LETTERS PUBLISHED ONLINE: 2 DECEMBER 2012 | DOI: 10.1038/NGEO1649 Two pulses of extinction during the Permian–Triassic 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 Earth history. Over 90% of marine 70.9% respectively (Fig. 2a), suggesting a two-episode extinction species 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 extinction event around 252.3 million with Meldahl's simulated stepwise mass extinction11, supporting a years ago2,4–6, and has been variously attributed to the eruption clear two-episode extinction pattern (Fig. 2b). of the Siberian Traps 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-year 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 stage 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 corals, 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 fossil 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 China that record about 450 kyr of conodonts, ostracods, bivalves, brachiopods 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 conodont zones which have graph, but it does not provide a statistical test 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 sedimentation 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 extinctions 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 group-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, sponges, trilobites and radiolarians suffered a single sponges, trilobites, small foraminifers, ostracods, gastropods, bra- extinction in the first pulse whereas small foraminifers, ostracods, chiopods, bivalves, bryozoans, crinoids, ophiuroids and blastoids 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, ostracod (484/537) became extinct in the P–Tr boundary interval (from range data suggest a single extinction event near the P–Tr boundary the Neogondolella 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 Stratotype 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 Geology, China University of Geosciences, Wuhan 430074, China, 2School of Earth and Environment, University of Leeds, Leeds LS2 9JT, UK. *e-mail: [email protected]. 52 NATURE GEOSCIENCE j VOL 6 j JANUARY 2013 j www.nature.com/naturegeoscience © 2013 Macmillan Publishers Limited. All rights reserved. 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 Hindeodus 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 j 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 j 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 NATURE GEOSCIENCE j VOL 6 j JANUARY 2013 j www.nature.com/naturegeoscience 53 © 2013 Macmillan Publishers Limited. All rights reserved. LETTERS NATURE GEOSCIENCE DOI: 10.1038/NGEO1649 Total in Conodontzones Age (kyr) CalcareousAlgae FusulinidsRugosecorals Sponges Trilobites Radiolarians SmallForaminifersOstracods BrachiopodsBivalves Gastropods Ammonoids