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Ecosystem-wide body-size trends in Cambrian–Devonian marine invertebrate lineages

Published online by Cambridge University Press:  08 April 2016

Philip M. Novack-Gottshall
Philip M. Novack-Gottshall*
Affiliation:
Department of Geosciences, University of West Georgia, Carrollton, Georgia 30118-3100. E-mail: pnovackg@westga.edu
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Abstract

Fossil marine lineages are generally expected to exhibit long-term trends of increasing body size because of inherent fitness advantages or secular changes in environmental conditions. Because empirical documentation of this trend during the Paleozoic has been lacking for most taxonomic groups, the magnitude, timing, and taxonomic breadth of the trend have remained elusive. This study uses the largest existing database of fossil invertebrate sizes from four faunally important phyla to document ecosystem-wide size trends in well-preserved biotas from deep-subtidal, soft-substrate assemblages during the Cambrian through Devonian. Size of type specimens was measured along standard body axes from monographic plates and converted to body volume by using a broadly applicable empirical regression. Results demonstrate that mean body size (herein volume) of individual genera doubles during this interval, especially from the Late Ordovician through Early Devonian. The timing is gradual in spite of major radiations and extinctions, and the increase is primarily attributable to a net increase in the three-dimensionality of genera. The overall increase is not caused by replacement among clades because increases are widespread among arthropods, brachiopods, and echinoderms, at the phylum and class levels; in contrast, mollusks do not display a net size change at either taxonomic level. The increase is also more pronounced in microbivores than in carnivores. Combined with known environmental changes during this interval, and especially records of carbon dioxide, these trends provide support for the claim that primary productivity increased during the early to mid Paleozoic.

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Articles
Information
Paleobiology , Volume 34 , Issue 2 , Spring 2008 , pp. 210 - 228
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Copyright © The Paleontological Society 

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References

Literature Cited

Akaike, H. 1974. A new look at the statistical model identification. IEEE Transactions on Automatic Control 19:716–723.CrossRefGoogle Scholar
Alroy, J. 1998. Cope's rule and the dynamics of body mass evolution in North American mammals. Science 280:731–734.CrossRefGoogle Scholar
Alroy, J. 2000. Understanding the dynamics of trends within evolving lineages. Paleobiology 26:319–329.2.0.CO;2>CrossRefGoogle Scholar
Alroy, J., Marshall, C. R., Bambach, R. K., Bezusko, K., Foote, M., Fürsich, F. T., Hansen, T. A., Holland, S. M., Ivany, L. C., Jablonski, D., Jacobs, D. K., Jones, D. C., Kosnik, M. A., Lidgard, S., Low, S., Miller, A. I., Novack-Gottshall, P. M., Olszewski, T. D., Patzkowsky, M. E., Raup, D. M., Roy, K., Sepkoski, J. J. Jr., Sommers, M. G., Wagner, P. J., and Webber, A. 2001. Effects of sampling standardization on estimates of Phanerozoic marine diversification. Proceedings of the National Academy of Sciences USA 98:6261–6266.CrossRefGoogle ScholarPubMed
Anderson, D. R., Burnham, K. P., and Thompson, W. L. 2000. Null hypothesis testing: problems, prevalence, and an alternative. Journal of Wildlife Management 64:912–923.CrossRefGoogle Scholar
Bambach, R. K. 1977. Species richness in marine benthic habitats through the Paleozoic. Paleobiology 3:152–167.CrossRefGoogle Scholar
Bambach, R. K. 1993. Seafood through time: changes in biomass, energetics, and productivity in the marine ecosystem. Paleobiology 19:372–397.CrossRefGoogle Scholar
Bambach, R. K. 1999. Energetics in the global marine fauna: a connection between terrestrial diversification and change in the marine biosphere. Geobios 32:131–144.CrossRefGoogle Scholar
Berner, R. A. 2004. The Phanerozoic carbon cycle: CO2 and O2 . Oxford University Press, New York.CrossRefGoogle Scholar
Berner, R. A. 2006. GEOCARBSULF: a combined model for Phanerozoic atmospheric O2 and CO2 . Geochimica et Cosmochimica Acta 70:5653–5664.CrossRefGoogle Scholar
Bowring, S. A., Grotzinger, J. P., Isachsen, C. E., Knoll, A. H., Pelechaty, S. M., and Kolosov, P. 1993. Calibrating rates of Early Cambrian evolution. Science 261:1293–1298.CrossRefGoogle ScholarPubMed
Brett, C. E. 1990. Obrution deposits. Pp. 239–243 in Briggs, D. E. G. and Crowther, P. R., eds. Palaeobiology: a synthesis. Blackwell Scientific, London.Google Scholar
Brett, C. E., and Allison, P. A. 1998. Paleontological approaches to the environmental interpretation of marine mudrocks. Pp. 301–349 in Schieber, J., Zimmerle, W., and Sethi, P., eds. Shales and mudstones, Vol. 1. E. Schweizerbart, Stuttgart.Google Scholar
Calder, W. A. III. 1984. Size, function and life history. Harvard University Press, Cambridge.Google Scholar
Came, R. E., Eiler, J. M., Veizer, J., Azmy, K., Brand, U., and Weidman, C. R. 2007. Coupling of surface temperatures and atmospheric CO2 concentrations during the Palaeozoic era. Nature 449:198–201.CrossRefGoogle ScholarPubMed
Chamberlain, T. C. 1890. The method of multiple working hypotheses. Science 15:92–96.CrossRefGoogle Scholar
Churchill-Dixon, L. 2001. Late Ordovician increase in trilobite size and its evolutionary implications. PaleoBios 21:41–42.Google Scholar
Cloud, P. E. Jr. 1948. Assemblages of diminutive brachiopods and their paleoecological significance. Journal of Sedimentary Petrology 18:56–60.CrossRefGoogle Scholar
Connolly, S. R., and Miller, A. I. 2002. Global Ordovician faunal transitions in the marine benthos: ultimate causes. Paleobiology 28:26–40.2.0.CO;2>CrossRefGoogle Scholar
Cooper, R. A., Maxwell, P. A., Crampton, J. S., Beu, A. G., Jones, C. M., and Marshall, B. A. 2006. Completeness of the fossil record: estimating losses due to small body size. Geology 34:241–244.CrossRefGoogle Scholar
Dommergues, J.-L., 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
Efron, B., and Tibshirani, R. J. 1993. An introduction to the bootstrap. Chapman and Hall, New York.CrossRefGoogle Scholar
Feist, R. 1992. The Late Devonian trilobite crises. Historical Biology 5:197–214.CrossRefGoogle Scholar
Finkel, Z. V., Katz, M. E., Wright, J. D., Schofield, O. M. E., and Falkowski, P. G. 2005. Climatically driven macroevolutionary patterns in the size of marine diatoms over the Cenozoic. Proceedings of the National Academy of Sciences USA 102:8927–8932.CrossRefGoogle ScholarPubMed
Finnegan, S., and Droser, D. L. 2006. Body size trends and energetic constraints predict declining abundance of trilobites in the Ordovician of North America. Geological Society of America Abstracts with Programs 38:514.Google Scholar
Foote, M. 2005. Pulsed origination and extinction in the marine realm. Paleobiology 31:6–20.2.0.CO;2>CrossRefGoogle Scholar
Fortey, R. A., and Owens, R. M. 1990. Trilobites. Pp. 121–142 in McNamara, 1990.Google Scholar
Frey, R. C. 1989. Paleoecology of a well-preserved nautiloid assemblage from a Late Ordovician shale unit, southwestern Ohio. Journal of Paleontology 63:604–620.CrossRefGoogle Scholar
Gaines, R. R., and Droser, M. L. 2003. Paleoecology of the familiar trilobite Elrathia kingii: an early exaerobic zone inhabitant. Geology 31:941–944.CrossRefGoogle Scholar
Gould, S. J. 1988. Trends as changes in variance: a new slant on progress and directionality in evolution. Journal of Paleontology 62:319–329.CrossRefGoogle Scholar
Gradstein, F. M., Ogg, J. G., and Smith, A. G., eds. 2004. A geologic time scale 2004. Cambridge University Press, New York.CrossRefGoogle Scholar
Hallam, A., and Wignall, P. B. 1997. Mass extinctions and their aftermath. Oxford University Press, New York.CrossRefGoogle Scholar
Haq, B. U., and Al-Qahtani, A. M. 2005. Phanerozoic cycles of sea-level change on the Arabian Platform. GeoArabia 10:127–160.CrossRefGoogle Scholar
Harper, D. A. T., Cocks, L. R. M., Popov, L. E., Sheehan, P. M., Bassett, M. G., Copper, P., Holmer, L. E., Jin, J., and Rong, J. 2006. Brachiopods. Pp. 157–178 in Webby, et al. 2004.Google Scholar
Harrington, H. J., Henningsmoen, G., Howell, B. F., Jaanusson, V., Lochman-Balk, C., Moore, R. C., Poulsen, C., Rasetti, F., Richter, E., Richter, R., Schmidt, H., Sdzuy, K., Struve, W., Størmer, L., Stubblefield, C. J., Tripp, R., Weller, J. M., and Whittington, H. B. 1959. Arthropoda 1, Trilobitomorpha. Part O of Moore, R. C., ed. Treatise on invertebrate paleontology. Geological Society of America, New York, and University of Kansas, Lawrence.Google Scholar
Holmes, R. W. 1957. Chapter 6. Solar radiation, submarine daylight, and photosynthesis. In Hedgpeth, J. W., ed. Treatise on marine ecology and paleoecology, Vol. 1. Ecology, Geological Society of America Memoir 67:109–128.CrossRefGoogle Scholar
Hone, D. W. E., and Benton, M. J. 2007. Cope's Rule in the Pterosauria, and differing perceptions of Cope's Rule at different taxonomic levels. Journal of Evolutionary Biology 20:1164–1170.CrossRefGoogle ScholarPubMed
Hunt, G. 2006a. Fitting and comparing models of phyletic evolution: random walks and beyond. Paleobiology 32:578–601.CrossRefGoogle Scholar
Hunt, G. 2006b. paleoTS: modeling evolution in paleontological time-series, Version 0.1–2. http://cran.r-project.org/web/packages/paleoTS/index.html Google Scholar
Hunt, G., and Roy, K. 2006. Climate change, body size evolution, and Cope's Rule in deep-sea ostracodes. Proceedings of the National Academy of Sciences USA 103:1347–1352.CrossRefGoogle ScholarPubMed
Hurlbert, S. H. 1971. The nonconcept of species diversity: a critique and alternative parameters. Ecology 52:577–586.CrossRefGoogle ScholarPubMed
Jablonski, D. 1997. Body-size evolution in Cretaceous mollusks and the status of Cope's rule. Nature 385:250–252.CrossRefGoogle Scholar
Jennette, D. C., and Pryor, W. A. 1993. Cyclic alternation of proximal and distal storm facies: Kope and Fairview Formations (Upper Ordovician), Ohio and Kentucky. Journal of Sedimentary Petrology 63:183–203.CrossRefGoogle Scholar
Jin, J. 2001. Evolution and extinction of the North American Hiscobeccus brachiopod fauna during the Late Ordovician. Canadian Journal of Earth Sciences 38:143–151.Google Scholar
Johnson, J. B., and Omland, K. S. 2004. Model selection in ecology and evolution. Trends in Ecology and Evolution 19:101–108.CrossRefGoogle ScholarPubMed
Kidwell, S. M. 2002. Mesh-size effects on the ecological fidelity of death assemblages: a meta-analysis of molluscan live–dead studies. Geobios Mémoire Special 24:107–119.CrossRefGoogle Scholar
Kingsolver, J. G., and Pfennig, D. W. 2004. Individual-level selection as a cause of Cope's rule of phyletic size increase. Evolution 58:1608–1612.Google ScholarPubMed
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 21:588–597.CrossRefGoogle Scholar
Krause, R. A., Stempien, J. A., Kowalewski, M., and Miller, A. I. 2002. Differences in size of Early Paleozoic bivalves and brachiopods: the influence of intrinsic and extrinsic factors on body size evolution. Geological Society of America Abstracts with Programs 34:33.Google 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: 22:63–76.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
MacFadden, B. J. 1986. Fossil horses from “Eohippus” (Hyracotherium) to Equus: scaling, Cope's Law, and the evolution of body size. Paleobiology 12:355–369.CrossRefGoogle Scholar
Marcot, J. D., and McShea, D. W. 2007. Increasing hierarchical complexity throughout the history of life: phylogenetic tests of trend mechanisms. Paleobiology 33:182–200.CrossRefGoogle Scholar
Martin, R. E. 1996. Secular increase in nutrient levels through the Phanerozoic: implications for productivity, biomass, and diversity of the marine biosphere. Palaios 11:209–219.CrossRefGoogle Scholar
Martin, R. E. 2003. The fossil record of biodiversity: nutrients, productivity, habitat area, and differential preservation. Lethaia 36:179–194.CrossRefGoogle Scholar
McClain, C. R., and Rex, M. A. 2001. The relationship between dissolved oxygen concentration and maximum size in deep-sea turrid gastropods: an application of quantile regression. Marine Biology 139:681–685.Google Scholar
McClain, C. R., Rex, M. A., and Jabbour, R. 2005. Deconstructing bathymetric patterns of body size in deep-sea gastropods. Marine Ecology Progress Series 297:181–187.CrossRefGoogle Scholar
McKinney, M. L. 1990. Trends in body-size evolution. Pp. 75–118 in McNamara, 1990.Google Scholar
McMahon, T. 1973. Size and shape in biology. Science 179:1201–1204.CrossRefGoogle ScholarPubMed
McNamara, K. J. 1990. Evolutionary trends. University of Arizona Press, Tucson.Google Scholar
McShea, D. W. 1994. Mechanisms of large-scale evolutionary trends. Evolution 48:1747–1763.CrossRefGoogle ScholarPubMed
McShea, D. W. 2000. Trends, tools, and terminology. Paleobiology 26:330–333.2.0.CO;2>CrossRefGoogle Scholar
Miller, A. I., and Foote, M. 1996. Calibrating the Ordovician Radiation of marine life: implications for Phanerozoic diversity trends. Paleobiology 22:304–309.CrossRefGoogle ScholarPubMed
Miller, K. G., Kominz, M. A., Browning, J. V., Wright, J. D., Mountain, G. S., Katz, M. E., Sugarman, P. J., Cramer, B. S., Christie-Blick, N., and Pekar, S. F. 2005. The Phanerozoic record of global sea-level change. Science 310:1293–1298.CrossRefGoogle ScholarPubMed
Moore, R. C., Teichert, T., Robison, R. A., and Kaesler, R. L., eds. 1953–2006. Treatise on invertebrate paleontology. Geological Society of America, New York, and Boulder, Colo., and University of Kansas, Lawrence.Google 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. 2007. Using a theoretical ecospace to quantify the ecological diversity of Paleozoic and modern marine biotas. Paleobiology 33:273–294.CrossRefGoogle Scholar
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
Novack-Gottshall, P. M., and Lanier, M. A. 2008. Scale dependence of Cope's rule in body size evolution of Paleozoic brachiopods. Proceedings of the National Academy of Sciences USA 105:5430–5434.CrossRefGoogle ScholarPubMed
Novack-Gottshall, P. M., and Miller, A. I. 2003. Taxonomic richness and abundance of Late Ordovician gastropods and bivalves in mollusc-rich strata of the Cincinnati Arch. Palaios 18:559–571.2.0.CO;2>CrossRefGoogle Scholar
O'Brien, N. R., Brett, C. E., and Taylor, W. L. 1994. Microfabric and taphonomic analysis in determining sedimentary processes in marine mudstones: examples from Silurian of New York. Journal of Sedimentary Research A64:847–852.Google 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 Finnegan, S. 2006. Controls on marine animal biomass through geological time. Geobiology 4:1–10.CrossRefGoogle Scholar
Peters, R. H. 1983. The ecological implications of body size. Cambridge University Press, New York.CrossRefGoogle Scholar
Peters, S. E. 2004. Relative abundance of Sepkoski's evolutionary faunas in Cambrian–Ordovician deep subtidal environments in North America. Paleobiology 30:543–560.2.0.CO;2>CrossRefGoogle Scholar
R Development Core Team. 2007. R: a language and environment for statistical computing, Version 2. 5.0. R Foundation for Statistical Computing, Vienna. http://www.r-project.org/ [Checked 5-23-07] Google Scholar
Rex, M. A., Etter, R. J., Clain, A. J., and Hill, M. S. 1999. Bathymetric patterns of body size in deep-sea gastropods. Evolution 53:1298–1301.Google ScholarPubMed
Rohr, D. M., Blodgett, R. B., and Furnish, W. M. 1992. Maclurina manitobensis (Whiteaves) (Ordovician Gastropoda): the largest known Paleozoic gastropod. Journal of Paleontology 66:880–884.CrossRefGoogle Scholar
Rothman, D. H. 2002. Atmospheric carbon dioxide levels for the last 500 million years. Proceedings of the National Academy of Sciences USA 99:4167–4171.CrossRefGoogle ScholarPubMed
Roy, K. 2002. Bathymetry and body size in marine gastropods: a shallow water perspective. Marine Ecology Progress Series 237:143–149.CrossRefGoogle Scholar
Royer, D. L. 2006. CO2-forced climate thresholds during the Phanerozoic. Geochimica et Cosmochimica Acta 70:5665–5675.CrossRefGoogle Scholar
Royer, D. L., Berner, R. A., Montañez, I. P., Tabor, N. J., and Beerling, D. J. 2004. CO2 as a primary driver of Phanerozoic climate. GSA Today 14:4–10.2.0.CO;2>CrossRefGoogle Scholar
Rudkin, D. M., Young, G. A., Elias, R. J., and Dobrzanski, E. P. 2003. The world's biggest trilobite: Isotelus rex new species from the Upper Ordovician of northern Manitoba, Canada. Journal of Paleontology 77:99–112.2.0.CO;2>CrossRefGoogle Scholar
Sanders, H. L. 1968. Marine benthic diversity: a comparative study. American Naturalist 102:243–282.CrossRefGoogle Scholar
Schieber, J., Zimmerle, W., and Sethi, P., eds. 1998. Shales and mudstones. E. Schweizerbart, Stuttgart.Google Scholar
Schmidt-Nielsen, K. 1984. Scaling: why is animal size so important? Cambridge University Press, New York.CrossRefGoogle Scholar
Schovsbo, N. H. 2001. Why barren intervals? A taphonomic case study of the Scandinavian Alum Shale and its faunas. Lethaia 34:271–285.CrossRefGoogle Scholar
Sepkoski, J. J. Jr. 1981. A factor analytic description of the marine fossil record. Paleobiology 7:36–53.CrossRefGoogle Scholar
Sepkoski, J. J. Jr. 1997. Biodiversity: Past, present, and future. Journal of Paleontology 71:533–539.CrossRefGoogle ScholarPubMed
Sepkoski, J. J. Jr., and Miller, A. I. 1985. Evolutionary faunas and the distribution of Paleozoic benthic communities in space and time. Pp. 153–190 in Valentine, J. W., ed. Phanerozoic diversity patterns: profiles in macroevolution. Princeton University Press, Princeton, N.J. Google Scholar
Sheets, H. D., and Mitchell, C. E. 2001. Why the null matters: statistical tests, random walks, and evolution. Genetica 112–113:105–125.CrossRefGoogle Scholar
Smith, F. A., Betancourt, J. L. and Brown, J. H. 1995. Evolution of body size in the woodrat over the past 25,000 years of climate change. Science 270:2012–2014.CrossRefGoogle Scholar
Stanley, S. M. 1973. An explanation for Cope's rule. Evolution 27:1–26.CrossRefGoogle ScholarPubMed
Stempien, J. A., Krause, R. A. Jr., Kowalewski, M., and Miller, A. I. 2005. Brachiopod and bivalve size during the Ordovician: interpreting general trends. Geological Society of America Abstracts with Programs 37:14.Google Scholar
Thomas, R. D. K., Shearman, R. M., and Stewart, G. W. 2000. Evolutionary exploitation of design options by the first animals with hard skeletons. Science 288:1239–1242.CrossRefGoogle ScholarPubMed
Trammer, J., and Kaim, A. 1997. Body size and diversity exemplified by three trilobite clades. Acta Palaeontologica Polonica 42:1–12.Google Scholar
Vermeij, G. J. 1987. Evolution and escalation: an ecological history of life. Princeton University Press, Princeton, N.J. CrossRefGoogle Scholar
Vermeij, G. J. 1995. Economics, volcanoes, and Phanerozoic revolutions. Paleobiology 21:125–152.CrossRefGoogle Scholar
Vezier, J., Godderis, Y., and François, L. M. 2000. Evidence for decoupling of atmospheric CO2 and global climate during the Phanerozoic eon. Nature 408:698–701.CrossRefGoogle Scholar
Wang, S. C. 2005. Accounting for unequal variances in evolutionary trend mechanisms. Paleobiology 31:191–198.CrossRefGoogle Scholar
Webby, B. D., Paris, F., Droser, M. L., and Percival, I. G., eds. 2004. The great Ordovician biodiversification event. Columbia University Press, New York.CrossRefGoogle Scholar
Westermann, G. E. G. 1999. Life habits of nautiloids. Pp. 263–298 in Savazzi, E., ed. Functional morphology of the invertebrate skeleton. Wiley, New York.Google Scholar
Westermann, G. E. G., and Tsujita, C. J. 1999. Life habits of ammonoids. Pp. 299–325 in Savazzi, E., ed. Functional morphology of the invertebrate skeleton. Wiley, New York.Google Scholar