Abstract
The Late Permian mass extinction event about 252 million years ago was the most severe biotic crisis of the past 500 million years and occurred during an episode of global warming. The loss of around two-thirds of marine genera is thought to have had substantial ecological effects, but the overall impacts on the functioning of marine ecosystems and the pattern of marine recovery are uncertain. Here we analyse the fossil occurrences of all known benthic marine invertebrate genera from the Permian and Triassic periods, and assign each to a functional group based on their inferred lifestyle. We show that despite the selective extinction of 62–74% of these genera, all but one functional group persisted through the crisis, indicating that there was no significant loss of functional diversity at the global scale. In addition, only one new mode of life originated in the extinction aftermath. We suggest that Early Triassic marine ecosystems were not as ecologically depauperate as widely assumed. Functional diversity was, however, reduced in particular regions and habitats, such as tropical reefs; at these smaller scales, recovery varied spatially and temporally, probably driven by migration of surviving groups. We find that marine ecosystems did not return to their pre-extinction state, and by the Middle Triassic greater functional evenness is recorded, resulting from the radiation of previously subordinate groups such as motile, epifaunal grazers.
This is a preview of subscription content, access via your institution
Access options
Subscribe to this journal
Receive 12 print issues and online access
$259.00 per year
only $21.58 per issue
Buy this article
- Purchase on Springer Link
- Instant access to full article PDF
Prices may be subject to local taxes which are calculated during checkout
Similar content being viewed by others
References
Shen, S-Z. et al. Calibrating the end-Permian mass extinction. Science 334, 1367–1372 (2011).
Kearsey, T., Twitchett, R. J., Price, G. D. & Grimes, S. T. Isotope excursions and palaeotemperature estimates from the Permian/Triassic boundary in the Southern Alps (Italy). Palaeogeogr. Palaeoclimatol. Palaeoecol. 279, 29–40 (2009).
Sun, Y. et al. Lethally hot temperatures during the Early Triassic Greenhouse. Science 338, 366–370 (2012).
Raup, D. M. & Sepkoski, J. J. Mass extinctions in the marine fossil record. Science 215, 1501–1503 (1982).
Benton, M. J. & Twitchett, R. J. How to kill (almost) all life: the end-Permian extinction event. Trends Ecol. Evol. 18, 358–365 (2003).
Payne, J. L. & Clapham, M. E. End-Permian mass extinction in the oceans: An ancient analog for the twenty-first century?. Annu. Rev. Earth Planet. Sci. 40, 89–111 (2012).
McGhee, G. R., Sheehan, P. M., Bottjer, D. J. & Droser, M. Ecological ranking of Phanerozoic biodiversity crises: Ecological and taxonomic severities are decoupled. Palaeogeogr. Palaeoclimatol. Palaeoecol. 211, 289–297 (2004).
Wignall, P. B. & Twitchett, R. J. Extent, duration and nature of the Permian–Triassic superanoxic event. Geol. Soc. Am. Spec. Pap. 356, 395–413 (2002).
Twitchett, R. J., Krystyn, L., Baud, A., Wheeley, J. R. & Richoz, S. Rapid marine recovery after the end-Permian mass-extinction event in the absence of marine anoxia. Geology 32, 805–808 (2004).
Beatty, T. W., Zonneveld, J-P. & Henderson, C. M. Anomalously diverse Early Triassic ichnofossil assemblages in northwest Pangea; A case for a shallow-marine habitable zone. Geology 36, 771–774 (2008).
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).
Clapham, M. E., Fraiser, M. L., Marenco, P. J. & Shen, S-Z. Taxonomic composition and environmental distribution of post-extinction rhynchonelliform brachiopod faunas: Constraints on short-term survival and the role of anoxia in the end-Permian mass extinction. Palaeogeogr. Palaeoclimatol. Palaeoecol. 374, 284–292 (2013).
Wignall, P. B., Morante, R. & Newton, R. The Permo-Triassic transition in Spitsbergen: δ13Corg chemostratigraphy, Fe and S geochemistry, facies, fauna and trace fossils. Geol. Mag. 135, 47–62 (1998).
Twitchett, R. J. & Barras, C. G. Trace fossils in the aftermath of mass extinction events. Geol. Soc. Lond. Spec. Publ. 228, 397–418 (2004).
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).
Jacobsen, N. D., Twitchett, R. J. & Krystyn, L. Palaeoecological methods for assessing marine ecosystem recovery following the late Permian mass extinction event. Palaeogeogr. Palaeoclimatol. Palaeoecol. 308, 200–212 (2011).
Webb, A. E. & Leighton, L. R. in Topics in Geobiology 36 (eds Laflamme, M., Schiffbauer, J. D. & Dornbos, S. Q.) 185–220 (Springer, 2011).
Bambach, R. K., Bush, A. M. & Erwin, D. H. Autoecology and the filling of ecospace: key metazoan radiations. Palaeontology 50, 1–22 (2007).
Novack-Gottshall, P. M. Using theoretical ecospace to quantify the ecological diversity of Paleozoic and modern marine biotas. Paleobiology 33, 273–294 (2007).
Villéger, S., Novack-Gottshall, P. M. & Mouillot, D. The multidimensionality of the niche reveals functional diversity changes in benthic marine biotas across geological time. Ecol. Lett. 14, 561–568 (2011).
Sepkoski, J. J. A compendium of fossil marine animal genera. Bull. Am. Paleont. 362, 1–560 (2002).
Miller, A. I. & Foote, M. Epicontinental seas versus open-ocean settings: The kinetics of mass extinction and origination. Science 326, 1106–1109 (2009).
Green, R. H. Measurement of non-randomness in spatial distributions. Res. Population Ecol. 8, 1–7 (1966).
Clapham, M. E., Shen, S. & Bottjer, D. J. The double mass extinction revisited: Reassessing the severity, selectivity, and causes of the end-Guadalupian biotic crisis (Late Permian). Paleobiology 35, 32–50 (2009).
Miller, A. I. & Foote, M. Calibrating the Ordovician radiation of marine life: Implications for Phanerozoic diversity trends. Paleobiology 22, 304–309 (1996).
Lloyd, G. T. et al. Dinosaurs and the Cretaceous terrestrial revolution. Proc. R. Soc. B 275, 2483–2490 (2008).
Chen, Z-Q. & Benton, M. J. The timing and pattern of biotic recovery following the end-Permian mass extinction. Nature Geosci. 5, 375–383 (2012).
Bush, A. M., Bambach, R. K. & Daley, G. M. Changes in theoretical ecospace utilization in marine fossil assemblage between the mid-Paleozoic and late Cenozoic. Paleobiology 33, 76–97 (2007).
Erwin, D. H., Valentine, J. W. & Sepkoski, J. J. A comparative study of diversification events: The early Paleozoic versus the Mesozoic. Evolution 41, 1177–1196 (1987).
Valentine, J. W. Determinants of diversity in higher taxonomic categories. Paleobiology 6, 440–450 (1980).
Baumiller, T. K. et al. Post-Paleozoic crinoid radiation in response to benthic predation preceded the Mesozoic marine revolution. Proc. Natl Acad. Sci. USA 107, 5893–5896 (2010).
Bush, A. M. & Bambach, R. K. Paleoecologic megatrends in marine metazoa. Annu. Rev. Earth Planet. Sci. 39, 241–269 (2011).
Knoll, A. H., Bambach, R. K., Payne, J. L., Pruss, S. & Fischer, W. W. Paleophysiology and end-Permian mass extinction. Earth Planet. Sci. Lett. 256, 295–313 (2007).
Stanley, S. M. Post-Paleozoic adaptive radiation of infaunal bivalve molluscs: A consequence of mantle fusion and siphon formation. J. Paleontol. 42, 214–229 (1968).
Signor, P. W. & Brett, C. E. The mid-Paleozoic precursor to the Mesozoic marine revolution. Paleobiology 10, 229–245 (1984).
Vermeij, G. J. The Mesozoic marine revolution: evidence from snails, predators and grazers. Paleobiology 3, 245–258 (1977).
Allison, P. A. & Briggs, D. E. G. Paleolatitudinal sampling bias, Phanerozoic species diversity, and the end-Permian extinction. Geology 21, 65–68 (1993).
Bush, A. M. & Bambach, R. K. Did alpha diversity increase during the Phanerozoic? Lifting the veils of taphonomic, latitudinal, and environmental biases. J. Geol. 112, 625–642 (2004).
McGowan, A. J. & Smith, A. B. Are global Phanerozoic marine diversity curves truly global? A study of the relationship between regional rock records and global Phanerozoic marine diversity. Paleobiology 34, 80–103 (2008).
Flügel, E. in Phanerozoic Reef Patterns 72 (eds Kiessling, W., Flügel, E. & Golonka, J.) 391–463 (SEPM Special Publications, 2002).
Reichow, M. K. et al. The timing and extent of the eruption of the Siberian Traps large igneous province: Implications for the end-Permian environmental crisis. Earth Planet. Sci. Lett. 277, 9–20 (2009).
Brayard, A. et al. Transient metazoan reefs in the aftermath of the end-Permian mass extinction. Nature Geosci. 4, 693–697 (2011).
Pruss, S. B., Payne, J. L. & Bottjer, D. J. Placunopsis bioherms: The first metazoan buildups following the end-Permian mass extinction. Palaios 22, 17–23 (2007).
Payne, J. L., Lehrmann, D. J., Christensen, S., Wei, J. & Knoll, A. H. Environmental and biological controls on the initiation and growth of a Middle Triassic (Anisian) reef complex on the Great Bank of Guizhou, Guizhou Province, China. Palaios 21, 325–343 (2006).
Ausich, W. I. & Bottjer, D. J. in Palaeobiology II (eds Briggs, D. E. G. & Crowther, P. R.) 384–386 (Blackwell Science, Oxford, 2001).
Twitchett, R. J. The palaeoclimatology, palaeoecology and palaeoenvironmental analysis of mass extinction events. Palaeogeogr. Palaeoclimatol. Palaeoecol. 232, 190–213 (2006).
Hautmann, M. & Nützel, A. First record of a heterodont bivalve (Mollusca) from the early Triassic: Palaeoecological significance and implications for the ‘Lazarus Problem’. Palaeontology 48, 1131–1138 (2005).
Baud, A. et al. Lower Triassic bryozoan beds from Ellesmere Island, High Arctic, Canada. Polar Res. 27, 428–440 (2008).
Shigeta, Y., Zakharov, Y. D., Maeda, H. & Popov, A. M. The Lower Triassic system in the Abrek Bay area, south Primorye, Russia. (National Museum of Nature and Science Monographs 38, Tokyo 2009)
Acknowledgements
W.J.F. would like to thank S. Danise and G. Price for discussions on data handling, ecospace assignments and analytical approaches. W.J.F. would also like to thank G. Lloyd and M. Bell for discussions on subsampling and programming in R. This study was supported by a Natural Environment Research Council grant (NE/I005641/1) to R.J.T. This is Paleobiology Database official publication No. 195.
Author information
Authors and Affiliations
Contributions
W.J.F. and R.J.T. are equally responsible for the project design, interpretation and writing. W.J.F. compiled the databases and undertook the analyses.
Corresponding author
Ethics declarations
Competing interests
The authors declare no competing financial interests.
Supplementary information
Supplementary Information
Supplementary Information (PDF 3445 kb)
Rights and permissions
About this article
Cite this article
Foster, W., Twitchett, R. Functional diversity of marine ecosystems after the Late Permian mass extinction event. Nature Geosci 7, 233–238 (2014). https://doi.org/10.1038/ngeo2079
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1038/ngeo2079
This article is cited by
-
Evolvability and Macroevolution: Overview and Synthesis
Evolutionary Biology (2022)
-
Exceptional fossil assemblages confirm the existence of complex Early Triassic ecosystems during the early Spathian
Scientific Reports (2021)
-
A multiscale view of the Phanerozoic fossil record reveals the three major biotic transitions
Communications Biology (2021)
-
Complex marine bioturbation ecosystem engineering behaviors persisted in the wake of the end-Permian mass extinction
Scientific Reports (2020)
-
Great Paleozoic-Mesozoic Biotic Turnings and Paleontological Education in China: A Tribute to the Achievements of Professor Zunyi Yang
Journal of Earth Science (2018)