary animals, all of which occur in a variety of shallow-marine carbonate and innovation or extinction. However, there are a number of contro- siliciclastic environments (27). Although these assemblages appear to versies surrounding the Shuram, including its timing, duration, and hold up across Ediacaran paleocontinents, the fundamental lack of role in the concomitant biological and biogeochemical upheavals. Ediacaran geochronological constraints has precluded linking biotic Here we present radioisotopic dates bracketing the Shuram on two turnover to key tectonic or biogeochemical perturbations, such as the separate paleocontinents; our results are consistent with a global Shuram CIE (28, 29). and synchronous event between 574.0 ± 4.7 and 567.3 ± 3.0 Ma. In the absence of a reliable chronology, two age models for the These dates support the interpretation that the Shuram is a primary Shuram CIE and its relationship to Ediacaran geoevents and bio- and synchronous event postdating the Gaskiers glaciation. In addi- events have emerged (28). Both presume the termination occurs tion, our Re-Os ages suggest that the appearance of Ediacaran mac- circa 550 Ma, an assumption informed by an ash dated to 551.1 ± 0.7 rofossils in northwestern Canada is identical, within uncertainty, to Ma above the Shuram CIE in the Doushantuo Formation of South similar macrofossils from the Conception Group of Newfoundland, China (30), and which puts the CIE in association with a purported highlighting the coeval appearance of macroscopic metazoans extinction of the White Sea assemblage (18, 19). Critically, however, across two paleocontinents. Our temporal framework for the termi- these models differ in placing the onset of the Shuram CIE at circa nal Proterozoic is a critical step for testing hypotheses related to 580 Ma (thus potentially linked with the Gaskiers glaciation; ref. 17) extreme carbon isotope excursions and their role in the evolution versus circa 560 Ma. As a result, estimates for the duration of the of complex life. excursion range from <10 to ∼30 My, highlighting an ambiguity in current Ediacaran chronologies that makes it impossible to confi- Neoproterozoic | Shuram | Re-Os geochronology | Ediacaran | carbon dently link the Shuram CIE to global biogeochemical cycles or the isotopes radiation or extinction of soft-bodied Ediacaran fossils. n addition to recording the radiation of animals (1), extreme Significance Iclimate events (2), oscillating global redox conditions (3–5), and geomagnetic instability that could be linked to rapid plate Our understanding of the interactions between animal evolu- motion (6, 7), Neoproterozoic rocks host Earth’s most negative tion, biogeochemical cycling, and global tectonics during the carbon isotope excursions (CIEs) (8). These CIEs have been Ediacaran Period (635 to 541 Ma) is severely hampered by lack interpreted to record perturbations to the global carbon cycle of of a robust temporal framework. The appearance and extinc- a magnitude unlike any recorded before or since (9). The largest tion of the earliest fossil animals are hypothesized to correlate among them, the Shuram CIE is globally represented by an with upheavals in biogeochemical cycles—foremost the abrupt ∼17‰ drop from enriched carbonate carbon isotope Shuram carbon isotope excursion, possibly the largest known 13 (δ Ccarb) values to highly depleted values of −12‰, before disturbance to the global carbon cycle. However, without age slowly recovering to a less enriched background state (10) constraints on the excursion’s timing and duration, its driving (Fig. 1). Despite being recorded across more than six paleo- mechanisms, global synchroneity, and role in Ediacaran geo- continents and a variety of depositional settings, the Shuram CIE biological evolution cannot be evaluated. We provide radio- has remained one of the most enigmatic geochemical events of isotopic ages for the onset and termination of the Shuram, the Proterozoic Eon, with three key controversies surrounding evaluate its global synchroneity, and show that it is divorced this event: 1) its onset and duration (11, 12); 2) its primary or from the rise of the earliest preserved animal ecosystems. diagenetic origin (13–15); and 3) its temporal proximity and causal relationship to marine redox fluctuations, glaciation, and Author contributions: A.D.R., K.D.B., and J.V.S. designed research; A.D.R., M.D.C., I.G.-P., the evolution and/or extinction of the Ediacaran biota (16–20). B.A.B., T.H.B., J.F.B., E.A.S., and J.V.S. performed research; I.G.-P. contributed new re- Statistical analyses indicate that Ediacaran macrofossils can be agents/analytic tools; A.D.R., M.D.C., I.G.-P., B.A.B., J.F.B., and J.V.S. analyzed data; and A.D.R., M.D.C., and K.D.B. wrote the paper with contributions from all authors. assigned into three distinct recurrent taxonomic associations, termed assemblages, that may reflect successive episodes of biotic turnover (23, The authors declare no competing interest. 24). The rise and fall of Ediacaran assemblages is not well constrained This article is a PNAS Direct Submission. geochronologically, and the apparent appearances and disappearances Published under the PNAS license. of these assemblages may also be subject to potential paleoenvir- 1To whom correspondence may be addressed. Email: [email protected] or mcantine@ onmental biases. The earliest Avalon assemblage, which consists almost mit.edu. exclusively of fossils preserved in marine slope and basinal depositional This article contains supporting information online at https://www.pnas.org/lookup/suppl/ environments, is dominated by large fractal organisms (termed fronds) doi:10.1073/pnas.2002918117/-/DCSupplemental. and possible sponges and cnidarians (25). The younger, more diverse First published July 6, 2020. 16824–16830 | PNAS | July 21, 2020 | vol. 117 | no. 29 www.pnas.org/cgi/doi/10.1073/pnas.2002918117 Downloaded by guest on September 28, 2021 EARTH, ATMOSPHERIC, AND PLANETARY SCIENCES Fig. 1. Simplified stratigraphy and chemostratigraphy of Ediacaran sedimentary rocks in northwestern Canada and Oman. Sampled horizons indicated with stars and compilation of carbon isotope data are in SI Appendix, Table S1. Previously published geochronological constraints are from U-Pb zircon ages on ash beds (21) and Re-Os ages on organic-rich sedimentary rocks (22). Fm, Formation. Developing a high-resolution chronology for the Shuram CIE has by multiple drill cores in the South Oman Salt Basin and Huqf– proven difficult as Ediacaran fossil assemblages only have broad Haushi High areas (SI Appendix, Fig. S1). In the subsurface and in assemblage-scale biostratigraphic utility and previous radioisotopi- outcrops of the Huqf Desert, the Nafun Group has not undergone cally dated horizons only have provided loose constraints on the significant metamorphism or deformation, and its sedimentology, Shuram CIE’s termination (21, 30). Moreover, chemostratigraphic stratigraphy, and geochemistry has been extensively studied (32–39). correlations of well-dated fossiliferous Ediacaran successions, such Radioisotopic constraints on the Nafun Group are limited to mini- as the Conception Group of Newfoundland (17) or the Charnian mum depositional ages derived from detrital zircons (21, 40), al- Supergroup of the United Kingdom (31), are not possible due to the though extensive dating of volcaniclastic and ash units in the paucity of carbonate sedimentation in those basins. Here, we present overlying Ara Group and Fara Formation have yielded latest Edia- a high-resolution chronology for the Shuram CIE with five rhenium- caran ages (21). The Khufai Formation of the Nafun Group is predominantly osmium (Re-Os) dates from mixed carbonate and siliciclastic sedi- carbonate and lies stratigraphically above a Cryogenian (circa 635 mentary rocks bracketing the excursion on two different paleo- Ma) Marinoan diamictite and cap carbonate succession. The onset continents (Figs. 1 and 2). To develop this age
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