The -type impressions in the Jinxian successions of Liaoning Province, northeastern


Moczydłowska, M. & Meng, F. 2016: The Ediacaran Aspidella-type impressions in the Jinxian successions of Liaoning Province, northeastern China. Lethaia, DOI: 10.1111/let.12173.

Macroscopic impression from the Xingmincun Formation of the Jinxian Group, Liaoning Province of northeastern China, are identified as members of the Aspidella plexus of Ediacaran age. This is the first recognition of the taxon in the Liaoning Province, although such fossils have been previously recorded in the succes- sion, but were referred to as new species and relegated to an earlier age. A revision of the taxonomic interpretation and relative age estimation of the pre- vious record is provided, as well as an evaluation of abiotic vs. biotic processes that could produce similar structures to studied impressions. The mode of preservation of the fossils is considered from a biochemical point of view and along with the proper- ties of organic matter in the integument of soft-bodied metazoans. The selective preservation of the Ediacaran organisms, including metazoans, as impressions (moulds and casts) against the organically preserved contemporaneous cyanobacterial and algal , and an exceptionally small number of terminal Ediacaran meta- zoan fossils (Sabellidites, Conotubus and Shaanxilithes), demonstrates the non-resistant characteristics and the very different biochemical constitution of the Ediacaran meta- zoans compared with those that evolved in the and after. The refractory biomacromolecules in cell walls of photosynthesizing microbiota (bacterans, cutans, algaenan and sporopollenin groups) and in the chitinous body walls of Sabellidites contrast sharply with the labile biopolymers in Ediacaran metazoans known only from impressions. The newly emerging biosynthesis of resistant biopolymers in metazoans (chitin and collagen groups) initiated by the annelids at the end of Ediacaran and fully evolved in Cambrian metazoans, considered with the ability to biomineralize, made their body preservation possible. The Chengjiang and Burgess metazoans show evidence of this new biochemistry in body walls and cuticles, and not only because of the specific taphonomic window that enhanced their preservation. □ Aspidella plexus, early metazoans, organic biochemistry, selective preservation, .

Małgorzata Moczydłowska [malg[email protected]], Department of Sciences, Palaeobiology, Uppsala University, Villav€agen 16, SE 752 36 Uppsala, Sweden; Fanwei Meng [[email protected]], State Key Laboratory of Palaeontology and Stratigra- phy, Nanjing Institute of Geology and Palaeontology, Chinese Academy of Sciences, 39 East Beijing Road, Nanjing 210008, China; manuscript received on 25/04/2015; manuscript accepted on 3/12/2015.

Ediacaran macroscopic fossils are renowned for their the rationale used to describe their organic proper- preservation as impressions (moulds and casts), less ties. The exceptions are the organically preserved ter- frequently as carbonaceous compressions (contain- minal Ediacaran annelidan Sabellidites, whose robust ing organic biofilms) or traces, and exceptionally as wall is chitinous (Moczydłowska et al. 2014; M. organically preserved and biomineralized body fos- Moczydłowska, unpubl. data), and the carbonaceous sils (Gehling et al. 2000; Narbonne 2005; Fedonkin compressions of Conotubus, Shaanxilithes, Maw- et al. 2007; Hua et al. 2007; Cai et al. 2011; sonites, and Khatyspytia of as-yet- Laflamme et al. 2012; Moczydłowska et al. 2014; unresolved biochemistry and affinities (Hua et al. Tarhan et al. 2015). Recognized in various preserva- 2007; Zhu et al. 2008; Grazhdankin 2014; Tarhan tion modes and ecological niches on shallow shelves et al. 2014). Among them, Eoandromeda was inter- vs. deep marine slopes, the fossils represent soft- preted as a ctenophore (Tang et al. 2011). This is in bodied organisms including metazoans (Zhu et al. sharp contrast to contemporaneous uni- and multi- 2008; Ivantsov 2009; Xiao & Laflamme 2009; Sper- cellular fossils of cyanobacterial and algal origin that ling & Vinther 2010; Narbonne 2011; Narbonne synthesized cell walls and trichome sheaths that are et al. 2014; Liu et al. 2015). They comprised body extremely resistant to biodegradation, diagenesis, walls made from non-resistant organic matter, a fact and laboratory acid treatment (Moczydłowska et al. verified by observations in all known sites and 1993; Xiao et al. 2002; Grey 2005; Moczydłowska modes of preservation with a few exceptions, and 2008). Macroscopic carbonaceous compressions of

DOI 10.1111/let.12173 © 2016 The Authors. Lethaia published by John Wiley & Sons Ltd on behalf of Lethaia Foundation. This is an open access article under the terms of the Creative Commons Attribution-NonCommercial-NoDerivs License, which permits use and distribution in any medium, provided the original work is properly cited, the use is non-commercial and no modifications or adaptations are made. 2 M. Moczydłowska & F. Meng LETHAIA 10.1111/let.12173 the Lantian and Miaohe biotas (early and late Edi- 2013), or even non-metazoan, microbial organisms acaran respectively) showing complex morphologies (Grazhdankin 2014; Liu et al. 2015). of fan-shaped and branching algal thalli and colonial Aspidella fossils have been recently noted in South (Yuan et al. 1999, 2011; Xiao et al. China, in the Shibantan Member of the Dengying 2002) are also within the group of photosynthesizing Formation in the Yangtze Gorges area, Hubei Pro- organisms. Unnamed carbonaceous compressions vince (Meyer et al. 2013; Chen et al. 2014), although from the Ediacaran Khatyspyt Formation in not yet systematically described or compared with may be microbial colonies or seaweeds (Grazh- other modes of preservation. Specimens of a Sprig- dankin et al. 2008; Grazhdankin 2014). gia-type holdfast reported by Chen et al. (2014, fig. Biological affinities and phylogenetic relationships 3D) from the same area and stratigraphical interval of most Ediacaran taxa are not yet resolved, nor is of the Shibantan Member are considered here to be there consensus on whether certain taxa are meta- synonymous with Aspidella, as are those identified as zoans or of enigmatic affinities unknown among a possible Ediacaran-type by Duda et al. (2014, modern phyla (Erwin et al. 2011; Narbonne 2011; fig. 2A). These, together with the present specimens Yuan et al. 2011). It is generally accepted that the from the Liaoning Province, are the current records comprised representatives of pori- of Aspidella in China. fera, ctenophorans, cnidarians, aplacophorans, and We report a new record of discoidal impressions stem- and crown-group bilaterian metazoans, identified as an Aspidella form- preserved in including molluscs (Narbonne 2005; Fedonkin et al. several taphonomic morphs consistently bearing the 2007; Ivantsov 2009; Xiao & Laflamme 2009; Vinther characteristic of the Aspidella plexus, which is pri- et al. 2012; Laflamme et al. 2012; Menon et al. 2013; marily the disc-shaped body with concentric rings Gehling et al. 2014; Narbonne et al. 2014; Yin et al. and a central boss (Gehling et al. 2000; Fedonkin 2015). Recognition of siboglinid affinity of Sabel- et al. 2007; Laflamme et al. 2011). This is the first lidites suggests the presence of the crown-group recognition of the Aspidella plexus in the Liaoning Annelida (Moczydłowska et al. 2014; but see also Province of northeastern China and includes revised Parry et al. 2014). Alternative interpretations that taxa previously assigned to junior synonyms by certain taxa are fungi (Peterson et al. 2003), terres- Zhang et al. (2006). The age of strata containing the trial lichens and slime moulds (Retallack 2012, assemblage is estimated to be Ediacaran at c. 580– 2013), or microbial colonies (Grazhdankin et al. 550 Ma based on the global chronostratigraphical 2008; Grazhdankin 2014) have not received wide- range of such fossils (Grazhdankin 2014). spread support (Menon et al. 2013; Xiao et al. 2013; The assemblage studied here should not be con- Chen et al. 2014). fused with structures recorded approximately The disc-like, flat- to high-relief impressions pre- 1600 m below in the underlying Changlingzi Forma- served on bedding planes are the predominant fos- tion (Figs 1 and 2) that originally were attributed to sils within the Ediacaran assemblages in siliciclastic the fossils (Xing & Liu 1979) and sub- successions worldwide (Fedonkin et al. 2007; sequently interpreted as pseudo-fossils and repre- Laflamme et al. 2013), but they also occur in car- senting sedimentary, gas escape structures ( bonate facies (Grazhdankin et al. 2008; Chen et al. 1986; see below). 2014). Originally described as morphologically dis- parate genera and species, they have been substan- tially reduced as a result of depositional and taphonomic analyses that have eliminated superflu- Geological setting and age of ous synonyms (Gehling et al. 2000; Narbonne 2005; succession Fedonkin et al. 2007). The most common discoidal impression is the Aspidella plexus, which comprises The collection of fossils derives from clayey shale in a great variety of morphs, and its type species is A. the middle member of the Xingmincun Formation, terranovica Billings, 1872. It has been recognized as Jinxian Group, at the Yangjue and Yangtun localities a buried holdfast of frond-like organisms (Gehling in the Liaoning Province of northeastern China et al. 2000) and accepted as such in subsequent (Fig. 1). The Neoproterozoic (Sinian) and Cambrian works (Erwin et al. 2011; Chen et al. 2014; Nar- successions of the region comprise siliciclastic and bonne et al. 2014; Tarhan et al. 2015). Alternatively, carbonate rocks. They are divided into the Wuhang- Aspidella has been suggested to represent vagile, shan and Jinxian groups, which are paraconformably epifaunal of the cnidarian grade, having the overlain by the Cambrian Dalinzi and Jianchang for- ability to periodically burrow and actively move to mations (Hong et al. 1986, 1988; Zhang et al. 2006; adjust to accumulation of (Menon et al. Fig. 2). The entire succession is steeply dipping and LETHAIA 10.1111/let.12173 Ediacaran impressions from China 3

Fig. 1. Location map of fossil localities at Yangjue and Yangtun in the Liaoning Province, northeastern China. intruded by the andesites. A paraconformity 2011) also do not constrain the age. Values of geo- also separates the Xingmincun and the Getun forma- chemical signatures of d13C and 87Sr/86Sr from car- tions. The Jianchang Formation contains lower bonates in the Jinxian Group that contain Aspidella Cambrian Redlichia that indicate a high were suggested to be correlative with those from biostratigraphical position in older successions, such as the at c. (Peng et al. 2009). The Dalinzi Formation paracon- 800 Ma (Kuang et al. 2002). However, these older formably underlies the Jianchang Formation and is a records of elemental fractionation curves remain to relatively thin succession (c. 72 m). Although it is be constrained by numerical ages to be unequivo- unfossiliferous, it most likely belongs to the basal cally distinguished in the global Neoproterozoic pat- Cambrian (Fig. 2) because bradoriid fossils were tern of geochemical changes and applied in reported, although not illustrated, from the underly- chemostratigraphy. ing Getun Formation (Zhang et al. 2006). If this The proposed older-than-Ediacaran ages of the occurrence is confirmed, the latter formation should Jinxian Group are neither directly constrained by also be attributed to the Cambrian System. The Pre- isotopic datings nor indirectly by geochemical signa- cambrian relative age of the Jinxian and Wuhang- tures set in a chronostratigraphical time frame. The shan groups was inferred from the regional scale of Jinxian Group underlies the unequivocally, biostrati- the sequence of rocks containing with graphically recognized Cambrian strata with a para- age-diagnostic taxa, the Chuaria– conformable contact that is on a regional scale Tawuia assemblages, and discoidal impressions com- (Hong et al. 1988; Zhang et al. 2006) and probably parable to the Ediacara-type fauna (Hong et al. comprises a short time gap. This is inferred because 1988; Chen 1991; Hua & Cao 2003; Fig. 2). Stroma- there are no coarse-grained clastic rocks that would tolites from the Shisanlitai Formation are correlative indicate a major tectonic movement and involve a of the Upper Riphean or –Cryogenian substantial time interval. The lack of glacigenic sedi- (c.1000-650 Ma) assemblages (Hua & Cao 2003). ments correlative with the Neoproterozoic ice ages The shale in the Xingmincun Formation was in successions of the Liaoning Province dated to 650 Ma by the Rb-Sr method (Hong et al. indicates that they are either pre- or post-Cryogen- 1988), but not confirmed by other methods. The ian. detrital in the lower Xingmincun Formation Because the discoidal fossils were interpreted as dated to a minimum age of 924 Ma (Yang et al. non-Ediacara-type biota and because the succession 4 M. Moczydłowska & F. Meng LETHAIA 10.1111/let.12173

Fig. 2. Stratigraphical column of the Neoproterozoic-Ediacaran Wuhangshan and Jinxian groups of the Liaoning Province showing the occurrence of Aspidella in the Xingmincun Formation, and carbonaceous compression fossils throughout the entire succession. Record of carbonaceous films and microfossils according to Hong et al. (1988), Chen (1991) and Hua & Cao (2003). does not contain any glacigenic deposits, its relative Yangtun localities in the Liaoning Province, north- age was proposed to be Neoproterozoic and pre- eastern China. The specimens are preserved on bed- Ediacaran (Zhang et al. 2006). We contest both the ding planes (sole and surface) of shale and were identification of the aforementioned impression fos- recovered from six layers within a 68-m-thick inter- sils and the estimation of age of the succession by val of the Xingmincun Formation (Ou & Meng Zhang et al. (2006) and conclude that the assem- 2013; Fig. 2). The lithostratigraphical position of the blage is typical of the Aspidella plexus and of Edi- fossiliferous interval within the Jinxian Group is acaran age, as has been consistently established broadly 170–240 m below the paraconformity at the elsewhere (Gehling et al. 2000; Narbonne 2005; base of Cambrian in the regional scale of the geologi- Fedonkin et al. 2007; Laflamme et al. 2011; Grazh- cal succession. Some 220 specimens were studied dankin 2014; Narbonne et al. 2014; Tarhan et al. and measured under an optical reflected light micro- 2015). scope, and certain specimens are photographed and documented herein. Additional studies using a scan- ning electron microscope on the surface of speci- Material and methods mens and their perpendicular sections appeared inconclusive in detecting organic material preserva- The rock samples with discoidal impression speci- tion in contrast to mineral grains of the host sedi- mens were collected from two surface successions of ment. The moulds and casts were observed only as the Xingmincun Formation in the Yangjue and low relief or flat depressions within fine-grained sed- LETHAIA 10.1111/let.12173 Ediacaran impressions from China 5


Fig. 3. Aspidella plexus impressions preserved as low hyporelief on bed sole (A, B), and flat epirelief on bed surface (C). Central boss is prominent in morphs preserved as casts (hyporelief) as well as the concentric ring and marginal zone; the latter is diagenetically mineralized and seen as yellow crust in A (specimen NIGP 163245) and B (specimen NIGP 163246). Flat mould (epirelief) without central boss but with clear marginal zone, which is covered by circular patches of diagenetically precipitated pyrite, is seen in C (specimen NIGP 163247). iment. As in previous studies (Laflamme et al. 2011; with the Ediacaran or any other Precambrian biota. Meyer et al. 2013), the organic matter was not pre- The authors followed the taxonomic assignment of served even if the sediment layers surrounding the the species by Hong et al. (1986) and described flat, Aspidella moulds were recognized as chemically dis- circular and ellipsoidal in outline fossils with a mar- tinct by authigenic mineralization of the biofilm or ginal rim and concentric or spiral ridges on both microbial envelopes (Laflamme et al. 2011). sides that were preserved as thin membranes replaced The specimens are housed in the museum collec- by quartz and chlorite. The specimens had a diameter tions of the Nanjing Institute of Geology and of 1.5–45.0 mm. There was no information on the Palaeontology with the reference numbers NIGP position of fossils (surface or sole of beds) and their 163245, NIGP 163246, NIGP 163247 for specimens mode of preservation. It was inferred that the fossils illustrated in Figure 3A–C, respectively, and NIGP comprised two parallel layers (sheaths) resembling 163248, NIGP 163249, NIGP 163250 and NIGP biofilms with filament-like and -like granule 163251 for Figure 4A–D respectively. structures. We consider these structures to be micro- crystals of diagenetic minerals deposited or precipi- tated on the template of the decaying body, but no Revision of the previous records of convincing evidence of biofilms or organic matter the Jinxian fossils ultrastructure is apparent. The concentric and spiral ridges, it was suggested, show rhythmic growth lines, The discoidal macroscopic impressions were discov- whereas some specimens were juxtaposed against one ered in the middle part of the Xingmincun Forma- another like twins exhibiting an asexual reproduction tion, south Liaoning Province and attributed to the stage (Zhang et al. 2006). The ‘twin specimens’ are Sinian System (Hong et al. 1986). Three new genera not the result of reproduction but rather superposi- of ‘medusa-like’ fossils, Liaonanella, Jinxianella and tion and burial distortion. Whereas the concentric Daliania – each consisting of two species – were ridges are a consistent feature, the spiral geometry is established by Hong et al. (1986). Subsequently, an artefact of taphonomic deformation and not Hong et al. (1988) extended the documentation of clearly visible. The elliptical specimens do not show this assemblage, which consisted of moulds and casts any increased growth rate along their long axis, but of soft-bodied fossils preserved on bedding planes have gained their shape by lateral compression dur- and interpreted as metazoans. These fossils have been ing burial (the succession is tectonically deformed characterized as subcircular to ellipsoidal, possessing and cleaved), resulting in folds parallel to the long a central disc and an outer ring with radial canals, axis. Some radial wrinkles were probably caused by and have been attributed to six previously erected shrinkage of the soft bulbous body and its collapse. species. They have been considered taxonomically Similar to the ‘twin specimens’ reported by Zhang different from Ediacara-type fauna, and thus consid- et al. (2006) are those from the Aspidella assemblage ered new taxa, although of the same age. Study of in the Ediacara Member of South and impression fossils from the same succession by renamed as ‘kissing ‘individuals or pairs of Aspidella Zhang et al. (2006) did not draw any comparisons (Tarhan et al. 2015), yet without comparison to the 6 M. Moczydłowska & F. Meng LETHAIA 10.1111/let.12173



Fig. 4. Aspidella plexus impressions preserved as flat epirelief on bed surface (A-D) showing various taphonomic morphs. A, laterally compressed specimen with parallel taphonomic wrinkles that demonstrate original plasticity of soft body of the organism. Specimen NIGP 163248. B, D, specimens located in close proximity showing marginal zone encrusted by diagenetic pyrite mineralization (B, speci- men NIGP 163249) and smooth surface (D, specimen NIGP 163250). C, pyrite framboids crystallized in patches on specimen surface are a common feature, specimen NIGP 163251. former record. The Australian specimens are (Fig. 4A,C) are probably the result of distortion thought to have been deformed by non-synchronous caused by lateral compression of strata during tilting growth and not originated from asexual fission. and compressional stress that formed cleavage. In our opinion, the assemblage studied by Zhang The discoidal fossils possess sharply defined outli- et al. (2006) conforms to the taphonomic morphs of nes and circular, concentric structures in the form of the Aspidella plexus, as observed in the assemblage a wide marginal zone, with convex narrow ridges in of the same geological derivation considered in this approximately the middle of the disc radius, and a paper. small, elevated circular boss in the centre of the disc (Fig. 3A,B). The marginal zone is flat (Figs 3, 4B) or has a slightly raised, narrow rim (Fig. 4A,C). A cir- Morphology and preservation of cular ridge is prominent in specimens having posi- discoidal impressions tive relief (Fig. 3A,B), but not present or faintly visible in flat specimens (Figs 3C, 4). The central Our observations are based on over 200 specimens. boss is observed in low positive hyporelief specimens The specimens are circular to oval in outline and pre- (Fig. 3A,B). The overall diameter of specimens is – = – served as macroscopic inorganic impressions (follow- 2.0 25.0 mm (n 221), with a central boss 1.0 – ing the terminology of Gehling et al. 2000) that are 3.0 mm, and a circular ridge 1.0 2.0 mm wide – flat (epirelief) on the surface or with low convex relief (Fig. 5A C). These dimensions belong to the lowest (positive hyporelief) on the sole of the bedding planes sector of the total range of Aspidella morphs, which – of the shale. They occur as solitary individuals or, in a in a global compilation is commonly 2.0 80.0 mm, few cases, near one another (Figs 3, 4). The oval but reaches a diameter 500.0 mm (Gehling et al. shape and superficial folds parallel to the long axes of 2000; Fedonkin et al. 2007; Menon et al. 2013; Tar- the discs and extending across some specimens han et al. 2015). Large specimens newly recovered LETHAIA 10.1111/let.12173 Ediacaran impressions from China 7

(Gehling et al. 2000 and references therein) and its taphonomic morphs. The variability in Aspidella taphonomic morphs is the result of preservation and environmental conditions as has been analysed in other occurrences of discoidal impressions of Edi- acaran age (Gehling et al. 2000; Fedonkin et al. 2007; Gehling & Vickers-Rich 2007; Laflamme et al. 2011; Menon et al. 2013; Tarhan et al. 2015). The clayey shale of the Xingmincun Formation does not display any current or wave sedimentary structures and accumulated below wave-base level in shallow marine environments. We have observed neither any pattern of directional orientation due to current flow nor horizontal distribution of speci- mens along bedding planes or preservation gradients between morphotypes, which are rather uniform in morphology and size variation, more likely due to the random distribution. The preservation of Aspi- della by casts (infill of external mould by host sedi- ment) or moulds (imprinted marks by pressing against a surface) of soft bodies, which were subse- quently totally decayed, has left no organic, miner- alogical or geochemical record of the bodies. There is no evidence of microbial mats in the part of succession containing impressions. Direct evi- dence would be provided by the organic preserva- tion of laminae, microfossils, mat fabrics or biofilms, or at least organic draping of the sediment layers. Indirect evidence could be inferred from microbially induced sedimentary structures or a sediment texture that is like ‘elephant skin’ or with Fig. 5. Size distribution of Aspidella specimens in reference to a wrinkled surface (Gehling 1999; Gehling & Droser their length of the major axis (A), ratio of maximum to mini- 2009; Noffke 2010; Noffke et al. 2013; Mariotti et al. mum diameter (B) and surface area (C). 2014). It is unclear whether the so-called textured organic surface associated with Aspidella in South from India that are 75 cm in diameter (Srivastava Australia and attributed to the taxon Funisia of sup- 2014) may belong to this plexus. posed eukaryotic origin (Tarhan et al. 2015) is There is no observed relationship between diame- organic, and its origin is certainly unclear. ter and morphology (number of ridges or rings) However, the specimens studied are covered by among studied specimens and their size distribution pockets of authigenic pyrite framboids, mostly in is in the lower size range of the form-genus. The pre- marginal zones (Figs 3A, C, 4C), and by chlorite sent assemblage that is preserved in fine-grained particles. Pyrite framboids are a by-product of bacte- clayey sediment of the inner marine shelf differs rial decay of soft bodies and are typical of the preser- from the assemblages comprising more diverse vation in the presence of microbial mats or biofilms morphs and within broader size ranges, which were associated with clay particles (Gehling 1999; Gehling observed in medium- to coarse-grained et al. 2000; Laflamme et al. 2011). of shallow marine and deltaic facies (see Tarhan et al. 2015). There are no structures such as radiat- ing ridges or grooves, as observed in other morphs of the Aspidella plexus and that occur in coarser sed- Biotic vs. abiotic origin of studied iments, because the specimens are flat- or low-relief impression structures taphonomic morphs that are characteristic of clayey facies. The present preservation mode as simple, The studied impressions, among many others of rimmed impressions with a central boss is, however, such morphological appearance in the Ediacaran consistent with diagnostic features of the genus strata, are preserved without any remains of organic 8 M. Moczydłowska & F. Meng LETHAIA 10.1111/let.12173 matter that would directly prove their biotic origin. sediment laminae around the specimens (Sun 1986). We considered possible abiotic processes that could On the surface of beds, they appear as flat concentric produce comparable structures and mimic the shape rings or concave epireliefs. Such features are and relief of fossils that are left after a total decay of observed in sedimentary gas eruptions because of the organic matter in bodies of the organisms that the pulsating release of gas and water bubbles, such produced them. However, those abiotic structures as those formed in modern environments of a sandy do not conform to our morphological observations, beach intertidal zone (Sun 1986). They may be simi- which are consistent with the interpretation that lar in diameter and distribution on the bed surfaces they are moulds and casts of soft-bodied organisms. to true fossil impressions, but the persistent features The preservation of flat specimens of Aspidella on of gas/fluid escape structures seen in cross-sections the sole of shale from the of are the central, vertical channels and bent sediment the , eastern Newfoundland, and laminae around these channels. elegantly argued regarding its organic origin (Gehl- In thin sections of Aspidella that are cut perpen- ing et al. 2000; text-fig. 8E), is similar to the studied dicular to the bedding plane (Gehling et al. 2000; material. In the present assemblage, certain speci- Menon et al. 2013; Meyer et al. 2013; Tarhan et al. mens (Fig. 3A,B) are identical to variant morphs 2015), the specimens that are convex on both sides with simple rings being the only morphology pre- are observed as a sand-filled body, i.e. a cast, in mud served in the of the Ediacara Member of and silt layers, or lower-side convex and upper-side South Australia (Tarhan et al. 2015; fig. 3A, C). The truncated specimens, as sand casts in parallel-lami- latter Aspidella specimens are without any reserva- nated sandy event beds As a rule, where preserved in tion considered to be biogenic, moulds of multicel- coarse siliciclastic , the Aspidella casts lular benthic organisms, and part of a more diverse infilled by sand are more convex (or three-dimen- assemblage of its morphs and other Ediacaran sional) even if they are associated with inter-layers of genera. fine-grained mud or clay because of the differential In studies of the Ediacaran impression macrofos- compaction of the overlying and underlying mud sils, as well as trace fossils, the possibility of misiden- laminae (Gehling et al. 2000). Deformed specimens tifying abiotic structures has been tested in several are observed in slumped sand casts in mud-sand cases (Sun 1986; Farmer et al. 1992; Gehling et al. inter-layers. Convex specimens occur also in bitumi- 2000; Jensen et al. 2006; Chen et al. 2013; Menon nous laminated (Grazhdankin et al. et al. 2013; Meyer et al. 2014). The considered sedi- 2008). However, flat- or low-relief mould specimens mentary and mechanical structures, which may be resulting from the uniform compaction of clay are similar because of their discoidal shape and the pres- not clearly observed in thin sections, and this is the ence of concentric wrinkles, were interpreted as hav- case of studied specimens, which are evidently with- ing formed in mineral , rhythmically out vertical channels. precipitated silica, in moulds and casts of nodules, By documenting various morphs of the Aspidella gas and fluid eruptions or escape craters, and in plexus fossils in relation to different lithological set- dewatering pillars. Biogenic structures with some tings of their preservation in sand and clay substrate, resemblance include redeposited sheaths of algal Gehling et al. (2000) distinguished features of colonies and microbial mats (Gehling 1999; Noffke biomechanical deformation from those that were 2010; Noffke et al. 2013). genuinely organismal morphological features. Fea- Restudy of the Cyclomedusa-like impressions from tures produced by deformation and taphonomic the Precambrian strata of the southern Liaoning changes because of dewatering, collapse and com- Province (Fig. 1) resulted in their being recognized paction, and pattern of degradation dependent on as pseudo-fossils of mechanical origin (Sun 1986). the substrate properties and degree of decay are These impression structures derive from the Chan- numerous, such as concentric wrinkles, grooves, glingzi Formation of the Wuhangshan Group, which rings or annulations, marginal rim, and radial lies approximately 1600 m below the Xingmincun grooves. Genuine morphological features are few: Formation of the Jinxian Group (Fig. 2). They were bulb shape, basal protrusion and surface stem. Thus, originally attributed to several species of the fossil the surface marks preserved in Aspidella are mostly taxon Cyclomedusa (Xing 1976; Xing & Liu 1979), abiotically induced on the decaying organism. In which is now recognized as a junior of certain occurrences of Aspidella, the bedding surface Aspidella (Gehling et al. 2000; Fedonkin et al. 2007). textures of entombing sediments are consistent with Thin sections of the Cyclomedusa-like structures the presence of microbial mats (Gehling 1999). Indi- show funnel-shaped pits with prominent central, rect evidence of microbial mats are elephant skin vertical channels filled with calcite, and distorted texture, iron oxide or carbonaceous coating, bacteri- LETHAIA 10.1111/let.12173 Ediacaran impressions from China 9 ally induced mineralization, and enhanced pyrite similar and recognized as the Fermeuse-type (see framboid precipitation (Fedonkin 1992; Narbonne Gehling et al. 2000; Narbonne 2005; Laflamme et al. 1998; Gehling et al. 2000; Noffke et al. 2013). How- 2011). Moreover, a persistent feature that is univer- ever, even in successions rich in microbial mat lami- sal for the occurrences of the Ediacaran fossils, nation (Gehling 1999; Grazhdankin et al. 2008; regardless of the environmental and taphonomic Meyer et al. 2013; Chen et al. 2014), there are no conditions, is the selective preservation of macrofos- recorded specimens of preserved organic matter sils as inorganic impressions, with very few excep- from the body wall or integument and internal tions, in contrast to organically preserved tissue. microfossils within these successions. These organi- The specimens described as ‘discs of the Jinxian cally preserved microfossils, which are often three- biota’ and as a new type of fossil (Zhang et al. 2006; dimensional and robust enough to be extracted, are discussed above), which are here synonymized with recognized as photosynthetic cyanobacteria and Aspidella, have been observed in thin sections and algae (see below). Similarly, the macroscopic car- analysed in elemental composition by SEM/EDX bonaceous compressions recorded in the lower Edi- (scanning electron microscope with an energy-dis- acaran Lantian and Miaohe successions are algal in persive X-ray detector). They appear as thin micro- origin, perhaps with a few putative metazoans (Yuan crystalline quartz and chlorite membranes parallel to et al. 1999, 2011; Xiao et al. 2002). the bedding plane and without any carbonaceous In Finnmark, the assemblage of impressions material (Zhang et al. 2006). Thin and sandwiched derives from the Innerlev Member, Stappogiedde between the sediment layers, the specimens do not Formation (Farmer et al. 1992). The discoidal speci- show any vertical structures that could be abiotically mens preserved in epirelief and hyporelief in silt- formed. stone and fine-grained sandstone were originally We have not found any features attributed to the attributed to Cyclomedusa, , Beltanella, aforementioned abiotic structures in the cross-sec- Nimbia and . With the exception of Hie- tions of the layers containing the impressions in our malora, which shows radial impressions of morpho- collection. Neither distinct bacterial mat lamination logical structures, such as tentacles (Gehling et al. nor wrinkled surface structures or sediment micro- 2000; Fedonkin et al. 2007; Grazhdankin et al. bial textures have been observed in the sediment. 2008), surface features of these taxa are concentric in The specimens do not resemble microbial colonies geometry and mostly taphonomic. The specimens or rip-off fragments of mats. They are consistently are elliptical in outline (long axis parallel to the shaped as discs with very regular and sharp-outlined strike of the cleavage), with concentric furrows, edges that are in strong contrast to the appearance ridges or faint radial wrinkles, and a central boss. of redeposited microbial mats. Their smooth surface Their diameter ranges from 13.0 to 50.0 mm. They is dissimilar to the textured microbial mat frag- are taphonomic variants and belong to the Aspidella ments. We exclude abiotic mechanisms for forming plexus (Narbonne 2005; Hogstr€ om€ et al. 2013). the described structures from the Xingmincun For- The Finnmark assemblage is preserved without mation, or the possibility that they represent any evidence of organic body walls, associated reworked, resistant organic remains of microbial microbial mats, or biofilm coatings. Conversely, the mats being redeposited in local environments. The organically preserved cyanobacterial and algal structures are impression fossils of the soft-bodied microfossils occur in the underlying and succeeding organisms belonging to the Aspidella plexus. strata, whereas macroscopic Sabellidites occurs above the interval with impression fossils (Vidal & Siedle- cka 1983; Farmer et al. 1992; Hogstr€ om€ et al. 2013). Taphonomic comparisons This evident selective preservation indicates that the properties and biochemistry of organic matter com- The taphonomic variants and size range of Jinxian prising the Ediacaran soft-bodied metazoans (Aspi- Aspidella are similar to the assemblages occurring in della and Hiemalora) were very different from those the fine-grained siliciclastic successions in outer shelf of photosynthesizing microbiota and the annelidan to slope settings, such as in Avalonian England Sabellidites (Moczydłowska 2008; Moczydłowska (Charnwood Forest), the Avalon Peninsula in New- et al. 2014). Tectonic deformation and thermal foundland and northwest Canada, and Finnmark in activity affected the entire succession in Finnmark northeastern (Farmer et al. 1992; Narbonne during the early Palaeozoic Caledonian . 2005, 2007; Menon et al. 2013; Narbonne et al. The thermal processes altered the organic matter 2014; ). The burial and diagenetic conditions differ buried in sediments, as is shown by the maturation between these areas, but the preservation mode is of resistant walls, or transformed and 10 M. Moczydłowska & F. Meng LETHAIA 10.1111/let.12173 mobilized the hydrolysable and labile organic frac- dankin et al. 2008). Moreover, some are fragmentar- tion, causing its escape and leaving only the impres- ily preserved as carbonaceous compressions on sions of soft bodies behind. The selective impression moulds, but not Aspidella. Those frag- preservation of organic matter in fossils is explained ments of carbonaceous compressions may be attrib- by the constituent labile polymers in the body walls uted to algal thalli or microbial colonies rather than of Ediacaran metazoans, in contrast to refractory metazoan fossils (Grazhdankin et al. 2008). biomacromolecules in cell walls of photosynthetic Carbonaceous compressions of the Lantian and microbiota and in the chitinous wall of Sabellidites. Miaohe biotas in China are predominantly photosyn- Similarly, tectonic and thermal processes affected thetic cyanobacteria and algae, and even if they also the successions in the Avalon area (the early Palaeo- comprise metazoans, the properties of the organic zoic Appalachian Orogeny) and in northwest matter in these metazoans cannot be known because Canada (the Cordilleran Orogeny), where the successions are diagenetically permineralized. organic-walled microfossils are preserved in both the These biotas are preserved because of the silicification Proterozoic and Cambrian rocks (Hofmann 1985, of the host calcitic mudstone and thus cannot Hofmann 1994; Baudet et al. 1989; Parsons & contradict the observations and the proposed inter- Anderson 2000). However, the Ediacaran macrofos- pretation that the Ediacaran metazoan organisms sils are typically preserved as impressions (Narbonne were made of non-resistant biopolymers (see below). 2005, 2007; Narbonne et al. 2014). With regard to other carbonaceous compression In the White Sea area, the effect of selective fossils, it is true in some cases of conditions and preservation is even more distinct. The succession taphonomic modes leading to exceptional preser- lies almost horizontally and is highly uplifted, mildly vation, such as those in the terminal Ediacaran lithified, yet thermally altered because of granitic Gaojiashan biota or middle Cambrian Burges intrusions and volcanism. The organically preserved Shale biota, that authigenic mineralization (pyriti- Sabellidites-like and algal fossils are found in the zation and aluminosilicification) and kerogeniza- same sediment intervals with diverse fossils includ- tion allowed preservation of soft-bodied ing, among others, , , , metazoans (Gaines et al. 2008; Cai et al. 2012; and Aspidella, which are as a rule Schiffbauer et al. 2014). However, these processes impressions (Fedonkin et al. 2007). This supports are not the only causes for making possible the the interpretation that the thermal maturation of preservation of soft bodies, because without them organic matter eliminated the soft-bodied Ediacaran and in common burial conditions on shallow fossils from the record because of their biochemistry marine shelf, the tubular metazoan Sabellidites is and non-resistance. three-dimensionally organically preserved; it is not The classical Ediacaran deposits of South Australia mineralized and not coated by minerals. This are medium- to coarse-grained sandstones of the implies that the major factors leading to organic Ediacara Member of the Rawnsley Quartzite and preservation were refractory biopolymers in contain diverse assemblages of soft-bodied fossils organic matter in the integument of the organ- known as the Ediacara Biota, including a great vari- ism’s tube (chitin) and anoxic burial conditions ety of Aspidella morphs (Tarhan et al. 2015). Not a in the bottom sediment (Moczydłowska et al. single carbonaceous compression or organically pre- 2014). served specimen of any taxon is known in this site, which represents deposits accumulated in the delta front to canyon floor environments and below the Properties of organic matter in wave base (Gehling & Droser 2013). The red beds Aspidella and Ediacaran metazoans associated with the Ediacara Member indicate oxida- tion of the shallow marine strata in high-energy con- The lack of carbonaceous material preservation in ditions (evident by slumping, mass flow, transport Aspidella in all case studies, regardless of burial con- of sediment and fossils), but this process alone may ditions and preservation modes, suggests that the not be the only reason for the lack of organic preser- organic matter comprising the soft-bodied organ- vation of fossils, which are very abundant and den- isms producing the impressions was non-resistant as sely distributed. is typical of metazoan cells, which lack cell walls but The Ediacaran Biota preserved as moulds in lami- have cell membranes. In other words, the integu- nated limestone in the Khatyspyt Formation of the ment or body wall of Aspidella was made of biopoly- Olenek Uplift, northern Siberia, and deposited on mers that were mechanically firm enough to the ramp of a siliciclastic-carbonate platform, is produce morphologically persistent and abundantly comparable to the Avalon fossil assemblages (Grazh- preserved moulds but chemically labile to decay. By LETHAIA 10.1111/let.12173 Ediacaran impressions from China 11 contrast, the resistant walls in plant-like cells of pho- This continued throughout the Cambrian in other tosynthesizing microbes rendered possible the clades, especially successfully by . The preservation of microbial mats as distinct laminae in record of carbonaceous fossils representing frag- the entombing sediment and could serve as a death ments of non-mineralizing metazoans, such as mask for preserving impressions when metazoan annelidan chaetae, cuticles of sipunculan worms, bodies are gone. scales, scalids and pharyngeal teeth of possible pri- Photosynthetic micro-organisms are characterized apulids or of uncertain origins (), is well by refractory biomacromolecules that have been syn- known in the Cambrian Chengjiang, Kaili and thesized by cyanobacteria, bacterans in cell walls and assemblages (Harvey et al. 2012). trichome sheaths, and algae, algaenan and sporopol- However, some microscopic fossils of the same lenin groups in cyst walls (Tyson 1995; de Leeuw aspects occur in the terminal Ediacaran and earli- et al. 2006). Those microfossils that were inferred to est Cambrian on the East European Platform and represent algal cysts appear to have survived burial in South Australia, i.e. Ceratophyton and undeter- conditions and diagenesis for c. 1.8 Ga (Lamb et al. mined metazoan remains that are identical to cuti- 2009; Moczydłowska et al. 2011). Cyanobacterial cle fragments from the Kaili Formation microfossils may have been preserved for over 3 Ga (Moczydłowska 1991, 2008; Zang et al. 2007; (Schopf 2006; Schopf & Kudryavtsev 2009; Moczydłowska et al. 2015). These document the Schirrmeister et al. 2015). The oldest organically presence of lophotrochozoan-like metazoans pro- preserved macroscopic metazoan Sabellidites is c. ducing resistant polymers long before (c. 10 Ma) 550 Ma (Moczydłowska et al. 2014). The only older the Cambrian. It is apparent that more metazoans ones, c. 635–577 Ma, could be the Lantian putative of modern phyla affiliation not only evolved metazoans preserved as carbonaceous compressions, before the but also survived and reinterpreted by Van Iten et al. (2013, 2014) to the end-Ediacaran extinction as well. represent conulariid cnidarians or closely related The Ediacaran metazoans, with a few exceptions medusozoans after originally being recognized as of taxa related to modern clades, did not possess the algae or of unknown affinity (Yuan et al. 2011). ability to synthesize refractory compounds in body In newly recovered external moulds of the Edi- walls and, therefore, could not be preserved despite acaran organism Coronacollina, Clites et al. (2012) their macroscopic to large dimensions, abundance, inferred that it was either biomineralized or com- cosmopolitan distribution, and adaptation to vari- prised of chitin because it exhibits articulated ele- ous ecological niches. This probably ultimately ments such as rigid spicules, although not actually caused the extinction of most of them because of the preserved, and resembling a demosponge. The chitin lack of a body wall that was protective against rising is not preserved in this fossil, even if it had been pre- mobility, bioturbation, competition for food, and sent in a skeletal fibre as in demosponges, and thus predation among early metazoans. Also, the ecologi- was not considered to be preservable in siliciclastic cal impact of newly emerging metazoans and ecosys- sediments by Clites et al. (2012). This is not the case. tem engineering could have contributed to the Although not found in Coronacollina, chitin is extinction of the Ediacaran biota (Laflamme et al. preservable in siliciclastic sediments of the same age 2013). in the aforementioned annelidan fossils (Moczy- Two questions remain: 1, what was the biochemi- dłowska et al. 2014), and it could be synthesized by cal composition of their body wall; and 2, what trig- of this age because chitin is known in skele- gered the invention of refractory biopolymers in tons of both demosponges and hexactinellids (Ehr- metazoans, if not the stimuli mentioned? The change lich et al. 2007a,b). Coronacollina remains an in biosynthesis pathways in metazoans at the end of uncertain taxon, but -grade phosphatized the Ediacaran Period from non-resistant biopoly- body fossils with cellular resolution have actually mers to resistant chitin and collagen groups is a been recovered from the early Ediacaran Doushan- major event that constituted part of the success of tuo Formation (Yin et al. 2015). The latter Eocy- the metazoans. Biochemistry, including athispongia is preserved with various cell types and biomineralization, may be as important a factor in morphology of the poriferan affinity (Yin their evolution as environmental change in selecting et al. 2015). the fittest. It is exemplified by photosynthesizing Growing evidence shows that representatives of biota from cyanobacteria to vascular plants, which modern metazoan phyla began to synthesize resis- survived and thrived over 3 Ga because of the resis- tant chitin (annelids) and yet-unrecognized poly- tant cell walls they inherited in part from the earliest mers (cnidarians) at the end of the Ediacaran lineages though endosymbiosis and then shared in (Moczydłowska et al. 2014; Van Iten et al. 2014). all clades. 12 M. Moczydłowska & F. Meng LETHAIA 10.1111/let.12173

tions, and acknowledge the Editors Alan Owen and Peter Doyle Conclusions for thorough reading of the manuscript and editorial work.

The studied impressions from the Xingmincun For- mation are preserved as flat or low-epirelief moulds References on the bedding plane surfaces and low-hyporelief Baudet, D., Aitken, J.D. & Vanguestaine, M. 1989: Palynology of uppermost Proterozoic and lowermost Cambrian formations, casts on the bedding soles because the fine-grained, central Mackenzie Mountains, northwestern Canada. Cana- clayey host sediment is diagenetically compacted. dian Journal of Earth Sciences 26, 129–148. We positively recognize the Aspidella plexus fossils Cai, Y., Schiffbauer, J.D., Hua, H. & Xiao, S. 2011: Morphology and paleoecology of the late Ediacaran tubular fossil Cono- as organisms because of their morphology, dimen- tubus hemmianulatus from the Gaojiashan Lagerst€atte of sions, distribution, and environmental context com- southern Shaanxi Province, South China. Precambrian parable to other examples of Aspidella and by Research 191,46–57. Cai, Y., Schiffbauer, J.D., Hua, H. & Xiao, S. 2012: Preservational excluding abiotic processes as the source of the modes in the Ediacaran Gaojiashan Lagerst€atte: pyritization, structures. aluminosilicification, and carbonaceous compression. Palaeo- Typical features of Aspidella that are universally geography, Plalaeoclimatology, Palaeoecology 326–328, 109–117. Chen, M.E. 1991: Discussion on the stratigraphic significance of preserved in all depositional facies are circular struc- macrofossils from the late Precambrian sequences in the south- tures (rings, ridges or rims) and a central boss, and ern Liaoning Province. Acta Geologica Sinica 65, 120–128. these elements are visible in the present collection, Chen, Z., Zhou, C., Meyer, M., Xiang, K., Schiffbauer, J.D. & Yuan, X. 2013: Trace fossils evidence for Ediacaran bilaterian although other features observed in this fossil plexus animals with complex behaviors. Precambrian Research 224, are not present. We conform to the prevalent 690–701. hypothesis that the Aspidella impressions were Chen, Z., Zhou, C., Xiao, S., Wang, W., Guan, C., Hua, H. & Yuan, X. 2014: New Ediacara fossils preserved in marine lime- formed by holdfasts of frondose, soft-bodied sessile stone and their ecological implications. Scientific Reports 4,1– organisms that were partly buried in the sediment 10. surface while alive. We also agree with inferences Clites, E.C., Droser, M.L. & Gehling, J.G. 2012: The advent of hard-part structural support among the Ediacaran biota: edi- that the organisms were metazoan in origin. acaran harbinger of a Cambrian mode of body construction. Lack of organic matter preservation in Aspidella, Geology 40, 307–310. regardless of preservation conditions, indicates that Duda, J.-P., Blumenberg, M., Thiel, V., Simon, K. & Zhu, M. 2014: of a palaeoecosystem with Ediacara-type fos- biopolymers in its body were labile. This is in a sharp sils: the Shibantan Member (Dengying Formation, South contrast to refractory biomolecules that have been China). Precambrian Research 255,48–62. synthesized by contemporaneous photosynthetic Ehrlich, H., Malgonado, M., Spindler, K.-D., Eckert, C., Hanke, T., Born, R., Goebel, C., Simon, P., Heinemann, S. & Worch, uni- and multicellular biota of cyanobacterial, algae H. 2007a: First evidence of chitin as a component of the skele- and some of unknown origins, and a few organically tal fibers of marine sponges. Part I. Verongidae (Demospon- preserved or by carbonaceous compression meta- gia: Porifera). Journal of Experimental Zoology (Molecular and Developmental Evolution) 308B, 347–356. zoans. Ehrlich, H., Krautter, M., Hanke, T., Simon, P., Knieb, C., The early metazoans, selectively preserved and Heinemann, S. & Worch, H. 2007b: First evidence of the pres- known mostly by their impressions in the Ediacaran, ence of chitin in skeletons of marine sponges. Part II. Glass sponges (Hexactinellida: Porifera). Journal of Experimental were comprised of non-resistant biopolymers and Zoology (Molecular and Developmental Evolution) 308B, 473– differed from the subsequently evolved metazoans 483. by this property. The synthesis of compounds in the Erwin, D.H., Laflamme, M., Tweedt, S.M., Sperling, E.A., Pisani, D. & Peterson, K.J. 2011: The Cambrian conundrum: early body integument of early metazoans changed divergence and late ecological success in the early history of between these extinct Ediacaran clades and those animals. Science 334, 1091–1097. that evolved at the end of the Ediacaran and in the Farmer, J., Vidal, G., Moczydłowska, M., Strauss, H., Ahlberg, P. & Siedlecka, A. 1992: Ediacaran fossils from the Innerelv Cambrian, producing refractory biopolymers of the Member (late Proterozoic) of the Tanafjorden area, northeast chitin and collagen groups that were also biominer- Finnmark. Geological Magazine 129, 181–195. alized. Still not fully appreciated, we consider the Fedonkin, M.A. 1992: Vendian faunas and the early evolution of Metazoa. In Lipps, J.H. & Signor, P. (eds): Origin and Early change of organic synthesis in metazoans as a bio- Evolution of the Metazoa,87–129. Plenum Press, New York. chemical revolution that played a major role in the Fedonkin, M.A., Gehling, J.G., Grey, K., Narbonne, G.M. & Vick- Cambrian radiations. ers-Rich, P. 2007: The Rise of Animal Evolution and Diversifica- tion of the Kingdom Animalia. The Johns Hopkins University Acknowledgements. – Our research was supported by the Swedish Press, Baltimore 326 p. Research Council (Vetenskapsradet) project grant Nr 621-2012- Gaines, R.R., Briggs, D.E.G. & Yuanlong, Z. 2008: Cambrian Bur- 1669 to MM, which made possible the research visit of FM to gess Shale–type deposits share a common mode of fossiliza- Uppsala University, and the National Natural Science Foundation tion. Geology 36, 755–758. of China (No. 41173051) to FM. We thank the Reviewers James Gehling, J.G. 1999: Microbial mats in terminal Proterozoic silici- Schiffbauer and Alex Liu for their comments and useful sugges- clastics: ediacaran death masks. Palaios 14,40–57. LETHAIA 10.1111/let.12173 Ediacaran impressions from China 13

Gehling, J.G. & Droser, M.L. 2009: Textured organic surfaces Laflamme, M., Darroch, S.A.F., Tweedt, S.M., Peterson, K.J. & associated with the Ediacara Biota in South Australia. Earth- Erwin, D.H. 2013: The end of the Ediacaran biota: extinction, Science Review 96, 196–206. biotic replacement, or Cheshire cat? Gondwana Research 23, Gehling, J.G. & Droser, M.L. 2013: How well do fossil assem- 558–573. blages of the Ediacara Biota tell time? Geology 41, 447–450. Lamb, D.M., Awramik, S.M., Chapman, D.J. & Zhu, S. 2009: Evi- Gehling, J.G. & Vickers-Rich, P. 2007: The Ediacara Hills. In dence for eukaryotic diversification in the ~1800 million-- Fedonkin, M.A., Gehling, J.G., Grey, K., Narbonne, G.M. & old Changzhougou Formation, North China. Precambrian Vickers-Rich, P. (eds), The Rise of Animals. Evolution and Research 173,93–104. Diversification of the Kingdom Animalia,89–113. Johns Hop- de Leeuw, J.W., Versteegh, G.J.M. & van Bergen, P.F. 2006: kins University Press, Baltimore, MD. Biomacromolecules of plants and algae and their fossil ana- Gehling, J.G., Narbonne, G.M. & Anderson, M.M. 2000: The first logues. Plant Ecology 189, 209–233. named Ediacaran body fossil: Aspidella terranovica. Palaeontol- Liu, A.G., Kenchington, C.G. & Mitchell, E.G. 2015: Remarkable ogy 43, 427–456. insights into the paleoecology of the Avalonian Ediacaran Gehling, J.G., Runnegar, B.N. & Droser, M.L. 2014: Scratch macrobiota. Gondwana Research 27, 1355–1380. traces of large Ediacara bilaterian Animals. Journal of Paleon- Mariotti, G., Pruss, S.B., Perron, J.T. & Bosak, T. 2014: Microbial tology 88, 284–298. shaping of sedimentary wrinkle structures. Geoscience Grazhdankin, D.V. 2014: Patterns of evolution of the Ediacaran 7, 736–740. soft-bodied biota. Journal of 88, 269–283. Menon, L.R., McIlroy, D. & Brasier, M.D. 2013: Evidence for Grazhdankin, D.V., Balthasar, U., Nagovitsin, K.E. & Kochnev, -like behavior in ca. 560 Ma Ediacaran Aspidella. B.B. 2008: Carbonate-hosted Avalon-type fossils in arctic Geology 41, 895–898. Siberia. Geology 36, 803–806. Meyer, M.B., Xiao, S., Schiffbauer, J.D. & Gill, B.C.. 2013: Aspi- Grey, K. 2005: Ediacaran palynology of Australia. Memoir of the della in repose: taphonomy of a frondose Ediacaran fossil pre- Association of Australasian Palaeontologists 31,1–439. served in carbonate rocks. Abstracts with Programs, GSA Harvey, T.H.P., Ortega-Hernandez, J., Lin, J.-P., Yuanlong, Z. & Annual Meeting 2013, Vol. 45, 621 pp. Butterfield, N.J. 2012: Burgess Shale-type microfossils from Meyer, M.B., Xiao, S., Gill, B.C., Schiffbauer, J.D., Chen, Z., the middle Cambrian Kaili Formation, Guizhou Province, Zhou, C. & Yuan, X. 2014: Interactions between Ediacaran ani- China. Acta Palaeontologica Polonica 57, 423–436. mals and microbial mats: Insights from Lamonte trevallis,a Hofmann, H.J. 1985: The mid-Proterozoic Little Dal macrobiota, new from the Dengying Formation of South Mackenzie Mountains, north-west Canada. Palaeoontology 28, China. Palaeogeography, Palaeoclimatology, Palaeoecology 396, 331–354. 62–74. Hofmann, H.J. 1994: Proterozoic carbonaceous compression Moczydłowska, M. 1991: biostratigraphy of the Lower (‘metaphytes’ and ‘worms’). In Bengtson S. (ed.), Early on Cambrian and the Precambrian-Cambrian boundary in south- Earth. Nobel Symposium No. 84, p. 342–357. Columbia Univer- eastern Poland. Fossils and Strata 29, 127 pp. sity Press, New York. Moczydłowska, M. 2008: New records of late Ediacaran micro- Hogstr€ om,€ A.E.S., Jensen, S., Palacios, T. & Ebbestad, J.O.R. biota from Poland. Precambrian Research 167,71–92. 2013: New information on the Ediacaran-Cambrian transition Moczydłowska, M., Vidal, G. & Rudavskaya, V.A. 1993: Neopro- in the Vestertana Group, Finnmark, northern Norway, from terozoic (Vendian) phytoplankton from the Siberian Platform, trace fossils and organic-walled microfossils. Norwegian Jour- Yakutia. Palaeontology 36, 495–521. nal of Geology 93,95–106. Moczydłowska, M., Landing, E., Zang, W. & Palacios, T. 2011: Hong, Z.M., Huang, Z.F., Yang, X.D., Lan, J., Xian, B.C., Yang, Proterozoic phytoplankton and timing of chlorophyte algae Y.J., Liang, Y., Sun, T., Wang, F.J. & Song, S. 1986: The finding origins. Palaeontology 54, 721–733. of metazoan fossils from Xingmincun Formation of Sinian in Moczydłowska, M., Westall, F. & Foucher, F. 2014: Microstruc- South Liaoning. Liaoning Geology 4, 289–298 (in Chinese with ture and biogeochemistry of the organically preserved Edi- English abstract). acaran metazoan Sabellidites. Journal of Paleontology 88, 224– Hong, Z.M., Huang, Z.F., Yang, X.D., Lan, J., Xian, B.C. & Yang, 239. Y.J. 1988: Medusoid fossils from the Sinian Xingmincun For- Moczydłowska, M., Budd, G.E. & Agic, H. 2015: Ecdysozoan-like mation of Southern Liaoning. Acta Geologica Sinica 3, 200–209 sclerites among Ediacaran microfossils. Geological Magazine (in Chinese with English abstract). 152, 1145–1148. Hua, H. & Cao, R.J. 2003: Neoproterozoic assem- Narbonne, G.M. 1998: The Ediacaran biota: a terminal Neopro- blages from the Shisanlitai stage and its significance in the terozoic experiment in the evolution of life. GSA Today 8,1–6. regional and continental correlation. Journal of Narbonne, G.M. 2005: The Ediacaran biota: Neoproterozoic ori- 27,19–25 (in Chinese with English abstract). gin of animals and their Ecosystems. Annual Review of Earth Hua, H., Chen, Z. & Yuan, X. 2007: The advent of mineralized and Planetary Sciences 33, 421–442. skeletons in Neoproterozoic Metazoa–new fossil evidence Narbonne, G.M. 2007: The Canadian Cordillera. In Fedonkin from the Gaojiashan Fauna. Geological Journal 42, 263–279. M.A., Gehling J.G., Grey K., Narbonne G.M., Vickers-Rich P., Ivantsov, A.Y. 2009: New reconstruction of Kimberella, problem- (eds), The Rise of Animals. Evolution and Diversification of the atic Vendian metazoan. Palaeontological Journal 43, 601–611. Kingdom Animalia, p. 175–183, The Johns Hopkins University Jensen, S., Droser, M.L. & Gehling, J.G. 2006: A critical look at Press, Baltimore. the Ediacaran trace fossil record. In Xiao, S. & Kaufman, A.J. Narbonne, G.M. 2011: When life got big. Nature 470, 339–340. (eds): Neoproterozoic Geobiology and Paleontology, 115–157. Narbonne, G.M., Laflamme, M., Trusler, P.W., Dalrymple, R.W. Springer, Berlin. & Greentree, C. 2014: Deep-water Ediacaran fossils from Kuang, H.W., Liu, Y.Q., Peng, N. & Liu, L.J. 2002: Geo- northwestern Canada: taphonomy, ecology, and evolution. chemistry of the Neoproterozoic molar-tooth carbonates in Journal of Paleontology 88, 207–223. Dalian, eastern Liaoning, China, and its geological implica- Noffke, N. 2010: Geobiology Microbial Mats in Sandy deposits tions. Earth Science Frontiers 18,25–40 (in Chinese with from the Archean to Today. Springer, Berlin 194 pp. English abstract). Noffke, N., Christian, D., Wacey, D. & Hazen, R.M. 2013: Micro- Laflamme, M., Schiffbauer, J.D., Narbonne, G.M. & Briggs, bially induced sedimentary structures recording an ancient D.E.G. 2011: Microbial biofilms and the preservation of the ecosystem in the ca, 3.48 billion-year-old Dresser Formation, Ediacaran Biota. Lethaia 44, 203–213. Pilbara. . Astrobiology 13, 1103–1124. Laflamme, M., Flude, L.I. & Narbonne, G.M. 2012: Ecological Ou, Z. & Meng, F. 2013: Precambrian ‘medusoid’ fossils from tiering and the evolution of a stem: the oldest stemmed frond the Xingmincun Formation of southern Liaoning Province: a from the Ediacaran of Newfoundland, Canada. Journal of Pale- new insight. Acta Micropalaeontologica Sinica 30,99–106 (In ontology 86, 193–200. Chinese with English abstract). 14 M. Moczydłowska & F. Meng LETHAIA 10.1111/let.12173

Parry, L., Tanner, A. & Vinther, J. 2014: The origin of annelids. Van Iten, H., Marques, A.C., de Moraes Leme, J., Forancelli Palaeontology 57, 1091–1103. Pacheco, M.J.A. & Guimaraes Simoes,~ M. 2014: Origin and Parsons, M.G. & Anderson, M.M. 2000: Acritarch microfloral early diversification of the Cnidaria Verrill: major succession from the late Cambrian and (early Tre- developments in the analysis of the taxon’s Proterozoic-Cam- madoc) of Random Island, Eastern Newfoundland, and its brian history. Palaeontology 57, 677–690. comparison to coeval microfloras, particularly those of the Vidal, G. & Siedlecka, A. 1983: Planktonic, acid-resistant East European Platform. AASP Contributions Series Number microfossils from the Upper Proterozoic strata of the Bar- 38, 129 pp. ents Sea region of Varanger Peninsula, East Finnmark, Peng, S.C., Babcock, L.E., Zuo, J.X., Lin, H.L., Zhu, X.J., Yang, Northern Norway. Norges Geologiske Undersøkelse, Bulletin X.F., Robison, R.A., Qi, Y.P., Bagnoli, G. & Chen, Y. 2009: The 382,45–79. Global boundary Stratotype section and point of the Guzhan- Vinther, J., Sperling, E.A., Briggs, D.E.G. & Peterson, K.J. 2012: A gian Stage (Cambrian) in the Wuling Mountains, northwest- molecular palaeobiological hypothesis for the origin of apla- ern Hunan, China. Episodes 32,41–55. cophoran mollusks and their derivation from chiton-like Peterson, K.J., Waggoner, B. & Hagadorn, J.W. 2003: A fungal ancestors. Proceedings of the Royal Society B 279, 1259–1268. analog for Newfoundland Ediacaran fossils? Integrative and Xiao, S. & Laflamme, M. 2009: On the eve of animal radiation: Comparative 43, 127–136. phylogeny, ecology and evolution of the Ediacaran biota. Retallack, G.J. 2012: Were Ediacaran siliciclastics of South Trends in Ecology and Evolution 24,31–40. Australia coastal or deep marine? Sedimentology 59, Xiao, S., Yuan, X., Steiner, M. & Knoll, A.H. 2002: Macroscopic 1208–1236. carbonaceous compressions in a terminal Proterozoic shale: a Retallack, G.J. 2013: Ediacaran life on land. Nature 493,89–92. systematic reassessment of the Miaohe biota, South China. Schiffbauer, J.D., Xiao, S., Cai, Y., Wallace, A.F., Hua, H., Hun- Journal of Paleontology 76, 347–376. ter, J., Xu, H., Peng, Y. & Kaufman, A.J. 2014: A unifying Xiao, S., Droser, M., Gehling, J.G., Hughes, I.V., Wan, B., Chen, model for Neoproterozoic-Palaeozoic exceptional fossil Z. & Yuan, X. 2013: Affirming life aquatic for the Ediacaran preservation through pyritization and carbonaceous compres- biota in China and Australia. Geology 41, 1095–1098. sion. Nature Communications 5,1–12. Xing, Y. 1976: The Sinian System of China,1–17, Institute of Schirrmeister, B.E., Gugger, M. & Donoghue, P.C.J. 2015: Geology and Mineral Resources. Chinese Academy of Sciences, Cyanobacteria and the : evidence from Peking. genes and fossil. Palaeontology 58, 769–785. Xing, Y. & Liu, G. 1979: Coelenterate fossils from the Sinian Sys- Schopf, J.W. 2006: Fossil evidence of Archean life. Transactions of tem of southern Liaoning and its stratigraphic significance. the Royal Society Series B 361, 869–885. Acta Geologica Sinica 53, 167–172. Schopf, J.W. & Kudryavtsev, A.B. 2009: Confocal laser scanning Yang, D.B., Xu, W.L., Xu, Y.G., Wang, Q.H. & Pei, F.P. 2011: microscopy and Raman imagery of ancient microscopic fossils. Neoproterozoic of detrital zirons from northern Precambrian Research 173,39–49. Jiangsu Province and southern Liaoning Province: constrain Sperling, E.A. & Vinther, J. 2010: A placozoan affinity for Dickin- on tectonic Tanlu Fault zone. Bulletin of , Petrology sonia and the evolution of late Proterozoic metazoan feeding and Geochemistry 30, 557(in Chinese). modes. Evolution and Development 12, 199–207. Yin, Z., Zhu, M., Davidson, E.H., Bottjer, D.J., Zhao, F. & Taf- Srivastava, P. 2014: Largest Ediacaran discs from the Jodhpur foreau, P. 2015: Sponge grade body fossil with cellular resolu- Sandstone, Marwar Supergroup, India: their palaeobiological tion dating 60 Myr before the Cambrian. Proceedings of the significance. Geoscience Frontiers 5, 183–191. National Academy of Sciences USA 112, E1453–E1460. Sun, W. 1986: Precambrian medusoids: the Cyclomedusa plexus Yuan, X., Li, J. & Cao, R. 1999: A diverse metaphyte assemblage and Cyclomedusa-like pseudofossils. Precambrian Research 31, from the Neoproterozoic black of South China. Lethaia 325–360. 32, 143–155. Tang, F., Bengtson, S., Wang, Y., Wang, X.-L. & Yin, C.-Y. 2011: Yuan, X., Chen, Z., Xiao, S., Zhou, C. & Hua, H. 2011: An early Eoandromeda and the origin of . Evolution & Ediacaran assemblage of macroscopic and morphologically Development 13, 408–414. differentiated . Nature 470, 390–393. Tarhan, L.G., Hughes, N.C., Myrow, P.M., Bhargava, O.N., Ahlu- Zang, W.-L., Moczydłowska, M. & Jago, J.B. 2007: Early Cam- walia, A.D. & Kudryavtsev, A.B. 2014: Precambrian-Cambrian brian acritarch assemblage zones in South Australia and global boundary interval occurrence and form of the enigmatic tubu- correlation. Memoirs of the Association of Australasian Palaeon- lar body fossil Shaanxilithes ningqiangensis from the Lesser tologists 33, 141–177. Himalaya of India. Palaeontology 57, 283–298. Zhang, X., Hua, H. & Reitner, J. 2006: A new type of Precam- Tarhan, L.G., Droser, M.L., Gehling, J.G. & Dzaugis, M.P. 2015: brian megascopic fossils: the Jinxian biota from northeastern Taphonomy and morphology of the Ediacara from genus Aspi- China. Facies 52, 169–181. della. Precambrian Research 257, 124–136. Zhu, M., Gehling, J.G., Xiao, S., Zhao, Y.-L. & Droser, M. 2008: Tyson, R.V. 1995: Sedimentary Organic Matter. Organic Facies Eight-armed Ediacaran fossils preserved in contrasting tapho- and Palynofacies. Chapman & Hall, London 615 p. nomic windows from China and Australia. Geology 36, 867– Van Iten, H., de M.Leme, J., Marques, A.C. & Simoes,~ M.G. 870. 2013: Alternative interpretations of some earliest Ediacaran fossils from China. Acta Palaeontologica Polonica 58,11–113.