Hostname: page-component-78c5997874-8bhkd Total loading time: 0 Render date: 2024-11-05T13:37:38.580Z Has data issue: false hasContentIssue false
  • English
  • Français

Body size, sampling completeness, and extinction risk in the marine fossil record

Published online by Cambridge University Press:  30 January 2020

Jonathan L. Payne Open the ORCID record for Jonathan L. Payne [Opens in a new window]  and
Noel A. Heim Open the ORCID record for Noel A. Heim [Opens in a new window]
Jonathan L. Payne
Affiliation:
Department of Geological Sciences, Stanford University, Stanford, California94305, U.S.A. E-mail: [email protected]
Noel A. Heim
Affiliation:
Department of Geological Sciences, Stanford University, Stanford, California94305, U.S.A. E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

Larger body size has long been assumed to correlate with greater risk of extinction, helping to shape body-size distributions across the tree of life, but a lack of comprehensive size data for fossil taxa has left this hypothesis untested for most higher taxa across the vast majority of evolutionary time. Here we assess the relationship between body size and extinction using a data set comprising the body sizes, stratigraphic ranges, and occurrence patterns of 9408 genera of fossil marine animals spanning eight Linnaean classes across the past 485 Myr. We find that preferential extinction of smaller-bodied genera within classes is substantially more common than expected due to chance and that there is little evidence for preferential extinction of larger-bodied genera. Using a capture–mark–recapture analysis, we find that this size bias of extinction persists even after accounting for a pervasive bias against the sampling of smaller-bodied genera within classes. The size bias in extinction also persists after including geographic range as an additional predictor of extinction, indicating that correlation between body size and geographic range does not provide a simple explanation for the association between size and extinction. Regardless of the underlying causes, the preferential extinction of smaller-bodied genera across many higher taxa and most of geologic time indicates that the selective loss of large-bodied animals is the exception, rather than the rule, in the evolution of marine animals.

Type
Articles
Information
Paleobiology , Volume 46 , Issue 1 , February 2020 , pp. 23 - 40
Copyright
Copyright © The Paleontological Society. All rights reserved 2020

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

Footnotes

Data available from the Dryad Digital Repository: https://doi.org/10.5061/dryad.zpc866t5b

References

Literature Cited

Alroy, J. 1999. Putting North America's end-Pleistocene megafaunal extinction in context. Pp.105–143in MacPhee, R. D. E., ed. Extinctions in near time: causes, contexts, and consequences. Springer, Boston.CrossRefGoogle Scholar
Alroy, J., Marshall, C. R., Bambach, R. K., Bezusko, K., Foote, M., Fursich, 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., 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
Boyer, A. G. 2010. Consistent ecological selectivity through time in Pacific Island avian extinctions. Conservation Biology 24:511–519.CrossRefGoogle ScholarPubMed
Brown, J. H. 1995. Macroecology. University of Chicago Press, Chicago.Google Scholar
Cardillo, M., Mace, G. M., Jones, K. E., Bielby, J., Bininda-Emonds, O. R. P., Sechrest, W., Orme, C. D. L., and Purvis, A.. 2005. Multiple causes of high extinction risk in large mammal species. Science 309:1239–1241.CrossRefGoogle ScholarPubMed
Chen, X., Melchin, M. J., Sheets, H. D., Mitchell, C. E., and Fan, J.-X.. 2005. Patterns and processes of latest Ordovician graptolite extinction and recovery based on data from south China. Journal of Paleontology 79:842–861.Google Scholar
Clauset, A., and Erwin, D. H.. 2008. The evolution and distribution of species body size. Science 321:399–401.CrossRefGoogle ScholarPubMed
Collins, K. S., Edie, S. M., Hunt, G., Roy, K., and Jablonski, D.. 2018. Extinction risk in extant marine species integrating palaeontological and biodistributional data. Proceedings of the Royal Society of London B 285:20181698.CrossRefGoogle ScholarPubMed
Connolly, S. R., and Miller, A. I.. 2001a. Global Ordovician fauna transitions in the marine benthos: proximate causes. Paleobiology 27:779–795.2.0.CO;2>CrossRefGoogle Scholar
Connolly, S. R., and Miller, A. I.. 2001b. Joint estimation of sampling and turnover rates from fossil databases: capture-mark-recapture methods revisited. Paleobiology 27:751–767.2.0.CO;2>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
Conroy, M. J., and Nichols, J. D.. 1984. Testing for variation in taxonomic extinction probabilities: a suggested methodology and some results. Paleobiology 10:328–337.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
Cormack, R. M. 1964. Estlimates of survival from the sighting of marked animals. Biometrika 51:429–438.CrossRefGoogle Scholar
Crampton, J. S., Cooper, R. A., Beu, A. G., Foote, M., and Marshall, B. A.. 2010. Biotic influences on species duration: interactions between traits in marine molluscs. Paleobiology 36:204–223.CrossRefGoogle Scholar
Davidson, A. D., Hamilton, M. J., Boyer, A. G., Brown, J. H., and Ceballos, G.. 2009. Multiple ecological pathways to extinction in mammals. Proceedings of the National Academy of Sciences USA 106:10702–10705.CrossRefGoogle ScholarPubMed
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
Finarelli, J. A., and Liow, L. H.. 2016. Diversification histories for North American and Eurasian carnivorans. Biological Journal of the Linnean Society 118:26–38.CrossRefGoogle Scholar
Foote, M. 2005. Pulsed origination and extinction in the marine realm. Paleobiology 31:6–20.2.0.CO;2>CrossRefGoogle Scholar
Foote, M. 2006. Substrate affinity and diversity dynamics of Paleozoic marine animals. Paleobiology 32:345–366.CrossRefGoogle Scholar
Foote, M., and Miller, A. I.. 2013. Determinants of early survival in marine animal genera. Paleobiology 39:171–192.CrossRefGoogle Scholar
Foote, M., Crampton, J. S., Beu, A. G., and Cooper, R. A.. 2008. On the bidirectional relationship between geographic range and taxonomic duration. Palaeobiology 34:421–433.CrossRefGoogle Scholar
Friedman, M. 2009. Ecomorphological selectivity among marine teleost fishes during the end-Cretaceous extinction. Proceedings of the National Academy of Sciences USA 106:5218–5223.CrossRefGoogle ScholarPubMed
Gaston, K. J. 1990. Patterns in the geographical ranges of species. Biological Reviews of the Cambridge Philosophical Society 65:105–129.CrossRefGoogle Scholar
Gaston, K. J., and Blackburn, T. M.. 1995. Birds, body size and the threat of extinction. Philosophical Transactions of the Royal Society of London B 347:205–212.Google Scholar
Goodwin, N. B., Dulvy, N. K., and Reynolds, J. D.. 2005. Macroecology of live-bearing in fishes: latitudinal and depth range comparisons with egg-laying relatives. Oikos 110:209–218.CrossRefGoogle Scholar
Harnik, P. G. 2011. Direct and indirect effects of biological factors on extinction risk in fossil bivalves. Proceedings of the National Academy of Sciences USA 108:13594–13599.CrossRefGoogle ScholarPubMed
Harnik, P. G., Simpson, C., and Payne, J. L.. 2012. Long-term differences in extinction risk among the seven forms of rarity. Proceedings of the Royal Society of London B 279:4969–4976.CrossRefGoogle ScholarPubMed
Harnik, P. G., Fitzgerald, P. C., Payne, J. L., and Carlson, S. J.. 2014. Phylogenetic signal in extinction selectivity in Devonian terebratulide brachiopods. Paleobiology 40:675–692.CrossRefGoogle Scholar
Heim, N. A., Knope, M. L., Schaal, E. K., Wang, S. C., and Payne, J. L.. 2015. Cope's rule in the evolution of marine animals. Science 347:867–870.CrossRefGoogle ScholarPubMed
Jablonski, D. 1995. Extinctions in the fossil record. Pp. 25–44in Lawton, J. H. and May, R. M., eds. Extinction rates. Oxford University Press, Oxford.Google Scholar
Jablonski, D. 1996. Body size and macroevolution. Pp. 256–289in Jablonski, D., Erwin, D. H., and Lipps, J. H., eds. Evolutionary paleobiology. University of Chicago Press, Chicago.Google ScholarPubMed
Jablonski, D., and Raup, D. M.. 1995. Selectivity of end-Cretaceous marine bivalve extinctions. Science 268:389–391.CrossRefGoogle ScholarPubMed
Jablonski, D., Roy, K., Valentine, J. W., Price, R. M., and Anderson, P. S.. 2003. The impact of the Pull of the Recent on the history of marine diversity. Science 300:1133–1135.CrossRefGoogle ScholarPubMed
Jolly, G. M. 1965. Explicit estimates from capture-recapture data with both death and immigration-stochastic model. Biometrika 52:225–247.CrossRefGoogle ScholarPubMed
Kidwell, S. M., and Bosence, D. W. J.. 1991. Taphonomy and time-averaging of marine shelly faunas. Pp. 115–209in Allison, P. A. and Briggs, D. E. G., eds. Taphonomy: releasing the data locked in the fossil record. Plenum Press, New York.CrossRefGoogle Scholar
Koenker, R. 2018. quantreg: Quantile regression, R package version 5.38. https://CRAN.R-project.org/package=quantreg, accessed 15 January 2018.Google 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 21:588–597.CrossRefGoogle Scholar
Kröger, B. 2005. Adaptive evolution in Paleozoic coiled cephalopods. Paleobiology 31:253–268.CrossRefGoogle Scholar
Laake, J. L., Johnson, D. S., and Conn, P. B.. 2013. marked: an R package for maximum likelihood and Markov Chain Monte Carlo analysis of capture-recapture data. Methods in Ecology and Evolution 4:885–890.CrossRefGoogle Scholar
Liow, L. H. 2007. Does versatility as measured by geographic range, bathymetric range and morphological variability contribute to taxon longevity? Global Ecology and Biogeography 16:117–128.CrossRefGoogle Scholar
Liow, L. H., and Finarelli, J. A.. 2014. A dynamic global equilibrium in carnivoran diversification over 20 million years. Proceedings of the Royal Society of London B 281:20132312.CrossRefGoogle ScholarPubMed
Liow, L. H., and Nichols, J. D.. 2010. Estimating rates and probabilities of origination and extinction using taxonomic occurrence data: capture-recapture approaches. In Alroy, J. and Hunt, G., eds. Quantitative methods in paleobiology. Paleontological Society Papers 16:81–94. Paleontological Society, Knoxville, Tenn.Google Scholar
Liow, L. H., Fortelius, M., Bingham, E., Lintulaakso, K., Mannila, H., Flynn, L., and Stenseth, N. C.. 2008. Higher origination and extinction rates in larger mammals. Proceedings of the National Academy of Sciences USA 105:6097–6102.CrossRefGoogle ScholarPubMed
Lockwood, R. 2005. Body size, extinction events, and the early Cenozoic record of veneroid bivalves: a new role for recoveries? Paleobiology 31:578.CrossRefGoogle Scholar
Lyons, S. K., Smith, F. A., and Brown, J. H.. 2004. Of mice, mastodons and men: human-mediated extinctions on four continents. Evolutionary Ecology Research 6:339–358.Google Scholar
Marshall, C. R. 1997. Confidence intervals on stratigraphic ranges with nonrandom distributions of fossil horizons. Paleobiology 23:165–173.CrossRefGoogle Scholar
Martins, M. J. F., Puckett, T. M., Lockwood, R., Swaddle, J. P., and Hunt, G.. 2018. High male sexual investment as a driver of extinction in fossil ostracods. Nature 556:366–369.CrossRefGoogle ScholarPubMed
Maurer, B. A., Brown, J. H., and Rusler, R. D.. 1992. The micro and macro in body size evolution. Evolution 46:939–953.CrossRefGoogle ScholarPubMed
McKinney, M. L. 1997. Extinction vulnerability and selectivity: combining ecological and paleontological views. Annual Review of Ecology and Systematics 28:495–516.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
Nichols, J. D., and Pollock, K. H.. 1983. Estimating taxonomic diversity, extinction rates, and speciation rates from fossil data using capture-recapture models. Paleobiology 9:150–163.CrossRefGoogle Scholar
Nichols, J. D., Morris, R. W., Brownie, C., and Pollock, K. H.. 1986. Sources of variation in extinction rates, turnover, and diversity of marine invertebrate families during the Paleozoic. Paleobiology 4:421–432.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
Olden, J. D., Hogan, Z. S., and Vander Zanden, M. J.. 2007. Small fish, big fish, red fish, blue fish: size-biased extinction risk of the world's freshwater and marine fishes. Global Ecology and Biogeography 16:694–701.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 Finnegan, S.. 2007. The effect of geographic range on extinction risk during background and mass extinction. Proceedings of the National Academy of Sciences USA 104:10506–10511.CrossRefGoogle ScholarPubMed
Payne, J. L., Bush, A. M., Heim, N. A., Knope, M. L., and McCauley, D. J.. 2016. Ecological selectivity of the emerging mass extinction in the oceans. Science 353:1284–1286.CrossRefGoogle ScholarPubMed
Peters, S. E., and Heim, N. A.. 2011. Macrostratigraphy and macroevolution in marine environments: testing the common-cause hypothesis. Geological Society of London Special Publication 358:95–104.CrossRefGoogle Scholar
Powell, M. G. 2008. Timing and selectivity of the Late Mississippian mass extinction of brachiopod genera from the Central Appalachian Basin. Palaios 23:525–534.CrossRefGoogle Scholar
Pradel, R. 1996. Utilization of capture-mark-recapture for the study of recruitment and population growth rate. Biometrics 52:703–709.CrossRefGoogle Scholar
Raup, D. M. 1986. Biological extinction in earth history. Science 231:1528–1533.CrossRefGoogle ScholarPubMed
Raup, D. M., and Sepkoski, J. J.. 1982. Mass extinctions in the marine fossil record. Science 215:1501–1503.CrossRefGoogle ScholarPubMed
R Core Team. 2018. R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org, accessed 15 January 2018.Google Scholar
Ripple, W. J., Wolf, C., Newsome, T. M., Hoffmann, M., Wirsing, A. J., and McCauley, D. J.. 2017. Extinction risk is most acute for the world's largest and smallest vertebrates. Proceedings of the National Academy of Sciences USA 114:201702078.CrossRefGoogle ScholarPubMed
Rivadeneira, M. M., and Marquet, P. A.. 2007. Selective extinction of late Neogene bivalves on the temperate Pacific coast of South America. Paleobiology 33:455–468.CrossRefGoogle Scholar
RStudio Team. 2016. RStudio: integrated development for R. http://www.rstudio.com, accessed 15 January 2018.Google Scholar
Rudwick, M. J. S. 1997. Georges Cuvier, fossil bones, and geological catastrophes: new translations and interpretations of the primary texts. University of Chicago Press, Chicago.CrossRefGoogle Scholar
Seber, G. A. F. 1965. A note on multiple-recapture census. Biometrika 52:249–259.CrossRefGoogle ScholarPubMed
Sessa, J. A., Patzkowsky, M. E., and Bralower, T. J.. 2009. The impact of lithification on the diversity, size distribution, and recovery dynamics of marine invertebrate assemblages. Geology 37:115–118.CrossRefGoogle Scholar
Smith, J. T., and Roy, K.. 2006. Selectivity during background extinction: Plio-Pleistocene scallops in California. Paleobiology 32:408–416.CrossRefGoogle Scholar
Smith, F. A., Elliott Smith, R. E., Lyons, S. K., and Payne, J. L.. 2018. Body size downgrading of mammals over the late Quaternary. Science 360:310–313.CrossRefGoogle ScholarPubMed
Strauss, D., and Sadler, P. M.. 1989. Classical confidence intervals and Bayesian probability estimates for ends of local taxon ranges. Mathematical Geology 21:411–427.CrossRefGoogle Scholar
Strona, G., Galli, P., Montano, S., Seveso, D., and Fattorini, S.. 2012. Global-scale relationships between colonization ability and range size in marine and freshwater fish. PLoS ONE 8:e49465.CrossRefGoogle Scholar
Tingley, R., Hitchmough, R. A., and Chapple, D. G.. 2013. Life-history traits and extrinsic threats determine extinction risk in New Zealand lizards. Biological Conservation 165:62–68.CrossRefGoogle Scholar
Tomiya, S. 2013. Body size and extinction risk in terrestrial mammals above the species level. American Naturalist 182:E196–E214.CrossRefGoogle ScholarPubMed
Valentine, J. W., and Jablonski, D.. 1986. Mass extinctions: sensitivity of marine larval types. Proceedings of the National Academy of Sciences USA 83:6912–6914.CrossRefGoogle ScholarPubMed
Valentine, J. W., Jablonski, D., Kidwell, S., and Roy, K.. 2006. Assessing the fidelity of the fossil record by using marine bivalves. Proceedings of the National Academy of Sciences USA 103:6599–6604.CrossRefGoogle ScholarPubMed
Wallace, A. R. 1889. Darwinism: an exposition of the theory of natural selection, with some of its applications. Macmillan and Co., London.Google Scholar
Zhang, Z., Augustin, M., and Payne, J. L.. 2015. Phanerozoic trends in brachiopod body size from synoptic data. Paleobiology 41:491–501.CrossRefGoogle Scholar