Migration controls extinction and survival patterns of foraminifers during the Permian-Triassic crisis in South China

Abstract The Permian-Triassic mass extinction, the greatest biotic crisis in Earth history, triggered the complete replacement of ecosystems with the 5–10% surviving species giving rise to the Mesozoic fauna. Despite a long history of systematic studies on Permian-Triassic foraminifera, there have been few investigations into spatial and temporal patterns of survivorship and evolution during this critical interval. We interrogate a high-resolution data set comprising newly obtained and previously published foraminiferal data (including 13,422 specimens in 173 species in 62 genera) from seven well-studied Permian-Triassic successions that record a transect of platform to basin facies in South China. Shallow-water settings seen at the Cili and Dajiang sections suffered a single-pulse, sudden extinction with high extinction rates at the end of the Palaeofusulina sinensis Zone; deeper-water and slope environments seen at Liangfengya and Meishan experienced a two-pulse extinction in the Clarkina yini and Isarcicella staeschei zones; basinal settings, seen at Shangsi, Gujiao and Sidazhai, record a single, less devastating extinction pulse in and slightly above the C. yini Zone. In the Late Permian, foraminiferal diversity was greatest on the shallow platforms, where 76.4% of species recorded in our study lived. The two pulses of the Permian-Triassic extinction prompted this foraminiferal diversity hotspot to move to deeper slope settings (comprising 75.6% of contemporary species) and finally basinal settings (comprising 88.8% of species). We propose that foraminifera migrated to deeper water to avoid overheating and toxicity in shallow waters that were driven by the emplacement of the Siberian Traps and coeval volcanic activities around the Paleotethys Ocean. This study provides a methodological framework for investigating survival mechanisms for foraminifers and other taxonomic groups during mass extinction events.

[1]  M. McIlvin,et al.  Denitrification likely catalyzed by endobionts in an allogromiid foraminifer , 2011, The ISME Journal.

[2]  Danielita gailloti n.gen., n. sp., within the Evolutionary Framework of Middle-Late Permian Dagmaritins , 2010 .

[3]  H. Pörtner,et al.  Oxygen- and capacity-limitation of thermal tolerance: a matrix for integrating climate-related stressor effects in marine ecosystems , 2010, Journal of Experimental Biology.

[4]  F. Jorissen,et al.  Widespread occurrence of nitrate storage and denitrification among Foraminifera and Gromiida , 2009, Proceedings of the National Academy of Sciences.

[5]  M. Mckinney Extinction Vulnerability and Selectivity: Combining Ecological and Paleontological Views , 1997 .

[6]  Feng Yang,et al.  Radiolarian evolution during the Permian and Triassic transition in South and Southwest China , 2000 .

[7]  D. Vachard,et al.  Timing and progression of the end-Guadalupian crisis in the Fars province (Dalan Formation, Kuh-e Gakhum, Iran) constrained by foraminifers and other carbonate microfossils , 2011, Facies.

[8]  Lars Peter Nielsen,et al.  Evidence for complete denitrification in a benthic foraminifer , 2006, Nature.

[9]  Isozaki,et al.  Permo-Triassic Boundary Superanoxia and Stratified Superocean: Records from Lost Deep Sea , 1997, Science.

[10]  Alfred R. Loeblich,et al.  Foraminiferal Genera and Their Classification , 1988 .

[11]  P. Wignall,et al.  Lethally Hot Temperatures During the Early Triassic Greenhouse , 2012, Science.

[12]  Songzhu Gu,et al.  Latest Permian deep-water foraminifers from Daxiakou, Hubei, South China , 2015, Journal of Paleontology.

[13]  D. Vachard Permian smaller foraminifers: taxonomy, biostratigraphy and biogeography , 2016, Special Publications.

[14]  M. Gaetani,et al.  The latest Permian mass extinction in the Alborz Mountains (North Iran) , 2010 .

[15]  J. Tong,et al.  Foraminiferal survivors from the Permian-Triassic mass extinction in the Meishan section, South China , 2007 .

[16]  F. Kobayashi LATE PERMIAN (LOPINGIAN) FORAMINIFERS FROM THE TSUKUMI LIMESTONE, SOUTHERN CHICHIBU TERRANE OF EASTERN KYUSHU, JAPAN , 2013 .

[17]  P. Wignall,et al.  Permian-Triassic conodonts from Dajiang (Guizhou, South China) and their implication for the age of microbialite deposition in the aftermath of the End-Permian mass extinction , 2014, Journal of Earth Science.

[18]  J. Tong,et al.  A Griesbachian (Early Triassic) Mollusc Fauna from the Sidazhai Section, Southwest China, with Paleoecological Insights on the Proliferation of Genus Claraia (Bivalvia) , 2018, Journal of Earth Science.

[19]  H. Pörtner,et al.  Oxyconformity in the intertidal worm Sipunculus nudus: the mitochondrial background and energetic consequences. , 2001, Comparative biochemistry and physiology. Part B, Biochemistry & molecular biology.

[20]  D. Vachard,et al.  Middle-Late Permian (Murgabian-Djulfian) foraminifers of the northern Maku area (western Azerbaijan, Iran) , 2015 .

[21]  Songzhu Gu,et al.  UPPERMOST CHANGXINGIAN (PERMIAN) RADIOLARIAN FAUNA FROM SOUTHERN GUIZHOU, SOUTHWESTERN CHINA , 2002, Journal of Paleontology.

[22]  S. Sommer,et al.  The role of benthic foraminifera in the benthic nitrogen cycle of the Peruvian oxygen minimum zone , 2012 .

[23]  Oren Levy,et al.  Symbiosis drove cellular evolution , 2010, Symbiosis.

[24]  J. Tong,et al.  Ecological evolution across the Permian/Triassic boundary at the Kangjiaping Section in Cili County, Hunan Province, China , 2009 .

[25]  P. Wignall,et al.  Restudy of conodont zonation and evolution across the P/T boundary at Meishan section, Changxing, Zhejiang, China , 2007 .

[26]  J. Tyszka,et al.  The Late Cretaceous–Early Paleocene palaeobathymetric trends in the southwestern Barents Sea — Palaeoenvironmental implications of benthic foraminiferal assemblage analysis , 2011 .

[27]  S. Stanley,et al.  A Double Mass Extinction at the End of the Paleozoic Era , 1994, Science.

[28]  A. Paytan,et al.  Calcium isotope constraints on the end-Permian mass extinction , 2010, Proceedings of the National Academy of Sciences.

[29]  M. Novacek The biodiversity crisis : losing what counts , 2001 .

[30]  Jing Chen,et al.  Rapid biotic rebound during the late Griesbachian indicates heterogeneous recovery patterns after the Permian-Triassic mass extinction , 2018, GSA Bulletin.

[31]  Feng Qinglai,et al.  The last Permian deep-water fauna: Latest Changhsingian small foraminifers from southwestern Guangxi, South China , 2007 .

[32]  Yi‐chun Zhang,et al.  MIDDLE PERMIAN NON-FUSULINE FORAMINIFERS FROM THE MIDDLE PART OF THE XIALA FORMATION IN XAINZA COUNTY, LHASA BLOCK, TIBET , 2016 .

[33]  A. Knoll,et al.  Comparative Earth History and Late Permian Mass Extinction , 1996, Science.

[34]  Haijun Song,et al.  End-Permian mass extinction of calcareous algae and microproblematica from Liangfengya, South China , 2018, Geobios.

[35]  Kliti Grice,et al.  Photic Zone Euxinia During the Permian-Triassic Superanoxic Event , 2005, Science.

[36]  R. Boyd,et al.  Influence of sediment transport dynamics and ocean floor morphology on benthic foraminifera, offshore Fraser Island, Australia , 2008 .

[37]  A. R. Loeblich,et al.  Foraminiferal evolution, diversification, and extinction , 1988 .

[38]  S. Bowring,et al.  Initial pulse of Siberian Traps sills as the trigger of the end-Permian mass extinction , 2017, Nature Communications.

[39]  D. Lehrmann,et al.  Permian–Triassic Boundary Sections from Shallow-Marine Carbonate Platforms of the Nanpanjiang Basin, South China: Implications for Oceanic Conditions Associated with the End-Permian Extinction and Its Aftermath , 2003 .

[40]  D. Vachard,et al.  New latest Permian foraminifers from Laren (Guangxi Province, South China): Palaeobiogeographic implications , 2009 .

[41]  L. Kump,et al.  Enhanced nitrogen fixation in the immediate aftermath of the latest Permian marine mass extinction , 2011 .

[42]  R. Martindale,et al.  Facies selectivity of benthic invertebrates in a Permian/Triassic boundary microbialite succession: Implications for the “microbialite refuge” hypothesis , 2019, Geobiology.

[43]  D. Altıner,et al.  Late Permian Foraminiferal Biofacies Belts in Turkey: Palaeogeographic and Tectonic Implications , 2000, Geological Society, London, Special Publications.

[44]  P. Harries,et al.  The importance of crisis progenitors in recovery from mass extinction , 1996, Geological Society, London, Special Publications.

[45]  D. Osleger,et al.  Relation of eustasy to stacking patterns of meter-scale carbonate cycles, Late Cambrian, U.S.A. , 1991 .

[46]  T. Lenton,et al.  Ocean acidification and the Permo-Triassic mass extinction , 2015, Science.

[47]  P. Wignall,et al.  Pyrite framboid study of marine Permian-Triassic boundary sections: A complex anoxic event and its relationship to contemporaneous mass extinction , 2010 .

[48]  M. Rampino,et al.  Evidence for abrupt latest Permian mass extinction of foraminifera: Results of tests for the Signor-Lipps effect , 1998 .

[49]  P. Wignall,et al.  Depositional conditions and revised age of the Permo-Triassic microbialites at Gaohua section, Cili County (Hunan Province, South China) , 2016 .

[50]  J. Tong,et al.  Evolutionary dynamics of the Permian–Triassic foraminifer size: Evidence for Lilliput effect in the end-Permian mass extinction and its aftermath , 2011 .

[51]  S. Sommer,et al.  Metabolic preference of nitrate over oxygen as an electron acceptor in foraminifera from the Peruvian oxygen minimum zone , 2019, Proceedings of the National Academy of Sciences.

[52]  R. Saraswat,et al.  Response of benthic foraminifera Rosalina leei to different temperature and salinity, under laboratory culture experiment , 2008, Journal of the Marine Biological Association of the United Kingdom.

[53]  F. Kobayashi Middle and Late Permian Foraminifers from the Chichibu Belt, Takachiho Area, Kyushu, Japan: Implications For Faunal Events , 2012, Journal of Paleontology.

[54]  P. Collin,et al.  Ostracods (Crustacea) through the Permian-Triassic boundary in South China: the Meishan stratotype (Zhejiang Province) , 2010 .

[55]  P. Wignall,et al.  Ammonium ocean following the end-Permian mass extinction , 2019, Earth and Planetary Science Letters.

[56]  K. Kaiho,et al.  Survival strategies of brachiopod faunas from the end-Permian mass extinction , 2005 .

[57]  D. Altıner,et al.  ORIGIN AND EARLY EVOLUTIONARY RADIATION OF THE ORDER LAGENIDA (FORAMINIFERA) , 2003 .

[58]  J. Payne,et al.  δ13C evidence that high primary productivity delayed recovery from end-Permian mass extinction , 2011 .

[59]  V. Vuks Olenekian (Early Triassic) foraminifers of the Gorny Mangyshlak, Eastern Precaucasus and Western Caucasus , 2007 .

[60]  T. Kolar-Jurkovšek,et al.  Foraminifera from the Permian-Triassic transition in western Slovenia , 2011 .

[61]  B. Beauchamp,et al.  Isotopic signatures of mercury contamination in latest Permian oceans , 2017 .

[62]  P. Wignall,et al.  Palaeoenvironmental changes across the Permian/Triassic boundary at Shangsi (N. Sichuan, China) , 1995 .

[63]  P. Wignall,et al.  Revised conodont zonation and conodont evolution across the Permian–Triassic boundary at the Shangsi section, Guangyuan, Sichuan, South China , 2011 .

[64]  Xiaochi Jin,et al.  Paleogeographic implications of the Shanita-Hemigordius fauna (Permian foraminifer) in the reconstruction of Permian Tethys , 2004 .

[65]  A. Knoll,et al.  Large Perturbations of the Carbon Cycle During Recovery from the End-Permian Extinction , 2004, Science.

[66]  M. Forel The Permian–Triassic mass extinction: Ostracods (Crustacea) and microbialites , 2013 .

[67]  Page C. Quinton,et al.  Warming and increased aridity during the earliest Triassic in the Karoo Basin, South Africa , 2017 .

[68]  H. Youbin,et al.  Lithofacies palaeogeography of the Upper Permian Changxing Stage in the Middle and Upper Yangtze Region, China , 2013 .

[69]  R. Martindale,et al.  Persistent Environmental Stress Delayed the Recovery of Marine Communities in the Aftermath of the Latest Permian Mass Extinction , 2018 .

[70]  D. Erwin,et al.  Pattern of marine mass extinction near the Permian-Triassic boundary in South China. , 2000, Science.

[71]  J. B. Maynard,et al.  Changes in productivity and redox conditions in the Panthalassic Ocean during the latest Permian , 2010 .

[72]  Xiangning Yang,et al.  Extinction process and patterns of Middle Permian Fusulinaceans in southwest China , 2004 .

[73]  Haijun Song,et al.  Mass extinction and Pangea integration during the Paleozoic-Mesozoic transition , 2013, Science China Earth Sciences.

[74]  S. Shen,et al.  Climate warming in the latest Permian and the Permian-Triassic mass extinction , 2012 .

[75]  D. Lehrmann Early Triassic calcimicrobial mounds and biostromes of the Nanpanjiang Basin , 1999 .

[76]  F. Kobayashi Upper Permian foraminifers from the Iwai-Kanyo area, West Tokyo, Japan , 1997 .

[77]  J. Payne,et al.  END-PERMIAN MASS EXTINCTION OF LAGENIDE FORAMINIFERS IN THE SOUTHERN ALPS (NORTHERN ITALY) , 2007, Journal of Paleontology.

[78]  J. Chen,et al.  Recovery tempo and pattern of marine ecosystems after the end-Permian mass extinction , 2011 .

[79]  N. Planavsky,et al.  Two pulses of oceanic environmental disturbance during the Permian–Triassic boundary crisis , 2016 .

[80]  C. Shields,et al.  Transition into a Hothouse World at the Permian–Triassic boundary—A model study , 2015 .

[81]  A. Racey,et al.  Ecology of extant nummulitids and other larger benthic foraminifera: applications in palaeoenvironmental analysis , 2004 .

[82]  Haishui Jiang,et al.  High-resolution variation in ostracod assemblages from microbialites near the Permian-Triassic boundary at Zuodeng, Guangxi region, South China , 2019 .

[83]  G. Shi,et al.  Evolution of the Permian and Triassic foraminifera in South China , 2000 .

[84]  M. Waldrop After the Fall: Although the dust was bad, the chemical fallout from the Cretaceous-Tertiary impact was worse--much worse. , 1988, Science.

[85]  R. Saraswat,et al.  Difference in optimum temperature for growth and reproduction in benthic foraminifer Rosalina globularis: Implications for paleoclimatic studies , 2011 .

[86]  Dong-xun Yuan,et al.  Artinskian (Early Permian) fusuline fauna from the Rongma area in northern Tibet: palaeoclimatic and palaeobiogeographic implications , 2013 .

[87]  G. R. Mcghee,et al.  A new ecological-severity ranking of major Phanerozoic biodiversity crises , 2013 .

[88]  A. Virgone,et al.  Upper Dalan Member and Kangan Formation between the Zagros Mountains and offshore Fars, Iran: depositional system, biostratigraphy and stratigraphic architecture , 2006, GeoArabia.

[89]  A. Kaim,et al.  Olenekian (Early Triassic) fossil assemblage from eastern Julian Alps (Slovenia) , 2018 .

[90]  Dong-xun Yuan,et al.  Changhsingian conodont succession and the end-Permian mass extinction event at the Daijiagou section in Chongqing, Southwest China , 2015 .

[91]  C. Marshall,et al.  Sudden and Gradual Molluscan Extinctions in the Latest Cretaceous of Western European Tethys , 1996, Science.

[92]  Douglas H. Erwin,et al.  The Permo–Triassic extinction , 1994, Nature.

[93]  J. Guex,et al.  La limite Permien-Trias dans quelques localités du Moyen-Orient: Recherches stratigraphiques et micropaléontologique , 1980 .

[94]  K. Krainer,et al.  Transported foraminifera in Palaeozoic deep red nodular limestones exemplified by latest Permian "Neoendothyra" in the Zal section (Julfa area, NW Iran) , 2009 .

[95]  L. Hinnov,et al.  Time-calibrated Milankovitch cycles for the late Permian , 2013, Nature Communications.

[96]  Yanan Shen,et al.  Multiple S-isotopic evidence for episodic shoaling of anoxic water during Late Permian mass extinction , 2011, Nature communications.

[97]  Curtis Deutsch,et al.  Climate change tightens a metabolic constraint on marine habitats , 2015, Science.

[98]  Robert K. Colwell,et al.  INTERPOLATING, EXTRAPOLATING, AND COMPARING INCIDENCE-BASED SPECIES ACCUMULATION CURVES , 2004 .

[99]  K. Grice,et al.  Microbial-algal community changes during the latest Permian ecological crisis: Evidence from lipid biomarkers at Cili, South China , 2013 .

[100]  D. Vachard,et al.  Palaeozoic Foraminifera: Systematics, palaeoecology and responses to global changes , 2010 .

[101]  G. F. Forsey Fossil evidence for the escalation and origin of marine mutualisms , 2013 .

[102]  P. Wignall,et al.  Early Triassic disaster and opportunistic foraminifers in South China , 2015, Geological Magazine.

[103]  N. Planavsky,et al.  Evidence for a prolonged Permian–Triassic extinction interval from global marine mercury records , 2019, Nature Communications.

[104]  K. Al-Ramadan,et al.  Foraminiferal biofacies and depositional environments of the Burdigalian mixed carbonate and siliciclastic Dam Formation, Al-Lidam area, Eastern Province of Saudi Arabia , 2017 .

[105]  F. Schuster,et al.  Symbiosis and the evolution of larger foraminifera , 1979 .

[106]  P. Wignall,et al.  Anoxia/high temperature double whammy during the Permian-Triassic marine crisis and its aftermath , 2014, Scientific Reports.

[107]  Wencheng Xia,et al.  The end-Permian regression in South China and its implication on mass extinction , 2014 .

[108]  C. Hemleben,et al.  Paleoecology, biostratigraphy, paleoceanography and taxonomy of agglutinated foraminifera , 1990 .

[109]  R. Twitchett,et al.  Oceanic Anoxia and the End Permian Mass Extinction , 1996, Science.

[110]  Wang Yigang,et al.  Permian-Triassic boundary in middle and eastern Tethys , 1984 .

[111]  Lei Shi,et al.  Complete biotic and sedimentary records of the Permian–Triassic transition from Meishan section, South China: Ecologically assessing mass extinction and its aftermath , 2015 .

[112]  Haijun Song,et al.  A new Griesbachian–Dienerian (Induan, Early Triassic) ammonoid fauna from Gujiao, South China , 2018, Journal of Paleontology.

[113]  C. Deutsch,et al.  Temperature-dependent hypoxia explains biogeography and severity of end-Permian marine mass extinction , 2018, Science.

[114]  A. Knoll,et al.  Paleophysiology and End-Permian Mass Extinction , 2007 .

[115]  Rainer Knust,et al.  Climate Change Affects Marine Fishes Through the Oxygen Limitation of Thermal Tolerance , 2007, Science.

[116]  M. Benton Hyperthermal-driven mass extinctions: killing models during the Permian–Triassic mass extinction , 2018, Philosophical Transactions of the Royal Society A: Mathematical, Physical and Engineering Sciences.

[117]  S. Gallagher Controls on the distribution of calcareous Foraminifera in the Lower Carboniferous of Ireland , 1998 .

[118]  M. Brasier Fossil indicators of nutrient levels. 2: Evolution and extinction in relation to oligotrophy , 1995, Geological Society, London, Special Publications.

[119]  Karen M. Layou,et al.  Phanerozoic Trends in the Global Diversity of Marine Invertebrates , 2008, Science.

[120]  Richard Cowen,et al.  Algal Symbiosis and Its Recognition in the Fossil Record , 1983 .

[121]  P. Wignall,et al.  Facies change and the end-Permian mass extinction in S.E. Sichuan, China , 1996 .

[122]  E. Alve Benthic foraminifera in sediment cores reflecting heavy metal pollution in Sorfjord, western Norway , 1991 .

[123]  Jing Chen,et al.  Recovery dynamics of foraminifers and algae following the Permian-Triassic extinction in Qingyan, South China , 2015 .

[124]  Robert K. Colwell,et al.  Models and estimators linking individual-based and sample-based rarefaction, extrapolation and comparison of assemblages , 2012 .

[125]  W. Yue,et al.  Foraminiferal diversification during the late Paleozoic ice age , 2009, Paleobiology.

[126]  Hua Zhang,et al.  Integrative timescale for the Lopingian (Late Permian): A review and update from Shangsi, South China , 2019, Earth-Science Reviews.

[127]  P. Wignall,et al.  Geochemical evidence from bio-apatite for multiple oceanic anoxic events during Permian-Triassic transition and the link with end-Permian extinction and recovery , 2012 .

[128]  K. Meldahl Sampling, species abundance, and the stratigraphic signature, of mass extinction: A test using Holocene tidal flat molluscs , 1990 .

[129]  D. Lehrmann,et al.  ENVIRONMENTAL CONTROLS ON THE GENESIS OF MARINE MICROBIALITES AND DISSOLUTION SURFACE ASSOCIATED WITH THE END-PERMIAN MASS EXTINCTION: NEW SECTIONS AND OBSERVATIONS FROM THE NANPANJIANG BASIN, SOUTH CHINA , 2015 .

[130]  D. Altıner,et al.  MORPHOLOGICAL VARIATION IN HEMIGORDIUS HARLTONI CUSHMAN A WATERS, 1928: REMARKS ON THE TAXONOMY OF CARBONIFEROUSAND PERMIAN HEMIGORDIOPSIDS , 2003 .

[131]  P. Collin,et al.  Facies changes and diagenetic processes across the Permian–Triassic boundary event horizon, Great Bank of Guizhou, South China: a controversy of erosion and dissolution , 2009 .

[132]  D. Lehrmann,et al.  Controls on Facies Architecture of a Large Triassic Carbonate Platform: the Great Bank of Guizhou, Nanpanjiang Basin, South China , 1998 .

[133]  D. Robertson,et al.  Survival in the first hours of the Cenozoic , 2004 .

[134]  D. J. Strauss,et al.  Classical confidence intervals and Bayesian probability estimates for ends of local taxon ranges , 1989 .

[135]  P. Rosenstiel,et al.  A novel eukaryotic denitrification pathway in foraminifera , 2018, Current Biology.

[136]  K. Kaiho,et al.  Onset of biotic and environmental recovery from the end-Permian mass extinction within 1–2 million years: A case study of the Lower Triassic of the Meishan section, South China , 2007 .

[137]  M. Nestell,et al.  Late Changhsingian foraminifers of the northwestern Caucasus , 2001 .

[138]  Yi‐chun Zhang,et al.  The Changhsingian foraminiferal fauna of a Neotethyan seamount: the Gyanyima Limestone along the Yarlung‐Zangbo Suture in southern Tibet, China , 2010 .

[139]  Zhong-Qiang Chen,et al.  Two episodes of foraminiferal extinction near the Permian–Triassic boundary at the Meishan section, South China , 2009 .

[140]  D. Erwin The End-Permian Mass Extinction , 1990 .

[141]  D. Erwin,et al.  A sudden end-Permian mass extinction in South China , 2018, GSA Bulletin.

[142]  J. Chen,et al.  Composition and structure of microbialite ecosystems following the end-Permian mass extinction in South China , 2011 .

[143]  H. Sanei,et al.  Latest Permian mercury anomalies , 2012 .

[144]  Shaun T. Brown,et al.  Evidence for end-Permian ocean acidification from calcium isotopes in biogenic apatite , 2012 .

[145]  Charles R. Marshall,et al.  Confidence intervals on stratigraphic ranges , 1990, Paleobiology.

[146]  J. Sepkoski,et al.  A factor analytic description of the Phanerozoic marine fossil record , 1981, Paleobiology.

[147]  Steve C. Wang,et al.  Confidence intervals for pulsed mass extinction events , 2007, Paleobiology.

[148]  John W. Murray,et al.  Ecology and applications of benthic foraminifera , 2006 .

[149]  D. Vachard,et al.  Kubergandian (Roadian, Middle Permian) of the Lycian and Aladağ Nappes (Southern Turkey)☆ , 2013 .

[150]  D. Lehrmann,et al.  Early and Middle Triassic trends in diversity, evenness, and size of foraminifers on a carbonate platform in south China: implications for tempo and mode of biotic recovery from the end-Permian mass extinction , 2011, Paleobiology.

[151]  W. Parker,et al.  Quantitative methods of data analysis in foraminiferal ecology , 1999 .

[152]  G. Luo,et al.  Contrasting microbial community changes during mass extinctions at the Middle/Late Permian and Permian/Triassic boundaries , 2017 .

[153]  P. Wignall,et al.  Two pulses of extinction during the Permian–Triassic crisis , 2012, Nature Geoscience.

[154]  F. Kobayashi,et al.  PALEOBIOGEOGRAPHIC ANALYSIS OF YAHTASHIAN TO MIDIAN FUSULINACEAN FAUNAS OF THE SURMAQ FORMATION IN THE ABADEH REGION, CENTRAL IRAN , 2003 .

[155]  Zheng Quan-feng,et al.  Geological event sequences of the Permian-Triassic transition recorded in the microfacies in Meishan section , 2009 .

[156]  C. Teichert,et al.  Mixed Permian-Triassic Fauna, Guryul Ravine, Kashmir , 1970, Science.

[157]  C. Henderson,et al.  Precarious ephemeral refugia during the earliest Triassic , 2017 .

[158]  D. Altıner,et al.  Survival and recovery of calcareous foraminifera pursuant to the end-Permian mass extinction , 2005 .

[159]  Charles R. Marshall,et al.  Improved confidence intervals for estimating the position of a mass extinction boundary , 2004, Paleobiology.

[160]  David M. Raup,et al.  Taxonomic diversity estimation using rarefaction , 1975, Paleobiology.

[161]  M. Clapham,et al.  Acidification, anoxia, and extinction: A multiple logistic regression analysis of extinction selectivity during the Middle and Late Permian , 2011 .

[162]  B. Halpern,et al.  Ocean community warming responses explained by thermal affinities and temperature gradients , 2019, Nature Climate Change.

[163]  Yin Hongfu,et al.  The Global Stratotype Section and Point (GSSP) of the Permian-Triassic boundary , 2001 .

[164]  D. Altıner,et al.  EXTINCTION, SURVIVAL, AND RECOVERY OF LAGENIDE FORAMINIFERS IN THE PERMIAN–TRIASSIC BOUNDARY INTERVAL, CENTRAL TAURIDES, TURKEY , 2005, Journal of Paleontology.

[165]  Weihong He,et al.  CHANGXINGIAN (UPPER PERMIAN) RADIOLARIAN FAUNA FROM MEISHAN D SECTION, CHANGXING, ZHEJIANG, CHINA, AND ITS POSSIBLE PALEOECOLOGICAL SIGNIFICANCE , 2005, Journal of Paleontology.

[166]  Yue Wang,et al.  A NEW FUSULINOIDEAN GENUS DILATOFUSULINA FROM THE LOPINGIAN (UPPER PERMIAN) OF SOUTHERN TIBET, CHINA , 2009 .

[167]  M. Forel Ostracods (Crustacea) associated with microbialites across the Permian-Triassic boundary in Dajiang (Guizhou Province, South China) , 2012 .

[168]  John J. Lee,et al.  Algal Symbiosis as the Driving Force in the Evolution of Larger Foraminifera a , 1987 .

[169]  P. Wignall,et al.  Decoupled taxonomic and ecological recoveries from the Permo-Triassic extinction , 2018, Science Advances.

[170]  P. Wignall,et al.  Latitudinal selectivity of foraminifer extinctions during the late Guadalupian crisis , 2009, Paleobiology.

[171]  Haijun Song,et al.  A Changhsingian (late Permian) nautiloid assemblage from Gujiao, South China , 2019, Papers in Palaeontology.

[172]  D. Vachard,et al.  The Khuff Formation (Middle East) and time-equivalents in Turkey and South China: biostratigraphy from Capitanian to Changhsingian times (Permian), new foraminiferal taxa, and palaeogeographical implications , 2008 .

[173]  H. Sanei,et al.  Catastrophic dispersion of coal fly ash into oceans during the latest Permian extinction , 2011 .

[174]  S. Grasby,et al.  Ecological disturbance in tropical peatlands prior to marine Permian-Triassic mass extinction , 2020, Geology.

[175]  Michael T. Black,et al.  Synchrony and Causal Relations Between Permian-Triassic Boundary Crises and Siberian Flood Volcanism , 1995, Science.

[176]  K. Kaiho Benthic foraminiferal dissolved-oxygen index and dissolved-oxygen levels in the modern ocean , 1994 .

[177]  D. Vachard,et al.  Late Permian foraminiferal assemblages from the Hambast region (central Iran) and their extinctions , 2005 .

[178]  Yue Wang,et al.  Permian fusuline biostratigraphy , 2017, Special Publications.

[179]  J. Tong,et al.  End-Permian Mass Extinction of Foraminifers in the Nanpanjiang Basin, South China , 2009, Journal of Paleontology.