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Diversity dynamics of Phanerozoic terrestrial tetrapods at the local-community scale

Abstract

The fossil record provides one of the strongest tests of the hypothesis that diversity within local communities is constrained over geological timescales. Constraints to diversity are particularly controversial in modern terrestrial ecosystems, yet long-term patterns are poorly understood. Here we document patterns of local richness in Phanerozoic terrestrial tetrapods using a global data set comprising 145,332 taxon occurrences from 27,531 collections. We show that the local richness of non-flying terrestrial tetrapods has risen asymptotically since their initial colonization of land, increasing at most threefold over the last 300 million years. Statistical comparisons support phase-shift models, with most increases in local richness occurring: (1) during the colonization of land by vertebrates, concluding by the late Carboniferous; and (2) across the Cretaceous/Paleogene boundary. Individual groups, such as mammals, lepidosaurs and dinosaurs also experienced early increases followed by periods of stasis often lasting tens of millions of years. Mammal local richness abruptly tripled across the Cretaceous/Paleogene boundary, but did not increase over the next 66 million years. These patterns are consistent with the hypothesis that diversity is constrained at the local-community scale.

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Fig. 1: Patterns of local richness for Phanerozoic terrestrial non-flying tetrapods and time series of key fossil-record sampling metrics.
Fig. 2: Comparison between the empirical curve of local species richness (quantile = 0.9) for terrestrial tetrapods and simulated null distributions.
Fig. 3: Residual sums of squares for simulated null distributions of local richness (quantile = 0.9) using Phanerozoic, pre-/post-K/Pg and era pools.
Fig. 4: Rarefaction curves of local richness (quantile = 0.95) per period bin for terrestrial tetrapods.
Fig. 5: Clade-level patterns of local species richness.
Fig. 6: Rarefaction curves of local richness (quantile = 0.95) per period bin for major tetrapod subclades (non-avian dinosaurs, non-chiropteran mammaliamorphs and squamates).

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Data availability

The data used in this study were downloaded from the PaleoDB (http://www.paleobiodb.org) and have been archived, together with all custom analysis scripts, on Dryad (https://doi.org/10.5061/dryad.3v0p84v).

References

  1. Benton, M. J. Diversification and extinction in the history of life. Science 268, 52–58 (1995).

    Article  CAS  Google Scholar 

  2. Alroy, J. in Speciation and Patterns of Diversity (eds Butlin, R. et al.) (Cambridge Univ. Press, Cambridge, 2009).

    Google Scholar 

  3. Benton, M. J. & Emerson, B. C. How did life become so diverse? The dynamics of diversification according to the fossil record and molecular phylogenetics. Palaeontology 50, 23–40 (2007).

    Article  Google Scholar 

  4. Kalmar, A. & Currie, D. J. The completeness of the continental fossil record and its impact on patterns of diversification. Paleobiology 36, 51–60 (2010).

    Article  Google Scholar 

  5. Vermeij, G. J. & Grosberg, R. K. The great divergence: when did diversity on land exceed that in the sea? Integr. Comp. Biol. 50, 675–682 (2010).

    Article  Google Scholar 

  6. Harmon, L. J. & Harrison, S. Species diversity is dynamic and unbounded at local and continental scales. Am. Nat. 185, 584–593 (2015).

    Article  Google Scholar 

  7. Benson, R. B. J. et al. Near-stasis in the long-term diversification of Mesozoic tetrapods. PLoS Biol. 14, e1002359 (2016).

    Article  Google Scholar 

  8. Rabosky, D. L. & Hurlbert, A. H. Species richness at continental scales is dominated by ecological limits. Am. Nat. 185, 572–583 (2015).

    Article  Google Scholar 

  9. Liow, L. H. & Finarelli, J. A. A dynamic global equilibrium in carnivoran diversification over 20 million years. Proc. Biol. Sci. 281, 20132312 (2014).

    Article  Google Scholar 

  10. Close, R. A., Benson, R. B. J., Upchurch, P. & Butler, R. J. Controlling for the species-area effect supports constrained long-term Mesozoic terrestrial vertebrate diversification. Nat. Commun. 8, 15381 (2017).

    Article  CAS  Google Scholar 

  11. Cantalapiedra, J. L., Domingo, M. S. & Domingo, L. Multi-scale interplays of biotic and abiotic drivers shape mammalian sub-continental diversity over millions of years. Sci. Rep. 8, 13413 (2018).

    Article  Google Scholar 

  12. Bambach, R. K. Species richness in marine benthic habitats through the Phanerozoic. Paleobiology 3, 152–167 (1977).

    Article  Google Scholar 

  13. Wiens, J. J. The causes of species richness patterns across space, time, and clades and the role of ‘ecological limits’. Q. Rev. Biol. 86, 75–96 (2011).

    Article  Google Scholar 

  14. Alroy, J. Limits to species richness in terrestrial communities. Ecol. Lett. 21, 1781–1789 (2018).

    Article  Google Scholar 

  15. Davis, E. B. Mammalian beta diversity in the Great Basin, western USA: palaeontological data suggest deep origin of modern macroecological structure. Glob. Ecol. Biogeogr. 14, 479–490 (2005).

    Article  Google Scholar 

  16. Vavrek, M. J. & Larsson, H. C. E. Low beta diversity of Maastrichtian dinosaurs of North America. Proc. Natl Acad. Sci. USA 107, 8265–8268 (2010).

    Article  CAS  Google Scholar 

  17. Primack, R. B. et al. Biodiversity gains? The debate on changes in local- vs global-scale species richness. Biol. Conserv. 219, A1–A3 (2018).

    Article  Google Scholar 

  18. Cardinale, B. J., Gonzalez, A., Allington, G. R. H. & Loreau, M. Is local biodiversity declining or not? A summary of the debate over analysis of species richness time trends. Biol. Conserv. 219, 175–183 (2018).

    Article  Google Scholar 

  19. Sepkoski, J. J. Jr. A kinetic model of Phanerozoic taxonomic diversity. III. Post-Paleozoic families and mass extinctions. Paleobiology 10, 246–267 (1984).

    Article  Google Scholar 

  20. Alroy, J. Dynamics of origination and extinction in the marine fossil record. Proc. Natl Acad. Sci. USA 105(Suppl 1), 11536–11542 (2008).

    Article  CAS  Google Scholar 

  21. Knoll, A. H in Community Ecology (eds Diamond, J. & Case, T. J.) (Harper and Row, New York, 1986).

    Google Scholar 

  22. Powell, M. G. & Kowalewski, M. Increase in evenness and sampled alpha diversity through the Phanerozoic: comparison of early Paleozoic and Cenozoic marine fossil assemblages. Geology 30, 331 (2002).

    Article  Google Scholar 

  23. Stucky, R. K. Evolution of land mammal diversity in North America during the Cenozoic. Curr. Mammal. 2, 375–432 (1990).

    Google Scholar 

  24. Barry, J. C. et al. Faunal and environmental change in the late Miocene Siwaliks of northern Pakistan. Paleobiology 28, 1–71 (2002).

    Article  Google Scholar 

  25. Brocklehurst, N., Upchurch, P., Mannion, P. D. & O’Connor, J. K. The completeness of the fossil record of Mesozoic birds: implications for early avian evolution. PLoS ONE 7, e39056 (2012).

    Article  CAS  Google Scholar 

  26. The Paleobiology Database (PDBD, accessed 18 January 2019); https://paleobiodb.org/#/

  27. Alroy, J. The fossil record of North American mammals: evidence for a Paleocene evolutionary radiation. Syst. Biol. 48, 107–118 (1999).

    Article  CAS  Google Scholar 

  28. Wilson, G. P., Clemens, W. A., Horner, J. R. & Hartman, J. H. Through the End of the Cretaceous in the Type Locality of the Hell Creek Formation in Montana and Adjacent Areas. Vol. 503 (Geological Society of America, Boulder, 2014).

    Book  Google Scholar 

  29. Tóth, A. B., Lyons, S. K. & Behrensmeyer, A. K. A century of change in Kenya’s mammal communities: increased richness and decreased uniqueness in six protected areas. PLoS ONE 9, e93092 (2014).

    Article  Google Scholar 

  30. Wall, P. D., Ivany, L. C. & Wilkinson, B. H. Impact of outcrop area on estimates of Phanerozoic terrestrial biodiversity trends. Geol. Soc. London Spec. Publ. 358, 53–62 (2011).

    Article  Google Scholar 

  31. Holland, S. M. The non-uniformity of fossil preservation. Philos. Trans. R. Soc. Lond., B, Biol. Sci. 371, 20150130 (2016).

    Article  Google Scholar 

  32. Benton, M. J. Origins of biodiversity. PLoS Biol. 14, e2000724 (2016).

    Article  Google Scholar 

  33. Mateo, R. G., Mokany, K. & Guisan, A. Biodiversity models: what if unsaturation is the rule? Trends Ecol. Evol. 32, 556–566 (2017).

    Article  Google Scholar 

  34. Lyons, S. K. et al. Holocene shifts in the assembly of plant and animal communities implicate human impacts. Nature 529, 80–83 (2016).

    Article  Google Scholar 

  35. Hubbell, S. P The Unified Neutral Theory of Biodiversity and Biogeography (MPB-32) (Princeton Univ. Press, Princeton, 2011).

    Book  Google Scholar 

  36. Connell, J. H. Diversity in tropical rain forests and coral reefs. Science 199, 1302–1310 (1978).

    Article  CAS  Google Scholar 

  37. Huston, M. A general hypothesis of species diversity. Am. Nat. 113, 81–101 (1979).

    Article  Google Scholar 

  38. Benson, R. B. J. & Mannion, P. D. Multi-variate models are essential for understanding vertebrate diversification in deep time. Biol. Lett. 8, 127–130 (2012).

    Article  Google Scholar 

  39. Benson, R. B. J. & Upchurch, P. Diversity trends in the establishment of terrestrial vertebrate eco­systems: interactions between spatial and temporal sampling biases. Geology 41, 43–46 (2013).

    Article  Google Scholar 

  40. Hyndman, R. J. & Khandakar, Y. Automatic time series forecasting: the forecast package for R. J. Stat. Softw. 27, 1–22 (2008).

    Article  Google Scholar 

  41. Alroy, J. et al. Phanerozoic trends in the global diversity of marine invertebrates. Science 321, 97–100 (2008).

    Article  CAS  Google Scholar 

  42. Sessa, J. A., Patzkowsky, M. E. & Bralower, T. J. The impact of lithification on the diversity, size distribution, and recovery dynamics of marine invertebrate assemblages. Geology 37, 115–118 (2009).

    Article  Google Scholar 

  43. Hendy, A. J. W. The influence of lithification on Cenozoic marine biodiversity trends. Paleobiology 35, 51–62 (2009).

    Article  Google Scholar 

  44. Jass, C. N. & George, C. O. An assessment of the contribution of fossil cave deposits to the Quaternary paleontological record. Quat. Int. 217, 105–116 (2010).

    Article  Google Scholar 

  45. Allison, P. A. & Briggs, D. E. G. Paleolatitudinal sampling bias, Phanerozoic species diversity, and the end-Permian extinction. Geology 21, 65–68 (1993).

    Article  Google Scholar 

  46. Noto, C. R. in Taphonomy (eds Allison, P. A. & Bottjer, D. J.) (Springer, Dordrecht, 2010).

    Google Scholar 

  47. Behrensmeyer, A. K., Kidwell, S. M. & Gastaldo, R. A. Taphonomy and paleobiology. Paleobiology 26, 103–147 (2000).

    Article  Google Scholar 

Download references

Acknowledgements

We thank all contributors to the PaleoDB. This is PaleoDB official publication #334. This research was funded by the European Union’s Horizon 2020 research and innovation programme under grant agreement no. 637483 (ERC Starting Grant TERRA, R.J.B.). P.D.M. was supported by a Leverhulme Trust Early Career Fellowship (no. ECF-2014-662) and a Royal Society University Research Fellowship (no. UF160216).

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R.A.C., R.B.J.B. and R.J.B. conceived the study. J.A., A.K.B., J.B., R.B.J.B., R.J.B., M.T.C., T.J.C., E.M.D., P.D.M. and M.D.U. contributed to the data set. R.A.C. designed and conducted the analyses and wrote the manuscript. R.B.J.B., J.A. and M.T.C. provided methodological advice. R.J.B. and R.B.J.B. drafted portions of the manuscript. All authors provided critical comments on the manuscript.

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Correspondence to Roger A. Close.

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Close, R.A., Benson, R.B.J., Alroy, J. et al. Diversity dynamics of Phanerozoic terrestrial tetrapods at the local-community scale. Nat Ecol Evol 3, 590–597 (2019). https://doi.org/10.1038/s41559-019-0811-8

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