492
PERSPECTIVES
National Science Review, 2014, Vol. 1, No. 4
the split between actinopterygians and
sarcopterygians [7, 8]. However, the tandem duplications of sparc1 genes that
gave rise to acidic SCPP genes might
have happened before the split between
chondrichthyans and osteichthyans (unlike [8]), possibly at the node where perichondral bone arose [5].
REFERENCES
1. Karsenty, G. Nature 2003; 423: 316–8.
2. Boyle, WJ, Simonet, WS and Lacey, DL. Nature
2003; 423: 337–42.
3. Hall, BK. Bones and Cartilage: Developmental Skeletal Biology. Amsterdam: Elsevier,
2005.
4. Eames, BF, Allen, N and Young, J, et al. J Anat
2007; 210: 542–4.
5. Ryll, B, Sanchez, S and Haitina, T et al. Evol Dev
Min Zhu
Institute of Vertebrate Paleontology and
Paleoanthropology, Chinese Academy of Sciences,
2014; 16: 123–4.
6. Kawasaki, K and Weiss, KM. J Dent Res 2008; 87:
520–53.
China
E-mail: [email protected]
GEOSCIENCES
Special Topic: Paleontology in China
The end-Permian mass extinction: a still
unexplained catastrophe
Shu-zhong Shen1,∗ and Samuel A. Bowring2
The end-Permian mass extinction is
widely regarded as the largest mass extinction in the past 542 million years with
loss of about 95% of marine species and
75% of terrestrial species. There has been
much focus and speculation on what
could have caused such a catastrophe.
Despite decades of study, the cause or
causes remain mysterious. Numerous
scenarios have been proposed, including
asteroid impact, Siberian flood basalt
volcanism, marine anoxia and euxinia,
sea-level change, thermogenic methane
release and biogenic methane release due
to explosive growth of a methanogenic
microbe.
It is now clear that a number of major
environmental perturbations are approximately coincident with the end-Permian
mass extinction. These include global
negative excursions of both δ 13 Ccarb and
δ 13 Corg near the extinction interval (see a
review by Korte and Kozur [1] and a recent study by Shen et al. [2]); distinctive
calcium isotope excursions [3]; a sudden
expansion of microbialites [4]; a rapid
temperature rise of ∼8◦ C in the extinction interval [5] followed by a long ‘hothouse’ period in the Early Triassic [6],
large regression followed by rapid transgression [7], evidence for wildfires and
cyanobacteria blooms [8], etc. There remains disagreement over the nature, timing and duration of the environmental
perturbations and how they relate to detailed patterns of extinction, resolution
of which is critical for understanding the
causative mechanism(s).
TIMING AND DURATION
The timing and duration of the endPermian extinction at the Meishan sections in South China has been studied
for over two decades. In many ways, successive publications track the evolution
of high-precision U-Pb geochronological
techniques that have led to increasingly
precise and accurate constraints on the
extinction.
7. Kawasaki, K, Buchanan, AV and Weiss, KM. Annu
Rev Genet 2009; 43: 119–42.
8. Venkatesh, B, Lee, AP and Ravi, V, et al. Nature
2014; 505: 174–9.
9. Donoghue, PCJ, Sansom, IJ and Downs, JP. J Exp
Zool Part B 2006; 306: 278–94.
10. Brazeau, MD. Nature 2009; 457: 305–8.
11. Zhu, M, Yu, XB and Ahlberg, PE, et al. Nature
2013; 502: 188–93.
12. Friedman, M and Brazeau, MD. Nature 2013; 502:
175–7.
doi: 10.1093/nsr/nwu062
Advance access publication 10 October 2014
Burgess et al. [9] review the evolution of increasing precise and accurate
geochronological constraints on the
age and duration of the extinction. For
example, the published ages of Bed 25
at Meishan have varied from 251.4 ±
0.3 to >254 Ma and the duration of
the extinction from 500 to 61 ± 48 kyr.
The latter reflects the latest work using
EARTHTIME protocols [9]. In addition
to U-Pb zircon geochronology of ash
beds, the floating astronomical time scale
(ATS) has been applied to the extinction
interval at Meishan and Shangsi. The
ATS is based on recognizing astronomically forced stratigraphy and the latest
effort has yielded an extinction duration
of 112 kyr at Meishan and 83 kyr at
Shangsi in South China [10]. Thus,
both the most recent high-precision
CA-TIMS U-Pb dates and the ATS are
consistent with a catastrophic event that
occurred in less than 100 kyr. Higher
temporal resolution estimates from
Shangsi and Meishan will likely be
limited by the condensed nature of the
sections.
EXTINCTION PATTERN
In addition to timing of the extinction,
another fundamental issue is how to reconstruct and understand patterns of biological diversity. A single catastrophic
event between Bed 25 and 28 was proposed based on detailed paleontological
PERSPECTIVES
study of the Meishan sections using a
confidence interval approach [11]. More
recently, a new analysis of the diversity
patterns based on a much larger database,
including tens of sections in South China
and the peri-Gondwanan region, using
the constrained optimization (CONOP)
approach also supports a single event
[12,13]. In contrast, Song et al. [14, fig. 1]
proposed a two-phase extinction at Meishan, one at Bed 25 and the other at Bed
28 and suggest that these two pulses can
be recognized in other sections. Moreover, many previous studies reported
multiple pulses of extinction based on
different fossil groups from single horizons and sections (see those summarized
in [13], fig. 8). These two different views
of the extinction patterns likely reflect
different inventories of fossils in collections from different sections and different analytical/statistical approaches.
Shen and Bowring
Although the fossil record can be a spectacular archive of patterns of biodiversity providing a vital deep-time perspective on extinction patterns, the record
is commonly biased by the incompleteness of fossil preservation, facies changes
and time averaging of fossil collections.
For example, the observed local end of
a fossil taxon in a section is almost always a truncated false last occurrence
of the true extinction. In assessing extinction, it is imperative to not just
look at the total number of species lost
within a certain interval or on a bedding plane, but more importantly to
elucidate the true pattern after eliminating sampling biases caused by facies
change, incorrect or imprecise biostratigraphical correlation, incomplete preservation and collecting intensity with different analytical approaches across a wide
geographic area.
493
At present, many agree that the main
pulse of end-Permian extinction occurred at Bed 25 at the Meishan section,
but it is controversial whether the interval between Bed 25 and 28 that contains
some relict Permian taxa as well as the
occurrences of rare Triassic taxa (e.g.,
Hypophiceras, Claraia, Eumorphotis)
represents
continued
extinction
during severe environmental stress
[12,13] or a new ameliorated stage
followed by another extinction pulse
at Bed 28 [14]. Strong evidence for
euxinic condition with cyanobacterial
blooms [15], oceanic acidification [3],
microbialite expansion [4] and the
distinct Lilliput effect [16] indicates
that the entire extinction interval was
characterized by extreme environmental
stress (Fig. 1). Accurate patterns of
biodiversity throughout the extinction
interval must come from multiple
Figure 1. Temporal order of series of events and environmental preturbations plotted on the Permian–Triassic boundary (PTB) interval at the Meishan
section in South China. Time scale and carbon isotope curve and conodont zonation after [2,9,12]. Dashed bar showing event/phenomenon extending
below or above. The yellow bar indicates the maximum extinction interval and rapidly increasing environmental deterioration.
494
PERSPECTIVES
National Science Review, 2014, Vol. 1, No. 4
sections and especially ones that reflect
higher sediment accumulation rates than
are preserved at Meishan and Shangsi.
CONTEXT OF THE EXTINCTION
A deeper understanding of the endPermian extinction must rely on integration of palaeontological, geochronological, geological and geochemical data
from multiple sections and palaeoenvironments so that the magnitudes and
patterns of extinction can be correlated
within the context of multiple proxies
from before, during and after the event
(Fig. 1). The onset of the globally recognized δ 13 Ccarb excursion began about
60 kyr below Bed 25 at the Meishan section, and the abrupt decline of δ 13 Ccarb
marking the onset of the extinction is estimated to have lasted less than 10 kyr
[9]. A protracted but gradual negative
downturn of δ 13 Ccarb refined by Burgess
et al. [9], beginning at Bed 30 of the
Yinkeng Formation in the lower Triassic, was proposed to correspond to a second phase of the extinction based on carbon isotope and cyanobacterial bloom of
Xie et al. [15]. Burgess et al. [9] show
that this interval is about 50 kyr younger
than the end of the main extinction interval (Fig. 1) and lasted nearly half a
million years until Bed 39 at Meishan.
The double negative shifts of δ 13 Corg
of Cao et al. [17] are before the onset
(between Bed 23 and 24) and within
the extinction interval (Bed 26) at the
Meishan section, but only one negative
shift of δ 13 Corg has been recorded in
southwest China [12]. The first evidence
of a cyanobacterial bloom at Meishan is in
Bed 26 within the extinction interval, but
the second interval of the cyanobacterial
bloom is in the Triassic, ca 300 kyr after
the end of extinction (Fig. 1). While the
rapid rise in sea surface temperature reported by Joachimski et al. [5] post-dates
the negative spike in δ 13 Ccarb and is approximately coincident with the onset of
the extinction at Meishan section, but a
more precise relationship with the extinction requires additional study in multiple
sections, especially those with higher sediment accumulation rates. For example, if
the temperature increase lagged the on-
set of the extinction, high temperatures
could not be invoked as a major killing
mechanism.
Previous studies have noted the approximate coincidence between the timing of the extinction and the eruption
of the Siberian flood basalt lava flow
province, but given the very short duration of the extinction, testing a precise relationship is not yet possible. Many
mafic rocks in the region are younger than
the end-Permian mass extinction based
on dates from the Meishan section in
South China. However, the available, relatively imprecise, geochronological data
from the Siberian Traps cannot be used
to determine whether the eruption predates and/or overlaps the mass extinction
interval.
Given the apparent brevity of the extinction interval, two issues must yet be
clarified before a definitive link can be
made. (1) What is the temporal relationship between eruption of the Siberian
Traps and the mass extinction? (2) What
is the source of isotopically light carbon
associated with the extinction interval?
Did the eruption begin before the extinction? And if the eruption of the Siberian
Traps lasted ca 1–2 Myr, much longer
than the mass extinction, is the extinction
related to one pulse of Siberian magmatism or the cumulative effects of the eruption up to the time of the extinction? The
last question is crucial as it is possible that
Late Permian ecosystems were undergoing stress well before the sudden collapse
as evidenced by the progressive negative
shift before the abrupt decline of δ 13 Ccarb
[2, 8, 12, 17], marine anoxic and euxinic
conditions before the extinction [17] and
changes of rates of taxon turnover and
diversification before the sudden extinction [13]. In this scenario, once a critical
threshold is reached, total collapse of marine and terrestrial ecosystems result.
It has long been argued based on
Triassic palaeoclimate, evidence for a calcification crisis at the extinction, palaeophysiology of the ecosystem collapse
and a sudden perturbation of the carbon cycle with addition of isotopically
light carbon, that elevated atmospheric
CO2 played a major role in the extinction. Although volcanism undoubtedly
contributed to the elevated CO2 con-
tents in the atmosphere, it is doubtful
if volcanism alone could have released
enough magmatic CO2 to cause the
higher temperatures. Debate continues
regarding the source of the isotopically
light carbon. It has been suggested that
Siberian large igneous province (LIP)
magmatism triggered the massive release
of greenhouse gases from thick organicrich deposits or rapid venting of coalderived methane or massive combustion
of coal [18]. Another recent hypothesis
is that the dramatic rise of greenhouse
gas was produced by rapid expansion of
a methanogenic microbe fuelled by addition of nickel to the oceans from the
eruption [19].
There is still, much unknown about
the exact cause(s) of the extinction,
but the timing constraints leave little
doubt that it was a catastrophic event.
Although the Meishan section in South
China contains two Global Stratotype
Section and Points (GSSPs) that have
been intensively studied, one obvious
drawback is that the section is highly
condensed. The extinction interval is 26
cm thick with distinct hiatuses and facies
changes making accurate calculation of
sediment accumulation rates and internal
data difficult, even with closely spaced ash
beds. Much more work is needed in other
more expanded sections.
TRIASSIC RECOVERY
Marine ecosystems underwent a revolutionary reorganization from Late
Permian benthic shelly-dominated
communities in shallow marine carbonate environments to widespread
microbial communities with low-oxygen
conditions across the Permian–Triassic
boundary [20]. However, a recent
analysis challenges the severity of the
ecological effect of the end-Permian
extinction. Statistical analysis of benthic
marine invertebrate fossils indicates
that there is no significant loss of functional diversity at the global scale [21],
although fossil diversity was massively
reduced during the extinction. A key
question is how rapidly biota and ecosystems recovered and how evolutionary
processes led to occupation of vacated
PERSPECTIVES
ecospaces in the Triassic. It has been
traditionally postulated that the Early
Triassic recovery took at least 5–6 Myr or
until the early Middle Triassic (Anisian).
However, new and abundant palaeontological data suggest that different fossil
groups had different recovery patterns.
Triassic disaster taxa such as Claraia began to occur in the latest Permian before
the onset of the extinction in Guangxi,
South China, whereas conodonts experienced turnover at species and genus
levels only. Triassic ammonoids first
appear in the extinction interval, but
rapidly diversify after the extinction,
and bivalves, foraminifers also recovered
rapidly. Fishes and marine reptiles show
apparently explosive diversification very
early in the Early Triassic. Brachiopods
and ostracods took a longer time to
recover until late Early Triassic to early
Middle Triassic.
There are also wider debates about the
dynamics of the Triassic recovery. The
recovery was associated with a number of
repeated large carbon isotope excursions
[22], but their age and causal-effect relationship remains unclear. Apparently, the
large perturbations in carbon isotope signatures are not correspondingly reflected
in biodiversity change during Early and
Middle Triassic. Triassic carbon isotope
profiles indicate a rapid recovery before
the Dienerian. In contrast, the whole
Early Triassic is characterized by high sea
surface temperatures with little fluctuation in temperature [6]. In addition to
global warming, elevated CO2 also likely
led to ocean acidification, increased
erosion rates and raised inputs of
nutrients into the oceans that led to
widespread anoxia. If high temperatures
and anoxic conditions led to a prolonged
recovery, it is still unclear how to explain
Shen and Bowring
the latitudinal and palaeogeographic
control on the timing and patterns of
recovery. Similar to the extinction, the
recovery must be also examined using a
number of temporally calibrated sections
from a broad range of paleogeographic
and paleoenvironemental settings with
high-quality palaeontogical data. Again,
fossil incompleteness and sampling
biases must be considered carefully. A
new effort will most likely lead to insights
into the recovery as well as the extinction.
ACKNOWLEDGEMENTS
495
3. Hinojosa, JL, Brown, ST and Chen, J et al. Geology 2012; 40: 743–6.
4. Kershaw, S, Crasquin, S and Li, Y et al. Geobiology 2012; 10: 25–47.
5. Joachimski, MM, Lai, XL and Shen, SZ et al. Geology 2012; 40: 195–8.
6. Sun, YD, Joachimski, MM and Wignall, PB et al.
Science 2012; 338: 366–70.
7. Yin, HF, Jiang, HS and Xia, WC et al. Earth-Sci
Rev 2014; http://dx.doi.org/10.1016/j.earscirev.
2013.06.003.
8. Xie, SC, Pancost, RD and Huang, JH et al. Geology
2007; 35: 1083–6.
9. Burgess, SD, Bowring, SA and Shen, SZ. Proc Natl
Acad Sci USA 2014; 111: 3316–21.
We thank two anonymous reviewers for their helpful comments. We acknowledge many papers on the
topics discussed that we were not able to cite due to
journal requirements.
10. Wu, HC, Zhang, SH and Hinnov, LA et al. Nat Commun 2013; 4: 1–7.
11. Jin, YG, Wang, Y and Wang, W et al. Science
FUNDING
2011; 334: 1367–72.
13. Wang, Y, Sadler, PM and Shen, SZ et al. Paleobiology 2014; 40: 113–29.
The work of SS is supported by National Natural Science Foundation of China (41290260).
The work of SAB is supported by National Science Foundation Continental Dynamics Grant
(EAR-0807475) and Instrumentation and Facilities
(EAR-0931839).
Shu-zhong Shen1,∗ and Samuel A. Bowring2
of Palaeobiology and
Stratigraphy, Nanjing Institute of Geology and
1 State Key Laboratory
Palaeontology, China
2 Department of Earth, Atmospheric and Planetary
Sciences, Massachusetts Institute of Technology,
USA
∗ Corresponding author.
E-mail: [email protected]
REFERENCES
1. Korte, C and Kozur, HW. J Asian Earth Sci 2010;
39: 215–35.
2. Shen, SZ, Cao, CQ and Zhang, H et al. Earth Planet
Sci Lett 2013; 375: 156–65.
2000; 289: 432–6.
12. Shen, SZ, Crowley, JL and Wang, Y et al. Science
14. Song, HJ, Wignall, PB and Tong, JN et al. Nat
Geosci 2013; 6: 52–6.
15. Xie, SC, Pancost, RD and Wang, YB et al. Geology
2010; 38: 447–50.
16. Twitchett, RJ. Paleogeogr Paleoclimatol Paleoecol 2007; 252: 132–44.
17. Cao, CQ, Love, GD and Hays, LE, et al. Earth
Planet Sci Lett 2009; 281: 188–201.
18. Ogden, DE and Sleep, NH. Proc Natl Acad Sci USA
2012; 109: 59–62.
19. Rothman, DH, Fournier, GP and French, KL et al.
Proc Natl Acad Sci USA 2014; 111: 5462–67.
20. Chen, ZQ and Benton, MJ. Nat Geosci 2012; 5:
375–83.
21. Foster, WJ and Twitchett, RJ. Nat Geosci 2014; 7:
233–8.
22. Payne, JL, Lehrmann, DJ and Wei, JY et al. Science 2004; 305: 506–9.
doi: 10.1093/nsr/nwu047
Advance access publication 21 August 2014