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The evolutionary events during the Ediacaran–Cambrian transition (~541 Myr ago) are unparalleled in Earth history. The fossil record suggests that most extant animal phyla appeared in a geologically brief interval, with the oldest unequivocal bilaterian body fossils found in the Early Cambrian. Molecular clocks and biomarkers provide independent estimates for the timing of animal origins, and both suggest a cryptic Neoproterozoic history for Metazoa that extends considerably beyond the Cambrian fossil record. We report an assemblage of ichnofossils from Ediacaran–Cambrian siltstones in Brazil, alongside U–Pb radioisotopic dates that constrain the age of the oldest specimens to 555–542 Myr. X-ray microtomography reveals three-dimensionally preserved traces ranging from 50 to 600 μ m in diameter, indicative of small-bodied, meiofaunal tracemakers. Burrow morphologies suggest they were created by a nematoid-like organism that used undulating locomotion to move through the sediment.This assemblage demonstrates animal–sediment interactions in the latest Ediacaran period, and provides the oldest known fossil evidence for meiofaunal bilaterians. Our discovery highlights meiofaunal ichnofossils as a hitherto unexplored window for tracking animal evolution in deep time, and reveals that both meiofaunal and macrofaunal bilaterians began to explore infaunal niches during the late Ediacaran.
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DOI: 10.1038/s41559-017-0301-9
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1 Palaeobiology, Royal Ontario Museum, 100 Queen’s Park, Toronto, Ontario M5S 2C6, Canada. 2 Department of Ecology and Evolutionary Biology, University
of Toronto, 25 Willcocks Street, Toronto, Ontario M5S 3B2, Canada. 3 Instituto de Geociências, Universidade de São Paulo, Rua do Lago, 562, 05508-080
São Paulo, Brazil. 4 NERC Isotope Geosciences Laboratory, British Geological Survey, Keyworth, Nottinghamshire NG12 5GG, UK. 5 School of Earth and
Environmental Sciences, University of Manchester, Manchester M13 9PL, UK. 6 Department of Earth Sciences, Natural History Museum, Cromwell Road,
London SW7 5BD, UK. 7 Department of Earth Sciences, Memorial University of Newfoundland, Alexander Murray Building, 300 Prince Philip Drive, St. John’s,
Newfoundland and Labrador A1B 3X5, Canada. 8 Department of Earth Sciences, University of Oxford, South Parks Road, Oxford OX1 3AN, UK.
9 Departamento de Geofisica, Instituto de Astronomia, Geofísica e Ciências Atmosféricas, Universidade de São Paulo, Rua do Matão 1226, 05508-900
São Paulo, Brazil. 10 Department of Biology, Federal University of São Carlos. Rodovia João Leme dos Santos - Parque Reserva Fazenda Imperial, Km 104,
18052780 Sorocaba, Brazil. 11 Department of Earth Sciences, University of Cambridge, Downing Street, Cambridge CB2 3EQ, UK. Martin D. Brasier is
deceased. *e-mail: lparry@rom.on.ca
The Lower Cambrian fossil record documents a major radia-
tion of macroscopic animals (particularly bilaterian phyla),
coupled with significant expansion of their behavioural inter-
actions with substrates and other organisms1,2. However, a growing
catalogue of evidence from body fossils, trace fossils, biomarkers
and molecular clocks indicates a protracted Neoproterozoic history
for the Metazoa, with the origin of animals significantly pre-dating
the base of the Cambrian3.
A range of biological phenomena typically associated with ani-
mals first appears during the late Ediacaran interval (~580–541 Myr
ago (Ma)), including skeletogenesis4, reef building5 and macroscopic
predation6. Body fossils of late Ediacaran macro-organisms include
at least some early animals3, but crucially, most plausible claims
for metazoans lie within the diploblasts rather than the Bilateria3.
Kimberella, which is potentially a stem mollusc7, is a notable excep-
tion, but some authors suggest that it can only be reliably considered
as a member of total group Bilateria3.
Our understanding of early animal evolution is complemented
by ichnological investigations of latest Ediacaran to Ordovician
strata1,2,8. Diverse ichnofossil assemblages in the earliest Cambrian
place an important constraint on the tempo of bilaterian origins, as
they indicate that some groups, including total group panarthropods
and priapulid-like scalidophorans2,9, were globally distributed and
abundant by this point. The major bilaterian divergences (that is,
the protostome–deuterostome and ecdysozoan–lophotrochozoan
divergences) must therefore pre-date the Ediacaran–Cambrian
boundary. So far, the Ediacaran trace fossil record has provided lim-
ited insight into these early divergences. Most Ediacaran ichnofossils
are either surface traces or simple under-mat burrows, created either
on or immediately beneath matgrounds10. Such traces extend back
to ~565 Ma11,16, including inferred grazing traces (Kimberichnus12)
associated with the body fossil Kimberella, vertical adjustment
structures in response to seafloor aggradation13 and, in the latest
Ediacaran, shallow vertical burrows10 and treptichnid-like burrows
just below the Ediacaran–Cambrian boundary14. Most Ediacaran
ichnofossils are considered to have been made by total group
bilaterian15 or cnidarian13,16 eumetazoans. Notwithstanding con-
troversial claims for bioturbation and complex burrows ~553 Ma17,
widespread substrate-penetrating burrows capable of significant
sediment mixing do not appear until close to the Precambrian–
Cambrian boundary14.
Molecular clock analyses predict an earlier, pre-Ediacaran ori-
gin for the Metazoa and Eumetazoa, and an early Ediacaran origin
for Bilateria, Protostomia and Deuterostomia18. Palaeontological
Ichnological evidence for meiofaunal bilaterians
from the terminal Ediacaran and earliest Cambrian
of Brazil
Luke A. Parry 1,2*, Paulo C. Boggiani3, Daniel J. Condon 4, Russell J. Garwood 5,6, Juliana de M. Leme3,
Duncan McIlroy7, Martin D. Brasier8, Ricardo Trindade9, Ginaldo A. C. Campanha3,
Mírian L. A. F. Pacheco10, Cleber Q. C. Diniz3 and Alexander G. Liu 11
The evolutionary events during the Ediacaran–Cambrian transition (~541 Myr ago) are unparalleled in Earth history. The fossil
record suggests that most extant animal phyla appeared in a geologically brief interval, with the oldest unequivocal bilaterian
body fossils found in the Early Cambrian. Molecular clocks and biomarkers provide independent estimates for the timing of
animal origins, and both suggest a cryptic Neoproterozoic history for Metazoa that extends considerably beyond the Cambrian
fossil record. We report an assemblage of ichnofossils from Ediacaran–Cambrian siltstones in Brazil, alongside U–Pb radioiso-
topic dates that constrain the age of the oldest specimens to 555–542 Myr. X-ray microtomography reveals three-dimensionally
preserved traces ranging from 50 to 600 μ m in diameter, indicative of small-bodied, meiofaunal tracemakers. Burrow morphol-
ogies suggest they were created by a nematoid-like organism that used undulating locomotion to move through the sediment.
This assemblage demonstrates animal–sediment interactions in the latest Ediacaran period, and provides the oldest known
fossil evidence for meiofaunal bilaterians. Our discovery highlights meiofaunal ichnofossils as a hitherto unexplored window for
tracking animal evolution in deep time, and reveals that both meiofaunal and macrofaunal bilaterians began to explore infaunal
niches during the late Ediacaran.
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support for these suggestions is limited to purported body fossils
of sponges19 and demosponge biomarkers20. A considerable gap
therefore remains between the fossil record of the late Ediacaran
and molecular clock estimates for deep splits in the animal tree, for
example the origin of Metazoa and Eumetazoa3. Assuming that con-
temporary molecular clock analyses yield accurate, if imprecise18,
node ages for animal divergences, a small body size and concomi-
tant limited fossilization potential21 could reconcile these discordant
records of animal evolution (but see ref. 22).
The small body size of the ancestral bilaterian is supported by
recent phylogenomic analyses of deep animal relationships, with
acoel flatworms and xenoturbellids (Xenacoelomorpha) being a
sister group to all remaining bilaterians (Nephrozoa)23, and small-
bodied spiralian taxa (the ‘Platyzoa’) recognized as a paraphyletic
grade with respect to macroscopic trochozoans24. This suggests that
early bilaterians and spiralians were small bodied, possibly meiofau-
nal, and moved using ciliary gliding.
Meiofauna comprises all organisms between 32 and 1,000 μ m in
size that inhabit pore-water-rich sediments in freshwater to deep-
marine environments25. Modern meiofaunal communities include
animals, foraminifera and some ciliates, and contribute significantly
to sediment bioturbation and bioirrigation26,27. The meiofauna can be
divided into permanent members (that is, animals with organisms of a
small size adapted and restricted to the meiofaunal, interstitial realm)
and temporary meiofauna (for example, the larvae of macrobiota)25.
Despite its ecological and evolutionary importance, the deep-
time record of the meiofauna has received little discussion, prin-
cipally due to the low preservation potential of both meiofaunal
body fossils and traces. Although meiofaunal burrows (some-
times described as burrow mottling or cryptobioturbation) have
occasionally been reported from Cambrian to Recent sediments26,
they are rarely subjected to detailed study. Body fossil discoveries
also reveal organisms inhabiting meiofaunal niches within Early
Cambrian communities, highlighting the potential for their preser-
vation within particular taphonomic windows28,29.
Here we report a new assemblage of meiofaunal ichnofossils from
siltstones of the Ediacaran–Cambrian Tamengo and Guaicurus for-
mations, Corumbá Group, central western Brazil (Fig.1). The age of
the assemblage is constrained by U–Pb (zircon) isotope dilution ther-
mal ionization mass spectrometry (ID-TIMS) dating of inter-stratified
ash beds. The dates indicate that the Tamengo Formation specimens
are late Ediacaran in age, and those in the Guaicurus Formation lie
close to the Ediacaran–Cambrian boundary. Our results constitute the
oldest documented meiofaunal burrows in the geological record, plac-
ing a constraint on the minimum age of this key ecological innovation.
The Corumbá Group
The Corumbá Group, part of the Southern Paraguay Belt, is a
~600-m-thick sedimentary unit comprising carbonate and silici-
clastic facies deposited on a stable continental margin following a
late Neoproterozoic rift event30,31 (Fig.1). The lowermost units of
the Corumbá Group are the terrigenous Cadieus and Cerradinho
formations, which are probably contemporaneous with the Puga
Formation of the Amazon Craton30 (and thus possibly Marinoan-
equivalent). Stromatolitic dolostones and phosphorites of the
Bocaina Formation lie above those siliciclastic units. The lower
Corumbá Group is unconformably overlain by the fossiliferous dark
organic-rich marls and limestones of the Tamengo Formation, and
laminated siltstones of the Guaicurus Formation31 (Fig.1). A breccia
horizon marks the base of the Tamengo Formation in several sec-
tions, and is concordantly overlain by interbedded mudstones and
grainstones deposited in a shallow platform setting. The laminated
calcareous siltstones of the Guaicurus Formation indicate deposi-
tion in a setting with low hydrodynamic energy, probably below
fair-weather wave base. The sedimentary succession has previously
yielded macroscopic body fossils including the scyphozoan-like
Corumbella werneri and Paraconularia4, along with Cloudina lucia-
noi, in the upper Tamengo Formation, and possible vendotaenid
algae (Eoholynia) in the lowermost Guaicurus Formation31 (Fig.1).
Results
U–Pb geochronology. Three volcanic tuff horizons were sampled
within the Corumbá Group (Fig.1) and zircons from these tuffs
were dated using U–Pb chemical abrasion ID-TIMS (CA-ID-TIMS)
methods (see Methods for full methodology). An ash bed from the
top of the Bocaina Formation (from Porto Morrinhos; Fig.1) yielded
a weighted mean 206Pb/238U date of 555.18 ± 0.30/0.34/0.70 Ma
(mean square weighted deviation (MSWD) = 1.6, n = 8 out of 8)
(Supplementary Fig.6; Supplementary Tables3 and 4), which we
consider to approximate the age of the sample. This date provides
a maximum age for the overlying Tamengo Formation. Two fur-
ther ash beds (samples 1.08 and 1.04) were collected from the top
of the Tamengo Formation. Zircons from sample 1.04 yielded U–Pb
CA-ID-TIMS dates that ranged from 541.2 to 548 Ma, with a clus-
ter of the five youngest concordant analyses defining a weighted
mean 206Pb/238U date of 541.85 ± 0.75/0.77/0.97 Ma (MSWD = 3.3,
n = 5 out of 11) (Supplementary Fig. 6; Supplementary Tables 3
and 4) that we consider approximates the age of the sample.
Zircons from sample 1.08 yielded U–Pb CA-ID-TIMS dates that
ranged from 537 to 552 Ma, with a coherent cluster of four con-
cordant analyses (Fig. 2) defining a weighted mean 206Pb/238U
date of 542.37 ± 0.28/0.32/0.68 Ma (MSWD = 0.68, n = 4 out of 8)
(Supplementary Fig.6; Supplementary Tables3 and 4). We consider
the single significantly older data point to result from the incorpo-
ration of xenocrystic zircon, perhaps during eruption. The three
younger 206Pb/238U dates from sample 1.08 are considered to reflect
Pb loss based on the observations that (1) they are non-overlapping;
(2) the 207Pb/206Pb dates are similar to those that define the ~542 Ma
population in both this sample and sample 1.04; and (3) the derived
dates from both upper Tamengo Formation samples are consistent.
Therefore 542.37 ± 0.28/0.32/0.68 Ma is taken to approximate the
age of sample 1.08. The data from samples 1.04 and 1.08 indicate an
age of ~542 Ma for the top of the Tamengo Formation, constraining
the age of the upper Corumbá Group as late Ediacaran (uppermost
Bocaina–Tamengo formations, 555–542 Ma) to earliest Cambrian
(lower Guaicurus Formation, < 542 Ma). The current accepted age
for the base of the Cambrian is 541.00 ± 0.29 Ma32 (level Y uncer-
tainty, excluding the systematic 238U decay constant uncertainty).
Trace fossils of the Guaicurus and Tamengo formations. Three-
dimensionally mineralized fossils were collected from approxi-
mately 30–40 m above the base of the Tamengo Formation at two
levels in the Ladário section (Fig.1), and from a single horizon and
loose material ~7 m above the base of the Guaicurus Formation from
the Laginha Mine section (Fig.1). The latter horizon is < 542.0 Ma in
age based on the U–Pb CA-ID-TIMS data presented above.
Bi-lobed horizontal, iron-oxide-filled ichnofossils occur in a sin-
gle hand specimen, preserving part and counterpart, derived from
float in the lower Guaicurus Formation (Fig.2c,d). The burrows are
straight to curving, approximately 2 mm in width, and exhibit dor-
sal and ventral median depressions, creating the bi-lobed appear-
ance typical of Didymaulichnus lyelli33.
Small sub-horizontal structures occur in abundance in both the
lower Guaicurus (Fig.2) and Tamengo formations (Fig.3). These
consist of irregular multi-tiered networks connected by short
sub-vertical shafts. In bedding plane view, the fossils are dark in
colour relative to the matrix, forming dense assemblages compris-
ing sinuous structures with rare dichotomous branches (Fig.2a,b).
The fossils are filled with oxidized iron-rich minerals with fram-
boidal morphologies, and authigenic microcrystalline calcite
(Fig.2eh). Framboids suggest that the fossils were originally pyri-
tized, and subsequently oxidized to iron oxides and oxyhydroxides
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(Supplementary Fig. 1). The presence of calcite and framboids
throughout the infill suggests that the framboids and calcite formed
at a similar time.
The density contrast between the fossils and the host rock allows
the traces to be visualized through X-ray microtomography (μ CT;
Figs.35), revealing a dense ichnofabric (Figs.3eg, 4e,f and 5f).
Amazon Craton
Brazil
58°
16°
56°
22°
Craton/mobile
belt limit
Corumbá
Urucum
Massif
Porto
Morrinhos
0 20 km
Rio Apa
Block
Cenozoic sediment and cover
Araras Group
Corumbá Group
Itapucumi Group
Puga Formation/Cuiabá Gr
oup
Serra da Bodoquena
Laginha
Mine
Granitic gneiss basement
Cenozoic sediment and Palaeozoic cover
Corumbá Group
Guaicurus Formation (pelite)
Tamengo Formation
(organic limestone and shale)
Bocaina Formation
(stromatolites dolostone)
Urucum Formation (Jacadigo Group)
(arkose)
Corumbá
Sobramil Harbour
Ladário
Paraguay
River
Corcal
Bolivia
Brazil
30
25
15
20
20
30
30
25
30
km
02
BR-262 road
Laginha Syncline
Guaicurus
Formation
Tamengo
Formation
Bocaina
Formation
Cerradinho
& Cadieus
formations
Phosphorite 555.18 ± 0.3 Ma
Mudstone/organic shale rhythmite
Ichnofossils
Ichnofossils
Siltstone
Mudstone
Grainstone
Dolomite
Sandstone
Conglomerate
Organic shale
Erosive discordance
Corumbella
Vase-shaped
microfossils
Cloudina
Paraconularia
Eoholynia
corumbensis
Stromatolite
Slump
Ooids
Diamictite
Post-riftRift
541.85 ± 0.75 Ma
542.37 ± 0.28 Ma
b
a
Key
400 m
0
– 2 + 2 %
d13CPDB
Fig. 1 | Locality map and stratigraphic column of the Ediacaran–Early Cambrian Corumbá Group: composite section compiled from logs in the Corumbá–
Ladário region, Mato Grosso do Sul State, Brazil. a,b, Locality map (a) and stratigraphic column (b). Dates are derived from this study. White stars
indicate localities from which samples for geochronology were obtained. Black stars indicate ichnofossil localities described in this study: Laginha Mine
(Guaicurus Formation) 19° 07 09.8 S, 057° 38 40.4 W; Ladário (Tamengo Formation) 19° 0 04.0 S, 57° 36 00.7 W. Carbon isotope stratigraphy
comes from the Laginha Mine section52. Age uncertainties are expressed as MSWD.
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Although many of the burrows are restricted to single horizons, some
cut across up to ~7 mm of stratigraphic thickness, indicating inter-
stratal burrowing (Fig.4g). Burrow diameters range from 45 to 573 µ m
(Fig.5g; mean = 193.2 µ m, n = 393). The Shapiro–Wilks test indicates
these data are not drawn from a normal distribution (P < 0.01), and
univariate Bayesian information criterion (BIC) analysis supports
either a two- or three-component model. The lower limits of this
distribution are probably dictated by the voxel size of the scans and
so it is possible that the smallest size fractions are omitted.
Discussion
The Guaicurus Formation assemblage is dated at < 541.85 ± 0.77 Ma
and is broadly contemporaneous with the Ediacaran–Cambrian
boundary32. The Tamengo Formation ichnofossils lie stratigraphi-
cally below our dated horizon of 542.37 ± 0.32 Ma, and are thus
between 542 and 555 Ma in age (late Ediacaran). The presence of dif-
ferent size classes within the Corumbá Group data indicates different
populations, further supporting a biological, rather than abiological,
mode of formation (seeSupplementary Information). As the struc-
tures are preserved as discrete, rounded authigenically mineralized
tubes, they cannot be shrinkage features such as synaeresis cracks.
A body fossil explanation for these structures is considered
unlikely as authigenically mineralized body fossils (for example,
algal filaments) would be expected to be confined to discrete hori-
zons in finely laminated sediments rather than crossing multiple
horizons. Some Ediacaran body fossils, such as the simple conical
Conotubus, can grow through sedimentary laminae if felled34. In
contrast, the branching ichnofossils of the Guaicurus Formation are
~0.5 mm wide and cross up to ~7 mm of stratigraphic thickness.
The contemporaneous (Fig.1) vendotaenid alga Eoholynia corum-
bensis is superficially similar in size and morphology to the ichno-
fossils described herein31. Two factors make algal origins for the
fossils we describe unlikely: mode of preservation, and morphology.
First, in contrast to these authigenically mineralized trace fossils,
Eoholynia specimens in the Corumbá Group are preserved as two-
dimensional (2D) carbon films with some accessory oxides (possi-
bly after pyrite) (Supplementary Fig.5d–f). A comprehensive study
of early Palaeozoic non-biomineralized macroalgal taxa found that
2D compression (with some accessory mineralization) is the only
taphonomic pathway through which macroalgae fossilize during
this time interval35, consistent with the algal affinities of Eoholynia
and similar fossils. Although taphonomic mode should not be con-
flated with affinity, the absence of three-dimensionally pyritized
algae from similar localities of the same age renders an algal affin-
ity for the proposed ichnofossils unlikely. Secondly, Eoholynia have
straight branches (rather than undulating/sinusoidal) that taper
after regular (dichotomous to polychotomous) branching from a
distinct main branch and have rounded terminal structures inter-
preted as sporangia31. Polychotomous branching, tapering and
rounded termini are not present in the ichnofossils.
Iron oxides form a patina on the outer margin of some larger
endichnial burrows, possibly reflecting pyritization of a mucous bur-
row lining36 (Fig.2e). 3D preservation as authigenic pyrite and calcite
suggests that the burrows were open prior to burial and compaction,
and were not backfilled by the tracemaker. Preservation in almost
undistorted full relief is uncommon in mudstones in the absence of
burrow fill, except where significant early diagenesis and dewater-
ing occurs before burial36. Similar sized burrows of modern nema-
todes possess a polysaccharide-rich mucous burrow lining37, which
would provide a locus for the microbial reduction of sulfate from
seawater within the burrows, causing pyrite precipitation and con-
sequently burrow preservation38: a mechanism we consider to have
been responsible for preservation of the Corumbá Group structures.
The poorly organized, vertically stacked, network-like galler-
ies connected by short oblique shafts are typical of the ichnoge-
nus Multina. A combination of size range and irregularly sinuous
gallery morphology allows attribution to M. minima39. The small
burrow diameter, originally circular cross-sections and lack of
dorso-ventral differentiation characteristic of the Corumbá Group
Multina are consistent with a narrow-bodied vermiform trace-
maker. It is unclear how many infaunalization events are repre-
sented by the assemblages reconstructed in 3D (for example,
Fig.5e), but the presence of continuous oblique shafts between
levels suggests that the burrows remained open throughout the life
of the tracemaker.
Animal burrowing is typically achieved either (1) by peristal-
sis (for example, in annelids like the Arenicolidae); (2) through
the extension and retraction of an introvert (for example, loric-
iferans, kinorynchs, sipunculans); or (3) by a combination of the
two (for example, priapulids)40. These mechanisms compact sedi-
ment laterally at the burrow margins41, but such compaction is
absent in the Guaicurus traces (Fig.2eg). Compression burrow-
ing is similar and involves the tracemaker forcing its way through
the sediment, compacting it at the margins42. Trochozoan taxa
a
b
c
d
e
f g h
10 mm
10 mm
10 mm
10 mm 100 µm
400 µm100 µm200 µm
Fig. 2 | Hand specimens and scanning electron microscopy
photomicrographs of M. minima and D. lyelli traces from the Guaicurus
Formation, Laginha Mine, Mato Grosso do Sul State, Brazil. a, Hand
specimen of small M. minima, OUMNH ÁU.4c. b, Bedding plane view of
M. minima (inset of a). c,d, Bedding plane view of bi-lobed D. lyelli (part
and counterpart, OUMNH ÁU.2). eh, Scanning electron microscopy
photomicrographs of bedding-normal polished thin sections of samples
containing M. minima. Framboidal iron oxide (originally pyrite) burrow fills
are clearly observed. Burrows in eg are viewed in cross-section through
the burrow diameter. h, A burrow in lateral view.
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such as annelids, molluscs and nemerteans can be excluded as
potential tracemakers because the minimum diameter M. minima
resolved in the Guaicurus Formation is ~45 μ m; significantly
smaller than recently hatched trochophore larvae, which are
approximately 100 μ m in diameter and pelagic, not endobenthic43.
Annelids can be further excluded as potential tracemakers as the
smallest annelid eggs (50–70 μ m diameter43) exceed the diameter
of the smallest traces.
Early spiralians may have been small bodied, with taxa such
as gastrotrichs and gnathiferans recovered as a paraphyletic grade
in phylogenomic analyses24. Many spiralian meiofaunal groups
move using ciliary gliding, which is unlikely to have formed con-
tinuous open burrows or achieved the sediment movement respon-
sible for interstratal burrowing. Mucociliary gliding by extant
platyhelminths44 creates traces similar in gross morphology to
horizontal Ediacaran trails, and so members of the total groups of
Bilateria, Xenacoelomorpha and Nephrozoa are candidate trace-
makers for late Ediacaran surficial traces. Ciliary gliding has prob-
ably been independently lost multiple times within Nephrozoa (for
example, Ecdysozoa, which lack external ciliation). Ciliary gliding
is retained in some macroscopic spiralians, including Nemertea,
Platyhelminthes and molluscan classes in which the foot is used in
locomotion, such as gastropods. Nevertheless, ciliary gliding was
the probable locomotory mechanism for the last common ances-
tor of both Bilateria and Nephrozoa. Ciliary gliding is unlikely to
produce open burrows in fine-grained sediments and in the meio-
fauna it is most commonly used by organisms that live in interstitial
spaces between sand grains.
ab
cd
ef
g
10 mm
1 mm
1 mm
1 mm
1 mm1 mm
5 mm
Fig. 3 | Photographs and CT volume renders of M. minima burrows from the Ediacaran Tamengo Formation, Ladário, Mato Grosso do Sul State, Brazil.
a, Representative hand specimen of Tamengo Formation samples, specimen GPIE 11048b. bd, Oxidized burrows with sub-horizontal trajectories, viewed
in plan view on a bedding surface, GPIE-11048b (b), GPIE-11004b (c) and GPIE-11005a (d). Note that these specimens have been heavily weathered.
eg, Volume renders of CT slice data through the burrows constructed using the program Drishti. The burrows show curved, sub-horizontal trajectories,
and are mostly < 100 µ m in diameter.
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Free-living nematodes use undulating motions to move through
fine-grained soft sediments, the low viscosity of which limits them
to small body size45. Organisms without body appendages possessing
only longitudinal muscles, such as nematodes46, are restricted
to sinusoidal locomotion as they lack the antagonistic circular
muscles necessary for peristalsis. Nematodes are common biotur-
bators of modern muddy sediments and can create open mucus-
lined burrows of a size range comparable to that of the Brazilian
M. minima (Fig.5g). Similar but slightly larger M. minima, poten-
tially attributable to marine nematodes, have been described from
the Cambrian and Ordovician47,48, but do not preserve the tiered
networks of M. minima we report. Burrow morphologies pro-
duced by extant or extinct nematomorphs are unknown.
The size and morphology of the meiobenthic Multina is consis-
tent with a nematoid-like tracemaker that lacked body appendages
and did not move by peristalsis or ciliary gliding. As the ancestral
bilaterian and nephrozoan moved using ciliary gliding, this burrow-
ing style suggests a tracemaker that phylogenetically postdates the
nephrozoan crown node. These burrows may potentially provide an
age constraint for total group Nematoida (that is, nematodes plus
nematomorphs). This is consistent with Early Cambrian body fos-
sils, which include representatives of most ecdysozoan phyla, along
with meiofaunal groups28. Total group nematoids are therefore likely
to have diverged from their closest living relatives by at least 520 Ma,
regardless of their controversial position within Ecdysozoa49. An
alternative interpretation is that these trace fossils were produced
by a stem group ecdysozoan that phylogenetically pre-dates the evo-
lution of an introvert but had already evolved a chitinous cuticle
and thus was unable to use ciliary gliding. A similar body plan is
present in larval insects, which produce freshwater and terrestrial
Cochlichnus burrows and move in a similar fashion to nematodes10.
The Proterozoic–Phanerozoic biological radiation and the ori-
gin of the meiofauna. The Corumbá Group trace fossils place an
important latest Ediacaran (541–555 Ma) minimum constraint
on the origin of meiofaunal animals and their interactions with
soft substrates. Meiofauna are ubiquitous in both modern marine
and freshwater environments, and their origin in deep time has
been often discussed21,22 but little explored from an evidential
palaeontological perspective. Extant meioendobenthic organ-
isms are particularly important contributors to biogeochemical
cycling, microbial ecology and ecosystem productivity, especially
in muddy sediments27,37. Multiple studies discuss the trace fossil
record of macrofaunal behaviour from the late Ediacaran onwards,
its postulated impacts on sediment geochemistry and benthic ecol-
ogy, and its role in ecosystem engineering and ecological escala-
tion1,2,8. Constraining the deep time origins of a meiofaunal mode
of life may be equally important for understanding the biological
and chemical evolution of marine sedimentary environments. It is
unlikely that the meiofaunal burrowing described here had a sub-
stantial impact on substrate mixing, due to its small depth of pene-
tration leaving sedimentary laminae largely undisturbed (Fig.4e).
10 mm 10 mm
a
b
c
de
20 mm
20 mm
f
Fig. 4 | CT slices and 3D reconstructions of a burrow assemblage in specimen OUMNH ÁU.3 from the Early Cambrian/latest Ediacaran Guaicurus
Formation. ac, Representative CT X-ray slices through the specimen in plan view, showing burrows in light grey against a dark grey rock matrix. Scale bar
in a also applies to b and c. d, 3D render of the specimen produced using Blender, showing individual burrows in different colours. e, The same CT data
volume rendered in Drishti, with burrows in gold. f, Drishti volume render normal to bedding, showing interstratal burrowing.
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Our geochronological framework places temporal constraints
on the first appearance of several biological and ecological
innovations in the South American fossil record, and permits
correlation of these events to other dated sections worldwide
(Fig.6). Biomineralizing macro-organisms (Cloudina), annulated
tubular macrofossils (Corumbella) and meiofaunal burrowers
all appear in the Corumbá sections after 555 Ma, but before
542 Ma. The temporal range for the macrofossils corresponds
well to similar latest Ediacaran fossil assemblages, some of
which record evidence for predation50, a decline in Ediacaran soft-
bodied macro-organisms51 and the appearance of macroscopic
burrows10,17 in the interval immediately preceding the Ediacaran–
Cambrian boundary. Taken together, these records bear witness
to several major biological innovations among eumetazoans,
indicating that this key interval may offer significant scope for
unravelling the intricacies surrounding the early stages of bilat-
erian evolution.
Methods
U–Pb geochronology. U–Pb dates were obtained by the CA-ID-TIMS method
on selected single zircon grains (Supplementary Tables3 and 4), extracted from
an aliquot of samples ‘Porto Morrinhos’, ‘1.04’ and ‘1.08’. Zircon grains were
a
b
c
d
e
f(ii)
(iii) (iv)
(iv) (v)
(i)
10 mm
10 mm
10 mm
n = 393
60
50
40
30
Frequency
Density
20
10
0
0100 200300
Burrow diameter (
µ
m)
400500 600
0.007
0.006
0.005
0.004
0.003
0.002
0.001
0.000
g
Fig. 5 | Specimen OUMNH ÁU.4/p1 from the Guaicurus Formation from which burrow measurement data were obtained. a, Hand specimen from
the Laginha Mine section, plan view. b, Drishti volume render of 3D CT scan data, plan view. c,d, Individual CT slices in plan view, from which burrow
measurements were obtained via comparison of 3D volume render to determine the maximum diameter of each burrow. Scale bar as in b. e, The Drishti
volume render in b in lateral view. f, Individual burrow morphologies extracted from the volume render in b. g, Histogram plotting burrow width
against frequency.
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isolated from the rock samples using standard magnetic and density separation
techniques, and annealed in a mue furnace at 900 °C for 60 h in quartz beakers.
Zircon crystals from sample Porto Morrinhos have aspect ratios varying from
~2 to ~5 and are typically 150 to 300 μ m in their longest dimension, and oen
contained a medial melt inclusion typical of volcanic zircon. Zircon from samples
1.04 were smaller, with the long dimension of the order of 50 to 100 μ m,
with lower aspect ratios (~2) and were doubly terminated. Zircon from samples
1.08 had aspect ratios ranging from 2 to 4, long dimension of the order of 100
to 200 μ m and were doubly terminated. No cathodoluminescence imaging was
undertaken due to the small size of the zircons, and because the presence of
medial melt inclusions and the general external morphologies were indicative
of inherited cores not being present. Zircons selected for analyses based on
external morphology were transferred to 3 ml Teon PFA beakers, washed
in dilute HNO3 and water, and loaded into 300 μ l Teon PFA microcapsules.
Fieen microcapsules were placed in a large-capacity Parr vessel, and the crystals
partially dissolved in 120 μ l of 29 M HF for 12 h at 180 °C. e contents of each
microcapsule were returned to 3 ml Teon PFA beakers, the HF removed and
the residual grains immersed in 3.5 M HNO3, ultrasonically cleaned for an hour,
and uxed on a hotplate at 80 °C for an hour. e HNO3 was removed and the
grains were rinsed twice in ultrapure H2O before being reloaded into the same
300 μ l Teon PFA microcapsules (rinsed and uxed in 6 M HCl during crystal
sonication and washing) and spiked with the EARTHTIME mixed 233U–235U–205Pb
tracer solution (ET535). ese chemically abraded grains were dissolved in
Parr vessels in 120 μ l of 29 M HF with a trace of 3.5 M HNO3 at 220 °C for 60 h,
dried to uorides and then re-dissolved in 6 M HCl at 180 °C overnight. U and
Pb were separated from the zircon matrix using an HCl-based anion exchange
chromatographic procedure, eluted together and dried with 2 μ l of 0.05 N H3PO4.
Pb and U were loaded on a single outgassed Re lament in 5 μ l of a silica gel/
phosphoric acid mixture53, and U and Pb isotopic measurements made on a
ermo Triton multi-collector thermal ionization mass spectrometer equipped
with an ion-counting secondary electron multiplier (SEM) detector. Pb isotopes
were measured by peak-jumping all isotopes on the SEM detector for 100 to 150
cycles. Pb mass fractionation was externally corrected using a mass bias factor of
0.14 ± 0.03% per mass unit determined via measurements of 202Pb/205Pb (ET2535)-
spiked samples analysed during the same experimental period. Transitory isobaric
interferences due to high-molecular-weight organics, particularly on 204Pb,
disappeared within approximately 30 cycles or earlier, and ionization eciency
averaged 104 cps pg1 of each Pb isotope. Linearity (to 1.4 × 106 cps) and the
associated deadtime correction of the SEM detector were monitored by repeated
analyses of NBS982, and have been constant since installation in 2006. Uranium
was analysed as UO2 + ions in static Faraday mode on 1012 Ω resistors for 150 to
200 cycles, and corrected for isobaric interference of 233U18O16O on 235U16O16O
with an 18O/16O ratio of 0.00206. Ionization eciency averaged 20 mV ng1 of each
U isotope. U mass fractionation was corrected using the known 233U/235U ratio of
the ET2535 tracer solution.
We used the ET535 tracer solution54,55 and U decay constants recommended
in ref. 56. A value of 137.818 ± 0.045 was used for the 238U/235Uzircon based on
the work of ref. 57. 206Pb/238U ratios and dates were corrected for initial 230Th
disequilibrium using a Th/Umagma = 3 ± 1 resulting in an increase in the 206Pb/238U
dates of ~0.09 Myr. All common Pb in analyses was attributed to laboratory blank
and subtracted based on the measured laboratory Pb isotopic composition and
associated uncertainty. U blanks were estimated at 0.1 pg, based on replicate total
procedural blanks.
Here, the date uncertainties reporting is as X/Y/Z and reflects the following
sources: (X) analytical, (Y) analytical + tracer solution and (Z) analytical + tracer
solution + decay constants. The X uncertainty is the internal error based on only
analytical uncertainties, including counting statistics, subtraction of tracer solution,
and blank and initial common Pb subtraction. It is given at the 2σ confidence
interval. This error should be considered when comparing our dates with 206Pb/238U
dates from other laboratories that used the same EARTHTIME tracer solution
or a tracer solution that was cross-calibrated using related gravimetric reference
materials. The Y uncertainty includes uncertainty in the tracer calibration and
538540542
544546548
550
552
554556558560562
564
566568570
Ediacaran Cambrian
Ash bed age ± age uncertainty (2σ),
number refers to cited reference. Inferred time interval for which
there is no stratigraphic record
Meiofaunal trace fossils
Macro-surface and/or under-
mat mining trace fossils
Macro-burrow trace fossils
Weakly calcified tubes Ediacaran soft-bodied macro-organisms
South China Platform
South Oman Salt Basin, Oman
Avalonia (Newfoundland and England)
Corumbá Group, Brazil
Age (Ma)
**
*
64 64 64 64
3
65 66
67 68
32 32 32
32
69 70 7069
70
Nama Group, Namibia
White Sea, northwest Russia
Fig. 6 | Plot showing the temporal distribution of body and trace fossils from key Ediacaran and earliest Cambrian stratigraphic sections that are radio-
isotopically constrained to a useful level of precision. Uncertainty in the temporal occurrence of a given fossil is constrained by dated ash layers that
occur above or below the fossil type occurrence. The uncertainty in the placement of the first and last occurrence datum increases away from the dated
levels. *Data from this study.
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should be used when comparing our dates with those derived from laboratories
that did not use the same EARTHTIME tracer solution or a tracer solution that was
cross-calibrated using relatable gravimetric reference material. The Z uncertainty
includes the above in addition to uncertainty in the 238U decay constant56. This
uncertainty level should be used when comparing our dates with those derived
from other decay schemes (for example, 40Ar/39A r, 187Re–187Os).
CT. Four individual hand specimens were scanned using Nikon XTH-225 μ CT
scanners at the Natural History Museum (London), and the Life Sciences
Building, University of Bristol. X-rays were generated using a tungsten target. Scan
parameters are provided in theSupplementary Information.
Following μ CT scanning, the data were imported into the program Drishti.
We used this program both to volume render the data following the methods in
ref. 58 and to reslice the volumes to create a TIFF stack of images approximately
parallel to bedding. The data were also segmented using the SPIERS software
suite59 following the methods of ref. 60, exported as stereolithography meshes,
and then imported into the open source raytracer Blender40. In Blender,
the mesh of the surface was rendered partially transparent, and the mesh
encompassing all burrows was split into its component islands, allowing them to
be coloured separately.
Burrow measurements. No statistical methods were used to predetermine sample
size. Burrow measurements were obtained using ImageJ61. Measurements of
burrow diameter were taken from individual slices from specimen OUMNH ÁU.3,
to characterize the size frequency distribution of the trace fossils (Fig.5g). Burrows
were measured from approximately bedding-parallel µ CT slices at maximum
burrow width. This was preferred over systematically measuring burrows from a
sample of slices, as such a method would not necessarily sample burrows at their
maximum diameter, and consequently would skew the size frequency distribution
towards a smaller mean diameter. The smallest burrows observed in μ CT slices
are approximately 2 pixels (~40 μ m) in diameter, and are thus at the limit of scan
resolution. A Shapiro–Wilks test and BIC analysis (using the R package mclust62)
were used to determine population structure in the measurement data63.
Data availability. U–Pb isotopic data used in this study are available in
theSupplementary Information. CT data are freely available at Zenodo (doi:
10.5281/zenodo.842847). All specimens analysed are held at the University of Sao
Paulo and Oxford University Museum of Natural History.
Received: 8 December 2016; Accepted: 28 July 2017;
Published: xx xx xxxx
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Acknowledgements
We acknowledge the support and guidance of our co-author M. Brasier in the early
stages of this work, and particularly his invitation for L.A.P. to undertake fieldwork in
Brazil in 2012. Field costs for L.A.P. were supported by an undergraduate travel grant
from St. Anne’s College, University of Oxford. Fieldwork costs for M.D.B. were supported
by CNPq-Conselho Nacional Desenvolvimento Científico e Tecnológico- Brazil (Proc.
451245/2012-1). This project was supported by an NERC Isotope Geoscience Facilities
Steering Committee grant (project IP-1560-0515). J.M.L., P.C.B., R.T., G.A.C.C.,
C.Q.C.D. and M.L.A.F.P. were supported by grant numbers 2009/02312-4, 2010/02677-0,
2013/17835-8 and 2016-06114-6, São Paulo Research Foundation (FAPESP), Brazil.
A.G.L. and L.A.P. are supported by the Natural Environment Research Council (grant
numbers NE/L011409/2 and NE/L501554/1, respectively). R.J.G. is a Scientific Associate
at the Natural Histor y Museum, London, and a member of the Interdisciplinary Centre
for Ancient Life (UMRI). D.M. recognizes the support of an NSERC discovery grant. We
are grateful to L. A. dos Santos Reis (Votorantim Cimentos) for facilitating access to the
Laginha Mine. We thank L. Tarhan and S. Darroch for constructive reviews.
Author contributions
L.A.P. found and initially identified the Multina specimens in the Guaicurus Formation.
P.C.B., A.G.L., C.Q.C.D. and J.M.L. found the Multina specimens in Tamengo Formation.
All authors collaborated to develop this research project. A.G.L. and D.J.C. secured
funding for geochronological dating. L.A.P., D.J.C. and R.J.G. conducted the analyses.
P.C.B., R.T., J.M.L., C.Q.C.D., M.L.A.F.P. and G.A.C.C. measured the stratigraphic
section and collected samples for dating. L.A.P., D.M., D.J.C. and A.G.L. developed
the manuscript, and all the authors were involved in data interpretation and the final
redrafting of the manuscript.
Competing interests
The authors declare no competing financial interests.
Additional information
Supplementary information is available for this paper at doi:10.1038/s41559-017-0301-9.
Reprints and permissions information is available at www.nature.com/reprints.
Correspondence and requests for materials should be addressed to L.P.
Publisher’s note: Springer Nature remains neutral with regard to jurisdictional claims in
published maps and institutional affiliations.
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... These occur as wormlike phosphatic microfossils with radial proboscis spines interpreted as total-group Scalidophora (Liu et al. , 2018(Liu et al. , 2019Zhang et al. 2015Zhang et al. , 2018Shao et al. 2016Shao et al. , 2020aShao et al. , 2020bWang et al. 2019Wang et al. , 2020. However, trace fossil evidence of ecdysozoan affinity extends to the latest Ediacaran (Buatois 2018), with a maximum age of more equivocal examples ranging from 551 to 555 Ma (Parry et al. 2017;Chen et al. 2018Chen et al. , 2019. Indeed, the trace fossil Treptichnus pedum, long attributed to a priapulan trace-maker (Vannier et al. 2010;Kesidis et al. 2019), defines the Ediacaran-Cambrian boundary. ...
... The rock-clock mismatch in Ecdysozoa As anticipated, the composite interval shown in Figure 6 for the divergence of ecdysozoans precedes the first appearance of ecdysozoan fossils. The oldest possible Ecdysozoan fossils are traces from the terminal portion of the Ediacaran (younger than 556 Ma) equivocally attributed to nematoids (Parry et al. 2017) and panarthropods (Chen et al. 2018(Chen et al. , 2019, and small carbonaceous cuticular fragments compared with scalids also date from a similar time (Moczydłowska et al. 2015). The possible nematoid traces are meiofaunal worm burrows showing undulating nematoid-like movement from the Corumbá Group of Brazil, constrained to a maximum age of c. 555 Ma (Parry et al. 2017). ...
... The oldest possible Ecdysozoan fossils are traces from the terminal portion of the Ediacaran (younger than 556 Ma) equivocally attributed to nematoids (Parry et al. 2017) and panarthropods (Chen et al. 2018(Chen et al. , 2019, and small carbonaceous cuticular fragments compared with scalids also date from a similar time (Moczydłowska et al. 2015). The possible nematoid traces are meiofaunal worm burrows showing undulating nematoid-like movement from the Corumbá Group of Brazil, constrained to a maximum age of c. 555 Ma (Parry et al. 2017). The possible panarthropod traces are from the Shibantan Lagerstätte of South China (Xiao et al. 2021) showing locomotion perhaps associated paired appendages (Chen et al. 2018) and body segmentation (Chen et al. 2019), constrained to a maximum age of c. 551 Ma. ...
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Ecdysozoans (Phyla Arthropoda, Kinorhyncha, Loricifera, Nematoda, Nematomorpha, Onychophora, Priapulida, Tardigrada) are invertebrates bearing a tough, periodically moulted cuticle that predisposes them to exceptional preservation. Ecdysozoans dominate the oldest exceptionally-preserved bilaterian animal biotas in the early-mid Cambrian (∼520–508 Ma), with possible trace fossils in the latest Ediacaran (<556 Ma). The fossil record of Ecdysozoa is among the best understood of major animal clades and is believed to document their origins and evolutionary history well. Strikingly, however, molecular clock analyses have implied a considerably deeper Precambrian origin for Ecdysozoa, much older than their earliest fossils. Here, using an improved set of fossil calibrations, we performed Bayesian analyses to estimate an evolutionary time-tree for Ecdysozoa, sampling all eight phyla for the first time. Our results recover Scalidophora as the sister group to Nematoida + Panarthropoda (=Cryptovermes nov .) and suggest that the Ediacaran divergence of Ecdysozoa occurred at least 23 million years before the first potential ecdysozoan trace fossils. This finding is impervious to the use of all plausible phylogenies, fossil prior distributions, evolutionary rate models and matrix partitioning strategies. Arthropods exhibit more precision and less incongruence between fossil- and clock-based estimates of clade ages than other ecdysozoan phyla. Thematic collection: This article is part of the Advances in the Cambrian Explosion collection available at: https://www.lyellcollection.org/cc/advances-cambrian-explosion Supplementary material: https://doi.org/10.6084/m9.figshare.c.5811381
... Both lithologies yield macroscopic body fossils, the most conspicuous of which are the skeletonized eumetazoans Cloudina lucianoi (in limestone) and Corumbella werneri (in silty shale). The Corumbá Group terminates with the Guaicurus Formation, a thick package of uniform shale which has yielded trace fossils of meiofaunal bilaterians (Parry et al., 2017). ...
... High-precision dating of two volcanic tuffs situated a few meters below the top of the Tamengo Formation yielded mean U-Pb ages of 541.85 ± 0.75 Ma and 542.27 ± 0.38 Ma, respectively (Parry et al., 2017). Combined with an age of 555.18 ± 0.30 Ma for a tuff bed near the top of the underlying Bocaina Formation (Parry et al., 2017), these two dates indicate that the entire Tamengo Formation is latest Ediacaran in age. ...
... High-precision dating of two volcanic tuffs situated a few meters below the top of the Tamengo Formation yielded mean U-Pb ages of 541.85 ± 0.75 Ma and 542.27 ± 0.38 Ma, respectively (Parry et al., 2017). Combined with an age of 555.18 ± 0.30 Ma for a tuff bed near the top of the underlying Bocaina Formation (Parry et al., 2017), these two dates indicate that the entire Tamengo Formation is latest Ediacaran in age. This conclusion is corroborated by the presence throughout the Tamengo Formation of Cloudina (Figure 2), a likely index fossil for the latest Ediacaran (Xiao et al., 2016). ...
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Paraconularia ediacara n. sp., the oldest documented conulariid cnidarian, is described based on a compressed thin specimen from the terminal Ediacaran Tamengo Formation near Corumbá, Mato Grosso do Sul State, Brazil. The conulariid was collected from a laminated silty shale bed also containing Corumbella werneri and vendotaenid algae. The specimen consists of four partial faces, two of which are mostly covered, and one exposed corner sulcus. The two exposed faces exhibit 32 bell-curve-shaped, nodose transverse ribs, with some nodes preserving a short, adaperturally directed interspace ridge (spine). The transverse ribs bend adapertureward on the shoulders of the corner sulcus, within which the ribs terminate, with the end portions of the ribs from one face alternating with and slightly overlapping those from the adjoining face. This is the first Ediacaran body fossil showing compelling evidence of homology with a particular conulariid genus. However, unlike the periderm of Phanerozoic conulariids, the periderm of P . ediacara lacks calcium phosphate, a difference which may be original or an artifact of diagenesis or weathering. The discovery of P . ediacara in the Tamengo Formation corroborates the hypothesis, based in part on molecular clock studies, that cnidarians originated during mid-late Proterozoic times, and serves as a new internal calibration point, dating the split between scyphozoan and cubozoan cnidarians at no later than 542 Ma. Furthermore, P. ediacara reinforces the argument that the final phase of Ediacaran biotic evolution featured the advent of large-bodied eumetazoans, including, possibly, predators.
... Indeed, recent studies consider two of the major Ediacaran clades (the Arboreomorpha and Rangeomorpha) as members of total group Eumetazoa [8]. Evidence for the existence of Ediacaran animals includes: preserved cnidarian muscles (in the staurozoan-like Haootia [9,10]) and surface locomotion trails [11] both from around 565 Ma; the mollusk-like grazing trace Kimberichnus [12] c. 550 Ma; serial impressions of placozoan-type feeding (Dickinsonia, Epibaion [13][14][15] c. 550 Ma; as well as bilaterian burrows [16] and possible annelid trails [17] close to the basal Cambrian both c. 542 Ma. Debates around whether the Cambrian explosion of complex animal life had a short or long Ediacaran fuse [18,19] have thus mostly converged on a consensus that there was a long Ediacaran pre-history to the Cambrian biotas. ...
... The stresses on the matground biotope that dominated hiatal marine seafloors of the Proterozoic largely result from the effects of bioturbation, which seemingly started in the Ediacaran with the evolution of bilaterian burrowers [16] along with the grazing activity of metazoans [12,17,83]. This matground stress likely escalated with the evolution of larger bulk-sediment deposit feeders around the base of Cambrian Stage 2 [80], becoming better established as bioturbators increasingly sought out surficial and buried organic rich substrates through the lower Palaeozoic ( Figure 2A). ...
... The net-like Graphoglyptida are some of the most complex burrow systems in marine depositional settings. If they were to be created by burrowing, their excavation would require complex "programming" [98] to evolve at or before the Ediacaran-Cambrian boundary since the net-like graphoglyptids are known from the latest Ediacaran (described as Multina or Olenichnus [3,16,112]; Figure 7). Modern soft-sediment cores have occasionally recovered shallow-tier polygonal xenophyophore-like protistan organisms [113] comparable to partial Paleodictyon and sponge markers have been associated with Paleodictyon-like openings [104]. ...
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This review asks some hard questions about what the enigmatic graphoglyptid trace fossils are, documents some of their early fossil record from the Ediacaran–Cambrian transition and explores the idea that they may not have been fossils at all. Most researchers have considered the Graphoglyptida to have had a microbial-farming mode of life similar to that proposed for the fractal Ediacaran Rangeomorpha. This begs the question “What are the Graphoglyptida if not the Rangeomorpha persevering” and if so then “What if . . . ?”. This provocative idea has at its roots some fundamental questions about how to distinguish burrows sensu-stricto from the external molds of endobenthic sediment displacive organisms.
... Recently, a rich assemblage of ichnofossils, vendotaenids, and organic-walled microfossils was also described (e.g., Adôrno, 2019). These fossil assemblages have drawn most part of the attention in the studies on the Tamengo Formation (Fairchild, 1978;Walde et al., 1982;Zaine and Fairchild, 1985;Zaine, 1991;Hidalgo, 2002;Gaucher et al., 2003;Kerber et al., 2013;Tobias, 2014;Walde et al., 2015;Adôrno et al., 2017;Becker-Kerber et al., 2017;Parry et al., 2017;Walde et al., 2019;Diniz et al., 2021) C. lucianoi is usually found in limestones, whereas C. werneri occurs in shales (Adôrno et al., 2017;Oliveira et al., 2019;Adôrno, 2019;Amorim et al., 2020). Boggiani (1998) suggests that the Tamengo Formation formed above the Bocaina Formation during a transgression, establishing a slope-break ramp system marked by reworking of the shallower sediment. ...
... Concerning the age of the Corumbá Group, U-Pb dating of zircons from volcanic ash by Parry et al. (2017) provide ages of 555.18 ± 0.7 Ma for the top of the Bocaina Formation and 542.37 ± 0.7 Ma for the top of the Tamengo Formation. These ages agree with the 543 ± 3 Ma provided before by Babinski et al. (2008). ...
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The Ediacaran is a period characterized by the diversification of early animals and extensive neritic carbonate deposits. These deposits are still not well understood in terms of facies and carbon isotope composition (δ13C). In this study we focus on the Tamengo Formation, in southwestern Brazil, which constitutes one of the most continuous and well-preserved sedimentary record of the late Ediacaran in South America. We present new detailed lithofacies and stable isotopes data from two representative sections (Corcal and Laginha) and revise the paleoenvironmental and stratigraphic interpretation of the Tamengo Formation. The Corcal section consists of neritic deposits including shallow-water limestone beds, alternated with shale and subordinate marl beds. These facies yield specimens of the Ediacaran fossils Cloudina lucianoi and Corumbella werneri. On the other hand, the Laginha section shows more heterogeneous facies, such as impure carbonates, breccias, marls, and subordinate mudstone beds, as well as no evidence of Corumbella werneri. The stable carbon isotope record is also different between the two sections, despite belonging to the same unit. The Corcal section displays higher and more homogeneous δ13C values, consistent with those of Ediacaran successions worldwide. The Laginha section, instead, displays more variable δ13C values, which suggest the influence of local and post depositional processes. The difference between the two sections was attributed to the different distance from the shore. We propose that the difference is due to topographic variations of the continental platform, which, at the Laginha site, was steeper and controlled by extensional faults. Therefore, the Corcal section is a better reference for the Tamengo Formation, whereas the Laginha is more particular and influenced by local factors. Besides, the lithofacies associations of the Tamengo Formation are like those of the Doushantuo and Dengying formatios, in South China, with no significant biogenic carbonate buildups, and different from those of other important Ediacaran units, such as the Nama Group in Nmibia and the Buah Formation in Oman. Our work highlights the complexity and heterogeneity of Ediacaran carbonate platforms and of their carbon isotopic composition. In addition, we characterize the Corcal section as a possible reference for the Ediacaran in South America.
... Nasep-Huns transition preserves a varied suite of trace and body fossils from a shallow marine environment that was at least intermittently colonized by seafloor microbial mats. These ichnofossil communities, comprising Archaeonassa, Helminthopsis, Helminthoidichnites, Gordia, Torrowangea, sub-centimeter-scale treptichnids, and meiofaunal burrow systems represent a trace-fossil assemblage that is either of comparable diversity to, or significantly more diverse than, those described from other late Ediacaran localities worldwide (Narbonne and Aitken, 1990;Weber et al., 2007;Högström et al., 2013;Parry et al., 2017;Tarhan et al., 2020). Material from the upper Nasep/lower Huns is further notable for its relatively high intraslab trace diversity, including a number of ichnotaxa in direct association with each other (Fig. 5.2). ...
... The meiofaunal traces noted here bear superficial morphological similarities to Ediacaran nematode traces from Brazil (see Parry et al., 2017) and are of comparable size. Although these burrows exhibit frequent overcrossing (and thus give the impression of forming genuine "networks"), they also appear to possess rare instances of dichotomous branching (see Fig. 8). ...
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The Nasep and Huns members of the Urusis Formation (Nama Group), southern Namibia, preserve some of the most diverse trace-fossil assemblages known from the latest Ediacaran worldwide, including potentially the world's oldest “complex” vertical sediment-penetrating burrows. These sediments record relatively diverse communities of bilaterian metazoans existing before the base of the Cambrian and an increase in the intensity of metazoan ecosystem engineering behaviors that could eventually produce profound changes in the character of the Phanerozoic sedimentary record (the “agronomic revolution”). Despite this, relatively little about this trace-fossil assemblage is known. We explore the Nasep–Huns transition at two localities in the Witputs sub-basin and describe the trace- and body-fossil diversity present in these horizons alongside a paleoenvironmental reconstruction. We document eight unique ichnotaxa from these localities, including well-preserved “probes” potentially left by priapulids. We also report the first occurrence of Corumbella from Namibia, helping to establish a biostratigraphic link between Namibia, Brazil, Paraguay, Iran, and the southwestern United States. Last, we find that several ichnotaxa, in particular small treptichnids, appear to be preferentially preserved on the bases of gutter casts, hinting at the potential existence of an unusual late Ediacaran preservational window with possible implications for timing the first appearance of key bilaterian behaviors.
... These units are overlain by the Guaicurus Formation that records a transgressive event (Alvarenga et al., 2009). The Late Ediacaran age of the Corumbá Group is constrained by its acritarch assemblage (comparable to the Kotlin-Rovno Assemblage) and presence of the Cloudina index-fossil, both restricted to the Bocaina, Tamengo and Guaicurus formations, C and Sr isotopes curves similar to other Late Ediacaran curves and U-Pb zircon ages of 541.85 ± 0.75 and 542.37 ± 0.28 Ma obtained from ash layers interbedded with limestones at the top of the Tamengo Formation, and 555.18 ± 0.3 Ma for the top of Bocaina Formation (Gaucher et al., 2003;Alvarenga et al., 2009;Boggiani et al., 2010;Parry et al., 2017). The Corumbá Group fossil content presents organic-walled microfossils (Bavlinella faveolata, Siphonophycus robustun, Leiosphaeridia tanuissima, Myxococcoides sp, Soldadophycus bossi), vendotaenids (Eoholynia, Vendotaenia), benthic skeletal fossils of possible metazoans and protists (Cloudina, Titanotheca), and soft-bodied cnidarians (Corumbella) of late Ediacaran age (Zaine and Fairchild, 1985;Gaucher et al., 2003), restricted to the mid and upper intervals of the Corumbá Group (Cerradinho, Bocaina, Tamengo and Guaicurus formations; Parry et al., 2017). ...
... The Late Ediacaran age of the Corumbá Group is constrained by its acritarch assemblage (comparable to the Kotlin-Rovno Assemblage) and presence of the Cloudina index-fossil, both restricted to the Bocaina, Tamengo and Guaicurus formations, C and Sr isotopes curves similar to other Late Ediacaran curves and U-Pb zircon ages of 541.85 ± 0.75 and 542.37 ± 0.28 Ma obtained from ash layers interbedded with limestones at the top of the Tamengo Formation, and 555.18 ± 0.3 Ma for the top of Bocaina Formation (Gaucher et al., 2003;Alvarenga et al., 2009;Boggiani et al., 2010;Parry et al., 2017). The Corumbá Group fossil content presents organic-walled microfossils (Bavlinella faveolata, Siphonophycus robustun, Leiosphaeridia tanuissima, Myxococcoides sp, Soldadophycus bossi), vendotaenids (Eoholynia, Vendotaenia), benthic skeletal fossils of possible metazoans and protists (Cloudina, Titanotheca), and soft-bodied cnidarians (Corumbella) of late Ediacaran age (Zaine and Fairchild, 1985;Gaucher et al., 2003), restricted to the mid and upper intervals of the Corumbá Group (Cerradinho, Bocaina, Tamengo and Guaicurus formations; Parry et al., 2017). ...
Article
Ediacaran organic-walled microfossils (OWM) were recently reported for the Camaquã Basin. Sphaeromorphic acritarchs, such as Leiosphaeridia sp, Lophosphaeridium sp. and Germinosphaera, as well as one kind of ornamented microfossil (Tanarium irregulare) were extracted from rocks of either marine (Maricá Group) or continental (Bom Jardim, Santa Bárbara groups) depositional systems. The stratigraphic distribution of organic-walled microfossils within well age-constrained siliciclastic successions made it possible to correlate these microfossils with other coeval Ediacaran assemblages in the world, especially in southwestern Proto-Gondwana. This comparison has shown similarities and differences among them. The Camaquã Basin microfossils register a more extended time interval, but present a smaller diversification than the other assemblages, probably due to have lived within more stressing environments. These differences led us to create a new microfossil assemblage, the CAMBAP (Camaquã Basin Palynoflora) Assemblage, which represents an ecozone, with cosmopolitan microfossils living closely associated with microbial mats.
... Previous outcrop-based facies analysis of these successions allowed the establishment of a robust stratigraphic database, including the positioning of microbialite strata and valuable paleoenvironmental reconstructions. , Boggiani et al. 2010, Parry et al. 2017, Oliveira et al. 2019, Amorim et al. 2020, Romero et al. 2020, Santos et al. 2021. We used the key surfaces represented by Cryogenian-Ediacaran and Ediacaran-Cambrian boundaries to position the classical measured sections with occurrences of microbialites ( Fig. 1). ...
Article
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Microbialites are the most abundant life evidence in Precambrian sedimentary rocks. They are produced by microbial interaction activity and sedimentary processes reflecting paleoenvironmental conditions. The Ediacaran-Cambrian carbonate and siliciclastic successions in the Southern Amazon Craton in Central Brazil, provide a key opportunity to understand how the metazoan life coexisted with the microbial communities. The spatial and temporal distribution of microbialites as well as morphological and paleoenvironmental changes have been assessed, reinterpret-ing previous works and including new data from the Araras-Alto Paraguai and Corumbá basins. The deposition was controlled by subsidence and sea-level changes that affected these basins, considered extensions of epicontinental seas during the Gondwana assembly. The stromatolites are restricted to coastal deposits and experienced thriving flourishment intervals after the Marinoan Glaciation (635 Ma). Post-glacial transgression was marked by microbial colonization in shallow platforms represented by stratiform and giant domical stromatolites in the Araras-Alto Paraguai Basin. The continuity of the transgression generated a moderately deep aragonite sea at about 622 Ma. A progressive sea-level fall caused the im-plantation of coastal environments under greenhouse conditions with tidal flat and sabkha settings colonized by centimetric-scale stromatolites. The sea retreat was accompanied by progressive uplift, causing a moderate inversion of the basin and erosion of the succession until ~560 Ma with the deposition of the last preserved tidal flat deposits with the occurrence of thrombolites. The subsiding Corumbá Basin was the site of microbially-induced deposition of carbonates in a shallow platform connected to an offshore setting with the proliferation of metazoan straddling the Ediacaran-Cambrian boundary. Microbial communities were restricted to lagoon deposits during the Lower Cambrian transgression in the Araras-Alto Paraguai Basin and the last phase refers to the sea retreat towards southeast, developing a fluvial system connected with the arid and evaporitic tidal flats colonized by microbialites that lasted until the upper Cambrian. Except for the post-glacial stromatolites, the columnar and domal microbialite indicate that the coastal settings dominated the Ediacaran-Cambrian transition. The preservation of microbialites in the post-glacial intervals can be associated with the Mg-Ca-CO 3 oversaturation in dolomitic platforms. The rapid calcification and ability to resist the dissolution and replacement have increased the stromatolites' preservation potential reported here, where its well-preserved occurrence in tidal flats and sabkha occurs due to intense early diagenetic silicification. The change from carbonate accumulation to siliciclastic-rich environments contributed to the demise of microbially-induced strata. In general, the scarce coexistence between coastal stromatolite and metazoan-bearing marine deposits makes it challenging to establish a competitive relationship between these organisms, as previously postulated.
... The proliferation of Re-Os dating on organic-rich shales, and more widespread application of chemical-abrasion high-precision U-Pb zircon dating have resulted in dramatic improvements in the agecalibration of the late Neoproterozoic to early Cambrian record of paleoenvironmental changes (e.g. Bowring et al., 2007;Linnemann et al., 2019;Parry et al., 2017;Rooney et al., 2015Rooney et al., , 2020Matthews et al., 2021). Accompanying the increase in number of radioisotopic ages for this time interval has been the application of complementary chronological techniques, such as Bayesian time scale modelling (Matthews et al., 2021) and astrochronological inversion of cyclostratigraphy (e.g. ...
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The Ediacaran Period (ca. 635–539 Ma) represents a major transition in Earth history, beginning with the end of the Cryogenian snowball Earth glaciation and ending with the appearance and early diversification of bilaterian animals. Whereas a steady flow of new radioisotopic ages from key stratigraphic successions has resulted in much improved age constraints for the earliest and latter Ediacaran, few ages exist for the middle Ediacaran Period. The Jibalah Group, in the eastern part of the Arabian Shield, comprises minimally deformed volcano-sedimentary successions deposited in discrete basins, previously constrained to date between ca. 620 Ma and 560 Ma. The Antaq basin is one of the largest and best exposed of the Jibalah basins and contains the Muraykhah Formation (upper Jibalah Group), which is of particular interest because it contains putative Ediacaran fossils, textured organic surfaces, multiple tuff horizons, and spectacular 1–10 m-scale siltstone-sandstone cycles. Here we report new high-precision U-Pb zircon ages from the Muraykhah Formation anchoring an astrochronological analysis of these cycles. The radioisotopic ages confirm that two strong peaks identified in the stratigraphic height domain reflect accumulation paced by the long (405 kyr) and short (131–91 kyr) eccentricity cycles, the latter of which corresponds to the m-scale cyclicity that is visually apparent in the stratigraphy. The combination of radioisotopic ages and astrochronology allows us to develop a continuous, tuned record spanning from 599.1 ± 0.4 to 590.4 ± 0.6 Ma. This record complements other astrochronological analyses from slightly younger Ediacaran strata spanning the global Shuram negative carbon isotope excursion. The integrated radioisotopic and astronomical time scale ages also provides new constraints on the Ediacaran tectonic evolution of the eastern Arabian Shield.
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The Corumbá Group is a Neoproterozoic succession of terrigenous and carbonate sedimentary rocks located at the southern Paraguay Belt, central Brazil. The upper units of the Corumbá Group include the Ediacaran carbonate Bocaina and Tamengo formations, whose limit is characterized by polymictic breccias recognized in several sites from Corumbá to Serra da Bodoquena, Mato Grosso do Sul. Despite the widespread occurrence, the breccias are poorly described and their origin is uncertain. The aim of this study is to present the differences between sedimentary and tectonic breccias of the Corumbá Group and propose a genesis model for each. The sedimentary breccias comprise mainly matrix-supported chaotic facies that formed by submarine mass flows on slope aprons. Sea level fall and/or increased faulting rates exposed the underlying units and triggered the gravity fluxes by creating a steep slope. The base of the sedimentary breccia represents a major unconformity within the carbonate sedimentation of the Corumbá Group, with potential correlation to other Ediacaran units. The subsequent development of the Paraguay fold-thrust belt caused the formation of tectonic breccias in reverse fault zones. Cataclasis and mylonitization deformed the dolomitic host rock by fracturing and produced a fine foliated matrix.
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The controversial hypothesis that ‘Oumuamua (1I/2017 U1) was an alien craft dominated by a solar sail is considered using known physics for the two possible cases: controlled and uncontrolled flight. The reliability engineering challenges for an artefact designed to operate for ~10 ⁵ –10 ⁶ year are also considerable. All three areas generate research programmes going forward. The uncontrolled case could be either ‘anonymous METI’ (messaging extraterrestrial intelligence) or ‘inadvertent METI’. In the controlled case the nature of the origin star, trajectory guidance from the origin star to the Sun, and the identity of a destination star are all undecided. The ‘controlled’ case has more strikes against it than the ‘uncontrolled’ case, but neither suffers a knock-out blow, as yet. Some of the issues turn out not to be major obstacles to the alien craft hypothesis, but others weaken the case for it. Most, however, imply new studies. Some of these, e.g. intercept missions for new interstellar objects, are concepts being developed, and will be of value whatever these objects turn out to be. Overall, these considerations show that a many-pronged, targeted, research programme can be built around the hypothesis that ‘Oumuamua is an alien craft. The considerations presented here can also be applied to other interstellar visitors, as well as to general discussions of interstellar travel.
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Ichnology is the study of traces created in the substrate by living organisms. This is the first book to systematically cover basic concepts and applications in both paleobiology and sedimentology, bridging the gap between the two main facets of the field. It emphasizes the importance of understanding ecologic controls on benthic fauna distribution and the role of burrowing organisms in changing their environments. A detailed analysis of the ichnology of a range of depositional environments is presented using examples from the Precambrian to the recent, and the use of trace fossils in facies analysis and sequence stratigraphy is discussed. The potential for biogenic structures to provide valuable information and solve problems in a wide range of fields is also highlighted. An invaluable resource for researchers and graduate students in paleontology, sedimentology and sequence stratigraphy, this book will also be of interest to industry professionals working in petroleum geoscience.
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