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Decoupling of body-plan diversification
and ecological structuring during the
Ediacaran – Cambrian transition:
evolutionary and geobiological feedbacks
M. Gabriela Mángano and Luis A. Buatois
Department of Geological Sciences, University of Saskatchewan, Saskatoon, Saskatchewan, Canada SK S7N 5E2
Research
Cite this article: Mángano MG, Buatois LA.
2014 Decoupling of body-plan diversification
and ecological structuring during the
Ediacaran – Cambrian transition: evolutionary
and geobiological feedbacks. Proc. R. Soc. B
281: 20140038.
http://dx.doi.org/10.1098/rspb.2014.0038
Received: 7 January 2014
Accepted: 21 January 2014
Subject Areas:
palaeontology, evolution
Keywords:
Ediacaran – Cambrian, trace fossils,
Cambrian explosion, agronomic revolution,
ecosystem engineering
Author for correspondence:
M. Gabriela Mángano
e-mail: [email protected]
Electronic supplementary material is available
at http://dx.doi.org/10.1098/rspb.2014.0038 or
via http://rspb.royalsocietypublishing.org.
The rapid appearance of bilaterian clades at the beginning of the Phanerozoic
is one of the most intriguing topics in macroevolution. However, the complex
feedbacks between diversification and ecological interactions are still poorly
understood. Here, we show that a systematic and comprehensive analysis of
the trace-fossil record of the Ediacaran–Cambrian transition indicates that
body-plan diversification and ecological structuring were decoupled. The
appearance of a wide repertoire of behavioural strategies and body plans
occurred by the Fortunian. However, a major shift in benthic ecological structure, recording the establishment of a suspension-feeder infauna, increased
complexity of the trophic web, and coupling of benthos and plankton took
place during Cambrian Stage 2. Both phases were accompanied by different
styles of ecosystem engineering, but only the second one resulted in the establishment of the Phanerozoic-style ecology. In turn, the suspension-feeding
infauna may have been the ecological drivers of a further diversification of
deposit-feeding strategies by Cambrian Stage 3, favouring an ecological
spillover scenario. Trace-fossil information strongly supports the Cambrian
explosion, but allows for a short time of phylogenetic fuse during the terminal
Ediacaran–Fortunian.
1. Introduction
The Ediacaran–Cambrian transition represents a critical time in the history of
the biosphere both in terms of animal diversity and ecosystem construction
[1–4]. Historically, two conflicting views on the early evolution of animals have
emerged. One view takes the fossil record at face value, envisaging a scenario of
rapid origination of modern phyla (the Cambrian explosion), whereas the other
emphasizes the imperfect nature of the fossil record, assuming deep Precambrian
roots in the evolutionary history of animals (the slow phylogenetic fuse) [5,6].
In this second view, the Cambrian explosion is an artefact resulting from an
increase in preservability of body fossils related to the acquisition of mineralized
skeletons, probably linked to major changes in the chemistry of the oceans [7,8].
This debate has mostly revolved around two different datasets: the bodyfossil record and molecular clocks. Although the body-fossil record supports the
notion that the Cambrian event of diversification is real and unparalleled in
the history of life [9,10], interpretation of molecular clock evidence has been
quite controversial. Earlier studies did not support the explosion scenario,
suggesting deeper divergence among animals [11,12]. Although a growing
number of recent studies tend to be more consistent with the body-fossil record,
divergence times are still hard to reconcile with the explosion scenario [13,14].
There is an approximately 20 Myr gap between the youngest exceptional
preservation of Ediacaran body-fossil assemblages, the Nama assemblage
(549–541 Ma), and that of the Cambrian Stage 3 Burgess shale-type assemblages,
such as Chengjiang and Sirius Passet (521–514 Ma). However, trace fossils,
namely trackways, trails, burrows and borings [15], offer an independent line of
evidence to calibrate the Cambrian explosion. A systematic trace-fossil survey
& 2014 The Author(s) Published by the Royal Society. All rights reserved.
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The global database (see the electronic supplementary material)
is based on systematic and critical examination of the literature,
collection material and field data. Six time slices (two informal
Ediacaran subdivisions—Vendian and Nama [17]—and the
four official Lower Cambrian stages) are considered. An older
subdivision (Avalon) has not been included, because uncontroversial bilaterian trace fossils are not known from this time
slice. Although our study addresses the macroevolutionary
changes that took place at the beginning of the Cambrian, the
Ediacaran is included in order to calibrate the ichnological
record of the evolutionary explosion against the much more limited Ediacaran record. In particular, the Nama bin is critical
because it records the appearance of some behavioural types
that represent a prelude to the Cambrian explosion and because
of the controversies surrounding some of the Vendian bin trace fossils. Information was compiled from 369 stratigraphic units. About
20% of these units have been examined by the authors in the field.
Another 20% of the units were analysed based on collection specimens. The remaining units were evaluated based on detailed and
critical literature review. The trace-fossil database includes taxonomical composition, preservation styles, ethology, feeding strategies,
degree of bioturbation, tiering structure, architectural designs,
potential tracemakers, age and depositional environment. Critical
reassessment of published identifications was of paramount importance (see also [17,18]). Synonyms have been checked, and we have
adopted a consistent taxonomical approach to trace fossils. Each
original taxonomic determination has been revised based on reexamination of the original material, photographs and descriptions.
Assessment of degree of bioturbation followed standard ichnological practice using a bioturbation index (BI) [19]. The BI
indicates the extent to which the primary sedimentary fabric is
still visible. In this scheme, BI ¼ 0 is characterized by no bioturbation (0%), and the primary fabric remains intact. BI ¼ 1 (1–4%)
is for sparse bioturbation with few discrete traces locally overprinting the well-preserved sedimentary fabric. BI ¼ 2 (5–30%) is
represented by low bioturbation in sediment that still has wellpreserved sedimentary structures. BI ¼ 3 (31–60%) describes an
ichnofabric with discrete trace fossils, moderate bioturbation and
still distinguishable bedding boundaries. BI ¼ 4 (61–90%) is
3. Results
(a) Ediacaran
A global maximum of 10 ichnogenera has been documented for
the Ediacaran. Of these, nine ichnogenera were already known
2
Proc. R. Soc. B 281: 20140038
2. Material, methods and concepts
represented by intense bioturbation, high trace-fossil density, trace
fossils and primary sedimentary structures mostly erased. BI ¼ 5
(91–99%) is characterized by sediment with completely disturbed
bedding and intense bioturbation. BI ¼ 6 (100%) is for completely
bioturbated and reworked sediment, related to repeated overprinting of trace fossils. In the cases of units analysed by the authors in
the field, BI was assessed for individual beds and summarized by
facies types. In the case of units not studied by the authors in the
field, BI was assessed by evaluating representative samples or by
checking the literature based on original determinations and photos.
Tier classification follows previously established schemes (see
[15] for review). The shallow tier comprises structures produced in
the upper 6 cm of the substrate, the mid-tier those produced
between 6 and 12 cm of the substrate, and the deep tier those
emplaced below 12 cm. The 6 cm boundary reflects approximately
a depth above which organisms are challenged by disturbance
rather than by maintaining contact with the sediment–water interface and below which these difficulties are reversed in severity. The
12 cm boundary marks a boundary within the sediment below
which stresses linked to limited food supply and oxygen content,
as well as by increased substrate compaction, become extreme limiting factors. A very deep tier (more than 100 cm) may also be
considered, but it has been essentially empty prior to the
Mesozoic marine revolution.
Temporal trends in trace-fossil distribution were assessed by a
combined analysis of (global and alpha) ichnodiversity and ichnodisparity [15,20] (table 1; electronic supplementary material, table
S1). Global ichnodiversity (i.e. number of ichnogenera per time
slice) provides a proxy to behavioural changes and evolutionary
innovations during the Earth’s history. To account for the different
duration of the time slices, ichnodiversity has been standardized
per Myr following usual practices in analytical palaeobiology.
Alpha ichnodiversity (i.e. number of ichnogenera recorded for
individual trace-fossil suites) provides a glimpse into ecological
complexity at the scale of individual communities. Although ichnodiversity simply refers to trace-fossil richness, ichnodisparity
(i.e. number of trace-fossil architectural designs) provides a
measure of the variability of basic morphological plans in biogenic
structures, and consequently best records innovations in body
plan, locomotory system and behavioural programme [20]. It is
the tacit premise in our reasoning that, in most cases, major
changes in trace-fossil architecture and in fabricational design are
biologically wired. The fact that ichnodiversity and ichnodisparity
are not necessarily concordant is illustrated in this study. Assessment of morphological and behavioural complexity follows
previous studies [15,20,22].
This approach provides an insight into the complex history of
interactions between animals and sediment, and among organisms also at the community level. Although a univocal link
between the animal producer and the trace fossil is not commonly possible, the appearance of some architectural designs
may be directly linked to a group of producers, such as trackways (arthropods) and pentameral-shaped impressions
(asteroids and ophiuroids), revealing evolutionary innovations
in the fossil record. In addition, the appearance of other architectural designs (e.g. vertical simple burrows, burrows with
horizontal or vertical spreiten), although more equivocal in
terms of the affinities of the producer, certainly reflects novel
ways of interacting with the sediment, allowing us to picture in
finer detail the early steps of the Cambrian diversification event.
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of Ediacaran–Cambrian sections worldwide, involving the
construction of a comprehensive database (see the electronic
supplementary material), demonstrates that the record of
animal–sediment interactions across the Ediacaran–Cambrian
boundary is far more continuous than the body-fossil record,
particularly with respect to that of soft-bodied organisms.
Accordingly, trace fossils represent a key element to evaluate
the timing of diversification and ecosystem construction
during the Cambrian explosion. Bilaterian diversification
resulted in the appearance of ecosystem engineers that actively
modified sedimentary substrates, altering and creating habitats
[3]. However, our understanding of the driving mechanisms
and complex feedback loops involved in these processes
during the Ediacaran–Cambrian transition is quite limited.
The aims of this paper are to (i) demonstrate that the tracefossil record strongly supports the Cambrian explosion scenario,
(ii) provide solid evidence that body-plan diversification and the
establishment of a Phanerozoic benthic ecological structure were
distinct and decoupled events, and (iii) provide insights into the
differential role of ecosystem engineers and feedback loops
during the successive phases of the radiation. Prior to this
study, animal diversification and colonization of the infaunal
ecospace have been considered roughly synchronous [16].
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Ediacaran
(Nama)
Fortunian
Cambrian
Stage 2
Cambrian
Stage 3
Cambrian
Stage 4
global ichnodiversity
9
7
42
43
55
51
global ichnodiversity (standardized per Myr)
appearance of new ichnogenera
0.9
9
0.8
1
3.8
33
5.4
14
7.9
14
10.2
2
maximum alpha ichnodiversity
average alpha ichnodiversity
6
2.6
4
2.0
14
3.3
18
4.0
28
5.4
28
4.8
global ichnodisparity
maximum local ichnodisparity
6
4
5
4
22
11
23
13
29
15
27
15
maximum bioturbation index
0
1
3
6
6
6
average bioturbation index
maximum depth of bioturbation (cm)
0
0.2
0.1
1.0
0.5
8
2.3
100
2.4
100
2.3
100
from the Vendian and seven were recorded in the Nama (table 1
and figure 1). Standardization to reflect ichnodiversity per
geological time shows very low values (0.9 and 0.8 ichnogenera
per Ma, respectively), further reinforcing the view of limited behavioural diversity during the Ediacaran (table 1). Alpha
ichnodiversity is up to 6; 52% of occurrences are monospecific,
in sharp contrast to Phanerozoic ichnofaunas. Ichnodisparity
and behavioural complexity are also remarkably limited, with
only six architectural designs recorded globally. Simple horizontal grazing trails, mostly associated with microbial mat
textures, are by far the dominant elements, representing matground grazing (59% of all recorded cases). Shallow-tier,
actively filled (massive) horizontal burrows (e.g. Torrowangea)
record incipient substrate penetration.
Fan-like arrangements of paired scratch marks produced
on microbial mats are in some cases directly associated with
Kimberella [30]. Ichnological evidence (e.g. the animal located
at the apex of the fan) suggests that Kimberella was the producer
of the scratch traces, recording epibenthic grazing on microbial
mats. However, the phylogenetic affinity of Kimberella remains
controversial. Possible resting and locomotion trace fossils
(Epibaion) produced by dickinsonids occur in direct association
with Dickinsonia and Yorgia [31–33]. However, passive transport has been suggested as an alternative [34]. Because the
affinities of Dickinsonia are uncertain [35] and its morphology
is hard to reconcile with a bilaterian origin, Epibaion is not
included in table 1.
With the exception of the problematic Nenoxites (a controversial ichnogenus that needs further revision) and Epibaion,
which are restricted to the Ediacaran, all the other ichnogenera
present in the Ediacaran continue into the Phanerozoic, and
their production by bilaterians is well supported by neoichnological data, making ad hoc to assume that in the Ediacaran
identical structures were produced by non-bilaterians.
Feeding modes include epifaunal to very shallow infaunal grazers, and non-attached, absorptive or chemosymbiotic feeders.
Restriction of biogenic structures to bedding planes indicates a
negligible use of the infaunal ecospace and the virtual absence
of infaunal tiering. Information from the Nama bin reveals
some changes in ichnofaunal composition. Very shallow,
three-dimensional burrow systems occur, for the first time, in
the Nama [36], revealing an increase in complexity. In any
case, these three-dimensional burrow systems are far simpler
than their Cambrian counterparts, including T. pedum, whose
first appearance datum is indicative of the Ediacaran–Cambrian
boundary [1]. The degree of bioturbation (as seen in crosssection) is invariably 0 in the Vendian, reaching 1 occasionally
in the Nama (table 1 and figure 1).
Of equal importance is the absence of trace fossils produced
by some key players of Phanerozoic communities. Structures
previously interpreted as guided meandering grazing trails
are no longer considered trace fossils, because careful re-analysis
fails to reveal the presence of actual meanders, suggesting that
these were body fossils instead [17,18,33,37]. Therefore, animals
displaying sophisticated feeding strategies involving strophotaxis (i.e. proclivity to make U-turns so that the animal turns
around 1808 at intervals), phobotaxis (i.e. tendency to avoid
crossing its own and other trails) or thigmotaxis (i.e. propensity
to keep close contact with a former segment of the trail) are not
present in Ediacaran rocks. Arthropod trace fossils are strikingly
absent. Unquestionable examples of vertical burrows in highto moderate-energy facies recording activities of suspension
feeders have not been documented from the Ediacaran.
(b) Fortunian
The trace-fossil evidence from the earliest Cambrian shows a
substantially different scenario with the appearance of diverse
and complex ichnofaunas, revealing a wide variety of behavioural patterns (figure 2a–l) and a new cast of characters,
including most notably arthropods (e.g. Rusophycus, Diplichnites,
Allocotichnus). A global maximum of 42 ichnogenera has been
documented for the Fortunian (table 1 and figure 1). The increase
in ichnodiversity is even more remarkable when standardized
to account for differences in duration between the Fortunian
and the terminal Ediacaran (table 1). Alpha ichnodiversity
Proc. R. Soc. B 281: 20140038
Ediacaran
(Vendian)
3
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Table 1. Quantitative summary of ichnofaunal changes across the Ediacaran–Cambrian transition. Ichnodiversity and ichnodisparity assessed after [15,20] and
degree of bioturbation based on [19]. Because of uncertainties in the phylogenetic affinities of Dickinsonia and Yorgia, their trace fossils (Epibaion) have not been
included in this table. With respect to the Ediacaran, we agree with more conservative estimations that the oldest bilaterian trace fossils are dated to approximately
560 Ma [17]. The Ediacaran bin has been further divided using the informal subdivision of Vendian (560–550 Ma) and Nama (550–541 Ma) [17]. The oldest
subdivision (Avalon; 575–560 Ma) does not contain undisputed bilaterian trace fossils, and therefore has not been considered. However, there is increased
evidence of possible mobility by non-bilaterian organisms in Avalon rocks [21].
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polarity
chron
ichnodisparity
(no. architectural
designs)
main behavioural
innovations
0
0
2
4
6
0
1 10 100
Vendian
deep-tier simple and J-, Y- and U-shaped burrows
Nama
trackways
Fortunian
shallow-tier mazes and networks
shallow-tier radial trace fossils
shallow- to mid-tier spreiten burrows
560
0 10 20 30 40 50 60
Stage 2
shallow-tier bilobate trails and burrows
1
30
Stage 3
scratch trace fossils
very shallow-tier
actively filled burrows
shallow-tier branching burrows
Proterozoic
Ediacaran
2 540
20
maximum
burrowing depth
(cm)
Stage 4
very shallow-tier
horizontal trails
3
Phanerozoic
Cambrian
Terrenuvian Series 2
4 520
10
maximum
bioturbation
index
Figure 1. Summary diagram of changes in architectural designs, global ichnodiversity, maximum degree of bioturbation and maximum burrowing depth during the
Ediacaran – Cambrian transition. Maximum burrowing depth is expressed on a logarithmic scale. 1, first evidence of bilaterian trace fossils; 2, major diversification of
trace-fossil bauplans; 3, onset of vertical bioturbation, and coupling of benthos and plankton; 4, earliest fossil lagerstätte (Chengjiang) and Cambrian explosion
according to body fossils. In contrast to fossil lagerstätten, the trace-fossil record is continuous through the critical Ediacaran – Cambrian interval. Higher BIs
have been indicated recently for the Ediacaran [23], but the illustrated structures consist of serially repeated elements, identical to those in problematic body fossils
such as Helanoichnus, Palaeopascichnus and Shaanxilithes [24], arguing against a trace-fossil origin [25]. Trace fossils documented in the Avalon assemblage
(565 Ma) [21] have not been attributed to bilaterians and therefore they have not included in the diagram. An earlier appearance of bilaterian trails
(585 Ma) has been recently suggested [26]. However, the age of the trace-fossil-bearing strata is highly contended, probably being Late Palaeozoic [27]. Therefore,
the structures previously mentioned [21,23,26] have not been included in our database. The appearance of a wide repertoire of behavioural strategies occurred by
the terminal Ediacaran and particularly the Fortunian, preceding the establishment of a modern ecological structure, which took place during Cambrian Stage 2. This
ecological structure was characterized by the appearance of a suspension-feeder infauna, an increased complexity of the food route and trophic web, and a reorganization of the infaunal ecospace, resulting in a dramatic increase in depth and degree of bioturbation. Note that although scratch trace fossils are present in the
Ediacaran, these are associated with Kimberella rather than representing production by arthropods. Carbon isotope curve and the trend of geomagnetic polarity
reversals ( polarity chron column; black, normal polarity; white, reversed polarity) based on [28,29].
reached 14; only 27% of occurrences are monospecific. Ichnodisparity and behavioural complexity also show a remarkable
increase, with 22 architectural designs recorded globally. Some
distinctive structures of selective deposit feeders consist of
systematic guided meanders (e.g. Psammichnites), revealing the
onset of sophisticated grazing strategies that require more
advanced navigational devices. In addition, radial branching
structures (e.g. Volkichnium) are recorded for the first time.
Branching burrow systems (e.g. Treptichnus, Streptichnus,
Multina) became more abundant and diverse, at least some of
them indicating systematic probing of the sediment in search
of food. Surface-coverage branching burrows (e.g. Oldhamia)
are remarkably complex and characterized by closely spaced
probings forming lobate and hook-like patterns that record
sophisticated undermat-mining feeding strategies [18]. Overall,
these searching programmes reflect strophotactic, phobotactic and thigmotactic behaviour, and the development of a
higher-grade nervous system.
The degree of bioturbation in Fortunian deposits remains
notably low (average BI: 0.5, maximum BI: 3), revealing only
a very slight increase with respect to Ediacaran levels (table 1
and figure 1). Although there is a significant expansion in
terms of the represented architectural designs, the infaunal ecospace remains underexploited in comparison with younger
Cambrian deposits. Trace fossils only penetrate the uppermost
centimetres of the sediment, and are typically oriented parallel
to the bedding plane, causing little disturbance in the primary
sedimentary fabric. Isolated vertically oriented trace fossils
are rare, being present in silty and muddy firmgrounds
rather than in moderate- to high-energy shifting sands [38].
Skolithos piperock (i.e. near-shore sandstone containing high
density of vertical burrows produced by suspension feeders
or passive predators) is absent.
(c) Cambrian Stage 2
A maximum number of 43 ichnogenera has been recorded
worldwide for Cambrian Stage 2 (table 1 and figure 1). Alpha
ichnodiversity is up to 18. Ichnodisparity and behavioural complexity show a slight increase, with 23 architectural designs
recorded globally. By contrast, the degree of bioturbation
shows a sharp increase with respect to previous levels (average:
2.3; maximum: 6) and a dramatic increase in maximum
burrowing depth is recorded (up to 1 m).
The most important innovation is the appearance of
sandstone deposits displaying profusion of vertical burrows
(figure 3a–i) forming Skolithos piperock. Most of these vertical
burrows are lined, representing permanent domiciles of suspension feeders and passive predators. The fact that moderate- to
high-energy near-shore, non-bioturbated sandstone is a common
facies in the Fortunian argues against preservational or sampling
biases and in favour of the true appearance of this guild during
Cambrian Stage 2. These low-diversity to monospecific assemblages indicate that worm-like coelomate organisms were able
to colonize the deep infaunal ecospace in mobile sandy substrates of high- to moderate-energy coastal settings for the first
time [39]. In low-energy offshore deposits, intense bioturbation was evidenced by a diverse set of simple and branching
probing structures, commonly bearing distinctive spreite and
representing feeding structures of deposit feeders.
4
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time in millions of years (Ma)
–9 –6 –3 0 3 6
global
ichnodiversity
(no. ichnogenera)
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d 13C
(average
carbonate
values/mil)
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5
(b)
(a)
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(c)
(f)
(e)
(h)
(g)
(k)
Proc. R. Soc. B 281: 20140038
(d )
(i)
( j)
(l)
Figure 2. Representative Fortunian trace fossils, illustrating a rapid increase in ichnodiversity and ichnodisparity. Note the wide variety of architectural designs and the
overwhelming dominance of horizontal shallow-tier trace fossils. Architectural design is indicated between brackets. All are bedding-plane views. (a) Treptichnus isp.
(horizontal to oblique branching burrows). Lower Member, Breivik Formation, northern Norway. (b) Oldhamia alata (surface-coverage branching burrows). Puncoviscana
Formation, northwest Argentina. (c) Monomorphichnus isp., Dimorphichnus isp. (scratch marks) and Helminthopsis abeli (simple horizontal trails). Lower Member, Breivik
Formation, northern Norway. (d) Rusophycus avalonenesis (bilaterally symmetrical short, shallow to deep scratched impressions). Member 2B, Chapel Island Formation,
eastern Newfoundland, eastern Canada. (e) Palaeophycus tubularis (passively filled horizontal burrows). Puncoviscana Formation, northwest Argentina. (f ) Pilichnus cf.
dichotomus (horizontal branched burrow systems). Puncoviscana Formation, northwest Argentina. (g) Didymaulichnus lyelli (bilobate trails and paired grooves). Puncoviscana Formation, northwest Argentina. Coin diameter, 1.8 cm. (h) Cochlichnus anguineus. Puncoviscana Formation, northwest Argentina. (i) Torrowangea rosei (actively
filled, massive, horizontal burrows). Lintiss Vale Formation, southern Australia. ( j) Teichichnus rectus (burrows with vertical spreiten). Member 3, Chapel Island Formation,
eastern Newfoundland, eastern Canada. (k) Gyrolithes polonicus (vertical helicoidal burrows). Lower Member, Breivik Formation, northern Norway. (l ) Psammichnites
saltensis (actively filled, complex meniscate, horizontal burrows). Puncoviscana Formation, northwest Argentina. (a–f, h– l) Scale bars, 1 cm.
(d) Cambrian Stage 3
Cambrian Stage 3 global ichnodiversity is 55, revealing a significant further increase with respect to Cambrian Stage 2,
which is even more pronounced when standardized to account
for differences in duration between both stages (table 1 and
figure 1). This increase took place mostly in connection with
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(b)
(c)
(d )
6
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(a)
(f)
(g)
(h)
(i)
Figure 3. Representative trace fossils associated with the appearance of sedimentary fabrics characterized by vertical burrows, leading to a dramatic increase in depth of bioturbation. (a) Diplocraterion parallelum in cross-section view. Dividalen Group, Imobekken, northern Norway. Cambrian Stages 2–3. Scale bar, 2 cm. (b) Diplocraterion parallelum in
bedding-parallel view. Dividalen Group, Imobekken, northern Norway. Cambrian Stages 2–3. Scale bar, 2 cm. (c) Diplocraterion parallelum in cross-section view. Parachilna
Formation, Flinders Ranges, southern Australia. Cambrian Stage 2. Lens cap diameter, 5.5 cm. (d) High density of Diplocraterion parallelum in bedding-plane view. Balka Sandstone, Bornholm, Denmark. Cambrian Stages 2–3. Scale bar, 10 cm. (e) High density of Skolithos linearis in bedding-plane view. St Piran Formation, western Canada. Cambrian
Stages 3–4. (f) Wave-rippled sandstone bed with several specimens of Skolithos linearis. Note associated U-shaped Arenicolites isp. (arrowed). Forteau Formation, western Newfoundland, eastern Canada. Cambrian Stages 3–4. Scale bar, 5 cm. (g) Deep Arenicolites isp. Campanario Formation, northwestern Argentina. Cambrian Stage 4 to Cambrian
Series 3. Lens cap diameter, 5.5 cm. (h) Rosselia isp. St Piran Formation, western Canada. Cambrian Stages 3–4. Coin diameter, 2.3 cm. (i) Syringomorpha nilssoni in an erratic
block. Kiersgoube Pastz, Berlin, Germany. Identical forms are known from Cambrian Stage 2–4 strata in Scandinavia. Scale bar, 1 cm.
the appearance of novel deposit-feeding ichnotaxa. Maximum
alpha ichnodiversity is 28. Ichnodisparity and behavioural complexity are slightly higher than those of Cambrian
Stage 2, with 28 architectural designs recorded globally. No
further increase in degree of bioturbation has been detected
(average 2.4, maximum 6). The fact that the remarkable
increase in global ichnodiversity is not paralleled by an equally
significant increase in ichnodisparity suggests increasing
Proc. R. Soc. B 281: 20140038
(e)
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Ediacaran
Cambrian
Stage 2
Fortunian
N
N
RDS
Mn
matground-dominated
ecology
O2
N
N
P
O2
O2
N
O2 P
O2
suspension feeders as drivers of
diversification of deposit-feeding
strategies
O2
Fe
sediment bulldozing in diffusiondominated benthic systems
suspension feeding in advectiondominated benthic systems
diversity within clades and minor behavioural variations of
previously established architectural plans rather than the
introduction of clades and major behavioural innovations.
This increase in ichnodiversity is roughly coincident with the
bilaterian radiation based on skeletonized animals [2,4].
(e) Cambrian Stage 4
Ichnofaunas from Cambrian Stage 4 show no significant
change in global ichnodiversity, alpha ichnodiversity and ichnodisparity in comparison with those from Cambrian Stage 3
(table 1 and figure 1). An increase in ichnodiversity is apparent
when data are standardized to show ichnodiversity per Myr.
However, this is simply an artefact resulting from the shorter
duration of Cambrian Stage 4 and the lack of biostratigraphic
resolution to differentiate Stages 3 and 4 in some stratigraphic
crucial units. Degree of bioturbation also remains constant.
Based on available data, the most likely interpretation of this
pattern is that near the end of the ‘early’ Cambrian, the evolutionary radiation was essentially over. The body-fossil
record also shows no further significant increase in diversity
and disparity by this time [2,4]. The consistency between the
trace- and body-fossil records provides a strong support to
the accepted timing of the close of the explosion.
4. Discussion
Trace-fossil data strongly support a rapid increase of animal
diversity in the Early Cambrian (i.e. the Cambrian explosion
scenario). However, our systematic analysis also points to the
existence of a relatively short period of phylogenetic fuse
during the terminal Ediacaran and the Fortunian. By the end
of the Fortunian, the diversification event evidenced by the
appearance of complex architectural designs reflecting bodyplan diversification and behavioural innovations was well
under way. Therefore, the trace-fossil record indicates that
the evolutionary radiation occurred earlier than suggested
according to the classic Cambrian explosion scenario based
on the appearance of the main phyla in the body-fossil
record [2,4].
Under detailed scrutiny, the trace-fossil record clearly points
to two major evolutionary breakthroughs—the Fortunian diversification event, and the Cambrian Stage 2 agronomic revolution
that marks the establishment of a Phanerozoic-style ecology
[40]—followed by a positive spillover effect driven by the activities of benthic suspension feeders by Stage 3. In contrast to the
prevailing view that diversification of animals and infaunal
colonization were roughly coincident during the Cambrian
explosion [16], our study indicates that the presence of a wide
array of metazoan behaviours preceded the establishment of a
modern infaunal ecological structure (i.e. mixground ecology),
indicating a decoupling of cladogenesis and the major shift in
benthic ecology that typifies the Phanerozoic.
The Cambrian explosion was characterized by the onset of
ecosystem engineers that were capable of significantly affecting
the physical and chemical environment. Physical changes may
have included structural or architectural activities, sediment
mixing and sediment stabilization, whereas chemical engineering encompassed nutrient transfer and oxygenation of the water
column and sediment [3]. Although some of these changes are
evident from the skeletal fossils (e.g. structural modification
by the formation of reefs) [3], other effects are more difficult to
detect from the body-fossil record. Cambrian soft-bodied
faunas produce additional information to evaluate ecosystem
engineering, but they are absent from 541–521 Ma, a critical
time for evaluating the onset of the explosion. The fact that
trace fossils occur all through this interval, recording the interaction of soft-bodied organisms with the sediment, makes
them ideally suited to evaluate the impact of ecosystem engineers at this critical time, allowing to establish a detailed
chronology of ecological changes.
The Fortunian diversification event and the Cambrian
Stage 2 agronomic revolution undoubtedly have had different impacts from the perspective of ecosystem engineering
(figure 4). The first event involves the appearance of a wide
repertoire of behavioural strategies reflecting the interactions
of newly developed, distinctive body plans with the substrate. Most of these interactions were characterized by the
reworking of fine-grained sediments by sediment bulldozers
in diffusion-dominated benthic systems [41], as typified by
bioturbation in offshore deposits. This style of biogenic
reworking was probably conducive to large-scale changes
in both the sediment and the water column, including promotion of water fluxes at the sediment –water interface,
average deepening of the redox discontinuity surface, release
of nitrogen from the sediment, increase in the sediment –
water flux of iron and manganese, and several-fold increase
in seawater sulfate concentration [41,42]. By being the primary
determinant of oxygen concentration in the sediment, bioturbation may have also influenced the biomass of organisms,
the expansion of aerobic bacteria, the rate of organic matter
decomposition and the regeneration of nutrients vital for primary productivity, among other aspects [43–45]. However,
the exploitation of matgrounds, a typical Ediacaran strategy,
largely persisted during the Fortunian, probably as a result of
the low levels of bioturbation. The restriction of most
Proc. R. Soc. B 281: 20140038
Figure 4. Evolutionary changes in benthic faunas and ecosystem engineering through the Ediacaran – Cambrian transition. Note deepening of the redox discontinuity
surface (RDS) and complex feedback loops.
7
rspb.royalsocietypublishing.org
onset of mixground ecology
(coupling of plankton and benthos)
increase in ocean ventilation
large-scale changes in
sediment and water column
SO4
Cambrian
Stage 3
Downloaded from http://rspb.royalsocietypublishing.org/ on June 18, 2017
Acknowledgements. We thank reviewers of Proc. R. Soc. B Nic Butterfield
and Jonathan Antcliffe, and editors Gary Carvalho and Norman
Macleod for their useful comments. Doug Erwin and Nic Minter
critically read an early version of this manuscript and provided
valuable feedback. A large number of colleagues showed us outcrops
and collections, namely John Almond, Richard Callow, Peter Crimes,
Jim Gehling, Gerard Germs, Liam Herringshaw, Richard Jenkins,
Sören Jensen, Alex Liu, Duncan McIlroy, Guy Narbonne, Brian
Pratt and Dolf Seilacher, further helping to shape our view on
Ediacaran– Cambrian ichnology.
Funding statement. Financial support for this study was provided by
Natural Sciences and Engineering Research Council (NSERC) Discovery grants nos 311727-05/08 and 311726-05/08/13, awarded to
Mángano and Buatois, respectively.
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