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

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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.
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L
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
1,4–6
.
e disappearance of ~90% of skeletonized marine species
7
marked the end of Palaeozoic marine faunas and the rise of the
replacing ‘modern fauna
1
. 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
8–11
. 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
8,15,18–21
, complex ecosystem interactions
9,14,22,23
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
1
and Michael J. Benton
2
*
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
1,2,24–26
.
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
27,28
.
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
10,24,29,30
. 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
31
. 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
2
concentrations and global anoxia, euxinia (anoxic
and sulphidic conditions), hypercapnia (CO
2
poisoning), a bolide
impact, rapid global warming and plume-induced volcanic
eruption
36
. e most widely accepted model
7,10,37,38
begins with
eruption of the Siberian traps, huge volumes of basaltic lava that
produced CO
2
, which led to global warming and the short-term
1
State Key Laboratory of Biogeology and Environmental Geology, China University of Geosciences, Wuhan 430074, China.
2
School of Earth Sciences,
University of Bristol, Bristol, BS8 1RJ, UK. *e-mail: Mike.Benton@bristol.ac.uk
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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
39,40
. e massive
erosion was associated with wildres, perhaps triggered during
the unusually arid conditions
35
. Sedimentation rates in terrestrial
successions increased
41
and there was an abrupt, increased inux
of terrigenous siliciclastics to the oceans
42,43
, associated with soil-
derived biomarkers
44
.
In marine environments, heightened CO
2
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
45
. Furthermore, interaction between
Siberian-trap magma and organic-rich sedimentary rocks could
have greatly increased release of CO
2
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
37
.
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
35,46
. e EPME was calibrated to the base
of a volcanic ash bed just below the PTB in the Meishan section,
south China
31
, 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
48
and astrochronology
49
. Terrestrial
successions are harder to date accurately, but a combination of
radiometric dating, magnetostratigraphy and chemostratigraphy is
improving the situation
35,47,48
.
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
precipitation
43
. ese unusual conditions are matched by the ‘coral
gap, when there were no reefs built by colonial metazoans in shallow
water
3,43
, and the ‘coal gap
50–52
on land, during which forests, and
hence coal deposits, were absent (Fig.1).
Anoxia has long been documented as a key element of the
EPME
35–45
, and it seems to have been a recurring condition
throughout the Early Triassic
19,36
. Upwelling of CO
2
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
7
. Oceanic euxinia (anoxic and
sulphur-rich stratied ocean) is indicated by the loss of dissolved
oxygen and free H
2
S in the water column, as shown by biomarkers,
pyrite framboid sizes, S-isotopic compositions and Ce anomalies
43,53
.
e massive release of sulphides into the oceans adds H
2
S toxicity to
the cocktail of potential killers
54
.
Redox changes may have been caused either by chemocline-
upward excursions
53,54
or by upwelling of deep anoxic water
masses
43,55
. ese massive changes in seawater chemistry are
attested by repeated C-isotopic excursions
19
, but the origins of these
are uncertain. Clues may come from correlations with uctuations
in other geochemical proxies, such as
29
C/
30
C hopane and 2-MHP
biomarker ratios, and increased concentrations of
34
S-depleted
pyrite
53–55
, which can indicate upwelling of
13
C-depleted, sulphidic
deep waters.
End-Permian
mass extinction
Environments
Time-
scale
Age
242
244
246
Macroalgae
Microbialites
Deep sea
Shallow sea
Bioturbation level
Seafloor carbonate precipitates
CoralsCORAL GAP
Radiolarians
Foraminifera
Burrow depth, size and complexity
Ammonoids
Plants
Tetrapods
Brachiopods
Metazoan reefs
CHERT GAP
COAL GAP
Conodonts
Ophiuroids
248
STLIP eruption
250
252
Vol.
Anoxia
Unusual
facies
Trace
fossils
Reefs, reef-
builders, cherts
Ma
–2 02468
Marine ecosystems
Biodiversity changesBiodiversity changes
Te rrestrial ecosystems
13
C (

)
Illy.
Middle TriassicEarly Triassic
OlenekianInduan
Gr. Sm. Ae. Bith.Spathian PelsonianDi.
Anisian
Late
Permian
Changh-
singian
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.
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Negative excursions in carbon isotope ratios, indicating
repeated greenhouse crises
51
, 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
2
were repeatedly released from coal beds
51
or
frequent volcanic eruptions
36
.
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
12
and
conodonts
56,57
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
predicted
58–61
. 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
14
. 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
19,20,56,62
and on land
11,16,21
, so global species and ecosystem
stability had not yet been achieved.
e recovery of life on land indicates similar patterns
11,16,21,51
.
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
62–64
, resulting in reduced sequestration of organic matter
in terrestrial facies during the Early Triassic coal gap
50–52
. 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
62,63
.
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
11
. 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
65,66
.
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)
65
, rhynchosaurs and
diademodont cynodonts.
Trace fossils (burrows and trails) provide alternative evidence for
recovery patterns, especially in the sea
67,68
. Although several diversity
spikes among trace fossils have been recognized from the Induan
age
59,69,70
, multiple lines of evidence, including diversity, burrow
size, complexity, tiering levels and bioturbation levels, show that
trace fossil assemblages recovered in the Spathian
67,68,71–73
(Fig.1).
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
96
, 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
conodonts
96
. 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
a
b
c
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Several benthic assemblages were found to be rather diverse in the
aermath of the EPME, indicating an earlier benthic recovery
58,74
.
However, benthic communities in most areas of the world remained
at low diversity through the Early Triassic
17,75,76
.
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
14,77,78
; although,
body sizes of some clades (for example, gastropods
61
) 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
19
.
Slow or fast recovery?
A key question concerns the timing of Triassic recovery. e
standard view
8,15,18–21,43,79
is that the recovery lasted some 5–9Myr,
whereas others
14,61,80
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
81
, 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
11,16,82
. 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
20
.
Delayed recovery could reect poor sampling in the Early
Triassic
12
. 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
83
. 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
12,56
. 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
12
, 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
23
: 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
23
, the lag time to biotic recovery increases
signicantly as biotic interactions become more important in the
recovery process, an example of positive feedback
9
. ese models
are developed with equilibrium assumptions — of the world before
and aer extinction having a xed carrying capacity— that have
been questioned
99
.
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
23,95
, 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
rate
23
. 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
20
.
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
100
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
a
b
c
0 100 200 300 400 500
40 50 60 70 80 90 100
40 60 80 100 120 140
0.0
0.25
0.5
0.75
1.0
0.0
0.25
0.5
0.75
1.0
0.0
0.25
0.5
0.75
1.0
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a single clade, the Ceratitina, and the global diversity of ammonoids
did not reach maximum levels until the mid Anisian
79
.
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
14
.
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
84,85
.
Corals suered a major diversity loss in the EPME and did not
re-occur until the middle Anisian
86
. is is also true for radiolarians,
a clade that suered a large depletion in diversity during the Early
Triassic and early Anisian
87,88
. Among echinoderms, crinoids were
absent for much of the Early Triassic and rebounded at the end of
the Spathian
89
, whereas ophiuroids experienced diversity increase
and geographic expansions immediately aer the EPME (ref.90).
Habitat may also matter. It has been argued
14,20
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
14
.
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
8
, and
a wider ecological approach is essential
3
. For example, ammonoid
diversity rose in the Smithian (Fig. 1), but their morphological
disparity (range of form) did not expand until the end-Spathian
91
.
is diversity-rst model may not be ubiquitous, however, and many
tetrapod groups in the Triassic show the more typical disparity-rst
pattern
92–94
. 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
22,23,57
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
14
, but ought to be considered
together with intrinsic rates of evolution of each clade
22,57
. Here, we
broaden the ecological network model
23,95
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
76
. 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
17
.
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
17
(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
96
(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
MC
2
P
2
P
1
Rb
MC
1
PC
PP
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
1
), such as endo-faunal trace-markers;
meso-consumers (MC
2
), such as benthos; reef-building meso-consumers
(Rb); predatory invertebrates (P
1
), such as gastropods; and predatory fishes
and reptiles (P
2
).
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from low to top trophic levels through Early–Middle Triassic
times (Fig.4) following logistic growth of biotic recovery, based on
theoretical modelling
23,95
.
Reasons for delayed recovery
Life began to recover quickly in the Early Triassic, but full recovery
took some 8–9 Myr
8,15,18–20,97
in the sea, and the same or longer
on land
11,16,21
. 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
95
,
resistant to environmental perturbation. According to these models,
delay to recovery is proportional to the amount of interaction
between species
23
.
Even though biotic interactions may have played a role and some
taxa were little aected by extrinsic perturbations
12,14,22,61,80
, it is widely
accepted
3,7,15,19,21,22,51,57,67,97
that poor environmental conditions in the
post-extinction world slowed full recovery. An exception may be
the benthic foraminifera
14
, which radiated slowly through the Early
Triassic, and at most were aected by the end-Smithian event
62
. In
a further example, metazoan reefs have been reported
80
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
32,97
by favouring bacteria. Observed bursts of primary productivity
immediately aer the EPME
32
and later in the earliest Triassic
43
seem
to relate to phases of terrestrial erosion and ushing of sediment into
the sea
43
. 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
abc
def
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.
REVIEW ARTICLE
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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
6,9,20,98
.
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
98
. 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.
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Acknowledgements
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 www.nature.com/naturegeoscience.
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... 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). ...
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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: http://zoobank.org/0f435f27-1767-473d-955c-57fe869faa0f
... 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). ...
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... 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. ...
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... 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 . ...
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... 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). ...
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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. ...
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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. ...
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... 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. ...
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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’.
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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.
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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.
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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.
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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.
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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.
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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.
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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.
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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.