LETTERS PUBLISHED ONLINE: 28 SEPTEMBER 2015 | DOI: 10.1038/NGEO2537 Protracted development of bioturbation through the early Palaeozoic Era Lidya G. Tarhan1,2*, Mary L. Droser2, Noah J. Planavsky1 and David T. Johnston3 Bioturbation, the physical and chemical mixing of sediment the basis of facies, fauna and palaeogeographic reconstruction, by burrowing animals, exerts an important control on the to represent deposition under shallow oxygenated marine waters. character of modern marine sediments and biogeochemical Sedimentological, ichnological and taphonomic data were collected cycling1–9. Here we show that the mixing of sediments on from >700 m of section, comprising >40,200 discrete beds, to marine shelves remained limited until at least the late Silurian, determine the extent of biogenic sediment mixing typical of early 120 million years after the Precambrian–Cambrian transition. Palaeozoic marine shelfal environments. We present ichnological, stratigraphic and taphonomic data To track mixing intensity we evaluated the rock record according from a range of lower Phanerozoic siliciclastic successions to six criteria: bedding thickness; depth of bioturbation; biogenic spanning four palaeocontinents. The protracted development fabric disruption; fidelity of trace fossil preservation (that is, of the sediment mixed layer is also consistent with sulphur bioglyphic preservation); complexity of trace fossil assemblages data and global sulphur model simulations. The slow increase and abundance of surficially produced physical sedimentary in the intensity of bioturbation in the sediment record structures. Although these metrics are related, they each provide suggests that evolutionary advances in sediment colonization unique information concerning substrate consistency, infaunal outpaced advances in sediment mixing. We conclude that behaviour and the extent of seafloor sediment mixing (see ecosystem restructuring caused by the onset of significant Methods and Supplementary Information). The resulting suite infaunal mobile deposit feeding (‘bulldozing’) occurred well of Cambrian–Silurian data represents the most high-resolution, after both the Cambrian Explosion and the Great Ordovician stratigraphically and sedimentologically constrained and spatially Biodiversification Event. and temporally representative database for this time interval. The modern seafloor and the majority of the Phanerozoic Data were grouped into three chronological intervals: lower– stratigraphic record are characterized by biogenically reworked, middle Cambrian (∼542–507 Myr ago (Ma)), Cambro-Ordovician well-churned sediment7–10. In modern oceans the `mixed layer,' the (∼500–458 Ma) and Ordovician–Silurian (∼450–420 Ma). zone of sediment which has been homogenized and fluidized by the Lower–middle Cambrian strata (Fig.1 a–d; see ref. 11 for activity of bioturbating organisms, extends to a depth of ∼10 cm further details) are characterized by thin coherent beds (mm- to below the sediment–water interface4–9. This extensive sediment cm-scale; mean sandstone bed thickness D 1.3 cm (Fig.2 )) and mixing, which is responsible for heightened nutrient cycling and well-preserved conformable bed junctions, without evidence for the deep and widespread oxidation of the sediment pile, shapes significant exhumation (for example, scouring, rip-ups, truncated the ecological and biogeochemical character of the seafloor1–3. burrows). Trace fossils are abundant along bed bases and burrows However, the geologic timing of the development of the mixed are most commonly preserved as passively infilled casts rather than layer has not been well constrained11. Previous attempts to track the bed-penetrative intra-bed structures. `Floating' mm-scale burrows, global development of sediment mixing (for example, ref. 12) have infilled by means of bypass sedimentation, are common. Maximum largely not employed a stratigraphically continuous, field-based burrow depth is typically on the mm scale and, excepting piperock and facies-controlled approach, have focused on infaunalization (see Supplementary Information), never exceeds 3 cm. Millimetre- rather than mixed layer development or have lacked sufficient scale tool marks are common and occur densely. Trace fossil geographic or temporal coverage (see Supplementary Information). preservation is of a very high fidelity; discrete shallowly emplaced As a result, the influence of bioturbation on ecosystem structuring and surficial traces are sharply preserved; bioglyphs such as scratch and the evolution of global biogeochemical cycling remains marks and appendage imprints occur frequently, even where poorly quantified. Here we provide a new and stratigraphically assemblage density approaches the highest levels of bedding plane constrained, global and multiproxy record of the early development surface coverage (bedding plane bioturbation index15 [BPBI] 4–5). of sediment mixing. However, in spite of the dense colonization of bedding planes, Bioturbation data were collected from lowermost Cambrian stratigraphic fabrics—that is, the extent of disruption of depositional through upper Silurian heterolithic siliciclastic shallow marine fabrics by burrowing (measured by ichnofabric index [ii], with successions worldwide (Supplementary Fig. 1). Siliciclastic sediment ii 1 denoting laminated and ii 6 completely homogenized16)— and strata represent the vast majority of the modern seafloor and are characterized by an almost complete lack of disruption. The the stratigraphic record (for example, ref. 13), and shallow marine most disrupted intervals are characterized by a maximum ii of 3, settings are the site of the majority of marine biogeochemical cycling but these zones of disruption are commonly confined to very (80–90% organic matter remineralization14). Data were collected limited spatial scales (mm to cm); average sample- and bed-scale from 22 units (see Supplementary Information) determined, on ichnofabrics rarely exceed ii 2 (sample-averaged mean ii D 2.1; 1Department of Geology and Geophysics, Yale University, 210 Whitney Ave, New Haven, Connecticut 06511, USA. 2Department of Earth Sciences, University of California-Riverside, 900 University Ave, Riverside, California 92521, USA. 3Department of Earth and Planetary Sciences, Harvard University, 20 Oxford St., Cambridge, Massachusetts 02138, USA. *e-mail: [email protected] NATURE GEOSCIENCE | VOL 8 | NOVEMBER 2015 | www.nature.com/naturegeoscience 865 © 2015 Macmillan Publishers Limited. All rights reserved LETTERS NATURE GEOSCIENCE DOI: 10.1038/NGEO2537 a ei b fj c gk dhl Figure 1 | Lower Palaeozoic trace fossil preservation and ichnofabrics. Characteristic bioglyphically preserved trace fossil assemblages and poorly developed bioturbational fabrics of lower–middle Cambrian (a–d), Cambro-Ordovician (e–h) and Ordovician–Silurian (i–l) heterolithic siliciclastic successions. a,e,i, Characteristic style of bedding for each temporal interval. b, Treptichnus (UEXP853Gu1:004). c, Dense assemblage of intergradational Rusophycus and Cruziana (UCR 11140/1). d, Lower–middle Cambrian ichnofabric, ii 2 (YPM-IP.237260). f, Bioglyphically preserved arthropodal scratch marks and tool marks. g, Dense assemblage of high-relief and bioglyphically preserved treptichnids, Cruziana and other shallow-tier trace fossils. h, Cambro-Ordovician ichnofabric, ii 2 (UCR 11135/3). j, Dense and bioglyphic assemblage of Arthrophycus. k, Bioglyphically preserved Rusophycus of nearly dm-scale diameter (YPM-IP.237261). l, Ordovician–Silurian ichnofabric, ii 3 (YPM-IP.237262). b,c,f,g,j,k, Hyporelief. Scale bars, 1 cm. Field photographs unless otherwise noted. Specimens from Chapel Island Formation (a), Torreárboles Sandstone (b), Pioche Formation (c,d), Beach Formation (e,h), Powers Steps Formation (f,g), Tuscarora Formation (i), Clinch Formation (j), Juniata Formation (k), Miintown Formation (l). Fig.3 ) and zones of ii 1 are common within individual samples fidelity of preservation of discrete and high-relief shallowly and stratigraphic intervals. Moreover, ichnofabrics are typically emplaced structures; bioglyphs are common even where dominated by sub-mm- to mm-scale `microburrows' (meiofauna- assemblages are dense (up to BPBI 5) or multi-generational. scale cryptobioturbation) cast on the bases of sub-mm- to mm-scale In spite of the density and large size of Cambro-Ordovician laminae, without significant disruption to the overall laminated trace fossils, ichnofabrics are poorly developed (sample-averaged fabric of the rock; large, fabric-disruptive burrows are rare. mean ii D 2.4; Fig.3 ). Although Cambro-Ordovician strata rarely Cambro-Ordovician strata (Fig.1 e–h; see ref. 17 for further attain a maximum ii of 5, these more intensely disrupted zones details) are also characterized by thin, coherent beds (mm- are commonly either of limited scale (not representative of a to cm-scale; mean sandstone bed thickness D 3.4 cm (Fig.2 )) bed or stratigraphic interval) or consist largely of sub-mm-scale separated by well-defined and commonly non-erosive junctions. cryptobioturbation or mm-scale macroburrows. Delicate (mm- to cm-scale length, sub-mm- to mm-scale width) Ordovician–Silurian strata (Fig.1 i–l) are also characterized by tool marks are common. Trace fossils occur abundantly along bed thin (mm- to cm-scale; mean sandstone bed thickness D 3.1 cm junctions and are notably larger (cm-scale; up to 10 cm diameter, (Fig.2 )), coherent and largely conformable beds. Ordovician– 30 cm length and 5.5 cm depth), on average, than those