Abstract
Predation is one of the most fundamental ecological and evolutionary drivers in modern and ancient ecosystems. Here, we report the discovery of evidence of the oldest scavenging of shallowly buried bodies of iconic soft-bodied members of the Ediacara Biota by cryptic seafloor mat-burrowing animals that produced the furrow and levee trace fossil, Helminthoidichnites isp. These mat-burrowers were probably omnivorous, stem-group bilaterians that largely grazed on microbial mats but when following mats under thin sands, they actively scavenged buried Dickinsonia, Aspidella, Funisia and other elements of the Ediacara Biota. These traces of opportunistic scavengers of dead animals from the Ediacaran of South Australia represent a fundamental ecological innovation and a possible pathway to the evolution of macrophagous predation in the Cambrian. While the Ediacaran oceans may have had oxygen levels too low to support typical large predators, the Helminthoidichnites maker lived in and grazed on microbial mats, which may have provided a localized source of oxygen.
Introduction
The advent of predation is one of the most significant events for the development of metazoan ecosystem function and structure and is widely accepted as a driver in evolution throughout the Phanerozoic [1]. From a biological perspective, macrophagous scavenging at the very least requires a gut, chemosensory system and comes with an energetic cost. Predation among unicellular organisms may date back 2 GA [2]; however, the earliest definitive evidence of active predation by protists preying on protists has recently been described from eukaryote fossils from the Chuar Group dating from 780 to 740 Ma [3]. Predation has also been recorded in boring holes in the mineralized tubes of Cloudina from the uppermost Ediacaran of China [2,4,5]. Other than this late Ediacaran evidence, Precambrian ecosystems have been considered void of active metazoan macroscopic predation or even carnivorous scavenging. However, the radiation of actively predating carnivores is considered an intrinsic ecological driver of the subsequent ‘Cambrian explosion’ [6–8]. Here, we report the discovery of evidence of the oldest scavenging of shallowly buried bodies of iconic soft-bodied members of the Ediacara Biota by cryptic seafloor mat-burrowing animals.
In composition, the Ediacara Biota consisted of soft-bodied, dominantly sessile enigmatic organisms [9]. Although the affinities of fossils of the Ediacara Biota are still strongly debated, the late Ediacaran trace fossil record (ca. 560–541 Ma) is generally accepted as the earliest reliable evidence of motile eumetazoans in the Ediacaran Period (635–541 Ma) [10–14], prior to the dramatic expansion of metazoan body plans and ecological strategies, such as penetrative burrowing, recorded by the early Cambrian records of both body and trace fossils.
Geologic setting
Set in the Flinders Ranges of South Australia, 400 km north of Adelaide (Supplementary Figure S1), the Adelaide Rift Complex preserves a 10–12 km thick Cryogenian, Ediacaran and early Cambrian succession. Capping the Ediacaran succession, the Rawnsley Quartzite, including the Ediacara Member (Supplementary Figure S2), consists of a succession of shallow marine and deltaic facies that contain one of the best records of fossils of the Ediacara Biota, worldwide. Excavation of in situ, serial fossil beds from the Ediacara Member at the National Heritage Site, Nilpena [13,15], the Ediacara Conservation Park and other sites in the northern Flinders Ranges region [16] has enabled documentation of trace and body fossil associations with respect to the thickness, orientation and structure of the fossil-bearing sandstone beds. The body and trace fossil record is largely the product of storm events that transported sand and smothered benthic communities that lived below fair-weather wave-base (Supplementary Figure S3) ([17], see also ref. [18]). Body fossils are preserved as casts and molds on the base of sandstone beds ranging between 0.2 and 10 cm in thickness. Textured organic surfaces (TOSs) are widespread and are well accepted as evidence of ubiquitous organic mats on the Ediacaran seafloor [18–20].
Results
Meandering furrow (groove) trace fossils, 1–3 mm wide, with levees bearing faint transverse ridges, assigned to as Helminthoidichnites isp. [21], are preserved in rippled marine sandstone beds in the Ediacara Member. Commonly, Helminthoidichnites is preserved on the top of beds (Figure 2B), but also occurs in negative relief, complete with levees, on the bases of very thin sandstone beds (Figures 1–5 and Supplementary Figure S4A–C), together with body fossil impressions.
(A) Dickinsonia costata body segments cross-cut by Helminthoidichnites on bed-sole of H/I (STC excavation, Nilpena; SAM P35740; see Supplementary Figures S1a and S2). (B) Inset of body segments cross-cut by the Helminthoidichnites trace-maker. (C) Helminthoidichnites cutting through clustered pedal surfaces of Beltanelliformis on the base of a 13 mm thick bed (Stirrup Iron Range, SAM P35741). (D and E) Helminthoidichnites cutting pedal casts of Aspidella on bed-soles (Bathtub Gorge, SAM P35742; Nilpena, SAM P42553). (F) Helminthoidichnites associated with a tubular body fossil; directionality of burrowing organisms, inferred from scalloping of levees and denoted by arrows (Bathtub Gorge, SAM P35744). (G) Casts of Funisia dorothea cut by Helminthoidichnites on sole of a 10–13 mm thick bed (Ediacara Conservation Park, SAM P51210); for detail, see Figure 4). All specimens from the Ediacara Member, Rawnsley Quartzite, Flinders Ranges South Australia. Scale bars 10 mm.
(A) Sole of a 3–6 mm thick sandstone bed (here referred to as a sandstone ‘shim’) with groove and levee traces of Helminthoidichnites isp., in alternating relief, made above and within a buried, cryptic microbial mat. Traces display inverted relief in proximity to intersection with a previously made trace (arrowed) (Bathtub Gorge, SAMP35746). (B) Top surface of a 10 mm thick, medium- to coarse-grained sandstone bed with patterns of Helminthoidichnites grooves with distinct levees (Nilpena, SAMP35747); apparent triple junctions represent sites where the trace disappears as the animal moves above or below the mat–sediment interface to avoid the previously constructed trace. (C) Bed-sole of medium-grained sandstone shim with Helminthoidichnites in trails between but three small specimens of Spriggina sp. preserved in negative hyporelief. (D). Bed-sole Helminthoidichnites traces with scalloped levees indicating peristaltic movements (Nilpena, wave-base sand facies, SAMP43192). Scale bars 10 mm.
Helminthoidichnites, as preserved on bed-soles, clearly cuts through the external molds and casts of buried bodies of common macro-organisms of the Ediacara Biota preserved on the same surfaces. Body fossils include Dickinsonia (Figure 1A,B), clusters of casts of the close-packed, discoidal organisms, Beltanelliformis (Figure 1C), solitary specimens of Aspidella (Figure 1D,E), unidentified tubular bodies (Figure 1F) and serially ornamented tubes of Funisia (Figure 1G). The trajectory of Helminthoidichnites is characterized by a tendency to deflect (turning or spiraling) towards, and cut through, the external boundaries and internal structures of these megascopic organisms. Inspections of the soles of suitably thin beds bearing large numbers of both body fossils and trace fossils are rare mainly due to the difficulty with intact extraction in the field. Prior to the current practice of bed-by-bed excavation at Nilpena and Ediacara C.P., material was limited to surface shards of such beds where there was insufficient area to enable interpretive observation. However, even with careful excavation, very thin sandstone beds are difficult to conserve for close examination after transport and cleaning examination under controlled conditions. While limited to relatively few successfully collected specimens, such as that illustrated in Figures 3A,B and 4, and Supplementary Figure S6A,B, these fossiliferous bed-soles show post-burial, preferential cross-cutting and intersection of the macro-organisms by Helminthoidichnites. Owing to the limited access to large areas of such conserved beds preserving both body and trace fossils, there is no easy statistical measure of this implied association. An excavated 8–13 mm thick, aggregate 1.2 m2 sandstone bed, from north Ediacara Conservation Park, revealed clusters of Funisia specimens on a 1500 cm2 bed-sole fragment (Figures 1G, 4 and Supplementary Figure S6A,B) that coincided with multiple crossings by Helminthoidichnites. However, the area encompassing Helminthoidichnites traces in Figure 4, to the nearest 2 cm, clearly overlaps the body fossils, Funisia, Eoporpita, Wutubus and Dickinsonia, on this surface. Demonstrably, the ‘upside-down’ groove trace fossils were not simply over-printed by the macro-organisms, but actively penetrated the sand-buried bodies and microbial-mat substrates. The lack of fine-grained silty or clayey sediment separating sand layers in the Ediacara Member is one of the key reasons for interpreting the TOSs on these fossiliferous beds as being imprints of the cryptic microbial mats. Conversely, in most Phanerozoic trace fossil-bearing strata bearing bed-parallel traces, organic-rich silts and clays account for bed partings.
(A) Bed-sole view of a collected sample of H&I sandstone shim (SAM P51211), excavated from the STC site at Nilpena. (B) Sketch of H/I rippled sandstone shim (SAM P51211), contoured for thickness (2–38 mm) on a 10 cm grid for analysis of spatial distribution of Helminthoidichnites groove and levee traces, plus body fossils of Dickinsonia costata, Rugoconites enigmaticus on the bed-sole, as indicated by symbols. The majority of traces, made along the mat–sand interface recorded by the H/I shim, were restricted to sand cover of less than 15 mm thickness. Specimen of Dickinsonia costata, illustrated in Figure 1, is a separate fragment of H/I shim.
Bed-sole assemblage of Funisia dorothea, Dickinsonia costata, Eoporpita sp. and Wutubus sp. cut by Helminthoidichnites isp., from a 5–12 mm thick sandstone shim (SAM P51210) excavated from Ediacara Conservation Park, below Greenwood Cliff. Criss-crossing groove and levee traces, referred to Helminthoidichnites isp., cutting through a bed-sole assemblage dominated by packed specimens of Funisia dorothea, in addition to the other body fossils (shaded area), preserved in collapsed positive hyporelief.
In the shallow marine settings, interpreted as environments between the shoreface and wave-base, several excavated, intact lenticular beds of sandstone feature Helminthoidichnites on bed bases. The largest collected example, H&I shim (Figures 3A,B), is a 2–38 mm thick bed that features an uneven distribution of Helminthoidichnites on bed bases at Nilpena STC Excavation Site (Supplementary Figure S3). The vast majority of these ‘upside-down’ groove trace fossils occur on bed-soles where the bed is less than 15 mm thick, and none have ever been recorded on soles of beds greater than 25 mm in thickness. There is no physical evidence of vertical penetration of sand layers by trace fossils, regardless of facies or lithology, within the Ediacara Member. Furthermore, spatial analysis demonstrates that the majority of such traces are limited to the thinnest portions of lenticular beds, typically the outer margins (Figure 3B).
Helminthoidichnites burrows either show avoidance of self-crossing (Figure 2B) or inversion of relief (between positive and negative relief) where these meandering traces intersect one another (arrows, Figure 2A). At an intersection, burrow levees of the through-going burrow are not broken at the point where the other burrow ‘disappears’ (Figure 2A–D) as it changes levels.
Discussion
The occurrence of Helminthoidichnites in negative relief on the base of beds is striking and rare among trace fossil assemblages in younger rocks that include Olenichnus [22], and uncommon Psammichnites [23]. The Helminthoidichnites animals appear to have occupied microbial mats at the sediment–water interface [21]. Where such mats were buried below thin veneers of sand, the burrowing organisms behaved as ‘under-mat miners’ [24] by burrowing horizontally along the shallowly buried mats, displacing the sand above and thus leaving bed-base grooves and levees (Supplementary Figure S4A–C). As such these traces are easily mistaken as being made on bed-tops. Bed-by-bed excavation demonstrates that these ‘inverted’ groove and levee burrows are entirely limited to the bases of sand-sheets less than 15 mm thick. Where the burrower encountered shallowly buried carcasses of epimat-dwelling macro-organisms, such as Dickinsonia (Figure 1A,B), Beltanelliformis (Figure 1C), Aspidella (Figure 1D,E), Spriggina (Figure 2C) and Funisia (Figures 1G and 4), arguably they targeted and cut through these buried cadavers, but only when the overlying sand was less than 15 mm thick (Figure 3A,B). The preservation of Ediacara trace fossils in negative relief, on the bases of discontinuous sandstone beds, indicates that these burrows had to have been made after the deposition of these thin sand layers and the burial of these macro-organisms on the seafloor (Supplementary Figure S4A–C). We hypothesize that, after deposition of a thin veneer of discontinuous sand on the biomat, small mat-dwelling Helminthoidichnites makers moved along the interface between this sand veneer and the underlying biomat, in order to scavenge the decaying microbial mats and opportunistically targeting the buried corpses of decaying soft-bodied Ediacaran organisms. Much later, external molds of more resilient bodies and casts of decaying carcasses, including the burrows that cut through them under the thin sand, were conserved in the manner characteristic of all fossils of the Ediacara Biota in South Australia [25,26], namely by very early lithification of these bed-sole surfaces. This record of scavenging of buried mats and corpses, by-bed-parallel burrowing organisms, represents an ecological innovation previously unreported from the Ediacaran strata.
Horizontal burrows preserved in micro-laminated limestone of the Shibantan Member of the upper Ediacaran Dengying Formation, in the Yangtze Gorges area of South China [27–29], are clearly associated with microbial mat-laminated sediment with an intensity that might also be interpreted as scavenging of buried organic mats. These confirm the increasing incidence of bed-parallel burrowing in organic-rich sediments in the late Ediacaran.
The uneven spatial distribution of Helminthoidichnites indicates that the makers penetrating beneath the thin sand cover were constrained by the thickness of the overlying sand body which we suggest was an intra-mat redox boundary. The thicker the overlying sand and the greater the distance from the edge of discontinuous sand layers, the lower are the levels of ambient oxygen within the smothered microbial mat. Furthermore, large bed-sole samples bearing Helminthoidichnites make it clear that burrowers remained near the edges of thin sandstone beds (Fig. 4, Supplementary Figs S6A,B). Intrastratal burrowing may have been limited by not only intra-mat and intra-sediment redox gradients, but also by the efficacy of oxygen diffusion through the sand layer from the overlying water column. Thus, the aggregation of these bed-base furrow traces near the margins of thin sand-sheets may reflect both lateral and vertical intra-mat gradients in the concentration of oxygen, as well as of byproducts of anaerobic decay toxic to most metazoans (e.g. hydrogen sulfide). The Helminthoidichnites organism appears to have been attracted to shallowly buried bodies of recently deceased epimat-dwelling macro-organisms, but only when these bodies were close to (<20 cm from) the edge of a lenticular sand sheet or buried below a very thin (<15 mm) sand cover (Figures 3B and 5A–D). The restriction of scavenging to carcasses buried by thin, discontinuous sand layers markedly contrasts with the more common burial events that involved continuous, thick sand cover and the consequent lethal smothering of entire (both epifaunal and infaunal) benthic communities, without the possibility of post-depositional burrowing along the buried interface.
(A) Dickinsonia costata on microbial mat, burrowed by small scavenging metazoans leaving bed top grooves and levees in sand below the mat. Only mat–sand interface traces are preserved; intra-mat burrowing is not preserved. (B) Partial smothering of seafloor assemblage below fair-weather wave-base by storm-deposited sand transported from the shore face. (C) A small bilaterian scavenger penetrates the interface between the burial sands and the partially smothered, feeding on the mat and decaying organisms buried below a thin (<15 mm) veneer of sand, and avoiding the lower levels of the mat and thicker sand cover where the ambient oxygen was too low for vital activity. (D) Bed-sole external mold of mat-mediated TOS and groove traces made where a scavenging organism moved between the mat and smothering sand, cutting through decaying bodies. Based on specimen in Figure 1A,B.
The style of preservation is typical of bed-base Helminthoidichnites traces, which are distinguished from those occurring along bed-tops by intermittent inversion of positive and negative relief, especially where these meandering traces intersect one another (arrows, Figure 2A). These bed-base furrows and levees are interpreted as galleries resulting from displacement of the sand as the animal moved at the interface between the mat and an overlying thin sand deposit (Figures 2A and 5, and Supplementary Figure S4A–C). Relief inversion occurred when the animal galleries penetrated downwards into the microbial mat to avoid previously made passages. Subsequently, these intra-mat galleries collapsed and were cast from above by the burial sand layer. It has been suggested that Ediacaran mat mining was analogous in the construction and variable relief to galleries made by modern tree borers [24] as they change levels between the inner and outer layers of tree bark. Changes in relief of Helminthoidichnites reflect whether galleries were made at the mat–water interface or within partially buried mats.
The majority of Helminthoidichnites specimens, as recorded from the Ediacara Member do not typically cross-cut macroscopic body fossils [21,30]. Thus, the maker of these trace fossils was probably largely an intra-mat grazer. However, the Helminthoidichnites animal may have had an ecology similar to modern earthworms or certain nematodes [31], which operate as omnivores that scavenge both plant detritus and dead animals. That the Helminothoidichnites animal was able to scavenge dead animals as well as buried microbial mats demonstrates a level of biological, metabolic and chemosensory sophistication. Furthermore, exclusive carnivory requires more oxygen than simple grazing [8,32]. However, recent studies of modern microbial mats have demonstrated that oxygen levels within and just above the mats can be up to four times higher than in the overlying water column [33], providing a ready source for the Helminthoidichnites scavenger even if general oxygen levels in the shallow oceans were still well below those which would typically be required for a predator [34] or were unpredictable in a dynamic redox landscape [35].
These trace fossils appear to represent the reactive interaction of infaunal organisms with their surrounding biotic, chemical and physical environment. The Helminthoidichnites trace-maker actively changed levels when crossing previously made furrows (Figure 2A), as well as cutting through the carcasses of shallowly buried macro-organisms, such as Dickinsonia (Figure 1A,B), Beltanelliformis (Figure 1C), Aspidella (Figure 1D,E) and Funisia (Figures 1G, 4). This scavenging of buried carcasses is consistent with the recent suggestion that the organic carbon resource heterogeneity generated by Ediacaran ecology and in this case, shallow burial of large organisms, may have actually directly been a cause of the radiation of mobile bilaterians [14,36].
The affinities of the trace-maker of Helminthoidichnites remain uncertain. No known named Ediacara organisms of appropriate dimensions, such as Praecambridium, or juvenile specimens of Kimberella, Parvancorina and Spriggina, have been discovered in apposition with Helminthoidichnites. This suggests that the cryptic Ediacaran burrowing organism responsible for Helminthoidichnites was too small to be easily resolved as a cast or mold.
Studies of exposed modern intertidal sand flats reveal the capacity of small gastropods to produce groove traces, with beveled levees, leaving directional evidence while remaining hidden within the sand (Supplementary Figure S5A,B). The tiny gastropod traces are easily distinguished from small bivalve mollusc traces that produce no levees, due to differences in locomotion. Evidence of peristaltic locomotion apparent in Ediacaran specimens of Helminthoidichnites comes from analogous V-shaped bevels in the levees of modern gastropod traces.
Our observations of Ediacaran Helminthoidichnites (Figures 1 and 2C) validate predictions that the Precambrian stem-groups for bilaterian animal clades possessed the genetic toolkit for a well-developed chemosensory capacity [37,38], and that this toolkit may therefore have been part of the repertoire of Ediacaran animals (Figure 5).
The topology of recently published molecular trees representing the rise and diversification of animal phyla, recalibrated to include the earliest fossil record of stem- and crown-groups of modern animal phyla, places the earliest divergence of bilaterian animals in the Ediacaran, prior to the Cambrian radiation [8,39,40]. For the majority of the Ediacara Biota, phylogenetic affiliations are contentious and will not be easily resolved. However, while potential makers of Helminthoidichnites were too small to resolve characters that differentiate extant animal clades, the maker was, due to the tissue-grade requirements of true furrow excavation, almost certainly a bilaterian [14].
Motility appears to have evolved late in the Ediacaran. Potential rudimentary traces occur sparsely in the 565 Ma rocks of the Conception Group in SE Newfoundland [41,42], whereas furrows and feeding traces are relatively common in late Ediacaran (<560 Ma) strata of South Australia, NW Canada and Russia [43]. This transition in the diversity and abundance of trace fossil forms was accompanied by major changes in benthic life mode and trophic strategy. Older, rangeomorph-dominated Ediacara Biota-bearing assemblages (e.g. Mistaken Point, SE Newfoundland) were characterized by passive, potentially osmotrophic feeding on relatively deep seafloors. Younger Ediacara Biota assemblages, in contrast, were characterized by a major diversification of taxa and ecologies in shallower marine settings such as those recorded by the White Sea and Nama assemblages. Among the ecologies to emerge in this ‘second wave’ of late Ediacaran communities were complex matground-faunal interactions, including the radiation of early motile grazers [44] and meiofaunal- to small macrofaunal-scale mat-dwelling and scavenging bilaterians [45]. Arguably, the evolution of a gut and chemosensory system and scavenging behavior evidenced by Helminthoidichnites were the first steps towards the radiation of actively predatory carnivores as intrinsic ecological drivers of the ‘Cambrian explosion’ [6,7,46]. The association of the meander trace fossil Gordia within apparently unmineralized body fossils of Pararotadiscus in the Kaili Biota of South China [47] and a similar eldonioid from the Emu Bay Shale in South Australia [48] are examples of dynamic animal interactions preserved by the exceptional body and trace fossil deposits of early Cambrian strata, that are, herein, described as scavenging during the late Ediacaran.
Summary
Ediacaran trace fossils represent evidence of the existence of small bilaterian animals prior to the ‘Cambrian explosion’ of animals.
Small Ediacaran animals were intra-mat miners that followed organic horizons buried by thin layers of sand.
Mat scavenging included shallowly buried bodies of common members of the Ediacara biota.
This late Ediacaran innovation led to the eventual loss of preservation of buried microbial mats and soft-bodied animals in sand, due to bioturbation: the burrowing of shallowly buried organic-rich sedimentary layers that became common in all well-oxygenated sedimentary settings from the beginning of the Cambrian Period.
This record of latest late Ediacaran (Precambrian) behaviours suggests that the claimed ‘extinction’ of the Ediacara biota, at the beginning of the Cambrian, was largely due to active bioturbation of Ediacaran microbial mats responsible for the preservation of soft-bodies, as casts and molds, in layered sand in the late Ediacaran time.
Funding
The project was funded by the Australian Research Council [grant DP0453393] to J.G.G., NASA Exobiology Program [NASA; grant NNG04GJ42G] to M.L.D., The Ediacaran Foundation, South Australian Museum Waterhouse Club, University of California Riverside and Beach Energy.
Competing Interests
The Authors declare that there are no competing interests associated with the manuscript.
Acknowledgements
We thank R. and J. Fargher for access to the National Heritage Nilpena Ediacara fossil site on their property, acknowledging that this land lies within the Adnyamathanha Traditional Lands. Excavations and bed preparation was by L. Joel, Dzaugis, M.E. Dzaugis, P. Dzaugis, R. Crowder, N. Anderson, J. Doggett, R. Droser, C. Armstrong, J. Perry, D. Reid, D. Rice, M.I. Smith, J. McEntee and E. Gouch; important material was discovered by L. Ragless at Ediacara Conservation Park; M.A. Binnie and M. Ellis provided vital technical support. All numbered fossil specimens are lodged within the South Australian Museum, North Terrace, Adelaide, South Australia 5000.
Abbreviations: TOSs, textured organic surfaces
- Received March 23, 2018.
- Revision received June 19, 2018.
- Accepted June 19, 2018.
- © 2018 The Author(s). Published by Portland Press Limited on behalf of the Biochemical Society and the Royal Society of Biology
References
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