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The Ediacaran Aspidella-type impressions in the Jinxian successions of Liaoning Province, northeastern China MAŁGORZATA MOCZYDŁOWSKA AND FANWEI MENG

Moczydłowska, M. & Meng, F. 2016: The Ediacaran Aspidella-type impressions in the Jinxian successions of Liaoning Province, northeastern China. Lethaia , Vol. 49, pp. 617–630. Macroscopic impression fossils 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 succession, but were referred to as new species and relegated to an earlier Neoproterozoic age. A revision of the taxonomic interpretation and relative age estimation of the previous 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 properties 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 microfossils, and an exceptionally small number of terminal Ediacaran metazoan fossils (Sabellidites, Conotubus and Shaanxilithes), demonstrates the non-resistant characteristics and the very different biochemical constitution of the Ediacaran metazoans compared with those that evolved in the Cambrian 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 Shale 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, taphonomy. Małgorzata Moczydłowska [[email protected]], Department of Earth Sciences, Palaeobiology, Uppsala University, Villav€agen 16, SE 752 36 Uppsala, Sweden; Fanwei Meng [[email protected]], State Key Laboratory of Palaeontology and Stratigraphy, 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 preservation as impressions (moulds and casts), less frequently as carbonaceous compressions (containing organic biofilms) or traces, and exceptionally as organically preserved and biomineralized body fossils (Gehling et al. 2000; Narbonne 2005; Fedonkin et al. 2007; Hua et al. 2007; Cai et al. 2011; Laflamme et al. 2012; Moczydłowska et al. 2014; Tarhan et al. 2015). Recognized in various preservation modes and ecological niches on shallow shelves vs. deep marine slopes, the fossils represent softbodied organisms including metazoans (Zhu et al. 2008; Ivantsov 2009; Xiao & Laflamme 2009; Sperling & Vinther 2010; Narbonne 2011; Narbonne et al. 2014; Liu et al. 2015). They comprised body walls made from non-resistant organic matter, a fact verified by observations in all known sites and modes of preservation with a few exceptions, and

the rationale used to describe their organic properties. The exceptions are the organically preserved terminal Ediacaran annelidan Sabellidites, whose robust wall is chitinous (Moczydłowska et al. 2014; M. Moczydłowska, unpubl. data), and the carbonaceous compressions of Conotubus, Shaanxilithes, Mawsonites, Eoandromeda and Khatyspytia of as-yetunresolved biochemistry and affinities (Hua et al. 2007; Zhu et al. 2008; Grazhdankin 2014; Tarhan et al. 2014). Among them, Eoandromeda was interpreted as a ctenophore (Tang et al. 2011). This is in sharp contrast to contemporaneous uni- and multicellular fossils of cyanobacterial and algal origin that synthesized cell walls and trichome sheaths that are extremely resistant to biodegradation, diagenesis, and laboratory acid treatment (Moczydłowska et al. 1993; Xiao et al. 2002; Grey 2005; Moczydłowska 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.

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the Lantian and Miaohe biotas (early and late Ediacaran respectively) showing complex morphologies of fan-shaped and branching algal thalli and colonial cyanobacteria (Yuan et al. 1999, 2011; Xiao et al. 2002) are also within the group of photosynthesizing organisms. Unnamed carbonaceous compressions from the Ediacaran Khatyspyt Formation in Siberia may be microbial colonies or seaweeds (Grazhdankin et al. 2008; Grazhdankin 2014). Biological affinities and phylogenetic relationships of most Ediacaran taxa are not yet resolved, nor is there consensus on whether certain taxa are metazoans or of enigmatic affinities unknown among modern phyla (Erwin et al. 2011; Narbonne 2011; Yuan et al. 2011). It is generally accepted that the Ediacaran biota comprised representatives of porifera, ctenophorans, cnidarians, aplacophorans, and stem- and crown-group bilaterian metazoans, including molluscs (Narbonne 2005; Fedonkin et al. 2007; Ivantsov 2009; Xiao & Laflamme 2009; Vinther et al. 2012; Laflamme et al. 2012; Menon et al. 2013; Gehling et al. 2014; Narbonne et al. 2014; Yin et al. 2015). Recognition of siboglinid affinity of Sabellidites suggests the presence of the crown-group Annelida (Moczydłowska et al. 2014; but see also Parry et al. 2014). Alternative interpretations that certain taxa are fungi (Peterson et al. 2003), terrestrial lichens and slime moulds (Retallack 2012, 2013), or microbial colonies (Grazhdankin et al. 2008; Grazhdankin 2014) have not received widespread support (Menon et al. 2013; Xiao et al. 2013; Chen et al. 2014). The disc-like, flat- to high-relief impressions preserved on bedding planes are the predominant fossils within the Ediacaran assemblages in siliciclastic successions worldwide (Fedonkin et al. 2007; Laflamme et al. 2013), but they also occur in carbonate facies (Grazhdankin et al. 2008; Chen et al. 2014). Originally described as morphologically disparate genera and species, they have been substantially reduced as a result of depositional and taphonomic analyses that have eliminated superfluous synonyms (Gehling et al. 2000; Narbonne 2005; Fedonkin et al. 2007). The most common discoidal impression is the Aspidella plexus, which comprises a great variety of morphs, and its type species is A. terranovica Billings, 1872. It has been recognized as a buried holdfast of frond-like organisms (Gehling et al. 2000) and accepted as such in subsequent works (Erwin et al. 2011; Chen et al. 2014; Narbonne et al. 2014; Tarhan et al. 2015). Alternatively, Aspidella has been suggested to represent vagile, epifaunal animals of the cnidarian grade, having the ability to periodically burrow and actively move to adjust to accumulation of sediment (Menon et al.

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2013), or even non-metazoan, microbial organisms (Grazhdankin 2014; Liu et al. 2015). Aspidella fossils have been recently noted in South China, in the Shibantan Member of the Dengying Formation in the Yangtze Gorges area, Hubei Province (Meyer et al. 2013; Chen et al. 2014), although not yet systematically described or compared with other modes of preservation. Specimens of a Spriggia-type holdfast reported by Chen et al. (2014, fig. 3D) from the same area and stratigraphical interval of the Shibantan Member are considered here to be synonymous with Aspidella, as are those identified as a possible Ediacaran-type fossil by Duda et al. (2014, fig. 2A). These, together with the present specimens from the Liaoning Province, are the current records of Aspidella in China. We report a new record of discoidal impressions identified as an Aspidella form-genus preserved in several taphonomic morphs consistently bearing the characteristic of the Aspidella plexus, which is primarily the disc-shaped body with concentric rings and a central boss (Gehling et al. 2000; Fedonkin et al. 2007; Laflamme et al. 2011). This is the first recognition of the Aspidella plexus in the Liaoning Province of northeastern China and includes revised taxa previously assigned to junior synonyms by Zhang et al. (2006). The age of strata containing the assemblage is estimated to be Ediacaran at c. 580– 550 Ma based on the global chronostratigraphical range of such fossils (Grazhdankin 2014). The assemblage studied here should not be confused with structures recorded approximately 1600 m below in the underlying Changlingzi Formation (Figs 1 and 2) that originally were attributed to the Cyclomedusa fossils (Xing & Liu 1979) and subsequently interpreted as pseudo-fossils and representing sedimentary, gas escape structures (Sun 1986; see below).

Geological setting and age of succession The collection of fossils derives from clayey shale in the middle member of the Xingmincun Formation, Jinxian Group, at the Yangjue and Yangtun localities in the Liaoning Province of northeastern China (Fig. 1). The Neoproterozoic (Sinian) and Cambrian successions of the region comprise siliciclastic and carbonate rocks. They are divided into the Wuhangshan and Jinxian groups, which are paraconformably overlain by the Cambrian Dalinzi and Jianchang formations (Hong et al. 1986, 1988; Zhang et al. 2006; Fig. 2). The entire succession is steeply dipping and

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Fig. 1. Location map of fossil localities at Yangjue and Yangtun in the Liaoning Province, northeastern China.

intruded by the Jurassic andesites. A paraconformity also separates the Xingmincun and the Getun formations. The Jianchang Formation contains lower Cambrian Redlichia trilobites that indicate a high biostratigraphical position in Cambrian Series 2 (Peng et al. 2009). The Dalinzi Formation paraconformably underlies the Jianchang Formation and is a relatively thin succession (c. 72 m). Although it is unfossiliferous, it most likely belongs to the basal Cambrian (Fig. 2) because bradoriid fossils were reported, although not illustrated, from the underlying Getun Formation (Zhang et al. 2006). If this occurrence is confirmed, the latter formation should also be attributed to the Cambrian System. The Precambrian relative age of the Jinxian and Wuhangshan groups was inferred from the regional scale of the sequence of rocks containing stromatolites with age-diagnostic Proterozoic taxa, the Chuaria– Tawuia assemblages, and discoidal impressions comparable to the Ediacara-type fauna (Hong et al. 1988; Chen 1991; Hua & Cao 2003; Fig. 2). Stromatolites from the Shisanlitai Formation are correlative of the Upper Riphean or Tonian–Cryogenian (c.1000-650 Ma) assemblages (Hua & Cao 2003). The shale in the Xingmincun Formation was dated to 650 Ma by the Rb-Sr method (Hong et al. 1988), but not confirmed by other methods. The detrital zircons in the lower Xingmincun Formation dated to a minimum age of 924 Ma (Yang et al.

2011) also do not constrain the age. Values of geochemical signatures of d13C and 87Sr/86Sr from carbonates in the Jinxian Group that contain Aspidella were suggested to be correlative with those from older successions, such as the Cryogenian at c. 800 Ma (Kuang et al. 2002). However, these older records of elemental fractionation curves remain to be constrained by numerical ages to be unequivocally distinguished in the global Neoproterozoic pattern of geochemical changes and applied in chemostratigraphy. The proposed older-than-Ediacaran ages of the Jinxian Group are neither directly constrained by isotopic datings nor indirectly by geochemical signatures set in a chronostratigraphical time frame. The Jinxian Group underlies the unequivocally, biostratigraphically recognized Cambrian strata with a paraconformable contact that is on a regional scale (Hong et al. 1988; Zhang et al. 2006) and probably comprises a short time gap. This is inferred because there are no coarse-grained clastic rocks that would indicate a major tectonic movement and involve a substantial time interval. The lack of glacigenic sediments correlative with the Neoproterozoic ice ages in Precambrian successions of the Liaoning Province indicates that they are either pre- or post-Cryogenian. Because the discoidal fossils were interpreted as non-Ediacara-type biota and because the succession

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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 age was proposed to be Neoproterozoic and preEdiacaran (Zhang et al. 2006). We contest both the identification of the aforementioned impression fossils and the estimation of age of the succession by Zhang et al. (2006) and conclude that the assemblage is typical of the Aspidella plexus and of Ediacaran age, as has been consistently established elsewhere (Gehling et al. 2000; Narbonne 2005; Fedonkin et al. 2007; Laflamme et al. 2011; Grazhdankin 2014; Narbonne et al. 2014; Tarhan et al. 2015).

Material and methods The rock samples with discoidal impression specimens were collected from two surface successions of the Xingmincun Formation in the Yangjue and

Yangtun localities in the Liaoning Province, northeastern China. The specimens are preserved on bedding planes (sole and surface) of shale and were recovered from six layers within a 68-m-thick interval of the Xingmincun Formation (Ou & Meng 2013; Fig. 2). The lithostratigraphical position of the fossiliferous interval within the Jinxian Group is broadly 170–240 m below the paraconformity at the base of Cambrian in the regional scale of the geological succession. Some 220 specimens were studied and measured under an optical reflected light microscope, and certain specimens are photographed and documented herein. Additional studies using a scanning electron microscope on the surface of specimens and their perpendicular sections appeared inconclusive in detecting organic material preservation in contrast to mineral grains of the host sediment. The moulds and casts were observed only as low relief or flat depressions within fine-grained sed-

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C

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; Meyer et al. 2013), the organic matter was not preserved even if the sediment layers surrounding the Aspidella moulds were recognized as chemically distinct by authigenic mineralization of the biofilm or microbial envelopes (Laflamme et al. 2011). The specimens are housed in the museum collections of the Nanjing Institute of Geology and Palaeontology with the reference numbers NIGP 163245, NIGP 163246, NIGP 163247 for specimens illustrated in Figure 3A–C, respectively, and NIGP 163248, NIGP 163249, NIGP 163250 and NIGP 163251 for Figure 4A–D respectively.

Revision of the previous records of the Jinxian fossils The discoidal macroscopic impressions were discovered in the middle part of the Xingmincun Formation, south Liaoning Province and attributed to the Sinian System (Hong et al. 1986). Three new genera of ‘medusa-like’ fossils, Liaonanella, Jinxianella and Daliania – each consisting of two species – were established by Hong et al. (1986). Subsequently, Hong et al. (1988) extended the documentation of this assemblage, which consisted of moulds and casts of soft-bodied fossils preserved on bedding planes and interpreted as metazoans. These fossils have been characterized as subcircular to ellipsoidal, possessing a central disc and an outer ring with radial canals, and have been attributed to six previously erected species. They have been considered taxonomically different from Ediacara-type fauna, and thus considered new taxa, although of the same age. Study of impression fossils from the same succession by Zhang et al. (2006) did not draw any comparisons

with the Ediacaran or any other Precambrian biota. The authors followed the taxonomic assignment of the species by Hong et al. (1986) and described flat, circular and ellipsoidal in outline fossils with a marginal rim and concentric or spiral ridges on both sides that were preserved as thin membranes replaced by quartz and chlorite. The specimens had a diameter of 1.5–45.0 mm. There was no information on the position of fossils (surface or sole of beds) and their mode of preservation. It was inferred that the fossils comprised two parallel layers (sheaths) resembling biofilms with filament-like and bacteria-like granule structures. We consider these structures to be microcrystals of diagenetic minerals deposited or precipitated on the template of the decaying body, but no convincing evidence of biofilms or organic matter ultrastructure is apparent. The concentric and spiral ridges, it was suggested, show rhythmic growth lines, whereas some specimens were juxtaposed against one another like twins exhibiting an asexual reproduction stage (Zhang et al. 2006). The ‘twin specimens’ are not the result of reproduction but rather superposition and burial distortion. Whereas the concentric ridges are a consistent feature, the spiral geometry is an artefact of taphonomic deformation and not clearly visible. The elliptical specimens do not show any increased growth rate along their long axis, but have gained their shape by lateral compression during burial (the succession is tectonically deformed and cleaved), resulting in folds parallel to the long axis. Some radial wrinkles were probably caused by shrinkage of the soft bulbous body and its collapse. Similar to the ‘twin specimens’ reported by Zhang et al. (2006) are those from the Aspidella assemblage in the Ediacara Member of South Australia and renamed as ‘kissing ‘individuals or pairs of Aspidella (Tarhan et al. 2015), yet without comparison to the

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C

D

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, specimen 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 thought to have been deformed by non-synchronous growth and not originated from asexual fission. In our opinion, the assemblage studied by Zhang et al. (2006) conforms to the taphonomic morphs of the Aspidella plexus, as observed in the assemblage of the same geological derivation considered in this paper.

Morphology and preservation of discoidal impressions Our observations are based on over 200 specimens. The specimens are circular to oval in outline and preserved as macroscopic inorganic impressions (following the terminology of Gehling et al. 2000) that are flat (epirelief) on the surface or with low convex relief (positive hyporelief) on the sole of the bedding planes of the shale. They occur as solitary individuals or, in a few cases, near one another (Figs 3, 4). The oval shape and superficial folds parallel to the long axes of the discs and extending across some specimens

(Fig. 4A,C) are probably the result of distortion caused by lateral compression of strata during tilting and compressional stress that formed cleavage. The discoidal fossils possess sharply defined outlines and circular, concentric structures in the form of a wide marginal zone, with convex narrow ridges in approximately the middle of the disc radius, and a 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 circular ridge is prominent in specimens having positive relief (Fig. 3A,B), but not present or faintly visible in flat specimens (Figs 3C, 4). The central boss is observed in low positive hyporelief specimens (Fig. 3A,B). The overall diameter of specimens is 2.0–25.0 mm (n = 221), with a central boss 1.0– 3.0 mm, and a circular ridge 1.0–2.0 mm wide (Fig. 5A–C). These dimensions belong to the lowest sector of the total range of Aspidella morphs, which in a global compilation is commonly 2.0–80.0 mm, but reaches a diameter 500.0 mm (Gehling et al. 2000; Fedonkin et al. 2007; Menon et al. 2013; Tarhan et al. 2015). Large specimens newly recovered

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Fig. 5. Size distribution of Aspidella specimens in reference to their length of the major axis (A), ratio of maximum to minimum diameter (B) and surface area (C).

from India that are 75 cm in diameter (Srivastava 2014) may belong to this plexus. There is no observed relationship between diameter and morphology (number of ridges or rings) among studied specimens and their size distribution is in the lower size range of the form-genus. The present assemblage that is preserved in fine-grained clayey sediment of the inner marine shelf differs from the assemblages comprising more diverse morphs and within broader size ranges, which were observed in medium- to coarse-grained sandstones of shallow marine and deltaic facies (see Tarhan et al. 2015). There are no structures such as radiating ridges or grooves, as observed in other morphs of the Aspidella plexus and that occur in coarser sediments, because the specimens are flat- or low-relief taphonomic morphs that are characteristic of clayey facies. The present preservation mode as simple, rimmed impressions with a central boss is, however, consistent with diagnostic features of the genus


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(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 Ediacaran 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 specimens 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 Aspidella by casts (infill of external mould by host sediment) or moulds (imprinted marks by pressing against a surface) of soft bodies, which were subsequently totally decayed, has left no organic, mineralogical or geochemical record of the bodies. There is no evidence of microbial mats in the part of succession containing impressions. Direct evidence would be provided by the organic preservation of microbial mat 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 a wrinkled surface (Gehling 1999; Gehling & Droser 2009; Noffke 2010; Noffke et al. 2013; Mariotti et al. 2014). It is unclear whether the so-called textured organic surface associated with Aspidella in South Australia and attributed to the taxon Funisia of supposed eukaryotic origin (Tarhan et al. 2015) is organic, and its origin is certainly unclear. However, the specimens studied are covered by pockets of authigenic pyrite framboids, mostly in marginal zones (Figs 3A, C, 4C), and by chlorite particles. Pyrite framboids are a by-product of bacterial decay of soft bodies and are typical of the preservation in the presence of microbial mats or biofilms associated with clay particles (Gehling 1999; Gehling et al. 2000; Laflamme et al. 2011).

Biotic vs. abiotic origin of studied impression structures The studied impressions, among many others of such morphological appearance in the Ediacaran strata, are preserved without any remains of organic

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matter that would directly prove their biotic origin. We considered possible abiotic processes that could produce comparable structures and mimic the shape and relief of fossils that are left after a total decay of the organic matter in bodies of the organisms that produced them. However, those abiotic structures do not conform to our morphological observations, which are consistent with the interpretation that they are moulds and casts of soft-bodied organisms. The preservation of flat specimens of Aspidella on the sole of shale from the Fermeuse Formation of the Avalon Peninsula, eastern Newfoundland, and elegantly argued regarding its organic origin (Gehling et al. 2000; text-fig. 8E), is similar to the studied material. In the present assemblage, certain specimens (Fig. 3A,B) are identical to variant morphs with simple rings being the only morphology preserved in the sandstone of the Ediacara Member of South Australia (Tarhan et al. 2015; fig. 3A, C). The latter Aspidella specimens are without any reservation considered to be biogenic, moulds of multicellular benthic organisms, and part of a more diverse assemblage of its morphs and other Ediacaran genera. In studies of the Ediacaran impression macrofossils, as well as trace fossils, the possibility of misidentifying abiotic structures has been tested in several cases (Sun 1986; Farmer et al. 1992; Gehling et al. 2000; Jensen et al. 2006; Chen et al. 2013; Menon et al. 2013; Meyer et al. 2014). The considered sedimentary and mechanical structures, which may be similar because of their discoidal shape and the presence of concentric wrinkles, were interpreted as having formed in mineral concretions, rhythmically precipitated silica, in moulds and casts of nodules, gas and fluid eruptions or escape craters, and in dewatering pillars. Biogenic structures with some resemblance include redeposited sheaths of algal colonies and microbial mats (Gehling 1999; Noffke 2010; Noffke et al. 2013). Restudy of the Cyclomedusa-like impressions from the Precambrian strata of the southern Liaoning Province (Fig. 1) resulted in their being recognized as pseudo-fossils of mechanical origin (Sun 1986). These impression structures derive from the Changlingzi Formation of the Wuhangshan Group, which lies approximately 1600 m below the Xingmincun Formation of the Jinxian Group (Fig. 2). They were originally attributed to several species of the fossil taxon Cyclomedusa (Xing 1976; Xing & Liu 1979), which is now recognized as a junior synonym of Aspidella (Gehling et al. 2000; Fedonkin et al. 2007). Thin sections of the Cyclomedusa-like structures show funnel-shaped pits with prominent central, vertical channels filled with calcite, and distorted

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sediment laminae around the specimens (Sun 1986). On the surface of beds, they appear as flat concentric rings or concave epireliefs. Such features are observed in sedimentary gas eruptions because of the pulsating release of gas and water bubbles, such as those formed in modern environments of a sandy beach intertidal zone (Sun 1986). They may be similar in diameter and distribution on the bed surfaces to true fossil impressions, but the persistent features of gas/fluid escape structures seen in cross-sections are the central, vertical channels and bent sediment laminae around these channels. In thin sections of Aspidella that are cut perpendicular to the bedding plane (Gehling et al. 2000; Menon et al. 2013; Meyer et al. 2013; Tarhan et al. 2015), the specimens that are convex on both sides are observed as a sand-filled body, i.e. a cast, in mud and silt layers, or lower-side convex and upper-side truncated specimens, as sand casts in parallel-laminated sandy event beds As a rule, where preserved in coarse siliciclastic sediments, the Aspidella casts infilled by sand are more convex (or three-dimensional) even if they are associated with inter-layers of fine-grained mud or clay because of the differential compaction of the overlying and underlying mud laminae (Gehling et al. 2000). Deformed specimens are observed in slumped sand casts in mud-sand inter-layers. Convex specimens occur also in bituminous laminated limestone (Grazhdankin et al. 2008). However, flat- or low-relief mould specimens resulting from the uniform compaction of clay are not clearly observed in thin sections, and this is the case of studied specimens, which are evidently without vertical channels. By documenting various morphs of the Aspidella plexus fossils in relation to different lithological settings of their preservation in sand and clay substrate, Gehling et al. (2000) distinguished features of biomechanical deformation from those that were genuinely organismal morphological features. Features produced by deformation and taphonomic changes because of dewatering, collapse and compaction, and pattern of degradation dependent on the substrate properties and degree of decay are numerous, such as concentric wrinkles, grooves, rings or annulations, marginal rim, and radial grooves. Genuine morphological features are few: bulb shape, basal protrusion and surface stem. Thus, the surface marks preserved in Aspidella are mostly abiotically induced on the decaying organism. In certain occurrences of Aspidella, the bedding surface textures of entombing sediments are consistent with the presence of microbial mats (Gehling 1999). Indirect evidence of microbial mats are elephant skin texture, iron oxide or carbonaceous coating, bacteri-

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ally induced mineralization, and enhanced pyrite framboid precipitation (Fedonkin 1992; Narbonne 1998; Gehling et al. 2000; Noffke et al. 2013). However, even in successions rich in microbial mat lamination (Gehling 1999; Grazhdankin et al. 2008; Meyer et al. 2013; Chen et al. 2014), there are no recorded specimens of preserved organic matter from the body wall or integument and internal tissue. The specimens described as ‘discs of the Jinxian biota’ and as a new type of fossil (Zhang et al. 2006; discussed above), which are here synonymized with Aspidella, have been observed in thin sections and analysed in elemental composition by SEM/EDX (scanning electron microscope with an energy-dispersive X-ray detector). They appear as thin microcrystalline quartz and chlorite membranes parallel to the bedding plane and without any carbonaceous material (Zhang et al. 2006). Thin and sandwiched between the sediment layers, the specimens do not show any vertical structures that could be abiotically formed. We have not found any features attributed to the aforementioned abiotic structures in the cross-sections of the layers containing the impressions in our collection. Neither distinct bacterial mat lamination nor wrinkled surface structures or sediment microbial textures have been observed in the sediment. The specimens do not resemble microbial colonies or rip-off fragments of mats. They are consistently shaped as discs with very regular and sharp-outlined edges that are in strong contrast to the appearance of redeposited microbial mats. Their smooth surface is dissimilar to the textured microbial mat fragments. We exclude abiotic mechanisms for forming the described structures from the Xingmincun Formation, or the possibility that they represent reworked, resistant organic remains of microbial mats being redeposited in local environments. The structures are impression fossils of the soft-bodied organisms belonging to the Aspidella plexus.

Taphonomic comparisons The taphonomic variants and size range of Jinxian Aspidella are similar to the assemblages occurring in the fine-grained siliciclastic successions in outer shelf to slope settings, such as in Avalonian England (Charnwood Forest), the Avalon Peninsula in Newfoundland and northwest Canada, and Finnmark in northeastern Norway (Farmer et al. 1992; Narbonne 2005, 2007; Menon et al. 2013; Narbonne et al. 2014; ). The burial and diagenetic conditions differ between these areas, but the preservation mode is


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similar and recognized as the Fermeuse-type (see Gehling et al. 2000; Narbonne 2005; Laflamme et al. 2011). Moreover, a persistent feature that is universal for the occurrences of the Ediacaran fossils, regardless of the environmental and taphonomic conditions, is the selective preservation of macrofossils as inorganic impressions, with very few exceptions, in contrast to organically preserved microfossils within these successions. These organically preserved microfossils, which are often threedimensional and robust enough to be extracted, are recognized as photosynthetic cyanobacteria and algae (see below). Similarly, the macroscopic carbonaceous compressions recorded in the lower Ediacaran Lantian and Miaohe successions are algal in origin, perhaps with a few putative metazoans (Yuan et al. 1999, 2011; Xiao et al. 2002). In Finnmark, the assemblage of impressions derives from the Innerlev Member, Stappogiedde Formation (Farmer et al. 1992). The discoidal specimens preserved in epirelief and hyporelief in siltstone and fine-grained sandstone were originally attributed to Cyclomedusa, Ediacaria, Beltanella, Nimbia and Hiemalora. With the exception of Hiemalora, which shows radial impressions of morphological structures, such as tentacles (Gehling et al. 2000; Fedonkin et al. 2007; Grazhdankin et al. 2008), surface features of these taxa are concentric in geometry and mostly taphonomic. The specimens are elliptical in outline (long axis parallel to the strike of the cleavage), with concentric furrows, ridges or faint radial wrinkles, and a central boss. Their diameter ranges from 13.0 to 50.0 mm. They are taphonomic variants and belong to the Aspidella plexus (Narbonne 2005; H€ ogstr€ om et al. 2013). The Finnmark assemblage is preserved without any evidence of organic body walls, associated microbial mats, or biofilm coatings. Conversely, the organically preserved cyanobacterial and algal microfossils occur in the underlying and succeeding strata, whereas macroscopic Sabellidites occurs above the interval with impression fossils (Vidal & Siedlecka 1983; Farmer et al. 1992; H€ ogstr€ om et al. 2013). This evident selective preservation indicates that the properties and biochemistry of organic matter comprising the Ediacaran soft-bodied metazoans (Aspidella and Hiemalora) were very different from those of photosynthesizing microbiota and the annelidan Sabellidites (Moczydłowska 2008; Moczydłowska et al. 2014). Tectonic deformation and thermal activity affected the entire succession in Finnmark during the early Palaeozoic Caledonian Orogeny. The thermal processes altered the organic matter buried in sediments, as is shown by the maturation of microfossil resistant walls, or transformed and

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mobilized the hydrolysable and labile organic fraction, causing its escape and leaving only the impressions of soft bodies behind. The selective preservation of organic matter in fossils is explained by the constituent labile polymers in the body walls of Ediacaran metazoans, in contrast to refractory biomacromolecules in cell walls of photosynthetic microbiota and in the chitinous wall of Sabellidites. Similarly, tectonic and thermal processes affected the successions in the Avalon area (the early Palaeozoic Appalachian Orogeny) and in northwest Canada (the Mesozoic Cordilleran Orogeny), where organic-walled microfossils are preserved in both the Proterozoic and Cambrian rocks (Hofmann 1985, Hofmann 1994; Baudet et al. 1989; Parsons & Anderson 2000). However, the Ediacaran macrofossils are typically preserved as impressions (Narbonne 2005, 2007; Narbonne et al. 2014). In the White Sea area, the effect of selective preservation is even more distinct. The succession lies almost horizontally and is highly uplifted, mildly lithified, yet thermally altered because of granitic intrusions and volcanism. The organically preserved Sabellidites-like and algal fossils are found in the same sediment intervals with diverse fossils including, among others, Charnia, Dickinsonia, Kimberella, Tribrachidium and Aspidella, which are as a rule impressions (Fedonkin et al. 2007). This supports the interpretation that the thermal maturation of organic matter eliminated the soft-bodied Ediacaran fossils from the record because of their biochemistry and non-resistance. The classical Ediacaran deposits of South Australia are medium- to coarse-grained sandstones of the Ediacara Member of the Rawnsley Quartzite and contain diverse assemblages of soft-bodied fossils known as the Ediacara Biota, including a great variety of Aspidella morphs (Tarhan et al. 2015). Not a single carbonaceous compression or organically preserved specimen of any taxon is known in this site, which represents deposits accumulated in the delta front to canyon floor environments and below the wave base (Gehling & Droser 2013). The red beds associated with the Ediacara Member indicate oxidation of the shallow marine strata in high-energy conditions (evident by slumping, mass flow, transport of sediment and fossils), but this process alone may not be the only reason for the lack of organic preservation of fossils, which are very abundant and densely distributed. The Ediacaran Biota preserved as moulds in laminated limestone in the Khatyspyt Formation of the Olenek Uplift, northern Siberia, and deposited on the ramp of a siliciclastic-carbonate platform, is comparable to the Avalon fossil assemblages (Grazh-

LETHAIA 49 (2016)

dankin et al. 2008). Moreover, some are fragmentarily preserved as carbonaceous compressions on impression moulds, but not Aspidella. Those fragments of carbonaceous compressions may be attributed to algal thalli or microbial colonies rather than metazoan fossils (Grazhdankin et al. 2008). Carbonaceous compressions of the Lantian and Miaohe biotas in China are predominantly photosynthetic cyanobacteria and algae, and even if they also comprise metazoans, the properties of the organic matter in these metazoans cannot be known because the successions are diagenetically permineralized. These biotas are preserved because of the silicification of the host calcitic mudstone and thus cannot contradict the observations and the proposed interpretation that the Ediacaran metazoan organisms were made of non-resistant biopolymers (see below). With regard to other carbonaceous compression fossils, it is true in some cases of conditions and taphonomic modes leading to exceptional preservation, such as those in the terminal Ediacaran Gaojiashan biota or middle Cambrian Burges Shale biota, that authigenic mineralization (pyritization and aluminosilicification) and kerogenization allowed preservation of soft-bodied metazoans (Gaines et al. 2008; Cai et al. 2012; Schiffbauer et al. 2014). However, these processes are not the only causes for making possible the preservation of soft bodies, because without them and in common burial conditions on shallow marine shelf, the tubular metazoan Sabellidites is three-dimensionally organically preserved; it is not mineralized and not coated by minerals. This implies that the major factors leading to organic preservation were refractory biopolymers in organic matter in the integument of the organism’s tube (chitin) and anoxic burial conditions in the bottom sediment (Moczydłowska et al. 2014).

Properties of organic matter in Aspidella and Ediacaran metazoans The lack of carbonaceous material preservation in Aspidella in all case studies, regardless of burial conditions and preservation modes, suggests that the organic matter comprising the soft-bodied organisms producing the impressions was non-resistant as is typical of metazoan cells, which lack cell walls but have cell membranes. In other words, the integument or body wall of Aspidella was made of biopolymers that were mechanically firm enough to produce morphologically persistent and abundantly preserved moulds but chemically labile to decay. By

LETHAIA 49 (2016)

contrast, the resistant walls in plant-like cells of photosynthesizing microbes rendered possible the preservation of microbial mats as distinct laminae in the entombing sediment and could serve as a death mask for preserving impressions when metazoan bodies are gone. Photosynthetic micro-organisms are characterized by refractory biomacromolecules that have been synthesized by cyanobacteria, bacterans in cell walls and trichome sheaths, and algae, algaenan and sporopollenin groups in cyst walls (Tyson 1995; de Leeuw et al. 2006). Those microfossils that were inferred to represent algal cysts appear to have survived burial conditions and diagenesis for c. 1.8 Ga (Lamb et al. 2009; Moczydłowska et al. 2011). Cyanobacterial microfossils may have been preserved for over 3 Ga (Schopf 2006; Schopf & Kudryavtsev 2009; Schirrmeister et al. 2015). The oldest organically preserved macroscopic metazoan Sabellidites is c. 550 Ma (Moczydłowska et al. 2014). The only older ones, c. 635–577 Ma, could be the Lantian putative metazoans preserved as carbonaceous compressions, and reinterpreted by Van Iten et al. (2013, 2014) to represent conulariid cnidarians or closely related medusozoans after originally being recognized as algae or of unknown affinity (Yuan et al. 2011). In newly recovered external moulds of the Ediacaran organism Coronacollina, Clites et al. (2012) inferred that it was either biomineralized or comprised of chitin because it exhibits articulated elements such as rigid spicules, although not actually preserved, and resembling a demosponge. The chitin is not preserved in this fossil, even if it had been present in a skeletal fibre as in demosponges, and thus was not considered to be preservable in siliciclastic sediments by Clites et al. (2012). This is not the case. Although not found in Coronacollina, chitin is preservable in siliciclastic sediments of the same age in the aforementioned annelidan fossils (Moczydłowska et al. 2014), and it could be synthesized by sponges of this age because chitin is known in skeletons of both demosponges and hexactinellids (Ehrlich et al. 2007a,b). Coronacollina remains an uncertain taxon, but sponge-grade phosphatized body fossils with cellular resolution have actually been recovered from the early Ediacaran Doushantuo Formation (Yin et al. 2015). The latter Eocyathispongia is preserved with various cell types and morphology of the poriferan affinity animal (Yin et al. 2015). Growing evidence shows that representatives of modern metazoan phyla began to synthesize resistant chitin (annelids) and yet-unrecognized polymers (cnidarians) at the end of the Ediacaran (Moczydłowska et al. 2014; Van Iten et al. 2014).


627

This continued throughout the Cambrian in other clades, especially successfully by arthropods. The record of carbonaceous fossils representing fragments of non-mineralizing metazoans, such as annelidan chaetae, cuticles of sipunculan worms, scales, scalids and pharyngeal teeth of possible priapulids or of uncertain origins (Wiwaxia), is well known in the Cambrian Chengjiang, Kaili and Burgess Shale assemblages (Harvey et al. 2012). However, some microscopic fossils of the same aspects occur in the terminal Ediacaran and earliest Cambrian on the East European Platform and in South Australia, i.e. Ceratophyton and undetermined metazoan remains that are identical to cuticle fragments from the Kaili Formation (Moczydłowska 1991, 2008; Zang et al. 2007; Moczydłowska et al. 2015). These document the presence of lophotrochozoan-like metazoans producing resistant polymers long before (c. 10 Ma) the Cambrian. It is apparent that more metazoans of modern phyla affiliation not only evolved before the Cambrian explosion but also survived the end-Ediacaran extinction as well. The Ediacaran metazoans, with a few exceptions of taxa related to modern clades, did not possess the ability to synthesize refractory compounds in body walls and, therefore, could not be preserved despite their macroscopic to large dimensions, abundance, cosmopolitan distribution, and adaptation to various ecological niches. This probably ultimately caused the extinction of most of them because of the lack of a body wall that was protective against rising mobility, bioturbation, competition for food, and predation among early metazoans. Also, the ecological impact of newly emerging metazoans and ecosystem engineering could have contributed to the extinction of the Ediacaran biota (Laflamme et al. 2013). Two questions remain: 1, what was the biochemical composition of their body wall; and 2, what triggered the invention of refractory biopolymers in metazoans, if not the stimuli mentioned? The change in biosynthesis pathways in metazoans at the end of the Ediacaran Period from non-resistant biopolymers to resistant chitin and collagen groups is a major event that constituted part of the success of the Phanerozoic metazoans. Biochemistry, including biomineralization, may be as important a factor in their evolution as environmental change in selecting the fittest. It is exemplified by photosynthesizing biota from cyanobacteria to vascular plants, which survived and thrived over 3 Ga because of the resistant cell walls they inherited in part from the earliest lineages though endosymbiosis and then shared in all clades.

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Conclusions The studied impressions from the Xingmincun Formation are preserved as flat or low-epirelief moulds on the bedding plane surfaces and low-hyporelief casts on the bedding soles because the fine-grained, clayey host sediment is diagenetically compacted. We positively recognize the Aspidella plexus fossils as organisms because of their morphology, dimensions, distribution, and environmental context comparable to other examples of Aspidella and by excluding abiotic processes as the source of the structures. Typical features of Aspidella that are universally preserved in all depositional facies are circular structures (rings, ridges or rims) and a central boss, and these elements are visible in the present collection, although other features observed in this fossil plexus are not present. We conform to the prevalent hypothesis that the Aspidella impressions were formed by holdfasts of frondose, soft-bodied sessile organisms that were partly buried in the sediment surface while alive. We also agree with inferences that the organisms were metazoan in origin. Lack of organic matter preservation in Aspidella, regardless of preservation conditions, indicates that biopolymers in its body were labile. This is in a sharp contrast to refractory biomolecules that have been synthesized by contemporaneous photosynthetic uni- and multicellular biota of cyanobacterial, algae and some of unknown origins, and a few organically preserved or by carbonaceous compression metazoans. The early metazoans, selectively preserved and known mostly by their impressions in the Ediacaran, were comprised of non-resistant biopolymers and differed from the subsequently evolved metazoans by this property. The synthesis of compounds in the body integument of early metazoans changed between these extinct Ediacaran clades and those that evolved at the end of the Ediacaran and in the Cambrian, producing refractory biopolymers of the chitin and collagen groups that were also biomineralized. Still not fully appreciated, we consider the change of organic synthesis in metazoans as a biochemical revolution that played a major role in the Cambrian radiations. Acknowledgements. – Our research was supported by the Swedish Research Council (Vetensk apsr adet) project grant Nr 621-20121669 to MM, which made possible the research visit of FM to Uppsala University, and the National Natural Science Foundation of China (No. 41173051) to FM. We thank the Reviewers James Schiffbauer and Alex Liu for their comments and useful sugges-

LETHAIA 49 (2016) tions, and acknowledge the Editors Alan Owen and Peter Doyle for thorough reading of the manuscript and editorial work.

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