Evidence for Cnidaria-like behavior in ca. 560 Ma Ediacaran Aspidella Latha R. Menon1, Duncan McIlroy2, and Martin D. Brasier1, 2 1
Department of Earth Sciences, University of Oxford, South Parks Road, Oxford OX1 3AN, UK Department of Earth Sciences, Memorial University of Newfoundland, St John’s, Newfoundland A1B 3X5, Canada
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GEOLOGY, August 2013; v. 41; no. 8; p. 1–4; Data Repository item 2013246
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Gibbett Hill
Avalon Peninsula 54°W
Cappahayden
53°W
Renews Head 48°N
Fermeuse Trepassey
St. John’s AVALON PENINSULA
Mistaken Point Briscal
Atlantic Ocean
Ferryland
Drook
47°N
Gaskiers diamictite
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50 km
Mistaken Point
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SIGNAL HILL GROUP
NEWFOUNDLAND
ST. JOHN’S GROUP
INTRODUCTION The affinities and nature of the Ediacaran biota have remained persistently uncertain (Seilacher et al., 2003; Narbonne, 2005). Nevertheless, the claim by Retallack (2012) that a number of these forms may have been lichens and slime molds living in soils rather than marine organisms is provocative, and emphasizes the crucial importance of correctly interpreting the Ediacaran biota in order to understand early animal evolution and the roots of the Cambrian explosion. Molecular clock estimates indicate a Cryogenian (ca. 800 Ma) origin for Metazoa (Erwin et al., 2011). Yet, while bilaterian traces have been described from the latest Ediacaran rocks (e.g., Fedonkin and Waggoner, 1997; Jensen et al., 2006; Rogov et al., 2012; see also Brasier et al., 2013), the apparent lack of evidence for animal activity prior to ca. 555 Ma, among the characteristic frondose and discoidal Ediacaran macrobiota, has been baffling. A report by Liu et al. (2010) of an assemblage of horizontal trails in the Mistaken Point Formation (Newfoundland, Canada), dated as 565 ± 3 Ma (Benus, 1988), raised the possibility of motile metazoans amid the sessile fronds and holdfasts of this oldest Ediacaran assemblage. The evidence presented here directly links similar horizontal traces to the Ediacaran discoidal fossil Aspidella terranovica. Aspidella is one of the earliest named Ediacaran body fossils (Billings, 1872; Gehling et al., 2000) and forms a conspicuous component of those assemblages in South Australia (Gehling and Vickers-Rich, 2007) that were reinterpreted by Retallack (2012) as lichen-like growths within terrestrial soils. Here we analyze new specimens in 560 Ma rocks from the type area in Newfoundland that clearly reveal evidence for animal-like behavior within demonstrably shallow-marine sediments.
Discoidal impressions represent a substantial proportion of the Ediacaran fossil record (MacGabhann, 2007). Originally thought to be medusoid impressions (Glaessner, 1959), their creators are now mostly regarded as partially buried holdfasts of Ediacaran fronds (Gehling et al., 2000), although microbial colonies (Grazhdankin and Gerdes, 2007) and fungal-grade organisms (Peterson et al., 2003) have also been proposed. Given their morphological variety, several types of organism are probably represented, while some discs may not be biological at all (Cloud, 1960). The fossils described here come from the upper part of the Fermeuse Formation, St. John’s Group, within the Neoproterozoic of the Avalon Peninsula in Newfoundland (Fig. 1). Exposures are dominated by discoidal impressions, mostly Aspidella, captured by rapid burial under sand and silt from hypopycnal flows. The Fermeuse Formation consists of dark mudstones with finegrained siltstone laminae in its lower part, giving way to increasingly thick siltstone and sandstone beds alternating with mudstone at its top, forming a package ~1400 m thick (Williams and King, 1979). The Fermeuse Formation shows evidence for slumps and slides and there is evidence of storm-worked sediments. The environmental setting is interpreted as the shallow-marine slope of a prograding delta (Gehling et al., 2000; Wood et al., 2003). The Fermeuse Formation lacks dated tuffs. However, based on the age constraints provided by the Mistaken Point Formation below (dated as 565 Ma) and the correlation of the top of the Signal Hill Group above with formations in the nearby Burin Peninsula that underlie the defined Precambrian-Cambrian boundary (King, 1980; Landing, 1994), the age of the Fermeuse Formation is generally estimated as ca. 560 Ma. This is also supported by lithostratigraphic correlation with similar Ediacaran
565 ± 3 Ma (Benus, 1988) CONCEPTION GROUP
ABSTRACT The first appearance of animals in the geological record is a matter of continuing debate: how deep were the roots of the Cambrian explosion? Molecular clock estimates indicate that the deepest divergences of the Metazoa had occurred by the Ediacaran Period (635–541 Ma), yet evidence of animal activity from well below the Ediacaran-Cambrian boundary has been rare and often questionable. Meanwhile, the Ediacaran macrobiota has remained enigmatic, as emphasized by recent controversial claims that South Australia Ediacaran forms were not marine animals at all, but land-based lichens and microbial colonies. Here we report evidence for animallike behavior in a submerged setting in a key Ediacaran form, Aspidella terranovica Billings 1872, a discoidal fossil from the ca. 560 Ma Fermeuse Formation of Newfoundland (Canada). We describe sedimentary fabrics indicating progressive vertical movement of an organism through sediment in response to an aggrading sedimentwater interface. Such equilibrium traces are familiar from the Phanerozoic and are observed in partially buried marine animals such as tube anemones today. Furthermore, horizontal trails closely comparable to trails previously described from ~565 m.y. old Mistaken Point (Newfoundland) are now linked to Aspidella. Our findings constitute evidence of both vertical and horizontal movement in a key Ediacaran taxon, consistent with an animal of cnidarian grade. Moreover, because Aspidella is also reported from the Rawnsley Quartzite of South Australia, our evidence conflicts with the proposed radical interpretation of that Ediacaran fossil assemblage. We demonstrate that at least some Ediacaran forms were probably early animals, and that they lived underwater.
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Figure 1. A: Location map of fossil localities, Newfoundland. B: Stratigraphic column. Double ring indicates position of Aspidella beds of Fermeuse Formation.
doi:10.1130/G34424.1
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outcrops in England that are between 566.6 ± 2.9 Ma and 555.9 ± 3.5 Ma (Compston et al., 2002). SEDIMENTARY STRUCTURES ASSOCIATED WITH ASPIDELLA Numerous bedding-plane exposures at Ferryland, Newfoundland, are covered with discs of several distinct morphologies that Gehling et al. (2000), in a detailed study, explained as taphomorphs of Aspidella. The discs are mostly 0.3–0.5 cm in diameter, typically preserved in negative epirelief (Fig. 2A). We report here a number of short horizontal trails in association with these small discs (Figs. 2B and 2C; see Figs. DR1 and DR2 in the GSA Data Repository1). Such trails are uncommon, and the most striking examples have been observed in an exceptionally heavily colonized portion of a bed. Some trails show radiating sculpture
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Figure 2. Aspidella and associated short horizontal trails, Ferryland locality, Newfoundland. A: Large specimen of Aspidella in negative epirelief, showing characteristic ornamentation of central ridge from which finer ridges radiate. Scale bar is 0.5 cm. B: Distinct trail showing indications of characteristic Aspidella radial ornamentation in crescentic spaces between menisci. Scale bar is 3 mm. C: Short trails (arrows, bottom right) in diverging directions, obliquely pushing into sediment (arrow, top left). Scale bar is 1 cm.
characteristic of the holotype Aspidella terranovica (Fig. 2B), confirming that these traces were made by Aspidella. Their crescentic ridges and raised marginal rims are consistent with movement of Aspidella along a soft substrate. Adjacent trails vary in direction (Fig. 2C), with some pushing into the substrate, inconsistent with their formation by simple gravitational sliding or as current-driven tilting marks (Wetzel, 2013). Moreover, the restriction of trails to some individuals among otherwise static neighbors (Fig. DR1) makes movement through the action of even rapidly fluctuating currents unlikely. It is interesting that crescentic marks associated with a disc described as Bergaueria in a specimen from slightly younger Ediacaran rocks of Podolia, Ukraine (Fedonkin, 1983), may represent a similar short trail. Blocks of several centimeters thickness were sectioned in parallel cuts 1 cm apart. The polished sections reveal rounded profiles with sand or silt infill of the kind typically observed for Aspidella impressions at colonized surfaces (Gehling et al., 2000; Laflamme et al., 2011), set amid undisturbed thin sand and silt layers interbedded with shale. Importantly, polished vertical sections through slabs at two localities reveal rare, vertically stacked meniscate structures a few millimeters wide extending below rounded profiles taken to be Aspidella in cross section (Figs. 3A–3E). Where these structures arise from the base of the block they are directly above simple rounded, rimmed disc impressions of similar scale on the sole of the block (Fig. 3G; Fig. DR3). The structures tend to arise only from certain beds and terminate at the same sand layer. They are broadly vertical, although some are oblique. In thin section under the microscope, the rounded profiles topping the structures, and to a lesser extent the menisci below, are observed to have concentrations of coarser grains (primarily quartz and some feldspar) of the kind typically found associated with Aspidella, as confirmed by scanning electron microscopy and energy dispersive spectrometry elemental mapping (see Fig. DR4). Fine, dark layers rich in clay minerals extend from the surrounding matrix and beneath the menisci. These mud layers do not encase the menisci and are discontinuous in the manner of simple mud drapes. Features diagnostic of microbial mats (e.g., Noffke 2010), such as trapped grains, are not apparent here, although microbially induced framboidal pyrite grains are observed. INTERPRETATION OF SEDIMENTARY STRUCTURES In interpreting such unusual structures, abiogenic processes must first be considered. The Fermeuse structures show none of the features characteristic of water or gas escape (Cloud, 1960; Lowe, 1975; Frey et al., 2009). We find no signs of fluidized pillar structures cutting downwarping strata, as typically seen in examples of water escape. Gas escape may also be ruled out. Gas bubbles rarely leave any lasting signs of disturbance on strata, but under some conditions can produce upwarping of laminae (Frey et al., 2009), not observed here. Another possible explanation for the vertical structures invokes gravitational sediment collapse into a void. Such voids might have been created by decomposition of the body tissues of the bulb-like portion of the Aspidella-making organism. Gravitational collapse has previously been observed typically to produce a flame-like, downward-pointing profile, and increasingly shallow dips in overlying strata (Buck and Goldring, 2003). To test this further, we conducted experiments in small aquaria, in which mud and sand layers were built up over buried dissolving fluidfilled capsules. The dissolution of the capsules produced voids into which the overlying sediment layers collapsed. The resultant sedimentary fabrics show increasingly shallow dips upward through the sediment pile overlying the position of the dissolved (void producing) structure (Fig. 3F). This is contrary to observations of the Fermeuse structures, which show
1 GSA Data Repository item 2013246, supplemental images of horizontal trails and correspondence of vertical traces with surface features, SEM-EDS elemental mapping of vertical trace, and schematic diagram showing mode of formation of equilibrium traces, is available online at www.geosociety.org/pubs/ft2013.htm, or on request from
[email protected] or Documents Secretary, GSA, P.O. Box 9140, Boulder, CO 80301, USA.
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Figure 3. Vertical structures associated with Aspidella, with experimental structure for comparison. A–E: Examples of structures in sectioned slabs from two localities in Ferryland, Newfoundland, here interpreted as equilibrium traces (horizontal line in E is crack in sectioned rock). Scale bars are 2 mm. F: Experimentally produced structure resulting from gravitational collapse of sand and mud layers into artificially induced void. Scale bar is 1 cm. G: Positive rimmed impressions on sole of sectioned slab, Ferryland, associated with vertical structures as shown in A–E. Scale bar is 5 mm.
broadly parallel inwardly dipping laminae, often slightly thickened with coarser grains, and usually culminating in a rounded form with coarse sediment infill. Such vertically stacked meniscate structures are unlikely to have formed by gravitational collapse above a decayed Aspidella body. We therefore interpret the observed structures as resulting from vertical movement, and propose that they are equilibrium traces created by marine organisms that were partially buried in normal life position. Such traces arise from intermittent vertical movement, and are characterized by recurring meniscus-shaped sedimentary structures of approximately equal width, produced as the animal moves up to maintain its position at the sediment-water interface, in response to new pulses of sediment (see Fig. DR5). The resultant menisci then simply represent consecutive resting positions of the partially buried organism, although they do not always correlate with layers of bedding; extra menisci may be produced. Unlike traces produced
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by rapid escape of a buried form through sediment, equilibration involves only small vertical adjustments, with gaps in time in between, so bedding layers are usually unbroken, and there may be mud drapes (and biofilms may form) between the menisci (for Phanerozoic examples of equilibrium traces, see Buck and Goldring, 2003; Bromley, 1990). All these features are observed here. The association of our traces with simple round, rimmed impressions on bed soles (Fig. 3G) rather than with ornamented high-relief Aspidella specimens may be explained if the round structure represents the lower surface expression of a trace fossil, while the type Aspidella replicates a taphonomically-influenced body impression. The concentration of coarse grains at the top of the traces, representing the final resting position of the organism, but also found to some extent in menisci below, and frequently observed to extend a short distance on either side, is difficult to explain by sand ingestion during life, as proposed by Laflamme et al. (2011). The vertical alignment is especially conspicuous at levels having few individuals, and observed in more than 10 examples, so that coincidental stacking of separate individuals seems very unlikely. We propose that Aspidella may have been loosely coated with grains, shed on moving upward (perhaps in addition to sand incorporation). External adhesion of a layer of size-selected sediment grains is commonly observed in some actinians today (Hyman, 1940). DISCUSSION While giant deep-sea protists are known to agglutinate and have been observed to move horizontally (Matz et al., 2008), they have never been observed to create crescentic horizontal trails (Liu et al., 2010). The appearance of the characteristic ornamentation of Aspidella on crescentic trails is also inconsistent with impressions of giant protists. The same caution applies to trails made by slug-aggregating phases of slime molds (Bengtson et al., 2007; Retallack, 2012). It is even more significant that no large protist has ever been observed to adjust its vertical height in this way. Although a living infaunal xenophyophoran protist is known, it is associated with regular, horizontal, Paleodictyon-like hexagonal tests (Levin, 1994). In contrast, equilibrium traces typically result from life at, or with continuous access to, the sediment-water interface. Equilibration therefore implies complex behavior, involving life at the boundary layer, and the ability to respond rapidly to mild environmental stress induced by sedimentation. Furthermore, since sponges cannot move vertically through sediment, such behavior indicates a eumetazoan trace-maker, able to propel itself through small pulses of fine sediment by muscular contraction. Unlike modern burrowing cerianthids (tube anemones), however, there is no evidence of a lined burrow. The simplest explanation is that Aspidella was a burrowing or facultatively vagile epifaunal animal of cnidarian grade. The vertical traces observed have all been associated with discs of just a few millimeters diameter. Such movement may have been limited to juveniles. Moreover, these observations by no means imply that all Ediacaran discoidal forms were metazoan. It is probable that several types of organism are represented among discs. Nevertheless, the trails and traces are clearly associated with Aspidella terranovica as originally described by Billings (1872). These findings force us to consider Aspidella, a key Ediacaran taxon, as a eumetazoan displaying characteristically animal behavior (contra Retallack, 2012). If so, these represent the earliest vertical animal traces described so far and demonstrate that such behavior existed ~20 m.y. before the Ediacaran-Cambrian boundary. Furthermore, they add to the evidence for a marine environment for characteristic Ediacaran taxa, contrary to recent claims (Retallack, 2012). ACKNOWLEDGMENTS We thank Owen Green and Norman Charnley for technical assistance and Alex Liu and Jack Matthews for help in the field. McIlroy acknowledges the support of the NSERC and a Canada Research Chair.
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