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Biotic Replacement and Mass Extinction of the Ediacara Biota

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Biotic Replacement and Mass Extinction of the Ediacara Biota Downloaded from http://rspb.royalsocietypublishing.org/ on September 9, 2015 Biotic replacement and mass extinction of rspb.royalsocietypublishing.org the Ediacara biota Simon A. F. Darroch1,2, Erik A. Sperling3,4, Thomas H. Boag5, Rachel A. Racicot6, Sara J. Mason5, Alex S. Morgan3, Sarah Tweedt1,7, Research Paul Myrow8, David T. Johnston3, Douglas H. Erwin1 and Marc Laflamme5 1 Cite this article: Darroch SAF et al. 2015 Smithsonian Institution, PO Box 37012, MRC 121, Washington, DC 20013-7012, USA 2Department of Earth and Environmental Sciences, Vanderbilt University, 2301 Vanderbilt Place, Nashville, Biotic replacement and mass extinction of the TN 37235-1805, USA Ediacara biota. Proc. R. Soc. B 282: 20151003. 3Department of Earth and Planetary Sciences, Harvard University, 20 Oxford Street, Cambridge, MA 02138, USA http://dx.doi.org/10.1098/rspb.2015.1003 4Department of Geological Sciences, Stanford University, 450 Serra Mall Bldg. 320, Stanford, CA 94305, USA 5Department of Chemical and Physical Sciences, University of Toronto Mississauga, 3356 Mississauga Road, Ontario, Canada L5 L 1C6 6Department of Biology, Howard University, 415 College Street NW, Washington, DC 20059, USA 7Department of Behavior, Ecology, Evolution & Systematics, University of Maryland, College Park, Received: 28 April 2015 MD 20742, USA Accepted: 4 August 2015 8Geology Department, Colorado College, 14 E. Cache La Poudre, Colorado Springs, CO 80903, USA The latest Neoproterozoic extinction of the Ediacara biota has been variously attributed to catastrophic removal by perturbations to global geochemical cycles, ‘biotic replacement’ by Cambrian-type ecosystem engineers, and a tapho- Subject Areas: nomic artefact. We perform the first critical test of the ‘biotic replacement’ ecology, evolution, palaeontology hypothesis using combined palaeoecological and geochemical data collected from the youngest Ediacaran strata in southern Namibia. We find that, even Keywords: after accounting for a variety of potential sampling and taphonomic biases, the Ediacaran, Cambrian, extinction, ecology, Ediacaran assemblage preserved at Farm Swartpunt has significantly lower diversity, ecosystem engineers genus richness than older assemblages. Geochemical and sedimentological ana- lyses confirm an oxygenated and non-restricted palaeoenvironment for fossil- bearing sediments, thus suggesting that oxygen stress and/or hypersalinity are unlikely to be responsible for the low diversity of communities preserved at Author for correspondence: Swartpunt. These combined analyses suggest depauperate communities charac- Simon A. F. Darroch terized the latest Ediacaran and provide the first quantitative support for the biotic e-mail: [email protected] replacement model for the end of the Ediacara biota. Although more sites (especially those recording different palaeoenvironments) are undoubtedly needed, this study provides the first quantitative palaeoecological evidence to suggest that evolutionary innovation, ecosystem engineering and biological inter- actions may have ultimately caused the first mass extinction of complex life. 1. Introduction The terminal Neoproterozoic (Ediacaran: 635–541 Ma) Ediacara biota was an enigmatic assemblage of large, morphologically complex eukaryotes that rep- resent the first major radiation of multicellular life. The biological affinities of these organisms have been much debated, but recent work suggests they rep- resent a mixture of stem- and crown-group animals, as well as extinct higher order clades with no modern representatives [1–3]. With the exception of a few isolated occurrences [4,5], Ediacara-type fossils are absent from Cambrian and younger strata. Three competing hypotheses have been proposed to explain their disappearance around the Ediacaran–Cambrian boundary [6]: (1) a ‘cata- strophic’ extinction event precipitated by perturbations to global geochemical cycles in the terminal Ediacaran [7–12]; (2) the result of ‘biotic replacement’, whereby members (or precursors) of the Cambrian evolutionary fauna gradually Electronic supplementary material is available outcompeted Ediacaran biotas through ecological engineering of Ediacaran at http://dx.doi.org/10.1098/rspb.2015.1003 or ecosystems [6,13]; and (3) a taphonomic artefact, whereby the conditions requi- red for Ediacaran preservation disappeared at the Ediacaran–Cambrian via http://rspb.royalsocietypublishing.org. boundary [6]. This third model has been convincingly rejected [12], however, & 2015 The Author(s) Published by the Royal Society. All rights reserved. Downloaded from http://rspb.royalsocietypublishing.org/ on September 9, 2015 few studies have attempted to directly test predictions sample-standardization from original field data, as opposed to 2 stemming from the two more plausible models. global compilations of taxa. We therefore undertook an intensive rspb.royalsocietypublishing.org The ‘biotic replacement’ model implies a gradual palaeo- survey of the latest Ediacaran fossil-bearing horizons preserved ecological change through the Ediacaran, and therefore makes on Farm Swartpunt and performed rarefaction analyses to inves- two predictions: (1) latest Ediacaran assemblages should be tigate richness estimates at a range of sampling intensities. We ecologically and taxonomically depauperate when compared recovered 106 individual fossils from the surveyed area, both in to those in older assemblages; and (2) evidence for ecosystem place and as float specimens (from numerous horizons—see elec- engineering, such as bioturbation, should be more abundant tronic supplementary material, S2 and S3), 79 of which were in terminal Ediacaran sections. In this model, the extinction readily attributable to known Ediacaran taxa (complete dataset event is protracted and begins earlier in the Ediacaran with given in electronic supplementary material, S4). In addition to the first appearance of metazoan ecosystem engineers. Abun- Swartpuntia and Pteridinium,werecoverednumerousAspidella, dant evidence supporting the second prediction of the ‘biotic an erniettomorph taxon provisionally assigned to Ernietta,and Proc. R. Soc. B replacement’ model is provided by the relatively high diversity a rangeomorph form provisionally assigned to Bradgatia (elec- of metazoan traces in the uppermost Ediacaran and lowermost tronic supplementary material, S5). At least one of our Aspidella Cambrian rocks [6,14–16], however, the first prediction of this specimens preserves the trace of a segmented stem structure model has yet to be critically examined. In this study, we test readily attributable to Swartpuntia (electronic supplementary 282 the first prediction of the ‘biotic replacement’ model. We per- material, S5). Of the 79 identifiable fossil specimens, 28 were form palaeoecological analyses of the latest Ediacaran (‘Nama’ found in place on the top surface of one stratigraphic horizon : 20151003 assemblage: approx. 545–542 Ma) fossil localities preserved in (‘Bed 1’—see electronic supplementary material, S2), allowing Farm Swartpunt, southern Namibia, and compare the resulting single bed comparisons with other datasets. diversity indices with older Ediacaran assemblages worldwide, In order to test whether these latest Ediacaran assemblages which form a time series through the Mid- to End-Ediacaran. are relatively depauperate, we performed the same analyses Discovery of lower species richness and evenness in terminal on three older Ediacaran assemblages, from Mistaken Point, Ediacara fossil assemblages would support the predictions of Newfoundland (‘Avalon’ assemblage, dating between approx. the ‘biotic replacement’ hypothesis. Alternatively, finding 579 and approx. 565 Ma and comprising eight fossiliferous sur- equivalent richness and diversity metrics relative to older faces, using data from [30]), Nilpena, South Australia (‘White assemblages would instead support the ‘catastrophe’ hypo- Sea’ assemblage, between approx. 555–550 Ma, comprising thesis and suggest that Edicaran ecosystems suffered abrupt five facies associations, using data from [31]), and the White extinction at the Ediacaran–Cambrian boundary. Sea, Russia (‘White Sea’ assemblage, using data from [32]). The fossil-bearing horizons at Farm Swartpunt are part of Locality summaries are given in electronic supplementary the latest Ediacaran Nama Group, Urusis Formation (Spits- material, S6. Richness estimates from fossil data can be heavily kopf Member), of southern Namibia (figure 1). The Nama influenced by stratigraphic (i.e. counted from in situ populations Group records mixed siliciclastic–carbonate sedimentation on a single bedding plane, versus collected from loose material into a foreland basin related to convergence along the and therefore likely aggregated over several fossiliferous hor- Damara and Gariep deformational belts and was deposited izons), and taphonomic (i.e. two-dimensional versus three- into two sub-basins separated by the palaeo-topographic dimensional preservation) contexts. We therefore performed high of the Osis Arch [17,19–21]. Farm Swartpunt belongs additional comparisons after adjusting the Mistaken Point, Nil- to the southernmost of these two basins—the Witputs sub- pena and White Sea datasets to account for these differences, basin—and preserves rocks that regionally dip approximately and thus form more realistic comparisons with our dataset 18 to the west. An ash bed in the lower carbonate package of from Swartpunt. In terms of stratigraphic context, we aggregated the Urusis Formation has been
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