Skip to main content Accessibility help
×
×
Home

Comparative size evolution of marine clades from the Late Permian through Middle Triassic

  • Ellen K. Schaal (a1), Matthew E. Clapham (a2), Brianna L. Rego (a1), Steve C. Wang (a3) (a4) and Jonathan L. Payne (a1)...

Abstract

The small size of Early Triassic marine organisms has important implications for the ecological and environmental pressures operating during and after the end-Permian mass extinction. However, this “Lilliput Effect” has only been documented quantitatively in a few invertebrate clades. Moreover, the discovery of Early Triassic gastropod specimens larger than any previously known has called the extent and duration of the Early Triassic size reduction into question. Here, we document and compare Permian-Triassic body size trends globally in eight marine clades (gastropods, bivalves, calcitic and phosphatic brachiopods, ammonoids, ostracods, conodonts, and foraminiferans). Our database contains maximum size measurements for 11,224 specimens and 2,743 species spanning the Late Permian through the Middle to Late Triassic. The Permian/Triassic boundary (PTB) shows more size reduction among species than any other interval. For most higher taxa, maximum and median size among species decreased dramatically from the latest Permian (Changhsingian) to the earliest Triassic (Induan), and then increased during Olenekian (late Early Triassic) and Anisian (early Middle Triassic) time. During the Induan, the only higher taxon much larger than its long-term mean size was the ammonoids; they increased significantly in median size across the PTB, a response perhaps related to their comparatively rapid diversity recovery after the end-Permian extinction. The loss of large species in multiple clades across the PTB resulted from both selective extinction of larger species and evolution of surviving lineages toward smaller sizes. The within-lineage component of size decrease suggests that only part of the size decrease can be related to the end-Permian kill mechanism; in addition, Early Triassic environmental conditions or ecological pressures must have continued to favor small body size as well. After the end-Permian extinction, size decrease occurred across ecologically and physiologically disparate clades, but this size reduction was limited to the first part of the Early Triassic (Induan). Nektonic habitat or physiological buffering capacity may explain the contrast of Early Triassic size increase and diversification in ammonoids versus size reduction and slow recovery in benthic clades.

Copyright

References

Hide All
Arnold, A. J., Kelly, D. C., and Parker, W. C.. 1995. Causality and Cope’s rule: evidence from the planktonic foraminifera. Journal of Paleontology 69:203210.
Arnold, A. J., Parker, W. C., and Hansard, S. P.. 1995b. Aspects of the post-Cretaceous recovery of Cenozoic planktic foraminifera. Marine Micropaleontology 26:319327.
Arthur, M. A., Zachos, J. C., and Jones, D. S.. 1987. Primary productivity and the Cretaceous/Tertiary boundary event in the oceans. Cretaceous Research 8:4354.
Baarli, B. G. 2014. The early Rhuddanian survival interval in the Lower Silurian of the Oslo Region: a third pulse of the end-Ordovician extinction. Palaeogeography, Palaeoclimatology, Palaeoecology 395:2941.
Balinski, A. 2002. Frasnian-Famennian brachiopod extinction and recovery in southern Poland. Acta Palaeontologica Polonica 47(2), 289305.
Borths, M., and Ausich, W.. 2011. Ordovician-Silurian Lilliput crinoids during the end-Ordovician biotic crisis. Swiss Journal of Palaeontology 130(1), 718.
Boyd, D. W., and Newell, N. D.. 1972. Taphonomy and diagenesis of a Permian fossil assemblage from Wyoming. Journal of Paleontology 46:114.
Brayard, A., Escarguel, G., Buchner, H., Monnet, C., Brühwiler, T., Goudemand, N., Galfetti, T., and Guex, J.. 2009. Good genes and good luck: ammonoid diversity and the end-Permian mass extinction. Science 325:11181121.
Brayard, A., Nützel, A., Kaim, A., Escarguel, G., Hautmann, M., Stephen, D. A., Bylund, K. G., Jenks, J., and Bucher, H.. 2011. Gastropod evidence against the Early Triassic Lilliput effect: REPLY. Geology 39:e233.
Brayard, A., Nützel, A., Stephen, D. A., Bylund, K. G., Jenks, J., and Bucher, H.. 2010. Gastropod evidence against the Early Triassic Lilliput effect. Geology 38:147150.
Brown, J. H. 1995. Macroecology. University of Chicago Press, Chicago.
Brown, W. L., and Wilson, E. O.. 1956. Character displacement. Systematic Zoology 5:4964.
Burgess, S. D., Bowring, S., and Shen, S.-Z.. 2014. High-precision timeline for Earth’s most severe extinction. Proceedings of the National Academy of Sciences USA 111:33163321.
Calder, W. A. 1984. Size, function, and life history. Harvard University Press, Cambridge, Mass.
D’Hondt, S., Donaghay, P., Zachos, J. C., Luttenburg, D., and Lindinger, M. 1998. Organic carbon fluxes and ecological recovery from the Cretaceous-Tertiary mass extinction. Science 282:276279.
Dommergues, J., Montuire, S., and Neige, P.. 2002. Size patterns through time: the case of the Early Jurassic ammonite radiation. Paleobiology 28:423434.
Fraiser, M. L., and Bottjer, D. J.. 2004. The non-actualistic Early Triassic gastropod fauna: a case study of the Lower Triassic Sinbad Limestone Member. Palaios 19:259275.
Gabbott, S. E., Aldridge, R. J., and Theron, J. N.. 1995. A giant conodont with preserved muscle tissue from the Upper Ordovician of South Africa. Nature 374:800803.
Gingerich, P. D. 2009. Rates of evolution. Annual Review of Ecology, Evolution, and Systematics 40:657675.
Gingerich, P. D., Smith, H., and Rosenberg, K.. 1982. Allometric scaling in the dentition of primates and prediction of body weight from tooth size in fossils. American Journal of Physical Anthropology 58:81100.
Gooday, A. J., Levin, L. A., Aranda da Silva, A., Bett, B. J., Cowie, G. L., Dissard, D., Gage, J. D., Hughes, D. J., Jeffreys, R., Lamont, P. A., Larkin, K. E., Murty, S. J., Schumacher, S., Whitcraft, C., and Woulds, C.. 2009. Faunal responses to oxygen gradients on the Pakistan margin: a comparison of foraminiferans, macrofauna and megafauna. Deep-Sea Research II 56:488502.
Grice, K., Cao, C. Q., Love, G. D., Bottcher, M. E., Twitchett, R. J., Grosjean, E., Summons, R. E., Turgeon, S. C., Dunning, W., and Jin, Y. G.. 2005. Photic zone euxinia during the Permian-Triassic superanoxic event. Science 307:706709.
Hallam, A. 1991. Why was there a delayed radiation after the end-Paleozoic extinction? Historical Biology 5:257262.
Harper, E. M., Peck, L. S., and Hendry, K. R.. 2009. Patterns of shell repair in articulate brachiopods indicate size constitutes a refuge from predation. Marine Biology 156:19932000.
Harries, P. J., and Knorr, P. O.. 2009. What does the ‘Lilliput Effect’ mean? Palaeogeography, Palaeoclimatology. Palaeoecology 284:410.
He, W.-H., Shi, G. R., Feng, Q.-L., Campi, M. J., Gu, S.-Z., Bu, J.-J., Peng, Y.-Q., and Meng, Y.-Y.. 2007. Brachiopod miniaturization and its possible causes during the Permian-Triassic crisis in deep water environments, South China. Palaeogeography, Palaeoclimatology, Palaeoecology 252:145163.
He, W.-H., Twitchett, R. J., Zhang, Y., Shi, G. R., Feng, Q.-L., Yu, J.-X., Wu, S.-B., and Peng, X.-F.. 2010. Controls on body size during the Late Permian mass extinction event. Geobiology 8:391402.
Holland, C. H., and Copper, P.. 2008. Ordovician and Silurian nautiloid cephalopods from Anticosti Island: traject across the Ordovician-Silurian (O-S) mass extinction boundary. Canadian Journal of Earth Sciences 45:10151038.
Huang, B., Harper, D. A. T., Zhan, R., and Rong, J.. 2010. Can the Lilliput Effect be detected in the brachiopod faunas of. South China following the terminal Ordovician mass extinction? Palaeogeography, Palaeoclimatology, Palaeoecology 285:277286.
Hutchinson, G. E. 1959. Homage to Santa-Rosalia or why are there so many kinds of animals. American Naturalist 93:145159.
Isozaki, Y. 1997. Permo-Triassic boundary superanoxia and stratified superocean: records from lost deep sea. Science 276:235238.
Jablonski, D. 1996. Body size and macroevolution. Pp. 256289In D. Jablonski, D. H. Erwin. and J. H. Lipps, eds. Evolutionary paleobiology. University of Chicago Press, Chicago.
Jablonski, D 1997. Body-size evolution in Cretaceous mollusks and the status of Cope’s rule. Nature 385:250252.
Jablonski, D., and Raup, D. M.. 1995. Selectivity of end-Cretaceous marine bivalve extinctions. Science 268:389391.
Knoll, A. H., Bambach, R. K., Payne, J. L., Pruss, S., and Fischer, W. W.. 2007. Paleophysiology and end-Permian mass extinction. Earth and Planetary Science Letters 256:295313.
Kosnik, M. A., Jablonski, D., Lockwood, R., and Novack-Gottshall, P. M.. 2006. Quantifying molluscan body size in evolutionary and ecological analyses: maximizing the return on data-collection efforts. Palaios 21(6), 588597.
Kowalewski, M., Dulai, A., and Fürsich, F. T.. 1998. A fossil record full of holes: the Phanerozoic history of drilling predation. Geology 26:10911094.
Krause, R. A., Stempien, J. A., Kowalewski, M., and Miller, A. I.. 2007. Body size estimates from the literature: utility and potential for macroevolutionary studies. Palaios 22:6073.
Krejsa, R. J., Bringas, P. Jr., and Slavkin, H. C.. 1990. A neontological interpretation of conodont elements based on agnathan cyclostome tooth structure, function, and development. Lethaia 23:359378.
Kump, L. R., Pavlov, A., and Arthur, M. A.. 2005. Massive release of hydrogen sulfide to the surface ocean and atmosphere during intervals of oceanic anoxia. Geology 33:397400.
Levin, L. A. 2003. Oxygen minimum zone benthos: adaptation and community response to hypoxia. Oceanography and Marine Biology 41:134.
Lister, A. M. 1989. Rapid dwarfing of red deer on Jersey in the Last Interglacial. Nature 342:539542.
Lockwood, R. 2005. Body size, extinction events, and the early Cenozoic record of veneroid bivalves: a new role for recoveries? Paleobiology 31:578590.
Luo, G.-M., Lai, X.-L., Jiang, H.-S., and Zhang, K.-X.. 2006. Size variation of the end Permian conodont Neogondolella at Meishan Section, Changxing, Zhejiang and its significance. Science in China Series D: Earth Sciences 49:337347.
Luo, G.-M., Lai, X.-L., Shi, G. R., Jiang, H.-S., Yin, H.-F., Xie, S.-C., Tong, J.-N., Zhang, K.-X., He, W.-H., and Wignall, P. B.. 2008. Size variation of conodont elements of the Hindeodus-Isarcicella clade during the Permian-Triassic transition in South China and its implication for mass extinction. Palaeogeography, Palaeoclimatology, Palaeoecology 264:176187.
Marshall, C. R., and Jacobs, D. K.. 2009. Flourishing after the end-Permian mass extinction. Science 325:10791080.
McGhee, G. R., Sheehan, P. M., Bottjer, D. J., and Droser, M. L.. 2004. Ecological ranking of Phanerozoic biodiversity crises: ecological and taxonomic severities are decoupled. Palaeogeography, Palaeoclimatology, Palaeoecology 211:289297.
McRoberts, C. A., and Newton, C. R.. 1995. Selective extinction among end-Triassic European bivalves. Geology 23:102104.
Metcalfe, B., Twitchett, R. J., and Price-Lloyd, N.. 2011. Changes in size and growth rate of ‘Lilliput’ animals in the earliest Triassic. Palaeogeography, Palaeoclimatology, Palaeoecology 308:171180.
Meyer, K. M., Kump, L. R., and Ridgwell, A.. 2008. Biogeochemical controls on photic-zone euxinia during the end-Permian mass extinction. Geology 36:747750.
Meyer, K. M., Yu, M., Jost, A. B., Kelley, B. M., and Payne, J. L.. 2011. δ13C evidence that high primary productivity delayed recovery from end-Permian mass extinction. Earth and Planetary Science Letters 302:378384.
Morten, S. D., and Twitchett, R. J.. 2009. Fluctuations in the body size of marine invertebrates through the Pliensbachian-Toarcian extinction event: extinction, dwarfing and the Lilliput effect. Palaeogeography, Palaeoclimatology, Palaeoecology 284:10301032.
Niklas, K. J. 1994. The scaling of plant and animal body mass, length, and diameter. Evolution 48:4454.
Novack-Gottshall, P. M. 2008. Using simple body-size metrics to estimate fossil body volume: empirical validation using diverse Paleozoic invertebrates. Palaios 23:163173.
Orchard, M. J. 2007. Conodont diversity and evolution through the latest Permian and Early Triassic upheavals. Palaeogeography, Palaeoclimatology, Palaeoecology 252:93117.
Ovtcharova, M., Bucher, H., Schalteger, U., Galfetti, T., Brayard, A., and Guex, J.. 2006. New Early to Middle Triassic U-Pb ages from South China: calibration with ammonoid biochronozones and implications for the timing of the Triassic biotic recovery. Earth and Planetary Science Letters 243:463475.
Ozaki, K., Tajima, S., and Tajika, E.. 2011. Conditions required for oceanic anoxia/euxinia: constraints from a one-dimensional ocean biogeochemical cycle model. Earth and Planetary Science Letters 304:270279.
Paine, R. T. 1976. Size-limited predation: an observational and experimental approach with the Mytilus: Pisaster interaction. Ecology 57:858873.
Payne, J. L. 2005. Evolutionary dynamics of gastropod size across the end-Permian extinction and through the Triassic recovery interval. Paleobiology 31:269290.
Payne, J. L., and Clapham, M. E.. 2012. End-Permian mass extinction in the oceans: an ancient analog for the 21st century? Annual Reviews of Earth and Planetary Science 40:89111.
Payne, J. L., and Finnegan, S.. 2006. Controls on marine animal biomass through geologic time. Geobiology 4:110.
Payne, J. L., Summers, M., Rego, B. L., Altiner, D., Wei, J.-Y., Yu, M.-Y., and Lehrmann, D. J.. 2011. 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 37:409425.
Peters, R. H. 1983. The ecological implications of body size. Cambridge University Press, New York.
Pruss, S. B., and Bottjer, D. J.. 2004. Early Triassic trace fossils of the Western United States and their implications for prolonged environmental stress from the end-Permian mass extinction. Palaios 19:551564.
Purnell, M. A. 1994. Skeletal ontogeny and feeding mechanisms in conodonts. Lethaia 27:129138.
Randall, J. E. 1973. Size of the great white shark (Carcharodon). Science 181:169170.
Rego, B. L., Wang, S. C., Altiner, D., and Payne, J. L.. 2012. Within- and among-genus components of size evolution during mass extinction, recovery, and background intervals: a case study of Late Permian through Late Triassic foraminifera. Paleobiology 38:627643.
Renaud, S., and Girard, C.. 1999. Strategies of survival during extreme environmental perturbations: evolution of conodonts in response to the Kellwasser Crisis (Upper Devonian). Palaeogeography, Palaeoclimatology, Palaeoecology 146:1932.
Schmidt-Nielsen, K. 1984. Scaling: why is animal size so important? Cambridge University Press, New York.
Schubert, J. K., and Bottjer, D. J.. 1995. Aftermath of the Permian-Triassic mass extinction event: paleoecology of Lower Triassic carbonates in the western USA. Palaeogeography, Palaeoclimatology, Palaeoecology 116:139.
Seibel, B. A., Chausson, F., Lallier, F. H., Zal, F., and Childress, J. J.. 1999. Vampire blood: respiratory physiology of the vampire squid (Cephalopoda: Vampyromorpha) in relation to the oxygen minimum layer. Experimental Biology Online 4(1): 110.
Smith, A. B., and Jeffery, C. H.. 1998. Selectivity of extinction among sea urchins at the end of the Cretaceous period. Nature 392:6971.
Song, H., Tong, J., Algeo, T. J., Horacek, M., Qiu, H., Song, H., Tian, L., and Chen, Z. Q.. 2013. Large vertical δ13CDIC gradients in Early Triassic seas of the South China craton: implications for oceanographic changes related to Siberian Traps volcanism. Global and Planetary Change 105:720.
Song, H.-J., Tong, J.-N., and Chen, Z. Q.. 2011. Evolutionary dynamics of the Permian-Triassic foraminifer size: evidence for Lilliput effect in the end-Permian mass extinction and its aftermath. Palaeogeography, Palaeoclimatology, Palaeoecology 308:98110.
Stanley, S. M. 1973. An explanation for Cope’s Rule. Evolution 27:126.
Stanley, S. M 1986. Population size, extinction, and speciation: the fission effect in Neogene Bivalvia. Paleobiology 12:89110.
Trammer, J. 2005. Maximum body size in a radiating clade as a function of time. Evolution 59(5): 941947.
Twitchett, R. J. 1999. Palaeoenvironments and faunal recovery after the end-Permian mass extinction. Palaeogeography, Palaeoclimatology, Palaeoecology 154:2737.
Twitchett, R. J 2001. Incompleteness of the Permian-Triassic fossil record: a consequence of productivity decline? Geological Journal 36:341353.
Twitchett, R. J 2007. The Lilliput effect in the aftermath of the end-Permian extinction event. Palaeogeography, Palaeoclimatology, Palaeoecology 252:132144.
Twitchett, R. J., and Barras, C. G.. 2004. Trace fossils in the aftermath of mass extiniction events. In D. McIlroy, ed. The application of ichnology to palaeoenvironmental and stratigraphic analysis. Geological Society of London, Special Publication 228:397418.
Urbanek, A. 1993. Biotic crises in the history of Upper Silurian graptoloids: a palaeobiological model. Historical Biology 7:2950.
Valentine, J. W. 1973. Evolutionary paleoecology of the marine biosphere. Prentice Hall, Englewood, N. J.
Vartanyan, S. L., Garutt, V. E., and Sher, A. B.. 1993. Holocene dwarf mammoths from Wrangel Island in the Siberian Arctic. Nature 362:337340.
Végh-Neubrandt, E. 1982. Triassische Megalodontaceae. Akadémiai Kiadó, Budapest.
Wignall, P. B., and Twitchett, R. J.. 2002. Extent, duration, and nature of the Permian-Triassic superanoxic event. In C. Koeberl and K. G. MacLeod, eds. Catastrophic events and mass extinctions: impacts and beyond. Geological Society of America Special Paper 356:395-413.
Xie, S. C., Pancost, R. D., Jin, H. F., Wang, H. M., and Evershed, R. P.. 2005. Two episodes of microbial change coupled with Permo/Triassic faunal mass extinction. Nature 434:494497.
Recommend this journal

Email your librarian or administrator to recommend adding this journal to your organisation's collection.

Paleobiology
  • ISSN: 0094-8373
  • EISSN: 1938-5331
  • URL: /core/journals/paleobiology
Please enter your name
Please enter a valid email address
Who would you like to send this to? *
×

Metrics

Altmetric attention score

Full text views

Total number of HTML views: 0
Total number of PDF views: 0 *
Loading metrics...

Abstract views

Total abstract views: 0 *
Loading metrics...

* Views captured on Cambridge Core between <date>. This data will be updated every 24 hours.

Usage data cannot currently be displayed