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

Published online by Cambridge University Press:  06 November 2015

Ellen K. Schaal ,
Matthew E. Clapham ,
Brianna L. Rego ,
Steve C. Wang  and
Jonathan L. Payne
Ellen K. Schaal
Affiliation:
Department of Geological and Environmental Sciences, Stanford University, Stanford, California 94305, U.S.A. E-mail: [email protected].
Matthew E. Clapham
Affiliation:
Department of Earth and Planetary Sciences, University of California, Santa Cruz, California 95064, U.S.A.
Brianna L. Rego
Affiliation:
Department of Geological and Environmental Sciences, Stanford University, Stanford, California 94305, U.S.A. E-mail: [email protected].
Steve C. Wang
Affiliation:
Department of Mathematics and Statistics, Swarthmore College, Swarthmore, Pennsylvania 19081, U.S.A. Department of Geological and Environmental Sciences, Stanford University, Stanford, California 94305, U.S.A.
Jonathan L. Payne
Affiliation:
Department of Geological and Environmental Sciences, Stanford University, Stanford, California 94305, U.S.A. E-mail: [email protected].
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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.

Type
Articles
Information
Paleobiology , Volume 42 , Issue 1 , February 2016 , pp. 127 - 142
Copyright
Copyright © 2015 The Paleontological Society. All rights reserved. 

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References

Literature Cited

Arnold, A. J., Kelly, D. C., and Parker, W. C.. 1995. Causality and Cope’s rule: evidence from the planktonic foraminifera. Journal of Paleontology 69:203–210.CrossRefGoogle Scholar
Arnold, A. J., Parker, W. C., and Hansard, S. P.. 1995b. Aspects of the post-Cretaceous recovery of Cenozoic planktic foraminifera. Marine Micropaleontology 26:319–327.CrossRefGoogle Scholar
Arthur, M. A., Zachos, J. C., and Jones, D. S.. 1987. Primary productivity and the Cretaceous/Tertiary boundary event in the oceans. Cretaceous Research 8:43–54.CrossRefGoogle Scholar
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 395:29–41.CrossRefGoogle Scholar
Balinski, A. 2002. Frasnian-Famennian brachiopod extinction and recovery in southern Poland. Acta Palaeontologica Polonica 47(2), 289–305.Google Scholar
Borths, M., and Ausich, W.. 2011. Ordovician-Silurian Lilliput crinoids during the end-Ordovician biotic crisis. Swiss Journal of Palaeontology 130(1), 7–18.CrossRefGoogle Scholar
Boyd, D. W., and Newell, N. D.. 1972. Taphonomy and diagenesis of a Permian fossil assemblage from Wyoming. Journal of Paleontology 46:1–14.Google Scholar
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 325:1118–1121.CrossRefGoogle Scholar
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.CrossRefGoogle Scholar
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 38:147–150.CrossRefGoogle Scholar
Brown, J. H. 1995. Macroecology. University of Chicago Press, Chicago.Google Scholar
Brown, W. L., and Wilson, E. O.. 1956. Character displacement. Systematic Zoology 5:49–64.CrossRefGoogle Scholar
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 111:3316–3321.CrossRefGoogle ScholarPubMed
Calder, W. A. 1984. Size, function, and life history. Harvard University Press, Cambridge, Mass.Google Scholar
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 282:276–279.CrossRefGoogle ScholarPubMed
Dommergues, J., Montuire, S., and Neige, P.. 2002. Size patterns through time: the case of the Early Jurassic ammonite radiation. Paleobiology 28:423–434.2.0.CO;2>CrossRefGoogle Scholar
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 19:259–275.2.0.CO;2>CrossRefGoogle Scholar
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 374:800–803.CrossRefGoogle Scholar
Gingerich, P. D. 2009. Rates of evolution. Annual Review of Ecology, Evolution, and Systematics 40:657–675.CrossRefGoogle Scholar
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 58:81–100.CrossRefGoogle ScholarPubMed
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 56:488–502.CrossRefGoogle Scholar
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 307:706–709.CrossRefGoogle ScholarPubMed
Hallam, A. 1991. Why was there a delayed radiation after the end-Paleozoic extinction? Historical Biology 5:257–262.CrossRefGoogle Scholar
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 156:1993–2000.CrossRefGoogle Scholar
Harries, P. J., and Knorr, P. O.. 2009. What does the ‘Lilliput Effect’ mean? Palaeogeography, Palaeoclimatology. Palaeoecology 284:4–10.CrossRefGoogle Scholar
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 252:145–163.CrossRefGoogle Scholar
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 8:391–402.CrossRefGoogle ScholarPubMed
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 45:1015–1038.CrossRefGoogle Scholar
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 285:277–286.CrossRefGoogle Scholar
Hutchinson, G. E. 1959. Homage to Santa-Rosalia or why are there so many kinds of animals. American Naturalist 93:145–159.CrossRefGoogle Scholar
Isozaki, Y. 1997. Permo-Triassic boundary superanoxia and stratified superocean: records from lost deep sea. Science 276:235–238.CrossRefGoogle ScholarPubMed
Jablonski, D. 1996. Body size and macroevolution. Pp. 256–289In D. Jablonski, D. H. Erwin. and J. H. Lipps, eds. Evolutionary paleobiology. University of Chicago Press, Chicago.Google Scholar
Jablonski, D 1997. Body-size evolution in Cretaceous mollusks and the status of Cope’s rule. Nature 385:250–252.CrossRefGoogle Scholar
Jablonski, D., and Raup, D. M.. 1995. Selectivity of end-Cretaceous marine bivalve extinctions. Science 268:389–391.CrossRefGoogle ScholarPubMed
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 256:295–313.CrossRefGoogle Scholar
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), 588–597.CrossRefGoogle Scholar
Kowalewski, M., Dulai, A., and Fürsich, F. T.. 1998. A fossil record full of holes: the Phanerozoic history of drilling predation. Geology 26:1091–1094.2.3.CO;2>CrossRefGoogle Scholar
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 22:60–73.CrossRefGoogle Scholar
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 23:359–378.CrossRefGoogle Scholar
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 33:397–400.CrossRefGoogle Scholar
Levin, L. A. 2003. Oxygen minimum zone benthos: adaptation and community response to hypoxia. Oceanography and Marine Biology 41:1–34.Google Scholar
Lister, A. M. 1989. Rapid dwarfing of red deer on Jersey in the Last Interglacial. Nature 342:539–542.CrossRefGoogle Scholar
Lockwood, R. 2005. Body size, extinction events, and the early Cenozoic record of veneroid bivalves: a new role for recoveries? Paleobiology 31:578–590.CrossRefGoogle Scholar
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 49:337–347.CrossRefGoogle Scholar
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 264:176–187.CrossRefGoogle Scholar
Marshall, C. R., and Jacobs, D. K.. 2009. Flourishing after the end-Permian mass extinction. Science 325:1079–1080.CrossRefGoogle ScholarPubMed
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 211:289–297.CrossRefGoogle Scholar
McRoberts, C. A., and Newton, C. R.. 1995. Selective extinction among end-Triassic European bivalves. Geology 23:102–104.2.3.CO;2>CrossRefGoogle Scholar
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 308:171–180.CrossRefGoogle Scholar
Meyer, K. M., Kump, L. R., and Ridgwell, A.. 2008. Biogeochemical controls on photic-zone euxinia during the end-Permian mass extinction. Geology 36:747–750.CrossRefGoogle Scholar
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 302:378–384.CrossRefGoogle Scholar
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 284:1030–1032.CrossRefGoogle Scholar
Niklas, K. J. 1994. The scaling of plant and animal body mass, length, and diameter. Evolution 48:44–54.CrossRefGoogle ScholarPubMed
Novack-Gottshall, P. M. 2008. Using simple body-size metrics to estimate fossil body volume: empirical validation using diverse Paleozoic invertebrates. Palaios 23:163–173.CrossRefGoogle Scholar
Orchard, M. J. 2007. Conodont diversity and evolution through the latest Permian and Early Triassic upheavals. Palaeogeography, Palaeoclimatology, Palaeoecology 252:93–117.CrossRefGoogle Scholar
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 243:463–475.CrossRefGoogle Scholar
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 304:270–279.CrossRefGoogle Scholar
Paine, R. T. 1976. Size-limited predation: an observational and experimental approach with the Mytilus: Pisaster interaction. Ecology 57:858–873.CrossRefGoogle Scholar
Payne, J. L. 2005. Evolutionary dynamics of gastropod size across the end-Permian extinction and through the Triassic recovery interval. Paleobiology 31:269–290.CrossRefGoogle Scholar
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 40:89–111.CrossRefGoogle Scholar
Payne, J. L., and Finnegan, S.. 2006. Controls on marine animal biomass through geologic time. Geobiology 4:1–10.CrossRefGoogle Scholar
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 37:409–425.CrossRefGoogle Scholar
Peters, R. H. 1983. The ecological implications of body size. Cambridge University Press, New York.CrossRefGoogle Scholar
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 19:551–564.2.0.CO;2>CrossRefGoogle Scholar
Purnell, M. A. 1994. Skeletal ontogeny and feeding mechanisms in conodonts. Lethaia 27:129–138.CrossRefGoogle Scholar
Randall, J. E. 1973. Size of the great white shark (Carcharodon). Science 181:169–170.CrossRefGoogle ScholarPubMed
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 38:627–643.CrossRefGoogle Scholar
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 146:19–32.CrossRefGoogle Scholar
Schmidt-Nielsen, K. 1984. Scaling: why is animal size so important? Cambridge University Press, New York.CrossRefGoogle Scholar
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 116:1–39.CrossRefGoogle Scholar
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): 1–10.CrossRefGoogle Scholar
Smith, A. B., and Jeffery, C. H.. 1998. Selectivity of extinction among sea urchins at the end of the Cretaceous period. Nature 392:69–71.CrossRefGoogle Scholar
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 105:7–20.CrossRefGoogle Scholar
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 308:98–110.CrossRefGoogle Scholar
Stanley, S. M. 1973. An explanation for Cope’s Rule. Evolution 27:1–26.CrossRefGoogle ScholarPubMed
Stanley, S. M 1986. Population size, extinction, and speciation: the fission effect in Neogene Bivalvia. Paleobiology 12:89–110.CrossRefGoogle Scholar
Trammer, J. 2005. Maximum body size in a radiating clade as a function of time. Evolution 59(5): 941–947.Google Scholar
Twitchett, R. J. 1999. Palaeoenvironments and faunal recovery after the end-Permian mass extinction. Palaeogeography, Palaeoclimatology, Palaeoecology 154:27–37.CrossRefGoogle Scholar
Twitchett, R. J 2001. Incompleteness of the Permian-Triassic fossil record: a consequence of productivity decline? Geological Journal 36:341–353.CrossRefGoogle Scholar
Twitchett, R. J 2007. The Lilliput effect in the aftermath of the end-Permian extinction event. Palaeogeography, Palaeoclimatology, Palaeoecology 252:132–144.CrossRefGoogle Scholar
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 228:397–418.CrossRefGoogle Scholar
Urbanek, A. 1993. Biotic crises in the history of Upper Silurian graptoloids: a palaeobiological model. Historical Biology 7:29–50.CrossRefGoogle Scholar
Valentine, J. W. 1973. Evolutionary paleoecology of the marine biosphere. Prentice Hall, Englewood, N. J.Google Scholar
Vartanyan, S. L., Garutt, V. E., and Sher, A. B.. 1993. Holocene dwarf mammoths from Wrangel Island in the Siberian Arctic. Nature 362:337–340.CrossRefGoogle ScholarPubMed
Végh-Neubrandt, E. 1982. Triassische Megalodontaceae. Akadémiai Kiadó, Budapest.Google Scholar
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.CrossRefGoogle Scholar
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 434:494–497.CrossRefGoogle ScholarPubMed