The end of the Ediacara biota: Extinction, biotic replacement, or Cheshire Cat?

Abstract

The Ediacaran–Cambrian transition signals a drastic change in both diversity and ecosystem construction. The Ediacara biota (consisting of various metazoan stem lineages in addition to extinct eukaryotic clades) disappears, and is replaced by more familiar Cambrian and Paleozoic metazoan groups. Although metazoans are present in the Ediacaran, their ecological contribution is dwarfed by Ediacaran-type clades of uncertain phylogenetic affinities, while Ediacaran-type morphologies are virtually non-existent in younger assemblages. Three alternative hypotheses have been advanced to explain this dramatic change at, or near, the Ediacaran–Cambrian boundary: 1) mass extinction of most Ediacaran forms; 2) biotic replacement, with early Cambrian organisms eliminating Ediacaran forms; and 3) a Cheshire Cat model, with Ediacaran forms gradually disappearing from the fossil record (but not necessarily going extinct) as a result of the elimination of unique preservational settings, primarily microbial matgrounds, that dominated the Ediacaran. To evaluate these proposed explanations for the biotic changes observed at the Ediacaran–Cambrian transition, environmental drivers leading to global mass extinction are compared to biological factors such as predation and ecosystem engineering. We explore temporal and biogeographic distributions of Ediacaran taxa combined with evaluations of functional guild ranges throughout the Ediacaran. The paucity of temporally-resolved localities with diverse Ediacaran assemblages, combined with difficulties associated with differences in taphonomic regimes before, during, and after the transition hinders this evaluation. Nonetheless, the demonstration of geographic and niche range changes offers a novel means of assessing the downfall of Ediacara-type taxa at the hands of emerging metazoans, which we hypothesize to be most likely due to the indirect ecological impact metazoans had upon the Ediacarans. Ultimately, the combination of studies on ecosystem construction, biostratigraphy, and biogeography showcases the magnitude of the transition at the Ediacaran–Cambrian boundary.

Full text

GR Focus Review
The end of the Ediacara biota: Extinction, biotic replacement, or Cheshire Cat?
Marc Laflamme
a,
⁎, Simon A.F. Darroch
b
, Sarah M. Tweedt
a,c
, Kevin J. Peterson
d
, Douglas H. Erwin
a,e
a
Department of Paleobiology, MRC-121, National Museum of Natural History, Washington, D.C. 20013-7012, USA
b
Department of Geology and Geophysics, Yale University, PO Box 208109, New Haven, CT 06520-8109, USA
c
Behavior, Ecology, Evolution & Systematics (BEES), University of Maryland, College Park, MD 20742, USA
d
Department of Biological Sciences, Dartmouth College, Hanover, NH, USA
e
Santa Fe Institute, 1399 Hyde Park Road, Santa Fe, NM 87501, USA
abstractarticle info
Article history:
Received 18 May 2012
Received in revised form 9 November 2012
Accepted 13 November 2012
Available online 27 November 2012
Handling Editor: M. Santosh
Keywords:
Mass extinction
Cambrian explosion
Ecosystem engineering
Predation
Biogeography
Biostratigraphy
Ecospace occupation
Osmotrophy
The Ediacaran–Cambrian transition signals a drastic change in both diversity and ecosystem construction.
The Ediacara biota (consisting of various metazoan stem lineages in addition to extinct eukaryotic clades)
disappears, and is replaced by more familiar Cambrian and Paleozoic metazoan groups. Although metazoans
are present in the Ediacaran, their ecological contribution is dwarfed by Ediacaran-type clades of uncertain
phylogenetic affinities, while Ediacaran-type morphologies are virtually non-existent in younger assem-
blages. Three alternative hypotheses have been advanced to explain this dramatic change at, or near, the
Ediacaran–Cambrian boundary: 1) mass extinction of most Ediacaran forms; 2) biotic replacement, with
early Cambrian organisms eliminating Ediacaran forms; and 3) a Cheshire Cat model, with Ediacaran forms
gradually disappearing from the fossil record (but not necessarily going extinct) as a result of the elimination
of unique preservational settings, primarily microbial matgrounds, that dominated the Ediacaran. To evaluate
these proposed explanations for the biotic changes observed at the Ediacaran–Cambrian transition, environ-
mental drivers leading to global mass extinction are compared to biological factors such as predation and
ecosystem engineering. We explore temporal and biogeographic distributions of Ediacaran taxa combined
with evaluations of functional guild ranges throughout the Ediacaran. The paucity of temporally-resolved
localities with diverse Ediacaran assemblages, combined with difficulties associated with differences in taph-
onomic regimes before, during, and after the transition hinders this evaluation. Nonetheless, the demonstra-
tion of geographic and niche range changes offers a novel means of assessing the downfall of Ediacara-type
taxa at the hands of emerging metazoans, which we hypothesize to be most likely due to the indirect ecolog-
ical impact metazoans had upon the Ediacarans. Ultimately, the combination of studies on ecosystem con-
struction, biostratigraphy, and biogeography showcases the magnitude of the transition at the Ediacaran–
Cambrian boundary.
© 2012 International Association for Gondwana Research. Published by Elsevier B.V. All rights reserved.
Contents
1. Introduction ............................................................. 559
2. Ediacaran classification: stems, crowns, and extinct clades ........................................ 559
3. Caveats on Ediacaran preservation: closing a taphonomic window .................................... 561
4. Biostratigraphic and biogeographic distribution of Ediacaran clades .................................... 563
4.1. Ediacaran temporal distribution ................................................. 563
4.2. Putative Cambrian ‘survivors’.................................................. 565
5. Ediacaran paleoecology: engineering competitive guilds ......................................... 566
6. Mass extinctions through time ..................................................... 567
7. Evaluation of alternative models for the Ediacaran–Cambrian transition .................................. 567
7.1. Cheshire Cat model ....................................................... 568
7.2. Mass extinction model ..................................................... 568
7.3. Biotic replacement model .................................................... 568
7.3.1. Predatory displacement ................................................ 568
7.3.2. Ecosystem engineering ................................................. 569
Gondwana Research 23 (2013) 558–573
⁎Corresponding author at: Department of Chemical and Physical Sciences, University of Toronto at Mississauga, Mississauga, Ontario, Canada L5L 1C6.
E-mail address: marc.laflamme@utoronto.ca (M. Laflamme).
1342-937X/$ –see front matter © 2012 International Association for Gondwana Research. Published by Elsevier B.V. All rights reserved.
http://dx.doi.org/10.1016/j.gr.2012.11.004
Contents lists available at SciVerse ScienceDirect
Gondwana Research
journal homepage: www.elsevier.com/locate/gr

8. Conclusions ............................................................. 570
Acknowledgments ............................................................. 570
References ................................................................ 570
1. Introduction
The Cambrian explosion of metazoans represents the greatest
and most rapid expansion in higher-order animal disparity, with
crown members of nearly every animal phylum originating within
10–20 million years (Knoll and Carroll, 1999; Erwin et al., 2011).
This biological diversification has been extensively studied (see
reviews by Marshall, 2006; Erwin et al., 2011; Erwin and
Valentine, 2012). However, the burst of crown group metazoans
near the base of the Cambrian was preceded by a less widely ap-
preciated suite of large complex multicellular organisms of con-
siderable diversity and morphological disparity: the Ediacara
biota (Fig. 1;Narbonne, 2005; Fedonkin et al., 2007a; Xiao and
Laflamme, 2009).
The Ediacara biota are globally-distributed and temporally re-
stricted (579–542 Ma; Narbonne et al., 2012) macroscopic organisms
traditionally regarded as closely related to metazoans, either as stem/
crown group animals (e.g. Gehling, 1991), or more controversially, as
belonging to the extinct clade Vendobionta (previously Vendozoa;
Buss and Seilacher, 1994). The variability in overall shape, growth po-
larity, body symmetry, and branching modularity found across the
Ediacara biota is such that these organisms most likely represent an
assortment of clades, including extinct lineages as well as potentially
stem- and even crown-group animals, with distinct evolutionary his-
tories, all sharing a common mode of preservation (Narbonne, 2005;
Xiao and Laflamme, 2009; Erwin et al., 2011). In this review, we
restrict the term Ediacara biota to refer to lineages of large,
soft-bodied organisms preserved as casts and molds in sediments of
Ediacaran (and perhaps Cambrian) age. This excludes metazoan
trace fossils (e.g. Jensen et al., 2005) and the earliest skeletal fossils
of late Ediacaran age.
The claim that the disappearance of the Ediacara biota repre-
sents a global mass extinction event provides a series of testable
hypotheses. Sepkoski (1986) argued that a mass extinction required a
“substantial increase in the amount of extinction (i.e., lineage termina-
tion) suffered by more than one geographically widespread higher
taxon during a relatively short interval of geologic time, resulting in
an at least temporary decline in their standing diversity”.Assuch,this
review will evaluate the higher-order diversity (i.e. disparity) during
the Ediacaran by investigating the biostratigraphic and biogeographic
distributions of the newly defined Ediacaran clades. As Ediacaran fossil
localities are exceptional in preserving soft-bodied organisms, under-
standing the nuances in Ediacaran preservation is necessary to disentan-
gle taphonomic biases associated with proposed temporal and spatial
trends in Ediacaran fossil distributions, and in evaluating the hypothesis
suggesting that the disappearance of the Ediacara biota is largely a taph-
onomic artifact. Furthermore, as mass extinctions drastically affect
the ecological structure of communities, Ediacaran paleoecology
and niche subdivision will be investigated. With this conceptual
framework in place, this review will evaluate evidence for three dif-
ferent primary causes of the Ediacaran–Cambrian transition: a mass
extinction model, which posits a rapid, environmentally-driven event,
analogous to Phanerozoic mass extinctions; a biotic replacement model,
in which the expansion of new clades in the Cambrian ecologically
displaced Ediacaran clades; and a Cheshire Cat modelfocusingontaphon-
omy, in which the Ediacara biota effectively vanish from the fossil record
due to the disappearance of the unique circumstances allowing for their
preservation (closing of a taphonomic window). Each of these models al-
lows for basic predictions that can be tested against existing data.
Furthermore, this predictive approach will highlight areas where data
are deficient and therefore provide fruitful avenues of future research.
2. Ediacaran classification: stems, crowns, and extinct clades
Although pioneering studies by Billings (1872),Gürich (1929, 1930,
1933), and most famously Sprigg (1947, 1949) were the first to describe
what have come to be known as Ediacarabiota,theseeffortsweremostly
overlooked until Ford (1958) and Glaessner and Daily (1959) demon-
strated a pre-Cambrian age for these fossils (as reviewed in Fedonkin et
al., 2007a). Previous attempts at classification (see review in Fedonkin
et al., 2007a) focused on their gross morphology, assigning forms to
crownanimalclades(Glaessner, 1979; Gehling, 1991) including (but by
no means limited to) cnidarians (Glaessner and Wade, 1966), sponges
(Gehling and Rigby, 1996; Sperling et al., 2011), annelids (Wade, 1972),
arthropods (Lin et al., 2006), and echinoderms (Gehling, 1987). Others
have allied at least some of these fossils with algae (Ford, 1958), fungi
(Peterson et al., 2003) and even lichen (Retallack, 1994, 2007).
A major paradigm shift occurred when Seilacher (1984, 1985, 1989,
1992) proposed, based primarily on similarities in morphological con-
struction and mode of preservation, that the Ediacara biota were inde-
pendent of Metazoa and constituted an extinct, higher-order clade of
giant single-celled organisms he termed Vendozoa (Seilacher, 1989;
amended to Vendobionta Seilacher, 1992; Buss and Seilacher, 1994).
According to Seilacher (1984, 1992), the Vendobionta was a diverse
and highly successful group of macroscopic organisms who actively
competed with metazoans, and he hypothesized that theywere eventu-
ally driven to extinction by macroscopic predation (Seilacher et al.,
2003). The Vendobionta hypothesis highlights the “fractal quilting”
(Fig. 1.1–3) and “serial quilting”(Fig. 1.6–7) common to many Ediacar-
an fossils but seemingly absent from known metazoan body plans.
Seilacher (1992) also underscored the preservational style in which
coarse sands were able to cast the external morphology of non-
skeletonized Ediacarans. Later refinements (Seilacher et al., 2003;
Seilacher, 2007) of the Vendobionta focused on the fractally- and
serially-quilted forms, citing their modular construction (and specifical-
ly the ensuing compartmentalization) to argue for a unicellular mode of
life similar to xenophyophores, a group of giant single-celled protists
that inhabit the deepest regions of the ocean. Several difficulties arise
with a unicellular interpretation though, most notably the ability of
Ediacaran fronds to construct meter-long complex morphologies com-
plete with varying integument strength and rigidity (Laflamme et al.,
2004; Laflamme and Narbonne, 2008a; Laflamme et al., 2012).
Despite their fundamental differences, the Metazoa vs. Vendobionta
hypotheses both interpret the majority of the Ediacara biota as
representing a single clade. Recently, Xiao and Laflamme (2009) and
Erwin et al. (2011) have instead proposed that members of the Ediacara
fauna represent several independent clades, including extinct lineages
as well as stem/crown group animals. This marks an important shift
from considering all Ediacara biota as a unified group, as these studies
subdivide fossils into subsets that can be studied independently.
Erwin et al. (2011) emphasized branching and segmented architecture,
body symmetry, associated trace fossils, and growth parameters, while
limiting direct comparisons with modern taxa unless they share un-
questionable synapomorphies. Whenever possible, unique synapomor-
phies were used to recognize clades within the Ediacara biota; however
the phylogenetic relationships amongst these clades is difficult to pin-
point, especially as most do not share characters with any extant
eukaryotes.
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Because this taxonomic framework is new, we briefly review it here.
Using the compilation assembled by Fedonkin et al. (2007a) in addition
to adding new taxa described since its publication, seven clades
(Rangeomorpha, Fig. 1.1–3; Arboreomorpha, Fig. 1.4; Kimberellomor-
pha, Fig. 1.5; Erniettomorpha Fig. 1.6; Dickinsoniomorpha, Fig. 1.7;
Triradialomorpha, Fig. 1.8, and Porifera Fig. 1.9–10), and three likely
groups (Bilateralomorphs Fig. 1.11; Tetraradialomorphs, Fig. 1.12;
Pentaradialomorphs, Fig. 1.13) were defined. These groupings consist
of multiple species, with the exception of the Tetraradialomorphs
and Pentaradialomorphs, and several include morphotypes occupying
different benthic tiers or ecological guilds of Bush et al. (2011), reduc-
ing the likelihood that their shared morphology simply reflects ecolo-
gy (Laflamme and Narbonne, 2008a,b). We use the term “group”to
indicate probable polyphyletic assemblages that are unlikely to repre-
sent true clades.
Rangea was first described by Gürich (1929), although subsequent
analyses by Pflug (1972) and Jenkins (1985) were essential in highlight-
ing the modular and self-repeating branching pattern (termed “frondlets”
by Narbonne, 2004;Fig. 1.1–2) shared by all of the Rangeomorpha
(Fig. 1.1–3; Narbonne, 2004; Narbonne et al., 2009; Brasier and
Antcliffe, 2009; Brasier et al., 2012). These frondlets are subsequently as-
sembled into larger constructions (Laflamme and Narbonne, 2008b),
including fronds (Grazhdankin and Seilacher, 2005; Laflamme and
Narbonne, 2008a), bushes (Flude and Narbonne, 2008), fences
(Bamforth et al., 2008), and mats (Gehling and Narbonne, 2007).
The repeated branching of the rangeomorph frondlet results in a signif-
icant increase in surface area, which could have allowed for effective
osmotrophic feeding (Seilacher, 1992; Sperling et al., 2007; Laflamme
et al., 2009).
The Arboreomorpha (Fig. 1.4) is exemplified by the globally-
distributed frond Charniodiscus (Ford, 1958; Jenkins and Gehling,
1978; Laflamme et al., 2004), which possesses primary branches
that are stitched together into a large leaf-like sheet, with teardrop-
shaped secondary branches.
The Kimberellomorpha (Fig. 1.5) is a clade of oval-shaped
bilaterally-symmetrical fossils with at least three concentrically-
arranged zones and clear anteroposterior differentiation (Fedonkin
et al., 2007b). A distal rasping radula-like appendage, combined
with the close association of Kimberella with Radulichnus traces
(Ivantsov, 2009, 2010), have resulted in this group being considered
as stem group mollusks (Fedonkin and Waggoner, 1997).
Two clades are composed of cylindrical units. The Erniettomorpha
(Fig. 1.6) consist of modular organisms constructed entirely of tubu-
lar units arranged into either multifolliate fronds (Narbonne et al.,
1997), “sac-like”or “canoe-shaped”benthic recliners (Pflug, 1966;
Grazhdankin and Seilacher, 2002), or flat-lying mats (Jenkins and
Gehling, 1978). In contrast, the Dickinsoniomorpha (Fig. 1.7) consist
of modular organisms with anteroposterior differentiation. Speci-
mens of Dickinsonia have been found with contracted cylindrical
units (Gehling, 1991), in addition to being associated with likely
trace fossils (Ivantsov and Malakhovskaya, 2002; Ivantsov, 2011).
These features are lacking from Erniettomorphs and suggest the
tubular units are not homologous between the groups, although it is
difficult to be certain without comparative outgroups. At the very
least, they represent two clades that may (or may not) be related.
The identification of traces associated with assumed feeding via
basal surface absorption lead Sperling and Vinther (2010) to propose
a Placozoan-grade affinity for the Dickinsoniomorpha.
The Triradialomorpha clade (Fig. 1.8) is characterized by three
plains of symmetry (Gehling et al., 2000) or by the spiral rotation of
three independent arm-like structures (Glaessner and Wade, 1966).
Each arm is typically composed of smaller tubular branching units
that may have served as the primary feeding apparatus in these
organisms.
The final clade consists of several fossils interpreted to be Poriferan
(Fig. 1.9–10), which include examples of possible spicular ridges and a
central osculum (Fig. 1.9). However, no undisputed siliceous or calcare-
ous sponge spicules have been reported prior tothe Cambrian (Sperling
et al., 2010).
The Bilateralomorpha (Fig. 1.11) are a likely polyphyletic grouping
of bilaterally-symmetrical (or offset bilateral symmetry, Fedonkin,
1985) forms with anteroposterior differentiation. Several species have
modular units branching off a central axis (e.g. Spriggina), which have
been contentiously interpreted as evidence of segmentation (Lin et al.,
2006), while others are delineated by an outer rim and lack any
outward signs of modularity (e.g. Parvancorina). Tetraradialomorphs
(Fig. 1.12) and Pentaradialomorphs (Fig. 1.13) each consist of a single
species with four- or five-fold symmetry, respectively. Their morpho-
logical construction is unique from all other Ediacarans, however,
since both groups are monospecific their higher-order status is difficult
to elucidate.
This emphasis on several independent higher-order clades draws
attention to a long-recognized difficulty associated with Ediacaran
classification: a substantially greater amount of disparity between
morphologically-defined groups as compared to overall species diversi-
ty; a pattern often seen at the base of major metazoan clades (Erwin,
2007). For example, the overwhelming number of Ediacaran genera
are monospecific, and with the exception of the Rangeomorpha
(Brasier and Antcliffe, 2009; Narbonne et al., 2009; Brasier et al., 2012;
Laflamme et al., 2012) no taxonomic hierarchical relationships have
been established amongst these forms. Most emphasis has been placed
on establishing their relationships to extant phyla rather than
establishing the framework of evolutionary relationships among taxa.
This is likely a result of the overwhelming disparity found between
different Ediacaran forms, their depauperate diversity in fossil collec-
tions, andthe absence of clearphylogeneticcharacters that would other-
wise allow recognition of distinct clades. In the context of a potential
extinction event at the close of the Ediacaran, the loss of disparity may
be more telling than the overall number of species that disappear
approaching the Ediacaran–Cambrian boundary. However, before inves-
tigating Ediacaran clades from a biogeographic,biostratigraphic, and pa-
leoecological perspective, taphonomic issues relating to their unique
mode of preservation must be addressed.
3. Caveats on Ediacaran preservation: closing a
taphonomic window
The exceptional preservation of soft-bodied Ediacara biota in
coarse, seemingly normal marine sediments has complicated their
study, as these environmental settings are typically inappropriate
for soft-tissue preservation in the Phanerozoic (Briggs, 2003). Under-
standing the chemical, sedimentary, and biological processes that
govern soft-tissue preservation are necessary to assess the quality of
the Ediacaran record, to address the taphonomic discrepancy be-
tween Proterozoic and Phanerozic fossil assemblages, and to evaluate
Fig. 1. Ediacaran macrofossils representative of higher-order clades. 1. Rangeomorpha Avalofractus abaculus (NFM F-754) from the Avalon Peninsula of Newfoundland with inset
(2) showing self-repeating primary branching. 3. Rangeomorpha Charnia masoni from the White Sea of Russia. 4. Arboreomorpha Charniodiscus procerus from the Bonavista of
Newfoundland. 5. Kimberellomorpha Kimberella quadrata from the White Sea of Russia. 6. Erniettomorpha Pteridinium simplex from Namibia. 7. Dickinsoniomorpha Dickinsonia
costata (SAM P18888) from the Flinders Ranges, South Australia. 8. Triradialomorpha Tribrachidium heraldicum (SAM P12889) from the Flinders Ranges, South Australia. 9–10.
sponges Paleophragmodictya reticulate (SAM P32352) (9) from the Flinders Ranges, South Australia and Thectardis avalonensis (10) from the Avalon Peninsula of Newfoundland.
11. Biradialomorpha Spriggina floundersi (SAM P29801-2) from the Flinders Ranges, South Australia. 12. Tetraradialomorpha Conomedusites lobatus (SAM P13789) from the Flinders
Ranges, South Australia. 13. Pentaradialomorpha Arkarua adami (SAM P26768) from the Flinders Ranges, South Australia. Scale bars 1 cm. Images (5–6) copyright Smithsonian
Institution.
561M. Laflamme et al. / Gondwana Research 23 (2013) 558–573

how the disappearance of these unique conditions is related to the
vanishing Ediacarans.
The framework for modern Ediacaran taphonomic studies is based
on the work of Glaessner and Wade (1966) and Wade (1968).Wade
(1968) proposed that the nature of the Ediacaran body fossil, either
convex (positive; Fig. 2.1) or concave (negative; Fig. 2.2) with rela-
tion to the bottom (hyporelief; Fig. 2.1) or top (epirelief; Fig. 2.2) of
beds, could be related to the strength of the tissue being fossilized.
Norris (1989) and Bruton (1991) were the first to attempt to repro-
duce Ediacaran preservation experimentally, and highlighted the
difficulties in replicating Ediacaran preservation even under ideal
conditions. Structural distortions and the inability to preserve jelly-
fish smaller than 3–4 cm prompted Norris (1989) to suggest that
Ediacaran integuments must have been stiffer and more resistant to
decay. Bruton (1991) observed that, unless stranded on a beach, jelly-
fish were incapable of producing external molds in sediment due to
their neutral buoyancy. Combined, these studies identified difficulties
with the model of Ediacarans as cnidarians fossilized under normal
marine settings. Seilacher (1992) utilized this evidence to forward the
Vendobionta hypothesis of non-metazoan affinities for the fossils, while
Gehling (1999) instead focused on the non-actualistic preservational
setting.
Gehling (1999) proposed a microbial ‘death mask’model for the
preservation of soft-bodied Ediacaran organisms (Gehling et al.,
2005; Gehling and Droser, 2009). The model predicts that, following
a storm event and mass-burial of Ediacaran benthic communities, hy-
drogen sulfide generated from bacterial metabolism and organismal
decay below the mat surface would react with iron-rich sediment/
pore waters, resulting in the precipitation of iron sulfides. Sulfide
minerals would then cement the sediment adjacent to carcasses and
effectively ‘cast’the buried organism (Gehling, 1999). Gehling (1999)
observed key sedimentary and biogenic features associated with
Ediacaran fossils, most notably the ubiquitous hematite and limonite
coatings interpreted as the products of weathering of iron sulfides.
These coatings are occasionally associated with pyritized filaments
(Gehling et al., 2005; Callow and Brasier, 2009) and pyrite framboids
(Laflamme et al., 2011a), both of which are predicted by the death
mask model. Furthermore, presumed microbially-induced sedimentary
structures are ubiquitous on fossiliferous surfaces (‘MISS’;Noffke et al.,
2001; Laflamme et al., 2011b). Recent attempts to replicate Ediacaran
death mask preservation (Darroch et al., 2012)demonstratedthat
microbial mats effectively extended the active preservational window
of soft-tissues, allowing for faithful preservation of fine-scale mor-
phological details after as much as six weeks of tissue decay. Fur-
thermore, these experiments demonstrated the precipitation of
black, aluminosilicate-like precipitates sharing a striking mineral-
ogical composition to those found in cross-sections of Ediacaran
fossils, including probable iron sulfides (Laflamme et al., 2011a).
Narbonne (2005) refined the death mask model, noting that
modes of preservation associated with two- (Fig. 2.1, 2, 4) and
three-dimensional (Fig. 2.3) fossils are associated with distinct envi-
ronmental facies and sedimentary regimes. These preservational
modes were found to be independent of temporal or geographical dis-
tributions, with several localities displaying multiple preservational types.
Exploration of additional sedimentary facies has expanded the bound-
aries on Ediacaran preservation, with diverse assemblages found hosted
within turbidites (Narbonne, 2004), carbonates (Grazhdankin et al.,
2008), and even as carbonaceous impressions reminiscent of Burgess
Shale-type localities (Yuan et al., 2011).
Recent taphonomic studies have focused on the biases associated
with Ediacaran preservational regimes to evaluate the quality of the
Ediacaran dataset. Brasier et al. (2010) argued that the preservation
of soft tissues and cellular structure in the Ediacaran is vastly superior
to modern settings due in large part to the almost complete absence
of vertical bioturbation prior to the Cambrian explosion. This absence
of vertical sediment mixing would result in a sharp redox boundary at
(or near) the sediment–water interface, allowing for rapid cementa-
tion, sediment lithification, and ultimately the preferential preserva-
tion of soft tissues. Liu et al. (2011) have argued that post-mortem
decay could also significantly affect the overall fidelity of the fossil
being preserved, to a point where amorphous structures could in
fact represent decomposed individuals of well-established Ediacaran
taxa (although see Wilby et al., 2011; Laflamme et al., 2011b). This
greater awareness of the importance of taphonomy when considering
the Ediacara biota will ultimately result in more accurate description
of both taxonomic diversity and –potentially –phylogenetic affinity.
In summary, the taphonomic settings prior to the advent of wide-
spread bioturbation favored soft-tissue preservation, allowing for a
more faithful representation of true biological patterns when com-
pared to Phanerozoic settings (Brasier et al., 2010). As microbial
mats were intimately linked to Ediacaran fossilization, the ubiquitous
geographic and bathymetric extent of microbial colonies prior to the
Fig. 2. Range in Ediacaran preservation of the frond Beothukis mistakensis. 1. Specimen (SAM P41109) in positive hyporelief from South Australia. 2. Specimen in negative epirelief
from Newfoundland. 3. Specimen preserved in three-dimensions within a turbidite bed from Newfoundland. 4. Specimen preserved as a dark impression (ROM 38648) from
Newfoundland. Scale bars 1 cm.
562 M. Laflamme et al. / Gondwana Research 23 (2013) 558–573

Cambrian explosion of burrowing metazoans supports the use of bio-
geographic and biostratigraphic patterns to evaluate the severity of
their disappearance. However, the rapid demise of extensive microbi-
al textures and fabrics with the onset of active metazoan burrowing
and grazing would have significantly diminished the likelihood of
Ediacaran-style preservation in Phanerozoic settings (Gehling, 1999).
4. Biostratigraphic and biogeographic distribution of
Ediacaran clades
Early biogeographic studies of Ediacaran fossils (Waggoner, 1999)
resulted in a biostratigraphic subdivision of the latest Ediacaran
(Waggoner, 2003). A newly-compiled dataset of generic-level
presence–absence data of Ediacaran taxa from most known geo-
graphic localities, subdivided into newly assigned clades (Fig. 3)
and combined with available geochronological data and interpre-
tive facies assignments, clearlyidentified three temporally restricted as-
semblages of taxa (Narbonne et al., 2012). Meert and Lieberman (2008)
interpreted the three assemblages as representing areas of Ediacaran
provinciality; others have offered paleoecological (Grazhdankin, 2004)
and to a lesser extent taphonomic (Narbonne, 2005) explanations for
the trend. However, thebiological turnover associated with each assem-
blage could equally represent an evolutionary progression through the
Ediacaran.
In order to re-explore the Ediacaran record for biogeographic
trends, each presumed temporal assemblage was evaluated from a
paleogeographic standpoint by mapping known Ediacaran fossil lo-
calities, and their respective taxonomic diversity divided into the
newly defined Ediacaran clades, onto C. Scotese's paleocontinental re-
constructions (Fig 4). Exact plate reconstructions for the Ediacaran
are controversial and poorly constrained (Li et al., 2008; Meert and
Lieberman, 2008). We utilized Point Tracker software (Scotese
Paleomap Project, 2011) to reconstruct latitude and longitude coordi-
nates for fossil localities into two time slices: 580 Ma reconstruction
for the Avalon assemblage, and a 540 Ma reconstruction for the
White Sea and Nama assemblages (described below). The resulting
coordinates were then plotted onto plate reconstructions (Scotese
Paleomap Project, 2011) in ArcGIS.
4.1. Ediacaran temporal distribution
The Avalon is the oldest (579–560 Ma) of the three assemblages
identified, and includes sections from Newfoundland (Wood et al.,
2003; Ichaso et al., 2007; Hofmann et al., 2008), England (Wilby et
al., 2011), and the Mackenzie Mountains of northwestern Canada
(Narbonne and Aitken, 1990)(Fig. 4D). The oldest Ediacara fossils
are from the Drook Formation of the Mistaken Point Ecological
Reserve in Newfoundland, Canada (Narbonne and Gehling, 2003).
These fossils appear in the immediate aftermath of the Gaskiers glaci-
ation (Thompson and Bowring, 2000; Bowring et al., 2003), perhaps
not coincidently following a noticeable rise in oxygen as measured
by the ratio of highly reactive iron to total iron (FeHR/FeT) in this
deep ocean basin (Canfield et al., 2007;seealsoFike et al., 2006; Sahoo
et al., 2012). The Rangeomorpha, Arboreomorpha, and Triradialomorpha,
in addition to the likely sponge Thectardis (Sperling et al., 2011)andenig-
matic surface traces of uncertain affinity (Liu et al., 2010), first appear in
the Avalon assemblage. The presence of the Avalon assemblage in
deeper-water localities influenced by contour currents (Wood et al.,
2003; Ichaso et al., 2007) suggests the importance of these currents in
transporting oxygen from surface waters. The distribution of the oldest
Ediacaran localities in circumpolar regions (Fig. 4D) may also highlight
the critical role upwelling played in the early evolution of macroscopic
Eukaryotes by making nutrient-rich waters available to these organisms.
The White Sea assemblage (~560–550 Ma) is globally-widespread
and faunally-diverse, with sections in South Australia (Droser et al.,
2006), the White Sea and Urals of Russia (Grazhdankin, 2004;
Grazhdankin et al., 2009), the Wernecke and Mackenzie Mountains
of northwestern Canada (Narbonne, 1994), and the Olenek Uplift of
Siberia (Grazhdankin et al., 2008)(Fig. 4C). The White Sea assem-
blage has over three times as many genera as the preceding Avalon
Fig. 3. Ediacaran temporal distribution. Greyscale, from lightest to darkest, representing Avalon, White Sea, and Nama assemblages respectively.
Ediacaran clades from Erwin et al. (2011) (supplemental). Modified from radiometric age compilation by Herbert et al., 2010 (references therein). First and last
occurrences compiled from Fedonkin et al., 2007a (references therein), with additional ranges from Bamforth and Narbonne, 2009; Bamforth et al., 2008; Hofmann
et al., 2008; Hofmann and Mountjoy, 2010; Liu et al., 2012; Narbonne et al., 2009; Wilby et al., 2011; Xiao and Laflamme, 2009 (references therein).
563M. Laflamme et al. / Gondwana Research 23 (2013) 558–573

Fig. 4. Ediacaran geographic distribution by Avalon, White Sea, and Nama assemblages.
Modified from Fedonkin et al. (2007a), with the addition of Bamforth and Narbonne (2009),Bamforth et al. (2008),Grazhdankin
(2004),Grazhdankin et al. (2008, 2009),Hofmann et al. (2008),Hofmann and Mountjoy (2010),Ivantsov (2009, 2010),Narbonne et
al. (2009),Wilby et al. (2011) and Xiao and Laflamme (2009).
564 M. Laflamme et al. / Gondwana Research 23 (2013) 558–573

Assemblage, almost all of which are first appearances (Shen et al.,
2008; Erwin et al., 2011). It incorporates a marked expansion in
ecospace occupation (Bush et al., 2011), coupled with an increase in
behavioral complexity as reflected by an expanded trace fossil record
(Jensen et al., 2005). This assemblage documents the first appearance
of the Erniettomorpha, Dickinsoniomorpha, Kimberellomorpha,
Bilaterialomorphs, Tetraradialomorphs, and Pentaradialomorphs.
Two of the most fossiliferous localities, the Flinders Ranges in
South Australia (Fig. 4C locality 1) and the White Sea region in
Russia (Fig. 4C localities 5–6) occupy positions in the equatorial
northern hemisphere (~ 15° N) and polar southern hemisphere
(~60° S) respectively. Furthermore, all clades (save for the
Pentaradialomorphs), have been recovered from both of these re-
gions, implying a global distribution for almost all higher taxo-
nomic groupings of Ediacara biota. Thus, as would be predicted,
although individual species may not be shared between regions,
higher-order clades are broadly distributed. This requires effec-
tive dispersal mechanisms between large marine basins for these
organisms, but over a timescale that facilitates regional differenti-
ation at the species level (Darroch et al., submitted).
The youngest assemblage is the Nama, described from the Kuibis
and Schwarzrand subgroups of Namibia (Grotzinger et al., 1995,
2005; Narbonne et al., 1997; Elliott et al., 2011), the Khatyspyt Forma-
tion in central Siberia (Grazhdankin et al., 2008), and the Mojave
Desert of western USA (Hagadorn and Waggoner, 2000; Hagadorn
et al., 2000)(Fig. 4B). The Nama taxa are presently restricted to
Rangeomorpha, Erniettomorpha, Arboreomorpha, and sponges, al-
though this could represent a taphonomic bias due to the predomi-
nance of 3D preservation which seems to preferentially preserve the
Rangeomorpha and Erniettomorpha (Narbonne, 2005; although see
Grazhdankin et al., 2008). The Nama assemblage also includes evi-
dence of macroscopic predation in the form of bore holes in the oldest
macroscopic biomineralizing organisms such as Cloudina (Bengtson
and Yue, 1992; Hua et al., 2003). The Nama Assemblage displays a
relatively widespread geographic distribution despite the decrease
in overall diversity, the limited number of fossil localities of this age,
and the possible taphonomic biases associated with these deposits
(see Narbonne, 2005). Furthermore, the presence of Rangeomorpha
and Arboreomorpha in the Nama make these some of the longest-
ranging clades, suggesting that they might represent good candidates
for global Ediacaran index fossils. Other classic Ediacaran fossils, for
example Tribrachidium,Dickinsonia,Kimberella, and Spriggina, appear
to be restricted to the White Sea assemblage, and may help future
subdivision of the Ediacaran Period into useful stages.
4.2. Putative Cambrian ‘survivors’
Reported “Cambrian survivors”of Ediacaran taxa are important to
consider in the context of a potential extinction event at the Ediacaran–
Cambrian boundary. Cambrian fronds such as Thaumaptilon (Conway
Morris, 1993;Fig. 5.1–2) and Stromatoveris (Shu et al., 2006)sharetheir
morphology with Ediacarans. However, Ediacaran fronds are described
from at least four clades (Laflamme and Narbonne, 2008a; Erwin et al.,
2011), and likely represent shared ecology, not ancestry (Laflamme and
Narbonne, 2008a,b). Cambrian Thaumaptilon and Stromatoveris can be
assigned to cnidarians (with zooids) and to ctenophores (with ciliated
comb rows), respectively; such synapomorphies are distinctly lack-
ing from Ediacaran examples (Fig. 5.3–6). Jensen et al. (1998) and
Hagadorn et al. (2000) figured several small, frond-like forms
from the Cambrian of South Australia and California, respectively.
These fronds possess a tubular branching morphology similar in
many respects to the Erniettomorpha (described below), and may
represent the best candidates for Cambrian survivors, however fur-
ther taxonomic and taphonomic studies are required.
Radial disk-like fossils are common throughout the Ediacaran.
Earlier studies allied these fossils to pelagic jellyfish (Glaessner and
Wade, 1966), however, subsequent taphonomic studies (e.g. Seilacher,
1989) have convincingly argued that these structures must have been
Fig. 5. Frond branching architecture and Cambrian holdovers. 1–2 Cambrian frond Thaumaptilon walcotti with cnidarian zooids. 3. Arboreomorph branching. 4 & 6. Rangeomorph
branching. 5. Erniettomorph branching. Scale bars 1 cm.
Images (1–2) provided by J.B. Caron, (4–5) by S. Xiao.
565M. Laflamme et al. / Gondwana Research 23 (2013) 558–573

benthic and likely represented the basal attachment structure of fronds
(e.g. Gehling et al., 2000). As such, not only are these structures difficult
(if not impossible) to assign directly to known Ediacaran taxa, they are
by no means restricted to Ediacaran organisms. For example, Ediacaria
booleyi reported from the Upper Cambrian of Wexford, Ireland, represents
circular disk-like structures akin to many circular Ediacaran-type fossils
(Crimes et al., 1995), although MacGabhann et al. (2007) argued against
any direct Ediacaran affinities. It is most likely that these holdfasts shared
a common preservational setting embedded within microbial biofilms
(Laflamme et al., 2011a), rather than representing true Ediacaran hold-
overs. Continued studies of Ediacaran-type microbial mat preservation
in the Phanerozic (Hagadorn et al., 2002) will likely shed light on the dif-
ficulties of assigning Ediacaran affinities to Cambrian and younger organ-
isms fossilized in coarse siliciclastic rocks. However as a general rule,
Phanerozoic Konservat Lagerstätten lack Ediacara biota, and settings per-
missive of Ediacaran-style preservation from the Cambrian onwards
also lack these fossils.
5. Ediacaran paleoecology: engineering competitive guilds
Studies of Ediacaran paleocommunities in the Avalon (Clapham and
Narbonne, 2002; Clapham et al., 2003; Liu et al., 2012)andWhiteSea
(Grazhdankin, 2004; Droser et al., 2006) assemblages have been
instrumental in identifying environmental constraints associated with
paleobathymetry, and restricting the range of biological metabolisms
that can be associated with certain Ediacara biota. Sedimentological
studies from Newfoundland, England, and northwestern Canada
(Dalrymple and Narbonne, 1996; Wood et al., 2003; Ichaso et al.,
2007; Wilby et al., 2011) have demonstrated that these sections were
deposited well below storm wave base (perhaps up to 1.5 km depth;
Dalrymple and Narbonne, 1996), implying that any organisms living in
these areas could not have sustained a photoautotrophic metabolism.
Although chemoautotrophy is a possible alternative for deep-water
communities, the absence of fossil aggregates (Clapham et al., 2003),
the sporadic and isolated occurrence of carbonates (in the form of
dolomite concretions), and chemical analyses of sulfides from Mistaken
Point (Canfield et al., 2007) do not support methane seep-like chemo-
synthesis (Little et al., 1998). Furthermore, competition within these
Ediacaran communities resulted in macroscopic tiering (Clapham and
Narbonne, 2002) strikingly similar to Phanerozoic communities, where
resource partitioning associated with filter-feedingor direct nutrient ab-
sorption (osmotrophy) results in vertical stratification of the water
column.
A useful means of representing ecological and functional guilds
within ecosystems was devised by Bambach et al. (2007) and Bush
et al. (2011), in which tiering, motility level, and preferred feeding
mechanisms are scored and graphically represented as an “ecospace
cube”(Fig. 6). For the Ediacaran, such an ecosystem representation
is significant in that it demonstrates an overwhelming scarcity of
occupied ecospace (Xiao and Laflamme, 2009; Bush et al., 2011). Ear-
liest Ediacaran assemblages possess a restricted ecospace, with most
forms occupying a surficial to erect tier of non-motile osmotrophs
(Fig. 6). Putative trace fossils (Liu et al., 2010; Pecoits et al., 2012)
could represent a deposit-feeding strategy, and a filter-feeding strat-
egy has been suggested for frondose organisms such as Charniodiscus
(Fig. 1.4). The younger White Sea and Nama assemblages mirror the
same trends seen in the Avalon, however, a greater number of likely
suspension feeders and the presence of undisputed surface grazers
does represent a major shift in ecosystem complexity. The increased
architectural diversity of trace fossils suggests expanded infaunal
tiering, although sub-surface traces are still mostly horizontal and
fail to penetrate to greater depths. In general, abundant penetrating
vertical burrows are absent until the base of the Cambrian. Another
important innovation is the diversification of the benthic surficial
guild, with a diversity which now dwarfs the previously dominant
frondose guild of erect, upper-tier organisms.
Although much of this ecosystem simplicity can be attributed to the
difficult nature of interpreting the functional biology of extinct
Fig. 6. Ecospace Occupation Cubes representing behavioral ecological guilds. Vertical axis represents vertical tiering in the water column and sediment, horizontal axis representing
major feeding strategies, and the z axis represents the level of mobility (fully mobile to non-motile and attached). Dark blue squares represent occupied niches, with the diversity
indicated within. Light blue squares indicate niches only represented by trace fossils. Pink cubes represent novel Cambrian innovations. Suspension feeding is not confirmed in
Ediacaran organisms (represented by “?”).
Modified from Bush et al., 2011.
566 M. Laflamme et al. / Gondwana Research 23 (2013) 558–573

organisms, the same could be said for the interpretation of Cambrian
fossils, which occupy a significantly larger amount of ecospace in com-
parison to the Ediacaran (Fig. 6). Some of this increase could be attribut-
ed to the greater diversity of biomineralized taxa which preserve much
more readily under normal taphonomic settings. Nonetheless, several
ecological guilds are represented by entirely soft-bodied organisms in
the Cambrian. Important innovations (Fig. 6, pink cubes) include theex-
pansion into the pelagic and deep-infaunal realms, representing the ad-
vent of motile swimmers, crawlers, and deep substrate burrowers.
Filter-feeding suspension guilds also become more prolific, representing
a greater ecosystem reliance on particulate matter as a food source.
Importantly, the Cambrian is also marked by the loss of primarily
osmotrophic organisms. Although some animals can feed via osmosis,
this activity is usually restricted to specific life stages (pelagic larvae;
Jaeckle and Manahan, 1989; Shilling and Manahan, 1990) or substantial-
ly supplemented by active filter feeding (sponges; de Goeij et al., 2008).
These innovations across the Ediacaran–Cambrian boundary constitute
significant ecosystem restructuring, and suggest major changes in the
way nutrients are acquired and distributed in the water column and
substrate. However, the extent to which this restructuring is a result of
environmentally-driven mass extinction is unclear.
6. Mass extinctions through time
The apparent restriction and eventual disappearance of the
Ediacaran biota has been interpreted as an environmentally-driven
mass extinction (Amthor et al., 2003) comparable in size and scope
to Phanerozoic examples. Much recent work has been conducted to
decipher the causes, consequences, and paleoecological signatures
of Phanerozic mass extinctions; consequently the potential for an
extinction eventat the end of the Ediacaran canbe tested against a num-
ber of criteria. Here we briefly summarize the history of scientific
thought on this subject, so that the available data on the Precambrian–
Cambrian transition can be compared.
Although the mass extinctions that close the Paleozoic and
Mesozoic Eras were first recognized by John Phillips in 1860, the sci-
entific study of these events only began in the early 1960s, with pub-
lications by Schindewolf (1963) and Newell (1967). What would
become known as the ‘big 5’mass extinctions were identified by
Raup and Sepkoski (1982) on the basis of statistically significant pro-
portional losses of marine genera. Historically, ‘mass’extinction events
have been identified in the geological record where there is evidence for
synchronous, global disappearance of metazoan groups (Twitchett,
2006). In the aftermath of the impact hypothesis for the Cretaceous–Pa-
leogene event, the causes and consequences of mass extinction events
have enjoyed a prolonged (~30 years) period of scientificinvestigation
(Twitchett, 2006), with much greater emphasis on the interrogation of
individual sections spanning boundary intervals, and the integration of
fossil datawith studies of geochemistry, sedimentology, geochronology
and other approaches.
Extinction events in the fossil record possess a continuum of magni-
tude (Raup, 1991; Bambach et al., 2004; Twitchett, 2006), and as such
the term ‘mass extinction’has been criticized by some as being largely ar-
bitrary (e.g. Hallam and Wignall, 1997; Benton, 2003). In-depth quantita-
tive treatments suggest a complex picture; when Bambach et al. (2004)
considered rates of both origination and extinction over the Phanerozoic,
only 3 (Ordovician–Silurian, Permian–Triassic, and Cretaceous–
Paleogene) of the ‘big 5’extinctions appear as statistical outliers
in terms of proportional extinction. Although most studies have
sought to quantify the taxonomic impact of the ‘big 5’events in
terms of absolute depletions in marine biodiversity at varying
levels of taxonomic classification (Sepkoski, 1982; Raup and Sepkoski,
1982; McGhee, 1989; Benton, 1995), others have stressed the impor-
tance of quantifying the ecological impact of these events (Droser et
al., 2000; McGhee et al., 2004, 2012), emphasizing their role in removing
incumbent faunas and profoundly changing the structure of ecosystems.
Taxic diversity and ecosystem restructuring are only two means by
which mass extinctions affect biodiversity, and may often be strongly
decoupled (Erwin, 2008a; Webb et al., 2009).
Rates of actual extinction seem to vary dramatically among the
‘big 5’events, likely reflecting different causal mechanisms and asso-
ciated rates of environmental change. However, the paucity of radio-
metric dates for some of these events limits the reliability of such
apparent differences in the rates. One generally accepted criterion
for the labeling an event a ‘mass’extinction has been that they
occur in a geologically brief period of time (Wood, 1999). At one
extreme, the late Devonian event comprised three separate phases
lasting a total of ~25 million years (Morrow et al., 2011). The most
recent estimates for the Ordovician–Silurian event vary between
500 kyr and 1 Myr (Sheehan et al., 1996), the Permian–Triassic
event lasted b200 kyr (Shen et al., 2011), and estimates for the
Triassic–Jurassic are in the range of ~ 50 kyr (Ward et al., 2001).
Rates of biotic extinction among the ‘big 5’events therefore span
many orders of magnitude, and although there is currently no accepted
cut-off for defining the duration of ‘mass extinctions’there is a growing
consensus that longer-term events (such as the late Devonian) should
be considered as phenomena separate from ‘true’mass extinction
events caused by relatively short-lived periods of environmental stress
(e.g. Bambach et al., 2004; Stigall, 2012)thatresultinthedemiseof
higher order clades.
These discussions identify a series of biological, ecological, and
chronological criteria for recognizing mass extinction events in the
fossil record, against which the putative existence of a mass extinc-
tion at the Ediacaran–Cambrian boundary can be critically tested:
(1) Mass extinction events are associated with relatively short-lived
episodes of ecological and environmental stress, that result in elevat-
ed rates of extinction and the truncation of taxonomic lineages. This
separates true extinction events in the fossil record from periods of
decreasing biodiversity brought about by depressed rates of specia-
tion (sensu Bambach et al., 2004); (2) Mass extinction events drasti-
cally affect the structure and composition of communities, typically
resulting in depressed evenness and diversity (Twitchett, 2006).
Blooms of ecological disaster taxa, which are replaced upsection
by opportunists and other survivors, characterize the immediate af-
termath, and ecological recovery proceeds in step-wise fashion
with the gradual re-filling of ecological guilds; and (3) Mass extinc-
tion events are a global and facies-independent phenomenon, that
can be demonstrated independent of geographic or taphonomic
bias.
7. Evaluation of alternative models for the
Ediacaran–Cambrian transition
The combined stratigraphic and paleoecologic data indicates an
ecological transition from dominantly osmotrophic ecosystems to
more ‘modern’marine ecosystems, with expansion of filter-feeding,
predation and other trophic interactions following the Ediacaran–
Cambrian boundary (Fig. 6). Our current temporal resolution of the
fossil data, and particularly the lack of continuous fossiliferous sec-
tions across the boundary, make it difficult to establish the nature of
this transition. Was there a single, rapid, environmental catastrophe
resulting in the first mass extinction episode (“mass extinction”
model)? Were Ediacaran clades driven to extinction due to biologi-
cal factors via a “biotic replacement”model, either by predation
by evolving metazoans (“predatory displacement”)orcompetitive
displacement by the bulldozing and other trophic activities of the
Cambrian clades (“ecosystem engineering”)? Or did the Ediacaran
clades disappear largely for taphonomic reasons, invisible to the
known record although present in actuality, as in the “Cheshire
Cat”model? In this section we evaluate these three alternative
models.
567M. Laflamme et al. / Gondwana Research 23 (2013) 558–573

7.1. Cheshire Cat model
Gehling (1999) proposes that non-actualistic taphonomic settings
dominated in the Neoproterozoic, and thus the end of the Ediacaran
marked the closing of a unique taphonomic window with no Phanerozoic
counterpart. This hypothesis suggests that Ediacaran preservation was
controlled by interactions between Ediacaran organisms and microbial
mats (Gehling et al., 2005), which were subsequently eliminated by
newly evolved animals. As this model does not necessarily require the ex-
tinction of Ediacaran clades, but merely the removal of environmental
controls allowing the preservation of soft-bodied Ediacaran organisms
at the onset of the Cambrian, we describe it as the “Cheshire Cat”
model. In this scenario, Ediacaran fossils are largely preserved only in set-
tings where both organisms and microbial mats could co-exist.
Studies of the distribution of microbial fabrics during the Ediacaran–
Cambrian interval have not found an abrupt shift during this transition,
but rather a more gradual conversion. Change in thecharacter of marine
substrates over this interval appears to be directly related to the dynam-
ics of the Cambrian diversification, with Proterozoic-style microbial sub-
strates persisting into Cambrian Stage 5 (Dornbos et al., 2004; Dornbos,
2006). This change across the boundary is subtlety different from a
Cheshire Cat scenario, differing principally in whether the taxa actually
go extinct as a result of these ecosystem changes, or simply disappear
from the record.
The Cheshire Cat model, however, does predict that Ediacaran
osmotrophic organisms, specifically Rangeomorphs, should persist
into the early stages of the Cambrian; as noted above, no definitive ex-
amples of such have been reported despite numerous examples of ap-
propriate Cambrian facies, nor have they been found in Cambrian or
younger Lagerstätten. This model is difficult to refute due to its reliance
on the absence of evidence(rather than evidence of absence), however
it does not explain the drastic change in ecosystem construction across
the Ediacaran–Cambrian boundary.
7.2. Mass extinction model
An environmentally-driven “mass extinction”model (e.g. Amthor
et al., 2003) proposes rapid ecological turnover and elevated extinc-
tion rates across several higher-order groups in response to environ-
mental stress at the Ediacaran–Cambrian boundary. In this scenario,
the Cambrian explosion sensu stricto represents an explosive adap-
tive radiation of Cambrian lineages into available ecological space in
the immediate aftermath of a mass extinction (with the clades having
been present in some form in the latest Neoproterozoic). This model
predicts a global and near-synchronous (within b1 Ma) truncation
of multiple higher-order Ediacaran lineages with the onset of envi-
ronmental stress followed by a rapid diversification of Cambrian
metazoans in the aftermath of extinction. Initially these might be
short-lived opportunistic or disaster taxa, which would be replaced
by more specialized and competitive Cambrian survivors. The mass
extinction model requires evidence for a global source of ecological
stress, such as perturbation to biogeochemical cycles or ocean chem-
istry (indicated by large-scale isotopic excursion), bolide impact, or
other short-term environmental disturbances.
The last occurrence of Cloudina in Oman (Amthor et al., 2003) and
Erniettomorphs from Namibia (Narbonne et al., 1997) co-occur at the
Ediacaran–Cambrian boundary (Narbonne et al., 2012), coeval with a
large negative δ
13
C excursion suggestive of a possible mass extinction
event. However, there are difficulties with this hypothesis. First, of the
seven clades and three groups of distinct Ediacara biota, only the
Erniettomorpha (and perhaps the Rangeomorpha) are found close to
the boundary. Due to the likely taphonomic signal overprinting Ediacaran
fossils from Namibia (Narbonne, 2005), it is difficult to pinpoint the over-
all temporal distribution of other higher order Ediacaran groups, and
whether they disappeared synchronously prior to the Cambrian (Fig. 3).
Nonetheless, current evidence points to a significant loss in diversity
and disparity following the White Sea assemblage, approximately five
million years prior to the Ediacaran–Cambrian boundary.
Second, geochemical studies have identified several extreme negative
δ
13
C excursions throughout the Ediacaran, including the one at the Edia-
caran–Cambrian boundary. The Ediacaran–Cambrian excursion has been
attributed to a collapse of the biosphere, supporting proposals of an ex-
tinction event (Seilacher, 1984; Brasier, 1989; Knoll and Carroll, 1999;
Zhuravlev et al., 2012). Verdel et al. (2011) have demonstrated at least
two additional negative δ
13
C excursions prior to the boundary excursion
in siliciclastic-dominated post-Shuram (~ 555 Ma; Fike et al., 2006)de-
posits from southwestern Laurentia, although these excursions have yet
to be confirmed from other localities, and isotopic profiles from
siliciclastic sediments have been shown to be problematic (Corsetti and
Kaufman, 2003). Sawakia et al. (2010) also identify multiple negative
δ
13
C excursions in the post-Marinoan Doshuantuo Fm. suggestive of re-
peated biotic turnovers. The recognition of at least three negative δ
13
Cex-
cursions in the latest Ediacaran (Sawakia et al., 2010; Verdel et al., 2011)
suggests that the Ediacara biota persisted through non-steady-state up-
heavals of the carbon cycle and repeated periods of large-magnitude fluc-
tuations in global ocean chemistry (Verdel et al., 2011) with no apparent
effect upon diversity or disparity. Continued research focusing on differ-
entiating global from local perturbations in ocean chemistry, as investi-
gated through geochemical proxies, will aid in characterizing Ediacaran
oceans, and shed light on the environmental background to the Cambrian
explosion. However, at face value, there is limited support for a cause and
effect relationship coupling a large excursion at the base of the Cambrian
with a biotic crisis, and thus at present, there is no direct geochemical ev-
idence supporting a short-lived environmental perturbation coincident
with the disappearance of Ediacaran-type fossils.
Therefore, the data currently available suggest a gradual extinc-
tion of much of the Ediacaran fauna, with some clades disappearing
at or near the boundary (e.g., Erniettomorphs), others disappearing
well before the boundary (e.g., Dickinsoniomorphs) and still others
surviving into the Phanerozoic (e.g., sponges). A major limitation
with assessing the possibility of a mass extinction closing the Protero-
zoic is the lack of well-studied, reasonably continuous, and fossilifer-
ous sections that span the Ediacaran–Cambrian boundary. Moreover,
high-precision geochronology in the latest Ediacaran, specifically in
localities with Ediacaran-type fossils, is limited, which hinders defin-
itive evaluations of the temporal distribution of Ediacaran taxa. As
these limitations are addressed with future research, the hypothesis
of a mass extinction event can be further tested and refined, but at
present the data suggest a different cause for the demise of the
Ediacara biota.
7.3. Biotic replacement model
Biologically-mediated replacement of the Ediacara biota followed
by a Cambrian radiation of complex metazoans would likely have oc-
curred over a much longer interval than in the mass extinction model,
and could have been driven by two different causes: 1) the advent of
predation –a direct biological interaction; and/or 2) replacement
through complex interactions arising from ecosystem engineering –
an indirect biological interaction. These two models are not mutually
exclusive, and both may have operated simultaneously.
7.3.1. Predatory displacement
This model (e.g. Seilacher, 1989, 1992) explains the disappearance
of the Ediacara biota as a consequence of predation by cryptic (i.e. not
fossilized) metazoans, whose presence in the Ediacaran is only
recorded by ichnofossils (Seilacher, 1989, 1992). The model predicts
a stable Ediacaran ecosystem prior to the advent of predation, and a
rapid decrease in diversity and abundance of Ediacaran organisms
concurrent with the appearance of either skeletonized metazoan
remains, and/or increased diversity of trace fossils indicative of
new feeding modes. Critically, this model requires evidence for
568 M. Laflamme et al. / Gondwana Research 23 (2013) 558–573

predatory interactions between Ediacaran organisms and unambig-
uously ‘Cambrian-type’fauna.
The earliest evidence of metazoan predation consists of round bor-
ings in Cloudina (Bengtson and Yue, 1992; Hua et al., 2003) from the
late Ediacaran. As Cloudina co-occurs with Erniettomorphs from the
Mojave Desert (Hagadorn and Waggoner, 2000; Hagadorn et al.,
2000), it suggests the co-occurrence of Ediacaran faunas with preda-
tors in the latest Ediacaran. However, it is not until the Cambrian that
predation, as inferred from both trace fossils and indications of
shell-crushing (see review by Leighton, 2011), becomes widespread.
Peterson and Butterfield (2005) note that biological drivers, most
notably predation, could be responsible for phyletic radiations in
morphological disparity and diversity, accounting for evolutionary
turnovers such as the appearance of “spiny”acritarchs and the
Cambrian explosion of metazoans. Butterfield (2007) invoked the ap-
pearance of complex Phanerozoic-style coevolution such as predator–
prey arms races resulting in novel complex trophic structures and
implied rapid rates of evolution, and he further argued that the evolu-
tion of highly-connected trophic structures would be more inclined to
large-scale turnovers and ultimately extinction. Ediacaran ecosystems
are relatively stable in terms of niche occupation until the transition
into the Cambrian (Fig. 6), wherein osmotrophy becomes restricted
and metazoan expansions into the pelagic and sub-surface realms
tap into novel food sources. Interestingly, despite important evolu-
tionary innovations (i.e. bilaterian grazing) and a 3-fold increase in
diversity (Erwin et al., 2011), overall Ediacaran morphospace occupa-
tion (Shen et al., 2008) and niche subdivision (Fig. 6;Xiao and
Laflamme, 2009) remain stable, likely due to diversification limited
almost entirely to osmotrophic guilds. In other words, neither the
tempo nor the mode of Ediacaran evolution lend any evidence to-
wards predation as a likely evolutionary driver prior to the Cambri-
an. The advent of predatory arms-races, complete with complex
multi-tiered ecosystems, would be predicted to have had profound
effects upon the ecosystem as a whole, however at present there is
no direct evidence of predation on Ediacara biota as well as no
indirect evidence for evolutionary trends spurred by predatory
arms-races prior to the Cambrian.
7.3.2. Ecosystem engineering
This model suggests that Ediacaran organisms were progressively
outcompeted by new clades, particularly bilaterians, due to their su-
perior ecological adaptations in securing both substrate and nutri-
ents, and in their ability to actively shape and alter the surrounding
environment to the detriment of Ediacaran clades (Erwin et al.,
2011; Erwin and Tweedt, 2012). Jones et al. (1994) highlighted the
importance of ecosystem engineers that “directly or indirectly modu-
late the availability of resources to other species, by causing physical
state changes in biotic or abiotic materials. In so doing they modify,
maintain and create habitats”.
The Ediacaran–Cambrian transition is marked by a remarkable
change in the structure of shallow marine sediments, with the end of
dominantly microbially-bound substrates with a sharp sediment–water
interface, to a bioturbated substrate with a mixed-boundary layer at
the sediment–water interface. The onset of metazoan-driven ecosystem
engineering resulted in the demise of microbially-dominated sedimenta-
ry facies such as stromatolitic fabrics, microbial wrinkle structures, and
flat-pebble conglomerates (Sepkoski, 1991; Schubert and Bottjer,
1992). Several authors have suggested that this transition may have
eliminated non-motile osmotrophic Ediacaran clades through indirect
competition for space (Seilacher and Pflüger, 1994; Gehling, 1999;
Seilacher, 1999; Dornbos and Bottjer, 2000; Dornbos, et al., 2004;
Callow and Brasier, 2009). As most Ediacarans were immobile and spe-
cifically equipped to deal with firm, microbially-reinforced substrates,
these organisms were unable to compete. This model predicts gradual,
profound changes in ecosystem structure, concurrent with a decline in
the diversity and abundance of Ediacaran organisms in the same settings.
Furthermore, we would expect evidence of metazoan radiation and/or
increased morphological disparity prior to the Ediacaran–Cambrian
boundary followed by the disappearance of Ediacaran taxa from normal
marine facies and/or biogeographical shifts into deeper or more restrict-
ed settings.
Erwin (2008b) and Erwin and Tweedt (2012) discussed these
changes in the context of ecosystem-wide changes at the Ediacaran–
Cambrian boundary, specifically the oxygenation and ventilation of the
water column through biogenic mixing and filtering by sponges, and
sediment bioturbation and bulldozing by grazing and burrowing
bilaterians. The biology and functioning of the Ediacara biota would
have been heavily affected by these changes, as the activities of meta-
zoans would have directlyaltered the micro- and macrohabitats housing
Ediacaran organisms. During the Ediacaran, the effects of ecosystem en-
gineers appears to have been limited (Erwin, 2008b; Erwin and Tweedt,
2012; Erwin et al., 2011), but with the expansion of vertical bioturbation
resulting in aerated and mixed sediments, greater structural and archi-
tectural innovations via the growth of carbonate reefs, and the evolution
of filter-feeding guilds during the Cambrian explosion, the resulting en-
vironmental and ecological changes irrevocably altered the biological
landscape. As ecosystem engineering has the potential to create, alter,
and ultimately destroy niches and biological guilds (Fig. 6;Erwin and
Tweedt, 2012; Erwin and Valentine, 2012), the effects of such activities
on Ediacaran communities would have been catastrophic.
Butterfield (2009) argued that filter-feeding metazoans, coupled
with the evolution of grazing mesozooplankton, were instrumental in
ventilating the water-column and evolving the modern biological
pump, while Gaidos et al. (2007) proposed that efficient filter-feeding
by early metazoans would have reduced microbial activities thus gener-
ating oligotrophic ocean conditions and allowing for a rise in oxygen.
The evolution of mesozooplankton near the base of the Cambrian
could also have had significant consequences on the distribution of
nutrients in the water column. It has been suggested that several
Ediacaran lineages, most importantly the Rangeomorpha and the
sponges, fed on DOC (Sperling et al., 2011) due to their measurably
high surface-area to volume ratios (Laflamme et al., 2009). For bioavail-
able (labile) DOC to be concentrated in large enough volumes to sustain
aprolific eukaryotic osmotrophic ecosystem in the deep ocean, such
DOC had to have been advected. In modern oceans, the bulk of
deep-ocean DOC is non-labile and effectively unusable by eukaryotes
(Sperling et al., 2011). As postulated by Sperling et al. (2011), the ab-
sence of metazoan zooplankton, which only evolved later in the Cam-
brian, would have resulted in a drastically different Ediacaran ocean
chemistry in comparison with the Phanerozoic, specifically in the con-
centration and distribution of labile DOC. Modern zooplankton produce
a disproportionate amount of labile DOC in shallow-water settings when
compared to deeper sections, via sloppy feeding on phytoplankton
(Moller et al., 2003) and the dissolution of mucus from gelatinous zoo-
plankton (Hansson and Norrman, 1995); a pre-zooplankton Ediacaran
Period could have favored the production/maintenance of labile DOC
throughout the water column. Furthermore, prior to the advent of excre-
ment packing by metazoan guts (Logan et al., 1995), the export of organic
carbon from the surface to greater depths was presumably achieved
through the aggregation of phytoplankton into marine snow, allowing
for prolonged dissolution during significantly slower sinking and ulti-
mately an expanded pool of labile DOC at depth (Sperling et al., 2011).
The evolution of predatory mesozooplankton and large zooplankton
may have ultimately consolidated slow-sinking pictoplankton into larger
particulate matter (Butterfield, 2009), which would have been inaccessi-
ble to osmotrophic Ediacarans and favored filter-feeding metazoans. This
would have also transferred a major source of bioavailable carbon from
the water column to the benthic substrate —resources inaccessible to
most Ediacaran osmotrophs but ideal for detritivores, which greatly di-
versify in the early Cambrian (Bush et al., 2011;Fig. 6).
As most Ediacarans lacked a mouth, tentacles, pores, or guts, theloss
of their primary food source of dissolved DOC, combined with the
569M. Laflamme et al. / Gondwana Research 23 (2013) 558–573

inability to ingest larger particulate matter accessible to filter-feeding
metazoans, would place these organisms at a significant competitive
disadvantage, and could explain the dramatic ecological transition
into filter-feeding dominated ecosystems in the Cambrian. Another
important constraint upon osmotrophic systems concerns trophic
structure: a restricted osmotrophic-specificconstructionwouldlimit
the ability of these organisms to escape their osmosis-specific trophic
level. Unlike filter-feeding metazoans, which may constructionally
evolve beyond their trophic level by developing predatory-specific
feeding apparatuses, osmotrophic forms would be unable to modify
their feeding behaviors to take advantage of other nutritional sources.
Major changes in nutrient supplies have been proposed as a cause of
the Cambrian explosion (Brasier, 1990, 1992a,b), however not from a
perspective of shifting nutrient supplies causing an extinction of the
Ediacara biota.
Most importantly, we suggest that the data compiled here are consis-
tent with a fundamental change in the drivers for evolution and diversifi-
cation at the Proterozoic–Phanerozoic boundary. We propose that the
primary driving force for biological innovation in the Ediacaran, and the
basis upon which evolutionary pressures were directed, concerned the
adsorption of nutrients. Biological competition in an osmotrophic world
resulted in the first macroscopic tiered ecosystems (Clapham and
Narbonne, 2002; Laflamme et al., 2012), with biologically-mediated
differentiation in construction and niche subdivision (Laflamme and
Narbonne, 2008b), complete with ecological succession (Clapham
et al., 2003). Competitive tiering has been demonstrated to result
in ecologically-driven speciation in frond populations adapted to
extract nutrients from different tiers (Laflamme et al., 2004), in
addition to species-specific behavior in current flow to possibly
allow for more effective diffusion across the boundary layer
(Singer et al., 2012). Functional constraints on Ediacaran construc-
tion limit any expansion in terms of trophic structure, restricting
clades such as the Rangeomorpha and Erniettomorpha to immobile,
non-predatory feeding via direct diffusion. Ecospace expansion,
driven by ecosystem engineers and macropredation by metazoans,
favored active or armored responses to competition, transitioning
from osmosis-driven Ediacaran systems wherein the acquisition of
dissolved organic nutrients controlled disparity, into predator–prey
systems controlled by metazoan co-evolution. The ecosystem-wide
consequences of active metazoan behavior, culminating in the evo-
lution of predator–prey driven evolutionary arms races, marks the
single most important differentiation between Ediacaran and Phan-
erozoic systems (Peterson and Butterfield, 2005; Butterfield, 2007).
8. Conclusions
As much as the Cambrian explosion marks the diversification of ani-
mals, the Ediacaran extinction marks the demise of a diverse array of
large multicellular organisms. Through the evaluation of the stratigraphic,
geographic, and ecological distribution of the newly described Ediacaran
clades (Erwin et al., 2011), it is possible to evaluate the tempo and
mode of the end Neoproterozoic extinction in the context of the great
Cambrian radiation. Rangeomorphs, Arboreomorphs, Triradialomorphs,
and sponges first appear in the Avalon assemblage, followed by an ex-
pansion of diversity, disparity, and ecospace occupation with the inclu-
sion of Dickinsoniomorphs, Kimberellomorphs, Erniettomorphs,
Bilateralomorphs, Tetraradialomorphs, and Pentaradialomorphs in
the White Sea Assemblage. Overall diversity and disparity drops
dramatically in the latest Ediacaran Nama assemblage, although
taphonomic biases could be responsible for this decrease. After
compiling the evidence to evaluate the three proposed explanations
for the Ediacaran/Cambrian turnover, ecosystem engineering seems
(at present) the most likely cause, even if it is currently not possible
to refute the other two hypotheses with any certainty.
It is proposed that behavioral innovations associated with the
advent of predation and ecosystem-wide changes triggered by
filter-feeding sponges, grazing and burrowing bilaterians, and the re-
placement of firm, microbially-bound substrates by aerated mixed
grounds, converged and resulted in the first large-scale extinction of
macroscopic life. With the continued interest in the Ediacaran extinc-
tion and the Cambrian explosion, we believe that targeted research
agendas will allow for a more definitive testing of our proposed
causes. From a temporal perspective, two major gaps are apparent
in the Ediacaran; Pre-Gaskiers and late Ediacaran (Early Cambrian?)
examples of Ediacaran-type fossils, specifically from sections accom-
panied by radiometric dates and geochemical data. Dedicated
searches in the latest Ediacaran will help substantiate the overall di-
versity at this time. Geochemical analysis of individual specimens
combined with targeted taphonomic experiments (see Darroch et
al., 2012) will aid in decoupling the observed distribution of Ediacaran
fossils from their temporal and spatial taphonomic window, allowing
an unbiased paleoecological analysis of their disappearance with regard
to the proposed Cheshire Cat model. In addition, abundance data
(i.e. Clapham et al., 2003; Droser et al., 2006; Wilby et al., 2011;
Liu et al., 2012) from Ediacaran sites will allow for a better evaluation
of the transition from Ediacaran- to Phanerozoic-style ecosystems.
Acknowledgments
We wish to thank Guy Narbonne for reading an earlier version of
this manuscript, and two anonymous reviewers for thoughtful com-
ments. Generous funding was provided by the NASA Astrobiology Insti-
tute (MIT Node; Peterson, Erwin, Laflamme, Tweedt) and Smithsonian
Institution Fellowship (Laflamme).
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Marc Laflamme is an assistant professor in the Depart-
ment of Chemical and Physical Sciences, University of
Toronto at Mississauga. He received his Ph.D. from Queen's
University in Kingston, Ontario. His research has addressed
topics ranging from functional morphology and ecosystem
evolution to the mineral/microbe interactions involved in
the exceptional preservation of soft-tissues in the fossil
record of earlylife. His research combineslaboratory experi-
mentation with field-based studies of Ediacaran fossils from
Newfoundland and South Australia.
Simon A. F. Darroch is a graduate student in Paleobiology
at Yale University, supervised by Derek Briggs. He received
his undergraduate training at Durham University (UK),
and completed a masters degree in Paleobiology at the
University of Tokyo (Japan) in 2008. Simon is active in
three main avenues of research: investigating the spatial
paleoecology of mass extinction events and developing
predictive models for biodiversity loss; testing the quality
of the fossil record in carbonate environments using
microfossils; and experimental taphonomy of Ediacaran
scenarios. Simon has previously worked in industry for
Royal Dutch Shell (Carbonate Research division).
Sarah M. Tweedt: studies paleobiology as a graduate stu-
dent in the Biological Sciences program at the University
of Maryland, College Park. She is currently beginning the
third year of a Ph.D. degree supervised by Douglas Erwin
(Smithsonian National Museum of Natural History) and
Charles Delwiche (UMD). Sarah received her Bachelors of
Science with honors in biology (cell and developmental)
at the University of Virginia in 2008. Her research is fo-
cused on the evolutionary origins of animal development,
specifically on the developmental requirements of the Edi-
acara biota and the evolution of development in the earli-
est animals of the Cambrian explosion.
Kevin J. Peterson is a professor of Biological Sciences at
Dartmouth College (Hanover, NH). He received his under-
graduate training in Biology at Carroll College (Helena,
MT), and earned his Ph.D. in Geological Science from the
University of California, Los Angeles. His works centers
on using molecular tools to address the origin and early
evolution of animals.
Douglas H. Erwin is a Senior Scientist at the National
Museum of Natural History, part of the Smithsonian Insti-
tution. Following an A.B. from Colgate University, he re-
ceived a Ph.D from University of California, Santa Barbara
in geology. His research has included systematics of
Permian gastropods, the causes of the end-Permian mass
extinction, and aspects of the Edicaran–Cambrian diversi-
fication of animals.
573M. Laflamme et al. / Gondwana Research 23 (2013) 558–573