The Ediacaran macrobiota is a polyphyletic assemblage of organisms (Darroch et al., 2018) which appear in the fossil record ∼575 million years ago and contain some of the oldest animals in the fossil record (Xiao and Laflamme 2009; Budd and Jensen 2017; Bobrovskiy et al., 2018; Dunn et al., 2018, 2021; Hoyal Cuthill and Han 2018; Wood et al., 2019). The morphologies of Ediacaran organisms from Newfoundland and the United Kingdom have few clear points of homology with living animal lineages or Phanerozoic fossil groups, which has historically limited our understanding of their phylogenetic affinities and hampers our understanding of the functional ecology of these organisms (Laflamme et al., 2013; Liu et al., 2015).

The Ediacaran communities of Eastern Newfoundland are dominated by the perhaps most distinct members of the Ediacaran macrobiota—the sessile, frondose rangeomorphs (Narbonne and Gehling 2003; Narbonne 2005). Rangeomorphs are characterised by a “fractal” branching architecture (Narbonne 2004; Hoyal Cuthill and Conway Morris 2014), and which increasing data supports as a clade of stem-group eumetazoans (Hoyal Cuthill and Han 2018; Dunn et al., 2021). Rangeomorphs numerically dominate these late-Ediacaran sea floors, but they lived alongside a number of different groups, the most abundant of which are the arboreomorphs (Clapham et al., 2003; Xiao and Laflamme 2009). These are similarly frondose, but unlike the rangeomorphs which can possess many orders of hierarchical branching, Newfoundland arboreomorphs possess only two orders (Laflamme et al., 2004; Laflamme and Narbonne 2008; Laflamme et al., 2018). Non-frondose fossils are also present, though rare in these fossil deposits–the most well-known is Thectardis, a conical to triangular organism which has been interpreted as a sponge (Clapham et al., 2004; Sperling et al., 2011).

Of these groups, rangeomorphs are not only the most diverse but display the greatest anatomical variation (Shen et al., 2008; Xiao and Laflamme 2009). Some rangeomorphs are preserved as single fronds (e.g., Charnia), but others were bushy (e.g., Bradgatia), spindle-shaped (e.g., Fractofusus) or arborescent (e.g., Primocandelabrum) (Gehling and Narbonne 2007; Bamforth et al., 2008; Flude and Narbonne 2008; Bamforth and Narbonne 2009; Dunn et al., 2019). Rangeomorph branches differentiated directly from one another or from a central stalk (Dunn et al., 2019) and some rangeomorphs additionally exhibited a naked stem that elevated the frond into the water column (Laflamme et al., 2012). Most rangeomorphs possessed a spheroidal-discoidal holdfast that anchored them within the sediment (Laflamme et al., 2004; Burzynski and Narbonne 2015), attaching the organism to the substrate and from which the stem or frond derived. Previous functional studies have demonstrated that the high surface area of the repeatedly branched frond maximised nutrient or gas exchange (Laflamme et al., 2009; Sperling et al., 2011; Liu et al., 2015). The phylogenetic relationship between frondose rangeomorphs and the coeval arboreomorphs is currently unclear (Dececchi et al., 2017; Hoyal Cuthill and Han 2018); some have argued that arboreomorphs are members of the Rangeomorpha (Brasier and Antcliffe 2009), but clear anatomical differences between at least some arboreomorphs and rangeomorphs mean that this view is not universally held, with others suggesting that overtly similar gross morphologies may have arisen through convergence (Laflamme et al., 2018). Indeed, in the modern, a sessile, frondose bodyplan is found in myriad different groups, such as ferns, cnidarians and bryozoans and has been acquired through different developmental processes, demonstrating that such a bodyplan can be the product of similar ecologies or function and is not necessarily indicative of close phylogenetic relationship.

Stems were originally thought to facilitate height-driven tiering in Avalonian communities, allowing taller fronds to reach higher-velocity conditions (Clapham and Narbonne, 2002; Ghisalberti et al., 2014), but more recent work has suggested that not all communities were tiered and that increased height may have additionally functioned in offspring dispersal (Mitchell and Kenchington 2018). Thickening of the stem close to the holdfast—optimisation of the stem as a cantilever beam—is observed in cnidarians (Koehl 1977a, b), and crinoids (Baumiller and Ausich 1996), where it permits orientation of the crown with the aboral surface facing the flow, initiating aboral inflow and recirculation (Dynowski et al., 2016). Rangeomorphs have been documented as showing a basal thickening of the stem and so may have functioned in the same way (Kenchington and Wilby 2017). By examining the different functional ecology of stemmed and non-stemmed organisms, we can investigate what the advantages of stems were in Ediacaran organisms.

These fossils are found preserved within turbiditic sequences, under thin layers of ash which blanketed large swathes of sea floor and smothered thousands of macro-organisms in a single event bed (Wood et al., 2003). Communities are exceptionally preserved and provide a near-census record of the benthos (Wood et al., 2003). This in-situ preservation, combined with the sessile habit of the organisms, means that detailed spatial ecological analyses can be used to investigate reproductive strategies (Mitchell et al., 2015), taxonomy (Mitchell et al., 2018), community interactions (Mitchell and Butterfield 2018) and evolutionary drivers (Mitchell et al., 2019, 2020), and in this study supplement functional ecology analyses of the organisms.

Here, we use statistical analyses of the orientations of 8 taxa from the E surface, Mistaken Point, Newfoundland: Beothukis, Bradgatia, Charniodiscus procerus, Charniodiscus spinosus, Plumeropriscum, Primocandelabrum, Thectardis, and Fractofusus. We determine the extent to which orientation distributions of populations of complete specimens, stems and fronds are randomly, normally and/or uniformly distributed, and how many sub-groups within each population exist. Where taxa exhibit multi-modal orientation distributions, we use random labelling spatial analyses to determine whether there are any spatial patterns to taxa orientations. These analyses enable us to investigate how morphological features, such as stems and number of folia influenced the stability of these organisms in the ancient oceans and their ability to withstand burial events of differing magnitudes.

For all taxa we found statistically significant non-random distributions using the Rao’s Spacing Test of Uniformity and the improved Hermans-Rasson—(all p < 0.01, Table 1). The majority of taxa exhibited a non-von Mises (i.e., non-normal) distributions as per the Watson’s test (Table 1). One Bradgatia cohort (p < 0.05), and the Primocandelabrum stems (p < 0.01), and fronds (p < 0.05) exhibited von Mises distributions (Table 1). The von Mises distributions for Primocandelabrum enabled model fitting to the orientation distributions of Primocandelabrum, which were found to exhibit bi-modal distributions (Supplementary Figure S2).

Analyses of the number of cohorts within each morphogroup orientation distribution varied between 1 and 5 (Table 2; Figure 4). For C. procerus and Plumeropriscum, the stems and fronds exhibited uni-modal distributions, with similar mean orientations of 195° and 192° for C. procerus stems and fronds and 178° and 177° for Plumeropriscum (Table 2; Figure 4). The majority (96.77%) of C. spinosus stems and fronds exhibited a unimodal distribution (190° and 183° respectively), with a single outlier orientated at 326° for stem and 328° for frond (Table 2; Figure 4, Supplementary Figure S3). Similarly, Primocandelabrum specimens exhibit a unimodal distribution for their fronds (95.74%, 187°) and with a minor bimodal component for the stems (89.36%, 183°; 6.38%, 237°), with two singleton outliers, and frond at 14° and the second with its stem at 119° and frond at 98° (Table 2; Figure 4, Supplementary Figure S3). Thectardis and Bradgatia exhibited bi-modal distributions, with different distributions indicated by the mean orientations being notably different between the two groups, in contrast to Primocandelabrum and C. spinosus (Table 2; Figure 4). The majority of Bradgatia specimens (57.69%) formed a cohort with the mean orientation of 15°, with the remainder (42.31%) within the cohort at 188° (Table 2; Figure 4). The majority of Thectardis specimens (74.07%) formed a cohort with the mean orientation of 199°, with the remainder (25.93%) within the cohort at 17° (Table 2; Figure 4). The distribution of sampled Beothukis specimens formed 5 distinct cohorts (Table 2), with one specimen notably different at 95° to the other four cohorts, which had similar mean orientations with the unimodal taxa orientations. The small number of specimens within the Beothukis distributions indicates that the relatively high number of cohorts could be an artefact of small sample sizes. Fractofusus exhibited a multi-modal distribution, with four cohorts at 11°, 72°, 126° and 167° within a 180° distribution (Table 2; Figure 4).

Inspection of the distributions in Figure 4 shows that while the number of statistically significant cohorts within each taxon varies, the stemmed taxa (C. spinosus, C. procerus, Plumeropriscum and Primocandelabrum) and Beothukis were all orientated in similar directions, while Bradgatia and Thectardis had a significant proportion of specimens with an antipodal orientation (Table 2; Figure 4). While the mean orientations of the multiple Beothukis cohorts were all tightly clustered, showing clear directionality in a single direction, the Fractofusus mean orientations were evenly distributed across the range, with no such directionality (Figure 4).

Analyses of the bimodally distributed taxa found no significant differences mean frond length for Bradgatia (p = 0.1850), or cone length for Thectardis (p = 0. 4547) between cohorts. Bradgatia was the only taxon that exhibited significant bidirectionality in numbers sufficient for RLA (Figure 5A). The Quotient test RLA, which describes the relative density dependence of different factors within a spatial population found that there was no density dependence between the two Bradgatia orientation groups (p _d = 0.8040, Figure 5B). The Difference test RLA, which tests for the difference between the spatial distributions of the two orientation groups, were not significantly different (p _d = 0.4104, Figure 3C), although the observed difference was close to the outside the simulation envelope which could indicate a larger spatial scale pattern not captured within out data.

The orientation distributions of fossil specimens are well established as a mechanism to indicate palaeocurrent directions (Toots 1965; Jones and Dennison 1970; Ichaso et al., 2007). The orientation distribution of a given taxon depends on its mode of life, with erect benthic organisms exhibiting strong directionality, in contrast to non-erect organisms which have limited directionality (Toots 1965; Jones and Dennison 1970; Smith 1980; Demko 1995). These explanations of orientation distributions have been used to understand the mode-of-life of Ediacaran taxa, with qualitative examination of Fractofusus specimens showing even orientation distribution suggestive of a reclining mode of life (Gehling and Narbonne 2007). In contrast, Ediacaran fronds such as Charniodiscus and Charnia have been interpreted as erect organisms, due to the morphological similarities to extant benthos such as sea pens (Seilacher 1992; Laflamme and Narbonne 2008; Laflamme et al., 2012) and—crucially—the orientation of these fronds are noted to have a strongly preferred orientation, suggested to be aligned to the contour-parallel current which felled them (Wood et al., 2003; Narbonne 2005; Ichaso et al., 2007; Laflamme et al., 2012). Strongly orientated organisms have been interpreted as erect because an organism attached to the seafloor at a single point will have the majority of its body pulled by the current, orientating it with its long axis parallel to this current (Hofmann et al., 2008). In contrast, if an organism is reclining on the substrate, it will not be subject to such currents, so will not display strong orientations (Gehling and Narbonne 2007; Bamforth and Narbonne 2009; Mitchell et al., 2015).

The relationship between fossil orientation and mode-of-life is pertinent because there has recently been revived debate surrounding the nature of the life habit of the Ediacaran rangeomorphs (e.g., McIlroy et al., 2020). Where fronds have historically been interpreted as displaying a mixture of upright and recumbent lifestyles (Ford 1958; Laflamme and Narbonne 2004; Laflamme and Narbonne 2008; Wilby et al., 2011), recent work has posited that recumbent lifestyles are more likely for some rangeomorph fronds. Orientation analyses allows us to test between these two different life habits in a statistically robust way. This study reflects the most statistically rigorous attempt to quantitatively test the orientation distributions of multiple E surface taxa, and quantify differences in orientations between the stems and fronds of these taxa. We find significant differences in felling behaviour between the stemless Bradgatia (sensu Flude and Narbonne 2008) and Thectardis (in broad agreement with Clapham et al., 2004), Fractofusus (Gehling and Narbonne 2007), and all other taxa (Beothukis, the arboreomorphs, Primocandelabrum, and Plumeropriscum), which show unidirectional felling all oriented towards the south. Fractofusus shows no notable directionality in any direction, whereas orientation distributions of Bradgatia and Thectardis both exhibit evidence of bidirectional felling. We found no significant height/sized-based correlations with orientation or outliers. Our results confirm the qualitative results of previous authors (Wood et al., 2003; Narbonne et al., 2005; Gehling and Narbonne 2007; Laflamme et al., 2012) whereby frondose taxa such as Beothukis, Charniodiscus and Primocandelabrum were erect in the water-column, anchored to the sea-floor, while Fractofusus lived close to the substrate in a reclined habit. Our results do not support recent suggestions that the fronds like Beothukis reclined on the sediment in life (McIlroy et al., 2020). The orientation distributions we find for Bradgatia and Thectardis are also consistent with an upright mode of life (Clapham et al., 2004; Flude and Narbonne 2008) and felling in a (bidirectional) current. All of our results and interpretations are based on the behaviour of the majority of specimens within a taxon, and confirm the utility of populations of specimens rather than outliers to infer the ecology for the entire population of a given taxon (e.g., Benhadi-Marín 2018). Describing population distributions enables intra-specific variability to be captured, and thus enables comparison between populations. Indeed, it is not possible to compare the orientations of two specimens in a statistically rigorous and robust way without accounting for intra-specific variability, i.e., without quantifying the population behaviour. There are, notably, multiple cohorts within the orientation distributions of Beothukis. However, while C. procerus, for example, exhibits different mean orientation directionality to Beothukis, the 95% confidence interval (as given by two sigma) places all bar one specimen of Beothukis (the holotype, oriented at 95°) within the C. procerus confidence interval—and indeed, within the 95% confidence intervals of all other southerly-oriented taxa. Thus, the Beothukis and C. procerus populations do not have significantly different orientations. It is possible of course that the Beothukis holotype belongs to a different species than the remainder of the population assigned by us to that taxon based on branching characters (McIlroy et al., 2020). However, recent work on the taxonomy of Beothukis, which demonstrates that the holotype is well within all other specimens with comparable morphology, and which were assigned by those authors to that taxon (Hawco et al., 2020) renders this unlikely. Indeed, an outlier of Primocandelabrum—whose morphology, and the orientations of the rest of the population, are entirely at odds with a reclined mode of life—is also oriented at 95°. Our orientation analyses of the Beothukis population demonstrates how the holotype orientation is an outlier and not representative of the population. Our results thus confirm an erect lifestyle for Beothukis (Wood et al., 2003; Laflamme and Narbonne 2008; Laflamme et al., 2012), contra McIlroy et al., 2020.

Charniodiscus procerus specimens—the taxon with the proportionally longest stem of any studied here (Laflamme et al., 2004)—are all oriented south, in a single cohort, with 1 outlier individual oriented antipodally (Supplementary Figure S3). All bar one specimen of Beothukis is oriented south, although notably with greater variance than the stemmed arboreomorphs (Figure 4). All Plumeropriscum specimens are oriented south, along with the majority of Primocandelabrum (Figure 4). Two Primocandelabrum specimens are oriented in a different orientation, away from the main direction (Figure 4, Supplementary Figure S3). In contrast, Bradgatia specimens are divided almost equally between north and south felling directions (Figure 4). These data would suggest that there is a correlation between proportional stem length and felling direction, and for the multifoliate taxa, there seems to be a strong correlation between presence of a stem and felling direction. Thectardis—with its narrow base and wide top—like Bradgatia, also shows a significant portion felled in the northern direction (Figure 4).

Together, our data suggest that those taxa with bases that are proportionally narrow compared to the widths of their tops (Thectardis and Bradgatia) show significantly different felling behaviours to those taxa that are more elongate and equal in shape, and that those taxa with the longest and thickest stems show the most consistent felling direction. Beothukis, for example, appears to show a sympodial central axis (Brasier et al., 2012; Hawco et al., 2020), and has the widest spread of any of the unifoliate and dominantly south-felled taxa. Equally, although Primocandelabrum has a sturdy stem, it has a proportionally wide top, and two specimens that are felled at a different angle from the main population. Charniodiscus spinosus has a much shorter stem than C. procerus, and also has a few specimens that are felled antipodally. The top-heavy morphology of Primocandelabrum, Bradgatia and Thectardis would presumably induce greater drag compared to the more stream-lined unifoliate fronds, making them more susceptible to felling—and also potentially to adhesion to the matground—though the sturdy stems of Primocandelabrum helping to redress this susceptibility in all bar a few individual cases.

Random labelling analyses suggest that these differences are not an artifact of different flow regimes in different areas, indicating that differences in orientations between stemmed and stemless organisms may reflect genuine differences in the effect of flow on stemmed and stemless taxa. Fronds and stems behave differently in flow: at a flow velocity of 0 ms⁻¹, both the frond and the stem will be fully upright, with no deflection, but as the flow velocity increases the tubular cross-section of the stem maximises the second moment of area, thus reducing the extent of bending under stress, and so this tubular morphology would serve to reduce the probability of failure via buckling (Wegst and Ashby 2007). Indeed, the high and positive epirelief of Charniodiscus procerus stems (Figure 2A) may indicate further biomechanical adaptation to flow conditions via wall thickening or changes in tissue rheology. Perhaps, because of this morphology the stem impeded felling of stemmed taxa within the enhanced velocities of the turbulent head of a turbidity flow, according with studies concerning the mechanical properties of stems, for example crinoids and aquatic plants (Baumiller and Ausich 1996; Ming-Chao and Chang-Feng 1996; Luhar and Nepf 2011).

Our interpretations are further supported by differential resolution of preservation between taxa. We observe the finest resolution of rangeomorph element preservation within Bradgatia (Figure 2B) and Beothukis (Figure 2A,C), whereas the primary branching units of Primocandelabrum and Plumeropriscum are rarely well-defined (Figure 2F,G). Though this may reflect a taphonomic signature, common membership within Rangeomorpha suggests similar modes of element construction, and instead we favour an interpretation comparable to that of Laflamme et al. (2004), wherein increasing volumes of sediment between the mat and the organism reduce preservation. This corroborates our model of comparatively rapid felling of the stemless Bradgatia and Beothukis (Thectardis does not possess rangeomorph branching, and thus cannot be considered here), whereas the stemmed Primocandelabrum and Plumeropriscum remained upright while small quantities of sediment were deposited out of the flow and onto the mat, precluding fine-scale preservation of the frondlets. Indeed, most Charniodiscus procerus specimens exhibit poorly-preserved fronds, consistent with our model—though note that arboreomorph tissue properties may differ from those of rangeomorphs, and thus may limit intercomparability.

These data support a two-phase model of felling (Figure 6), corresponding to the different flow regimes within a gravity flow. We infer that during the turbulent head of the flow, most fronds were buffeted by Kelvin-Helmholtz vortices. However, some easily-felled taxa (Bradgatia and Thectardis) were felled by this turbulence, producing a bimodal distribution of felling orientations (Figures 4, 6). The transition to laminar flow within the body of the turbidity flow led to the felling of most remaining fronds, in a unimodal distribution (Figures 4, 6). In Charnwood Forest, we know that at least some fronds were capable of surviving small-scale disturbance events (Wilby et al., 2015). Wilby et al. focussed on the bimodal population structures of the unifoliate rangeomorph Charnia, but documented other, stemmed taxa that were also preserved with a bimodal population structure (Primocandelabrum, Hylaecullulus and Charniodiscus). Together with our data, this suggests that stemmed and elongate taxa showed greater survivability in high velocity flow. Height in the water column has previously been demonstrated to increase propagule dispersal, and doesn’t appear to provide refuge from resource competition (Mitchell and Kenchington 2018). Our work suggests that stems may have had an additional function—lending greater resilience to felling in turbulent and high velocity flow regimes. These insights hint at potential environmental influences on the morphological composition of Ediacaran organisms.

We provide robust quantitative analyses of the orientation of populations of specimens from the Mistaken Point E surface. Our data support traditional palaeobiological models for the life habits of different organisms which lived in this community, with the majority of frondose organisms living upright in the water column while the spindle-shaped Fractofusus lived flat on the seafloor. Previous authors have suggested that current type and flow rate may impact community composition, but we demonstrate for the first time how the presence or absence of anatomical features impact survivability in different flow regimes. Specifically, we find that the presence of a stem (and potentially its proportional length) lends greater resilience to turbulent currents. Future work may find that such traits affect the presence and abundance of different morphologies under different environmental conditions, and potentially even the structuring of communities as they experience changing flow conditions.