ArticlePDF Available

The timing and pattern of biotic recovery following the end-Permian mass extinction


Abstract and Figures

The aftermath of the great end-Permian period mass extinction 252 Myr ago shows how life can recover from the loss of >90% species globally. The crisis was triggered by a number of physical environmental shocks (global warming, acid rain, ocean acidification and ocean anoxia), and some of these were repeated over the next 5-6 Myr. Ammonoids and some other groups diversified rapidly, within 1-3 Myr, but extinctions continued through the Early Triassic period. Triassic ecosystems were rebuilt stepwise from low to high trophic levels through the Early to Middle Triassic, and a stable, complex ecosystem did not re-emerge until the beginning of the Middle Triassic, 8-9 Myr after the crisis. A positive aspect of the recovery was the emergence of entirely new groups, such as marine reptiles and decapod crustaceans, as well as new tetrapods on land, including -- eventually -- dinosaurs. The stepwise recovery of life in the Triassic could have been delayed either by biotic drivers (complex multispecies interactions) or physical perturbations, or a combination of both. This is an example of the wider debate about the relative roles of intrinsic and extrinsic drivers of large-scale evolution.
Content may be subject to copyright.
ife came closest to complete annihilation 252.3 Myr ago
during the end-Permian mass extinction (EPME), which
occurred just before the Permo–Triassic boundary (PTB). is
largest crash in global biodiversity of the past 500Myr (refs1–3)
markedly redirected the course of evolution during the Mesozoic
and Cenozoic eras, and is responsible for much of the structure of
marine and terrestrial ecosystems today
e disappearance of ~90% of skeletonized marine species
marked the end of Palaeozoic marine faunas and the rise of the
replacing ‘modern fauna
. Formerly dominant denizens of the deep,
such as brachiopods, crinoids, trilobites and tabulate and rugose
corals, either disappeared or were massively reduced in diversity.
Other groups that were already present, but were minor components
of ecosystems, such as bivalves, gastropods, malacostracans (crabs
and lobsters), echinoids (sea urchins), scleractinian corals and bony
shes, took their places. ese are still the dominant groups in the
sea, so modern marine ecosystems date back to the Triassic recovery.
On land too, basal tetrapods gave way to archosaurs including
dinosaurs, as well as the ancestors of modern frogs, turtles, lizards,
crocodiles and mammals.
Many aspects of biotic recovery following the EPME, in the
Early and Middle Triassic, have been puzzling, including its tempo
and mechanism
. ere are three elements: timing; roles of
intrinsic and extrinsic processes; and signicance of trophic levels
in ecosystems. In terms of timing, some clades seemed to bounce
back relatively rapidly, within 1–2Myr (refs12–14), whereas others
experienced a long delay of 5–10Myr (refs8,9,15–17; Fig.1). e
relative roles of intrinsic (ecosystem dynamical) and extrinsic
(physical environmental) processes as drivers of the recovery
depend on the timing of recovery. If the recovery was slow, there are
questions about whether the delay was imposed by continuing poor-
quality environments
, complex ecosystem interactions
or a combination of both. Finally, trophic level might be crucial,
and we outline a multi-step recovery model involving the addition
of progressively higher trophic levels within marine ecosystems and
spanning some 8Myr.
Because the EPME was the most extreme of several mass
extinctions in the past 500Myr, the post-extinction recovery began
The timing and pattern of biotic recovery
following the end-Permian mass extinction
Zhong-Qiang Chen
and Michael J. Benton
The aftermath of the great end-Permian period mass extinction 252 Myr ago shows how life can recover from the loss of
>90% species globally. The crisis was triggered by a number of physical environmental shocks (global warming, acid rain,
ocean acidification and ocean anoxia), and some of these were repeated over the next 5–6Myr. Ammonoids and some other
groups diversified rapidly, within 1–3Myr, but extinctions continued through the Early Triassic period. Triassic ecosystems
were rebuilt stepwise from low to high trophic levels through the Early to Middle Triassic, and a stable, complex ecosystem
did not re-emerge until the beginning of the Middle Triassic, 8–9Myr after the crisis. A positive aspect of the recovery was
the emergence of entirely new groups, such as marine reptiles and decapod crustaceans, as well as new tetrapods on land,
including — eventually — dinosaurs. The stepwise recovery of life in the Triassic could have been delayed either by biotic drivers
(complex multispecies interactions) or physical perturbations, or a combination of both. This is an example of the wider debate
about the relative roles of intrinsic and extrinsic drivers of large-scale evolution.
from a much more devastated planet and biota than the others.
With only some 10% of species surviving, the EPME was much
harsher than the other mass extinctions, during which global species
diversity reduced to only about 50% of the pre-extinction total
is means that the Triassic recovery has two profound implications:
rst, it may show qualitative, as well as quantitative, dierences
from the other post-extinction recoveries; and, second, it can act
as an exemplar of what to expect, at its most extreme, when global
biodiversity is pushed to the brink. ere are obvious implications
for current concerns about biodiversity loss and recovery resulting
from human impacts
In the past ten years, attention has focused on the sedimentary
successions in south China. ese are enormously laterally
extensive, with some formations extending more than 2,000 km
from the Zhejiang to Yunnan provinces. e huge exposures, length
of the sections and improving dating open up the opportunity
to explore physical environmental and biotic changes through
the extinction and recovery times in varied marine habitats, and
compare these with patterns elsewhere in the world (Fig.1). A ne-
scale, forensic analysis of this extraordinary time in Earths history
now becomes possible.
The end-Permian mass extinction
e EPME killed 80–96% of marine animal species and 70% of
terrestrial vertebrate species
. In the intensively sampled
Meishan section in South China, 280 out of 329 marine
invertebrate species disappeared near the PTB, indicating an
abrupt, one-stage extinction pattern
. Closer study at Meishan
and adjacent areas indicates that the EPME may have followed a
two-stage pattern, with each crisis step separated by approximately
0.2Myr (refs32–35).
A number of potential triggers for the crisis have been identied:
increased CO
concentrations and global anoxia, euxinia (anoxic
and sulphidic conditions), hypercapnia (CO
poisoning), a bolide
impact, rapid global warming and plume-induced volcanic
. e most widely accepted model
begins with
eruption of the Siberian traps, huge volumes of basaltic lava that
produced CO
, which led to global warming and the short-term
State Key Laboratory of Biogeology and Environmental Geology, China University of Geosciences, Wuhan 430074, China.
School of Earth Sciences,
University of Bristol, Bristol, BS8 1RJ, UK. *e-mail:
PUBLISHED ONLINE: 27 MAY 2012 | DOI: 10.1038/NGEO1475
© 2012 Macmillan Publishers Limited. All rights reserved
production of acid rain. e acid rain killed plants on land, which
led to massive erosion as soil was released, all associated with a shi
from ne-grained sediments deposited in lakes and meandering
rivers to conglomeratic braided uvial facies
. e massive
erosion was associated with wildres, perhaps triggered during
the unusually arid conditions
. Sedimentation rates in terrestrial
successions increased
and there was an abrupt, increased inux
of terrigenous siliciclastics to the oceans
, associated with soil-
derived biomarkers
In marine environments, heightened CO
levels led to ocean
acidication; at the same time, global warming and raised inputs of
nutrients into the sea caused ocean anoxia, indicated by widespread
black sediments and sulphides
. Furthermore, interaction between
Siberian-trap magma and organic-rich sedimentary rocks could
have greatly increased release of CO
and other greenhouse gases.
e warming could also have triggered the release of methane from
deep ocean reserves and coals, which would have exacerbated the
global warming and ocean anoxia
e extinction and recovery episodes are well dated, especially
in marine sections. High-resolution fossil biozones from the PTB
beds and Triassic sequences of south China enable correlation of the
EPME and its aermath
. e EPME was calibrated to the base
of a volcanic ash bed just below the PTB in the Meishan section,
south China
, the world standard for the PTB (ref.46). In south
China (Fig.1), this crisis has been dated at 252.3Ma (ref.35) and
the Early–Middle Triassic successions are constrained by high-
resolution radiometric ages
and astrochronology
. Terrestrial
successions are harder to date accurately, but a combination of
radiometric dating, magnetostratigraphy and chemostratigraphy is
improving the situation
Physical environments in the aftermath of the EPME
Environmental conditions in the Early Triassic were poor. is
is indicated by unusual biosedimentary features (including
abundant microbialites, wrinkle structures and seaoor carbonate
precipitates) that reect the absence of metazoans devastated by the
EPME, combined with episodes of low oxygen and high chemical
. ese unusual conditions are matched by the ‘coral
gap, when there were no reefs built by colonial metazoans in shallow
, and the ‘coal gap
on land, during which forests, and
hence coal deposits, were absent (Fig.1).
Anoxia has long been documented as a key element of the
, and it seems to have been a recurring condition
throughout the Early Triassic
. Upwelling of CO
from anoxic
deep-ocean waters during the EPME may have increased the acidity
of surface waters for a short time, causing elevated mortality among
carbonate-secreting organisms
. Oceanic euxinia (anoxic and
sulphur-rich stratied ocean) is indicated by the loss of dissolved
oxygen and free H
S in the water column, as shown by biomarkers,
pyrite framboid sizes, S-isotopic compositions and Ce anomalies
e massive release of sulphides into the oceans adds H
S toxicity to
the cocktail of potential killers
Redox changes may have been caused either by chemocline-
upward excursions
or by upwelling of deep anoxic water
. ese massive changes in seawater chemistry are
attested by repeated C-isotopic excursions
, but the origins of these
are uncertain. Clues may come from correlations with uctuations
in other geochemical proxies, such as
C hopane and 2-MHP
biomarker ratios, and increased concentrations of
, which can indicate upwelling of
C-depleted, sulphidic
deep waters.
mass extinction
Deep sea
Shallow sea
Bioturbation level
Seafloor carbonate precipitates
Burrow depth, size and complexity
Metazoan reefs
STLIP eruption
Reefs, reef-
builders, cherts
–2 02468
Marine ecosystems
Biodiversity changesBiodiversity changes
Te rrestrial ecosystems
C (
Middle TriassicEarly Triassic
Gr. Sm. Ae. Bith.Spathian PelsonianDi.
Figure 1 | Environmental changes and biodiversity variations from the latest Permian to Middle Triassic. Arrows indicated on the conodont and ophiuroid
range bars show increasing data into the Middle Triassic; detailed data on genus diversity and principal authors are listed in Supplementary Table S1.
The timescale was based on new radiometric dates outlined in Supplementary Information S2. Carbon isotope fluctuations, Siberian Traps large igneous
province (STLIP) eruption, anoxia ranges, trace fossil data, and reef, reef builder, chert and coal gap data from references in Supplementary Information.
Ae., Aegean; Bith., Bithynian; Di., Dienerian; Gr., Griesbachian; Illy., Illyrian; Sm., Smithian; Vol., volcanism.
© 2012 Macmillan Publishers Limited. All rights reserved
Negative excursions in carbon isotope ratios, indicating
repeated greenhouse crises
, occurred as many as ve times during
the 5Myr of the Early Triassic and early Anisian age (Fig.1). It
is uncertain how such repeated light-carbon excursions could
be generated so frequently: one spike could exhaust the global
reserves of methane stored in deep ocean gas hydrates. Either the
methane reserves could recharge faster than had been assumed, or
large volumes of CO
were repeatedly released from coal beds
frequent volcanic eruptions
The pattern of Triassic recovery
e recovery of life began rapidly, within the rst 1–3Myr of the
Triassic. For example, among marine organisms, ammonoids
diversied in the rst 2 Myr of the Early Triassic,
reaching apparently stable local diversities. Further, some earliest
Triassic body and trace fossil assemblages are more diverse than
. e best example comes from foraminifera in the
south China sections, where recovery began 1Myr into the Triassic,
and was not much aected by Early Triassic crises
. is early phase
of recovery was short-lived for most groups, and there were further
extinctions at the end of the Smithian and Spathian sub-stages, both
in the sea
and on land
, so global species and ecosystem
stability had not yet been achieved.
e recovery of life on land indicates similar patterns
Plants declined rapidly in diversity through the EPME and
rebounded in the Smithian, but did not return to pre-extinction
levels until the Late Triassic (Fig. 1). However, extinction was
limited; rather, temporary ecological replacements arose, driven
by environmental changes. e spore spike in many sections before
the EPME was the rst sign of environmental deterioration, when
stable gymnosperm-dominated oras were replaced by rapidly
growing, early successional communities dominated by lycopods
and ferns
, resulting in reduced sequestration of organic matter
in terrestrial facies during the Early Triassic coal gap
. A
further spore spike occurred in the middle Smithian, preceding
the end-Smithian extinction when the lycopods were replaced by
woody gymnosperms, indicating a switch from warm and equable
climates to latitudinally dierentiated climates
Tetrapods also underwent massive extinction through the EPME
(Fig.1), with the destruction of complex latest Permian ecosystems
dominated by herbivorous pareiasaurs and dicynodonts, and
carnivorous gorgonopsians. Dicynodonts recovered to become major
herbivores again, passing through a bottleneck at the PTB, and smaller
groups, such as procolophonids and therocephalians, survived the
EPME. Tetrapod ecosystems in Russia, at least, showed considerable
volatility until the Ladinian age
. Further, the key tetrapod groups
had changed and new clades, the archosaurs and cynodonts, became
dominant, with dinosauromorphs originating earlier than had been
thought, in the maelstrom of the Spathian to Anisian recovery
Marine ecosystems had recovered substantially in the early to
middle Anisian, 8–9Myr aer the crisis, and perhaps at the same
time (or even later) on land. Importantly, this was the time when the
coral and coal gaps ended (Fig.1).
e EPME was positive in the emergence of new organisms.
Most striking were the marine reptiles (ichthyosaurs, thalattosaurs,
pachypleurosaurs, nothosaurs and placodonts) that emerged in
the Olenekian and Anisian ages, and decapod crustaceans (crabs
and lobsters). ese added new top trophic levels, creating a
typical Mesozoic, or even ‘modern, ecosystem — seen especially
in China (Box1). ese reptiles and decapods are new clades and
so technically not part of the recovery — where ‘recovery’ means
the return to a previous state — but these new predators were key
components of Mesozoic ecosystems. On land, too, major new
groups appeared in the aermath of the extinction, including frogs,
dinosauromorphs (and eventually dinosaurs)
, rhynchosaurs and
diademodont cynodonts.
Trace fossils (burrows and trails) provide alternative evidence for
recovery patterns, especially in the sea
. Although several diversity
spikes among trace fossils have been recognized from the Induan
, multiple lines of evidence, including diversity, burrow
size, complexity, tiering levels and bioturbation levels, show that
trace fossil assemblages recovered in the Spathian
e Triassic of south China is marked by several exceptionally
preserved fossil assemblages, in which a wide array of organisms,
those with skeletons and those without, are preserved. One
recently discovered example, the Luoping biota of the Yunnan
Province, southwest China
, dated as mid-Anisian, documents
the nal stages of recovery from the EPME. e Luoping biota
is dominated by lightly sclerotized arthropods, associated
with shes, marine reptiles, bivalves, gastropods, belemnoids,
ammonoids, echinoderms, brachiopods, foraminifers and
. So far, some 20,000 specimens have been collected.
Unusually, the commonest animals were arthropods (including
decapods), comprising 94% of all nds. e 25 species of shes
and diverse marine reptiles, comprising together 4% of nds,
show multiple new predatory levels in the ecosystems, and match
closely with well-known marine faunas from the Middle and
Late Triassic elsewhere in the world. e Luoping biota seems to
represent a stable, typically Mesozoic marine ecosystem.
e photographs above show exceptionally preserved shes
(a,b) and reptiles (c) from the Luoping biota, Yunnan, southwest
China: a, eugnathid sh; b, Saurichthys; c, ichthyosaur.
Box 1 | The Luoping biota
© 2012 Macmillan Publishers Limited. All rights reserved
Several benthic assemblages were found to be rather diverse in the
aermath of the EPME, indicating an earlier benthic recovery
However, benthic communities in most areas of the world remained
at low diversity through the Early Triassic
A nal ecological aspect of the Triassic recovery was the ‘Lilliput
eect’ (dwarng) shown by marine organisms, not only during the
EPME, but also through the entire Early Triassic
; although,
body sizes of some clades (for example, gastropods
) remained
unchanged or slightly increased in the Early Triassic. e dwarng
may have been driven by reductions in food supply, reductions
in oxygen levels during greenhouse crises, or changing ecological
pressures, and recovery of normal sizes corresponds to the return of
stable conditions in the early Anisian
Slow or fast recovery?
A key question concerns the timing of Triassic recovery. e
standard view
is that the recovery lasted some 5–9Myr,
whereas others
concentrate on the rst 1–3 Myr aer the
EPME. ere are issues concerning denitions of terms and possible
sampling bias.
Early phases of recovery may be indicated by recovery of species
numbers within 1Myr of the EPME (Fig.1), and yet these ecosystems
were oen unbalanced. For example, earliest Triassic terrestrial
faunas may have contained as many species as before the crisis
, but
species ‘evenness’ (the similarity of relative abundances of species)
was unbalanced, with individuals of the dicynodont Lystrosaurus
in huge abundance (>90%), together with rare amphibians, but
without diverse herbivores and top predators
. Most would
call this a ‘disaster fauna, a short-term community composed of
opportunistic species that did not form the basis for the balanced,
even ecosystems typical of later times. e same case has been made
concerning earliest Triassic marine faunas
Delayed recovery could reect poor sampling in the Early
. Perhaps the reefs and marine reptiles that emerged in
the Anisian are actually present in earlier Triassic rocks, but have
yet to be sampled. ere is no test to distinguish true absence from
simply a lack of sampling or fossilization
. Sampling of the Early
Triassic of south China, and other well-documented long sections,
has improved enormously in the past twenty years. Evidence has
yet to be found showing that lithologies or quality of exposure are
suciently dierent between, for example, the earliest Triassic and
the Anisian for early appearing reefs or marine reptiles to be missed.
If ecosystems recovered in a stepwise and steady fashion, then
individual taxonomic groups show major dierences. Fast-evolving
taxa, such as ammonoids and conodonts, apparently recovered
fast aer the EPME. eir high rates of speciation were associated
with considerable evolutionary volatility: both groups had suered
extinctions (particularly the ammonoids) during the EPME, as well
as during crisis intervals throughout the Early Triassic
. e story
is not quite so simple, however. Although ammonoids recovered
relatively rapidly, reaching a higher diversity by the Smithian than in
the Late Permian
, much of this Early Triassic radiation was within
From an evolutionary point of view, biotic recoveries following
mass extinctions are characterized by a complex set of dynamics,
including the rebuilding of whole ecologies from low-diversity
assemblages of survivors and opportunistic species. Biodiversity
recovery could follow one of three trajectories
: a, an immediate
linear response; b, a logistic recovery; or c, a simple positive feedback
pattern of species interaction that follows a hyperbolic trajectory.
In theoretical modelling
, the lag time to biotic recovery increases
signicantly as biotic interactions become more important in the
recovery process, an example of positive feedback
. ese models
are developed with equilibrium assumptions — of the world before
and aer extinction having a xed carrying capacity— that have
been questioned
e three models can characterize dierent trophic levels,
with producers recovering rst, according to a linear model, and
consumers taking longer to recover. Long delays in recovery are
expected at higher trophic levels in the food chain
, with predators
taking longer to recover than primary consumers (herbivores).
eoretical modelling supports the last model, but it will be
important to tease apart the eects of three possibly interacting
variables during recovery from mass extinction: the magnitude
of the extinction and consequent scale of the immediate recovery
faunas; the eects of continuing or repeated low-quality physical
environments; and the eects of species interactions throughout the
recovery time. If such interactions are absent, the linear or logistic
model might be expected; if they are present, the hyperbolic model
might be followed. If species interactions are indeed important
during post-extinction diversication, then the length of delay
before the onset of rapid recovery should scale with the speciation
. Further, if there is environmental inhibition of recovery, it
might be possible, with excellent dating and thorough sampling of
fossil records, to identify such a lag from the subsequent recovery
A further interesting theoretical question is whether
diversications following mass extinctions dier from other
kinds of clade expansions. In other words, are there dierences
in the dynamics and macroecological impacts of recoveries when
compared with ‘adaptive radiations, contrasting opportunistic
versus adaptive drivers? Broader macroecological questions for all
kinds of diversications
concern the timing: whether ecosystems
rebuild themselves in a wholesale manner or step-by-step; whether
the recovery passes up through the trophic chain from producers
to top carnivores; whether there is an ‘early burst’ of diversication
of disaster taxa and then a decline; and how dierent sub-clades
fare relative to each other.
Box 2 | Models of recovery
Proportion of species relative to pre-extinction levels
Time (arbitrary units)
Spindle diagrams
0 100 200 300 400 500
40 50 60 70 80 90 100
40 60 80 100 120 140
© 2012 Macmillan Publishers Limited. All rights reserved
a single clade, the Ceratitina, and the global diversity of ammonoids
did not reach maximum levels until the mid Anisian
A more slowly evolving group, the benthic foraminifera, took
10Myr to recover to pre-extinction diversity levels, even though their
recovery began 1Myr aer the EPME, and they were apparently not
much aected by the environmental shocks of the Early Triassic
Among other slowly evolving groups (Fig. 1; Supplementary
TableS1), brachiopods had been the commonest animals in Permian
oceans, but experienced a sharp decline in the Early Triassic and
their diversity did not rebound until the early Middle Triassic
Corals suered a major diversity loss in the EPME and did not
re-occur until the middle Anisian
. is is also true for radiolarians,
a clade that suered a large depletion in diversity during the Early
Triassic and early Anisian
. Among echinoderms, crinoids were
absent for much of the Early Triassic and rebounded at the end of
the Spathian
, whereas ophiuroids experienced diversity increase
and geographic expansions immediately aer the EPME (ref.90).
Habitat may also matter. It has been argued
that pelagic taxa
such as ammonoids and conodonts recovered before benthic forms:
pelagic recovery began immediately in the Induan, and then benthic
forams and others began to recover more slowly from the beginning
of the Olenekian
Most studies of Triassic recovery have used global or regional
diversity counts, typically numbers of genera or species. Such
palaeodiversity metrics cannot indicate all aspects of recovery
, and
a wider ecological approach is essential
. For example, ammonoid
diversity rose in the Smithian (Fig. 1), but their morphological
disparity (range of form) did not expand until the end-Spathian
is diversity-rst model may not be ubiquitous, however, and many
tetrapod groups in the Triassic show the more typical disparity-rst
. For ammonoids, then, the diversity-rst model indicates
rapid speciation of similar disaster taxa lling ecospace, followed by
more steady adaptive evolution into new sectors of morphospace as
ecosystems and community interactions stabilized. e disparity-rst
pattern seen among tetrapods indicates that clades explored the limits
of morphospace early, and then later lled the space by specialization.
Perhaps the two patterns reect overall rates of evolution (fast in
ammonoids), or whether a clade reacts in a ‘disaster-taxon’ way
(diversity-rst) or in a long-term ecosystem-stabilizing manner
(disparity-rst). e distinction between fast- and slow-evolving taxa
may relate to ecology, distinguishing opportunistic species that show
high rates of reproduction, many ospring and limited parental care
(r-selected), and those that produce few ospring infrequently and
invest in their nurture (K-selected). ese studies show the need to
consider more than palaeodiversity in seeking to understand the real
richness of diversication.
Multi-step trophic model of recovery
ere is some debate over whether trophic levels predict recovery
rates or not — the standard view
is that lower trophic levels
recover before higher levels, and this is supported by fundamental
ecological assumptions (Box2). However, the fact that ammonoids
and conodonts began to recover early, and that predatory shes
such as Birgeria and Saurichthys, as well as the rst ichthyosaurs,
occur in the Olenekian, indicates that trophic level is not on its
own a guide to the timing of recovery
, but ought to be considered
together with intrinsic rates of evolution of each clade
. Here, we
broaden the ecological network model
to explore the complete
trophic structure of fossilized ecosystems during the Permo-Triassic
transition (Fig.2), as a means of assessing the recovery.
During the Late Permian and Early Triassic, primary producers,
forming the lowest trophic level, were microbes. e middle part of
the food web comprises primary and meso-consumer trophic levels,
the former dominated by microorganisms such as foraminifers, and
the latter by opportunistic communities (that is, disaster taxa and
tracemakers), benthic shelly communities and reef-builders. ese
were consumed by invertebrate and vertebrate predators, the top
trophic level (Fig.2).
We track the recovery through rich evidence from the Late
Permian to Middle Triassic of south China (Fig.1). Latest Permian
ecosystems usually had a healthy trophic structure from primary
producer to top predator. Marine assemblages were dominated by
brachiopods, fusulinid foraminifers, corals and crinoids (Fig.3a),
and had low abundance, high diversity and low evenness
. ese
ecosystems collapsed during the EPME.
Marine ecosystems immediately aer the extinction were either
microbialite build-ups, formed from microbes associated with
tiny gastropods and ostracods (Fig.3b), or high-abundance, low-
diversity communities dominated by disaster taxa (Fig.3c). us,
marine ecosystems were degraded to a low level, typied by primary
producers or opportunistic consumers (Fig.3b,c). ese two types
of ecosystems prevailed through most of the Early Triassic.
In the Spathian, marine ecosystems (Fig.3d) comprised ever more
diverse trace fossil assemblages, as well as biodiversity increases of
some clades. is epoch was also marked by the emergence of some
high-tiering organisms such as crinoids, as well as rare predatory
shes and the rst ichthyosaurs. However, benthic communities
were still of low diversity and high abundance
Aer prolonged loss of dominance in Early Triassic marine
communities, Palaeozoic holdover faunas of brachiopods and
crinoids became signicant again in the Anisian. Corals and
metazoan reefs also reappeared in the Anisian, when marine
assemblages shared similar community structural indices with
pre-extinction communities
(Fig.3e). In the middle–late Anisian,
marine ecosystems were characterized by the common occurrence
of reptile- and sh-dominated communities (Fig.3e), such as the
Luoping biota in Yunnan, southwest China
(Box 1), in which
marine reptiles (ichthyosaurs, pachypleurosaurs, thalattosaurs
and prolacertiforms) diversied as top predators. With these top
predators, Middle Triassic ecosystems added a new trophic level
not seen in the Permian, when sharks, and not reptiles, had been
top predators. us, ecosystems were constructed step by step
Figure 2 | Outline trophic pyramid of a fossilized marine ecosystem in
the Permian or Triassic. From the bottom, the trophic levels are: primary
producers (PP), mainly microbes; primary consumers (PC), such as
foraminifers; meso-consumers (MC
), such as endo-faunal trace-markers;
meso-consumers (MC
), such as benthos; reef-building meso-consumers
(Rb); predatory invertebrates (P
), such as gastropods; and predatory fishes
and reptiles (P
© 2012 Macmillan Publishers Limited. All rights reserved
from low to top trophic levels through Early–Middle Triassic
times (Fig.4) following logistic growth of biotic recovery, based on
theoretical modelling
Reasons for delayed recovery
Life began to recover quickly in the Early Triassic, but full recovery
took some 8–9 Myr
in the sea, and the same or longer
on land
. A key question is whether this delay resulted from
complex ecosystem dynamics or from continuing grim physical
environmental conditions, or a combination of both. Current
theoretical models for recovery (Box2) indicate that a recovered
ecosystem should be at equilibrium, showing high biodiversity, low
turnover, resistance to invaders and a complex trophic structure
resistant to environmental perturbation. According to these models,
delay to recovery is proportional to the amount of interaction
between species
Even though biotic interactions may have played a role and some
taxa were little aected by extrinsic perturbations
, it is widely
that poor environmental conditions in the
post-extinction world slowed full recovery. An exception may be
the benthic foraminifera
, which radiated slowly through the Early
Triassic, and at most were aected by the end-Smithian event
. In
a further example, metazoan reefs have been reported
from the
Smithian, within 1.5Myr of the EPME, and these supposedly plug
the coral gap. However, these ‘reefs’ are microbial mats associated
with sponges and serpulid worms, and their occurrence is transient;
they do not indicate the permanent re-emergence of coral reefs,
delayed for some 8–9Myr aer the EPME.
Paradoxically, high productivity might have delayed recovery
by favouring bacteria. Observed bursts of primary productivity
immediately aer the EPME
and later in the earliest Triassic
to relate to phases of terrestrial erosion and ushing of sediment into
the sea
. Increased uxes of nutrients to marine systems would have
created eutrophic conditions that favoured stromatolitic microbes
over corals and other lter feeders.
Testing models of evolution
e distinction between early and late phases of recovery reects
groups and habitats. Fast-evolving taxa such as ammonoids and
conodonts recovered pre-extinction diversity fast, but continued
to show volatile responses to continuing environmental shocks in
the Early Triassic. More slowly evolving taxa, such as foraminifera
and brachiopods, began to re-emerge in the rst 1–2Myr of the
Early Triassic, but took 5–10Myr to achieve pre-extinction global
diversity, and were less subject to repeated turnovers. On land,
plants were slow to recover, and tetrapods rebuilt local diversity
very fast, but ecosystems remained unbalanced and unstable until
the Middle Triassic.
e ecosystem stepwise recovery pattern, however, must be
tested in a broad range of well-dated, high-quality fossil records
from dierent geographic regions. is requires correlation of
fossil records in various facies and latitudes worldwide, which is in
progress at present through the International Geological Correlation
Program 572: Permian–Triassic ecosystems (2008–12).
ere are several key concepts and predictions that may be
explored in the Triassic aermath of the EPME, as well as in other
recoveries. e length of time for recovery is proportional to the
depth of the extinction, but this is not linear. Recovery is slowest
if extinction is global in scale, not restricted to climatic belts.
Recovery on land may be slower than in the sea, perhaps because
Figure 3 | Reconstructed marine ecosystems before and after the end-Permian mass extinction in south China. a, Pre-extinction marine benthic ecosystem
in the latest Permian; low abundance, high diversity and dominated by brachiopods, corals, crinoids and fusulinid foraminifers. Scale bar, 10cm. b, Microbe-
dominated ecosystem immediately after the EPME in early Griesbachian (early Induan); primary producers dominate. Scale bar, 10cm. c, Opportunist-
dominated ecosystem in Griesbachian–Dienerian (Induan); high abundance, low diversity and dominated by disaster taxa (for example, the bivalve Claraia).
Scale bar, 5cm. d, Tracemaker-dominated ecosystem in Spathian (late Olenekian), indicating recovery of tracemakers. Scale bar, 6cm. e, Mid Anisian
(Middle Triassic) benthic ecosystem; low abundance, high diversity and dominated by brachiopods and crinoids. Scale bar, 8cm. f, Mid–late Anisian
ecosystem; dominated by marine fishes and reptiles, marking the rebuilding of top-predator trophic structure. Scale bar, 10cm. Drawings ©John Sibbick.
© 2012 Macmillan Publishers Limited. All rights reserved
terrestrial environments take longer to stabilize than marine ones.
Surviving taxa will not all recover equally well — some may adapt
rapidly to new environmental conditions, whereas others may not.
Lower portions of food chains will probably recover rst, followed
by ever higher trophic levels. High-level consumers may recover
early if they are fast speciators (for example, ammonoids), but
they may have to feed on unusual diets until full recovery occurs.
Disaster taxa may show diversity-rst responses, whereas others
may show the more usual disparity-rst patterns. Full recovery is
identied only when ecosystems are complete at all trophic levels,
and represent the longer-term stable pattern.
e contrast between the extrinsic and intrinsic models
exemplies a wider debate about macroevolution — whether the
key driver is the physical environment or biotic interactions
e ‘Red Queen’ model, the idea that large-scale evolution is
driven mainly by ecosystem-scale biotic interaction, contrasts
with the ‘Court Jester’ model, in which macroevolution is driven
by unpredictable perturbations in the physical environment
. e
balance between the Red Queen and Court Jester, as exemplied in
the Triassic recovery of life from near annihilation, may be core to a
comprehensive theory of evolution.
1. Sepkoski,J.J., Jr A kinetic model of Phanerozoic taxonomic diversity, III: Post-
Paleozoic families and mass extinctions. Paleobiology 10, 246–267 (1984).
2. Benton,M.J. Diversication and extinction in the history of life. Science
268, 52–58 (1995).
3. Alroy,J. etal. Phanerozoic trends in the global diversity of marine
invertebrates. Science 321, 97–100 (2008).
4. Van Valen,L. A resetting of Phanerozoic community evolution. Nature
307, 50–52 (1984).
5. Bowring,S.A. etal. U/Pb zircon geochronology and tempo of the end-
Permian mass extinction. Science 280, 1039–1045 (1998).
6. Benton,M.J. e origins of modern biodiversity on land. Phil. Trans. R. Soc.B
365,3667–3679 (2010).
7. Knoll,A.H., Bambach,R.K., Payne,J.L., Pruss,S. & Fischer,W.W.
Paleophysiology and the end-Permian mass extinction. Earth Planet. Sci. Lett.
256,295–313 (2007).
8. Erwin,D.H. Lessons from the past: biotic recoveries from mass extinctions.
Proc. Natl Acad. Sci. USA 98, 5399–5403 (2001).
9. Erwin,D.H. Disparity: morphological pattern and developmental context.
Palaeontology 50,57–73 (2007).
10. Benton,M.J. & Twitchett,R.J. How to kill (almost) all life: the end-Permian
extinction event. Trends Ecol. Evol. 18,358–365 (2003).
11. Benton,M.J., Tverdokhlebov,V.P. & Surkov,M.V. Ecosystem remodelling
among vertebrates at the Permian-Triassic boundary in Russia. Nature
432,97–100 (2004).
12. Brayard,A. etal. Good genes and good luck: Ammonoid diversity and the
end-Permian mass extinction. Science 325,1118–1121 (2009).
13. Stanley,S.M. Relation of Phanerozoic stable isotope excursions to climate,
bacterial metabolism, and major extinctions. Proc. Natl Acad. Sci. USA
107,19185–19189 (2010).
14. Song,H.J. etal. Recovery tempo and pattern of marine ecosystems aer the
end-Permian mass extinction. Geology 39,739–742 (2011).
15. Hallam,A. Why was there a delayed radiation aer the end-Palaeozoic
extinctions? Historical Biology 5, 257–262 (1991).
16. Sahney,S. & Benton,M.J. Recovery from the most profound mass extinction
of all time. Proc. R. Soc. B-Biol. Sci. 275, 759–765 (2008).
17. Chen,Z.Q., Tong, J., Liao, Z.T. & Song, H. Structural changes of marine
communities over the Permian-Triassic transition: Ecologically assessing
the end-Permian mass extinction and its aermath. Global Planet. Change
73,123–140 (2010).
18. Erwin,D.H. A preliminary classication of evolutionary radiations.
Historical Biology 6, 133–147 (1992).
19. Payne,J.L. etal. Large perturbations of the carbon cycle during recovery from
the end-Permian extinction. Science 305, 506–509 (2004).
20. Payne,J.L. etal. Early and Middle Triassic trends in diversity, evenness, and
size of foraminifers on a carbonate platform in south China: implications for
tempo and mode of biotic recovery from the end-Permian mass extinction.
Paleobiology 37,409–425 (2011).
21. Irmis,R.B. & Whiteside,J.H. Delayed recovery of non-marine tetrapods
aer the end-Permian mass extinction tracks global carbon cycle. Proc. R. Soc.
B-Biol. Sci. (2011).
22. Stanley,S.M. An analysis of the history of marine animal diversity.
Paleobiology 33,1–55 (2007).
23. Solé,R.V., Saldana,J., Montoya,J.M. & Erwin,D.H. Simple model ofrecovery
dynamics aer mass extinction. J. eor. Biol. 267,193–200 (2010).
24. Raup,D.M. Biases in the fossil record of species and genera. Bull. Carnegie
Museum Nat. Hist. 13,85–91 (1979).
25. Knoll,A., Bambach,R., Caneld,D. & Grotzinger,J. Comparative earth
history and Late Permian mass extinction. Science 273, 452–457 (1996).
Mid Anisian
Mid–late Anisian
Geological time (8–9 Myr)
Mid–late Anisian
Figure 4 | Stepwise rebuilding pattern of marine ecosystems from low to
top trophic levels in the aftermath of the EPME. Immediate post-extinction
ecosystems in the Griesbachian–Dienerian show only the lowest trophic
level. Further levels are added from Smithian to Anisian, with the topmost
level, of reptiles and large fishes that fed on other vertebrates, fully achieved
only by the mid–late Anisian, 8–9Myr after the mass extinction event.
© 2012 Macmillan Publishers Limited. All rights reserved
26. McGhee,G.R., Sheehan,P.M., Bottjer,D.J. & Droser,M.L. Ecological
ranking of Phanerozoic biodiversity crises: ecological and taxonomic
severities are decoupled. Palaeogeogr. Palaeoclimatol. Palaeoecol.
211, 289–297 (2004).
27. Butchart,S.H. M. etal. National indicators show biodiversity progress
response. Science 329, 900–901 (2010).
28. Barnosky,A. etal. Has the Earths sixth mass extinction already arrived?
Nature 471, 51–57 (2011).
29. McKinney,M. Extinction selectivity among lower taxa - gradational
patternsand rarefaction error in extinction estimates. Paleobiology
21,300–313 (1995).
30. Jablonski,D., Erwin,D.H. & Lipps,J.H. Evolutionary Paleobiology (Chicago
Univ. Press, 1996).
31. Jin,Y., Wang,Y., Wang,W., Shang,Q. & Erwin,D. Pattern of marine mass
extinction near the Permian-Triassic boundary in South China. Science
289,432–436 (2000).
32. Xie,S.C., Pancost,R.D., Yin,H.F., Wang,H.M. & Evershed,R.P. Two
episodes of microbial change coupled with Permo/Triassic faunal mass
extinction. Nature 434, 494–497 (2005).
33. Yin,H.F. etal. e prelude of the end-Permian mass extinction predates a
postulated bolide impact. Int. J. Earth Sci. 96, 903–909 (2007).
34. Chen,Z.Q. etal. Environmental and biotic turnover across the
Permian-Triassic boundary on a shallow carbonate platform in western
Zhejiang, South China. Aust. J. Earth Sci. 56, 775–797 (2009).
35. Shen,al. Calibrating the end-Permian mass extinction. Science
334,1367–1372 (2011).
36. Payne, J.L. & Kump, L. Evidence for recurrent Early Triassic massive
volcanism from quantitative interpretation of carbon isotope uctuations.
Earth Planet. Sci. Lett. 256, 264–277 (2007).
37. Wignall,P.B. Large igneous provinces and mass extinctions. Earth Sci. Rev.
53, 1–33 (2001).
38. Benton,M.J. When Life Nearly Died: e Greatest Mass Extinction of All Time
(ames & Hudson, 2003).
39. Newell,A.J., Tverdokhlebov,V.P. & Benton,M.J. Interplay of tectonics and
climate on a transverse uvial system, Upper Permian, Southern Uralian
Foreland Basin, Russia. Sedim. Geol. 127, 11–29 (1999).
40. Ward, P.D., Montgomery, D.R. & Smith, R.M. H. Altered river morphology
in South Africa related to the Permian-Triassic extinction. Science
289,1741–1743 (2000).
41. Retallack,G.J. Postapocalyptic greenhouse paleoclimate revealed by earliest
Triassic paleosols in the Sydney Basin, Australia. Geol. Soc. Am. Bull.
111,52–70 (1999).
42. Algeo,T.J. & Twitchett,R. Anomalous Early Triassic sediment uxes due
to elevated weathering rates and their biological consequences. Geology
38,1023–1026 (2010).
43. Algeo,T.J., Chen,Z.Q., Fraiser,M.L. & Twitchett,R.J. Terrestrial-marine
teleconnections in the collapse and rebuilding of Early Triassic marine
ecosystems. Palaeogeogr. Palaeoclimatol. Palaeoecol. 308, 1–11 (2011).
44. Wang,C. & Visscher,H. Abundance anomalies of aromatic biomarkers in
the Permian-Triassic boundary section at Meishan, China - Evidence of end-
Permian terrestrial ecosystem collapse. Palaeogeogr. Palaeoclimatol. Palaeoecol.
252, 291–303 (2007).
45. Wignall,P.B. & Twitchett,R.J. Oceanic anoxia and the end Permian mass
extinction. Science 272, 1155–1158 (1996).
46. Yin,H.F., Zhang,K., Tong,J., Yang,Z.Y. & Wu,S. e Global Stratotype
Section and Point (GSSP) of the Permian-Triassic boundary. Episodes
24,102–114 (2001).
47. Taylor,G.K. etal. Magnetostratigraphy of Permian/Triassic boundary
sequences in the Cis-Urals, Russia: No evidence for a major temporal hiatus.
Earth Planet. Sci. Lett. 281, 36–47 (2009).
48. Mundil,R., Pálfy,J., Renne,P. & Brack,P. in e Triassic Timescale Geological
Society Special Publication No. 334 (ed Lucas,S.G.) 41–60 (Geological Society
of London, 2010).
49. Huang,C., Tong,J., Hinnov,L. & Chen,Z. Did the great dying of life take
700k.y.? Evidence from global astronomical correlation of the Permian-
Triassic boundary interval. Geology 39, 779–782 (2011).
50. Retallack,G.J., Veevers,J. & Morante,R. Global coal gap between Permian-
Triassic extinction and Middle Triassic recovery of peat-forming plants.
Geol. Soc. Am. Bull. 108, 195–207 (1996).
51. Retallack,G.J. etal. Multiple Early Triassic greenhouse crises impeded
recovery from Late Permian mass extinction. Palaeogeogr. Palaeoclimatol.
Palaeoecol. 308, 233–251 (2011).
52. Rees,P. Land-plant diversity and the end-Permian mass extinction. Geology
30, 827–830 (2002).
53. Riccardi,A., Arthur,M.A. & Kump,L.R. Sulfur isotopic evidence for
chemocline upward excursions during the end-Permian mass extinction.
Geochim. Cosmochim. Acta 70, 5740–5752 (2006).
54. Kump,L.R., Pavlov,A. & Arthur,M.A. Massive release of hydrogen sulde to
the surface ocean and atmosphere during intervals of oceanic anoxia. Geology
33, 397–400 (2005).
55. Algeo,T.J., Lehrmann,D., Orchard,M. & Tong,J. e Permian-Triassic
boundary crisis and Early Triassic biotic recovery. Palaeogeogr. Palaeoclimatol.
Palaeoecol. 252, 1–3 (2007).
56. Orchard,M. Conodont diversity and evolution through the latest Permian
and Early Triassic upheavals. Palaeogeogr. Palaeoclimatol. Palaeoecol.
252, 93–117 (2007).
57. Stanley,S.M. Evidence from ammonoids and conodonts for multiple
Early Triassic mass extinctions. Proc. Natl Acad. Sci. USA
106, 15264–15267 (2009).
58. Twitchett,R.J., Krystyn, L., Baud, A., Wheeley, J. & Richoz, S. Rapid marine
recovery aer the end-Permian mass-extinction event in the absence of
marine anoxia. Geology 32, 805–808 (2004).
59. Beatty,T., Zonneveld,J. & Henderson,C. Anomalously diverse Early Triassic
ichnofossil assemblages in Northwest Pangea: A case for a shallow-marine
habitable zone. Geology 36, 771–774 (2008).
60. Hofmann,R., Goudemand,N., Wasmer,M., Bucher,H. & Hautmann,M.
New trace fossil evidence for an early recovery signal in the aermath of
the end-Permian mass extinction. Palaeogeogr. Palaeoclimatol. Palaeoecol.
310,216–226 (2011).
61. Brayard,A. etal. Gastropod evidence against the Early Triassic Lilliput eect.
Geology 38, 147–150 (2010).
62. Galfetti,T. etal. Smithian–Spathian boundary event: Evidence for global
climatic change in the wake of the end-Permian biotic crisis. Geology
35,291–294 (2007).
63. Hermann,E. etal. Organic matter and palaeoenvironmental signals during
the Early Triassic biotic recovery: e Salt Range and Surghar Range records.
Sedim. Geol. 234, 19–41 (2011).
64. Grauvogel-Stamm,L. & Ash,S. Recovery of the Triassic land ora from the
end-Permian life crisis. C.R. Palevol 4, 593–608 (2005).
65. Brusatte,S.L. etal. e origin and early radiation of dinosaurs. Earth Sci. Rev.
101, 68–100 (2010).
66. Nesbitt,S.J. etal. Ecologically distinct dinosaurian sister group shows early
diversication of Ornithodira. Nature 464, 95–98 (2010).
67. Twitchett, R.J. Palaeoenvironments and faunal recovery aer the end-Permian
mass extinction. Palaeogeogr. Palaeoclimatol. Palaeoecol. 154, 27–37 (1999).
68. Pruss,S.B. & Bottjer,D.J. Early Triassic trace fossils of the western United
States and their implications for prolonged environmental stress from the end-
Permian mass extinction. Palaios 19, 551–564 (2004).
69. Zonneveld,J.P., Gingras,M.K. & Beatty,T.W. Diverse ichnofossil
assemblages following the P-T mass extinction, Lower Triassic, Alberta
and British Columbia, Canada: evidence for shallow marine refugia on the
northwestern coast of Pangaea. Palaios 25, 368–392 (2010).
70. Knaust,D. e end-Permian mass extinction and its aermath on an
equatorial carbonate platform: insights from ichnology. Te rra Nova
22, 195–202 (2010).
71. Twitchett,R.J. & Wignall,P.B. Trace fossils and the aermath of the
Permo-Triassic mass extinction: Evidence from northern Italy. Palaeogeogr.
Palaeoclimatol. Palaeoecol. 124, 137–151 (1996).
72. Fraiser,M.L. & Bottjer,D.J. Opportunistic behaviour of invertebrate marine
tracemakers during the Early Triassic aermath of the end-Permian mass
extinction. Aust. J. Earth Sci. 56, 841–857 (2009).
73. Chen,Z.Q., Tong,J. & Fraiser,M. Trace fossil evidence for restoration
of marine ecosystems following the end-Permian mass extinction in the
Lower Yangtze region, South China. Palaeogeogr. Palaeoclimatol. Palaeoecol.
299,449–474 (2011).
74. Hautmann,M. etal. An unusually diverse mollusc fauna from the earliest
Triassic of South China and its implications for benthic recovery aer the end-
Permian biotic crisis. Geobios 44, 71–85 (2007).
75. Hallam,A. & Wignall,P.B. Mass Extinctions and eir Aermath (Oxford
Univ. Press, 1997).
76. Fraiser,M.L. & Bottjer,D.J. Restructuring in benthic level-bottom shallow
marine communities due to prolonged environmental stress following the
end-Permian mass extinction. C.R. Palevol 4, 583–591 (2005).
77. Twitchett,R.J. e Lilliput eect in the aermath of the end-Permian
extinction event. Palaeogeogr. Palaeoclimatol. Palaeoecol.
252, 132–144 (2007).
78. Fraiser,M.L., Twitchett,R.J., Frederickson,J., Metcalfe,B. & Bottjer,D.
Gastropod evidence against the Early Triassic Lilliput eect: comment.
Geology 39, E232–E232 (2011).
79. Whiteside,J.H. & Ward,P.D. Ammonoid diversity and disparity track
episodes of chaotic carbon cycling during the early Mesozoic. Geology
39,99–102 (2011).
80. Brayard,A. etal. Transient metazoan reefs in the aermath of the end-
Permian mass extinction. Nature Geosci. 4, 693–697 (2011).
© 2012 Macmillan Publishers Limited. All rights reserved
81. Botha,J. & Smith,R.M. H. Rapid vertebrate recuperation in the Karoo Basin
of South Africa following the End-Permian extinction. J. Afr. Earth Sci.
45,502–514 (2006).
82. Benton,M.J. Dinosaur success in the Triassic: a noncompetitive ecological
model. Q. Rev. Biol. 58, 29–55 (1983).
83. Wignall,P.B. & Benton,M.J. Lazarus taxa and fossil abundance at times of
biotic crisis. J. Geol. Soc. 156, 453–456 (1999).
84. Chen,Z.Q., Kaiho,K. & George,A. Survival strategies of brachiopod
faunas from the end-Permian mass extinction. Palaeogeogr. Palaeoclimatol.
Palaeoecol. 224, 232–269 (2005).
85. Chen,Z.Q., Kaiho,K. & George,A. Early Triassic recovery of the
brachiopod faunas from the end-Permian mass extinction: A global review.
Palaeogeogr. Palaeoclimatol. Palaeoecol. 224, 270–290 (2005).
86. Flügel,E. in Phanerozoic Reef Patterns Vol. 72 (eds Kiessling,W., Flügel,E. &
Golonka,J.) 391–463 (SEPM Special Publication, 2002).
87. Vishnevskaya,V. & Kostyuchenko,A. e evolution of radiolarian
biodiversity. Paleontol. J. 34, 124–130 (2000).
88. O’Dogherty,L., Carter,E., Goričan,Š. & Dumitrica,P. in e Triassic
Timescale Geological Society Special Publications 334 (eds SG Lucas) 163–200
(Geological Society of London, 2010).
89. Twitchett,R.J., Feinberg,J., OConnor,D., Alvarez,W. & McCollum,L. Early
Triassic ophiuroids: eir paleoecology, taphonomy, and distribution. Palaios
20, 213–223 (2005).
90. Chen,Z.Q. & McNamara,K. End-Permian extinction and subsequent
recovery of the Ophiuroidea (Echinodermata). Palaeogeogr. Palaeoclimatol.
Palaeoecol. 236, 321–344 (2006).
91. McGowan,A.J. Ammonoid taxonomic and morphologic recovery patterns
aer the Permian-Triassic. Geology 32, 665–668 (2004).
92. Brusatte,S.L., Benton,M.J., Ruta,M. & Lloyd,G.T. Superiority, competition,
and opportunism in the evolutionary radiation of dinosaurs. Science
321,1485–1488 (2008).
93. Brusatte,S.L., Benton,M.J., Lloyd,G., Ruta,M. &Wang, S.J.
Macroevolutionary patterns in the evolutionary radiation of archosaurs
(Tetrapoda: Diapsida). Earth Env. Sci. Trans. R. Soc. 101, 367–382 (2011).
94. Ruta,M. & Benton,M.J. Calibrated diversity, tree topology and the mother
of all mass extinctions: the lesson of the temnospondyls. Palaeontology
51,1261–1288 (2008).
95. Solé, R.V., Montoya, J.M. & Erwin, D.H. Recovery aer mass extinction:
evolutionary assembly in large-scale biosphere dynamics. Phil. Trans. R. Soc.
B-Biol. Sci. 357, 697–707 (2002).
96. Hu, S.-x. etal. e Luoping biota: exceptional preservation, and new evidence
on the Triassic recovery from end-Permian mass extinction. Proc. R. Soc.
B-Biol. Sci. 278, 2274–2282 (2011).
97. Meyer,K.M. etal. δ
C evidence that high primary productivity delayed
recovery from end-Permian mass extinction. Earth Planet. Sci. Lett.
302,378–384 (2011).
98. Benton,M.J. e Red Queen and the Court Jester: Species diversity
and the role of biotic and abiotic factors through time. Science
323, 728–732 (2009).
99. Carr,T.R. & Kitchell,J.A. Dynamics of taxonomic diversity. Paleobiology
6,427–443 (1980).
100. Gavrilets,S. & Losos,J. Adaptive radiation: contrasting theory with data.
Science 323, 732–737 (2009).
anks to John Sibbick for the spectacular artwork in Fig. 3, and to Ricard Solé
for supplying information for the gure in Box 2. is work was funded by ARC
Discovery Grant DP0770938 to Z.Q.C., NSFC grant 40830212 to J.Tong, the 111
program of China (grant No. B08030) to S.Xie, China Geological Survey Projects (No.
1212010610211, 1212011140051) and NERC grant NE/C518973/1 to M.J.B. is is a
contribution toIGCP572.
Additional information
e authors declare no competing nancial interests. Supplementary information
accompanies this paper on
© 2012 Macmillan Publishers Limited. All rights reserved
... Dated from immediately after the Smithian/Spathian boundary (ca. 249.2 Ma; Widmann et al., 2020), it challenges the often assumed scenario of a globally delayed and slow post-PTB marine biotic recovery (e.g., Erwin, 1998;Sahney and Benton, 2008;Song et al., 2011Song et al., , 2018Chen and Benton, 2012;Benton et al., 2013). This assemblage is all the more remarkable because the Smithian-Spathian transition corresponds to the most severe environmental perturbations documented for the Early Triassic (Tozer, 1982;Dagys, 1988;Hallam, 1996;Payne, 2004;Brayard et al., 2006;Romano et al., 2013;Jattiot et al., 2016;Goudemand et al., 2019;Leu et al., 2019). ...
... We can now assess that this material comprises at least four species representing three superfamilies of Decapoda. In comparison, the renowned and well-studied Anisian Luoping Biota (>18,500 arthropods; Hu et al., 2011), which is often regarded as the first fully recovered marine fauna following the PTB crisis (Hu et al., 2011;Chen and Benton, 2012;Benton et al., 2013), preserves seven species of four different superfamilies of Decapoda (Feldmann et al., 2012;Huang et al., 2013; (Besairie, 1932). Three species of Penaeidae (Ambilobeia karojoi Garrasino and Pasini, 2002;Ifasia dagascariensis (Van Straelen, 1933); Ifasia straeleni Garrasino and Teruzzi, 1995) have been reported from this area. ...
... Additionally, it appears that decapods were already well diversified as soon as the Early Triassic (at least relatively to what is actually known from the rest of the Triassic). This contrasts with the generally assumed model of a delayed post-PTB biotic recovery of Early Triassic marine organisms (e.g., Chen and Benton, 2012). ...
We describe here the early Spathian (Early Triassic) Paris Biota decapod fauna from the western USA basin. This fauna contains two taxa of Aegeridae (Dendobranchiata), namely Anisaeger longirostrus n. sp. and Aeger sp. that are the oldest known representatives of their family, thus extending its temporal range by 5 Myr back into the Early Triassic. This fauna also includes two representatives of Glypheida (Pleocyemata) with Litogaster turnbullensis and Pemphix krumenackeri n. sp., confirming for the former and extending for the latter the temporal ranges of their respective superfamilies back to the Early Triassic. Overall, the Paris Biota decapods are some of the oldest known representatives of Decapoda, filling in an important gap in the evolutionary history of this group, especially during the Triassic that marks the early diversification of this clade. Additionally, we compile and provide overviews for all known Triassic decapods, which leads to the revision of four species of Middle and Late Triassic Aegeridae, and to a revised family assignment of a Middle Triassic Glypheida. Based on this refined dataset, we also investigate decapod diversity throughout the Triassic. We show that the apparent increase in decapod taxonomic richness is probably driven by the heterogeneity of the fossil record and/or sampling effort, and that the decapod alpha diversity is actually relatively high as soon as the Early Triassic and remains rather stable throughout the Triassic. UUID:
... G lobal warming at the end-Permian initiated the most adverse and extended environmental crisis in the Phanerozoic [1][2][3][4][5] . This is the only known climate perturbation where carbon release rates and the initial pace of warming may have been comparable to modern rates [6][7][8][9] . ...
... A rapid temperature rise of >10°C 2,10 , acidification 11 , and marine O 2 decline 12,13 drove a massive loss in biodiversity and a major shift in marine ecosystem structure 5 . An estimated 85-95% of all marine animal species went extinct across the latest Permian/ Early Triassic transition-making it the most severe extinction event in Earth's history 1,5,13 . Despite the growing consensus for a causal link between the establishment of warm and anoxic oceans and the widespread loss of marine biodiversity 4,12,13 , basic aspects of the end-Permian crisis remain enigmatic. ...
... There is abundant evidence from the geologic record for a dramatic perturbation to the global silica cycle at the end-Permian. Perhaps most prominently, a pronounced collapse in both the diversity and abundance of siliceous organisms at the end-Permian crisis-commonly referred to as the Early Triassic "chert gap"-has been described in sections worldwide 1,39,[43][44][45] . Here, we present a global compilation (36 localities) of sedimentary chert (biogenic silica, nodules, and silica replacement) occurrences across the Late Permian to Middle Triassic interval that highlights this regime shift ( Fig. 4 and Supplementary Fig. 1). ...
Full-text available
In the wake of rapid CO2 release tied to the emplacement of the Siberian Traps, elevated temperatures were maintained for over five million years during the end-Permian biotic crisis. This protracted recovery defies our current understanding of climate regulation via the silicate weathering feedback, and hints at a fundamentally altered carbon and silica cycle. Here, we propose that the development of widespread marine anoxia and Si-rich conditions, linked to the collapse of the biological silica factory, warming, and increased weathering, was capable of trapping Earth’s system within a hyperthermal by enhancing ocean-atmosphere CO2 recycling via authigenic clay formation. While solid-Earth degassing may have acted as a trigger, subsequent biotic feedbacks likely exacerbated and prolonged the environmental crisis. This refined view of the carbon-silica cycle highlights that the ecological success of siliceous organisms exerts a potentially significant influence on Earth’s climate regime. The widespread disappearance of siliceous life sustained extreme temperatures in the wake of Earth’s most severe mass extinction event.
... However, little is known of the upper trophic level predators of such a lacustrine ecosystem, except that 'higher-order trophic levels being represented by predatory fish' was mentioned (Zhao et al., 2020). Large predators at upper trophic levels are highly susceptible to environmental fluctuations and stress (Steneck, 2012); thus, the recovery dynamics of large predators provides a key proxy for evaluating ecosystem recovery after extinction events (Chen and Benton, 2012;Scheyer et al., 2014). ...
... The recovery of marine ecosystems is thought to be delayed and stepwise because of harsh marine and terrestrial conditions after the EPME (Algeo et al., 2011;Chen and Benton, 2012). A marine ecosystem with a stable, complex structure did not re-emerge until the Middle Triassic (Chen and Benton, 2012). ...
... The recovery of marine ecosystems is thought to be delayed and stepwise because of harsh marine and terrestrial conditions after the EPME (Algeo et al., 2011;Chen and Benton, 2012). A marine ecosystem with a stable, complex structure did not re-emerge until the Middle Triassic (Chen and Benton, 2012). Lacustrine fossil records tend to be sporadic and fragmentary (Cohen, 2003;Benton and Newell, 2014), hence, the reconstruction of a lacustrine ecosystem is challenging. ...
The early Ladinian lacustrine ecosystem of the Chang 7 Member in the Ordos Basin was proposed as the earliest known Mesozoic-type, trophically multileveled lacustrine ecosystem after the end-Permian mass extinction (EPME). However, limited evidence of higher-order trophic levels represented by predatory fish has made this conclusion elusive. In this study, we investigated the external morphology, food inclusions, and geochemical composition of 54 vertebrate coprolites from organic-rich lacustrine sediments of Chang 7 Member, Yanchang Formation, in the Bawangzhuang section, Tongchuan City, Shaanxi Province, China. These coprolites were identified as seven morphotypes in three groups: three heteropolar spiral forms, two amphipolar spiral forms, and two non-spiral forms. Preserved inclusions (fish scales, bone fragments, teeth) indicated that the producers of these coprolites were piscivorous animals. Compared with coprolites previously researched, all coprolites described herein were inferred to be produced by fish: three heteropolar types of spiral coprolites derived from three types of hybodonts, two amphipolar spiral coprolites from coelacanth or Saurichthys with simple spiral valves, and non-spiral coprolites from at least two predatory actinopterygians. Thus, the biodiversity of the lacustrine paleoecosystem, particularly that of predators with upper trophic levels, was substantially enriched. The existence of large carnivorous predators of different taxa as apex predators in a trophically multileveled (at least six levels) lacustrine ecosystem indicates that the early Ladinian lacustrine ecosystem of the Ordos Basin marks the rebuilding of the top-predator trophic structure in the lacustrine ecosystem after the EPME.
... Although the oldest archosauromorphs are recorded in strata as old as Wuchiapingian (Permian), the early diversification of the group is detected in the aftermath of Earth's deadliest biotic crisis, the end-Permian mass extinction (∼252 million years) (Raup, 1979;Erwin, 1994;Chen and Benton, 2012). Soon after this event, archosauromorphs diversified and became abundant in most ecosystems across Pangea . ...
Early Triassic archosauriform remains are often related to the Proterosuchidae and the Erythrosuchidae, common stem-archosaurs in the aftermath of the end-Permian extinction event. South American proterosuchid remains are rare, with only a few specimens from the Lower Triassic Sanga do Cabral Formation briefly mentioned in literature. The Lower Triassic Sanga do Cabral Formation has a growing fossil record, thus far composed of procolophonids, temnospondyls, and early-branching archosauromorphs. In this work, new materials referred to cf. Chasmatosuchus and cf. Proterosuchus (Archosauriformes) are described, representing the first conclusive archosauriform records from the Lower Triassic of Brazil. Proterosuchids are among the stratigraphically oldest Archosauriformes, with their earliest unambiguous occurrences coming from the uppermost Permian of Russia. This clade is widely spread among well-explored Lower Triassic formations, flourishing during the recovery phase from the end-Permian mass extinction. The presence of nonarchosaurian archosauriforms in southwestern Gondwana reinforces the rapid diversification of archosauromorphs during the Early Triassic. The Sanga do Cabral Formation fossil assemblage is becoming important for understanding how the initial adaptive radiation of archosauromorphs took place.
... Although the recovery of nekton occurred at the same time as the full rebound of infaunal ecosystem engineering activities, their positive feedback effects remain partly undetermined. However, phylogenetic study of coeval fishes and marine reptiles has shown that explosive diversification occurred in the Early Triassic (39,40). These innovations and diversification were part of the opportunistic refilling of ecospace after the mass extinction (41,42). ...
Full-text available
The Permian-Triassic mass extinction severely depleted biodiversity, primarily observed in the body fossil of well-skeletonized animals. Understanding how whole ecosystems were affected and rebuilt following the crisis requires evidence from both skeletonized and soft-bodied animals; the best comprehensive information on soft-bodied animals comes from ichnofossils. We analyzed abundant trace fossils from 26 sections across the Permian-Triassic boundary in China and report key metrics of ichnodiversity, ichnodisparity, ecospace utilization, and ecosystem engineering. We find that infaunal ecologic structure was well established in the early Smithian. Decoupling of diversity between deposit feeders and suspension feeders in carbonate ramp-platform settings implies that an effect of trophic group amensalism could have delayed the recovery of nonmotile, suspension-feeding epifauna in the Early Triassic. This differential reaction of infaunal ecosystems to variable environmental controls thus played a substantial but heretofore little appreciated evolutionary and ecologic role in the overall recovery in the hot Early Triassic ocean.
... The draft genomes of softshell turtle and green sea turtle yield insights into the development and evolution of the turtlespecific body plan 7 0 2 VOLUME 45 | NUMBER 6 | JUNE 2013 Nature GeNetics l e t t e r s to the Upper Permian to Triassic period (Fig. 1b), overlapping or following shortly after the Permian extinction event 11 ; this raises the question of whether the emergence of the turtle group was related to this severe extinction event, which especially involved the extinction of marine species. ...
Full-text available
The unique anatomical features of turtles have raised unanswered questions about the origin of their unique body plan. We generated and analyzed draft genomes of the soft-shell turtle (Pelodiscus sinensis) and the green sea turtle (Chelonia mydas); our results indicated the close relationship of the turtles to the bird-crocodilian lineage, from which they split ~267.9–248.3 million years ago (Upper Permian to Triassic). We also found extensive expansion of olfactory receptor genes in these turtles. Embryonic gene expression analysis identified an hourglass-like divergence of turtle and chicken embryogenesis, with maximal conservation around the vertebrate phylotypic period, rather than at later stages that show the amniote-common pattern. Wnt5a expression was found in the growth zone of the dorsal shell, supporting the possible co-option of limb-associated Wnt signaling in the acquisition of this turtle-specific novelty. Our results suggest that turtle evolution was accompanied by an unexpectedly conservative vertebrate phylotypic period, followed by turtle-specific repatterning of development to yield the novel structure of the shell.
... Extinction patterns among benthos varied between shallowand deep-water facies according to previous PTME investigations (e.g., Groves et al., 2005;Shen et al., 2006;Chen and Benton, 2012). To examine the intrinsic connection about various extinction patterns among environments of different water depths, we here investigated the lithologic succession and benthonic assemblages from Late Permian to Early Triassic in two adjoining sections. ...
Full-text available
The divergent patterns of Permian–Triassic mass extinction (PTME) have been extensively documented in varying water depth settings. We here investigated fossil assemblages and sedimentary microfacies on high-resolution samples from two adjacent sections of the South China Block: Chongyang from shallow-water platform and Chibi from deeper-water slop. At Chongyang, abundant benthos (over 80%), including rugose corals, fusulinids, calcareous algae, and large foraminifers, disappeared precipitously at the topmost of Changxing Formation grainstone, which suggested complete damage of the benthic ecosystem, confirming a sudden single-pulse extinction pattern. The end-Permian regression, marked by a karst surface, provided a plausible explanation for this extinction pattern. Whereas for the fauna in Chibi, the benthos was relatively abundant (20%–55%) with more trace fossils and lacking calcareous algae. Benthic abundance in Chibi reduced by two steps at the two claystone beds (Beds 10 and 18): bioclastic content dropped from an average of 50% in Beds 1–9 to 10% in Beds 11–17 and then to less than 5% in Beds 19–23, suggesting a two-pulse extinction. At the first pulse, large foraminifers were prominent victims in both shallow- and deeper-water settings. A plausible survival strategy for small-sized foraminifers was to migrate to deeper water to avoid extreme heat in shallow water. The early Triassic transgression prompted some small foraminifers to migrate back to original platforms and flourish briefly as disaster forms. At the Early Triassic mudstone with bottom-water settings in Chibi, the appearance of abundant small pyrite framboids (diameters of 4.74–5.96 μm), an indicator of intensified oxygen deficiency, was simultaneous with the two-step reduction of benthic diversity and abundance. Thus, anoxic conditions might be the main cause of the PTME at deeper-water settings. Our study is an example of the wider debate about biotic response to rapid environmental change for both the Permian–Triassic transition and modern days.
... The first marine reptiles are known from the late Early Triassic, including ichthyosaurs, nothosaurs and pachypleurosaurs, while placodonts and thalattosaurs emerged soon after, in the early Middle Triassic (Chen et al. 2012;Liu et al. 2014). These marine reptiles swam in shallow seas around Pangaea, feeding generally on small to large prey ranging from crustaceans and other invertebrates to fishes. ...
Humanity has triggered the sixth mass extinction episode since the beginning of the Phanerozoic. The complexity of this extinction crisis is centred on the intersection of two complex adaptive systems: human culture and ecosystem functioning, although the significance of this intersection is not properly appreciated. Human beings are part of biodiversity and elements in a global ecosystem. Civilization, and perhaps even the fate of our species, is utterly dependent on that ecosystem's proper functioning, which society is increasingly degrading. The crisis seems rooted in three factors. First, relatively few people globally are aware of its existence. Second, most people who are, and even many scientists, assume incorrectly that the problem is primarily one of the disappearance of species, when it is the existential threat of myriad population extinctions. Third, while concerned scientists know there are many individual and collective steps that must be taken to slow population extinction rates, some are not willing to advocate the one fundamental, necessary, ‘simple’ cure, that is, reducing the scale of the human enterprise. We argue that compassionate shrinkage of the human population by further encouraging lower birth rates while reducing both inequity and aggregate wasteful consumption—that is, an end to growthmania—will be required. This article is part of the theme issue ‘Ecological complexity and the biosphere: the next 30 years’.
Full-text available
The end-Permian mass extinction was the most catastrophic event for life in the Phanerozoic eon because it impacted numerous organisms, from micro-sized photosynthetic organisms to large (meter-long) animals and fundamentally altered marine and terrestrial ecosystems. C33 n-alkyl cyclohexane (C33-ACH), an angstrom-size molecular fossil of phytoplankton, has been widely found in Permian–Triassic (P-Tr) marine sediments, associated with the collapse of the marine ecosystems at the end-Permian mass extinction. Here, we describe multiple C33-ACH spikes in the Lower Triassic succession at the Chaohu section of the South China Block, which imply that phytoplankton blooms occurred repeatedly during the early–middle Early Triassic. Comparison with previous studies shows that C33-ACH was not only globally enriched at the P-Tr boundary, but also abundant at the Induan–Olenekian boundary and middle Smithian in both the South China and Boreal seas. In addition, the Chaohu section record reveals a C33-ACH peak at the Smithian–Spathian boundary. Moreover, the C33-ACH spikes were synchronous with the peaks of mercury and the pristane/phytane (Pr/Ph) ratio. Since the peaks in mercury and the Pr/Ph ratio indicate increased volcanic activity and large influxes of terrestrial source material into the ocean, the correspondence between the high abundance of C33-ACH with mercury and Pr/Ph ratio peaks implies that volcanism and riverine nutrient input fertilized the surface phytoplankton, which triggered the expansion of anoxia that in turn delayed the benthic metazoan recovery.
Full-text available
The cause of the great Permian-Triassic (P-T) boundary mass extinctions remains unknown. A crucial step in identifying the cause involves a precise timing of the mass extinction interval (MEI) in order to reconstruct the pattern of biotic evolution and the chronologic record of potential triggers. Here we present an estimate of the P-T boundary MEI duration based on astronomical tuning of multiple cyclic sedimentary records. Magnetic susceptibility data from Shangsi, southern China, provide evidence for strong 405 k.y. orbital eccentricity forcing throughout the P-T boundary interval. Radioisotope dating combined with 405 k.y. tuning provides an absolute time scale through the P-T boundary interval at unprecedented high resolution. An estimated similar to 700 k.y. duration for the MEI at Shangsi is supported by eccentricity tuned estimates of four other sections in China and Austria. In addition, at Shangsi, the onset of mass extinction occurred shortly following a coincidence of minima in the observed similar to 1.5 m.y., 405 k.y., and similar to 100 k.y. cycles. A change in the magnetic susceptibility response to astronomical forcing occurred just prior to the onset of extinction, with reduced 100-k.y.-scale cyclicity continuing into the Early Triassic for more than 2 m.y.
A general model of taxonomic diversity, incorporating diversity-dependent rates of origination and extinction, is constructed to examine the dynamic responses of diversity to perturbation. The model predicts that the trajectories of diversification increase and decrease are substantially different. The trajectories of diversity during disequilibrium conditions are displayed in phase diagrams to permit a simple graphical analysis of stability. A positive displacement of diversity from equilibrium results in a rapid decline in diversity and may involve an initial overshoot of the equilibrium condition. A negative displacement of equal magnitude results in a gradual increase in diversity. The model is expressed as a nonlinear difference equation to incorporate intrinsically a delay time due to the characteristic noninstantaneous response of origination and extinction. The model initially assumes a parabolic curve expressing total taxon origination rate as a function of diversity. A second model, constructed assuming a sigmoidal total taxon origination rate derived from considerations of allopatric speciation, enhances the asymmetry of the diversity response. The delayed recovery of the Triassic fauna is shown to be characteristic of return to equilibrium from an undersaturated condition, whereas the more rapid “catastrophic” decline in the Late Permian fauna is shown to be characteristic of return to equilibrium from the oversaturated condition. It is proposed, although not assumed, that perturbation may include a degree of selectivity related to the dispersal abilities of organisms, thereby enhancing the observed asymmetry.
Radiolarians are protozoans that have existed for more than 500 million years. Paleozoic radiolarians (dating from 550-250 million years ago) were represented by three orders, 16 families, and 76 genera. Eighty per cent of Paleozoic radiolarians did not survive beyond the Paleozoic-Mesozoic boundary. Mesozoic Radiolaria (245-65 million years ago) were represented by three orders (two of which continued from the Paleozoic and one that appeared in the Mesozoic), 49 families, and 256 genera. The total number of known Cenozoic and recent Radiolaria is almost 5000 species. Analysis of radiolarian biodiversity over time reveals a trend toward decreasing numbers of the order Nasselaria contrasting with relatively stable or even increasing number of Spumellaria.
Documenting past environmental disturbances will provide a very incomplete explanation of extinctions until more data on intrinsic (e.g., phylogenetic) responses to disturbances are collected. Taxonomic selectivity can be used to infer phylogenetic inheritance of extinction-biasing traits. Selectivity patterns among higher taxa, such as between mammals and bivalves, are well documented. Selectivity patterns among lower taxa (genus, species) have great potential for understanding the dynamics underlying higher taxic turnover. Two echinoid data sets, of fossil and living taxa, indicate that species extinctions do not occur randomly within genera. Reverse rarefaction estimates of past species extinction rates assume random species extinction within higher taxa, so these widely cited extinction estimates may be inaccurate. Revised estimates based on a simulated curve imply that past species extinctions rates may be 6%–15% lower than previously cited. Possible causes for the observed selectivity patterns are discussed. These include nonrandom phylogenetic nesting of species with traits often cited as enhancing extinction vulnerability, into certain taxa. Such traits include low abundance, large body size, narrow niche breadth, and many others. Phylogenetic nesting of extinction-biasing traits at many taxonomic levels does not predict that a dichotomy of mass-background selectivity based on a few traits will occur. Instead, it predicts patterns of selectivity at many taxonomic levels, and at many spatio-temporal scales.
Analysis of 16 marine Permian-Triassic boundary sections with a near-global distribution demonstrates systematic changes in sediment fluxes and lithologies in the aftermath of the end-Permian crisis. Sections from continent-margin and platform settings exhibit higher bulk accumulation rates (BARs) and more clay-rich compositions in the Griesbachian (earliest Triassic) relative to the Changhsingian (latest Permian). These patterns, which largely transcend regional variations in tectonic setting, sequence stratigraphic factors, and facies, are hypothesized to have resulted from a substantial (average similar to 7x) increase in the flux of eroded material from adjacent land areas owing to accelerated rates of chemical and physical weathering as a function of higher surface temperatures, increased acidity of precipitation, and changes in landscape stability tied to destruction of terrestrial ecosystems. This sediment surge may have been a contributory factor to the latest Permian marine biotic crisis as well as to the delayed recovery of Early Triassic marine ecosystems owing to the harmful effects of siltation and eutrophication. Contemporaneous deep-sea sections show no increases in sediment flux across the Permian-Triassic boundary owing to their remoteness from continental siliciclastic sources and location below the paleo-carbonate compensation depth.
Episodes of mass extinction represent the largest events of biodiversity loss known in the geologic record, and may provide tests of biodiversity-ecosystem stability hypotheses. Here we present the first correlation between ammonoid diversity and disparity and ecosystem stability as represented by stable carbon isotopic records spanning the end-Permian through end-Triassic mass extinctions. Ammonoid generic richness from a single biogeographic realm shows that nearly all taxa disappeared coincident with major carbon isotopic shifts to lighter values. The intervals following these two major mass extinctions were characterized by multiple positive-negative couplets of chaotic carbon cycling and were composed of low-richness ammonoid faunas characterized by higher proportions of passively floating, non-swimming morphotypes than before or after. In contrast, richness was highest during intervals of stable carbon isotope values. We propose that these "chaotic carbon episodes" reflect the breakdown of functional redundancy in the ecosystem, and that the post-extinction carbon cycle did not stabilize until redundancy was restored.
The early evolutionary history of Ornithodira (avian-line archosaurs) has hitherto been documented by incomplete (Lagerpeton) or unusually specialized forms (pterosaurs and Silesaurus). Recently, a variety of Silesaurus-like taxa have been reported from the Triassic period of both Gondwana and Laurasia, but their relationships to each other and to dinosaurs remain a subject of debate. Here we report on a new avian-line archosaur from the early Middle Triassic (Anisian) of Tanzania. Phylogenetic analysis places Asilisaurus kongwe gen. et sp. nov. as an avian-line archosaur and a member of the Silesauridae, which is here considered the sister taxon to Dinosauria. Silesaurids were diverse and had a wide distribution by the Late Triassic, with a novel ornithodiran bauplan including leaf-shaped teeth, a beak-like lower jaw, long, gracile limbs, and a quadrupedal stance. Our analysis suggests that the dentition and diet of silesaurids, ornithischians and sauropodomorphs evolved independently from a plesiomorphic carnivorous form. As the oldest avian-line archosaur, Asilisaurus demonstrates the antiquity of both Ornithodira and the dinosaurian lineage. The initial diversification of Archosauria, previously documented by crocodilian-line archosaurs in the Anisian, can now be shown to include a contemporaneous avian-line radiation. The unparalleled taxonomic diversity of the Manda archosaur assemblage indicates that archosaur diversification was well underway by the Middle Triassic or earlier.