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LETTERS PUBLISHED ONLINE: 2 DECEMBER 2012 | DOI: 10.1038/NGEO1649

Two pulses of during the Permian– crisis

Haijun Song1*, Paul B. Wignall2, Jinnan Tong1 and Hongfu Yin1

The Permian–Triassic mass extinction is the most severe (bed 28 at Meishan), where the extinction rates are 56.5% and biotic crisis identified in history. Over 90% of marine 70.9% respectively (Fig. 2a), suggesting a two-episode extinction were eliminated1,2, causing the destruction of the pattern in the P–Tr boundary interval. The frequency distribution marine ecosystem structure3. This biotic crisis is generally of last occurrences for 508 species near the P–Tr boundary accords interpreted as a single around 252.3 million with Meldahl’s simulated stepwise mass extinction11, supporting a ago2,4–6, and has been variously attributed to the eruption clear two-episode extinction pattern (Fig. 2b). of the or possibly a bolide impact7–10. Here The extinction event near the top of the N. yini zone was reported we demonstrate that the marine extinction consisted of two to kill >90% species at Meishan2 and elsewhere15. However, our pulses, separated by a 180,000- recovery phase. We new collection has shown many more taxa survived this crisis than evaluated the range of 537 species representing 17 marine hitherto appreciated: about 111 species (28.7% of total species groups in seven Chinese sections from a 450,000-year interval in the N. yini zone) survived the first crisis and persisted into spanning the Permian–Triassic boundary. The first of the N. meishanensis-I. staeschei zones and were joined by 122 extinction occurred during the latest Permian, and was marked newcomers, indicating substantial origination rates in the aftermath by the extinction of 57% of species, namely all plankton of the first extinction pulse. Most of the survivors (87.4%; 97/111) and some benthic groups, including algae, rugose , and newcomers (83.6%; 102/122) did not survive beyond the and fusulinids. The second phase occurred in the earliest I. staeschei zone (the second extinction event horizon). Generally, Triassic, and resulted in the extinction of 71% of the remaining the last recorded occurrence of a species is earlier than the actual species. This second extinction phase fundamentally altered time of extinction (this is known as the Signor–Lipps effect13). the marine ecosystem structure that had existed for the The more common a species, the shorter the gap is likely to be previous 200 million years. Because the two pulses showed between the last occurrence and the time a species breathed different extinction selectivity, we conclude that they may have its last. Thus, common species are more useful to demonstrate had different environmental causes. the extinction horizon than uncommon species. To minimize The nature of the Permian–Triassic (P–Tr) mass extinction is the Signor–Lipps effect, Meldahl’s method (see Supplementary a subject of intense debate: both its timing and causation are key Methods) was applied to all of the major taxa occurrences, including facets that remain unresolved. Our study focuses on seven P–Tr calcareous algae, fusulinids, radiolarians, gastropods, ammonoids, boundary sections in South that record about 450 kyr of , , bivalves, and small foraminifers. marine deposition in habitats ranging from lagoon-shoals to basin This confirmed the two-episode extinction pattern near the P–Tr centre locations (Supplementary Table S1 and Figs S1 and S2). boundary (Fig. 2c). Meldahl’s method provides a useful visual Correlation is based on high-resolution zones which have graph, but it does not provide a statistical that can be associated an average duration of only 60 kyr. Fossil occurrences were obtained with a p-value. Furthermore, it is based on the assumption of from both published papers and our own continuous sampling uniform sampling density, which is not achievable in sections where (Supplementary Table S1) and both Meldahl’s method11 and the lithologies and rates varied. Therefore, a likelihood likelihood ratio test12 were applied to fossil range data to evaluate ratio test (see Supplementary Methods) was applied to all of the the Signor–Lipps effect (backward smearing of resulting major taxa from our six sections, and the results confirm the from incomplete sampling)13. two-pulsed extinction (Supplementary Figs S5–S10). A total of 537 species in 252 genera belonging to 17 groups Our study shows -specific extinction selection between were recorded in the P–Tr boundary strata, including radiolarians, the two P–Tr extinction pulses. Calcareous algae, fusulinids, ammonoids, conodonts, calcareous algae, fusulinids, rugose corals, rugose corals, , and radiolarians suffered a single sponges, trilobites, small foraminifers, ostracods, gastropods, bra- extinction in the first pulse whereas small foraminifers, ostracods, chiopods, bivalves, bryozoans, , ophiuroids and brachiopods, bivalves, gastropods, ammonoids and conodonts (Fig. 1, Supplementary Table S2). About 90% of the total species underwent a two-stage extinction (Fig. 3). In contrast, (484/537) became extinct in the P–Tr boundary interval (from range data suggest a single extinction event near the P–Tr boundary the yini zone to the Isarcicella staeschei zone). The from previous work at the Meishan section2. However, ostracods extinction rate (extinct species divided by total species at the same are rare and of low diversity in the N. meishanensis–I. staeschei slope level) does not exceed 30% at any level except at the top of N. facies of Meishan (only one species16). In contrast, over 20 ostracod yini zone (bed 24e at Meishan, the Global Section and species survived the latest Permian extinction event and occurred, Point of the P–Tr Boundary14) and the top of I. staeschei zone together with 13 newcomers, in N. meishanensis–I. staeschei zones

1State Key Laboratory of Biogeology and Environmental , China University of Geosciences, Wuhan 430074, China, 2School of Earth and Environment, University of Leeds, Leeds LS2 9JT, UK. *e-mail: [email protected].

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NATURE GEOSCIENCE DOI: 10.1038/NGEO1649 LETTERS

Species richness dont Beds in eishan300 200 100 0 Conozones M Species distribution 39¬46

Isarcicella 33¬38 isarcica 30¬32

29 ± Earliest Triassic extinction Triassic 28 252.10 0.06 Myr I. staeschei 27d

Hindeodus 27c parvus 50 kyr Neogondolella 27b taytorae 27a changxingensis 26 Neogondolella 252.28 ± 0.08 Myr meishanensis 25 Latest Permian extinction 24e Permian 24d Neogondolella yini 24c

24b

24a

050 100 150 200 250 300 350 400 450 500

Figure 1 | Stratigraphic ranges of fossil species (indicated by vertical grey lines) from the latest Permian to the earliest Triassic in seven P–Tr boundary sections of South China. This figure shows a two-step extinction pattern, which is not restricted to one section or palaeoenvironment (Supplementary Fig. S3) and also is not affected by these species in open nomenclature (Supplementary Fig. S4). Species numbers are shown on the x axis. The stratigraphic ranges of fossil species in each section are shown in the fossil database (Supplementary Table S2). Absolute age data are from ref. 6.

Conodont zones kyr 450 a b c

Isarcicella 400 Fusulinids isarcica Extinctions Calcareous 350 algae I.staeschei Radiolarians 300 Hindeodus parvus Gastropods

250 Ammonoids Neogondolella Originations taytorae 200 Conodonts Hindeodus changxingensis Neogondolella Ostracods meishanensis 150 Bivalves

100 PermianNeogondolella Triassic yini Brachiopods

50 Small foraminifers

0 0.0 0.2 0.4 0.6 0.8 0 50 100 150 0 20 40 60 80 100 Extinction and origination rates Number of last occurrence Stratigraphic abundance (%)

Figure 2 | Analysis of species ranges around the P–Tr boundary in South China. a, Species extinction and origination rates near the P–Tr boundary. b, Histograms plotting the total number of time intervals in which a species occurs versus the age of last occurrence for the major taxa. c, Plots of the stratigraphic abundance versus the age of last occurrence for the major taxa. in shallow platform facies (Supplementary Table S2; ref. 17). For in the second pulse (Supplementary Fig. S12); for ostracods, the three groups, which show two-stage extinctions, their record is first extinction pulse saw losses in all environments but they were sufficiently abundant to reveal distinct environmental differences especially severe in basin settings (Supplementary Fig. S13); for in their extinction history; for foraminifers, extinction losses were brachiopods, the two-stage extinction pattern occurred across the seen in most habitats during the first extinction pulse and they marine spectrum during both pulses (that is shallow-water, slope only remained diverse in slope settings before their elimination and basin facies; Supplementary Fig. S14). These observations reveal

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LETTERS NATURE GEOSCIENCE DOI: 10.1038/NGEO1649

Total in Conodontzones Age (kyr) CalcareousAlgae FusulinidsRugosecorals Sponges Trilobites Radiolarians SmallForaminifersOstracods BrachiopodsBivalves Gastropods Ammonoids Conodonts this study Data from ref.Data 6 from ref. 2 450

Isarcicella isarcica 400

350 Triassic Earliest Triassic extinction I. staeschei

300 Hindeodus parvus

250 Neogondolella taytorae 200 Hindeodus Latest Permian extinction changxingensis Neogondolella Number of species meishanensis 150 18 13 4 3 221102 41 85 47 27 25 30 Permian 100 Neogondolella yini 50

334219 110 0

Figure 3 | Species diversity pattern among marine taxa from Permian–Triassic boundary strata showing great variability in the extinction pattern. Calcareous algae, fusulinids, rugose corals, trilobites and radiolarians were entirely lost in the latest Permian (the top of Neogondolella yini zone or the base of Neogondolella meishanensis zone). A second group, including small foraminifers, ostracods, brachiopods, bivalves, gastropods, ammonoids and conodonts, seems to be less affected by this end-Permian mass extinction and exhibits a two-stage extinction pattern near the P–Tr boundary. Total diversity is clearly divided into three parts by the two extinction pulses, with three distinct species richness levels seen (Supplementary Fig. S11). The last two columns are from refs 2 and 6, respectively, and show a different species richness distribution: species richness in our data set is much higher than the other two (for example, 334 species in the latest Permian in our data set versus 219 species in ref. 6 and 110 species in ref. 2); our data set shows that the species richness levels are constant in Permian–Triassic boundary strata (N. meishanensis-Isarcicella staeschei zones) whereas both refs 2 and 6 show decreasing richness at this time. a hitherto unappreciated complexity to the crisis and show that Similarly, the proportion of physiologically buffered marine a true extinction pattern requires evaluation of the entire span of taxa remained stable in the last 200 Myr of the Palaeozoic3, but marine environments. changed observably during the earliest Triassic crisis (Fig. 4c). The origination rate increased in the interval between the Physiologically unbuffered taxa are characterized by low rates two extinction events (Fig. 2a), indicating partial recovery in the of metabolism, limited internal circulation and investment in aftermath of the first crisis. The mean value of the origination substantial CaCO3 , and include many typical denizens rate in the N. meishanensis–I. staeschei zones is 12.9%, which is of Palaeozoic seafloors (for example, brachiopods, corals, cal- higher than the 5.0% rate in the N. yini zone and 11.0% in the careous sponges, crinoids, ophiuroids, blastoids, radiolarians, I. isarcica zone. Of the 122 new species in the N. meishanensis–I. fusulinids and small foraminifers) whilst buffered taxa in- staeschei zones, conodonts (25 species), bivalves (24 species) and clude bivalves, gastropods, ammonoids, trilobites, ostracods and brachiopods (21 species) dominate, together with gastropods (16 conodonts. The proportion of unbuffered relative to buffered species), foraminifers (15 species), ammonoids (9 species) and taxa at the generic level fell from 57% before mass extinction ostracods (7 species). These newcomers plus survivors have been to 20% afterwards. termed a ‘mixed-fauna’18 or a ‘transitional fauna’19, because both It is commonly thought that the latest Permian mass extinction Permian-type survivors and Triassic-type newcomers co-occur. played a pivotal role in the reversal of taxonomic dominance All -building taxa and most radiolarians became extinct between brachiopods and bivalves22. Here, our data confirm this during the latest Permian crisis (Fig. 4a), marking the beginning changeover, but show that, in South China at least, it occurred of the ‘metazoan reef gap’ and ‘chert gap’ respectively20. In in the earliest Triassic after the second pulse of extinction. addition, the P–Tr marine mass extinction caused a great change Thus, the proportional change of species relative in dominance from non-motile to motile animals3,21. For the to bivalve species increased from <71% to >76% during the single-extinction and prolonged-crisis hypotheses this change is latest Permian, but there is little change at the genus level until envisaged to be synchronous with the crisis. However, we show the second extinction pulse (Fig. 4d). The relative proportion of here that the proportional diversity of motile and non-motile benthos versus nekton also shows significant changes, with the metazoans was unaffected by the first extinction pulse (Fig. 4b) latter group becoming more significant in the aftermath of the whereas non-motile taxa suffering markedly higher extinction rates extinction pulses (Fig. 4e). in the second pulse (Fig. 4b). Thus, the proportion of non-motile In summary, two episodes of marine extinction near the P–Tr taxa at genus level was 70% near the P–Tr boundary (a little boundary play different roles in the transition from a Palaeozoic higher than the post-Caradoc Palaeozoic average of 58% (ref. 3)), fauna to a Modern fauna: the latest Permian extinction killed but this decreased to 47% (close to the mean3) after reef-building taxa, most plankton and many benthic and nektonic the second pulse. groups whilst the earliest Triassic extinction not only resulted

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NATURE GEOSCIENCE DOI: 10.1038/NGEO1649 LETTERS

abcde

Isarcicella Motile Physiologically Bivalves Nekton isarcica animals buffered taxa Earliest Triassic extinction I. staeschei

Hindeodus parvus Benthos Non-motile Neogondolella animals Brachiopods Benthos taytorae

Hindeodus Physiologically unbuffered taxa changxingensis Latest Permian Neogondolella extinction meishanensis Permian Triassic Nekton Neogondolella yini Plankton Reef building taxa

0 100 200 300 0.0 0.2 0.4 0.6 0.8 1.0 0.0 0.2 0.4 0.6 0.8 1.0 0.0 0.2 0.4 0.6 0.8 1.0 0.0 0.2 0.4 0.6 0.8 1.0 Species richness Proportion of metazoan Proportion of taxa Brachiopod/bivalve ratio Proportion of taxa

Figure 4 | Changes of marine ecosystem structures in the P–Tr interval. a, Species diversity of benthos, nekton, plankton and reef-building taxa. b, The proportion of non-motile animals (epifaunal bivalves, brachiopods, corals, sponges, bryozoans, crinoids, ophiuroids and blastoids) versus motile animals (infaunal bivalves, gastropods, ammonoids and conodonts). c, The proportion of physiologically unbuffered taxa versus physiologically buffered taxa. d, The relative proportion of brachiopods versus bivalves. e, The proportion of benthos (bivalves, brachiopods, corals, sponges, crinoids, ophiuroids, blastoids, fusulinids, ostracods, gastropods, trilobites and algae) versus nekton (ammonoids and conodonts). Diamonds show genus levels and circles show species levels. in an observable biodiversity decrease but also wrought major spread of anoxia coincided with severe global warming, a stressor ecological change by preferentially eliminating both non-motile and expected to affect shallow rather than deep-water taxa and high physiologically unbuffered taxa. latitude rather than low latitude organisms30. Our data, from a A plethora of extinction mechanisms have been proposed for the single low-latitude continent, cannot truly address this factor, but P–Tr marine mass extinction, including marine anoxia, volcanic the loss of many shallow-water groups shows that it remains a winter, hypercapnia, global warming, ocean acidification and possibility. Preferential loss of unbuffered taxa is seen in both increased flux15,20,23–27. Assessing the relative significance extinction pulses and can be attributed to hypercapnia, although of these alternatives has proved difficult because the great scale the importance of this stress mechanism is difficult to unravel from of losses masks any extinction selectivity. Our recognition of two other factors, such as anoxia, warming and acidification. Unlike discrete events, separated by a 180 kyr period of recovery and the first extinction pulse, no subsequent rapid radiation has been radiation, with differing impact on community structure, allows reported, implying that the stressful conditions persisted at least some evaluation of proposed kill mechanisms. Aspects of first-pulse into the Griesbachian Stage. losses, including the loss of radiolarians, reef taxa and many shallow-water taxa indicates severe ecological devastation in warm, Received 13 June 2012; accepted 29 October 2012; shallow waters and surface waters. This accords with both volcanic published online 2 December 2012 winter and ocean acidification scenarios. Anoxia has also been implicated in this crisis and other facets of the first extinction pulse, References including the loss of all deep-water foraminifers and ostracods, 1. Erwin, D. H. The Permo-Triassic extinction. Nature 367, 231–236 (1994). 2. Jin, Y. G. et al. Pattern of marine mass extinction near the Permian–Triassic pointing to the role of a deep-water stressor such as anoxia-driven boundary in South China. Science 289, 432–436 (2000). habitat loss, especially in epicontinental basinal locations such as 3. Bambach, R. K., Knoll, A. H. & Sepkoski, J. J. Jr Anatomical and ecological those sampled in South China. However, the extinction record constraints on animal diversity in the marine realm. Proc. Natl from both open-ocean and deep-water continental margin sections Acad. Sci. USA 99, 6854–6859 (2002). reveals a diversity crash of before the onset of persistent 4. Wignall, P. B. & Hallam, A. Anoxia as a cause of the Permian/Triassic mass 28,29 extinction: Facies evidence from northern Italy and the western United States. anoxic deposition , indicating first-stage losses predate long- Palaeogeogr. Palaeoclimatol. Palaeoecol. 93, 21–46 (1992). term ocean redox changes. The first crisis was short lived because 5. Rampino, M. R. & Adler, A. C. Evidence for abrupt latest Permian mass recovery was underway immediately above the extinction horizon, extinction of : Results of tests for the Signor–Lipps effect. Geology suggesting that long-term changes, such as increased run-off, are 26, 415–418 (1998). 6. Shen, S. et al. Calibrating the end-Permian mass extinction. Science 334, unlikely to have played a role at this stage. Anoxia is clearly 1367–1372 (2011). related to the second extinction pulse in the : the 7. Renne, P., Black, M., Chao, Z. Z., Richards, M. & Basu, A. Synchrony and replacement of a benthos-dominated community with a nekton- causal relations between Permian–Triassic boundary crises and Siberian Flood dominated community, the complete loss of deep-water benthos Volcanism. Science 269, 1413–1416 (1995). and the relative success of bivalves, a dysoxia-tolerant group, can 8. Becker, L. et al. : A possible end-Permian offshore of Northwestern . Science 304, 1469–1476 (2004). all be accounted for by the spread of oxygen-poor conditions, for 9. Reichow, M. K. et al. The timing and extent of the eruption of the Siberian which there is overwhelming sedimentological and geochemical Traps large igneous province: Implications for the end-Permian environmental evidence at this time4,28,29. Marine temperature proxies suggest the crisis. Earth Planet. Sci. Lett. 277, 9–20 (2009).

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10. Kaiho, K. et al. End-Permian catastrophe by a bolide impact: Evidence of a 25. Grice, K. et al. Photic zone euxinia during the Permian–Triassic superanoxic gigantic relase of sulfur from the mantle. Geology 29, 815–818 (2001). event. Science 307, 706–709 (2005). 11. Meldahl, K. H. Sampling, species abundance, and the stratigraphic signature 26. Algeo, T. J. & Twitchett, R. J. Anomalous Early Triassic sediment fluxes due of mass extinction: A test using tidal flat molluscs. Geology 18, to elevated rates and their biological consequences. Geology 38, 890–893 (1990). 1023–1026 (2010). 12. Wang, S. C. & Everson, P. J. Confidence intervals for pulsed mass extinction 27. Clapham, M. E. & Payne, J. L. Acidification, anoxia, and extinction: A multiple events. Paleobiology 33, 324–336 (2007). logistic regression analysis of extinction selectivity during the Middle and Late 13. Signor, P. W. & Lipps, J. H. in Geological Implications of Impacts of Large Permian. Geology 39, 1059–1062 (2011). Asteroids and Comets on the Earth (eds Silver, L. T. & Schultz, P. H.) 291–296 28. Wignall, P. B. & Newton, R. Contrasting deep-water records from the upper (Geological Society of America Special Paper, 1982). Permian and lower Triassic of South Tibet and British Columbia: Evidence for 14. Yin, H., Zhang, K., Tong, J., Yang, Z. & Wu, S. The Global Stratotype a diachronous mass extinction. Palaios 18, 153–167 (2003). Section and Point (GSSP) of the Permian–Triassic boundary. Episodes 24, 29. Wignall, P. B. et al. An 80 million year oceanic redox history from Permian 102–114 (2001). to pelagic of the Mino-Tamba terrane, SW Japan, and the 15. Erwin, D. H. Extinction: How Life on Earth Nearly Ended 250 Million Years ago origin of four mass extinctions. Glob. Planet. Change 71, 109–123 (2010). (Princeton University Press, 2006). 30. Sun, Y. et al. Lethally hot temperatures during the early Triassic greenhouse. 16. Crasquin, S. et al. Ostracods (Crustacea) through the Permian–Triassic Science 338, 366–370 (2012). boundary in South China: The Meishan stratotype ( Province). J. Syst. Palaeontol. 8, 331–370 (2010). Acknowledgements 17. Liu, H. et al. Ostracod fauna across the Permian–Triassic boundary at This study was supported by the 973 Program (National Basic Research Program of Chongyang, Hubei Province, and its implication for the process of the mass China; 2011CB808800), the National Natural Science Foundation of China (40830212, extinction. Sci. China Earth Sci. 53, 810–817 (2010). 40921062, 41172312), the 111 Project (B08030), and the Fundamental Research Funds 18. Sheng, J. et al. Permian–Triassic boundary in middle and eastern Tethys. for the Central Universities, China University of Geosciences (Wuhan). J. Fac. Sci. Hokkaido Univ. 21, 133–181 (1984). 19. Yin, H. On the transitional bed and the Permian–Triassic boundary in South Author contributions China. Newsl. Stratigr. 15, 13–27 (1985). H.S. conceived the study. All authors participated in data preparation, discussion and 20. Knoll, A. H., Bambach, R. K., Payne, J. L., Pruss, S. & Fischer, W. W. interpretation. H.S. wrote the initial manuscript, and P.B.W. provided substantial Paleophysiology and end-Permian mass extinction. Earth Planet. Sci. Lett. 256, comments and editorial revisions to the manuscript. 295–313 (2007). 21. Sepkoski, J. J. Jr A factor anaytic description of the Phanerozoic marine fossil record. Paleobiology 7, 36–53 (1981). Additional information 22. Fraiser, M. L. & Bottjer, D. J. When bivalves took over the world. Paleobiology Supplementary information is available in the online version of the paper. Reprints and 33, 397–413 (2007). permissions information is available online at www.nature.com/reprints. 23. Hallam, A. & Wignall, P. B. Mass Extinctions and their Aftermath (Oxford Univ. Correspondence and requests for materials should be addressed to H.S. Press, 1997). 24. Benton, M. J. & Twitchett, R. J. How to kill (almost) all life: The end-Permian Competing financial interests extinction event. Trends Ecol. Evol. 18, 358–365 (2003). The authors declare no competing financial interests.

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