2 Full pages Scholarly review

10. L. Marrucci, C. Manzo, D. Paparo, Phys. Rev. Lett. 96, 163905 (2006).

11. G. Biener, A. Niv, V. Kleiner, E. Hasman, Opt. Lett. 27, 1875 (2002).

12. N. Yu et al., Science 334, 333 (2011). 13. M. Smit, J. van der Tol, M. Hill, Laser Photon. Rev. 6,

1 (2012). 14. C. R. Doerr, L. L. Buhl, Opt. Lett. 36, 1209 (2011). 15. K. J. Vahala, Nature 424, 839 (2003). 16. Materials and methods are available as supplementary

materials on Science Online. 17. A. B. Matsko, A. A. Savchenkov, D. Strekalov, L. Maleki,

Phys. Rev. Lett. 95, 143904 (2005). 18. D. Taillaert et al., Jpn. J. Appl. Phys. 45, 6071

(2006). 19. R. Dorn, S. Quabis, G. Leuchs, Phys. Rev. Lett. 91,

233901 (2003).

20. Z. Bomzon, V. Kleiner, E. Hasman, Opt. Lett. 26, 1424 (2001).

21. A. Niv, G. Biener, V. Kleiner, E. Hasman, Opt. Express 14, 4208 (2006).

22. I. Moreno, J. A. Davis, I. Ruiz, D. M. Cottrell, Opt. Express 18, 7173 (2010).

23. A. Yariv, Electron. Lett. 36, 321 (2000). 24. Y. Yu, R. O’Dowd, IEEE Photon. Technol. Lett. 14, 1397

(1992). 25. S. Manipatruni, Q. Xu, M. Lipson, Opt. Express 15, 13035

(2007). 26. K. Ladavac, D. Grier, Opt. Express 12, 1144 (2004).

Acknowledgments: We thank M. Berry and M. Dennis (Department of Physics, University of Bristol, UK), S. Barnett (Department of Physics, University of Strathclyde, UK), and M. Padgett (Department of Physics, University of Glasgow, UK)

for very useful discussions and C. Railton (Merchant Venturers School of Engineering, University of Bristol, UK) for providing the finite-difference time-domain simulation tool. J.W. is funded by European Union FP7 FET-OPEN project PHORBITEC.

Supplementary Materials www.sciencemag.org/cgi/content/full/338/6105/363/DC1 Materials and Methods Supplementary Text Figs. S1 to S7 References (27–31) Movies S1 to S4

25 June 2012; accepted 10 September 2012 10.1126/science.1226528

Lethally Hot Temperatures During the Early Triassic Greenhouse Yadong Sun,1,2* Michael M. Joachimski,3 Paul B. Wignall,2 Chunbo Yan,1 Yanlong Chen,4 Haishui Jiang,1 Lina Wang,1 Xulong Lai1

Global warming is widely regarded to have played a contributing role in numerous past biotic crises. Here, we show that the end-Permian mass extinction coincided with a rapid temperature rise to exceptionally high values in the Early Triassic that were inimical to life in equatorial latitudes and suppressed ecosystem recovery. This was manifested in the loss of calcareous algae, the near-absence 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 ecosystems and probably were a major cause of the end-Smithian crisis.

A nthropogenic global warming likely is contributing to the rapid loss of biolog- ical diversity currently occurring (1). Cli-

mate warming also has been implicated in severe biotic crises in the geological past, but only as a corollary to more direct causes of death such as

the spread of marine anoxia (2). Here, we show that lethally hot temperatures exerted a direct control on extinction and recovery during and in the aftermath of the end-Permian mass ex- tinction. As well as the scale of the losses, the aftermath of this event is remarkable for several

reasons, such as the prolonged delay in recov- ery (3), the prevalence of small taxa (4), and the absence of coal deposits throughout the Early Triassic (5). These and several facets of low- latitude fossil records shown below, including fish, marine reptile, and tetrapod distributions, can be related to extreme temperatures in excess of tolerable thermal thresholds.

Climate warming long has been implicated as one cause of the end-Permian crisis (2, 6), with carbon dioxide release from Siberian eruptions and related processes providing a potential trig- ger for it (7, 8). Conodont apatite oxygen isotope

1State Key Laboratory of Geobiology and Environmental Geology, China University of Geosciences (Wuhan), Wuhan 430074, People’s Republic of China. 2School of Earth and En- vironment, University of Leeds, Leeds LS2 9JT, UK. 3GeoZentrum Nordbayern, Universität Erlangen-Nürnberg, Schlossgarten 5, 91054 Erlangen, Germany. 4Institute of Earth Sciences–Geology andPaleontology,UniversityofGraz,Heinrichstrasse26,A-8010 Graz, Austria.

*To whom correspondence should be addressed. E-mail: [email protected]

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°Nand>40°S) throughout the Early Tri- assic,withrareexceptions 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).Fishandichthyo- saurs occurrences, see table S2. GBG, Great Bank of Guizhou.

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Fig. 2. Oxygen isotopes of conodont apatite and carbon isotopes of carbonates from the Nanpanjiang Basin. Oxygen isotopes show two thermal maxima in the late Griesbachian and late Smithian. Scanning electron microscope investigation of conodont surfaces shows microreticulation and no sign of recrystallization (supple- mentary text 3). Absolute age constraints are given in supplementary text 9; data for Meishan and Shangsi sections compiled from (9); leaf icons represent marine and terrestrial C3 plants (14). Modern equatorial SST ranges (annual mean) from (48).

The error bar stands for external reproducibility of d18Oapatite measurements (2s). The black trendline represents smoothed d18Oapatite fluctuations estimated from the upper water column taxa. Note uncertainty of correlating conodont zones with ab- soluteages.Aeg.,Aegean;Bith.,Bithynian.Conodontzonations:1,Ng.changxingensis; 2, Ng. yini; 3, Ng. meishanensis; 4, H. changxingensis; 5, H. parvus; 6, Is. staeschei; 7, Is. isarcica; 8, Ng. planata; for genera abbreviations, see table S4.VSMOW, Vienna Standard Mean Ocean Water; VPDB, Vienna Pee Dee Belemnite.

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ratio (d18O) is a reliable proxy for paleoseawater temperatures (9), and conodonts suffered few genus-level losses at the end of the Permian (10), allowing continuous sampling of the same gen- era over multimillion-year intervals (11). We used d18Oapatite of conodonts from sections in the Nanpanjiang Basin, South China, to reconstruct Late Permian to Middle Triassic equatorial sea- water temperatures (Fig. 1 and supplementary text 1). Our main record, measured on the genus Neospathodus, is a monitor of upper water col- umn temperatures (estimated ~70 m water depth, supplementary text 2), whereas data from ex- tremely shallow water taxa (Pachycladina or Parachirognathus spp., Platyvillosus spp.) pro- vide sea surface temperatures (SSTs).

Our results show large, near-synchronous per- turbations in both carbon isotope ratios (d13Ccarb) and d18Oapatite with three positive excursions observed in the Dienerian [~251.5 million years ago (Ma)], early Spathian (~250.5 Ma), and at the Spathian-Anisian (Early-Middle Triassic) transition (~247.5 Ma). The minima in d13Ccarb and d18Oapatite are measured in the Griesbachian (~252.1 Ma) and the Smithian-Spathian transi- tion (~250.7 Ma) (Fig. 2). The d18Oapatite values

of the analyzed conodonts taxa accord with their habitats in different water depth: Neospathodus spp. shows ~0.7 per mil (‰) heavier values than those from shallow-water Pachycladina/ Parachirognathus spp. and Platyvillosus spp. Deeper-water gondolellids show even heavier d18Oapatite (~0.4‰) than Neospathodus spp. (sup- plementary text 2 and table S1). Latest Spathian– early Anisian oxygen isotope data from Bianyang and Guandao are more scattered and up to 1.3‰ heavier compared with samples from other sec- tions. These two locations are close to the Great Bank of Guizhou (Fig. 1), and such 18O enrich- ment toward platform interior is interpreted to be due to evaporation as seen on the modern Bahama Bank (12). However, most of the presented data are from distal, open-water environments and therefore present a faithful paleotemperature record (supplementary texts 3 and 4).

Calculation of seawater temperatures from d18O values (supplementary text 5) reveals rapid warming across the Permian-Triassic boundary [21° to 36°C, over ~0.8 million years (My); (9)], reaching a temperature maximum within the Griesbachian (~252.1 Ma) followed by cooling in the Dienerian. A second rise to high temperatures

is seen in the late Smithian (~250.7 Ma), followed by relatively stable temperatures in the Spathian, cooling at the end of this stage and stabilization in the early Middle Triassic (Fig. 2). The late Smithian Thermal Maximum (LSTM) marks the hottest interval of entire Early Triassic, when up- per water column temperatures approached 38°C with SSTs possibly exceeding 40°C (Fig. 3).

The entire Early Triassic record shows tem- peratures consistently in excess of modern equa- torial annual SSTs. These results suggest that equatorial temperatures may have exceeded a tolerable threshold both in the oceans and on land. For C3 plants, photorespiration predom- inates over photosynthesis at temperatures in excess of 35°C (13), and few plants can survive temperatures persistently above 40°C (14). Sim- ilarly, for animals, temperatures in excess of 45°C cause protein damage that are only tem- porarily alleviated by heat-shock protein produc- tion (15). However, for most marine animals, the critical temperature is much lower, because metabolic oxygen demand increases with tem- perature while dissolved oxygen decreases (16). This causes hypoxaemia and the onset of an- aerobic mitochondrial metabolism that is only

Fig. 3. Early Triassic diversity of major marine groups and temperature trends showing inverse relationship: Peak diversity corresponds to cool climate conditions around the Dienerian-Smithian boundary, early Spathian, and early Anisian (named cooling events I to III), whereas low diversity in Griesbachian and Smithian correlates with peak temperatures. Diversity of marine groups from (37–39, 49–52); fish and marine reptile only show the general presence of taxa; no quantitative diversity data are available (sup-

plementary text 6). Floral data (28–30, 42) show the loss of equatorial conifer-dominated forests above the Permian-Triassic (PT) boundary, with the earlier reappearance of this forest type at high latitudes. Gray band represents the first-order seawater temperatures trend (upper water column, ~70-m water depth) estimated by this study; red trend line represents possible SST derived from shallow water taxa. Same stratigraphic scheme as Fig. 2.

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sustainable for short periods (17). As a conse- quence, marine animals cannot long survive tem- peratures above 35°C, particularly those with a high performance and high oxygen demand, such as cephalopods (16).

Extreme equatorial warmth should have left a distinct signature in the Early Triassic fossil records, a proposition that we examine here. The fossil fish record is exceptionally good in the Early Triassic, with many well-preserved faunas known from locations such as Madagas- car, Greenland, and British Columbia (supple- mentary text 6). This is related to the widespread distribution of anoxic facies (18) that provide ex- cellent preservational conditions for such fossils. However, our compilation of fish occurrences re- veals that they are very rare in equatorial locales, especially during the late Griesbachian and the Smithian, despite being common at higher lati- tudes at these times (fig. S1 and table S2). This rarity is extraordinary because Early Triassic units, such as the dysoxic-anoxic Daye Forma- tion of South China, are widespread (supple- mentary text 7) and yet do not yield a fossil fish fauna. The general absence of ichthyofauna in equatorial regions coincides with the temperature maxima reconstructed from the d18Oapatite record, and we interpret this coincidence as recording equatorial exclusion because of inhospitably high temperatures. In contrast, invertebrates remain common in these intervals (19), especially sessile mollusks with their better adapted oxyconform- ing metabolism allowing them to cope with syn- ergistic stresses of high temperature and low oxygen (17, 20). Like fish, marine reptiles also exhibit high aerobic activity and are likely to have had a relatively low oxygen-limited thermal tolerance. Examining Early Triassic marine rep- tile (ichthyosaur) occurrences reveals that they too are not found in equatorial waters until the middle-late Spathian (supplementary text 6), ~1 to 2 My after their first appearance in higher latitudes during the Smithian (21, 22). Other notable absences from equatorial oceans are cal- careous algae, whose outage spans the entire end- Permian–early Spathian interval although they are present in higher latitudes [e.g., Spitsbergen, (23)]. Their equatorial absence (supplementary text 8) likely reflects inhibiting temperatures, whereas the abundance of calcimicrobial carbon- ates in shelf waters, one of the stand-out features of the Early Triassic (24), was possible because of the much higher temperature tolerance of cyano- bacterial photosynthesis (16).

Critically high temperatures may also have excluded terrestrial animal life from equatorial Pangea, and with SSTs approaching 40°C the land temperatures are likely to have fluctuated to even higher levels. Our compilation of tetra- pod fossil occurrences reveals them to be gen- erally absent between 30°N and 40°S in the Early Triassic (Fig. 1), with rare exceptions (25, 26); this is a stark contrast to Middle and Late Triassic occurrences, when they occur at all latitudes (fig. S1). This equatorial “tetrapod gap” does

not reflect an absence of suitable strata for their preservation. For example, the Buntsandstein of Europe is one of the best known and most in- tensively investigated terrestrial formations of the Early Triassic; tetrapods are exceptionally rare in the lower part (Induan) and only become common in middle and upper units (late Early Triassic to Middle Triassic) (27). The tetrapod gap of equatorial Pangea coincides with an end- Permian to Middle Triassic global “coal gap” that indicates the loss of peat swamps (5). Peat for- mation, a product of high plant productivity, was only reestablished in the Anisian and then only in high southern latitudes (5), although gym- nosperm forests appeared earlier (in the Early Spathian), but again only in northern and south- ern higher latitudes (28, 29). In equatorial Pangea, the establishment of conifer-dominated forests was not until the end of the Spathian (30), and the first coals at these latitudes did not appear until the Carnian ~15 My after their end-Permian disappearance (5). These signals suggest equa- torial temperatures exceeded the thermal toler- ance for many marine vertebrates at least during two thermal maxima, whereas terrestrial equato- rial temperatures were sufficiently severe to sup- press plant and animal abundance during most of the Early Triassic.

Thermal tolerance is likely to decrease for organisms with larger body sizes (31). Nonlethal effects of temperature increase include smaller adult size, which, in conjunction with increased juvenile mortality at higher temperatures (32, 33), will produce a fossil record dominated by small individuals. This is a well-known phenomenon in the Early Triassic marine fossil record and has been termed the Lilliput effect (4). We suggest that this effect is a response to high tempera- tures and that it should be most clearly seen in equatorial assemblages, especially during the Griesbachian and Smithian thermal maxima. This prediction is confirmed by data from equatorial marine fossils where small body and trace fossil assemblages are confined to these intervals (34, 35). Low oxygen levels also are known to cause small size in marine invertebrates (36), but, although marine dysoxia was a global phenomenon in the Early Triassic (18), the restriction of the Lilliput effect to equatorial latitudes indicates that this was primarily a temperature-controlled phenomenon.

The relation between global warming and extinction can be examined in the Early Triassic. The rapid temperature rise across the Permian- Triassic boundary coincides with mass extinction, although absolute temperatures at the time of crisis were only modest [< 30°C (9)]. Together with temperature rise, synergistic factors, such as spread of anoxia, may also play important roles in marine extinction (2, 18). However, the sub- sequent loss of many Permian holdover taxa later in the Griesbachian (conodonts, radiolarian, and brachiopods) may reflect lethal temperatures fol- lowed by temporary recovery and radiation in the cooler Dienerian (Fig. 3). The clearest temperature- extinction link is with the LSTM and the end-

Smithian event that saw major losses among many marine groups, including bivalves, cono- donts, and ammonoids (37–39). Contemporane- ous losses among tetrapods on land (25) suggest that this was a crisis that affected a broad di- versity of ecosystems.

The ultimate driving factor behind the end- Permian warming long has been attributed to greenhouse gas emissions, either from volcano- genic (8) or thermogenic sources (40). Both are expected to leave a negative excursion in the d13C record, and this is the case for both the end Permian–Griesbachian and Smithian intervals (Fig. 2), although it has yet to be demonstrated that a second pulse of Siberian volcanism oc- curred in the Smithian. However, to maintain high temperatures for the ~5 My of the Early Triassic requires strong, persistent greenhouse conditions. High temperatures also could greatly enhance the activity of decomposers (e.g., fungi and bacteria), resulting in the release of large amounts of terrestrial light carbon into the at- mosphere (41) and consequently forming oligo- trophic, humus-poor soils as observed in modern Amazon rainforests and in Early Triassic soils of Australia and Antarctica (42). Together with global suspension of peat formation, elevated de- composition rates may have led to a significant reduction in organic carbon burial on land fur- ther contributing to higher atmospheric CO2 levels (43).

High and oscillating temperatures in the Early Triassic likely controlled the pace and nature of recovery in the aftermath of the end-Permian mass extinction as shown by an inverse relation- ship between the temperature and biodiversity changes, the temporary loss of both marine and terrestrial vertebrates, and the reduced size of the remaining invertebrates. SSTs derived from d18O data offer no evidence that a climate ther- mostat may ameliorate tropical warming by re- distributing warmth to the poles (44). Rather, extreme global warming may progressively force taxa to vacate the tropics and move to higher lat- itudes or become extinct. Marine organisms ex- hibiting low oxygen-dependent thermal tolerance, such as vertebrates, are the first to leave.

References and Notes 1. M. Bálint et al., Nat. Clim. Change 1, 313 (2011). 2. A. Hallam, P. B. Wignall, Mass Extinctions and Their

Aftermath (Oxford Univ. Press, Oxford, 1997). 3. J. L. Payne et al., Science 305, 506 (2004). 4. R. J. Twitchett, Palaeogeogr. Palaeoclimatol. Palaeoecol.

252, 132 (2007). 5. G. J. Retallack, J. J. Veevers, R. Morante, Geol. Soc.

Am. Bull. 108, 195 (1996). 6. D. L. Kidder, T. R. Worsley, Palaeogeogr. Palaeoclimatol.

Palaeoecol. 203, 207 (2004). 7. M. K. Reichow et al., Earth Planet. Sci. Lett. 277,

9 (2009). 8. S. V. Sobolev et al., Nature 477, 312 (2011). 9. M. M. Joachimski et al., Geology 40, 195 (2012).

10. D. L. Clark, W. Cheng-Yuan, C. J. Orth, J. S. Gilmore, Science 233, 984 (1986).

11. Information on materials and methods is available on Science Online.

12. T. D. Frank, Data report: Geochemistry of Miocene sediments, Site 1006 and 1007, Leeward margin, Great

www.sciencemag.org SCIENCE VOL 338 19 OCTOBER 2012 369

REPORTS

o n O

ct o b e r

2 2 , 2 0 1 2

w w

w .s

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Bahama Bank, in Proceedings of the Ocean Drilling Program, Scientific Results, P. K. Swart, G. P. Eberli, M. J. Malone, J. F. Sarg, Eds. (Ocean Drilling Program, College Station, TX, 2000), vol. 166, pp. 137–143.

13. J. Berry, O. Bjorkman, Annu. Rev. Plant Physiol. 31, 491 (1980).

14. R. J. Ellis, Nature 463, 164 (2010). 15. G. N. Somero, Annu. Rev. Physiol. 57, 43 (1995). 16. H. O. Pörtner, Comp. Biochem. Physiol. 132, 739

(2002). 17. H. O. Pörtner, Naturwissenschaften 88, 137 (2001). 18. P. B. Wignall, R. J. Twitchett, Spec. Pap. Geol. Soc. Am.

356, 395 (2002). 19. T. Galfetti et al., Sediment. Geol. 204, 36 (2008). 20. H.-O. Pörtner, J. Exp. Biol. 213, 881 (2010). 21. J. M. Callaway, D. B. Brinkman, Can. J. Earth Sci. 26,

1491 (1989). 22. C. B. Cox, D. G. Smith, Geol. Mag. 110, 405 (1973). 23. P. B. Wignall, R. Morante, R. Newton, Geol. Mag. 135,

47 (1998). 24. A. H. Knoll, R. K. Bambach, J. L. Payne, S. Pruss,

W. W. Fischer, Earth Planet. Sci. Lett. 256, 295 (2007). 25. S. G. Lucas, Palaeogeogr. Palaeoclimatol. Palaeoecol.

143, 347 (1998). 26. M. Borsuk-Białynicka, E. Cook, S. E. Evans, T. Maryań,

Acta Palaeontol. Pol. 44, 167 (1999). 27. H.-D. Sues, N. C. Fraser, Triassic Life on Land

(Columbia Univ. Press, New York, 2010). 28. T. Galfetti et al., Geology 35, 291 (2007). 29. E. Schneebeli-Hermann et al., Palaeogeogr.

Palaeoclimatol. Palaeoecol. 339–341, 12 (2012).

30. C. V. Looy, W. A. Brugman, D. L. Dilcher, H. Visscher, Proc. Natl. Acad. Sci. U.S.A. 96, 13857 (1999).

31. H. O. Pörtner, R. Knust, Science 315, 95 (2007). 32. M. J. Angilletta, Thermal Adaptation- A Theoretical and

Empirical Synthesis (Oxford Univ. Press, New York, 2009). 33. J. A. Sheridan, D. Bickford, Nat. Clim. Change 1, 401

(2011). 34. B. Metcalfe, R. J. Twitchett, N. Price-Lloyd, Palaeogeogr.

Palaeoclimatol. Palaeoecol. 308, 171 (2011). 35. R. J. Twitchett, Palaeogeogr. Palaeoclimatol. Palaeoecol.

154, 27 (1999). 36. G. Chapelle, L. S. Peck, Nature 399, 114 (1999). 37. S. M. Stanley, Proc. Natl. Acad. Sci. U.S.A. 106, 15264 (2009). 38. M. J. Orchard, Palaeogeogr. Palaeoclimatol. Palaeoecol.

252, 93 (2007). 39. J. Chen, in Mass Extinction and Recovery: Evidences from

the Palaeozoic and Triassic of South China, J. Rong, Z. Fang, Eds. (Univ. of Science and Technology of China Press, Heifei, 2004), vol. II, pp. 647–700.

40. H. Svensen et al., Earth Planet. Sci. Lett. 277, 490 (2009). 41. S. M. Stanley, Proc. Natl. Acad. Sci. U.S.A. 107, 19185

(2010). 42. G. J. Retallack, E. S. Krull, Aust. J. Earth Sci. 46, 785 (1999). 43. W. Broecker, S. Peacock, Global Biogeochem. Cycles 13,

1167 (1999). 44. M. Huber, Science 321, 353 (2008). 45. A. M. Ziegler, M. L. Hulver, D. B. Rowley, in Late Glacial

and Postglacial Environmental Changes–Quaternary, Carboniferous-Permian and Proterozoic, I. P. Martini, Ed. (Oxford Univ. Press, New York, 1997), pp. 111–146.

46. G. Muttoni et al., Geoarabia 14, 17 (2009).

47. D. J. Lehrmann et al., Palaios 18, 138 (2003). 48. R. A. Locarnini et al., World Ocean Atlas 2009, Volume 1:

Temperature, S. Levitus, Ed. [National Oceanic and Atmospheric Administration (NOAA) Atlas NESDros. Inf. Serv. 68, U.S. Government Printing Office, Washington, DC, 2010].

49. H. Song et al., Geology 39, 739 (2011). 50. D. Sun, S. Shen, in Mass Extinction and Recovery: Evidences

from the Palaeozoic and Triassic of South China, J. Rong, Z. Fang, Eds. (Univ. of Science and Technology of China Press, Heifei, China, 2004), vol. II, pp. 543–570.

51. H. Pan, D. H. Erwin, Palaeoworld 4, 249 (1994). 52. L. O'Dogherty et al., Geodiversitas 31, 213 (2009).

Acknowledgments: D. Lutz, F. Nenning, B. Yang, and X. Liu are acknowledged for lab and field assistance. This study was supported by Chinese 973 Program (2011CB808800) and the Natural Science Foundation of China (41172024 and 40830212). Y.S. acknowledges China University of Geosciences and China Scholarship Council for split-site Ph.D. at Wuhan, Leeds, and Erlangen.

Supplementary Materials www.sciencemag.org/cgi/content/full/338/6105/366/DC1 Materials and Methods Supplementary Text Fig. S1 Tables S1 to S4 References (53–150)

1 May 2012; accepted 4 September 2012 10.1126/science.1224126

A Complete Terrestrial Radiocarbon Record for 11.2 to 52.8 kyr B.P. Christopher Bronk Ramsey,1* Richard A. Staff,1 Charlotte L. Bryant,2 Fiona Brock,1 Hiroyuki Kitagawa,3 Johannes van der Plicht,4,5 Gordon Schlolaut,6 Michael H. Marshall,7 Achim Brauer,6 Henry F. Lamb,7 Rebecca L. Payne,8 Pavel E. Tarasov,9 Tsuyoshi Haraguchi,10 Katsuya Gotanda,11 Hitoshi Yonenobu,12 Yusuke Yokoyama,13 Ryuji Tada,13 Takeshi Nakagawa8

Radiocarbon (14C) provides a way to date material that contains carbon with an age up to ~50,000 years and is also an important tracer of the global carbon cycle. However, the lack of a comprehensive record reflecting atmospheric 14C prior to 12.5 thousand years before the present (kyr B.P.) has limited the application of radiocarbon dating of samples from the Last Glacial period. Here, we report 14C results from Lake Suigetsu, Japan (35°35′N, 135°53′E), which provide a comprehensive record of terrestrial radiocarbon to the present limit of the 14C method. The time scale we present in this work allows direct comparison of Lake Suigetsu paleoclimatic data with other terrestrial climatic records and gives information on the connection between global atmospheric and regional marine radiocarbon levels.

L ake Suigetsu contains annually laminated sediments that preserve both paleoclimate proxies and terrestrial plant macrofossils

that are suitable for radiocarbon dating. The lake’s

potential to provide an important archive of at- mospheric radiocarbon (14C) was realized in 1993 (1). However, the single SG93 sediment core then recovered included missing intervals be- tween successive sections (2). This, together with the difficulty of visual varve counting, resulted in inconsistency between the SG93 and other 14C calibration records (3). The SG06 core-set re- covered in 2006 consists of four parallel cores that together avoid any such sedimentary gaps (4). Here, we report 651 14C measurements cov- ering the period between 11.2 and 52.8 thousand years before the present (kyr B.P.) tied to a time scale derived from varve counting and temporal constraints from other records. Using visual mark- ers, we applied a composite depth (CD) scale to all cores, including SG93. We also define an event- free depth (EFD), which is the CD with substan-

tial macroscopic event layers (such as turbidites and tephras) removed.

Accelerator mass spectrometry radiocarbon dating (5) has been conducted on terrestrial plant macrofossils selected from the SG06 cores to cover the full 14C time range, from the present to the detection limit of the 14C method (0 to 41 m CD) (table S1). The results already reported from the control period (0 to 12.2 kyr B.P.) (6), covered by the tree-ring–derived calibration curve (7), act to demonstrate the integrity of the sediments and to anchor the floating SG06 varve chronology, because varves do not extend into the Holocene.

The varve-based chronology for SG06 (5, 8, 9) provides our best estimate of the true age of the cores for the period ~10.2 to 40.0 kyr B.P., based only on information from the site. It provides good relative chronological precision and has the advantage of being independent of other dating techniques. However, the cumulative counting un- certainty inevitably increases with age (~6% at 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.

To better constrain the uncertainties in the varve chronology, we can directly compare the Suigetsu data set and other archives that provide information on atmospheric 14C and associated independent ages. The two most useful records for this purpose are the Bahamas speleothem GB89- 25-3 (10) and the Hulu Cave speleothem H82 (11), both of which have extensive 14C- and U-Th– based chronologies. In both cases, we would ex- pect the radiocarbon in the speleothems to respond to changes in atmospheric 14C content, despite the groundwater containing a dead-carbon fraction (DCF) from dissolved carbonates. Estimated DCF for these speleothems was 2075 T 270 radiocarbon

1University of Oxford, Oxford, UK. 2Natural Environment Re- search Council Radiocarbon Facility, Scottish Universities Environmental Research Centre, East Kilbride, UK. 3Nagoya University, Nagoya, Japan. 4University of Groningen, Groningen, Netherlands. 5University of Leiden, Leiden, Netherlands. 6GeoForschungsZentrum German Research Centre for Geosci- ences, Potsdam, Germany. 7Aberystwyth University, Aberystwyth, UK. 8University of Newcastle, Newcastle upon Tyne, UK. 9Free University Berlin, Berlin, Germany. 10Osaka City University, Osaka, Japan. 11Chiba University of Commerce, Chiba, Japan. 12Naruto University of Education, Naruto, Japan. 13University of Tokyo, Tokyo, Japan.

*To whom correspondence should be addressed. E-mail: [email protected]

19 OCTOBER 2012 VOL 338 SCIENCE www.sciencemag.org370

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