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 Lethally Hot Temperatures During the Early Triassic Greenhouse
Yadong Sun et al.
Science 338, 366 (2012);
DOI: 10.1126/science.1224126

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10. L. Marrucci, C. Manzo, D. Paparo, Phys. Rev. Lett. 96, 20. Z. Bomzon, V. Kleiner, E. Hasman, Opt. Lett. 26, 1424 for very useful discussions and C. Railton (Merchant Venturers
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13. M. Smit, J. van der Tol, M. Hill, Laser Photon. Rev. 6, 18, 7173 (2010).
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16. Materials and methods are available as supplementary 25. S. Manipatruni, Q. Xu, M. Lipson, Opt. Express 15, 13035 Materials and Methods
materials on Science Online. (2007). Supplementary Text
17. A. B. Matsko, A. A. Savchenkov, D. Strekalov, L. Maleki, 26. K. Ladavac, D. Grier, Opt. Express 12, 1144 (2004). Figs. S1 to S7
Phys. Rev. Lett. 95, 143904 (2005). References (27–31)
18. D. Taillaert et al., Jpn. J. Appl. Phys. 45, 6071 Acknowledgments: We thank M. Berry and M. Dennis Movies S1 to S4
(2006). (Department of Physics, University of Bristol, UK), S. Barnett
19. R. Dorn, S. Quabis, G. Leuchs, Phys. Rev. Lett. 91, (Department of Physics, University of Strathclyde, UK), and 25 June 2012; accepted 10 September 2012
233901 (2003). M. Padgett (Department of Physics, University of Glasgow, UK) 10.1126/science.1226528

reasons, such as the prolonged delay in recov-

Lethally Hot Temperatures During the ery (3), the prevalence of small taxa (4), and the

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absence of coal deposits throughout the Early
Early Triassic Greenhouse Triassic (5). These and several facets of low-
latitude fossil records shown below, including
fish, marine reptile, and tetrapod distributions,
Yadong Sun,1,2* Michael M. Joachimski,3 Paul B. Wignall,2 Chunbo Yan,1 Yanlong Chen,4
can be related to extreme temperatures in excess
Haishui Jiang,1 Lina Wang,1 Xulong Lai1
of tolerable thermal thresholds.
Climate warming long has been implicated
Global warming is widely regarded to have played a contributing role in numerous past biotic crises. as one cause of the end-Permian crisis (2, 6), with
Here, we show that the end-Permian mass extinction coincided with a rapid temperature rise to carbon dioxide release from Siberian eruptions
exceptionally high values in the Early Triassic that were inimical to life in equatorial latitudes and and related processes providing a potential trig-
suppressed ecosystem recovery. This was manifested in the loss of calcareous algae, the near-absence ger for it (7, 8). Conodont apatite oxygen isotope
of fish in equatorial Tethys, and the dominance of small taxa of invertebrates during the thermal
maxima. High temperatures drove most Early Triassic plants and animals out of equatorial terrestrial 1
State Key Laboratory of Geobiology and Environmental
ecosystems and probably were a major cause of the end-Smithian crisis. Geology, China University of Geosciences (Wuhan), Wuhan
430074, People’s Republic of China. 2School of Earth and En-
nthropogenic global warming likely is the spread of marine anoxia (2). Here, we show vironment, University of Leeds, Leeds LS2 9JT, UK. 3GeoZentrum

A contributing to the rapid loss of biolog-

ical diversity currently occurring (1). Cli-
mate warming also has been implicated in severe
that lethally hot temperatures exerted a direct
control on extinction and recovery during and
in the aftermath of the end-Permian mass ex-
Nordbayern, Universität Erlangen-Nürnberg, Schlossgarten 5,
91054 Erlangen, Germany. 4Institute of Earth Sciences–Geology
and Paleontology, University of Graz, Heinrichstrasse 26, A-8010
Graz, Austria.
biotic crises in the geological past, but only as a tinction. As well as the scale of the losses, the *To whom correspondence should be addressed. E-mail:
corollary to more direct causes of death such as aftermath of this event is remarkable for several eeys@leeds.ac.uk

Fig. 1. Early Triassic pa-

leogeography showing
reported occurrences of
fish and marine reptiles
in the Smithian. Note rare
equatorial occurrence of
both groups when ich-
thyosaurs had evolved
in northern climes. The
global distribution of
tetrapods (25) indicates
occurrences almost ex-
clusively in higher lati-
tudes (>30°N and >40°S)
throughout the Early Tri-
assic, with rare exceptions
in Utah (Parotosuchus
sp., paleolatitude ~10°N)
and Poland (paleolatitude
~20°N), both probably of
middle-late Spathian age
(25, 26). (Inset) Paleo-
geography of Pangea and
Nanpanjiang Basin after
(45–47). Fish and ichthyo-
saurs occurrences, see table S2. GBG, Great Bank of Guizhou.

366 19 OCTOBER 2012 VOL 338 SCIENCE www.sciencemag.org

 REPORTS

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Fig. 2. Oxygen isotopes of conodont apatite and carbon isotopes of carbonates The error bar stands for external reproducibility of d18Oapatite measurements (2s). The
from the Nanpanjiang Basin. Oxygen isotopes show two thermal maxima in the black trendline represents smoothed d18Oapatite fluctuations estimated from the
late Griesbachian and late Smithian. Scanning electron microscope investigation of upper water column taxa. Note uncertainty of correlating conodont zones with ab-
conodont surfaces shows microreticulation and no sign of recrystallization (supple- solute ages. Aeg., Aegean; Bith., Bithynian. Conodont zonations: 1, Ng. changxingensis;
mentary text 3). Absolute age constraints are given in supplementary text 9; data 2, Ng. yini; 3, Ng. meishanensis; 4, H. changxingensis; 5, H. parvus; 6, Is. staeschei;
for Meishan and Shangsi sections compiled from (9); leaf icons represent marine 7, Is. isarcica; 8, Ng. planata; for genera abbreviations, see table S4.VSMOW,
and terrestrial C3 plants (14). Modern equatorial SST ranges (annual mean) from (48). Vienna Standard Mean Ocean Water; VPDB, Vienna Pee Dee Belemnite.

www.sciencemag.org SCIENCE VOL 338 19 OCTOBER 2012 367

REPORTS
ratio (d18O) is a reliable proxy for paleoseawater of the analyzed conodonts taxa accord with their is seen in the late Smithian (~250.7 Ma), followed
temperatures (9), and conodonts suffered few habitats in different water depth: Neospathodus by relatively stable temperatures in the Spathian,
genus-level losses at the end of the Permian (10), spp. shows ~ 0.7 per mil (‰) heavier values cooling at the end of this stage and stabilization
allowing continuous sampling of the same gen- than those from shallow-water Pachycladina/ in the early Middle Triassic (Fig. 2). The late
era over multimillion-year intervals (11). We used Parachirognathus spp. and Platyvillosus spp. Smithian Thermal Maximum (LSTM) marks the
d18Oapatite of conodonts from sections in the Deeper-water gondolellids show even heavier hottest interval of entire Early Triassic, when up-
Nanpanjiang Basin, South China, to reconstruct d18Oapatite (~0.4‰) than Neospathodus spp. (sup- per water column temperatures approached 38°C
Late Permian to Middle Triassic equatorial sea- plementary text 2 and table S1). Latest Spathian– with SSTs possibly exceeding 40°C (Fig. 3).
water temperatures (Fig. 1 and supplementary early Anisian oxygen isotope data from Bianyang The entire Early Triassic record shows tem-
text 1). Our main record, measured on the genus and Guandao are more scattered and up to 1.3‰ peratures consistently in excess of modern equa-
Neospathodus, is a monitor of upper water col- heavier compared with samples from other sec- torial annual SSTs. These results suggest that
umn temperatures (estimated ~70 m water depth, tions. These two locations are close to the Great equatorial temperatures may have exceeded a
supplementary text 2), whereas data from ex- Bank of Guizhou (Fig. 1), and such 18O enrich- tolerable threshold both in the oceans and on
tremely shallow water taxa (Pachycladina or ment toward platform interior is interpreted to be land. For C3 plants, photorespiration predom-
Parachirognathus spp., Platyvillosus spp.) pro- due to evaporation as seen on the modern Bahama inates over photosynthesis at temperatures in
vide sea surface temperatures (SSTs). Bank (12). However, most of the presented data excess of 35°C (13), and few plants can survive
Our results show large, near-synchronous per- are from distal, open-water environments and temperatures persistently above 40°C (14). Sim-
turbations in both carbon isotope ratios (d13Ccarb) therefore present a faithful paleotemperature ilarly, for animals, temperatures in excess of

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and d18Oapatite with three positive excursions record (supplementary texts 3 and 4). 45°C cause protein damage that are only tem-
observed in the Dienerian [~251.5 million years Calculation of seawater temperatures from porarily alleviated by heat-shock protein produc-
ago (Ma)], early Spathian (~250.5 Ma), and at d18O values (supplementary text 5) reveals rapid tion (15). However, for most marine animals,
the Spathian-Anisian (Early-Middle Triassic) warming across the Permian-Triassic boundary the critical temperature is much lower, because
transition (~247.5 Ma). The minima in d13Ccarb [21° to 36°C, over ~0.8 million years (My); (9)], metabolic oxygen demand increases with tem-
and d18Oapatite are measured in the Griesbachian reaching a temperature maximum within the perature while dissolved oxygen decreases (16).
(~252.1 Ma) and the Smithian-Spathian transi- Griesbachian (~252.1 Ma) followed by cooling in This causes hypoxaemia and the onset of an-
tion (~250.7 Ma) (Fig. 2). The d18Oapatite values the Dienerian. A second rise to high temperatures aerobic mitochondrial metabolism that is only

Fig. 3. Early Triassic diversity of major marine groups and temperature plementary text 6). Floral data (28–30, 42) show the loss of equatorial
trends showing inverse relationship: Peak diversity corresponds to cool conifer-dominated forests above the Permian-Triassic (PT) boundary, with
climate conditions around the Dienerian-Smithian boundary, early Spathian, the earlier reappearance of this forest type at high latitudes. Gray band
and early Anisian (named cooling events I to III), whereas low diversity in represents the first-order seawater temperatures trend (upper water column,
Griesbachian and Smithian correlates with peak temperatures. Diversity of ~70-m water depth) estimated by this study; red trend line represents
marine groups from (37–39, 49–52); fish and marine reptile only show the possible SST derived from shallow water taxa. Same stratigraphic scheme
general presence of taxa; no quantitative diversity data are available (sup- as Fig. 2.

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 REPORTS
sustainable for short periods (17). As a conse- not reflect an absence of suitable strata for their Smithian event that saw major losses among
quence, marine animals cannot long survive tem- preservation. For example, the Buntsandstein of many marine groups, including bivalves, cono-
peratures above 35°C, particularly those with a Europe is one of the best known and most in- donts, and ammonoids (37–39). Contemporane-
high performance and high oxygen demand, such tensively investigated terrestrial formations of ous losses among tetrapods on land (25) suggest
as cephalopods (16). the Early Triassic; tetrapods are exceptionally that this was a crisis that affected a broad di-
Extreme equatorial warmth should have left rare in the lower part (Induan) and only become versity of ecosystems.
a distinct signature in the Early Triassic fossil common in middle and upper units (late Early The ultimate driving factor behind the end-
records, a proposition that we examine here. Triassic to Middle Triassic) (27). The tetrapod Permian warming long has been attributed to
The fossil fish record is exceptionally good in gap of equatorial Pangea coincides with an end- greenhouse gas emissions, either from volcano-
the Early Triassic, with many well-preserved Permian to Middle Triassic global “coal gap” that genic (8) or thermogenic sources (40). Both are
faunas known from locations such as Madagas- indicates the loss of peat swamps (5). Peat for- expected to leave a negative excursion in the
car, Greenland, and British Columbia (supple- mation, a product of high plant productivity, was d13C record, and this is the case for both the end
mentary text 6). This is related to the widespread only reestablished in the Anisian and then only Permian–Griesbachian and Smithian intervals
distribution of anoxic facies (18) that provide ex- in high southern latitudes (5), although gym- (Fig. 2), although it has yet to be demonstrated
cellent preservational conditions for such fossils. nosperm forests appeared earlier (in the Early that a second pulse of Siberian volcanism oc-
However, our compilation of fish occurrences re- Spathian), but again only in northern and south- curred in the Smithian. However, to maintain
veals that they are very rare in equatorial locales, ern higher latitudes (28, 29). In equatorial Pangea, high temperatures for the ~5 My of the Early
especially during the late Griesbachian and the the establishment of conifer-dominated forests Triassic requires strong, persistent greenhouse

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Smithian, despite being common at higher lati- was not until the end of the Spathian (30), and conditions. High temperatures also could greatly
tudes at these times (fig. S1 and table S2). This the first coals at these latitudes did not appear enhance the activity of decomposers (e.g., fungi
rarity is extraordinary because Early Triassic until the Carnian ~15 My after their end-Permian and bacteria), resulting in the release of large
units, such as the dysoxic-anoxic Daye Forma- disappearance (5). These signals suggest equa- amounts of terrestrial light carbon into the at-
tion of South China, are widespread (supple- torial temperatures exceeded the thermal toler- mosphere (41) and consequently forming oligo-
mentary text 7) and yet do not yield a fossil fish ance for many marine vertebrates at least during trophic, humus-poor soils as observed in modern
fauna. The general absence of ichthyofauna in two thermal maxima, whereas terrestrial equato- Amazon rainforests and in Early Triassic soils
equatorial regions coincides with the temperature rial temperatures were sufficiently severe to sup- of Australia and Antarctica (42). Together with
maxima reconstructed from the d18Oapatite record, press plant and animal abundance during most of global suspension of peat formation, elevated de-
and we interpret this coincidence as recording the Early Triassic. composition rates may have led to a significant
equatorial exclusion because of inhospitably high Thermal tolerance is likely to decrease for reduction in organic carbon burial on land fur-
temperatures. In contrast, invertebrates remain organisms with larger body sizes (31). Nonlethal ther contributing to higher atmospheric CO2
common in these intervals (19), especially sessile effects of temperature increase include smaller levels (43).
mollusks with their better adapted oxyconform- adult size, which, in conjunction with increased High and oscillating temperatures in the Early
ing metabolism allowing them to cope with syn- juvenile mortality at higher temperatures (32, 33), Triassic likely controlled the pace and nature of
ergistic stresses of high temperature and low will produce a fossil record dominated by small recovery in the aftermath of the end-Permian
oxygen (17, 20). Like fish, marine reptiles also individuals. This is a well-known phenomenon in mass extinction as shown by an inverse relation-
exhibit high aerobic activity and are likely to the Early Triassic marine fossil record and has ship between the temperature and biodiversity
have had a relatively low oxygen-limited thermal been termed the Lilliput effect (4). We suggest changes, the temporary loss of both marine and
tolerance. Examining Early Triassic marine rep- that this effect is a response to high tempera- terrestrial vertebrates, and the reduced size of
tile (ichthyosaur) occurrences reveals that they tures and that it should be most clearly seen in the remaining invertebrates. SSTs derived from
too are not found in equatorial waters until the equatorial assemblages, especially during the d18O data offer no evidence that a climate ther-
middle-late Spathian (supplementary text 6), Griesbachian and Smithian thermal maxima. This mostat may ameliorate tropical warming by re-
~1 to 2 My after their first appearance in higher prediction is confirmed by data from equatorial distributing warmth to the poles (44). Rather,
latitudes during the Smithian (21, 22). Other marine fossils where small body and trace fossil extreme global warming may progressively force
notable absences from equatorial oceans are cal- assemblages are confined to these intervals (34, 35). taxa to vacate the tropics and move to higher lat-
careous algae, whose outage spans the entire end- Low oxygen levels also are known to cause small itudes or become extinct. Marine organisms ex-
Permian–early Spathian interval although they size in marine invertebrates (36), but, although hibiting low oxygen-dependent thermal tolerance,
are present in higher latitudes [e.g., Spitsbergen, marine dysoxia was a global phenomenon in the such as vertebrates, are the first to leave.
(23)]. Their equatorial absence (supplementary Early Triassic (18), the restriction of the Lilliput
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tial macroscopic event layers (such as turbidites

A Complete Terrestrial Radiocarbon and tephras) removed.
Accelerator mass spectrometry radiocarbon
Record for 11.2 to 52.8 kyr B.P. dating (5) has been conducted on terrestrial plant
macrofossils selected from the SG06 cores to
Christopher Bronk Ramsey,1* Richard A. Staff,1 Charlotte L. Bryant,2 Fiona Brock,1 cover the full 14C time range, from the present to
Hiroyuki Kitagawa,3 Johannes van der Plicht,4,5 Gordon Schlolaut,6 Michael H. Marshall,7 the detection limit of the 14C method (0 to 41 m
Achim Brauer,6 Henry F. Lamb,7 Rebecca L. Payne,8 Pavel E. Tarasov,9 Tsuyoshi Haraguchi,10 CD) (table S1). The results already reported from
Katsuya Gotanda,11 Hitoshi Yonenobu,12 Yusuke Yokoyama,13 Ryuji Tada,13 Takeshi Nakagawa8 the control period (0 to 12.2 kyr B.P.) (6), covered
by the tree-ring–derived calibration curve (7), act
Radiocarbon (14C) provides a way to date material that contains carbon with an age up to to demonstrate the integrity of the sediments and
~50,000 years and is also an important tracer of the global carbon cycle. However, the lack of to anchor the floating SG06 varve chronology,
a comprehensive record reflecting atmospheric 14C prior to 12.5 thousand years before the because varves do not extend into the Holocene.
present (kyr B.P.) has limited the application of radiocarbon dating of samples from the Last The varve-based chronology for SG06 (5, 8, 9)
Glacial period. Here, we report 14C results from Lake Suigetsu, Japan (35°35′N, 135°53′E), provides our best estimate of the true age of the
which provide a comprehensive record of terrestrial radiocarbon to the present limit of the cores for the period ~10.2 to 40.0 kyr B.P., based
14
C method. The time scale we present in this work allows direct comparison of Lake Suigetsu only on information from the site. It provides
paleoclimatic data with other terrestrial climatic records and gives information on the connection good relative chronological precision and has the
between global atmospheric and regional marine radiocarbon levels. advantage of being independent of other dating
techniques. However, the cumulative counting un-
ake Suigetsu contains annually laminated potential to provide an important archive of at- certainty inevitably increases with age (~6% at

L sediments that preserve both paleoclimate

proxies and terrestrial plant macrofossils
that are suitable for radiocarbon dating. The lake’s
mospheric radiocarbon (14C) was realized in 1993
(1). However, the single SG93 sediment core
then recovered included missing intervals be-
40 kyr B.P.). The full varve chronology (Fig. 1A
and table S1) has been extrapolated on the basis
of EFD to cover the period 40 to 53 kyr B.P.
tween successive sections (2). This, together with To better constrain the uncertainties in the
the difficulty of visual varve counting, resulted in varve chronology, we can directly compare the
1
University of Oxford, Oxford, UK. 2Natural Environment Re- inconsistency between the SG93 and other 14C Suigetsu data set and other archives that provide
search Council Radiocarbon Facility, Scottish Universities calibration records (3). The SG06 core-set re- information on atmospheric 14C and associated
Environmental Research Centre, East Kilbride, UK. 3Nagoya covered in 2006 consists of four parallel cores independent ages. The two most useful records
University, Nagoya, Japan. 4University of Groningen, Groningen,
that together avoid any such sedimentary gaps for this purpose are the Bahamas speleothem GB89-
Netherlands. 5University of Leiden, Leiden, Netherlands.
6
GeoForschungsZentrum German Research Centre for Geosci- (4). Here, we report 651 14C measurements cov- 25-3 (10) and the Hulu Cave speleothem H82
ences, Potsdam, Germany. 7Aberystwyth University, Aberystwyth, ering the period between 11.2 and 52.8 thousand (11), both of which have extensive 14C- and U-Th–
UK. 8University of Newcastle, Newcastle upon Tyne, UK. 9Free years before the present (kyr B.P.) tied to a time based chronologies. In both cases, we would ex-
University Berlin, Berlin, Germany. 10Osaka City University, scale derived from varve counting and temporal pect the radiocarbon in the speleothems to respond
Osaka, Japan. 11Chiba University of Commerce, Chiba, Japan.
12
Naruto University of Education, Naruto, Japan. 13University constraints from other records. Using visual mark- to changes in atmospheric 14C content, despite the
of Tokyo, Tokyo, Japan. ers, we applied a composite depth (CD) scale to groundwater containing a dead-carbon fraction
*To whom correspondence should be addressed. E-mail: all cores, including SG93. We also define an event- (DCF) from dissolved carbonates. Estimated DCF
christopher.ramsey@rlaha.ox.ac.uk free depth (EFD), which is the CD with substan- for these speleothems was 2075 T 270 radiocarbon

370 19 OCTOBER 2012 VOL 338 SCIENCE www.sciencemag.org

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