the tommotian phase of the early cambrian agronomic revolution in the carbonate mud environment of...

The Tommotian phase of the Early Cambrian AgronomicRevolution in the carbonate mud environment of centralSiberia

DAWID MAZUREK

Mazurek, D. 2013: The Tommotian phase of the Early Cambrian AgronomicRevolution in the carbonate mud environment of central Siberia. Lethaia, DOI:10.1111/let.12045.

The profound ecological change of the marine benthos that eventually led to thealmost complete destruction of the Precambrian matgrounds by benthic grazers andbioturbators (the agronomic revolution) was largely completed in the Tommotian. Atthat time, burrows produced by bottom-dwelling animals as shelters against predatorswere supplemented by burrowing for food by predators and sediment feeders. Thelimy mud ichnofauna of that age in Siberia was very different from the roughly coevalsand bottom faunas of Baltica. Although the exact zoological identity of the animalsforming the infaunal Tommotian traces remains unknown, they probably mostly rep-resent various kinds of early nemathelminthes. No apparent locomotion traces of mol-lusc origin have been encountered in the Early Cambrian, despite the abundantoccurrence of skeletal fossils attributed to molluscs. Possibly the standard muscularfoot, typical of modern molluscs, had not yet developed. Ichnotaxa represented areTeichichnus isp., Rhizocorallium isp., Chondrites isp., possibly the Buren ichnocomplexand others. □ Agronomic revolution, Cambrian explosion, infauna, Mollusca,Nemathelminthes.

Dawid Mazurek [[email protected]], Instytut Paleobiologii PAN, Twarda51/55 00-818 Warsaw, Poland; manuscript received on 18/10/2012; manuscript acceptedon 15/08/2013.

The Ediacaran–Cambrian boundary witnessed a pro-found ecological change of the marine benthos. TheCambrian revolution began near the end of the Edi-acaran, presumably with the macroscopic predatorpressure rise that forced some animals to develop aninfaunal style of life or skeletal shields on the bodiesnaked thus far (the Verdun Syndrome of Dzik 2005,2007). Much later, probably in the late Tommotian(for different opinion see Rogov et al. 2012), someof the infaunal worms gradually changed from sur-face detritus feeding to mud deposit feeding. Even-tually, enhanced level of organization, increaseddiversity of the fauna and size of animals led to thealmost complete destruction of the Precambrianmatgrounds by benthic grazers and bioturbators(the agronomic revolution of Seilacher 1999).Through the Early Palaeozoic, this ecological turn-over resulted in the formation of the mixed layer insoft marine sediments – soupy strata with a highwater content, being permanently bioturbated (theCambrian substrate revolution of Bottjer et al.2000). These events obviously resulted from a pro-found evolutionary change in the anatomy andmode of life of benthic animals, the transition onwhich data are still very incomplete. Moreover,although molecular clocks locates the origin of mostmajor groups to the relatively short time of the

Ediacaran and Cambrian, a contribution of ecologi-cal, geochemical, taphonomic and other factors tothe phenomenon of the ‘Cambrian explosion’ is pos-sible (e.g. Dzik 1994; Erwin et al. 2011; Kouchinskyet al. 2012). These could bias the fossil record andpresumably impact our views on the timing of manyevolutionary events visualizing the ‘Cambrian explo-sion’ as a more rapid event than it was in reality.

Most of the evidence on transformation of mar-ine environments and biota near the Ediacaran–Cambrian boundary comes from the skeletal fossilrecord. However, only a small fraction of the latestEdiacaran and Early Cambrian organisms had amineral skeleton – a feature dramatically increasingtheir chance for fossilization. Our knowledge ofrepresentatives of many phyla is restricted to theexceptional preservation of the fine-clastic BurgessShale-type environments. The carbonate mud envi-ronment, from which most of the skeletonized earlymetazoans are known, is mostly devoid of fossils ofsoft-bodied organisms.

Traces of activity left in ancient sediments by theearliest animals significantly supplement scarce evi-dence of the initial stages of diversification of animalphyla provided by body fossils (Droser et al. 2002a,b; Jensen 2003; Jensen et al. 2005; Seilacher et al.2005). The majority of studies on Cambrian trace

DOI 10.1111/let.12045 © 2013 The Authors, Lethaia © 2013 The Lethaia Foundation

fossils have dealt with siliciclastics although they arevery rare in the classic Ediacara Member of theRawnsley Quartzite in South Australia (Sappenfieldet al. 2011). Evidence of the evolution of behaviourof early infaunal animals is offered mostly by tracefossils from the Swedish Mickwitzia Sandstone (Jen-sen 1997) and coeval coarse clastics of Poland (Pac-ze�sna 1996), the Ukraine (Palij et al. 1983; Dzik2005), Latvia and Estonia (Jensen & Mens 1999,2001), China, Newfoundland (Droser et al. 2002b)and others (e.g. Droser et al. 2002a) and supple-mented by latest Precambrian occurrences (e.g. Jen-sen et al. 2000 for priapulid? treptichnid burrows).Thus, the record is restricted to a rather narrowspectrum of sedimentary environments, currentlybest shown from the relatively cold waters of the Bal-tica palaeocontinent. In contrast, the succession inSiberia, located that time near the equator, providesa valuable insight into the contemporaneous tropicalcarbonate ichnofauna.

Trace fossils have been known from the Tommo-tian of Siberia since its formal recognition (Rozanovet al. 1969). Although Bland and Goldring (1995)underlined that trace fossils in Cambrian carbonatefacies in Siberia are sparse or absent, numerousinsights into Siberian Cambrian trace fossils are dis-persed in the Russian literature (S. Jensen, personalcommunication 2012). A preliminary interpretationof some of these traces was attempted by Dzik (2005,2007), but they await more detailed description. TheSiberian fossils are of importance because of theunusual environment and relatively precise strati-graphical control of their geological age. Here, Ipresent a description of traces of activity of EarlyCambrian animals recorded in limestone facies ofthe classic Isyt’-Bydyangaia section.

Geological setting

A relatively thick Tommotian limestone successionis exposed in the central part of the SiberianPlatform near Yakutsk (Rozanov et al. 1969;Khomentovsky & Karlova 2005). The oldest archae-ocyathid–calcimicrobial bioherms are reported fromthere (Kruse et al. 1995), well above the base of theCambrian as defined in Newfoundland (Gehlinget al. 2001). It is also where the abundance of ‘smallshelly fossils’ was first recognized giving rationale tothe concept of the ‘Cambrian explosion’ (Rozanovet al. 1969; Missarzhevsky 1989; Maloof et al. 2010;Erwin et al. 2011).

The sections at the right bank of the Lena River,upstream of Sinsk village (Fig. 1) have beendescribed by Rozanov et al. (1969) and Rozanov and

Sokolov (1984). According to these authors, a bore-hole near the classic Isyt’ section contained 275.5 mof Tolbunsk Formation rocks and 10.5 m of lower-most Pestrotsvetnaya (Variegated) Formation lime-stone with numerous ‘small shelly fossils’:Hyolithellus, Conotheca, Cambrotubulus, Chancelloriaand others, all of the Ajacicyathus sunnaginicusZone.

The exposed profile at Isyt’ (section 3 in Roza-nov & Sokolov 1984) starts with extremely shallow-water stromatolitic strata of the lowermostTolbunsk Formation accessible on the river bank athigh water. About 9 m of the overlying strata iscovered with rubble, but the topmost part of thisunit is exposed in the left bank of the Bydyangaiacreek near its mouth (Fig. 1). This is a grey micrit-ic limestone with wavy bedding resulting fromnumerous non-deposition and dissolution events,topped with a bed with exhumed horizontal bur-rows. Both at Bydyangaia and in the Isyt’ escarp-ment on the Lena bank, a succession of pinklimestone with occasional small archaeocyathid bio-herms belongs to the Pestrotsvetnaya Formation.The rock contains glauconite, abundant in somebeds, associated with numerous phosphatized ‘smallshelly fossils’. This unit presumably corresponds tothe part of the section exposed at the mouth ofTiktirikteekh creek on the left bank of the Lena,about 12 km upstream. In both locations, largemollusc shells occur, which are unusual for the‘small shelly fossil’-dominated Cambrian of Siberia(Dzik 1991). The age of these strata was deter-mined as the Dokidocyathus regularis Zone (Roza-nov et al. 1969; Rozanov & Sokolov 1984).Upwards in the section at Isyt’ and Bydyangaiaglauconite disappears, and the rock contains anincreasing fine quartz fraction and clay minerals,but is still of dark-reddish coloration. Fossils indic-ative of the Dokidocyathus lenaicus Zone occur inthis part of the section, recognized as unit 10 inRozanov et al. (1969) and 13–14 in Rozanov andSokolov (1984). In this unit, Rozanov and Sokolov(1984, p. 35) found horizontal spreite structuresand minute burrows identified by them as Rhizo-corallium jenense Zenker and Chondrites sp. Higherin the section (their unit 15), the colour of thelimestone becomes lighter and horizontal burrowsoccur, identified as Plagiogmus sp. (Rozanov andSokolov 1984, p. 36). In light-coloured limestoneabove (unit 17) the trilobite Profallotaspis jakutensisoccurs and is diagnostic of the Atdabanian.

Horizontal burrows with spreite structures occuralso at the Zhurinsky Mys locality in the rock at themouth of a temporary creek. The part of the Pest-rotsvetnaya Formation exposed there represents the

2 D. Mazurek LETHAIA 10.1111/let.12045

D. lenaicus Zone and is thus coeval to the strata con-taining these trace fossils at Isyt’ (Kouchinsky et al.2005).

Material and methods

Most of the trace fossils studied come from the Byd-yangaia and Isyt’ sites. A few are from Tiktirikteekhand Zhurinsky Mys. They were collected by JerzyDzik while he participated in expeditions to Yakutiain 1987, led by Aleksey Rozanov from the Paleonto-logical Institute, Moscow (Tiktirikteekh and Zhurin-sky Mys), and in 2006, led by V.M. Sundukov fromthe Trofimuk Institute of Petroleum Geology andGeophysics, Novosibirsk (Bydyangaia, Isyt’). Thecollection is housed at the Institute of Paleobiology

of the Polish Academy of Sciences in Warsaw, abbre-viated ZPAL.

The majority of these trace fossils are recognizableonly on slightly weathered rock slabs and manyoccur on the bed sole. This makes collecting of infor-mative specimens directly in the section difficult andmost were found in the scree, thus precluding anassessment of the abundance and co-occurrence ofmembers of the ichnofauna. Some material comesfrom loose blocks, and it is virtually impossible toobtain more samples and data from the original sitesin remote Siberia; large specimens were photo-graphed in the field but not collected. The stratawere also sampled for phosphatic micro-fossil mate-rial (Dzik 1994).

The main objective of this study is to identifythose aspects of the life activity of trace fossil makers

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Fig. 1. Sections with traces of Early Cambrian sediment feeders on right bank of the Lena River upstream of Sinsk – rock columns witharrowed source strata (modified after Rozanov et al. 1969 and field sketches taken by J. Dzik in 1987).

LETHAIA 10.1111/let.12045 Tommotian ichnofauna from Siberia 3

that could be useful in restricting range of their pos-sible taxonomic affinities. Linnaean taxonomicnames are applied only in cases they are informativeenough to enable identification of their affiliation toa reasonably low-rank taxonomic unit (Dzik 2005,p. 519). The biological signal of these specific ichno-fossils may be seen as quite weak in comparison withother examples from the literature, but taking intoaccount their geological age, it is important to try tounravel the biological nature of their makers andbehaviours as crucial supplements to our scantknowledge of evolutionary changes in the Cambrianas read from empty shells alone. I have tried to pointto the most parsimonious interpretations, in aninevitably simplified mode of reasoning, but alterna-tives are also suggested in several cases.

Results

The Lena River localities Isyt’, Bydyangaia and Tik-tirikteekh are so close geographically to each otherthat the fossil material from there can be consideredas representing a single local succession of environ-

ments, each with a set of sympatric species exploit-ing the carbonate mud in various ways.Sedimentological descriptions and biological inter-pretations of the trace fossils presented below areaimed at the identification of their makers. However,in almost all cases, their precise zoological identityremains undetermined, and therefore, nomenclato-rial conclusions are only tentative and usually referto phylogenetic units much above the species rank.

Minute shallow near-surface burrows

ZPAL A7/30 is a slab of a reddish muddy limestonethat exposes, as a convex hyporelief on its sole,numerous limestone fills of nearly horizontal cylin-drical tunnels that penetrated the underlying mudshallowly (Fig. 2A). Most are widely U-shaped withboth entrances of the burrow at the mud surface. Afew of them show blind ends, which likely meansthat these were probing burrows, as they are alsoquite straight, vertical and shallow. Despite theirsimilar shape, the traces are of very different size.The widest burrow is 31 mm long and 7.5 mm wideat the blind end, while 3.9 mm wide along its length

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Fig. 2. Slab ZPAL A7/30 from the Tommotian Dokidocyathus lenaicus Zone of Isyt’ with cylindrical horizontal burrows and probings. A,lower surface of the slab. Star denotes large burrow with enlarged terminal portion. B, histogram showing size distribution of burrowsand probings. Note bimodal distribution. C, interpretative drawing showing the reconstructed morphology.


and at its entrance. Circular entrances of verticalprobings, all of similar size near their bases are scat-tered over the slab. Apart of these, there are also verylong and thin traces. The longest of these extends for49 mm between the entrances measured along thesinuosity of the burrow; the width is less than2 mm.

Some of the thinnest near-surface burrows arearranged in series as a result of periodic deeper bur-rowing by the animal. Rarely they seemingly bifur-cate or are arranged angularly, but this may be justincidental crossing of different tracks.

The size frequency distribution for both probingand horizontal burrows is indistinctly bimodal(Fig. 2B). The probings are generally larger, and theburrows dominate among smallest specimens.

Interpretation. – The non-overlapping size disparitybetween probing and horizontal burrows may meanthat two different kinds of animals are represented:smaller infaunal worms, and larger, possibly preda-tory, epifaunal ones. An alternative is that the behav-iour changed in ontogeny, juveniles being adaptedto shallow horizontal burrowing mainly to hideagainst predators, whereas adults hunted by probingthe sediment.

The traces are quite simple morphologically, andone may only postulate that they were made by peri-staltic action by animals with cylindrical, fluid-filledbodies (these could have been priapulids; Vannieret al. 2010).

Nomenclature. – Pacze�sna (1996) classified similarburrows as Artharia antiquata Billings 1872. Thetypotype material of Billings (1872) comes from theLower Ordovician of Newfoundland. Its biologicalunity (and thus synonymy) with the Polish and Sibe-rian traces is most dubious. Both are just simple,long U-shaped burrows made at the sediment-waterinterface (Fillion & Pickerill 1984). The smallest ofthe burrows on ZPAL A7/30 slab are similar in theirgeneral appearance to diminutive, un-named tracefossils from the Botomian of Chengjiang (Zhanget al. 2007).

Three-band burrows

Specimens ZPAL A7/20-22 are all parts of the sameslab with numerous limestone moulds of horizontalburrows made in a marly substrate (Fig. 3). Theseare either cylindrical burrows, originally penetratingthe substrate, or tripartite shallow elevations. Bothstructures are transversely wrinkled, which is unu-sual as for burrows from Isyt’. There are single-bandand three-banded burrows with annulation, as wellas three-banded without it. All three bands havetransverse wrinkles. At a few points, especially on atrail at A7/22, however, transverse wrinkles clearlydo continue as one ridge on all three longitudinalbands (Fig. 3C).

The central part of the three-banded traces ismore or less cylindrical, and it is clear in places thatthe lateral bands cover it from the sides. Cross-

A B C

Fig. 3. Portions of slabs ZPAL A7/20-22 from Isyt’ with three-banded traces on the bed sole. A, inorganic tool marks (to the left of thestar). B, slab ZPAL A7/21; note three-banded burrow, in which the central channel disappears (denoted by star). C, slab ZPAL A7/22showing trace with transverse wrinkles crossing all three bands (to the left of the star).


sections vary (Fig. 4D, E) because of differentiateddiagenesis, but potentially three separate backfillscould have existed.

The burrows vary in preservation, length (frommillimetres to almost 15 cm), sinuosity (straightand sinuous), direction and width (2–8 mm). Thereis no obvious spatial connection between differentspecimens on the slab. Some burrows cross atslightly different levels. The central band is the wid-est on straight traces, with the lateral ones beingsmaller. In some cross-sections, especially those ofsinuous burrows, only one or two bands are visible,and the size of the widest of them, as well as the sizeproportion, are altered by compaction and weather-ing.

The lateral bands are filled with a different mate-rial than the central one. In the case of the longesttrail in the middle of slab ZPAL A7/21, the central

cylindrical band terminates earlier than the lateralones and is filled with claystone, pointing to somelevel of independence in origin. In several othercases, it is the central band that is covered from thesides with the claystone matrix.

On ZPAL A7/21, pseudofossil tool marks ‘Eophy-ton lineatum’ are also visible (Fig. 3A). They are sim-ilar to Monomorphichnus, implying that knownreferences to this ichnogenus should be taken withcaution.

Interpretation. – Different infill of three partscould mean that the bands did not originate simul-taneously and that they were subjects of differentialearly cementation. One could speculate that thelateral body units were sufficiently separated fromthe central one to enable differential filling. Therelation between the central wide and the thin lat-eral ones of the three bands may suggest a central‘foot’ and two lateral units, all developed on ven-tral side only. This is contradicted by the presenceof transverse wrinkles formed on all three bandssimultaneously by peristaltic waves. Thus, noappendages were involved in digging and the bodywas likely a single unit.

The trace maker was probably an animal produc-ing transverse wrinkles by peristaltic action of itsventer and leaving behind a ventrally and centrallypositioned thick faecal rod, giving the central band amarly appearance (Fig. 4). The Siberian specimenshave a hyporelief similar to a three-banded burrowdescribed from the Late Carboniferous of Poland byGłuszek (1998) who suggested that they may havebeen made by bellerophontids.

Nomenclature. – In having three lobes with bands,the fossil superficially resembles Podolodes tripleu-rum as characterized by Dzik (2005). The inferredbehaviour of the maker precludes any close phyloge-netic relationship between the trace makers.

Systra and Jensen (2006) described three-lobedtraces from the Early Cambrian strata of the Divida-len Group of the Kilpisj€arvi area (Finland) and otherBaltic sites. None of the three-lobed traces describedso far bears signs of peristaltis, but there is a possibil-ity that the burrows described here belong to the‘Bure ichnocomplex’.

U-shaped burrows with horizontal spreiten

Specimens of large horizontal U-shaped burrowswith spreite structures are common at Isyt’ (Fig. 5;Rozanov & Sokolov 1984), Bydyangaia and Tik-tirikteekh (Dzik 2005, 2007). The spreite structure isusually poorly preserved, with details visible clearly

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Fig. 4. Sketches showing the morphology of three-banded tracesand inferred anatomy of their maker. A, B, C, different morpho-types as preserved (C similar to Curvolithus). D, E, two cross-sections showing diagenetic variants of preservation with indi-cated fields with different rock matrix coloration. F, G, priapulidmodel for the formation of the observed traces, with the gutmud-fill attached to the lower surface of the track as a result ofcompaction.


only when the surface is made wet. The successivelaminae of the spreiten are flat and thin, while theouter U-shaft (causative burrow in terminologyapplied to Zoophycos) has a more pronounced three-dimensional aspect. The burrow cross-section isoval, possibly in result of compaction assuming thatit was originally circular. The spreiten show sometelescoped laminae (i.e. compacted in situ while bur-rowing) next to the causative burrow.

No scratch marks, signs of peristalsis or otherdefining characters have been found on the burrowsor spreiten in any specimen. Scratch marks have notbeen reported in any Early Cambrian U-shaped bur-rows, despite good preservation of some of them;thus, the lack of such marks in the Siberian speci-mens seems genuine. No entrances or exits to theburrow are discernible.

Interpretation. – The disposition of laminae withinthe spreiten shows that the Siberian trace fossildeveloped by expansion of the U-shaped burrow for-ward, covering a larger and larger area. Helicoidalspreite traces from the Cambrian reflect an extremeresult of the same process. In similar Mid Palaeozoicforms, for example, Carboniferous ‘Zoophycos’ fromthe Borden Formation of Kentucky at my disposal

(collected by J. Dzik), the opposite was the case. Themarginal channel was burrowed initially at the deep-est level and widest area and then graduallyretreated. This is suggested by obliteration of thenear-margin (distal) lamination of the spreiten byproximal laminae.

Even more distant morphologically are the invertedconveyor annelidan spreiten of the Cenozoic, withtransport of organic detrital material from the sedi-ment surface to the burrow (Lewis 1970; Wetzel &Werner 1980; Ekdale & Lewis 1991; Wetzel 1992).

Protruding horizontal burrows with spreiten likethose described here were apparently produced bydeposit feeders successively browsing the mud (e.g.Schlirf 2011). The different mineralogy of the sprei-ten suggests that the sediment was most likely trans-ported via the gut and pelleted, not along the surfaceof the body. The animal presumably started with asub-vertical U-shaped burrow and then proceededforwards reproducing the same pattern, blurring themargins of earlier shafts. It remains unknown, howit repeated the burrowing activity. If the producerwas much smaller than the diameter of the burrow,it could turn around at the end of the burrow, likemany arthropod U-makers do today. Such behav-iour is consistent with the lack of any markings onthe walls and provides an explanation how the sedi-ment was grazed from one side and then put on theother. The alternatives are going back without turn-ing (observed, e.g. for polychaetes) or going out andentering again after turning at the surface (unknownin extant animals).

To explain why the outermost U-shaped shaft is afilled burrow, with a certain volume, while precedingU-s are merely flat markings one may suggest thatthe lining of the shaft decomposed through time,causing the collapse of shafts older than the newest.An alternative explanation is that while burrowingthe tunnel was unlined and empty, but after reachingsome size (both ZPAL A7/28 and 29 are of similardimensions), the burrow was lined and used as ashelter. This would mean that the animal changed itsbehaviour and dietary habits from mud-eating toscavenging and/or hunting within the burrow.

The Triassic Rhizocorallium crustacean (?) bur-row (H€antzschel 1975, p. W101, and referencestherein) has a similar configuration, that is, col-lapsed set of central shafts and a three-dimension-ally preserved outermost U-shaped burrow. Recentcounterparts are being formed by, among others,the amphipod Corophium volutator (Ingle 1966)and the holothurian Thyone briareus (Pearse 1908;Howard 1968).

Some of the Cambrian U-shaped burrows havepreviously been ascribed to echiurans but the oldest

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Fig. 5. Slab ZPAL A7/29 with U-shaped burrow with horizontalspreiten. A, seen under low angle light to show elevated lastchannel. B, with vertical light to enhance spreiten.


fossil echiuran is Carboniferous; the sole specimenof the Precambrian Protechiurus (Glaessner 1979)was proposed to represent a pteridiniid ‘vendozoan’,together with Vendoconularia (Dzik 2003, Fig. 8).The time of echiuran separation from the mainbranch of annelids is still unknown (see Struck et al.2011).

The described burrows could even be made by si-punculans, one of the earliest branches of annelidsaccording to Struck et al. (2011). The Early Cam-brian sipunculans have been described by Huanget al. (2004a).

Among the Chengjiang fauna (MaotianshanShale) nemathelminths, there are small dumb-bell-shaped forms (represented by Palaeopriapulites par-vus and Sicyophorus rarus) with an extremely shortbody filled with a coiled gut. Based on the gut lengthand infill, they might be sediment feeders (but seeMaas et al. 2007 for a different opinion). Recently,Weber et al. (2012) cast some doubt on sedimentfeeding by Cambrian priapulids citing Butterfield(2002), who considered that the mud-filling of thegut of one of the Burgess Shale arthropods resultedof the weathering of phosphate. This reasoning

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Fig. 6. An hypothesis of possible relationships between various burrows. An ‘evolutionary route’ leading from A to E may have devel-oped many times, independently and iteratively, by different ‘worms’, annelids and arthropods. Arrows denote actual evolutionary direc-tions of these convergence lines. A, simple J-shaped dominichnia of suspension feeders. B, U-shaped dominichnia of suspension feeders;ZPAL A7-30 belong here. C, D, rhizocorallid-type burrows of sediment feeders (annelids and arthropods) marks the onset of use of sedi-ment organic matter; ZPAL A7-24, 25, 28, 29 belong here (D). E, coiling of rhizocorallid-type burrows adjust space utilization; EarlyCambrian forms described by Jensen (1997) as Zoophycos (Rhizocorallium) isp. belongs here, as well as many other Palaeozoic examples;the Zoophycos group of Uchman and Dem�ırcan (1999). F, I, cache? structures of echiurans? or other annelids only generally similar inappearance to Zoophycos structures made by deposit feeders; here, the laminae are made of sediment from the seafloor, note also thateach lamina itself can be described as a spreite structure; Jurassic of France (F, after Gaillard & Olivero 1993; and Olivero & Gaillard1996; some Palaeozoic forms may belong here as well) and Cenozoic (also recent) ‘Spirophyton’ known worldwide in deep-sea settings(I). G, H, further advances of sediment utilization by deposit feeders developed by iteration of ‘Rhizocorallium’ exemplified by: Creta-ceous burrows from Sweden and Denmark (G, after Bromley et al. 1999; some Palaeozoic forms may belong here as well); Amuri-typeburrows from the Cretaceous of New Zealand and Echinospira from the Miocene of Turkey (H).


cannot, however, be extrapolated on all worms withtheir guts filled with sediment.

Also some lobopodians (Luolishania-Facivermislineage) were infaunal, but they probably con-structed only simple, vertical burrows feeding ondetritus or as predators.

A possible ‘evolutionary’ scenario for the kinds ofsediment exploitation discussed above is presentedin Figure 6.

Nomenclature. – Traces of such morphology aretraditionally classified as Rhizocorallium jenense(also at Isyt’; Rozanov & Sokolov 1984). The nameis based on Muschelkalk (Mid Triassic) traces(F€ursich 1974) probably produced by crustaceans(H€antzschel 1975, p. W101). The Early Cambrianspecimens lack scratch marks and are more similarto a segment of the ‘Zoophycos’ complex burrowthan to Rhizocorallium. Dzik (2005) used the nameaff. Diplocraterion sp. for the trace maker of thesefossils proposing that the ability to make horizon-tal spreiten originated from a vertical one. Thispoint was made earlier by Jensen (1997, fig. 22),who illustrated an evolutionary route: Diplocrateri-on parallellum ? Rhizocorallium jenense ? Zoo-phycos (Rhizocorallium?) isp. The once-proposedtype species of Zoophycos, Fucoides circinatus Bron-gniart 1828 was based on Early Cambrian verticalspreite structures having little to do with helicoidaltraces from younger strata (Jensen & Bergstr€om1995). The actual type species of Zoophycos(Zoophycos caput-medusae) is a plant fossil:Zoophycos brianteus being the proposed new typeichnospecies (Olivero 2007).

Horizontal burrows with vertical spreiten

Block ZPAL A7/17 (Fig. 7) from Zhurinsky Mysshows transverse sections of two burrows with sprei-ten below. Field photographs allows up–down orien-tation to be established with certainty. Thesediment, especially the burrow infill and spreiten, isalso secondarily bioturbated.

Pebble ZPAL A7/23 (Fig. 8) from Bydyangaiarepresents an isolated spreite structure. Polished sec-tions reveal wide simple U-shaped yellowish layersthat can be seen in reddish iron-oxidized matrix.The specimen is a part of a larger block photo-graphed in the field (Fig. 8A). Some minute, verydark-red, secondary traces are visible on the polishedsurface.

Slab ZPAL A7/26 (Fig. 9) from Bydyangaiaexposes the upper surface of a few large (somemore than 20 mm wide) burrows heavily biotur-bated by continuous generations of small burrow-

ers (ichnofabric index of Droser & Bottjer 1986about 5 – highly bioturbated); outside the largeburrows they are rare. The probable roofs of theburrows are flattened by compaction. Some ofthem cross each other, apparently proceeding onebeneath the other. The burrows are long and par-allel to the bedding. Some of the burrows appearto end abruptly without any signs of exit-charac-teristic structures.

Interpretation. – The inferred succession of eventsleading to formation of these traces (Fig. 7) is rathercomplicated: (1) a shallow and wide U-shaped bur-row was created and used for an extended time per-iod; (2) the usage caused parts of the ceiling to falldown and deposit on the tunnel floor, leading to anupwards shift of the tunnel and formation of sprei-ten under its floor; (3) spreite material was reworkedby other minute burrowers; (4) the roof collapsedand bottom currents probably reworked or win-nowed material in the newly formed groove; andeventually, (5) the burrows were covered by sedi-ment and lithified.

Presumably, to form vertical spreiten, the animalhad to move constantly along the tunnel in bothdirections. The burrower had to be smaller than theburrow’s diameter and armed with some kind ofappendages. The lack of any scratch marks and thegeological age older than the first arthropod recordmakes them unlikely candidates for the trace makers,although this cannot be completely refuted. Horizon-tal burrows with spreiten appear just before the firsttrilobites (Crimes 1987, 1992). This is clear in theIsyt’ section, in which the appearance of the trilobiteProfallotaspis marks the end of the Tommotian.

Similar traces to those described above are madetoday by the polychaete Nereis diversicolor. The old-est known polychaetes are those from the EarlyCambrian Sirius Passet (Conway Morris & Peel2008; Vinther et al. 2011), but these are morphologi-cally close to present-day errant annelids livingabove the sediment surface. If the Siberian burrowswere made by polychaetes, those would be the oldestinfaunal annelids.

Similar Carboniferous horizontal burrows withspreiten from Ireland grade into vertical shafts(Buckman 1996). No secondary bioturbation ofshafts, as well as spreiten from other sites andstrata, is mentioned in the literature, except forone Chondrites-like bioturbation (Bland & Gold-ring 1995).

Nomenclature. – A similar trace fossil was illus-trated from the Lower Cambrian ShiyantouFormation of China by Dornbos et al. (2005,


Fig. 3d), who classified it in Teichichnus. Anotherform was described from the Early CambrianCaerfai Group of Wales under this ichnotaxonom-ical name by Loughlin & Hillier (2010). The typespecies of the genus, T. rectus Seilacher 1955

comes from the Early Cambrian of Pakistan; thus,it and the Siberian trace maker might possiblyhave belonged to the same genus. Similar formsfrom roughly coeval strata of northern Polandwere described and illustrated by Pacze�sna (1996,

C

D

A

B

1 cm

lithifiedchannelinfill


spreitespreite

channelchannel

spreitespreite

channelchannel

lithified sedimentlithified sediment

soft sedimentsoft sediment

winnowed cavitywinnowed cavity

secondary infillsecondary infill



lithifiedsedimentlithifiedsediment

- 1st generation burrow- 1st generation burrow- 2nd generation burrow- 2nd generation burrow

Fig. 7. Sedimentary history of two horizontal burrows with vertical spreiten in specimen ZPAL A7/17 from Zhurinsky Mys. A, hypothet-ical original situation, with results of trace-maker activity. B, effects of winnowing of soft sediment from between burrows. C, D, two pol-ished sections across the slab (note generations of minute sediment feeder burrows).


p. 62, pl. 18: 6–7, 19: 1–9, 20: 1–2) and fromEngland by Bland & Goldring (1995).

Minute burrows penetrating larger ones

Large-diameter burrows in the Pestrotsvetnaya For-mation are usually penetrated by smaller, secondaryburrows, some reaching the surrounding matrix(Figs 7–9). All are preserved in brownish-reddishlimy mudstone. They bifurcate and extend for sev-eral centimetres. Their diameter is rather uniformand within the range of 1–2 mm; originally, theywere probably circular in section. They have at leasttwo discrete classes of coloration. Presumably, thelighter burrows represent an earlier generation judg-ing from the spatial relationships. There are no otherapparent differences between them.

Interpretation. – The bioturbators were millimetre-size animals which presumably entered the large bur-rows because it was easier to dig there or because ofthe high organic matter contents (or both). The sec-ond possibility could explain the lack of significantkerogen carbon in the burrows. EDS analyses showthat burrows are enriched in iron (possibly frompyrite oxidized in diagenesis) and calcium (from cal-careous sediment above) in respect to the surround-ing matrix, but there is more carbon in the matrix.

Since the seminal monograph by Conway Morris(1977) and subsequent discoveries of the Chengjiangfossils (e.g. Huang et al. 2004b), it is known that thepriapulomorphs dominated the infauna of the Cam-brian ecosystems, as shown by their numerous fossilsin Konservat Lagerst€atten. The circular body sectionand mode of sediment penetration make it likely

that the mud-eating Early Cambrian worms fromSiberia were also priapulids rather than relatives ofpresent-day animals of similar biology, not repre-sented among the known Cambrian body fossils.

Nomenclature. – The feeding burrows of typedescribed above are morphologically simple fodi-nichnia usually classified in Chondrites von Stern-berg, 1833, probably made by chemosymbioticanimals (Seilacher 1990; Fu 1991; Fu & Werner1995). Its type species is the Permian Fucoides lyco-podioides Brongniart 1828, distant in time and ecol-ogy from the Early Cambrian trace makers. Whetherthe trace maker of the fossils described here was achemosymbiotic animal cannot be proven; in fact,any burrow may be multi-functional.

Horizontal burrows with a peristaltic wave

A yellow block of dolomitized limestone ZPAL A7/27 with long, straight, roofed horizontal tunnels witha peristaltic wave exposed in positive relief on theirsoles (Fig. 10) was found at Isyt’ and probablycomes from bed 16 of Rozanov and Sokolov (1984).The width of the traces is constant, about 17.5 mm,while the wavelength between bars is about 3.9 mmand apparently constant as well. Stratification can beseen on polished sections: yellowish and brownishlayers with a high degree of bioturbation and mix-ing, and signs of the sediment from higher layersbeing pulled down to the burrows. The burrow’s fillis grey, and the surrounding matrix yellow. No signof the roof incision was observed. Polishing revealeda number of small skeletal fossils (mostly conchs ofprobable originally aragonitic composition), but no

A B CB

D

spreitespreite

spreitespreite

spreitespreite

1 cmC

Fig. 8. Pebble ZPAL A7/23 from Bydyangaia showing: A, transverse (field photo) and B, C, longitudinal sections of horizontal burrowswith vertical spreiten. Note oblique layering of the spreiten. D, interpretative drawing.


differences in sediment grain size between the fill ofburrows and the surrounding matrix. Dolomitiza-tion was apparently restricted to the sediment thatwas bioturbated. The sediment is also apparentlycompacted. No backfill is visible.

Interpretation. – The stable dimension of the trailand peristaltic waves implies a constant speed ofmovement, with some rigidity of the ventral bodycovers. With their high relief and wavy ornament,these traces are somewhat similar to those of theEarly Cambrian Psammichnites (McIlroy & Heys1997; Seilacher 1997), but evidence of a verticallyoriented organ cutting the sediment is missing.Psammichnites is known mainly from sandstone

(Jaeger & Martinsson 1980), and I am not awareof any earlier report on such burrow from car-bonate.

The wavy sole of the Siberian trace is of a kindknown among the Cambrian trace fossils only inthe Late Cambrian (Furongian) Climactichnitesfrom various sites in North America (Getty 2007;Getty & Hagadorn 2008, 2009). The surface trailsthere are associated with burrows and restingtraces. Seilacher (1997) was the first who correctlyinterpreted Climactichnites, inferring that the mus-cular contractions moved posteriorward along thefoot, with the movement starting from the restingtraces. The waves in Climactichnites wilsoni areV-shaped, not U-shaped. The morphology of

5 cm

A

B

- 1st generation channel - 1st generation channel

- 2nd generation channel - 2nd generation channel

- earlier burrow- earlier burrow

- late burrow- late burrow

- 1st generation channel - 1st generation channel

- 1st generation channel ?- 1st generation channel ?

- 2nd generation channel - 2nd generation channel

channel roof

channel roof

roofroof

Fig. 9. Upper surface of slab ZPAL A7/26 from Bydyangaia showing horizontal burrows with vertical spreiten penetrated by minute sedi-ment feeder burrows. A, photograph with enhanced contrast. B, interpretive, diagrammatic drawing showing the distribution of smallburrows and their spatial relationship to large burrows. Lining obliterating smaller burrows underneath, where preserved, showed in grey.Note that the visible surface represents a split surface at the level of roofs, within the bed.


waves in the Siberian burrow may have resultedfrom hydraulic peristalsis, not necessarily fromcontractions of a purely muscular foot. Peristalticmovement of recent gastropods may leave similartraces, and there is a possibility that trace maker

was a molluscan relative. Anyway, this is one ofthe oldest records of the ventral muscular struc-tures working in a peristaltic movement.

Burrows of similar size and morphology occur atthe bed sole in a pure, light-coloured micritic lime-

A B

C

Fig. 10. Slab ZPAL A7/27 from Isyt’ showing burrows with peristalsis structures. A, photograph. B, 3-D scan shown at angle to showrelief of burrows. C, diagrammatic drawing of cross-section (not to scale) of two burrows (shadowed) showing absence of funnels above.Note that whole volume of the slab is penetrated by similar burrows with poorly recognizable boundaries.

A

C

B

Fig. 11. Straight and circular horizontal burrows at the clay–lime mud interface preserved in light-coloured micritic limestone (fieldphotos). A, straight burrows on the bed sole of a slab of yellowish pure limestone from Isyt’ (probably bed 16 of Rozanov & Sokolov1984). B, C, rock matrix-filled straight burrows and collapsed circles on the sole of glauconitic light-grey limestone from the basal part ofthe section at Bydyangaia.


stone block found at Bydyangaia (Fig. 11), but theydo not show a peristaltic wave (Fig. 11B). Theblock contains glauconite grains and thus is pre-sumably derived from the basal part of section Thecourse of the burrows is either straight (and thenthey are filled with a lime mud matrix) or formspartially overlapping oval loops, being then filledwith clay matrix, presumably from the overlyingbed. Their exposed vault is smooth, without anysign of vertical cut by a proboscis or funnel. Preser-vation in two ways, both as concave and convex hy-poreliefs, clearly shows no snorkel was present.Another slab shows more regular loops, suggestiveof feeding behaviour (Fig. 11C). At Isyt’, straightmatrix-filled burrows of this kind occur in a lime-stone similar to that with peristaltic wave-bearingburrows (Fig. 11A). It is possible that all these arevarieties of life activity of the same organism. Whilefeeding at the clay–lime interface with loop-formingbehaviour, it did not strengthen the channel wallsthat were later filled with sediment from the claylayer.

Seilacher and Hagadorn (2010) included theEarly Cambrian Psammichnites in their proposedline of descendance of naked molluscs startingfrom the Ediacaran Kimberella (leaving also prob-able radular scratch marks), the Late Cambrian(Furongian) Climactichnites-Musculopodus animalwith radular scratches, and the mainly Carbonifer-ous ‘Aulichnites-Olivellites’ and Dictyodora(M�angano et al. 2002). There is a possibility thathalkieriid molluscs were involved in production ofthe Siberian traces (Seilacher-Drexler & Seilacher1999). The molluscan nature of the maker is,however, conjectural.

Nomenclature. – The animal that left the traces fitsneither the body plan of the Early Cambrian Psam-michnites (as it lacks any sediment-cutting dorsalorgan) nor the Furongian Climactichnites (as it has adifferent course of the bars produced by peristalsis),but seems intermediate between them in theseaspects.

Associated body fossils

A review of ‘small shelly fossils’ from Bydyangaiasupplementing data for Isyt’ presented by Rozanovet al. (1969) and Missarzhevsky (1989) was pub-lished in Dzik (1994). Macrofossils are representedthere mainly by sessile archaeocyaths and benthichyoliths, which are often found inside burrows(J. Dzik, personal communication, 2011), certainly –based on their inferred ecology and comparison with

similar organisms occurring in burrows from otherperiods – brought there by water currents. Aceticacid-resistant residues yielded juvenile hyoliths,chancelloriid and halkieriid sclerites, and simpletubes of unknown affinities. Minute molluscs arealso present, some being juveniles, others probablyminute adults (e.g. the bivalve Watsonella). Therecent finding that the celebrated Cambrian gastro-pod Pelagiella had chaetae (Thomas et al. 2010a,b;Thomas 2012) shows how misleading the traditionalapproach to early mollusc-like skeletal fossils maybe. Another example, helcionellid Bemella shells(Dzik 1991), usually interpreted as monoplacopho-ran (which seems unlikely; Dzik 2010) may well-represent halkieriid shells.

Among these, Cambrian animals only the appar-ently sluggish halkieriid ‘coeloscleritophorans’(possibly including Bemella) could have left mollus-can-like traces of movement within the sediment.Articulated halkieriids from Greenland are known tomeasure 80 mm in length and would fit in some ofthe traces described here. Possibly, an unknown soft-bodied organism left the traces. No arthropod skele-tal remnants are present in the ‘small shelly fossils’assemblages studied, nor are there any certainarthropod signs in the trace fossils assemblage,although some scratches could have been made byarthropods.

Sclerites of the tommotiid Camenella are commonin the pink marly limestone from Zhurinsky Mys,(Dzik 1994). Too little is known about tommotiidanatomy to risk speculation about their biology.Findings of early polyplacophorans without a foot(Sigwart & Sutton 2007; Sutton & Sigwart 2012; Sut-ton et al. 2012) call for care in interpreting such fos-sils. The general resemblance of the Camenellasclerites to those of the machaeridian polychaetes(e.g. Vinther & Rudkin 2010) makes them potentialepifaunal or infaunal trace makers. Advanced tom-motiids with rather irregular sclerites had bodiescompletely covered with them, thus probably beingsessile (Holmer et al. 2011), unless these were col-lected and glued together by a tube-constructing ani-mal. Both the halkieriid coeloscleritophorans andunderived tommotiids flourished in the Early Cam-brian. What is known about their anatomy is notincompatible with their molluscan affinities (e.g.Giribet et al. 2006; Wilson et al. 2010; Dzik 2011b).It is thus surprising that trace fossils that could beinterpreted as having been made by a molluscan footare missing in the Early Cambrian (as are annelid-specific traces of that age).

Clearly, most of the trace fossils were probablyproduced by animals lacking any skeletonized ana-tomical structures. The only way to identify them is


thus by comparison of the traces with anatomicalevidence of unskeletonized Cambrian animalsknown from Burgess Shale-type sites. The KonservatLagerst€atte geographically and stratigraphically clos-est to the Isyt’ area is the Sinsk Formation (Ivantsov& Wrona 2004; Ivantsov et al. 2005; Dzik 2011a). Inmost such localities infaunal ecdysozoans flourished,represented by priapulids (Conway Morris 1977)and palaeoscolecidans, with associated traces (Huet al. 2012; Weber et al. 2012).

Conclusions

Contrary to expectations, all well-understood EarlyCambrian traces come from ecdysozoans, not fromlophotrochozoans. Although the taxonomic identityof the animals forming the infaunal traces from theTommotian limestone of Siberia remains unknown,they may represent various kinds of early nemathel-minthes, the least derived representatives of theEcdysozoa (Telford et al. 2008). It seems the evolu-tionary success of this group can be envisaged as adriving force of the agronomic revolution. Noapparently molluscan locomotion traces have beenencountered in the Lower Cambrian, despite themass occurrence of skeletal fossils attributed to mol-luscs. This is not only the case of limy mud environ-ment studied here, but is apparent in other tracefossils assemblages reported around the globe. Possi-bly the standard muscular foot, typical of modernmolluscs had not yet developed (see also Thomaset al. 2010a), although the ventral muscular foot isgenerally believed to be an ancestral state of molluscs(Kocot et al. 2011; Smith et al. 2011; Vinther et al.2012; but see Caron et al. 2006). The late Ediacaran(Jensen 2003) to Mid Cambrian alleged gastropodtrails Archaeonassa (Fenton & Fenton 1937) arehardly of such origin (Yochelson & Fedonkin 1997;but see Buckman 1994). The late Ediacaran Kimbe-rella is generally envisaged as the earliest knownmollusc, but its dorsum was not covered with a mar-ginally growing shell (Dzik 2011b); it may be a basallophotrochozoan. No molluscan traces are associ-ated with it, and the purported radula scratch marksmay be interpreted as being from either a molluscanradula (e.g. Seilacher & Hagadorn 2010) or a poly-chaete jaw apparatus (Dzik 2011b).

Despite the apparent lack of unquestionable mac-roscopic molluscan trace fossils in the Early Cam-brian, members of the conchiferan molluscs of thistime are believed to be well represented in the ‘smallshelly fossils’ assemblages. A possible reason for sucha discrepancy is that the earliest molluscs were trulyof microscopic size at maturity and they arose

through a miniaturization evolutionary bottleneckand did not reach macroscopic sizes until the LateCambrian. This must be taken into account in phy-logenetic debates on the origin and early evolutionof the molluscs.

Acknowledgements. – Jerzy Dzik (Institute of Paleobiology PAS)provided the materials studied and access to literature data. Hepatiently read and greatly influenced the manuscript at all stagesof its production, discussed all my bad and good ideas andhelped with preparing the figures. The director and staff of theMuseum and Institute of Zoology of the Polish Academy of Sci-ences gave me an opportunity to use their 3D-scanner. KatarzynaJaniszewska and Marek Dec (both IP PAS) and Agnieszka Zga-gacz (Warsaw University of Life Sciences) assisted with graphicand 3D software. Rafał Skrzatek (Wrocław) helped with accessingthe literature. Earlier versions of this manuscript were revised inthe light of comments by anonymous referees and S€oren Jensen,which are greatly acknowledged. Special thanks are to AssociateEditor Alan Owen for major editorial improvements of the text.

References

Billings, E. 1872: On some fossils from the primordial rocks ofNewfoundland. Canadian Naturalist, new series 6, 465–479.

Bland, B.H. & Goldring, R. 1995: Teichichnus rectus Seilacherfrom the Charnian of Leicestershire. Neues Jahrbuch f€ur Geolo-gie and Pal€aontologie Abhandlungen 195, 5–23.

Bottjer, D.J., Hagadorn, J.W. & Dornbos, S.Q. 2000: The Cam-brian substrate revolution. GSA Today 10, 1–7.

Bromley, R.G., Ekdale, A.A.T. & Asgaard, U. 1999: Zoophycos inthe Upper Cretaceous chalk of Denmark and Sweden. Greifsw-alder Geowissenschaftliche Beitr€age 6, 133–142.

Brongniart, M.A. 1828: Histoire des v�eg�etaux fossiles ou recherchesbotaniques et g�eologiques sur les v�eg�etaux renferm�es dans les di-verses couches du globe, 1–136 pp. G. Dufour & E. d’Ocagne,Paris.

Buckman, J.O. 1994: Archaeonassa Fenton and Fenton 1937reviewed. Ichnos 3, 185–192.

Buckman, J.O. 1996: An example of ‘deep’ tier level Teichichnuswith vertical entrance shafts, from the Carboniferous of Ire-land. Ichnos 4, 241–248.

Butterfield, N.J. 2002: Leachoilia guts and the interpretation ofthree-dimensional structures in Burgess Shale-type fossils.Paleobiology 28, 155–171.

Caron, J.-B., Scheltema, A., Schander, C. & Rudkin, D. 2006: Asoft-bodied mollusc with radula from the Middle CambrianBurgess Shale. Nature 442, 159–163.

Conway Morris, S. 1977: Fossil priapulid worms. Special Papersin Palaeontology 20, 1–95.

Conway Morris, S. & Peel, J.S. 2008: The earliest annelids: lowerCambrian polychaetes from the Sirius Passet Lagerst€atte, PearyLand, North Greenland. Acta Palaeontologica Polonica 53, 137–148.

Crimes, T.P. 1987: Trace fossils and correlation of late Precam-brian and early Cambrian strata. Geological Magazine 124, 97–119.

Crimes, T.P. 1992: Changes in the trace fossil biota across theProterozoic-Phanerozoic boundary. Journal of the GeologicalSociety, London 149, 637–646.

Dornbos, S.Q., Bottjer, D.J. & Chen, J.Y. 2005: Paleoecology ofbenthic metazoans in the Early Cambrian Maotianshan Shalebiota and the Middle Cambrian Burgess Shale biota. Palaeoge-ography, Palaeoclimatology, Palaeoecology 220, 47–67.

Droser, M.L. & Bottjer, D.J. 1986: A semiquantitative field classi-fication of ichnofabric. Journal of Sedimentary Research 56,558–559.

Droser, M.L., Jensen, S. & Gehling, J.G. 2002a: Trace fossils andsubstrates of the terminal Proterozoic-Cambrian transition:


implications for the record of early bilaterians and sedimentmixing. Proceedings of the National Academy of Sciences of theUnited States of America 99, 12572–12576.

Droser, M.L., Jensen, S., Gehling, J.G., Myrow, P.M. & Nar-bonne, G.M. 2002b: Lowermost Cambrian ichnofabrics fromthe Chapel Island Formation, Newfoundland: implications forCambrian substrates. Palaios 17, 3–15.

Dzik, J. 1991: Is fossil evidence consistent with traditional viewsof the early Metazoan phylogeny? In Conway Morris, S. & Si-monetta, A. (eds): The Early Evolution of Metazoa and Signifi-cance of Problematic Taxa, 47–56. Cambridge University Press,Cambridge.

Dzik, J. 1994: Evolution of ‘small shelly fossils’ assemblages ofthe early Paleozoic. Acta Palaeontologica Polonica 39, 247–313.

Dzik, J. 2003: Anatomical information content in the Ediacaranfossils and their possible zoological affinities. Integrative andComparative Biology 43, 114–126.

Dzik, J. 2005: Behavioral and anatomical unity of the earliestburrowing animals and the cause of the “Cambrian explo-sion”. Paleobiology 31, 507–525.

Dzik, J. 2007: The Verdun Syndrome: simultaneous origin ofprotective armour and infaunal shelters at the Precambrian-Cambrian transition. In Vickers-Rich, P. & Komarower, P.(eds): The Rise and Fall of the Ediacaran Biota, 405–414. Geo-logical Society, London. Special Publication 286.

Dzik, J. 2010: Brachiopod identity of the alleged Late Cambrianmonoplacophoran ancestors of cephalopods. Malacologia 52,97–113.

Dzik, J. 2011a: The xenusian-to anomalocaridid transition withinthe lobopodians. Bolletino della Societ�a Paleontologica Italiana50, 65–74.

Dzik, J. 2011b: Possible Ediacaran ancestry of the halkieriids. Pal-aeontographica Canadiana 31, 205–217.

Ekdale, A.A. & Lewis, D.W. 1991: The New Zealand Zoophycosrevisited: morphology, ethology and paleoecology. Ichnos 1,183–194.

Erwin, D.H., Laflamme, M., Tweedt, S.M., Sperling, E.A., Pisani,D. & Peterson, K.J. 2011: The Cambrian conundrum: earlydivergence and later ecological success in the early history ofanimals. Science 334, 1091–1097.

Fenton, C.L. & Fenton, M.A. 1937: Archaeonassa: Cambrian snailtrails and burrows. American Midland Naturist 18, 454–456.

Fillion, D. & Pickerill, R.K. 1984: On Arthraria antiquata Billings,1872 and its relationship to Diplocraterion Torell, 1870 and Bi-fungites Desio, 1940. Journal of Paleontology 58, 683–696.

Fu, S. 1991: Funktion, Verhalten und Einteilung fucoider undlophocteniider Lebenspuren. Courier Forschungsinstitut Senc-kenberg, Senckenbergischen Naturforschende Gesellschaft 135, 1–79.

Fu, S. & Werner, F. 1995: Is Zoophycos a feeding trace? NeuesJahrbuch f€ur Geologie and Pal€aontologie Abhandlungen 195, 37–47.

F€ursich, F.T. 1974: Ichnogenus Rhizocorallium. Pal€aontologischeZeitschrift 48, 16–28.

Gaillard, C. & Olivero, D. 1993: Interpr�etatio pal�eo�ecologiquenouvelle de Zoophycos Massalongo, 1855. Comptes Rendus del’Acad�emie des Sciences de Paris, S�erie 2 316, 823–830.

Gehling, J.G., S€oren, J., Droser, M.L., Myrow, P.M. & Narbonne,G.M. 2001: Burrowing below the basal Cambrian GSSP, For-tune Head, Newfoundland. Geological Magazine 138, 213–218.

Getty, P.R. 2007: Paleobiology of Climactichnites tracemaker: Anenigmatic Late Cambrian animal known only from trace fos-sils. 1–131 pp. Unpublished MSc Thesis, University of Massa-chusetts.

Getty, P.R. & Hagadorn, J.W. 2008: Reinterpretation of Climac-tichnites Logan 1860 to include subsurface burrows, and erec-tion of Musculopodus for resting traces of the trackmaker.Journal of Paleontology 82, 1161–1172.

Getty, P.R. & Hagadorn, J.W. 2009: Palaeobiology of the Climac-tichnites tracemaker. Palaeontology 52, 753–778.

Giribet, G., Okusu, A., Lindgren, A.R., Huff, S.W., Schr€odl, M. &Nishiguchi, M.K. 2006: Evidence for a clade composed of mol-luscs with serially repeated structures: monoplacophorans are

related to chitons. Proceedings of the National Academy of Sci-ences of the United States of America 103, 7723–7728.

Glaessner, M.F. 1979: An echiurid worm from the Late Precam-brian. Lethaia 12, 121–124.

Głuszek, A. 1998: Trace fossils from Late Carboniferous stormdeposits, Upper Silesia Coal Basin, Poland. Acta Palaeontolog-ica Polonica 43, 517–546.

H€antzschel, W. (ed.) 1975: Treatise on Invertebrate Paleontology,Part W, Supp. 1, 269 pp (2nd edition). Geological Society ofAmerica and University of Kansas, Boulder, CO & Lawrence,KS.

Holmer, L.E., Skovsted, C.B., Larsson, C., Brock, G.A. & Zhang,Z. 2011: First record of a bivalved larval shell in Early Cam-brian tommotiids and its phylogenetic significance. Palaeontol-ogy 54, 235–239.

Howard, J.D. 1968: X-ray radiography for examination of bur-rowing in sediments by marine invertebrate organisms. Sedi-mentology 11, 249–258.

Hu, S.X., Steiner, M., Zhu, M.Y., Luo, H.L., Forchielli, A., Ke-upp, H., Zhao, F.C. & Liu, Q. 2012: A new priapulid assem-blage from the early Cambrian Guanshan fossil Lagerst€atte ofSW China. Bulletin of Geosciences 87, 93–106.

Huang, D.-Y., Chen, J.Y., Vannier, J. & Saiz Salinas, J.I. 2004a:Early Cambrian sipunculan worms from the southwest China.Proceedings of the Royal Society of London 271, 1671–1676.

Huang, D.-Y., Vannier, J. & Chen, J.Y. 2004b: Anatomy and life-styles of Early Cambrian priapulid worms exemplified by Co-rynetis and Anningvermis from the Maotianshan Shale (SWChina). Lethaia 37, 21–33.

Ingle, R.W. 1966: An account of the burrowing behaviour of theamphipod Corophium arenarium Crawford (Amphipoda: Cor-ophiidae). Annals and Magazine of Natural History 13, 309–317.

Ivantsov, A.Y. & Wrona, R. 2004: Articulated palaeoscolecidsclerite arrays from the Lower Cambrian of eastern Siberia.Acta Geologica Polonica 54, 1–22.

Ivantsov, A.Y., Zhuravlev, A.Y., Krassilov, V.A., Leguta, A.V.,Melnikova, L.M., Urbanek, A., Ushatinskaya, G.T. & Malak-hovskaya, Y.E. 2005: Unikalnoye sinskoye mestonakhozhdenierannekembriyskikh organizmov, Sibirskaya platforma. TrudyPaleontologicheskogo Instituta RAN 284, 1–143.

Jaeger, H. & Martinsson, A. 1980: The Early Cambrian trace fos-sil Plagiogmus in its type area. Geologiska F€oreningens i Stock-holm F€orhandlingar 102, 117–126.

Jensen, S. 1997: Trace fossils from the Lower Cambrian Mick-witzia sandstone, south-central Sweden. Fossils and Strata 42,1–111.

Jensen, S. 2003: The Proterozoic and earliest Cambrian trace fos-sil record; patterns, problems, and perspectives. Integrativeand Comparative Biology 43, 219–228.

Jensen, S. & Bergstr€om, J. 1995: The trace fossil Fucoides circina-tus Brongniart, 1828, from its type area, V€asterg€otland, Swe-den. GFF 117, 207–210.

Jensen, S. & Mens, K. 1999: Lower Cambrian shallow-wateroccurrence of the branching “deep-water” type of trace fossilDendrorhaphe from the Lontova Formation, eastern Latvia.Pal€aontologische Zeitschrift 73, 187–193.

Jensen, S. & Mens, K. 2001: Trace fossils Didymaulichnus cf. ti-rasensis and Monomorphichnus isp. from the Estonian LowerCambrian, with a discussion on the early Cambrian ichnocoe-noses of Baltica. Proceedings of the Estonian Acadademy of Sci-ences, Geology 50, 75–85.

Jensen, S., Saylor, B.Z., Gehling, J.G. & Germs, G.J.B. 2000: Com-plex trace fossils from the terminal Proterozoic of Namibia.Geology 28, 143–146.

Jensen, S., Droser, M.L. & Gehling, J.G. 2005: Trace fossil preser-vation and the early evolution of animals. Palaeogeography,Palaeoclimatology, Palaeoecology 220, 19–29.

Khomentovsky, V.V. & Karlova, G.A. 2005: The Tommotianstage base as the Cambrian lower boundary in Siberia. Stratig-rafija, Geologiskaja Korrelyatsiya 13, 26–40.

Kocot, K.M., Cannon, J.T., Todt, C., Citarella, M.R., Kohn, A.B.,Meyer, A., Santos, S.R., Schander, C., Moroz, L.L., Lieb, B. &


Halanych, K.M. 2011: Phylogenomics reveals deep molluscanrelationships. Nature 477, 452–456.

Kouchinsky, A., Bengtson, S., Pavlov, V., Runnegar, B., Val’kov,A. & Young, E. 2005: Pre-Tommotian age of the lowerPestrotsvet Formation in the Selinde section on the Siberianplatform: carbon isotopic evidence. Geological Magazine 142,319–325.

Kouchinsky, A., Bengtson, S., Runnegar, B., Skovsted, C., Steiner,M. & Vendrasco, M. 2012: Chronology of early Cambrian bio-mineralization. Geological Magazine 149, 221–251.

Kruse, P.D., Zhuravlev, A.Y. & James, N.P. 1995: Primordialmetazoan-calcimicrobial reefs: Tommotian (Early Cambrian)of the Siberian Platform. Palaios 10, 291–321.

Lewis, D.W. 1970: The New Zealand Zoophycos. New ZealandJournal of Geology and Geophysics 13, 295–315.

Loughlin, N.J.D. & Hillier, R.D. 2010: Early Cambrian Teichich-nus-dominated ichnofabrics and palaeoenvironmental analysisof the Caerfai Group, Southwest Wales, UK. Palaeogeography,Palaeoclimatology, Palaeoecology 297, 239–251.

Maas, A., Huang, D., Chen, J., Waloszek, D. & Braun, A. 2007:Maotianshan-Shale nemathelminths — Morphology, biology,and the phylogeny of Nemathelminthes. Palaeogeography, Pal-aeoclimatology, Palaeoecology 254, 288–306.

Maloof, A.C., Porter, S.M., Moore, J.L., Dud�as, F.€O., Bowring,S.A., Higgins, J.A., Fike, D.A. & Eddy, M.P. 2010: The earliestCambrian record of animals and ocean geochemical change.Geological Society of America Bulletin 122, 1731–1774.

M�angano, M.G., Buatois, L.A. & Rindsberg, A.K. 2002: Carbonif-erous Psammichnites: systematic re-evaluation, taphonomyand autecology. Ichnos 9, 1–22.

McIlroy, D. & Heys, G.R. 1997: Palaeobiological significance ofPlagiogmus arcuatus from the Lower Cambrian of central Aus-tralia. Alcheringa 21, 161–178.

Missarzhevsky, V.V. 1989: Oldest Skeletal Fossils and Stratigraphyof the Precambrian–Cambrian Boundary Strata, 1–237 pp.Nauka, Moscow.

Olivero, D. 2007: Zoophycos and the role of type specimens inichnotaxonomy. In Miller, W., III. (ed.): Trace Fossils – Con-cepts, Problems, Prospects, 219–231. Elsevier, Amsterdam.

Olivero, D. & Gaillard, C. 1996: Paleoecology of Jurassic Zoophy-cos from south-eastern France. Ichnos 4, 249–260.

Pacze�sna, J. 1996: The Vendian and Cambrian ichnocoenosesfrom the Polish part of the East-European Platform. PracePa�nstwowego Instytutu Geologicznego 152, 1–78.

Palij, W.M., Posti, E. & Fedonkin, M.A. 1983: Soft-bodied Meta-zoa and animal trace fossils in the Vendian and early Cam-brian. In Urbanek, A. & Rozanov, A.Y. (eds): UpperPrecambrian and Cambrian Palaeontology of the East EuropeanPlatform, 56–93. Publishing House Wydawnictwa Geolo-giczne, Warszawa.

Pearse, A.S. 1908: Observations on the behavior of the holothu-rian, Thyone briareus (Leseur). The Biological Bulletin 15, 247–303.

Rogov, V., Marusin, V., Bykova, N., Goy, Y., Nagovitsin, K.,Kochnev, B., Karlova, G. & Grazhankin, D. 2012: The oldestevidence of bioturbation on Earth. Geology 40, 395–398.

Rozanov, A.Y. & Sokolov B.S. (eds) 1984: Stage Subdivision of theLower Cambrian, Stratigraphy, 1–184 pp. Nauka, Moscow.

Rozanov, A.Y., Missarzhevsky, V.V., Volkova, N.A., Voronova,L.G., Krylov, I.N., Keller, B.M., Korolyuk, I.K., Lendzion, K.,Michniak, R., Pykhova, N.G. & Sidorov, A.D. 1969: Tommo-tian stage and the Cambrian lower boundary problem.Academy of Sciences of the USSR, Transactions 206, 1–380,Moscow.

Sappenfield, A., Droser, M.L. & Gehling, J.G. 2011: Problematica,trace fossils, and tubes within the Ediacara Member (SouthAustralia): redefining the Ediacaran trace fossil record onetube at a time. Journal of Paleontology 85, 256–265.

Schlirf, M. 2011: A new classification concept for U-shaped spre-ite trace fossils. Neues Jahrbuch f€ur Geologie und Pal€aontologie– Abhandlungen 260, 33–54.

Seilacher, A. 1955: Spuren und Fazies im Unterkambrium. InSchindewolf, O.H. & Seilacher, A. (eds): Beitr€age zur Kenntnis

des Kambriums in der Salt Range (Pakistan). Abhandlungen.Akademie der Wissenschaften und der Literatur, Mainz. Mathe-matisch-Naturwissenschaftliche Klasse 10, 373–399.

Seilacher, A. 1990: Aberrations in bivalve evolution related tophoto- and chemosymbiosis. Historical Biology 3, 289–311.

Seilacher, A. 1997: Fossil Art, 1–64 pp. Royal Tyrrell Museum ofPaleontology, Drumheller.

Seilacher, A. 1999: Biomat-related lifestyles in the Precambrian.Palaios 14, 86–93.

Seilacher, B. & Hagadorn, J.W. 2010: Early molluscan evolution:evidence from the trace fossil record. Palaios 25, 565–575.

Seilacher, A., Buatois, L.A. & Mangano, M.G. 2005: Trace fossilsin the Ediacaran-Cambrian transition: behavioral diversifica-tion, ecological turnover and environmental shift. Palaeogeog-raphy, Palaeoclimatology, Palaeoecology 227, 323–356.

Seilacher-Drexler, E. & Seilacher, A. 1999: Undertraces of SeaPens and Moon Snails and possible fossil counterparts. NeuesJahrbuch f€ur Geologie und Pal€aontologie – Abhandlungen 214,195–210.

Sigwart, J.D. & Sutton, M.D. 2007: Deep molluscan phylogeny:synthesis of palaeontological and neontological data. Proceed-ings of the Royal Society B: Biological Sciences 274, 2413–2419.

Smith, S.A., Wilson, N.G., Goetz, F.E., Feehery, C., Andrade,S.C.S., Rouse, G.W., Giribet, G. & Dunn, C.W. 2011: Resolvingthe evolutionary relationships of molluscs with phylogenomictools. Nature 480, 364–367.

Struck, T.H., Paul, C., Hill, N., Hartmann, S., H€osel, C., Kube,M., Lieb, B., Meyer, A., Tiedemann, R., Purschke, G. & Bleid-orn, C. 2011: Phylogenomic analyses unravel annelid evolu-tion. Nature 471, 95–98.

Sutton, M.D. & Sigwart, J.D. 2012: A chiton without a foot. Pal-aeontology 55, 401–411.

Sutton, M.D., Briggs, D.E.G., Siveter, D.J., Siveter, D.J. & Sig-wart, J.D. 2012: A Silurian armoured aplacophoran and impli-cations for molluscan phylogeny. Nature 490, 94–97.

Systra, Y.J. & Jensen, S. 2006: Trace fossils from the DividalenGroup of northern Finland with remarks on early Cambriantrace fossil provincialism. GFF 128, 321–325.

Telford, M.J., Bourlat, S.J., Economou, A., Papillon, D. & Rota-Stabelli, O. 2008: The evolution of the Ecdysozoa. PhilosophicalTransactions of the Royal Society B 363, 1529–1537.

Thomas, R.D.K. 2012: Implications of the occurrence of pairedanterior chaetae in the late Early Cambrian mollusc Pelagiellafrom the Kinzers Formation of Pennsylvania for relationshipsamong taxa and early evolution of the Mollusca. 2012 GSAAnnual Meeting in Charlotte (4–7 November 2012).

Thomas, R.D.K., Vinther, J. & Matt, K. 2010a: Structure and evo-lutionary implications of finely preserved chaetae associatedwith Pelagiella, a stem-group gastropod from the Kinzers For-mation (Early Cambrian) at Lancaster, Pennsylvania. ThirdInternational Palaeontological Congress, London (June 28–July 3, 2010).

Thomas, R.D.K., Vinther, J. & Matt, K. 2010b: Paired chaetaeassociated with spiral shells of the late Early Cambrian molluscPelagiella from the Kinzers Formation: taphonomy, functionalmorphology, and potential evolutionary relationships. 2010GSA Denver Annual Meeting (October 31–November 3 2010).

Uchman, A. & Dem�ırcan, H. 1999: A Zoophycos group trace fossilfrom Miocene flysch in southern Turkey: evidence for a U-shaped causative burrow. Ichnos 6, 251–259.

Vannier, J., Calandra, I., Gaillard, C. & _Zyli�nska, A. 2010: Priapu-lid worms: pioneer horizontal burrowers at the Precambrian-Cambrian boundary. Geology 38, 711–714.

Vinther, J. & Rudkin, D. 2010: The first articulated specimen ofPlumulites canadensis (Woodward, 1889) from the UpperOrdovician of Ontario, with a review of the anterior region ofPlumulitidae (Annelida: Machaeridia). Palaeontology 53, 327–334.

Vinther, J., Eibye-Jacobsen, D. & Harper, D.A.T. 2011: An EarlyCambrian stem polychaete with pygidial cirri. Biology Letters 7,929–932.

Vinther, J., Sperling, E.A., Briggs, D.E.G. & Peterson, K.J. 2012: Amolecular palaeobiological hypothesis for the origin of apla-


cophoran molluscs and their derivation from chiton-likeancestors. Proceedings of the Royal Society B 279, 1259–1268.

Weber, B., Hu, S.X., Steiner, M. & Zhao, F.C. 2012: A diverseichnofauna from the Cambrian Stage 4 Wulongqing Forma-tion near Kunming (Yunnan Province, South China). Bulletinof Geosciences 87, 71–92.

Wetzel, A. 1992: The New Zealand Zoophycos revisited - somenotes for clarification. Ichnos 2, 91–92.

Wetzel, A. & Werner, F. 1980: Morphology and ecological signifi-cance of Zoophycos in deep-sea sediments off NW Africa. Pal-aeogeography, Palaeoclimatology, Palaeoecology 32, 185–212.

Wilson, N.G., Rouse, G.W. & Giribet, G. 2010: Assessing themolluscan hypothesis Serialia (Monoplacophora + Polyplaco-phora) using novel molecular data. Molecular Phylogeneticsand Evolution 54, 187–193.

Yochelson, E.L. & Fedonkin, M.A. 1997: The type specimens(Middle Cambrian) of the trace fossil Archaeonassa Fentonand Fenton. Canadian Journal of Earth Sciences 34, 1210–1219.

Zhang, X.-G., Bergstr€om, J., Bromley, R.G. & Hou, X.G. 2007:Diminutive trace fossils in the Chengjiang Lagerst€atte. TerraNova 19, 407–412.


the tommotian phase of the early cambrian agronomic revolution in the carbonate mud environment of...

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