Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

The timing and pattern of biotic recovery following the end-Permian mass extinction

Abstract

The aftermath of the great end-Permian period mass extinction 252 Myr ago shows how life can recover from the loss of >90% species globally. The crisis was triggered by a number of physical environmental shocks (global warming, acid rain, ocean acidification and ocean anoxia), and some of these were repeated over the next 5–6 Myr. Ammonoids and some other groups diversified rapidly, within 1–3 Myr, but extinctions continued through the Early Triassic period. Triassic ecosystems were rebuilt stepwise from low to high trophic levels through the Early to Middle Triassic, and a stable, complex ecosystem did not re-emerge until the beginning of the Middle Triassic, 8–9 Myr after the crisis. A positive aspect of the recovery was the emergence of entirely new groups, such as marine reptiles and decapod crustaceans, as well as new tetrapods on land, including — eventually — dinosaurs. The stepwise recovery of life in the Triassic could have been delayed either by biotic drivers (complex multispecies interactions) or physical perturbations, or a combination of both. This is an example of the wider debate about the relative roles of intrinsic and extrinsic drivers of large-scale evolution.

This is a preview of subscription content, access via your institution

Access options

Rent or buy this article

Prices vary by article type

from$1.95

to$39.95

Prices may be subject to local taxes which are calculated during checkout

Figure 1: Environmental changes and biodiversity variations from the latest Permian to Middle Triassic.
Figure 2: Outline trophic pyramid of a fossilized marine ecosystem in the Permian or Triassic.
Figure 3: Reconstructed marine ecosystems before and after the end-Permian mass extinction in south China.
Figure 4: Stepwise rebuilding pattern of marine ecosystems from low to top trophic levels in the aftermath of the EPME.

References

  1. Sepkoski, J. J., Jr A kinetic model of Phanerozoic taxonomic diversity, III: Post-Paleozoic families and mass extinctions. Paleobiology 10, 246–267 (1984).

    Google Scholar 

  2. Benton, M. J. Diversification and extinction in the history of life. Science 268, 52–58 (1995).

    Google Scholar 

  3. Alroy, J. et al. Phanerozoic trends in the global diversity of marine invertebrates. Science 321, 97–100 (2008).

    Google Scholar 

  4. Van Valen, L. A resetting of Phanerozoic community evolution. Nature 307, 50–52 (1984).

    Google Scholar 

  5. Bowring, S. A. et al. U/Pb zircon geochronology and tempo of the end-Permian mass extinction. Science 280, 1039–1045 (1998).

    Google Scholar 

  6. Benton, M. J. The origins of modern biodiversity on land. Phil. Trans. R. Soc. B 365, 3667–3679 (2010).

    Google Scholar 

  7. Knoll, A. H., Bambach, R. K., Payne, J. L., Pruss, S. & Fischer, W. W. Paleophysiology and the end-Permian mass extinction. Earth Planet. Sci. Lett. 256, 295–313 (2007).

    Google Scholar 

  8. Erwin, D. H. Lessons from the past: biotic recoveries from mass extinctions. Proc. Natl Acad. Sci. USA 98, 5399–5403 (2001).

    Google Scholar 

  9. Erwin, D. H. Disparity: morphological pattern and developmental context. Palaeontology 50, 57–73 (2007).

    Google Scholar 

  10. Benton, M. J. & Twitchett, R. J. How to kill (almost) all life: the end-Permian extinction event. Trends Ecol. Evol. 18, 358–365 (2003).

    Google Scholar 

  11. Benton, M. J., Tverdokhlebov, V. P. & Surkov, M. V. Ecosystem remodelling among vertebrates at the Permian-Triassic boundary in Russia. Nature 432, 97–100 (2004).

    Google Scholar 

  12. Brayard, A. et al. Good genes and good luck: Ammonoid diversity and the end-Permian mass extinction. Science 325, 1118–1121 (2009).

    Google Scholar 

  13. Stanley, S. M. Relation of Phanerozoic stable isotope excursions to climate, bacterial metabolism, and major extinctions. Proc. Natl Acad. Sci. USA 107, 19185–19189 (2010).

    Google Scholar 

  14. Song, H. J. et al. Recovery tempo and pattern of marine ecosystems after the end-Permian mass extinction. Geology 39, 739–742 (2011).

    Google Scholar 

  15. Hallam, A. Why was there a delayed radiation after the end-Palaeozoic extinctions? Historical Biology 5, 257–262 (1991).

    Google Scholar 

  16. Sahney, S. & Benton, M. J. Recovery from the most profound mass extinction of all time. Proc. R. Soc. B-Biol. Sci. 275, 759–765 (2008).

    Google Scholar 

  17. Chen, Z. Q., Tong, J., Liao, Z. T. & Song, H. Structural changes of marine communities over the Permian-Triassic transition: Ecologically assessing the end-Permian mass extinction and its aftermath. Global Planet. Change 73, 123–140 (2010).

    Google Scholar 

  18. Erwin, D. H. A preliminary classification of evolutionary radiations. Historical Biology 6, 133–147 (1992).

    Google Scholar 

  19. Payne, J. L. et al. Large perturbations of the carbon cycle during recovery from the end-Permian extinction. Science 305, 506–509 (2004).

    Google Scholar 

  20. Payne, J. L. 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. Paleobiology 37, 409–425 (2011).

    Google Scholar 

  21. Irmis, R. B. & Whiteside, J. H. Delayed recovery of non-marine tetrapods after the end-Permian mass extinction tracks global carbon cycle. Proc. R. Soc. B-Biol. Sci. http://dx.doi.org/10.1098/rspb.2011.1895 (2011).

  22. Stanley, S. M. An analysis of the history of marine animal diversity. Paleobiology 33, 1–55 (2007).

    Google Scholar 

  23. Solé, R. V., Saldana, J., Montoya, J. M. & Erwin, D. H. Simple model of recovery dynamics after mass extinction. J. Theor. Biol. 267, 193–200 (2010).

    Google Scholar 

  24. Raup, D. M. Biases in the fossil record of species and genera. Bull. Carnegie Museum Nat. Hist. 13, 85–91 (1979).

    Google Scholar 

  25. Knoll, A., Bambach, R., Canfield, D. & Grotzinger, J. Comparative earth history and Late Permian mass extinction. Science 273, 452–457 (1996).

    Google Scholar 

  26. McGhee, G. R., Sheehan, P. M., Bottjer, D. J. & Droser, M. L. Ecological ranking of Phanerozoic biodiversity crises: ecological and taxonomic severities are decoupled. Palaeogeogr. Palaeoclimatol. Palaeoecol. 211, 289–297 (2004).

    Google Scholar 

  27. Butchart, S. H. M. et al. National indicators show biodiversity progress response. Science 329, 900–901 (2010).

    Google Scholar 

  28. Barnosky, A. et al. Has the Earth's sixth mass extinction already arrived? Nature 471, 51–57 (2011).

    Google Scholar 

  29. McKinney, M. Extinction selectivity among lower taxa - gradational patterns and rarefaction error in extinction estimates. Paleobiology 21, 300–313 (1995).

    Google Scholar 

  30. Jablonski, D., Erwin, D. H. & Lipps, J. H. Evolutionary Paleobiology (Chicago Univ. Press, 1996).

    Google Scholar 

  31. Jin, Y., Wang, Y., Wang, W., Shang, Q. & Erwin, D. Pattern of marine mass extinction near the Permian-Triassic boundary in South China. Science 289, 432–436 (2000).

    Google Scholar 

  32. Xie, S. C., Pancost, R. D., Yin, H. F., Wang, H. M. & Evershed, R. P. Two episodes of microbial change coupled with Permo/Triassic faunal mass extinction. Nature 434, 494–497 (2005).

    Google Scholar 

  33. Yin, H. F. et al. The prelude of the end-Permian mass extinction predates a postulated bolide impact. Int. J. Earth Sci. 96, 903–909 (2007).

    Google Scholar 

  34. Chen, Z. Q. et al. Environmental and biotic turnover across the Permian-Triassic boundary on a shallow carbonate platform in western Zhejiang, South China. Aust. J. Earth Sci. 56, 775–797 (2009).

    Google Scholar 

  35. Shen, S.-Z. et al. Calibrating the end-Permian mass extinction. Science 334, 1367–1372 (2011).

    Google Scholar 

  36. Payne, J. L. & Kump, L. Evidence for recurrent Early Triassic massive volcanism from quantitative interpretation of carbon isotope fluctuations. Earth Planet. Sci. Lett. 256, 264–277 (2007).

    Google Scholar 

  37. Wignall, P. B. Large igneous provinces and mass extinctions. Earth Sci. Rev. 53, 1–33 (2001).

    Google Scholar 

  38. Benton, M. J. When Life Nearly Died: The Greatest Mass Extinction of All Time (Thames & Hudson, 2003).

    Google Scholar 

  39. Newell, A. J., Tverdokhlebov, V. P. & Benton, M. J. Interplay of tectonics and climate on a transverse fluvial system, Upper Permian, Southern Uralian Foreland Basin, Russia. Sedim. Geol. 127, 11–29 (1999).

    Google Scholar 

  40. Ward, P. D., Montgomery, D. R. & Smith, R. M. H. Altered river morphology in South Africa related to the Permian-Triassic extinction. Science 289, 1741–1743 (2000).

    Google Scholar 

  41. Retallack, G. J. Postapocalyptic greenhouse paleoclimate revealed by earliest Triassic paleosols in the Sydney Basin, Australia. Geol. Soc. Am. Bull. 111, 52–70 (1999).

    Google Scholar 

  42. Algeo, T. J. & Twitchett, R. Anomalous Early Triassic sediment fluxes due to elevated weathering rates and their biological consequences. Geology 38, 1023–1026 (2010).

    Google Scholar 

  43. Algeo, T. J., Chen, Z. Q., Fraiser, M. L. & Twitchett, R. J. Terrestrial-marine teleconnections in the collapse and rebuilding of Early Triassic marine ecosystems. Palaeogeogr. Palaeoclimatol. Palaeoecol. 308, 1–11 (2011).

    Google Scholar 

  44. Wang, C. & Visscher, H. Abundance anomalies of aromatic biomarkers in the Permian-Triassic boundary section at Meishan, China - Evidence of end-Permian terrestrial ecosystem collapse. Palaeogeogr. Palaeoclimatol. Palaeoecol. 252, 291–303 (2007).

    Google Scholar 

  45. Wignall, P. B. & Twitchett, R. J. Oceanic anoxia and the end Permian mass extinction. Science 272, 1155–1158 (1996).

    Google Scholar 

  46. Yin, H. F., Zhang, K., Tong, J., Yang, Z. Y. & Wu, S. The Global Stratotype Section and Point (GSSP) of the Permian-Triassic boundary. Episodes 24, 102–114 (2001).

    Google Scholar 

  47. Taylor, G. K. et al. Magnetostratigraphy of Permian/Triassic boundary sequences in the Cis-Urals, Russia: No evidence for a major temporal hiatus. Earth Planet. Sci. Lett. 281, 36–47 (2009).

    Google Scholar 

  48. Mundil, R., Pálfy, J., Renne, P. & Brack, P. in The Triassic Timescale Geological Society Special Publication No. 334 (ed Lucas, S. G.) 41–60 (Geological Society of London, 2010).

    Google Scholar 

  49. Huang, C., Tong, J., Hinnov, L. & Chen, Z. Did the great dying of life take 700 k.y.? Evidence from global astronomical correlation of the Permian-Triassic boundary interval. Geology 39, 779–782 (2011).

    Google Scholar 

  50. Retallack, G. J., Veevers, J. & Morante, R. Global coal gap between Permian-Triassic extinction and Middle Triassic recovery of peat-forming plants. Geol. Soc. Am. Bull. 108, 195–207 (1996).

    Google Scholar 

  51. Retallack, G. J. et al. Multiple Early Triassic greenhouse crises impeded recovery from Late Permian mass extinction. Palaeogeogr. Palaeoclimatol. Palaeoecol. 308, 233–251 (2011).

    Google Scholar 

  52. Rees, P. Land-plant diversity and the end-Permian mass extinction. Geology 30, 827–830 (2002).

    Google Scholar 

  53. Riccardi, A., Arthur, M. A. & Kump, L. R. Sulfur isotopic evidence for chemocline upward excursions during the end-Permian mass extinction. Geochim. Cosmochim. Acta 70, 5740–5752 (2006).

    Google Scholar 

  54. Kump, L. R., Pavlov, A. & Arthur, M. A. Massive release of hydrogen sulfide to the surface ocean and atmosphere during intervals of oceanic anoxia. Geology 33, 397–400 (2005).

    Google Scholar 

  55. Algeo, T. J., Lehrmann, D., Orchard, M. & Tong, J. The Permian-Triassic boundary crisis and Early Triassic biotic recovery. Palaeogeogr. Palaeoclimatol. Palaeoecol. 252, 1–3 (2007).

    Google Scholar 

  56. Orchard, M. Conodont diversity and evolution through the latest Permian and Early Triassic upheavals. Palaeogeogr. Palaeoclimatol. Palaeoecol. 252, 93–117 (2007).

    Google Scholar 

  57. Stanley, S. M. Evidence from ammonoids and conodonts for multiple Early Triassic mass extinctions. Proc. Natl Acad. Sci. USA 106, 15264–15267 (2009).

    Google Scholar 

  58. Twitchett, R. J., Krystyn, L., Baud, A., Wheeley, J. & Richoz, S. Rapid marine recovery after the end-Permian mass-extinction event in the absence of marine anoxia. Geology 32, 805–808 (2004).

    Google Scholar 

  59. Beatty, T., Zonneveld, J. & Henderson, C. Anomalously diverse Early Triassic ichnofossil assemblages in Northwest Pangea: A case for a shallow-marine habitable zone. Geology 36, 771–774 (2008).

    Google Scholar 

  60. Hofmann, R., Goudemand, N., Wasmer, M., Bucher, H. & Hautmann, M. New trace fossil evidence for an early recovery signal in the aftermath of the end-Permian mass extinction. Palaeogeogr. Palaeoclimatol. Palaeoecol. 310, 216–226 (2011).

    Google Scholar 

  61. Brayard, A. et al. Gastropod evidence against the Early Triassic Lilliput effect. Geology 38, 147–150 (2010).

    Google Scholar 

  62. Galfetti, T. et al. Smithian–Spathian boundary event: Evidence for global climatic change in the wake of the end-Permian biotic crisis. Geology 35, 291–294 (2007).

    Google Scholar 

  63. Hermann, E. et al. Organic matter and palaeoenvironmental signals during the Early Triassic biotic recovery: The Salt Range and Surghar Range records. Sedim. Geol. 234, 19–41 (2011).

    Google Scholar 

  64. Grauvogel-Stamm, L. & Ash, S. Recovery of the Triassic land flora from the end-Permian life crisis. C.R. Palevol 4, 593–608 (2005).

    Google Scholar 

  65. Brusatte, S. L. et al. The origin and early radiation of dinosaurs. Earth Sci. Rev. 101, 68–100 (2010).

    Google Scholar 

  66. Nesbitt, S. J. et al. Ecologically distinct dinosaurian sister group shows early diversification of Ornithodira. Nature 464, 95–98 (2010).

    Google Scholar 

  67. Twitchett, R. J. Palaeoenvironments and faunal recovery after the end-Permian mass extinction. Palaeogeogr. Palaeoclimatol. Palaeoecol. 154, 27–37 (1999).

    Google Scholar 

  68. Pruss, S. B. & Bottjer, D. J. Early Triassic trace fossils of the western United States and their implications for prolonged environmental stress from the end-Permian mass extinction. Palaios 19, 551–564 (2004).

    Google Scholar 

  69. Zonneveld, J. P., Gingras, M. K. & Beatty, T. W. Diverse ichnofossil assemblages following the P-T mass extinction, Lower Triassic, Alberta and British Columbia, Canada: evidence for shallow marine refugia on the northwestern coast of Pangaea. Palaios 25, 368–392 (2010).

    Google Scholar 

  70. Knaust, D. The end-Permian mass extinction and its aftermath on an equatorial carbonate platform: insights from ichnology. Terra Nova 22, 195–202 (2010).

    Google Scholar 

  71. Twitchett, R. J. & Wignall, P. B. Trace fossils and the aftermath of the Permo-Triassic mass extinction: Evidence from northern Italy. Palaeogeogr. Palaeoclimatol. Palaeoecol. 124, 137–151 (1996).

    Google Scholar 

  72. Fraiser, M. L. & Bottjer, D. J. Opportunistic behaviour of invertebrate marine tracemakers during the Early Triassic aftermath of the end-Permian mass extinction. Aust. J. Earth Sci. 56, 841–857 (2009).

    Google Scholar 

  73. Chen, Z. Q., Tong, J. & Fraiser, M. Trace fossil evidence for restoration of marine ecosystems following the end-Permian mass extinction in the Lower Yangtze region, South China. Palaeogeogr. Palaeoclimatol. Palaeoecol. 299, 449–474 (2011).

    Google Scholar 

  74. Hautmann, M. et al. An unusually diverse mollusc fauna from the earliest Triassic of South China and its implications for benthic recovery after the end-Permian biotic crisis. Geobios 44, 71–85 (2007).

    Google Scholar 

  75. Hallam, A. & Wignall, P. B. Mass Extinctions and Their Aftermath (Oxford Univ. Press, 1997).

    Google Scholar 

  76. Fraiser, M. L. & Bottjer, D. J. Restructuring in benthic level-bottom shallow marine communities due to prolonged environmental stress following the end-Permian mass extinction. C.R. Palevol 4, 583–591 (2005).

    Google Scholar 

  77. Twitchett, R. J. The Lilliput effect in the aftermath of the end-Permian extinction event. Palaeogeogr. Palaeoclimatol. Palaeoecol. 252, 132–144 (2007).

    Google Scholar 

  78. Fraiser, M. L., Twitchett, R. J., Frederickson, J., Metcalfe, B. & Bottjer, D. Gastropod evidence against the Early Triassic Lilliput effect: comment. Geology 39, E232–E232 (2011).

    Google Scholar 

  79. Whiteside, J. H. & Ward, P. D. Ammonoid diversity and disparity track episodes of chaotic carbon cycling during the early Mesozoic. Geology 39, 99–102 (2011).

    Google Scholar 

  80. Brayard, A. et al. Transient metazoan reefs in the aftermath of the end-Permian mass extinction. Nature Geosci. 4, 693–697 (2011).

    Google Scholar 

  81. Botha, J. & Smith, R. M. H. Rapid vertebrate recuperation in the Karoo Basin of South Africa following the End-Permian extinction. J. Afr. Earth Sci. 45, 502–514 (2006).

    Google Scholar 

  82. Benton, M. J. Dinosaur success in the Triassic: a noncompetitive ecological model. Q. Rev. Biol. 58, 29–55 (1983).

    Google Scholar 

  83. Wignall, P. B. & Benton, M. J. Lazarus taxa and fossil abundance at times of biotic crisis. J. Geol. Soc. 156, 453–456 (1999).

    Google Scholar 

  84. Chen, Z. Q., Kaiho, K. & George, A. Survival strategies of brachiopod faunas from the end-Permian mass extinction. Palaeogeogr. Palaeoclimatol. Palaeoecol. 224, 232–269 (2005).

    Google Scholar 

  85. Chen, Z. Q., Kaiho, K. & George, A. Early Triassic recovery of the brachiopod faunas from the end-Permian mass extinction: A global review. Palaeogeogr. Palaeoclimatol. Palaeoecol. 224, 270–290 (2005).

    Google Scholar 

  86. Flügel, E. in Phanerozoic Reef Patterns Vol. 72 (eds Kiessling, W., Flügel, E. & Golonka, J.) 391–463 (SEPM Special Publication, 2002).

    Google Scholar 

  87. Vishnevskaya, V. & Kostyuchenko, A. The evolution of radiolarian biodiversity. Paleontol. J. 34, 124–130 (2000).

    Google Scholar 

  88. O'Dogherty, L., Carter, E., Goričan, Š. & Dumitrica, P. in The Triassic Timescale Geological Society Special Publications 334 (eds SG Lucas) 163–200 (Geological Society of London, 2010).

    Google Scholar 

  89. Twitchett, R. J., Feinberg, J., O'Connor, D., Alvarez, W. & McCollum, L. Early Triassic ophiuroids: Their paleoecology, taphonomy, and distribution. Palaios 20, 213–223 (2005).

    Google Scholar 

  90. Chen, Z. Q. & McNamara, K. End-Permian extinction and subsequent recovery of the Ophiuroidea (Echinodermata). Palaeogeogr. Palaeoclimatol. Palaeoecol. 236, 321–344 (2006).

    Google Scholar 

  91. McGowan, A. J. Ammonoid taxonomic and morphologic recovery patterns after the Permian-Triassic. Geology 32, 665–668 (2004).

    Google Scholar 

  92. Brusatte, S. L., Benton, M. J., Ruta, M. & Lloyd, G. T. Superiority, competition, and opportunism in the evolutionary radiation of dinosaurs. Science 321, 1485–1488 (2008).

    Google Scholar 

  93. Brusatte, S. L., Benton, M. J., Lloyd, G., Ruta, M. & Wang, S. J. Macroevolutionary patterns in the evolutionary radiation of archosaurs (Tetrapoda: Diapsida). Earth Env. Sci. Trans. R. Soc. 101, 367–382 (2011).

    Google Scholar 

  94. Ruta, M. & Benton, M. J. Calibrated diversity, tree topology and the mother of all mass extinctions: the lesson of the temnospondyls. Palaeontology 51, 1261–1288 (2008).

    Google Scholar 

  95. Solé, R. V., Montoya, J. M. & Erwin, D. H. Recovery after mass extinction: evolutionary assembly in large-scale biosphere dynamics. Phil. Trans. R. Soc. B-Biol. Sci. 357, 697–707 (2002).

    Google Scholar 

  96. Hu, S.-x. et al. The Luoping biota: exceptional preservation, and new evidence on the Triassic recovery from end-Permian mass extinction. Proc. R. Soc. B-Biol. Sci. 278, 2274–2282 (2011).

    Google Scholar 

  97. Meyer, K. M. et al. δ13C evidence that high primary productivity delayed recovery from end-Permian mass extinction. Earth Planet. Sci. Lett. 302, 378–384 (2011).

    Google Scholar 

  98. Benton, M. J. The Red Queen and the Court Jester: Species diversity and the role of biotic and abiotic factors through time. Science 323, 728–732 (2009).

    Google Scholar 

  99. Carr, T. R. & Kitchell, J. A. Dynamics of taxonomic diversity. Paleobiology 6, 427–443 (1980).

    Google Scholar 

  100. Gavrilets, S. & Losos, J. Adaptive radiation: contrasting theory with data. Science 323, 732–737 (2009).

    Google Scholar 

Download references

Acknowledgements

Thanks to John Sibbick for the spectacular artwork in Fig. 3, and to Ricard Solé for supplying information for the figure in Box 2. This work was funded by ARC Discovery Grant DP0770938 to Z.Q.C., NSFC grant 40830212 to J. Tong, the 111 program of China (grant No. B08030) to S. Xie, China Geological Survey Projects (No. 1212010610211, 1212011140051) and NERC grant NE/C518973/1 to M.J.B. This is a contribution to IGCP572.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Michael J. Benton.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Supplementary information

Supplementary information

Timing and pattern of biotic recovery following the end-Permian mass extinction (PDF 479 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Chen, ZQ., Benton, M. The timing and pattern of biotic recovery following the end-Permian mass extinction. Nature Geosci 5, 375–383 (2012). https://doi.org/10.1038/ngeo1475

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/ngeo1475

This article is cited by

Search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing