Geology, published online on 19 March 2012 as doi:10.1130/G32807.

The oldest evidence of bioturbation on Earth

Vladimir Rogov, Vasiliy Marusin, Natalia Bykova, Yuriy Goy, Konstantin Nagovitsin, Boris Kochnev, Galina Karlova, and Dmitriy Grazhdankin
Institute of Petroleum Geology and Geophysics, Koptyug Avenue 3, Novosibirsk 630090, Russia ABSTRACT Detailed study of the Khatyspyt Formation in arctic Siberia has shown that, contrary to common expectations, the earliest ichnofabric is of late Ediacaran age, records a food-seeking behavior, and is found in a distal carbonate ramp setting where it co-occurs with fossils of Avalon-type Ediacaran soft-bodied organisms. Preserved depth of bioturbation reaches 5 cm. The ichnofabric solely comprises Nenoxites, the oldest known meniscate trace fossil, which is interpreted as burrows with terminal backll structure formed as a result of active displacement of sediment to form a tunnel within the substrate, followed by emplacement of the material behind the animal as it progressed through the sediment. In addition to being the most reliable paleontological evidence for the existence of bilaterians at ca. 555 Ma, the late Ediacaran bioturbation is regarded as a key step in the escalatory engineering of Phanerozoic ecospace leading to sudden diversication of macroscopic organisms and macrocommunities. INTRODUCTION It is currently assumed that initial colonization of marine infaunal habitats occurred in inner-shelf environments, as opposed to middle- and outer-shelf environments, during the late Terreneuvian (Droser and Bottjer, 1988), and that infaunal activity started in siliciclastic sediments earlier than in carbonate (McIlroy and Logan, 1999; Droser and Li, 2001). Furthermore, it is thought that Ediacaran trace fossils were made close to the sediment surface (Droser et al., 1999, 2002; Jensen, 2003), suggesting that early mobile animals evolved in close proximity to microbial mats (Seilacher, 1999; Gingras et al., 2011). Many workers have argued that predation was a signicant force driving diversication, and some even view it as the primary trigger in the evolution of burrowing behavior (Dzik, 2005). Here we show that the earliest known bioturbation occurs in offshore carbonate settings in late Ediacaran time, and is directed at exploitation of a novel, untapped food source. GEOLOGIC SETTING We documented intensely bioturbated ichnofabric and associated discrete, identiable trace fossils in the Khatyspyt Formation cropping out on the Olenek Uplift in the northeastern part of central Siberia, Republic of Sakha (Yakutiya, Russia). The succession consists of 165 m of nely laminated, thin- to medium-bedded calcitic and dolomitic mudstones and wackestones with thin intercalated volcanic tuff layers deposited in a distal basinal setting (Knoll et al., 1995). The strata are exceptionally fossiliferous and yielded abundant (both numerically and taxonomically) fossils of Ediacaran soft-bodied organisms preserved by authigenic carbonate cementation and as carbonaceous compressions (Grazhdankin et al., 2008). The succession is overlain by the Turkut Formation, which consists of 100 m of microbial laminites, intraclastic and/or oncolitic, ne oolitic dolomitic grainstones and/or packstones, and stromatolitic biostromes. The Turkut strata contain fossils of shelly invertebrates Cambrotubulus decurvatus, of early Cambrian age (Anabarites trisulcatus zone). The Khatyspyt and Turkut Formations are intruded by diatremes consisting of tuff breccia that yielded a U-Pb zircon age of 543.9 0.3 Ma (Bowring et al., 1993; Knoll et al., 1995). The top of the Turkut Formation is marked by a karstic, subaerial exposure surface overlain by uviomarine sandstones (7 m) and laterally discontinuous stratiform bodies of diamictite (up to 37 m) localized around diatremes. Clasts in the diamictite contain tubular fossils C. decurvatus and A. trisulcatus. The uviomarine sandstones, in turn, are overlain by a package (26 m) of wavy-, hummocky-, and convolute-bedded sandstones interstratied with shales, siltstones, and calcitic mudstones. The package contains trace fossils (Treptichnus pedum), small skeletal fossils (Purella antiqua zone) and macrofossils (Sabellidites cambriensis) of early Cambrian (Fortunian) age. Upward the section is succeeded by a unit (70110 m) of alternating shale and siltstone, with laterally discontinuous sandstone and ooid grainstone beds, marked by the rst appearance of arthropod trace fossils Rusophycus avalonensis, macrofossils Platysolenites antiquissimus, and small skeletal fossils of the Tommotian Nochoroicyathus sunnaginicus zone (see the GSA Data Repository1). ICHNOFABRIC Stratigraphic sections of the Khatyspyt Formation were logged for indices of bioturbation (percentage of original sedimentary fabric disrupted by biogenic reworking). The upper member of the Khatyspyt Formation (85 m) consists of packages of nely laminated calcitic mudstones (1525 cm to 2.52.8 m thick) interstratied with units of medium- to coarse-bedded wackestones (0.30.5 m to 2.22.6 m) and intervals of alternating calcitic mudstones and shales (34 cm to 0.10.2 m, occasionally to 0.8 m). The ichnofabric is nearly always developed in nely laminated calcitic mudstones (Fig. 1). Medium- to coarse-bedded calcitic wackestones and intervals of alternating calcitic mudstones and shales remain largely unbioturbated, but contain discrete isolated trace fossils. In addition, the unbioturbated intervals of alternating calcitic mudstones and shales yielded abundant carbonaceous compression macrofossils. Overall, the upper member of the Khatyspyt Formation appears to be moderately to intensely bioturbated. There are two styles of ichnofabric preservation in the Khatyspyt Formation: three-dimensional and compressed. Three-dimensional preservation (Fig. 2; see the Data Repository) is attributed to early diagenetic silicication of discrete sedimentary layers and provides insights into the structure of both individual burrows and the entire ichnocoenosis. Each burrow represents a terminal backll structure that is a result of active displacement of a tunnel within the substrate and emplacement of the material behind the animal as it progressed through the sediment. There is no evidence suggesting wall lining in the tunnels. Branching burrows are not observed. Backll menisci are composed of minimally altered substrate sediment. Intervening menisci consist of early diagenetic microcrystalline silica (with dispersed grains of dolomitic mudstone), which may represent selective replacement of areas with elevated levels of organic matter (Bromley and Ekdale, 1984). In compressed preservation (Fig. 3), the intervening menisci consist of silicied mudstone with dispersed pyrite globules; the color contrast in these menisci can be greatly enhanced by diagenetic processes during fossilization. The appearance of ichnofabric can be signicantly altered by diagenetic overprint. For example, the menisci can be connected to each other by a string of silicied material or pyrite globules. The string could be interpreted as a silicied mucuswalled drain that cuts through the meniscus structure of the backll. In
1 GSA Data Repository item 2012122, composite stratigraphic section and supplementary ichnofabric images, is available online at www.geosociety.org /pubs/ft2012.htm, or on request from editing@geosociety.org or Documents Secretary, GSA, P.O. Box 9140, Boulder, CO 80301, USA.

2012 Geological Society of America. For permission to copy, contact Copyright Permissions, GSA, or editing@geosociety.org. GEOLOGY, May 2012 40; no. 5; p. 14; doi:10.1130/G32807.1; 3 gures; Data Repository item 2012122. Geology, May 2012; v.

Geology, published online on 19 March 2012 as doi:10.1130/G32807.1

48.65 m 0 50 100%

46.03

43.32

39.48 37.24 34.91 T T T T T T T T T T T 25.06 T T

75-100%

31.95

A
Si + O
50-75%

Ca + Mg
20.12 18.94 T

25-50%
10.72 9.87 T 6.58

Figure 2. Three-dimensional preservation of the ichnofabric in nely laminated silicied calcitic mudstones of Khatyspyt Formation (arctic Siberia). A and B: Vertical cross section of a sedimentary layer with ichnofabric (A) and undisrupted original sedimentary fabric preserved in the lowermost part of the layer (B). C: Elemental mapping of meniscate backll of a burrow. Scale bars: A, B = 10 mm; C = 1 mm.

2.83

0.00

0-25%

Figure 1. Bioturbation index in a logged section of the Khatyspyt Formation (Tvolcanic tuff beds) and representative examples of the ichnofabric. Scale bar: 5 mm.

other specimens, the original saucer-like shape of the menisci has been exaggerated and transformed beyond recognition, or the entire burrow is surrounded by a halo of microcrystalline quartz (Fig. 3). Burrows are sinuous, unbranching, and have a width 0.53.0 mm, with the maximum reaching 6.5 mm. The maximum depth of bioturbation was 5 cm, measured from silicied sedimentary layers, which were subject to minimum sediment compaction. The lowest stratigraphic occurrence of the ichnofabric is at the base of the Khatyspyt Formation 185 m below the rst appearance of C. decurvatus and 335 m below T. pedum. Apart from the Olenek Uplift, the meniscate trace fossil Nenoxites is also known from the Ust-Yudoma Formation cropping out along the Yudoma River of eastern Siberia from the stratigraphic interval ~140 m below the Ediacaran skeletal fossil Cloudina and ~230 m below the lowest occurrence of early Cambrian small skeletal fossils (P. antiqua zone) (Zhuravlev et al., 2009). The correlative

GEOLOGY, May 2012

Geology, published online on 19 March 2012 as doi:10.1130/G32807.1 The ichnofabric can be misinterpreted as body fossils. Despite an apparent similarity with coquina (Fig. 2), the structure never is preserved as a lag deposit nor shows any graded bedding; quite the opposite, it becomes less dense with depth of the sediment and clearly disturbs the primary thin lamination (Fig. 2B). Furthermore, the structure was not resistant to erosion during subsequent sediment deposition, which makes it unlikely to be fragmented parts of body fossils. Occasional vertical escape burrows can be seen in the structure. The meniscate trace fossils may have been widely distributed in late Ediacaran rocks. For example, the process of meniscate backlling better explains the nature of Ediacaran macrofossils Helanoichnus helanensis, Shaanxilithes ningqiangensis, Palaeopascichnus minimus, P. meniscatus, and P. jiumenensis from China (Shen et al., 2007; Dong et al., 2008), which all appear to be remarkably similar to the various taphonomically controlled morphologies of the trace fossil Nenoxites from the Khatyspyt Formation (Fig. 3). In fact, the possibility of some of these macrofossils being ichnofossils was considered but rejected in the recent study by Shen et al. (2007). The advent of bioturbation in the geological record coincides with the earliest diversication and ecological differentiation in macrocommunities. Prior to the advent of bioturbation, macrocommunities consisted of rangeomorphs and frondomorphs and were restricted to low-energy distal shelves, if not continental slopes. The appearance of Nenoxites ichnofabric in the low-energy shelf at 555 Ma is almost synchronized with the drop in rangeomorph diversity, expansion of macrocommunities into wave- and current-agitated prodelta and distributary channel systems, the sudden appearance of dickinsoniomorphs, tribrachiomorphs, and bilateromorphs (Grazhdankin, 2004), and an increase in size of macrophytes (up to 3 m in length and 0.15 m in width) (Grazhdankin et al., 2007, 2008; Marusin et al., 2011). These macroevolutionary innovations cannot be coincidental (Buttereld, 2011) and are interpreted as a direct expression of biotope engineering by eumetazoans. Bioturbation in modern seaoor habitats affects key ecosystem processes in marine sediments, including microbial abundances and activities, remineralization of organic matter, nutrient cycling, and biogeochemical interactions (Aller, 1994; Ziebis et al., 1996; Lohrer et al., 2004; Glud, 2008). The rst appearance and expansion of bioturbation in the late Ediacaran, therefore, must have had a profound effect on ecosystem structure and functioning (Seilacher and Pger, 1994). It has long been accepted that infaunal habit evolved concurrently with the origin of Bilateria, but the triggering mechanism remained unclear. Dzik (2005) argues that trace fossils from the VendianCambrian transition represent shelters of infaunal animals feeding from the sediment surface, and that infaunal habit evolved as a protective measure against predators. Several features of the Khatyspyt ichnofabric (absence of fecal material, avoidance of earlier self-made trails) suggest that the organism actively burrowed by peristalsis without processing sediment through the gut. The most likely purpose of borrowing was search for food. Organism-sediment interaction, therefore, started as exploration of new food resources, and not as sheltering from evolved predators. It is important that the oldest bioturbation is restricted to muddy sediment: recent developments in sediment mechanics indicate that burrowing in mud requires far less energy than does burrowing between sand grains (Dorgan et al., 2005), and there is normally more food resource in mud (Gingras et al., 1999). Whether or not Ediacaran macrofossils are related to the metazoan lineages that dene the Phanerozoic, the Nenoxites ichnofabric is of bilaterian origin and represents the rst ecologically successful exploitation of burrowing and sediment-mixing behavior. Certainly some aspects of Ediacaran life were transitory, but bioturbation arguably constitutes the key step in the escalatory engineering of Phanerozoic ecospace.

A C D E

Figure 3. Taphonomic variation of the meniscate backll structure in calcitic mudstones of Khatyspyt Formation (arctic Siberia). A, D and F: Shaanxilithes-type morphology. B: Horodyskia-type morphology. C: Helanoichnus-type morphology. E: Palaeopascichnus-type morphology. Scale bars: A, C, E = 10 mm; B, D, F = 5 mm.

strata of the Ust-Yudoma Formation yielded a Pb-Pb isochron date of 553 23 (2) Ma (Semikhatov et al., 2003). All evidence conrms that the Khatyspyt ichnofabric is of late Ediacaran age, and thus the oldest reliable paleontological evidence of bioturbation. DISCUSSION The trace fossil Nenoxites is identied as the sole contributor to the ichnofabric in the Khatyspyt Formation. It is also the oldest known meniscate trace fossil. The type ichnospecies Nenoxites curvus was originally described from the southeastern White Sea area as a horizontal trace fossil formed by peristaltic motion (Fedonkin, 1976). The age of Nenoxites is constrained by a tuff at the base of the Verkhovka Formation with a U-Pb zircon date of 558 1 Ma (Grazhdankin, 2004). Compared to essentially horizontal meandering trails from the White Sea area, the specimens of Nenoxites from the Olenek Uplift have a pronounced vertical component of movement. Although a cnidarian-like organism crawling across the sediment surface is capable of producing a simple horizontal trail with concave-forward hemispherical structures (Liu et al., 2010), the Khatyspyt ichnofabric could only have been produced by a bilaterian. Much of the early fossil record of bilaterian evolution comes from the late Ediacaran; however, fossils from this period are highly controversial, including the earliest generally accepted bilaterian, Kimberella, at 555 Ma (Martin et al., 2000). The Nenoxites ichnofabric, therefore, represents the most reliable paleontological evidence for the existence of triploblastic Eumetazoa at ca. 555 Ma.

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Geology, published online on 19 March 2012 as doi:10.1130/G32807.1

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Manuscript received 6 September 2011 Revised manuscript received 20 November 2011 Manuscript accepted 28 November 2011 Printed in USA

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