Ecological Expansion and Extinction in the Late Ediacaran: Weighing the Evidence for Environmental and Biotic Drivers

Ecological Expansion and Extinction in the Late Ediacaran: Weighing the Evidence for... Abstract The Ediacara Biota, Earth’s earliest communities of complex, macroscopic, multicellular organisms, appeared during the late Ediacaran Period, just prior to the Cambrian Explosion. Ediacara fossil assemblages consist of exceptionally preserved soft-bodied forms of enigmatic morphology and affinity which nonetheless represent a critical stepping-stone in the evolution of complex animal ecosystems. The Ediacara Biota has historically been divided into three successive Assemblages—the Avalon, the White Sea, and the Nama. Although the oldest (Avalon) Assemblage documents the initial appearance of several groups of Ediacara taxa, the two younger (White Sea and Nama) Assemblages record a particularly striking suite of ecological innovations, including the appearance of diverse Ediacara body plans—in tandem with the rise of bilaterian animals—as well as the emergence of novel ecological strategies such as movement, sexual reproduction, biomineralization, and the development of dense, heterogeneous benthic communities. Many of these ecological innovations appear to be linked to adaptations to heterogeneous substrates and shallow and energetic marine settings. In spite of these innovations, the majority of Ediacara taxa disappear by the end of the Ediacaran, with interpretations for this disappearance historically ranging from the closing of preservational windows to environmentally or biotically mediated extinction. However, in spite of the unresolved affinity and eventual extinction of individual Ediacara taxa, these distinctive ecological strategies persist across the Ediacaran–Cambrian boundary and are characteristic of younger animal-dominated communities of the Phanerozoic. The late Ediacaran emergence of these strategies may, therefore, have facilitated subsequent radiations of the Cambrian. In this light, the Ediacaran and Cambrian Periods, although traditionally envisioned as separate worlds, are likely to have been part of an ecological and evolutionary continuum. Introduction Fossil assemblages of the Ediacara Biota—Earth’s earliest record of ecosystems dominated by macroscopic, multicellular, complex organisms—provide us with a critical window into the radiation of complex life. Ediacara Biota assemblages occur worldwide in middle–upper Ediacaran (571–541 Ma) strata (Laflamme et al. 2013; Pu et al. 2016); over 40 fossil localities have been documented to date. The unfamiliar morphologies of Ediacara taxa—compounded by the unusual “Ediacara-style” preservation of many of these soft-bodied organisms as sandstone casts and molds (Gehling 1999)—have historically invited a wide range of speculation as to their phylogenetic affinity. Interpretations have ranged as broadly as stem- or crown-group animals (e.g., Glaessner 1984; Gehling 1999) to giant protists (Zhuravlev 1993), fungi (Peterson et al. 2003), lichens (Retallack 1994), or an extinct kingdom of “vendobionts” (Seilacher 1992). Ediacara Lagerstätten nonetheless provide an unparalleled record of the paleoecology of complex seafloor communities, and the paleoenvironmental conditions which fostered their diversification, roughly 35 million years prior to the Cambrian Explosion. Individual Ediacara Biota fossil assemblages have traditionally been divided, on the basis of taxonomic composition and age, into three distinct Assemblages: the Avalon, White Sea, and Nama Assemblages (Waggoner 2003; Narbonne 2005). The occurrence and relative abundance of particular Ediacara fossil taxa (and thus the apparent diversity of fossil assemblages) are likely strongly shaped by environmental and preservational factors (e.g., Gehling 1999; Grazhdankin 2004, 2014; Droser et al. 2006; Gehling and Droser 2013). Yet, in spite of taxonomic and chronostratigraphic revisions and expansion of fossil localities, the three Assemblages have remained statistically valid taxonomic groupings (Boag et al. 2016). The enduring taxonomic fidelity of the three Assemblages is complemented by morphological, paleoecological, and paleoenvironmental disparity—particularly between the older Avalon Assemblage and the younger White Sea and Nama Assemblages (Droser and Gehling 2015; Droser et al. 2017b)—which suggests that, despite the limited number of overall occurrences, the Assemblages may indeed represent distinct evolutionary groupings. Recent work has concurrently expanded the conceptual definition of the Ediacara Biota. Although the majority of Ediacara fossil assemblages are preserved in the distinctive “Ediacara style” as sandstone casts and molds (Tarhan et al. 2016 and references therein), they also occur in a variety of other taphonomic modes, including preservation in carbonate or as carbonaceous compressions or replicated by pyrite (e.g., Steiner and Reitner 2001; Dzik 2003; Grazhdankin et al. 2008; Zhu et al. 2008; Xiao et al. 2013; Chen et al. 2014; Bykova et al. 2017). Significantly, none of these taphonomic modes is confined to the Ediacaran Period; all persisted across the Ediacaran–Cambrian boundary and characterize a number of Phanerozoic Lagerstätten and, in fact, a number of them pre-date the Ediacara Biota (e.g., Butterfield 2003; Tarhan et al. 2016). Detailed taphonomic analyses have led to the breakdown of historical divisions between “classic” Ediacara Biota assemblages and other upper Ediacaran fossil assemblages, such as those preserved in the Doushantuo and Dengying Formations of South China—which, recent work has indicated, include Ediacara Biota taxa (Zhu et al. 2008; Xiao et al. 2013; Chen et al. 2014). Similarly, although upper Ediacaran tubular fossil Lagerstätten such as the Gaojiashan Biota of South China have long been considered distinct from Ediacara Biota fossil assemblages, the co-occurrence of “classic” Ediacara Biota taxa and “tubular” fossil taxa in a burgeoning number of Ediacaran fossil deposits of White Sea and Nama age (e.g., Droser and Gehling 2008; Sappenfield et al. 2011; Joel et al. 2014; Smith et al. 2017) has accelerated the breakdown of this dichotomy. Conversely, many Ediacaran-aged fossil assemblages do not contain Ediacara Biota taxa (cf. Cai et al. 2010; Yuan et al. 2011; Smith et al. 2016). In sum, taphonomic, paleodiversity, and paleoecological data clearly indicate that the Ediacara Biota should not be conflated with either the Ediacaran Period or Ediacara-style preservation. The Ediacara Biota is, like all biotas, a distinct category grounded in the co-occurrence and paleoecological association of Ediacara taxa, which may, in turn, include organisms of a wide range of affinities. That the Ediacara Biota is a polyphyletic grouping does not undermine its status as a paleo-community (contra MacGabhann 2014); polyphyletic communities are common in both the Phanerozoic fossil record (e.g., the Early Cretaceous Jehol Biota; cf. Pan et al. 2013) and modern seafloor settings. Despite many unresolved aspects of the Ediacara Biota, we propose that there is robust evidence for a “second-wave” radiation (cf. Droser and Gehling 2015; Droser et al. 2017b) that witnessed the emergence and widespread implementation of novel, animal-style ecologies—such as mobility, sexual reproduction, biomineralization, and the development of dense, heterogeneous communities—as recorded by the White Sea and Nama Assemblages. In support of this framework, we also present several examples drawn from the particularly well-characterized second-wave Ediacara Member fossil assemblages of the Nilpena National Heritage site in South Australia, at which >15 years of sequential excavation and reconstruction of fossiliferous bedding planes have uniquely facilitated collection of a large set of detailed paleoecological, sedimentary, and taphonomic data from in situ fossil assemblages. On the basis of data from the Ediacara Member and other second-wave assemblages, we argue that this transition was at least in part linked to dynamic environmental conditions associated with shallow marine settings and complex and diverse organic substrates. We propose that these second-wave communities were part of an ecological and evolutionary continuum with Phanerozoic ecosystems and may comprise a distinct Evolutionary Fauna (EF) (cf. Sepkoski 1981). Finally, we evaluate the robustness of the available evidence in support of a taphonomic, biotic, or environmental driver for potential intra-Ediacaran declines in taxonomic diversity and the end-Ediacaran disappearance of the Ediacara Biota. The “second wave” of the Ediacara Biota Expansion and adaptation to shallow marine environments and organically bound substrates In contrast to the older Avalon Assemblage, which appears to have been largely confined to deeper-water, continental slope settings, the majority of Ediacara fossil deposits of the White Sea and Nama Assemblages occur in facies recording shallow marine environments (Boag et al. 2016; Droser et al. 2017a). Moreover, the taxonomic composition of Ediacara fossil assemblages appears to be strongly correlated to sedimentary facies (Grazhdankin 2004; Gehling and Droser 2013), suggesting that many Ediacara organisms varied strongly in their environmental preferences (Droser et al. 2017b). A key component of these late Ediacaran shallow marine environments appears to have been organic “matgrounds.” The presence of these matgrounds is recorded by textured organic surfaces (TOS)—iterative organosedimentary textures which record interactions between mechanical sedimentary processes and the organically bound substrate. Unlike microbially induced sedimentary structures (MISS; cf. Noffke 2009), TOS include macroscopic and morphologically differentiated features and occur in direct association with Ediacara macrofossil assemblages (Gehling and Droser 2009; Tarhan et al. 2015b, 2017). These features indicate that Ediacara matgrounds were not solely consortia of single-celled organisms, but also included densely packed multicellular eukaryotic organisms. TOS are commonly accompanied by additional sedimentological features indicative of organic seafloor stabilization in high-energy sedimentary regimes characterized by rapid deposition and recurrent seafloor disturbance (Pflüger and Gresse 1996; Grazhdankin 2004; Bouougri and Porada 2007; Tarhan et al. 2017). A number of Ediacara macroorganisms appear to have been particularly adapted to organically-bound substrates. For instance, the recurrent association between Aspidella holdfasts and TOS composed of aggregated Funisia tubular organisms in the Ediacara Member suggests that holdfast-bearing frondose taxa may have preferentially colonized well-developed, thick Funisia matgrounds (Tarhan et al. 2015b). Similar associations are observed between matground textures and tubular fossils such as Cloudina and Gaojiashania (e.g., Cortijo et al. 2010; Cai et al. 2014; Wood and Curtis 2015), as well as between the Ediacara macrofossil Kimberella and Kimberichnus—fan-shaped arrays of radiating lineations interpreted as traces formed by mollusk-like rasping of organic biofilms (Seilacher 1999; Grazhdankin 2004; Gehling et al. 2014). Upper Ediacaran shallow marine deposits worldwide further contain meandering, delicately leveed trace fossils characterized by intra-trace variability in relief (cf. Helminthoidichnites) interpreted to reflect infaunal mining of matground–sediment interfaces (Gehling 1999; Seilacher 1999; Jensen et al. 2006; Carbone and Narbonne 2014; Tarhan et al. 2017). The ubiquity, complexity, and heterogeneity of TOS and of the macrofaunal–substrate interactions that they record distinguish the upper Ediacaran record from either the preceding or subsequent record of microbially mediated sedimentary structures (contra Davies et al. 2016). Matground development may have been pivotal to not only substrate stabilization, but also colonization of the Ediacaran sandy seafloor, and may have enhanced survivorship in these high-energy, dynamic shallow marine environments (Droser et al. 2017a). Moreover, the taxonomically richest (cf. Darroch et al. 2015) and most ecologically complex Ediacara fossil assemblages—those of the Ediacara Member of Australia and the White Sea succession of Russia—are intimately associated with evidence for diverse matgrounds and matground-mediated macrofaunal ecologies. The heterogeneity and patchiness characteristic of matgrounds in second-wave Ediacara communities (cf. Droser et al. 2017b) may, in this light, have fostered the biological and ecological diversification of these assemblages. Sedimentological, morphological, and taphonomic evidence indicates that Ediacara communities lived in highly dynamic seafloor environments, and episodically experienced high-energy disturbance. For instance, matground rip-ups and holdfast pull-out structures are common along the bases of sandstone event beds of the Ediacara Member (Tarhan et al. 2010, 2014); tool-gauged surfaces devoid of well-developed matground textures in otherwise matground-rich facies (Tarhan et al. 2015a) suggest that current-mediated perturbation was periodically responsible for matground removal. Morphological distortion of Ediacara macrofossils such as Dickinsonia is also indicative of current perturbation (Evans et al. 2015; Droser et al. 2017a). Moreover, the size distribution and relative abundance of Dickinsonia and other mobile taxa in White Sea-type deposits indicate that mobile individuals may have experienced preferential survivorship in high-energy, episodically disturbed settings and were commonly among the first to colonize newly deposited sediments and immature matgrounds (Zakrevskaya 2014; Evans et al. 2015; Droser et al. 2017a, 2017b; Tarhan et al. 2017). The emergence of complex ecological strategies Second-wave fossil assemblages record the emergence of new and complex ecological strategies involving unprecedented interaction with surrounding environmental conditions (Fig. 1). These ecologies appear to have been directly linked to the development of these communities in dynamic shallow marine environments, as well as to the organically-bound substrates on and in which Ediacara macroorganisms lived. Fig. 1 View largeDownload slide Ecological strategies associated with the emergence of Ediacaran and Phanerozoic Evolutionary Faunas. White denotes absence of fossil evidence for an ecology; light gray that it was likely present but rare (e.g., the narrow distribution of deep-burrowing ichnotaxa [e.g., Skolithos and Diplocraterion in littoral sandstones] during the Cambrian); dark gray that it was environmentally or ecologically widespread. Av, Avalon; Ed, Ediacara; Ca, Cambrian; Pz, Paleozoic; Md, modern. Data from taxonomic and paleoecological compilations of Bambach (1983), Bottjer and Ausich (1986), Harper (2006), Bush et al. (2016), and Droser et al. (2017b). Fig. 1 View largeDownload slide Ecological strategies associated with the emergence of Ediacaran and Phanerozoic Evolutionary Faunas. White denotes absence of fossil evidence for an ecology; light gray that it was likely present but rare (e.g., the narrow distribution of deep-burrowing ichnotaxa [e.g., Skolithos and Diplocraterion in littoral sandstones] during the Cambrian); dark gray that it was environmentally or ecologically widespread. Av, Avalon; Ed, Ediacara; Ca, Cambrian; Pz, Paleozoic; Md, modern. Data from taxonomic and paleoecological compilations of Bambach (1983), Bottjer and Ausich (1986), Harper (2006), Bush et al. (2016), and Droser et al. (2017b). Fossiliferous successions hosting White Sea and Nama Assemblage communities record the appearance of novel sessile and motile life modes. For instance, the unidirectional alignment of Ediacara Member Parvancorina assemblages suggests that Parvancorina may have practiced rheotaxis (Paterson et al. 2017), whereas computational fluid dynamic modeling has suggested that Tribrachidium—a common taxon in White Sea-type deposits (Hall et al. 2015)—may have been a passive suspension feeder (Rahman et al. 2015). The presence of well-developed and diverse organic substrates likely facilitated seafloor colonization by epimat taxa, while episodically high fluid velocities in these dynamic, storm-reworked settings permitted Parvancorina and Tribrachidium to practice ecologies requiring high fluid flow. Matgrounds are also directly linked to the emergence of an ecological strategy critical to a variety of Ediacara life modes, as well as to subsequent Phanerozoic ecosystems—the ability of organisms to move. The association, in White Sea-type deposits, of the Ediacara macrofossil Kimberella with Kimberichnus rasping traces (Gehling et al. 2014) indicates not only that Kimberella grazed upon the organically-bound substrate, but also that it was capable of movement. The common occurrence of Helminthoidichnites-type leveed trace fossils in second-wave and coeval upper Ediacaran shallow marine successions records not only the widespread implementation of a matground-specialized ecological strategy but also, significantly, the presence in late Ediacaran ecosystems of bilaterian, coelomic animals capable of systematically excavating and displacing coarse-grained sandy sediments—both at the sediment–water interface and at shallow depths in the sediment pile (Droser et al. 2006; Jensen et al. 2006). Although the majority of Ediacaran organisms were fully soft-bodied, the rare exceptions to this rule constitute the earliest known instances of macroorganism biomineralization. Coronacollina, an Ediacara Member taxon which occurs in direct association with well-developed TOS, consists of a truncated cone attached to long, radiating, and rigid (likely biomineralized) spicules (Clites et al. 2012). Several of the tubular fossil taxa associated with Nama Assemblage-type deposits also appear to have been lightly or even fully skeletonized—foremost the conical and stacked-funnel fossil Cloudina (e.g., Grant 1990; Hua et al. 2005; Cortijo et al. 2010, 2015; Warren et al. 2011; Cai et al. 2014; Wood and Curtis 2015); the corrugated and variably triradial, pentaradial, and hexaradial fossil Sinotubulites (Cai et al. 2015); and perhaps even the annulated fossil Gaojiashania (Cai et al. 2013). These instances of macroorganism biomineralization appear for the first time in second-wave, shallow-marine assemblages, and in some cases are associated with microbial bioherms or textural evidence for microbial matgrounds (e.g., Cortijo et al. 2010; Wood 2011; Cai et al. 2013, 2014). Other biomineralized taxa, such as Namacalathus and Namapoikia, also appear during this interval, associated with organically-bound substrates and microbialites in shallow marine environments (e.g., Wood and Curtis 2015). This latest Ediacaran radiation of biomineralizing taxa has several potential explanations, including predation (e.g., Bengtson and Zhao 1992); increased oxygen, nutrient, and dissolved calcium availability (e.g., Wood and Erwin 2018); or increasing substrate competition (Tarhan et al. 2015b; Wood and Curtis 2015; Droser et al. 2017a). Second-wave Ediacara fossil deposits are characterized by locally dense aggregations of macrofossils and TOS. This is observed foremost in the White Sea Assemblage (Droser and Gehling 2015; Tarhan et al. 2015b; Droser et al. 2017a, 2017b) and, to a lesser extent, the Nama Assemblage (Darroch et al. 2016), as well as Nama Group reefs of skeletonizing macroorganisms (Wood and Curtis 2015). In the Ediacara Member, dense fossil assemblages are characterized by remarkable spatial heterogeneity in taxonomic composition, paleoecology, substrate character, and sedimentology on both fine (meter) and coarse (dekameter to kilometer) scales, as well as by variable (including high) evenness values and high alpha and beta diversity (Droser et al. 2006, 2017b; Gehling and Droser 2013; Droser and Gehling 2015; Finnegan et al. 2017). Seafloor ecological heterogeneity may have been fostered by the emergence of complex reproductive strategies (Droser and Gehling 2008; Hall et al. 2015). For instance, the tubular fossil Funisia commonly occurs in dense aggregations of similarly sized individuals, as well as clusters of similarly sized attachment structures (Droser and Gehling 2008). These characteristics, as well as a serially tapering morphology, suggest that Funisia may have alternately reproduced asexually, via terminal addition, and sexually, via production and localized dispersal of spat cohorts, resulting in densely packed communities (Droser and Gehling 2008). The presence of organic seafloor-stabilizing biofilms and mats in energetic, shallow marine settings may have provided a particularly favorable substrate for localized larval dispersal and settlement (cf. Hadfield 2011; Hadfield et al. 2014), as well as fostering the development of novel ecological strategies. The disappearance of the Ediacara Biota The presence of these ecologies in early Phanerozoic ecosystems, coupled with growing recognition that many Ediacara taxa were likely stem- or even crown-group metazoans (cf. Xiao and Laflamme 2009), suggests that many lineages present in the Ediacaran must have persisted across the Ediacaran–Cambrian boundary. However, with rare exception (e.g., Jensen et al. 1998; Hagadorn et al. 2000), Ediacara Biota macrofossils are absent from lower Cambrian and younger strata. The relatively abrupt disappearance of the Ediacara Biota at the end of the Ediacaran has long been a subject of debate (e.g., Laflamme et al. 2013) and has contributed to characterization of the Ediacara Biota as a “failed evolutionary experiment” distinct from Phanerozoic organisms (e.g., Seilacher 1992). Discussion of the disappearance of the Ediacara Biota abounds, and arguments commonly exceed the resolution of the fossil record, entering the realm of speculation. Below we discuss the three chief models for the disappearance of the Ediacara Biota, with particular consideration of (1) the extent to which the Ediacara fossil record currently permits (or does not permit) these models to be considered scientifically testable hypotheses and (2) the available data supporting or contradicting these models. Model 1: Taphonomic Bias Multiple workers have suggested that the paucity of Ediacara Biota macrofossils in Cambrian and younger successions may reflect coeval deterioration of the taphonomic conditions responsible for the Ediacara fossil record, rather than an end-Ediacaran extinction event. This model (also termed the “Cheshire Cat” model by Laflamme et al. [2013]) suggests that the fossil record of these soft-bodied macroorganisms may, like all Konservat Lagerstätten, be biased by the availability of preservational windows reliant on temporally discontinuous environmental conditions. However, a recent literature survey (Tarhan et al. 2016) indicates that Ediacara-style preservation—the fossilization of soft-bodied organisms as sandstone casts and molds, which is the most common taphonomic mode in Ediacara Biota fossil assemblages—persists across the Ediacaran–Cambrian boundary. In fact, 10 of the 45 documented Ediacara-style fossil assemblages (a record which spans the Mesoproterozoic though the Devonian) occur in lower Paleozoic successions and consist largely of non-Ediacara-type taxa (Tarhan et al. 2016). Paleontological, petrographic, and geochemical data from the Ediacara Member indicate that Ediacara-style fossilization was facilitated by the early diagenetic precipitation of silica cements linked to high marine silica concentrations prior to the radiation of silica-biomineralizing taxa (Tarhan et al. 2016). Association between Ediacara-style fossils and other authigenic phases has been reported in other Ediacaran deposits (e.g., Liu 2016). High dissolved silica concentrations may, in fact, have also mediated authigenic precipitation of clays or pyrite or co-precipitation of these phases with siliceous phases in some upper Ediacaran as well as lower Paleozoic fossil assemblages, thereby facilitating additional pathways for Ediacara-style preservation. That the preservational window for Ediacara-style fossilization clearly did not close at the end of the Ediacaran, but in fact remained open for over a hundred million additional years suggests that the disappearance of Ediacara Biota fossils cannot be attributed to taphonomic bias. Ediacara-type macrofossils and other upper Ediacaran fossils (e.g., tubular fossils) are also preserved in other taphonomic styles, for instance as carbonaceous compressions, carbonate molds, and replaced by pyrite or phosphate (e.g., Xiao et al. 1998, 2013; Steiner and Reitner 2001; Dzik 2003; Grazhdankin et al. 2008; Zhu et al. 2008; Schiffbauer et al. 2014; Chen et al. 2014; Bykova et al. 2017). All of these preservational modes, like Ediacara-style preservation, are well-known from Phanerozoic Lagerstätten (and some—particularly preservation as carbonaceous compressions—also characterize pre-Ediacaran fossil assemblages) (cf. Butterfield 2003). Therefore, it is exceedingly unlikely that the lack of Ediacara-type taxa in Cambrian and younger successions is a taphonomic artifact—presumably this stratigraphic disappearance reflects a real evolutionary phenomenon. Model 2: Ecologically engineered extinction—“biotic replacement” If the Ediacara Biota really did disappear at the end of the Precambrian, it has been suggested that extinctions of Ediacara taxa were directly mediated by increasing competition with and predation by the bilaterian animals that replaced them (e.g., Laflamme et al. 2013; Darroch et al. 2015; Muscente et al. 2018). Proponents of this model have suggested that not only was the end-Ediacaran disappearance of Ediacara taxa a consequence of “biotic replacement” by crown-group metazoans, but that the apparent drop in species richness between the highly diverse White Sea Assemblage and the relatively taxonomically depauperate Nama Assemblage likewise reflects the deleterious impact of metazoan engineering (Darroch et al. 2015). Although the rarefaction curve for Nama Assemblage taxonomic richness at Swartpunt has not yet saturated, the Nama Assemblage appears to be markedly less diverse than the two key and roughly coeval White Sea Assemblage deposits of Nilpena (Ediacara Member) and Solza (Verkhovka Formation) (Darroch et al. 2015, fig. 2). Building from this view, various workers have suggested that the presence of trace fossils and tubular fossils in uppermost Ediacaran strata reflects an increased crown-group metazoan (and bilaterian) presence that was detrimental to Ediacara Biota taxa (Laflamme et al. 2013; Darroch et al. 2015; Muscente et al. 2018). However, an obvious question is, given the very limited number of sites from which detailed taxonomic relative abundance data have been systematically collected and rarefaction analyses performed, whether it is possible to accurately resolve shifts in diversity from only three units (e.g., two older, relatively high-diversity units and one younger, low-diversity unit), particularly in light of the striking spatial and environmental differences in diversity characteristic of modern marine ecosystems (e.g., Jablonski et al. 2006). Fig. 2 View largeDownload slide Simulation of the likelihood of reproducing observed shifts in Ediacara fossil diversity as recorded by individual localities of the White Sea and Nama Assemblages, assuming a null hypothesis that the diversity of Ediacara fossil localities is normally distributed, with no inter-Assemblage shifts in mean or distribution. (A) Schematic of test where X1 is set at “high” diversity and X2 and X3 are randomly chosen and compared to X1, where a is a range defining similarity to X1 and b defines difference between X3 and both X1 and X2. (B) The three cases that we highlight here. (C) The distribution of 1000 randomly chosen samples from our normally distributed dataset (n = 100,000). Rows reflect changes in the initial definition of X1; columns test the effects of varying a and b. Percentage values denote the percentage of simulations meeting each case. Fig. 2 View largeDownload slide Simulation of the likelihood of reproducing observed shifts in Ediacara fossil diversity as recorded by individual localities of the White Sea and Nama Assemblages, assuming a null hypothesis that the diversity of Ediacara fossil localities is normally distributed, with no inter-Assemblage shifts in mean or distribution. (A) Schematic of test where X1 is set at “high” diversity and X2 and X3 are randomly chosen and compared to X1, where a is a range defining similarity to X1 and b defines difference between X3 and both X1 and X2. (B) The three cases that we highlight here. (C) The distribution of 1000 randomly chosen samples from our normally distributed dataset (n = 100,000). Rows reflect changes in the initial definition of X1; columns test the effects of varying a and b. Percentage values denote the percentage of simulations meeting each case. Here, using an idealized global-scale Ediacara Biota diversity distribution, we explore the likelihood that, relative to two higher-diversity fossil localities of the White Sea Assemblage, the lower-diversity fossil assemblage at Swartpunt robustly records a drop in Ediacara diversity (represented in this exercise as X1, X2, and X3, respectively; Fig. 2). We considered a normally distributed dataset of 100,000 data points, each representing the taxonomic richness of a hypothetical Ediacara fossil locality. We assigned X1 a relatively high level of taxonomic richness, ranging from the 70th to 90th percentile of our data (Fig. 2C). We defined an interval of “similarity” (a, in Fig. 2A) around X1, within which X2 or X3 would be considered of similar diversity to X1. We additionally defined an interval of “difference” (b, in Fig. 2A), defining a P-value cutoff from X1 and X2 that X3 must fall below in order to be considered substantially lower in diversity (“Case 3” in Fig. 2A, B). Using this theoretical framework, we randomly choose X2 and X3 1000 times in order to visualize the distribution of potential cases, and consider the probability of recreating shifts in taxonomic diversity inferred from the fossil record (Fig. 2). Foremost, we observe that the likelihood of similarity between X1 and X2 is the factor primarily limiting the ultimate probability of randomly selecting a different and low value for X3. This observation, although straightforward, bears important implications for interpretation of the fossil record, and suggests that instances of recurrent similarity or a sustained signal may be more unique than variation. Critically, the probability of satisfying requirements for both X2 and X3 to match interpretations of the fossil record is relatively low (9.5–18.9%). This indicates that, under a null hypothesis of no inter-Assemblage shift in global taxonomic diversity, the likelihood of randomly sampling a “low-diversity” assemblage after sampling two relatively “high-diversity” assemblages is low—which may indicate that inferred decreases in diversity between the White Sea and Nama Assemblages are, in fact, robust. However, detailed facies characterization and collection of relative abundance data from additional Nama-type assemblages characterized by similar lithofacies and taphofacies to key White Sea-type assemblages will be critical to verify prior predictions (e.g., Boag et al., 2016) that this apparent diversity drop is not an environmental artifact, nor due to preservational or sampling biases. Further, if the taxonomic diversity of Ediacara Biota communities was actually characterized by a right-skewed distribution, the probability of randomly sampling a “low-diversity” assemblage (without any associated change in global diversity) may actually be much higher. Therefore, moving forward, it will be critical to establish whether the relatively large number of Ediacara assemblages of any age characterized by low diversity (e.g., Farmer et al. 1992) are characterized by lithofacies and taphofacies comparable to those of classic White Sea-type assemblages. However, assuming that future sampling and detailed paleoenvironmental study will verify that this trend reflects a drop in global diversity, a number of issues remain concerning linking potential diversity shifts to the putative “successors” of the Ediacara Biota on the basis of the fossil record. Darroch et al. (2016), for instance, suggested that association of the tubular fossil Shaanxilithes—inferred by the authors to be a metazoan—with discoidal fossils (cf. Aspidella) in the Schwarzrand Subgroup (Nama Group) of Namibia records direct and deleterious ecological interactions between Ediacara Biota macroorganisms and eumetazoans, driving decreases in Ediacara taxonomic diversity (Darroch et al. 2015, 2016). Schiffbauer et al. (2016) also characterized upper Ediacaran tubular fossils as “vermiform” and suggested that these organisms were directly responsible for the displacement of Ediacara-type macroorganisms. However, there is currently no compelling morphological or ecological evidence that tubular macrofossils are, in fact, truly “vermiform” (a term nearly universally considered to denote bilaterian metazoans; e.g., Ma et al. 2010) in affinity. Due to their relatively simple body plans and, in several cases, evidence of budding and light biomineralization (e.g., Hua et al. 2005; Droser and Gehling 2008; Cortijo et al. 2010, 2015), tubular fossils are commonly considered poriferan- or cnidarian-grade metazoans (or stem-group metazoans). Further, they do not appear to possess triploblastic tissues or other bilaterian synapomorphies such as anterior differentiation or bilateral symmetry (McMahon et al. 2017). Lack of features obviously suggestive of adaptations for efficient photosynthesis (e.g., branching, maximized surface area to volume ratios) has, historically, precluded consideration of tubular taxa as macroalgae. However, many modern algal species—e.g., the green alga Neomeris annulata—are characterized by unbranching, annulated tubular body plans (e.g., Littler and Littler 2000). Particularly in light of uncertainty regarding the timing of the appearance(s) of biomineralization in algae (e.g., Knoll 2003), an algal affinity for some upper Ediacaran tubular fossils should not be discounted. Therefore, to invoke the presence of tubular fossils, on the presumption of vermiform affinity, as evidence for ecological competition and biotic replacement is currently unwarranted. Proponents of the biotic replacement model have also pointed to higher trace fossil diversity (relative to preceding intervals) in uppermost Ediacaran strata as evidence of increased ecosystem engineering by infaunal bilaterian animals—foremost, infaunal predation upon the largely epifaunal and stationary Ediacara macroorganisms and disruption of the organically-bound substrate on which Ediacara macroorganisms lived (e.g., Laflamme et al. 2013; Darroch et al. 2015, 2016; Schiffbauer et al. 2016; Muscente et al. 2018). However, these trace fossils are small (largely sub-mm- to mm-scale diameters) and either horizontal or very shallowly penetrative (sub-mm- to mm-scale depths) (Jensen et al. 2000; Jensen and Runnegar 2005; Bouougri and Porada 2007; Macdonald et al. 2014; Meyer et al. 2014; Darroch et al. 2016; Parry et al. 2017). Uppermost Ediacaran trace fossils are, relative to lower Cambrian assemblages, low in diversity (e.g., Jensen et al. 2006) and exceedingly rare, commonly reported from only a single individual, bedding plane, or locality (Jensen et al. 2000; Jensen and Runnegar 2005; Bouougri and Porada 2007; Macdonald et al. 2014; Meyer et al. 2014; Darroch et al. 2016; Parry et al. 2017; Buatois et al. 2018). Although some of these forms are undoubtedly complex relative to older trace fossil occurrences, they do not record deep, intensive, or pervasive forms of sediment disturbance. On the whole, their small size, rarity, low diversity, and confinement to the shallowest region of the sediment pile suggest that the “engineering” effect of late Ediacaran burrowing would have been minimal (contra Darroch et al. 2015, 2016; Muscente et al. 2018). There is also no evidence for direct interaction between Nama Assemblage macroorganisms and infauna. In fact, the rare trace fossils which have been reported from the uppermost Ediacaran occur in strata (and commonly successions) devoid of Ediacara macrofossils (e.g., Darroch et al. 2016). Moreover, recent work in upper Ediacaran successions of Namibia and the western USA indicates that the stratigraphic ranges of Nama Assemblage-type Ediacara macrofossils, tubular fossils, and trace fossils overlap for at least the final 6 million years of the Ediacaran, without apparent decrease in Ediacara diversity during that interval (Smith et al. 2017). Additionally, tubular fossils and trace fossils occur abundantly and in direct spatial association with (within millimeters–decimeters of) Ediacara macrofossils in White Sea Assemblage deposits (e.g., Droser and Gehling 2008, 2015; Tarhan et al. 2015b, 2017). In the Ediacara Member, tubular fossils occur in all facies containing autochthonous Ediacara macrofossils, and are commonly intimately associated with them, as in the Aspidella–Funisia biofacies, in which >50 Aspidella and >1000 Funisia individuals may occur in a single square meter (Droser and Gehling 2008; Tarhan et al. 2015b; Droser et al. 2017a, 2017b). The Ediacara Member also contains a range of other tubular taxa (in direct spatial association with Ediacara macrofossils), comparable in diversity to tubular fossil assemblages in uppermost Ediacaran strata (Sappenfield et al. 2011; Joel et al. 2014; Droser et al. 2017a). Trace fossils in the Ediacara Member also occur in immediate proximity to Ediacara macrofossils (contra Darroch et al. 2016). Dickinsoniomorph “footprints” and Kimberichnus rasping traces are common in the Ediacara Member—the most richly fossiliferous assemblage of the Ediacara Biota (Droser et al. 2006; Droser and Gehling 2015; Droser et al. 2017a, 2017b; Tarhan et al. 2017)—and also co-occur with Ediacara macrofossils in the White Sea succession (e.g., Grazhdankin 2004). Helminthoidichnites-type burrows are abundant in the Ediacara Member and relatively common in other upper Ediacaran strata, including other strata containing White Sea-type Ediacara fossil assemblages, such as the Blueflower Formation of northwestern Canada (e.g., Carbone and Narbonne 2014). The common and direct co-occurrence of tubular fossils and trace fossils with Ediacara macrofossils of the highly diverse and ecologically complex White Sea Assemblage suggests that, rather than facilitating the decline of the Ediacara Biota, tubular macroorganisms and bilaterian infauna were common components of these ecosystems. In sum, although biotic replacement should not be discounted as a potential driver of declines in Ediacara taxonomic diversity, a paucity of direct evidence from the fossil record currently limits the testability of this model. Future discoveries, however, may bring greater light to bear on the question of whether interaction with crown-group metazoans was responsible for the disappearance of Ediacara taxa. Model 3: Environmentally mediated extinction A third possibility for the absence of Ediacara Biota macrofossils from Phanerozoic successions is extinction resulting from environmental perturbation (e.g., Amthor et al. 2003; Smith et al. 2016, 2017; and discussed at length in Laflamme et al. 2013; Schiffbauer et al. 2016; Muscente et al. 2018). Ediacara macrofossils appear to be absent from Cambrian lithofacies similar to those in which they are preserved in upper Ediacaran strata (Smith et al. 2017). This suggests that, in spite of the strong facies control upon the presence and taxonomic composition of Ediacara fossil assemblages (e.g., Grazhdankin 2004; Gehling and Droser 2013; Smith et al. 2017), the disappearance of the Ediacara Biota is not an artifact linked to changes in sedimentary environment. However, a longstanding corollary to all three models for the disappearance of the Ediacara Biota is that declines in the prevalence of microbial matgrounds—presumably mediated by increased epifaunal grazing and infaunal sediment churning by mobile bilaterians—may have been detrimental to the persistence (and fossilization potential) of Ediacara communities (e.g., Gehling 1999; Droser et al. 2006; Laflamme et al. 2013; Buatois et al. 2014; Darroch et al. 2016; Schiffbauer et al. 2016; Muscente et al. 2018). In contrast to the longstanding belief that MISS frequency decreases in post-Ediacaran strata, Davies et al. (2016) have recently argued that, at the level of stratigraphic units, the temporal distribution of MISS is geologically invariant. Additionally, various workers have suggested, on the basis of co-occurrence between MISS and trace fossil assemblages in certain lower Cambrian units, that matgrounds may have persisted, at least locally, in early Cambrian seafloor settings, due to the protracted development of infaunal sediment mixing (e.g., Hagadorn and Bottjer 1997; Bailey et al. 2006; Marenco and Bottjer 2008; Buatois et al. 2014). However, the unit-level MISS-tabulation approach of Davies et al. (2016) does not capture the heterogeneity, complexity, and relative ubiquity characteristic of upper Ediacaran TOS and TOS–macrofaunal associations in second-wave Ediacara fossil assemblages (Droser et al. 2017b). With rare exception—for instance, the middle Cambrian–Furongian Elk Mound Group, which contains a diverse range of organosedimentary features (Bottjer and Hagadorn 2007)—lower Paleozoic successions do not contain true TOS. Given the strong association, particularly in White Sea-type Ediacara assemblages, between TOS and Ediacara macrofossils characterized by matground-adapted life modes and ecological strategies, the disappearance of complex and heterogeneous organic substrates (particularly those comprised of densely aggregated multicellular organisms) may have been detrimental to the persistence of Ediacara communities. The paucity of TOS in post-Ediacaran successions may be linked to an environmentally mediated extinction of key TOS-forming organisms (such as the tubular fossil Funisia) which may, in turn, have compounded bottom-up or top-down drivers of extinction of Ediacara macrofossils. Biogeochemical perturbation may have also played a role in the disappearance of Ediacara taxa. It has long been recognized that the Ediacaran and Cambrian oceans experienced pronounced carbon cycle and redox perturbation. Recent work has suggested that turnover within the Ediacara Biota and its eventual disappearance at the end of the Ediacaran may be linked to environmental volatility and resulting ecosystem destabilization (e.g., Schröder and Grotzinger 2007; Verdel et al. 2011; Smith et al. 2016; Bowyer et al. 2017; Muscente et al. 2018). Others have suggested, in contrast, that redox perturbation may have spurred late Ediacaran and early Cambrian diversification and ecosystem restructuring (e.g., Johnston et al. 2012; Cui et al. 2016; Reinhard et al. 2016; Wood and Erwin 2018). Muscente et al. (2018) recently revisited the question of the Shuram negative carbon isotope excursion and its potential relationship to the evolutionary record of the Ediacara Biota. Muscente et al. (2018) suggested that, if the Shuram records deoxygenation and subsequent recovery in the wake of a major oxidation event, this environmental perturbation may have driven the transition between the Avalon and White Sea Assemblages, as well as that between the White Sea and Nama Assemblages. However, interpretation of the Shuram anomaly has long been hampered by mass-balance inconsistencies. If the Shuram does indeed reflect oxidation of a large pool of dissolved organic carbon (DOC), this would require an extremely large standing DOC reservoir (30 times as large as the modern dissolved inorganic carbon (DIC) pool; cf. Shields 2017). However, built-in negative feedbacks in the long-term carbon cycle should have prohibited such a DOC buildup (Laakso and Schrag 2014; Droser et al. 2017b). Moreover, DOC is efficiently removed from the modern ocean through hydrothermal–crustal interactions and hydrothermal particle scavenging (e.g., Elderfield and Schultz 1996; Lang et al. 2006; Hansell et al. 2009; Bennett et al. 2011; Catalá et al. 2015; German et al. 2015). Given that ocean water masses cycle through hydrothermal systems on time scales of thousands of years, it is improbable that the Ediacaran oceans could have sustained buildup of a DOC reservoir on the million-year time scales necessary to explain carbon isotope excursions such as the Shuram (Droser et al. 2017b). Similarly, the source of a sufficiently large oxidant reservoir to sustain the Shuram excursion (and achieve the markedly negative DIC δ13C values of its nadir), as well as direct evidence for an oxidation trigger, have long proved elusive (e.g., Grotzinger et al. 2011). Interpretation of the Shuram and its relationship to Ediacara fossil assemblages has also been hindered by limited geochronological constraints, and a paucity of sections containing both Ediacara macrofossils and the Shuram (e.g., Xiao et al. 2016). However, in South China, Australia and the western USA, the entirety of the Shuram excursion precedes the appearance of local Ediacara fossil assemblages by hundreds of meters (e.g., Verdel et al. 2011; Xiao et al. 2016; Smith et al. 2017). Therefore, based on available constraints, there is currently no robust evidence that Shuram-associated carbon cycle perturbation drove Ediacara taxonomic turnover (contra Muscente et al. 2018). While direct evidence for environmental drivers of taxonomic turnover within the Ediacara Biota is currently lacking, it is nonetheless possible that environmental perturbations contributed to the disappearance of the Ediacara Biota at the end of the Ediacaran. The highest stratigraphic occurrences of Ediacara-type and tubular macrofossils occur below the nadir of the basal Cambrian negative carbon isotope excursion (BACE)—a potentially global marker of carbon cycle perturbation—in uppermost Ediacaran strata in northwestern Canada, the western USA, and South China (Macdonald et al. 2013; Smith et al. 2016, 2017; Xiao et al. 2016). Future detailed facies work, and collection of integrated, high-resolution biostratigraphic, chemostratigraphic, and radiometric data will be essential to establish whether these correlations are global in nature, and whether there is a robust and causative relationship between environmental perturbation and Ediacara extinction. Ediacaran EFs: an ecological and evolutionary continuum with Phanerozoic ecosystems? Although most Ediacara taxa disappeared at the end of the Ediacaran Period, the Ediacara Biota should not be considered a “failed evolutionary experiment.” Although the precise affinities of many Ediacara taxa remain poorly resolved, it is increasingly apparent that second-wave Ediacara communities contained a number of stem- and potentially crown-group metazoans and macroalgae (e.g., Xiao and Laflamme 2009; Xiao et al. 2013; Droser et al. 2017b). Moreover, Ediacara organisms pioneered ecological strategies considered characteristic of Phanerozoic and modern complex animal ecosystems—foremost, motility, heterotrophy, sexual reproduction, biomineralization, and the formation of dense and heterogeneous seafloor communities (Droser and Gehling 2015; Droser et al. 2017b; Finnegan et al. 2017). In this light, the Ediacara fossil record should be considered part of an ecological and evolutionary continuum with that of the Phanerozoic, in the manner of Sepkoski’s (1981) EFs (Fig. 1). The Phanerozoic EFs indicate that standing taxonomic diversity is a function of not only species origination and extinction, but also dynamic interplay between ecological and environmental factors (Sepkoski 1981). Critically, the inter-EF boundaries are not defined by complete replacement of the members of one EF by those of the next, but rather by the rise to ecological dominance of groups whose origins significantly predate that rise, and which also postdate its waning. Turnover between EFs appears, in the Phanerozoic, to have been mediated by severe environmental perturbation. If the extinction of the Ediacara Biota (and turnover within the Ediacara Biota) was, as for Phanerozoic EFs, mediated by environmental perturbation (Smith et al. 2017), this suggests that Ediacara and Phanerozoic ecosystems may have followed a similar evolutionary trajectory. We therefore propose that two Ediacaran EFs be added to those of Sepkoski (1981): (1) An Avalon EF, containing rangeomorph-dominated ecosystems characterized by tiered benthic communities and the appearance of complex reproductive strategies; and (2) An Ediacara EF represented by the second-wave White Sea and Nama Assemblages. The Ediacara EF records the emergence and widespread implementation of a range of novel Ediacara-type body plans, mobility, sexual reproduction, biomineralization, and reef development in highly dynamic shallow marine environments and in ecological association with heterogeneous organically bound substrates (Fig. 1). The clear presence of complex, animal-style ecologies in second-wave White Sea- and Nama-type assemblages and evidence that these communities were also populated by animals for millions of years suggests that the Ediacara Biota cannot simply be dismissed as an evolutionary anomaly “outcompeted” by animals. Summary We propose that the ecological diversification of younger, second-wave Ediacara communities recorded by the White Sea and Nama Assemblages was mediated by the expansion of Ediacara taxa into dynamic, shallow marine environments characterized by episodic disturbance and heterogeneous organically-bound substrates. This interplay of environmental and substrate factors likely directly mediated the development of complex ecological strategies characteristic of Phanerozoic animal-dominated ecosystems. In light of evidence that Ediacara communities with animal-style ecologies coexisted with and included stem- and crown-group animals for millions of years prior to the Cambrian, we propose the addition of two new Ediacaran EFs to Sepkoski’s (1981) EF paradigm. The apparent disappearance of the Ediacara Biota at the end of the Ediacaran, and potential decreases in diversity between the White Sea and the Nama Assemblages, have, like many aspects of the Ediacara fossil record, inspired much debate. However, limited (and frequently spatially disparate) data and poor age constraints have hampered robust reconstructions of Ediacara paleodiversity. Future work, focusing on detailed facies characterization, the establishment of further high-precision radiometric age constraints, and integration of biostratigraphic and chemostratigraphic records in Ediacaran fossiliferous successions worldwide will be necessary to increase the resolution and facilitate robust assessment of the upper Ediacaran fossil record. Acknowledgments We are grateful to L. Parry, N. Planavsky, and E. Saupe for critical discussion, and to Ross and Jane Fargher for access to the National Heritage Nilpena Ediacara fossil site on their property, acknowledging that this land lies within the Adnyamathanha Traditional Lands. We thank R. Earley and four anonymous reviewers for critical comments that improved this manuscript. Funding This research was supported by the NASA Exobiology Program [grant NNX14AJ86G to M.L.D. and L.G.T.]; the Australian Research Council [grant DP0453393 to J.G.G.]; National Geographic Society [grant 9476-14 to M.L.D.]; and a National Science Foundation Earth Sciences Postdoctoral Fellowship [L.G.T.]. References Amthor JE, Grotzinger JP, Schröder S, Bowring SA, Ramezani J, Martin MW, Matter A. 2003. Extinction of Cloudina and Namacalathus at the Precambrian–Cambrian boundary in Oman. Geology  31: 431– 4. Google Scholar CrossRef Search ADS   Bailey JV, Corsetti FA, Bottjer DJ, Marenco KN. 2006. 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Ecological Expansion and Extinction in the Late Ediacaran: Weighing the Evidence for Environmental and Biotic Drivers

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Oxford University Press
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© The Author(s) 2018. Published by Oxford University Press on behalf of the Society for Integrative and Comparative Biology. All rights reserved. For permissions please email: journals.permissions@oup.com.
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Abstract

Abstract The Ediacara Biota, Earth’s earliest communities of complex, macroscopic, multicellular organisms, appeared during the late Ediacaran Period, just prior to the Cambrian Explosion. Ediacara fossil assemblages consist of exceptionally preserved soft-bodied forms of enigmatic morphology and affinity which nonetheless represent a critical stepping-stone in the evolution of complex animal ecosystems. The Ediacara Biota has historically been divided into three successive Assemblages—the Avalon, the White Sea, and the Nama. Although the oldest (Avalon) Assemblage documents the initial appearance of several groups of Ediacara taxa, the two younger (White Sea and Nama) Assemblages record a particularly striking suite of ecological innovations, including the appearance of diverse Ediacara body plans—in tandem with the rise of bilaterian animals—as well as the emergence of novel ecological strategies such as movement, sexual reproduction, biomineralization, and the development of dense, heterogeneous benthic communities. Many of these ecological innovations appear to be linked to adaptations to heterogeneous substrates and shallow and energetic marine settings. In spite of these innovations, the majority of Ediacara taxa disappear by the end of the Ediacaran, with interpretations for this disappearance historically ranging from the closing of preservational windows to environmentally or biotically mediated extinction. However, in spite of the unresolved affinity and eventual extinction of individual Ediacara taxa, these distinctive ecological strategies persist across the Ediacaran–Cambrian boundary and are characteristic of younger animal-dominated communities of the Phanerozoic. The late Ediacaran emergence of these strategies may, therefore, have facilitated subsequent radiations of the Cambrian. In this light, the Ediacaran and Cambrian Periods, although traditionally envisioned as separate worlds, are likely to have been part of an ecological and evolutionary continuum. Introduction Fossil assemblages of the Ediacara Biota—Earth’s earliest record of ecosystems dominated by macroscopic, multicellular, complex organisms—provide us with a critical window into the radiation of complex life. Ediacara Biota assemblages occur worldwide in middle–upper Ediacaran (571–541 Ma) strata (Laflamme et al. 2013; Pu et al. 2016); over 40 fossil localities have been documented to date. The unfamiliar morphologies of Ediacara taxa—compounded by the unusual “Ediacara-style” preservation of many of these soft-bodied organisms as sandstone casts and molds (Gehling 1999)—have historically invited a wide range of speculation as to their phylogenetic affinity. Interpretations have ranged as broadly as stem- or crown-group animals (e.g., Glaessner 1984; Gehling 1999) to giant protists (Zhuravlev 1993), fungi (Peterson et al. 2003), lichens (Retallack 1994), or an extinct kingdom of “vendobionts” (Seilacher 1992). Ediacara Lagerstätten nonetheless provide an unparalleled record of the paleoecology of complex seafloor communities, and the paleoenvironmental conditions which fostered their diversification, roughly 35 million years prior to the Cambrian Explosion. Individual Ediacara Biota fossil assemblages have traditionally been divided, on the basis of taxonomic composition and age, into three distinct Assemblages: the Avalon, White Sea, and Nama Assemblages (Waggoner 2003; Narbonne 2005). The occurrence and relative abundance of particular Ediacara fossil taxa (and thus the apparent diversity of fossil assemblages) are likely strongly shaped by environmental and preservational factors (e.g., Gehling 1999; Grazhdankin 2004, 2014; Droser et al. 2006; Gehling and Droser 2013). Yet, in spite of taxonomic and chronostratigraphic revisions and expansion of fossil localities, the three Assemblages have remained statistically valid taxonomic groupings (Boag et al. 2016). The enduring taxonomic fidelity of the three Assemblages is complemented by morphological, paleoecological, and paleoenvironmental disparity—particularly between the older Avalon Assemblage and the younger White Sea and Nama Assemblages (Droser and Gehling 2015; Droser et al. 2017b)—which suggests that, despite the limited number of overall occurrences, the Assemblages may indeed represent distinct evolutionary groupings. Recent work has concurrently expanded the conceptual definition of the Ediacara Biota. Although the majority of Ediacara fossil assemblages are preserved in the distinctive “Ediacara style” as sandstone casts and molds (Tarhan et al. 2016 and references therein), they also occur in a variety of other taphonomic modes, including preservation in carbonate or as carbonaceous compressions or replicated by pyrite (e.g., Steiner and Reitner 2001; Dzik 2003; Grazhdankin et al. 2008; Zhu et al. 2008; Xiao et al. 2013; Chen et al. 2014; Bykova et al. 2017). Significantly, none of these taphonomic modes is confined to the Ediacaran Period; all persisted across the Ediacaran–Cambrian boundary and characterize a number of Phanerozoic Lagerstätten and, in fact, a number of them pre-date the Ediacara Biota (e.g., Butterfield 2003; Tarhan et al. 2016). Detailed taphonomic analyses have led to the breakdown of historical divisions between “classic” Ediacara Biota assemblages and other upper Ediacaran fossil assemblages, such as those preserved in the Doushantuo and Dengying Formations of South China—which, recent work has indicated, include Ediacara Biota taxa (Zhu et al. 2008; Xiao et al. 2013; Chen et al. 2014). Similarly, although upper Ediacaran tubular fossil Lagerstätten such as the Gaojiashan Biota of South China have long been considered distinct from Ediacara Biota fossil assemblages, the co-occurrence of “classic” Ediacara Biota taxa and “tubular” fossil taxa in a burgeoning number of Ediacaran fossil deposits of White Sea and Nama age (e.g., Droser and Gehling 2008; Sappenfield et al. 2011; Joel et al. 2014; Smith et al. 2017) has accelerated the breakdown of this dichotomy. Conversely, many Ediacaran-aged fossil assemblages do not contain Ediacara Biota taxa (cf. Cai et al. 2010; Yuan et al. 2011; Smith et al. 2016). In sum, taphonomic, paleodiversity, and paleoecological data clearly indicate that the Ediacara Biota should not be conflated with either the Ediacaran Period or Ediacara-style preservation. The Ediacara Biota is, like all biotas, a distinct category grounded in the co-occurrence and paleoecological association of Ediacara taxa, which may, in turn, include organisms of a wide range of affinities. That the Ediacara Biota is a polyphyletic grouping does not undermine its status as a paleo-community (contra MacGabhann 2014); polyphyletic communities are common in both the Phanerozoic fossil record (e.g., the Early Cretaceous Jehol Biota; cf. Pan et al. 2013) and modern seafloor settings. Despite many unresolved aspects of the Ediacara Biota, we propose that there is robust evidence for a “second-wave” radiation (cf. Droser and Gehling 2015; Droser et al. 2017b) that witnessed the emergence and widespread implementation of novel, animal-style ecologies—such as mobility, sexual reproduction, biomineralization, and the development of dense, heterogeneous communities—as recorded by the White Sea and Nama Assemblages. In support of this framework, we also present several examples drawn from the particularly well-characterized second-wave Ediacara Member fossil assemblages of the Nilpena National Heritage site in South Australia, at which >15 years of sequential excavation and reconstruction of fossiliferous bedding planes have uniquely facilitated collection of a large set of detailed paleoecological, sedimentary, and taphonomic data from in situ fossil assemblages. On the basis of data from the Ediacara Member and other second-wave assemblages, we argue that this transition was at least in part linked to dynamic environmental conditions associated with shallow marine settings and complex and diverse organic substrates. We propose that these second-wave communities were part of an ecological and evolutionary continuum with Phanerozoic ecosystems and may comprise a distinct Evolutionary Fauna (EF) (cf. Sepkoski 1981). Finally, we evaluate the robustness of the available evidence in support of a taphonomic, biotic, or environmental driver for potential intra-Ediacaran declines in taxonomic diversity and the end-Ediacaran disappearance of the Ediacara Biota. The “second wave” of the Ediacara Biota Expansion and adaptation to shallow marine environments and organically bound substrates In contrast to the older Avalon Assemblage, which appears to have been largely confined to deeper-water, continental slope settings, the majority of Ediacara fossil deposits of the White Sea and Nama Assemblages occur in facies recording shallow marine environments (Boag et al. 2016; Droser et al. 2017a). Moreover, the taxonomic composition of Ediacara fossil assemblages appears to be strongly correlated to sedimentary facies (Grazhdankin 2004; Gehling and Droser 2013), suggesting that many Ediacara organisms varied strongly in their environmental preferences (Droser et al. 2017b). A key component of these late Ediacaran shallow marine environments appears to have been organic “matgrounds.” The presence of these matgrounds is recorded by textured organic surfaces (TOS)—iterative organosedimentary textures which record interactions between mechanical sedimentary processes and the organically bound substrate. Unlike microbially induced sedimentary structures (MISS; cf. Noffke 2009), TOS include macroscopic and morphologically differentiated features and occur in direct association with Ediacara macrofossil assemblages (Gehling and Droser 2009; Tarhan et al. 2015b, 2017). These features indicate that Ediacara matgrounds were not solely consortia of single-celled organisms, but also included densely packed multicellular eukaryotic organisms. TOS are commonly accompanied by additional sedimentological features indicative of organic seafloor stabilization in high-energy sedimentary regimes characterized by rapid deposition and recurrent seafloor disturbance (Pflüger and Gresse 1996; Grazhdankin 2004; Bouougri and Porada 2007; Tarhan et al. 2017). A number of Ediacara macroorganisms appear to have been particularly adapted to organically-bound substrates. For instance, the recurrent association between Aspidella holdfasts and TOS composed of aggregated Funisia tubular organisms in the Ediacara Member suggests that holdfast-bearing frondose taxa may have preferentially colonized well-developed, thick Funisia matgrounds (Tarhan et al. 2015b). Similar associations are observed between matground textures and tubular fossils such as Cloudina and Gaojiashania (e.g., Cortijo et al. 2010; Cai et al. 2014; Wood and Curtis 2015), as well as between the Ediacara macrofossil Kimberella and Kimberichnus—fan-shaped arrays of radiating lineations interpreted as traces formed by mollusk-like rasping of organic biofilms (Seilacher 1999; Grazhdankin 2004; Gehling et al. 2014). Upper Ediacaran shallow marine deposits worldwide further contain meandering, delicately leveed trace fossils characterized by intra-trace variability in relief (cf. Helminthoidichnites) interpreted to reflect infaunal mining of matground–sediment interfaces (Gehling 1999; Seilacher 1999; Jensen et al. 2006; Carbone and Narbonne 2014; Tarhan et al. 2017). The ubiquity, complexity, and heterogeneity of TOS and of the macrofaunal–substrate interactions that they record distinguish the upper Ediacaran record from either the preceding or subsequent record of microbially mediated sedimentary structures (contra Davies et al. 2016). Matground development may have been pivotal to not only substrate stabilization, but also colonization of the Ediacaran sandy seafloor, and may have enhanced survivorship in these high-energy, dynamic shallow marine environments (Droser et al. 2017a). Moreover, the taxonomically richest (cf. Darroch et al. 2015) and most ecologically complex Ediacara fossil assemblages—those of the Ediacara Member of Australia and the White Sea succession of Russia—are intimately associated with evidence for diverse matgrounds and matground-mediated macrofaunal ecologies. The heterogeneity and patchiness characteristic of matgrounds in second-wave Ediacara communities (cf. Droser et al. 2017b) may, in this light, have fostered the biological and ecological diversification of these assemblages. Sedimentological, morphological, and taphonomic evidence indicates that Ediacara communities lived in highly dynamic seafloor environments, and episodically experienced high-energy disturbance. For instance, matground rip-ups and holdfast pull-out structures are common along the bases of sandstone event beds of the Ediacara Member (Tarhan et al. 2010, 2014); tool-gauged surfaces devoid of well-developed matground textures in otherwise matground-rich facies (Tarhan et al. 2015a) suggest that current-mediated perturbation was periodically responsible for matground removal. Morphological distortion of Ediacara macrofossils such as Dickinsonia is also indicative of current perturbation (Evans et al. 2015; Droser et al. 2017a). Moreover, the size distribution and relative abundance of Dickinsonia and other mobile taxa in White Sea-type deposits indicate that mobile individuals may have experienced preferential survivorship in high-energy, episodically disturbed settings and were commonly among the first to colonize newly deposited sediments and immature matgrounds (Zakrevskaya 2014; Evans et al. 2015; Droser et al. 2017a, 2017b; Tarhan et al. 2017). The emergence of complex ecological strategies Second-wave fossil assemblages record the emergence of new and complex ecological strategies involving unprecedented interaction with surrounding environmental conditions (Fig. 1). These ecologies appear to have been directly linked to the development of these communities in dynamic shallow marine environments, as well as to the organically-bound substrates on and in which Ediacara macroorganisms lived. Fig. 1 View largeDownload slide Ecological strategies associated with the emergence of Ediacaran and Phanerozoic Evolutionary Faunas. White denotes absence of fossil evidence for an ecology; light gray that it was likely present but rare (e.g., the narrow distribution of deep-burrowing ichnotaxa [e.g., Skolithos and Diplocraterion in littoral sandstones] during the Cambrian); dark gray that it was environmentally or ecologically widespread. Av, Avalon; Ed, Ediacara; Ca, Cambrian; Pz, Paleozoic; Md, modern. Data from taxonomic and paleoecological compilations of Bambach (1983), Bottjer and Ausich (1986), Harper (2006), Bush et al. (2016), and Droser et al. (2017b). Fig. 1 View largeDownload slide Ecological strategies associated with the emergence of Ediacaran and Phanerozoic Evolutionary Faunas. White denotes absence of fossil evidence for an ecology; light gray that it was likely present but rare (e.g., the narrow distribution of deep-burrowing ichnotaxa [e.g., Skolithos and Diplocraterion in littoral sandstones] during the Cambrian); dark gray that it was environmentally or ecologically widespread. Av, Avalon; Ed, Ediacara; Ca, Cambrian; Pz, Paleozoic; Md, modern. Data from taxonomic and paleoecological compilations of Bambach (1983), Bottjer and Ausich (1986), Harper (2006), Bush et al. (2016), and Droser et al. (2017b). Fossiliferous successions hosting White Sea and Nama Assemblage communities record the appearance of novel sessile and motile life modes. For instance, the unidirectional alignment of Ediacara Member Parvancorina assemblages suggests that Parvancorina may have practiced rheotaxis (Paterson et al. 2017), whereas computational fluid dynamic modeling has suggested that Tribrachidium—a common taxon in White Sea-type deposits (Hall et al. 2015)—may have been a passive suspension feeder (Rahman et al. 2015). The presence of well-developed and diverse organic substrates likely facilitated seafloor colonization by epimat taxa, while episodically high fluid velocities in these dynamic, storm-reworked settings permitted Parvancorina and Tribrachidium to practice ecologies requiring high fluid flow. Matgrounds are also directly linked to the emergence of an ecological strategy critical to a variety of Ediacara life modes, as well as to subsequent Phanerozoic ecosystems—the ability of organisms to move. The association, in White Sea-type deposits, of the Ediacara macrofossil Kimberella with Kimberichnus rasping traces (Gehling et al. 2014) indicates not only that Kimberella grazed upon the organically-bound substrate, but also that it was capable of movement. The common occurrence of Helminthoidichnites-type leveed trace fossils in second-wave and coeval upper Ediacaran shallow marine successions records not only the widespread implementation of a matground-specialized ecological strategy but also, significantly, the presence in late Ediacaran ecosystems of bilaterian, coelomic animals capable of systematically excavating and displacing coarse-grained sandy sediments—both at the sediment–water interface and at shallow depths in the sediment pile (Droser et al. 2006; Jensen et al. 2006). Although the majority of Ediacaran organisms were fully soft-bodied, the rare exceptions to this rule constitute the earliest known instances of macroorganism biomineralization. Coronacollina, an Ediacara Member taxon which occurs in direct association with well-developed TOS, consists of a truncated cone attached to long, radiating, and rigid (likely biomineralized) spicules (Clites et al. 2012). Several of the tubular fossil taxa associated with Nama Assemblage-type deposits also appear to have been lightly or even fully skeletonized—foremost the conical and stacked-funnel fossil Cloudina (e.g., Grant 1990; Hua et al. 2005; Cortijo et al. 2010, 2015; Warren et al. 2011; Cai et al. 2014; Wood and Curtis 2015); the corrugated and variably triradial, pentaradial, and hexaradial fossil Sinotubulites (Cai et al. 2015); and perhaps even the annulated fossil Gaojiashania (Cai et al. 2013). These instances of macroorganism biomineralization appear for the first time in second-wave, shallow-marine assemblages, and in some cases are associated with microbial bioherms or textural evidence for microbial matgrounds (e.g., Cortijo et al. 2010; Wood 2011; Cai et al. 2013, 2014). Other biomineralized taxa, such as Namacalathus and Namapoikia, also appear during this interval, associated with organically-bound substrates and microbialites in shallow marine environments (e.g., Wood and Curtis 2015). This latest Ediacaran radiation of biomineralizing taxa has several potential explanations, including predation (e.g., Bengtson and Zhao 1992); increased oxygen, nutrient, and dissolved calcium availability (e.g., Wood and Erwin 2018); or increasing substrate competition (Tarhan et al. 2015b; Wood and Curtis 2015; Droser et al. 2017a). Second-wave Ediacara fossil deposits are characterized by locally dense aggregations of macrofossils and TOS. This is observed foremost in the White Sea Assemblage (Droser and Gehling 2015; Tarhan et al. 2015b; Droser et al. 2017a, 2017b) and, to a lesser extent, the Nama Assemblage (Darroch et al. 2016), as well as Nama Group reefs of skeletonizing macroorganisms (Wood and Curtis 2015). In the Ediacara Member, dense fossil assemblages are characterized by remarkable spatial heterogeneity in taxonomic composition, paleoecology, substrate character, and sedimentology on both fine (meter) and coarse (dekameter to kilometer) scales, as well as by variable (including high) evenness values and high alpha and beta diversity (Droser et al. 2006, 2017b; Gehling and Droser 2013; Droser and Gehling 2015; Finnegan et al. 2017). Seafloor ecological heterogeneity may have been fostered by the emergence of complex reproductive strategies (Droser and Gehling 2008; Hall et al. 2015). For instance, the tubular fossil Funisia commonly occurs in dense aggregations of similarly sized individuals, as well as clusters of similarly sized attachment structures (Droser and Gehling 2008). These characteristics, as well as a serially tapering morphology, suggest that Funisia may have alternately reproduced asexually, via terminal addition, and sexually, via production and localized dispersal of spat cohorts, resulting in densely packed communities (Droser and Gehling 2008). The presence of organic seafloor-stabilizing biofilms and mats in energetic, shallow marine settings may have provided a particularly favorable substrate for localized larval dispersal and settlement (cf. Hadfield 2011; Hadfield et al. 2014), as well as fostering the development of novel ecological strategies. The disappearance of the Ediacara Biota The presence of these ecologies in early Phanerozoic ecosystems, coupled with growing recognition that many Ediacara taxa were likely stem- or even crown-group metazoans (cf. Xiao and Laflamme 2009), suggests that many lineages present in the Ediacaran must have persisted across the Ediacaran–Cambrian boundary. However, with rare exception (e.g., Jensen et al. 1998; Hagadorn et al. 2000), Ediacara Biota macrofossils are absent from lower Cambrian and younger strata. The relatively abrupt disappearance of the Ediacara Biota at the end of the Ediacaran has long been a subject of debate (e.g., Laflamme et al. 2013) and has contributed to characterization of the Ediacara Biota as a “failed evolutionary experiment” distinct from Phanerozoic organisms (e.g., Seilacher 1992). Discussion of the disappearance of the Ediacara Biota abounds, and arguments commonly exceed the resolution of the fossil record, entering the realm of speculation. Below we discuss the three chief models for the disappearance of the Ediacara Biota, with particular consideration of (1) the extent to which the Ediacara fossil record currently permits (or does not permit) these models to be considered scientifically testable hypotheses and (2) the available data supporting or contradicting these models. Model 1: Taphonomic Bias Multiple workers have suggested that the paucity of Ediacara Biota macrofossils in Cambrian and younger successions may reflect coeval deterioration of the taphonomic conditions responsible for the Ediacara fossil record, rather than an end-Ediacaran extinction event. This model (also termed the “Cheshire Cat” model by Laflamme et al. [2013]) suggests that the fossil record of these soft-bodied macroorganisms may, like all Konservat Lagerstätten, be biased by the availability of preservational windows reliant on temporally discontinuous environmental conditions. However, a recent literature survey (Tarhan et al. 2016) indicates that Ediacara-style preservation—the fossilization of soft-bodied organisms as sandstone casts and molds, which is the most common taphonomic mode in Ediacara Biota fossil assemblages—persists across the Ediacaran–Cambrian boundary. In fact, 10 of the 45 documented Ediacara-style fossil assemblages (a record which spans the Mesoproterozoic though the Devonian) occur in lower Paleozoic successions and consist largely of non-Ediacara-type taxa (Tarhan et al. 2016). Paleontological, petrographic, and geochemical data from the Ediacara Member indicate that Ediacara-style fossilization was facilitated by the early diagenetic precipitation of silica cements linked to high marine silica concentrations prior to the radiation of silica-biomineralizing taxa (Tarhan et al. 2016). Association between Ediacara-style fossils and other authigenic phases has been reported in other Ediacaran deposits (e.g., Liu 2016). High dissolved silica concentrations may, in fact, have also mediated authigenic precipitation of clays or pyrite or co-precipitation of these phases with siliceous phases in some upper Ediacaran as well as lower Paleozoic fossil assemblages, thereby facilitating additional pathways for Ediacara-style preservation. That the preservational window for Ediacara-style fossilization clearly did not close at the end of the Ediacaran, but in fact remained open for over a hundred million additional years suggests that the disappearance of Ediacara Biota fossils cannot be attributed to taphonomic bias. Ediacara-type macrofossils and other upper Ediacaran fossils (e.g., tubular fossils) are also preserved in other taphonomic styles, for instance as carbonaceous compressions, carbonate molds, and replaced by pyrite or phosphate (e.g., Xiao et al. 1998, 2013; Steiner and Reitner 2001; Dzik 2003; Grazhdankin et al. 2008; Zhu et al. 2008; Schiffbauer et al. 2014; Chen et al. 2014; Bykova et al. 2017). All of these preservational modes, like Ediacara-style preservation, are well-known from Phanerozoic Lagerstätten (and some—particularly preservation as carbonaceous compressions—also characterize pre-Ediacaran fossil assemblages) (cf. Butterfield 2003). Therefore, it is exceedingly unlikely that the lack of Ediacara-type taxa in Cambrian and younger successions is a taphonomic artifact—presumably this stratigraphic disappearance reflects a real evolutionary phenomenon. Model 2: Ecologically engineered extinction—“biotic replacement” If the Ediacara Biota really did disappear at the end of the Precambrian, it has been suggested that extinctions of Ediacara taxa were directly mediated by increasing competition with and predation by the bilaterian animals that replaced them (e.g., Laflamme et al. 2013; Darroch et al. 2015; Muscente et al. 2018). Proponents of this model have suggested that not only was the end-Ediacaran disappearance of Ediacara taxa a consequence of “biotic replacement” by crown-group metazoans, but that the apparent drop in species richness between the highly diverse White Sea Assemblage and the relatively taxonomically depauperate Nama Assemblage likewise reflects the deleterious impact of metazoan engineering (Darroch et al. 2015). Although the rarefaction curve for Nama Assemblage taxonomic richness at Swartpunt has not yet saturated, the Nama Assemblage appears to be markedly less diverse than the two key and roughly coeval White Sea Assemblage deposits of Nilpena (Ediacara Member) and Solza (Verkhovka Formation) (Darroch et al. 2015, fig. 2). Building from this view, various workers have suggested that the presence of trace fossils and tubular fossils in uppermost Ediacaran strata reflects an increased crown-group metazoan (and bilaterian) presence that was detrimental to Ediacara Biota taxa (Laflamme et al. 2013; Darroch et al. 2015; Muscente et al. 2018). However, an obvious question is, given the very limited number of sites from which detailed taxonomic relative abundance data have been systematically collected and rarefaction analyses performed, whether it is possible to accurately resolve shifts in diversity from only three units (e.g., two older, relatively high-diversity units and one younger, low-diversity unit), particularly in light of the striking spatial and environmental differences in diversity characteristic of modern marine ecosystems (e.g., Jablonski et al. 2006). Fig. 2 View largeDownload slide Simulation of the likelihood of reproducing observed shifts in Ediacara fossil diversity as recorded by individual localities of the White Sea and Nama Assemblages, assuming a null hypothesis that the diversity of Ediacara fossil localities is normally distributed, with no inter-Assemblage shifts in mean or distribution. (A) Schematic of test where X1 is set at “high” diversity and X2 and X3 are randomly chosen and compared to X1, where a is a range defining similarity to X1 and b defines difference between X3 and both X1 and X2. (B) The three cases that we highlight here. (C) The distribution of 1000 randomly chosen samples from our normally distributed dataset (n = 100,000). Rows reflect changes in the initial definition of X1; columns test the effects of varying a and b. Percentage values denote the percentage of simulations meeting each case. Fig. 2 View largeDownload slide Simulation of the likelihood of reproducing observed shifts in Ediacara fossil diversity as recorded by individual localities of the White Sea and Nama Assemblages, assuming a null hypothesis that the diversity of Ediacara fossil localities is normally distributed, with no inter-Assemblage shifts in mean or distribution. (A) Schematic of test where X1 is set at “high” diversity and X2 and X3 are randomly chosen and compared to X1, where a is a range defining similarity to X1 and b defines difference between X3 and both X1 and X2. (B) The three cases that we highlight here. (C) The distribution of 1000 randomly chosen samples from our normally distributed dataset (n = 100,000). Rows reflect changes in the initial definition of X1; columns test the effects of varying a and b. Percentage values denote the percentage of simulations meeting each case. Here, using an idealized global-scale Ediacara Biota diversity distribution, we explore the likelihood that, relative to two higher-diversity fossil localities of the White Sea Assemblage, the lower-diversity fossil assemblage at Swartpunt robustly records a drop in Ediacara diversity (represented in this exercise as X1, X2, and X3, respectively; Fig. 2). We considered a normally distributed dataset of 100,000 data points, each representing the taxonomic richness of a hypothetical Ediacara fossil locality. We assigned X1 a relatively high level of taxonomic richness, ranging from the 70th to 90th percentile of our data (Fig. 2C). We defined an interval of “similarity” (a, in Fig. 2A) around X1, within which X2 or X3 would be considered of similar diversity to X1. We additionally defined an interval of “difference” (b, in Fig. 2A), defining a P-value cutoff from X1 and X2 that X3 must fall below in order to be considered substantially lower in diversity (“Case 3” in Fig. 2A, B). Using this theoretical framework, we randomly choose X2 and X3 1000 times in order to visualize the distribution of potential cases, and consider the probability of recreating shifts in taxonomic diversity inferred from the fossil record (Fig. 2). Foremost, we observe that the likelihood of similarity between X1 and X2 is the factor primarily limiting the ultimate probability of randomly selecting a different and low value for X3. This observation, although straightforward, bears important implications for interpretation of the fossil record, and suggests that instances of recurrent similarity or a sustained signal may be more unique than variation. Critically, the probability of satisfying requirements for both X2 and X3 to match interpretations of the fossil record is relatively low (9.5–18.9%). This indicates that, under a null hypothesis of no inter-Assemblage shift in global taxonomic diversity, the likelihood of randomly sampling a “low-diversity” assemblage after sampling two relatively “high-diversity” assemblages is low—which may indicate that inferred decreases in diversity between the White Sea and Nama Assemblages are, in fact, robust. However, detailed facies characterization and collection of relative abundance data from additional Nama-type assemblages characterized by similar lithofacies and taphofacies to key White Sea-type assemblages will be critical to verify prior predictions (e.g., Boag et al., 2016) that this apparent diversity drop is not an environmental artifact, nor due to preservational or sampling biases. Further, if the taxonomic diversity of Ediacara Biota communities was actually characterized by a right-skewed distribution, the probability of randomly sampling a “low-diversity” assemblage (without any associated change in global diversity) may actually be much higher. Therefore, moving forward, it will be critical to establish whether the relatively large number of Ediacara assemblages of any age characterized by low diversity (e.g., Farmer et al. 1992) are characterized by lithofacies and taphofacies comparable to those of classic White Sea-type assemblages. However, assuming that future sampling and detailed paleoenvironmental study will verify that this trend reflects a drop in global diversity, a number of issues remain concerning linking potential diversity shifts to the putative “successors” of the Ediacara Biota on the basis of the fossil record. Darroch et al. (2016), for instance, suggested that association of the tubular fossil Shaanxilithes—inferred by the authors to be a metazoan—with discoidal fossils (cf. Aspidella) in the Schwarzrand Subgroup (Nama Group) of Namibia records direct and deleterious ecological interactions between Ediacara Biota macroorganisms and eumetazoans, driving decreases in Ediacara taxonomic diversity (Darroch et al. 2015, 2016). Schiffbauer et al. (2016) also characterized upper Ediacaran tubular fossils as “vermiform” and suggested that these organisms were directly responsible for the displacement of Ediacara-type macroorganisms. However, there is currently no compelling morphological or ecological evidence that tubular macrofossils are, in fact, truly “vermiform” (a term nearly universally considered to denote bilaterian metazoans; e.g., Ma et al. 2010) in affinity. Due to their relatively simple body plans and, in several cases, evidence of budding and light biomineralization (e.g., Hua et al. 2005; Droser and Gehling 2008; Cortijo et al. 2010, 2015), tubular fossils are commonly considered poriferan- or cnidarian-grade metazoans (or stem-group metazoans). Further, they do not appear to possess triploblastic tissues or other bilaterian synapomorphies such as anterior differentiation or bilateral symmetry (McMahon et al. 2017). Lack of features obviously suggestive of adaptations for efficient photosynthesis (e.g., branching, maximized surface area to volume ratios) has, historically, precluded consideration of tubular taxa as macroalgae. However, many modern algal species—e.g., the green alga Neomeris annulata—are characterized by unbranching, annulated tubular body plans (e.g., Littler and Littler 2000). Particularly in light of uncertainty regarding the timing of the appearance(s) of biomineralization in algae (e.g., Knoll 2003), an algal affinity for some upper Ediacaran tubular fossils should not be discounted. Therefore, to invoke the presence of tubular fossils, on the presumption of vermiform affinity, as evidence for ecological competition and biotic replacement is currently unwarranted. Proponents of the biotic replacement model have also pointed to higher trace fossil diversity (relative to preceding intervals) in uppermost Ediacaran strata as evidence of increased ecosystem engineering by infaunal bilaterian animals—foremost, infaunal predation upon the largely epifaunal and stationary Ediacara macroorganisms and disruption of the organically-bound substrate on which Ediacara macroorganisms lived (e.g., Laflamme et al. 2013; Darroch et al. 2015, 2016; Schiffbauer et al. 2016; Muscente et al. 2018). However, these trace fossils are small (largely sub-mm- to mm-scale diameters) and either horizontal or very shallowly penetrative (sub-mm- to mm-scale depths) (Jensen et al. 2000; Jensen and Runnegar 2005; Bouougri and Porada 2007; Macdonald et al. 2014; Meyer et al. 2014; Darroch et al. 2016; Parry et al. 2017). Uppermost Ediacaran trace fossils are, relative to lower Cambrian assemblages, low in diversity (e.g., Jensen et al. 2006) and exceedingly rare, commonly reported from only a single individual, bedding plane, or locality (Jensen et al. 2000; Jensen and Runnegar 2005; Bouougri and Porada 2007; Macdonald et al. 2014; Meyer et al. 2014; Darroch et al. 2016; Parry et al. 2017; Buatois et al. 2018). Although some of these forms are undoubtedly complex relative to older trace fossil occurrences, they do not record deep, intensive, or pervasive forms of sediment disturbance. On the whole, their small size, rarity, low diversity, and confinement to the shallowest region of the sediment pile suggest that the “engineering” effect of late Ediacaran burrowing would have been minimal (contra Darroch et al. 2015, 2016; Muscente et al. 2018). There is also no evidence for direct interaction between Nama Assemblage macroorganisms and infauna. In fact, the rare trace fossils which have been reported from the uppermost Ediacaran occur in strata (and commonly successions) devoid of Ediacara macrofossils (e.g., Darroch et al. 2016). Moreover, recent work in upper Ediacaran successions of Namibia and the western USA indicates that the stratigraphic ranges of Nama Assemblage-type Ediacara macrofossils, tubular fossils, and trace fossils overlap for at least the final 6 million years of the Ediacaran, without apparent decrease in Ediacara diversity during that interval (Smith et al. 2017). Additionally, tubular fossils and trace fossils occur abundantly and in direct spatial association with (within millimeters–decimeters of) Ediacara macrofossils in White Sea Assemblage deposits (e.g., Droser and Gehling 2008, 2015; Tarhan et al. 2015b, 2017). In the Ediacara Member, tubular fossils occur in all facies containing autochthonous Ediacara macrofossils, and are commonly intimately associated with them, as in the Aspidella–Funisia biofacies, in which >50 Aspidella and >1000 Funisia individuals may occur in a single square meter (Droser and Gehling 2008; Tarhan et al. 2015b; Droser et al. 2017a, 2017b). The Ediacara Member also contains a range of other tubular taxa (in direct spatial association with Ediacara macrofossils), comparable in diversity to tubular fossil assemblages in uppermost Ediacaran strata (Sappenfield et al. 2011; Joel et al. 2014; Droser et al. 2017a). Trace fossils in the Ediacara Member also occur in immediate proximity to Ediacara macrofossils (contra Darroch et al. 2016). Dickinsoniomorph “footprints” and Kimberichnus rasping traces are common in the Ediacara Member—the most richly fossiliferous assemblage of the Ediacara Biota (Droser et al. 2006; Droser and Gehling 2015; Droser et al. 2017a, 2017b; Tarhan et al. 2017)—and also co-occur with Ediacara macrofossils in the White Sea succession (e.g., Grazhdankin 2004). Helminthoidichnites-type burrows are abundant in the Ediacara Member and relatively common in other upper Ediacaran strata, including other strata containing White Sea-type Ediacara fossil assemblages, such as the Blueflower Formation of northwestern Canada (e.g., Carbone and Narbonne 2014). The common and direct co-occurrence of tubular fossils and trace fossils with Ediacara macrofossils of the highly diverse and ecologically complex White Sea Assemblage suggests that, rather than facilitating the decline of the Ediacara Biota, tubular macroorganisms and bilaterian infauna were common components of these ecosystems. In sum, although biotic replacement should not be discounted as a potential driver of declines in Ediacara taxonomic diversity, a paucity of direct evidence from the fossil record currently limits the testability of this model. Future discoveries, however, may bring greater light to bear on the question of whether interaction with crown-group metazoans was responsible for the disappearance of Ediacara taxa. Model 3: Environmentally mediated extinction A third possibility for the absence of Ediacara Biota macrofossils from Phanerozoic successions is extinction resulting from environmental perturbation (e.g., Amthor et al. 2003; Smith et al. 2016, 2017; and discussed at length in Laflamme et al. 2013; Schiffbauer et al. 2016; Muscente et al. 2018). Ediacara macrofossils appear to be absent from Cambrian lithofacies similar to those in which they are preserved in upper Ediacaran strata (Smith et al. 2017). This suggests that, in spite of the strong facies control upon the presence and taxonomic composition of Ediacara fossil assemblages (e.g., Grazhdankin 2004; Gehling and Droser 2013; Smith et al. 2017), the disappearance of the Ediacara Biota is not an artifact linked to changes in sedimentary environment. However, a longstanding corollary to all three models for the disappearance of the Ediacara Biota is that declines in the prevalence of microbial matgrounds—presumably mediated by increased epifaunal grazing and infaunal sediment churning by mobile bilaterians—may have been detrimental to the persistence (and fossilization potential) of Ediacara communities (e.g., Gehling 1999; Droser et al. 2006; Laflamme et al. 2013; Buatois et al. 2014; Darroch et al. 2016; Schiffbauer et al. 2016; Muscente et al. 2018). In contrast to the longstanding belief that MISS frequency decreases in post-Ediacaran strata, Davies et al. (2016) have recently argued that, at the level of stratigraphic units, the temporal distribution of MISS is geologically invariant. Additionally, various workers have suggested, on the basis of co-occurrence between MISS and trace fossil assemblages in certain lower Cambrian units, that matgrounds may have persisted, at least locally, in early Cambrian seafloor settings, due to the protracted development of infaunal sediment mixing (e.g., Hagadorn and Bottjer 1997; Bailey et al. 2006; Marenco and Bottjer 2008; Buatois et al. 2014). However, the unit-level MISS-tabulation approach of Davies et al. (2016) does not capture the heterogeneity, complexity, and relative ubiquity characteristic of upper Ediacaran TOS and TOS–macrofaunal associations in second-wave Ediacara fossil assemblages (Droser et al. 2017b). With rare exception—for instance, the middle Cambrian–Furongian Elk Mound Group, which contains a diverse range of organosedimentary features (Bottjer and Hagadorn 2007)—lower Paleozoic successions do not contain true TOS. Given the strong association, particularly in White Sea-type Ediacara assemblages, between TOS and Ediacara macrofossils characterized by matground-adapted life modes and ecological strategies, the disappearance of complex and heterogeneous organic substrates (particularly those comprised of densely aggregated multicellular organisms) may have been detrimental to the persistence of Ediacara communities. The paucity of TOS in post-Ediacaran successions may be linked to an environmentally mediated extinction of key TOS-forming organisms (such as the tubular fossil Funisia) which may, in turn, have compounded bottom-up or top-down drivers of extinction of Ediacara macrofossils. Biogeochemical perturbation may have also played a role in the disappearance of Ediacara taxa. It has long been recognized that the Ediacaran and Cambrian oceans experienced pronounced carbon cycle and redox perturbation. Recent work has suggested that turnover within the Ediacara Biota and its eventual disappearance at the end of the Ediacaran may be linked to environmental volatility and resulting ecosystem destabilization (e.g., Schröder and Grotzinger 2007; Verdel et al. 2011; Smith et al. 2016; Bowyer et al. 2017; Muscente et al. 2018). Others have suggested, in contrast, that redox perturbation may have spurred late Ediacaran and early Cambrian diversification and ecosystem restructuring (e.g., Johnston et al. 2012; Cui et al. 2016; Reinhard et al. 2016; Wood and Erwin 2018). Muscente et al. (2018) recently revisited the question of the Shuram negative carbon isotope excursion and its potential relationship to the evolutionary record of the Ediacara Biota. Muscente et al. (2018) suggested that, if the Shuram records deoxygenation and subsequent recovery in the wake of a major oxidation event, this environmental perturbation may have driven the transition between the Avalon and White Sea Assemblages, as well as that between the White Sea and Nama Assemblages. However, interpretation of the Shuram anomaly has long been hampered by mass-balance inconsistencies. If the Shuram does indeed reflect oxidation of a large pool of dissolved organic carbon (DOC), this would require an extremely large standing DOC reservoir (30 times as large as the modern dissolved inorganic carbon (DIC) pool; cf. Shields 2017). However, built-in negative feedbacks in the long-term carbon cycle should have prohibited such a DOC buildup (Laakso and Schrag 2014; Droser et al. 2017b). Moreover, DOC is efficiently removed from the modern ocean through hydrothermal–crustal interactions and hydrothermal particle scavenging (e.g., Elderfield and Schultz 1996; Lang et al. 2006; Hansell et al. 2009; Bennett et al. 2011; Catalá et al. 2015; German et al. 2015). Given that ocean water masses cycle through hydrothermal systems on time scales of thousands of years, it is improbable that the Ediacaran oceans could have sustained buildup of a DOC reservoir on the million-year time scales necessary to explain carbon isotope excursions such as the Shuram (Droser et al. 2017b). Similarly, the source of a sufficiently large oxidant reservoir to sustain the Shuram excursion (and achieve the markedly negative DIC δ13C values of its nadir), as well as direct evidence for an oxidation trigger, have long proved elusive (e.g., Grotzinger et al. 2011). Interpretation of the Shuram and its relationship to Ediacara fossil assemblages has also been hindered by limited geochronological constraints, and a paucity of sections containing both Ediacara macrofossils and the Shuram (e.g., Xiao et al. 2016). However, in South China, Australia and the western USA, the entirety of the Shuram excursion precedes the appearance of local Ediacara fossil assemblages by hundreds of meters (e.g., Verdel et al. 2011; Xiao et al. 2016; Smith et al. 2017). Therefore, based on available constraints, there is currently no robust evidence that Shuram-associated carbon cycle perturbation drove Ediacara taxonomic turnover (contra Muscente et al. 2018). While direct evidence for environmental drivers of taxonomic turnover within the Ediacara Biota is currently lacking, it is nonetheless possible that environmental perturbations contributed to the disappearance of the Ediacara Biota at the end of the Ediacaran. The highest stratigraphic occurrences of Ediacara-type and tubular macrofossils occur below the nadir of the basal Cambrian negative carbon isotope excursion (BACE)—a potentially global marker of carbon cycle perturbation—in uppermost Ediacaran strata in northwestern Canada, the western USA, and South China (Macdonald et al. 2013; Smith et al. 2016, 2017; Xiao et al. 2016). Future detailed facies work, and collection of integrated, high-resolution biostratigraphic, chemostratigraphic, and radiometric data will be essential to establish whether these correlations are global in nature, and whether there is a robust and causative relationship between environmental perturbation and Ediacara extinction. Ediacaran EFs: an ecological and evolutionary continuum with Phanerozoic ecosystems? Although most Ediacara taxa disappeared at the end of the Ediacaran Period, the Ediacara Biota should not be considered a “failed evolutionary experiment.” Although the precise affinities of many Ediacara taxa remain poorly resolved, it is increasingly apparent that second-wave Ediacara communities contained a number of stem- and potentially crown-group metazoans and macroalgae (e.g., Xiao and Laflamme 2009; Xiao et al. 2013; Droser et al. 2017b). Moreover, Ediacara organisms pioneered ecological strategies considered characteristic of Phanerozoic and modern complex animal ecosystems—foremost, motility, heterotrophy, sexual reproduction, biomineralization, and the formation of dense and heterogeneous seafloor communities (Droser and Gehling 2015; Droser et al. 2017b; Finnegan et al. 2017). In this light, the Ediacara fossil record should be considered part of an ecological and evolutionary continuum with that of the Phanerozoic, in the manner of Sepkoski’s (1981) EFs (Fig. 1). The Phanerozoic EFs indicate that standing taxonomic diversity is a function of not only species origination and extinction, but also dynamic interplay between ecological and environmental factors (Sepkoski 1981). Critically, the inter-EF boundaries are not defined by complete replacement of the members of one EF by those of the next, but rather by the rise to ecological dominance of groups whose origins significantly predate that rise, and which also postdate its waning. Turnover between EFs appears, in the Phanerozoic, to have been mediated by severe environmental perturbation. If the extinction of the Ediacara Biota (and turnover within the Ediacara Biota) was, as for Phanerozoic EFs, mediated by environmental perturbation (Smith et al. 2017), this suggests that Ediacara and Phanerozoic ecosystems may have followed a similar evolutionary trajectory. We therefore propose that two Ediacaran EFs be added to those of Sepkoski (1981): (1) An Avalon EF, containing rangeomorph-dominated ecosystems characterized by tiered benthic communities and the appearance of complex reproductive strategies; and (2) An Ediacara EF represented by the second-wave White Sea and Nama Assemblages. The Ediacara EF records the emergence and widespread implementation of a range of novel Ediacara-type body plans, mobility, sexual reproduction, biomineralization, and reef development in highly dynamic shallow marine environments and in ecological association with heterogeneous organically bound substrates (Fig. 1). The clear presence of complex, animal-style ecologies in second-wave White Sea- and Nama-type assemblages and evidence that these communities were also populated by animals for millions of years suggests that the Ediacara Biota cannot simply be dismissed as an evolutionary anomaly “outcompeted” by animals. Summary We propose that the ecological diversification of younger, second-wave Ediacara communities recorded by the White Sea and Nama Assemblages was mediated by the expansion of Ediacara taxa into dynamic, shallow marine environments characterized by episodic disturbance and heterogeneous organically-bound substrates. This interplay of environmental and substrate factors likely directly mediated the development of complex ecological strategies characteristic of Phanerozoic animal-dominated ecosystems. In light of evidence that Ediacara communities with animal-style ecologies coexisted with and included stem- and crown-group animals for millions of years prior to the Cambrian, we propose the addition of two new Ediacaran EFs to Sepkoski’s (1981) EF paradigm. The apparent disappearance of the Ediacara Biota at the end of the Ediacaran, and potential decreases in diversity between the White Sea and the Nama Assemblages, have, like many aspects of the Ediacara fossil record, inspired much debate. However, limited (and frequently spatially disparate) data and poor age constraints have hampered robust reconstructions of Ediacara paleodiversity. Future work, focusing on detailed facies characterization, the establishment of further high-precision radiometric age constraints, and integration of biostratigraphic and chemostratigraphic records in Ediacaran fossiliferous successions worldwide will be necessary to increase the resolution and facilitate robust assessment of the upper Ediacaran fossil record. Acknowledgments We are grateful to L. Parry, N. Planavsky, and E. 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Integrative and Comparative BiologyOxford University Press

Published: Apr 27, 2018

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