Australia: The Land Where Time Began

A biography of the Australian continent 

Bilaterian – Oldest Specimen Found in the Ediacaran of South Australia

It was predicted by analysis of modern animals and trace fossils that the oldest bilaterians were simple and small. Such animals should have been part of the Ediacaran biota, which is the earliest known macroscopic complex animal communities that have been preserved, though they would be difficult to recognise in the fossil record. In this paper Evans et al. describe Ikaria wariootia gen.et sp. nov. from the Ediacara Member, South Australia, as a small, simple organism that has anterior/posterior differentiation. They found that the predictions for progenitor of the trace fossil Helminthoidichnites, which was indicative of soil movement and displacement, was matched by size and morphology of Ikaria. Helminthoidichnites occurs in the Ediacaran Member stratigraphically below classical body fossils. Together, it is suggested by these that the Ikaria is one of the oldest total group bilaterians that have been identified from South Australia, with little deviation from the characters that were predicted for their last common ancestor. Also, these trace fossils persist into the Phanerozoic, and provides a critical link between the Ediacaran and the Cambrian. Within the soft bodied biota from the Ediacara the first macroscopic fossil animals are recognised (Xiao & Laflamme, 2009; Erwin et al., 2011). Among these are candidate poriferans (Clites, Droser & Gehling, 2012), cnidarians (Droser & Gehling, 2008) and ctenophores (Zhu et al., 2008). Rare taxa of the Ediacaran biota have been interpreted as bilaterians, namely Kimberella (Ivantsov, 2013; Gehling, Runnegar & Droser, 2014). Small furrowed trace fossils have, however, been generally accepted as evidence for total group bilaterians in the Ediacaran (Jensen, 2003; Buatois & Mángano, 2016; Parry et al., 2017). It is suggested by the size and morphology of trace fossils that they were produced by millimetre-sized organisms that would be difficult to recognise in the fossil record (Gehling & Droser, 2018).

Helminthoidichnites are horizontal trace fossils that are found in deposits dating to the Ediacaran and Phanerozoic globally (Buatois et al., 2014; Wood et al., 2019). The burrow of Helminthoidichnites is curvilinear, and can be preserved on bed tops as well as bottoms and most commonly occurs on the base of thin (submillimetre to millimetre scale) discontinuous sand bodies, or shims (Jensen, 2003; Tarhan et al., 2017). It is indicated by the preservation of Helminthoidichnites in negative relief that are flanked by positive levees on the bed bottoms that the progenitor moved beneath thin sand bodies following deposition and burial, displacing sediments (Jensen, 2003; Buatois, 2016; Gehling & Droser, 2018; Tarhan et al., 2017). The ability of the progenitor to move vertically, though on millimetre scales, is indicated by relationships that have been observed between intersecting Helminthoidichnites (Gehling & Droser, 2018). According to Evans et al., the rare Helminthoidichnites that have been found penetrating body fossils of macroscopic taxa may represent the oldest evidence of scavenging (Gehling & Droser, 2018).

Helminthoidichnites-type structures can be produced by a variety of bilaterians in modern environments (Buatois & Mángano, 2016; Gehling & Droser, 2018). A likely progenitor for Helminthoidichnites from the Ediacaran has not yet been identified, though there have been suggestions that these were produced by simple “worm-like animals” (Buatois & Mángano, 2016). Critically, it would have been small, having a maximum diameter of less than that observed for Helminthoidichnites, based on the nature of sediment displacement by a horizontally burrowing organism. Anterior-posterior differentiation is necessitated by such behaviour, as well as a coelom, which is consistent with Bilaterian grade tissue organisation (Jensen, 2003; Buatois & Mángano, 2016; Gehling & Droser, 2018; Budd & Jensen, 2017). Within the Ediacara Member, Rawnsley Quartzite, in the Flinders Ranges and the surrounding regions of South Australia, Helminthoidichnites have been abundantly preserved (Jensen, Droser & Gehling, 2006). The Ediacaran Member consists of shallow marine sandstone event beds 50 to 500 m below a basal disconformity of Cambrian age (Gehling, 2000).

The excavation and reconstruction of 37 m scale fossiliferous bed surfaces have revealed in situ communities of the Ediacara Biota, at the National Heritage Nilpena site (Droser et al., 2019). Helminthoidichnites is found more than 100 m beneath the first appearance of Kimberella at Nilpena and the Flinders Ranges (Gehling & Droser, 2012; Gehling et al., 2019). Currently there are no radiometric dates that could constrain the absolute age of the Ediacaran Member; there are, however, significant overlap of taxa with deposits that are well established from the White Sea Region of Russia that indicates that these are likely to be between 560 and 551 million years old (Martin et al., 2000; Waggoner, 2003; Grazhdankin, 2014; Boag, Darroch & Laflamme, 2016). The early appearance of trace fossils in South Australia may be corroborated by a similar pattern of leveed, horizontal trace fossils (though in this case assigned to ichnogenus Archaeonassa) occurring stratigraphically below White Sea assemblage body fossils in Russia (Buatois & Mángano, 2018; Grazhdankin, 2014).

Systematic Description

Ikaria Wariootia gen. et sp. nov.

Etymology

The generic Name is after the word “Ikara,” Adnyamathanha name for Wilpena Pound, and means “meeting place” in the Adnyamathanha language. In the view from Nilpena Ikara is the major landmark, and the fossil has been named to acknowledge the original custodians of the land; species are named for Warioota Creek, which runs from the Flinders Ranges to Nilpena Station.

Holotype. P57685 (South Australian Museum)

Paratype.   P57686 (South Australian Museum) 

Field Paratypes. 1T-A bed 001to 007; Nilpena.

Horizon and Locality. Ediacaran Member, Rawnsley Quartzite at the National Heritage Nilpena field site and Bathtub Creek.

Diagnosis. Irregular millimetre-scale ovoid preserved in negative hyporelief. The major axis length averages 2.3 times the minor axis. There is a distinct asymmetry along the major axis with one end wider and more broadly curved. In profile the broader end is preserved in more significant negative relief and with a steeper curvature. Rare specimens are bent about the long axis and/or exhibit potential evidence of modularity, with 2 to 5 body divisions.

Description. I. wariootia are well-defined elongate ovals, fusiform in shape. Three-Dimensional (3-D) laser scans demonstrate clear anterior/posterior differentiation, with one end distinctly smaller and more tightly curved. Length of the major axis ranges from 1.9 to 6.7 mm and the minor axis from 1.1 to 2.4. Preserved depth ranges from 0.6 to 1.6 mm. There is a consistent linear relationship between total length and total width (SI Appendix, Fig. S1A) The relationships between total length and depth (SI Appendix, Fig. S1B) as well as a width and depth (SI Appendix, Fig. S2). Depth is always less than width, suggesting that the fossil of Ikaria is compressed. This confirms previous interpretations that the preserved depth of specimens from the Ediacaran Member is strongly influenced by taphonomic processes (e.g. ref. Evans, Droser & Gehling, 2017).

The morphology of Ikaria is consistent across specimens and is unambiguously distinct from other structures, though it is very simple. For rip-up clasts of organic mats, which are irregular, the consistent shape and length-to-width rations are not what is observed (Tarhan et al., 2017). Rip-ups do not occur in the same lithologies and facies as Ikaria (Tarhan et al., 2017; Gehling & Droser, 2013), which represent deposition in an environment of lower energy, though mat rip-ups are present within the Ediacara Member. Also, the biostratinomic and diagenetic history of rip-up clasts are different those of Ikaria and all other body fossils (Tarhan et al., 2017). Ikaria have a sharp outer margin and they are preserved with considerable relief, distinct from the surrounding matrix and organic mat textures. This is consistent with other taxa from the Ediacara Member that are nonsessile (Droser et al., 2018), which suggests that Ikaria represent the body of a free-living organism.

Ikaria can be easily differentiated from other taxa that are preserved on the same bed surface and of similar size and scale (SI Appendix Fig. S3).Therefore, it is not likely to be a juvenile form of a previously described taxon. A maximum size of ~7 mm is suggested by the lack of larger specimens with comparable morphology. The biologic, body fossil origin of Ikaria is corroborated by the recognition of other taxa on the same scale and with similarly well-defined out margins that are distinct from the organic mat.

There have been rare finds of specimens of Ikaria and Helminthoidichnites together. The range of widths of Ikaria plots entirely within those measured for Helminthoidichnites with the maximum size of body fossils no exceeding that of trace fossils (SI Appendix, Fig. S4). Also, it is indicated by the Anderson-Darling test that the size-frequency distributions do not differ significantly (P value 0.448). And, this combined with clear anterior-posterior differentiation, suggests that Ikaria is the only known contemporaneous body fossil that has the suite of body characters that have been predicted for the progenitor of Helminthoidichnites.

Discussion

It is rare, in general, to find trace fossils as well as the organism that produced them preserved together, in particular with respect to the mobile metazoans. According to Evans et al. this can be attributed to both different pathways of preservation between the body and trace fossils and the ability of the animal to move away from the area that contains evidence of its activity (Bromley, ed. 1996; Seilacher, ed., 2007). The morphological characteristics of body fossils from the same deposit can be used, in certain cases, to determine reliably the progenitors of particular trace fossils (e.g., Gibb, Pemberton & Chatterton, 2016).

In the Ediacara Member body fossils include Ikaria, are well preserved on the bottoms of centimetre-scale sandstone beds with the tops of these organisms being overlain with early mineralisation of sand casting following burial (Jensen, 2003; Tarhan et al., 2017; Jensen, Droser & Gehling, 2006). Though in rare cases counterparts are identified on bed tops, these are poorly preserved and at a resolution that is not likely to produce identifiable features at the same scale as Ikaria. Helminthoidichnites is found, in contrast, on both bed tops and bottoms, though most commonly on the base of millimetre-thick shims, where it is rare to find fossils that are well preserved (Jensen, 2003; Tarhan et al., 2017). It is indicated by negative hyporelief preservation that Helminthoidichnites formed after the deposition of overlying sand, with the organism that produced it capable of moving into and out of thin layers of sand (Gehling & Droser, 2018). It is predicted by this that Helminthoidichnites should only be found and its progenitor on the same bed bottom in rare instances when it died while it was burrowing underneath thin bodies of sand. Even if Ikaria was preserved at the end of a trail, it is not likely that it would be possible to identify as distinct from that trace, given the simple morphology and preservation of both body and trace fossil in negative relief. Evans et al. interpreted the surprising discovery of Helminthoidichnites with nearby Ikaria as the result of vertical movement from the bedding plane in the region between the end and its trace fossil and its final resting place. While it is likely that this scenario was exceedingly rare, it may represent the only situation when it would be possible to distinguish associated body and trace fossils, and corroborate further interpretations of Ikaria as the progenitor of Helminthoidichnites.

Evans et al. proposed that Ikaria is the trace marker of Helminthoidichnites and potentially the oldest, definitive bilaterian, at least as represented in the fossil record of South Australia. The only other bilaterian from the Ediacaran Member that is consistently reconstructed as a bilaterian, Kimberella, is found significantly higher stratigraphically than the earliest appearance of Helminthoidichnites (Ivantsov, 2013; Gehling, Runnegar & Droser, 2014; Gehling & Droser, 2012; Gehling; Gehling et al., 2019). Similarities between taxonomic assemblages have been consistently cited as evidence that White Sea assemblage fossils from the Ediacaran Member, Kimberella, are conservatively 560-551 Ma (Martin et al., 2000; Boag, Darroch & Laflamme, 2016). It is suggested by the stratigraphic position of Helminthoidichnites that the first appearance of Ikaria, was likely to be from within this age range, or even possibly earlier. In Uruguay, burrows that were initially interpreted to be from Ediacara age rocks that were much older have age constraints that are uncertain (Pecoits et al., 2012; Gaucher et al., 2013). Trace fossils from Brazil representing the activity of meiofaunal bilaterians, are present about 30-40 m above a tuff that has been dated to 555 Ma and it is in close association with Cloudina, which indicates that they are likely to be younger than Ikaria (Parry et al., 2017; Boag, Darroch & Laflamme, 2016). Recently, a segmented bilaterian from South China has been described, that was associated with trace fossils, was interpreted to be younger, larger and more complex than Ikaria (Chen, 2019).

According to Evans et al., the ability to move and produce trace fossils that are recognisable is not unique to bilaterians. It is probable that complex and trace fossils from older Ediacaran deposits produced by muscular eumetazoans that were interpreted to be cnidarians (Liu, 2014). It is not likely that the crown group bilaterians are represented by Dickinsonia and other similar fossils from the Ediacaran though were mobile and left trace fossils (Sperling & Vinther, 2010; Evans, Gehling & Droser, 2019). Simple burrows are generated by modern protists, though typically they are smaller than Ikaria (Serevin & Culver, 1982; Matz et al., 2008). It has been demonstrated in lab experiments that mobile foraminifera form burrows in clay and silt; they do not produce burrows, however, in fine-grained or coarse-grained sand (Serevin, Culvin & Blanpied, 1982). In deep sea environments large testate amoeba are associated with trails similar to those that have been observed in the Ediacara, though these are surficial and represent movement by rolling (Matz et al., 2008). Flatworms are mobile, though they do not burrow below the sediment-water interface, and only rarely leave fossil traces (Valentine, Erwin & Jablonski, 1996). Expression on bed bottoms with furrows is unique among these examples to Helminthoidichnites, which suggests movement associated with significant displacement of medium sand grains. This is consistent with reconstructions of Ikaria which has musculature and a coelom (Gehling & Droser, 2012; Clark, 1981). These characteristics are unique to bilaterians when combined with the relative size of the body and trace fossils.

Anterior/posterior differentiation in Ikaria is characterised by polarity and relief, which is supported by movement that is directed in trace fossils. Within Helminthoidichnites preservation of V-shaped transverse ridges suggests peristaltic mobility (Gehling & Droser, 2018). A potentially modular body construction of Ikaria is implied by its morphology, would have aided in the organisation of muscles that would be required for peristalsis (Carroll, Grenier & Weatherbee, 2001). It is revealed by sediment displacement and scavenging that Ikaria is likely to have had a coelom, mouth, anus, and through-gut (Gehling & Droser, 2018; Budd & Jensen, 2017; Clark, 1981), though it is not likely that these would have been preserved in the fossil record. It is indicated by preferential preservation of Helminthoidichnites beneath thin sand bodies that Ikaria sought out these environments, possibly as a result of increased availability of oxygen. Ultimately, due to decomposition of organic matter, which is supported by the restriction of Helminthoidichnites to beds <15 mm thick, as the depth of the overlying sand increases, oxygenated environments are gradually replaced by sulphidic, inhospitable settings (Gehling & Droser, 2018; Tarhan, 2017; Gehling, 2019). It is likely that Ikaria had the ability to detect organic matter that was buried in environments that were well oxygenated as well as conditions that were potentially toxic, which suggests rudimentary sensory abilities. These features combined suggest that this organism was markedly complex, compared with contemporaneous Ediacaran biota, in spite of the simple morphology that can be observed directly on fossil specimens of Ikaria. It has been demonstrated by molecular phylogenetic analysis of modern metazoans that developmental programming is highly conserved between disparate groups. This led initially to the hypothesis that the last common ancestor (LCA) of bilaterians (animals with an opening at each end of a trough-gut) was relatively complex, having many of the features that are common to a variety of such groups, which include eyes, segmentation, appendages, and a heart (Carroll, Grenier & Weatherbee, 2001; Knoll & Carroll, 1999; Robertis, 2008). It is indicated, instead, by expansion of this analysis to nonbilaterian animals and their closest single-celled ancestors that components of these conserved developmental pathways have deep ancestry (see Erwin, 2015 for discussion). This suggests, when combined with recent evidence for a sister group relationship between Xenacoelamorpha and Bilateria, that the bilaterian LCA was a simple, small, mobile organism with anterior/posterior differentiation and limited sensory abilities (Erwin, 2015; Erwin & Davidson, 2002; Struck et al., 2014; Hartenstein & Stollewerk, 2015; Cannon et al., 2016; Cunningham et al., 2017). According to Evans et al. it is remarkable that these predictions agree closely with characters identified by this study for Ikaria.

Body and associated trace fossils are relied upon for recognition of the totality of traits of Ikaria. It is not likely that given the simple morphology of Ikaria it would be possible to assign it confidently to the Bilateria, or even the Metazoa, without the relationship between Ikaria and Helminthoidichnites. This is consistent with hypotheses that predictions of the apparent gap between molecular clock predictions for the early divergence of bilaterians and their later appearance in the fossil record is a result of their predicted simple morphology (Erwin, 2015; Cunningham et al., 2017). Therefore, similar prephylum, total group bilaterians may be found in other deposits of the Precambrian fossil record; Ikaria provides a search image for the identification of such forms in the future.

It is suggested by the stratigraphic position of Helminthoidichnites that Ikaria is the oldest total group bilaterian from the fossil record of South Australia. Ikaria represents an example in early animal evolution where phylogenetic predictions correspond directly with the fossil record. Also, the global distribution and recognition of Helminthoidichnites in strata of Cambrian age (Buatois et al., 2014; Wood et al., 2019) is distinct from the overwhelming majority of the Ediacaran Biota. It is likely that Ikaria and/or related taxa existed across the Ediacaran-Cambrian boundary, though Ikaria is not necessarily responsible for the production of all Helminthoidichnites.

Evans, S. D., et al. (2020). "Discovery of the oldest bilaterian from the Ediacaran of South Australia." Proceedings of the National Academy of Sciences: 202001045.