Environmental change and biotic interactions both govern the evolution of the biosphere, but the relative importance of these drivers over geological time remains largely unknown. Previous work suggests that, unlike environmental parameters, diversity dynamics differ profoundly between the Palaeozoic and post-Palaeozoic eras. Here we use the fossil record to test the hypothesis that the influence of ocean chemistry and climate on the ecological success of marine calcifiers decreased throughout the Phanerozoic eon. Marine calcifiers build skeletons of calcite or aragonite, and the precipitation of these calcium carbonate polymorphs is governed by the magnesium-to-calcium ratio and temperature in abiotic systems. We developed an environmental forcing model based on secular changes of ocean chemistry and temperature and assessed how well the model predicts the proliferation of skeletal taxa with respect to calcium carbonate polymorphs. Abiotic forcing governs the ecological success of aragonitic calcifiers from the Ordovician to the Middle Jurassic, but not thereafter. This regime shift coincides with the proliferation of calcareous plankton in the mid-Mesozoic. The deposition of biomineralizing plankton on the ocean floor buffers CO2 excursions and stabilizes Earth’s biochemical cycle, and thus mitigates the evolutionary impact of environmental change on the marine biota.
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Is the relative thickness of ammonoid septa influenced by ocean acidification, phylogenetic relationships and palaeogeographic position?
Swiss Journal of Palaeontology Open Access 18 April 2022
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Alroy, J. The shifting balance of diversity among major marine animal groups. Science 329, 1191–1194 (2010).
Bambach, R. K., Knoll, A. H. & Sepkoski, J. J. Anatomical and ecological constraints on Phanerozoic animal diversity in the marine realm. Proc. Natl Acad. Sci. USA 99, 6854–6859 (2002).
Finnegan, S., McClain, C. M., Kosnik, M. A. & Payne, J. L. Escargots through time: an energetic comparison of marine gastropod assemblages before and after the Mesozoic Marine Revolution. Paleobiology 37, 252–269 (2011).
Heim, N. A., Knope, M. L., Schaal, E. K., Wang, S. C. & Payne, J. L. Cope’s rule in the evolution of marine animals. Science 347, 867–870 (2015).
Payne, J. L., Heim, N. A., Knope, M. L. & McClain, C. R. Metabolic dominance of bivalves predates brachiopod diversity decline by more than 150 million years. Proc. R. Soc. B 281, 20133122 (2014).
Ausich, W. I. & Bottjer, D. J. Tiering in suspension-feeding communities on soft substrata throughout the Phanerozoic. Science 216, 173–174 (1982).
Vermeij, G. J. The Mesozoic marine revolution: evidence from snails, predators and grazers. Paleobiology 3, 245–258 (1977).
Vermeij, G. J. Evolution and Escalation: an Ecological History of Life (Princeton Univ. Press, 1987).
Aberhan, M., Kiessling, W. & Fürsich, F. T. Testing the role of biological interactions in the evolution of mid-Mesozoic marine benthic ecosystems. Paleobiology 32, 259–277 (2006).
Sandberg, P. A. An oscillating trend in Phanerozoic non-skeletal carbonate mineralogy. Nature 305, 19–22 (1983).
Veizer, J., Godderis, Y. & François, L. M. Evidence for decoupling of atmospheric CO2 and global climate during the Phanerozoic eon. Nature 408, 698–701 (2000).
Ridgwell, A. A Mid Mesozoic Revolution in the regulation of ocean chemistry. Mar. Geol. 217, 339–357 (2005).
Bachan, A. et al. A model for the decrease in amplitude of carbon isotope excursions across the Phanerozoic. Am. J. Sci. 317, 641–676 (2017).
Alroy, J. Accurate and precise estimates of origination and extinction rates. Paleobiology 40, 374–397 (2014).
Balthasar, U. & Cusack, M. Aragonite–calcite seas—quantifying the gray area. Geology 43, 99–102 (2015).
Hardie, L. A. Secular variation in seawater chemistry: an explanation for the coupled secular variation in the mineralogies of marine limestones and potash evaporites over the past 600 m.y. Geology 24, 279–283 (1996).
Higuchi, T., Shirai, K., Mezaki, T. & Yuyama, I. Temperature dependence of aragonite and calcite skeleton formation by a scleractinian coral in low mMg/Ca seawater. Geology 45, 1087–1090 (2017).
Ramajo, L., Rodríguez-Navarro, A. B., Duarte, C. M., Lardies, M. A. & Lagos, N. A. Shifts in shell mineralogy and metabolism of Concholepas concholepas juveniles along the Chilean coast. Mar. Freshw. Res. 66, 1147–1157 (2015).
Ries, J. Review: geological and experimental evidence for secular variation in seawater Mg/Ca (calcite–aragonite seas) and its effects on marine biological calcification. Biogeosciences 7, 2795 (2010).
Harper, E. M., Palmer, T. J. & Alphey, J. Evolutionary response by bivalves to changing Phanerozoic sea-water chemistry. Geol. Mag. 134, 403–407 (1997).
Porter, S. Calcite and aragonite seas and the de novo acquisition of carbonate skeletons. Geobiology 8, 256–277 (2010).
Demicco, R. V., Lowenstein, T. K., Hardie, L. A. & Spencer, R. J. Model of seawater composition for the Phanerozoic. Geology 33, 877–880 (2005).
Veizer, J. & Prokoph, A. Temperatures and oxygen isotopic composition of Phanerozoic oceans. Earth-Sci. Rev. 146, 92–104 (2015).
Hannisdal, B., Henderiks, J. & Liow, L. H. Long‐term evolutionary and ecological responses of calcifying phytoplankton to changes in atmospheric CO2. Glob. Change Biol. 18, 3504–3516 (2012).
Kiessling, W., Aberhan, M. & Villier, L. Phanerozoic trends in skeletal mineralogy driven by mass extinctions. Nat. Geosci. 1, 527–530 (2008).
Foote, M., Crampton, J. S., Beu, A. G. & Nelson, C. S. Aragonite bias, and lack of bias, in the fossil record: lithological, environmental, and ecological controls. Paleobiology 41, 245–265 (2015).
Sugihara, G. et al. Detecting causality in complex ecosystems. Science 338, 496–500 (2012).
Knoll, A. H., Bambach, R. K., Payne, J. L., Pruss, S. & Fischer, W. W. Paleophysiology and end-Permian mass extinction. Earth Planet. Sci. Lett. 256, 295–313 (2007).
Grotzinger, J. P. & Knoll, A. H. Anomalous carbonate precipitates: is the Precambrian the key to the Permian? Palaios 10, 578–596 (1995).
Langdon, C. et al. Effect of calcium carbonate saturation state on the calcification rate of an experimental coral reef. Glob. Biogeochem. Cycles 14, 639–654 (2000).
De Choudens-Sanchez, V. & Gonzalez, L. A. Calcite and aragonite precipitation under controlled instantaneous supersaturation: elucidating the role of CaCO3 saturation state and Mg/Ca ratio on calcium carbonate polymorphism. J. Sediment. Res. 79, 363–376 (2009).
Webb, G. E. Was Phanerozoic reef history controlled by the distribution of non‐enzymatically secreted reef carbonates (microbial carbonate and biologically induced cement)? Sedimentology 43, 947–971 (1996).
Bown, P. R., Lees, J. A. & Young, J. R. in Coccolithophores (eds Thierstein, H. R. & Young, J. R.) 481–508 (Springer, 2004).
Ridgwell, A. & Zeebe, R. E. The role of the global carbonate cycle in the regulation and evolution of the Earth system. Earth Planet. Sci. Lett. 234, 299–315 (2005).
Clapham, M. E. & Renne, P. R. Flood basalts and mass extinctions. Annu. Rev. Earth Planet. Sci. 47, 275–303 (2019).
Wignall, P. B. The Worst of Times: How Life on Earth Survived Eighty Million Years of Extinctions (Princeton Univ. Press, 2015).
Zeebe, R. E. & Westbroek, P. A simple model for the CaCO3 saturation state of the ocean: The “Strangelove,” the “Neritan,” and the “Cretan” Ocean. Geochem. Geophys. Geosyst. 4, 1104 (2003).
Hudson, W., Hart, M. B. & Smart, C. W. Palaeobiogeography of early planktonic foraminifera. Bull. Soc. Geol. Fr. 180, 27–38 (2009).
Hart, M. B., Hudson, W., Smart, C. W. & Tyszka, J. A reassessment of ‘Globigerina bathoniana’ Pazdrowa, 1969 and the palaeoceanographic significance of Jurassic planktic foraminifera from southern Poland. J. Micropalaeontol. 31, 97–109 (2012).
Suchéras-Marx, B. et al. Impact of the Middle Jurassic diversification of Watznaueria (coccolith-bearing algae) on the carbon cycle and δ13C of bulk marine carbonates. Glob. Planet. Change 86, 92–100 (2012).
Roth, P. H. Mesozoic palaeoceanography of the North Atlantic and Tethys oceans. Geol. Soc. Lond. Spec. Publ. 21, 299–320 (1986).
Alroy, J. Dynamics of origination and extinction in the marine fossil record. Proc. Natl Acad. Sci. USA 105, 11536–11542 (2008).
Clapham, M. E. Organism activity levels predict marine invertebrate survival during ancient global change extinctions. Glob. Change Biol. 23, 1477–1485 (2017).
Falkowski, P. G. et al. The evolution of modern eukaryotic phytoplankton. Science 305, 354–360 (2004).
Meyer, K., Ridgwell, A. & Payne, J. The influence of the biological pump on ocean chemistry: implications for long‐term trends in marine redox chemistry, the global carbon cycle, and marine animal ecosystems. Geobiology 14, 207–219 (2016).
Lu, W. et al. Late inception of a resiliently oxygenated upper ocean. Science 361, 174–177 (2018).
Vermeij, G. J. Escalation and its role in Jurassic biotic history. Palaeogeogr. Palaeoclimatol. Palaeoecol. 263, 3–8 (2008).
Vermeij, G. J. On escalation. Annu. Rev. Earth Planet. Sci. 41, 1–19 (2013).
Foote, M. Origination and extinction components of taxonomic diversity: Paleozoic and post-Paleozoic dynamics. Paleobiology 26, 578–605 (2000).
R Core Team R: A Language and Environment for Statistical Computing (R Foundation for Statistical Computing, 2017); https://www.R-project.org/
Cherns, L. & Wright, V. P. Quantifying the impacts of early diagenetic aragonite dissolution on the fossil record. Palaios 24, 756–771 (2009).
Balthasar, U. et al. Relic aragonite from Ordovician–Silurian brachiopods: implications for the evolution of calcification. Geology 39, 967–970 (2011).
Madin, J. S. et al. Statistical independence of escalatory ecological trends in Phanerozoic marine invertebrates. Science 312, 897–900 (2006).
Hannisdal, B., Haaga, K. A., Reitan, T., Diego, D. & Liow, L. H. Common species link global ecosystems to climate change: dynamical evidence in the planktonic fossil record. Proc. R. Soc. B 284, 20170722 (2017).
Kocsis, Á. T. The R package icosa: Coarse resolution global triangular and penta-hexagonal grids based on tessellated icosahedra. R package version 0.9.81 (2017); https://CRAN.R-project.org/package=icosa
Casella, G. & Berger, R. L. Statistical Inference Vol. 2 (Duxbury Pacific Grove, 2002).
Brooks, S., Gelman, A., Jones, G. & Meng, X.-L. Handbook of Markov Chain Monte Carlo (CRC, 2011).
Plummer, M. JAGS Version 3.3.0 User Manual (International Agency for Research on Cancer, 2012).
Su, Y. & Yajima, M. R2jags: Using R to run ‘JAGS’. R package version 0.5–7 (2015); https://CRAN.R-project.org/package=R2jags
Faraway, J. J. Linear Models with R (CRC, 2014).
Pinheiro, J. et al. nlme: Linear and Nonlinear Mixed Effects Models. R package version 3.1-131 (2017); https://CRAN.R-project.org/package=nlme
Davison, A. C. Statistical Models Vol. 11 (Cambridge Univ. Press, 2003).
Kramer, M. R 2 statistics for mixed models. In 17th Annual Kansas State Univ. Conf. Appl. Stat. Agric. (ed. Boyer, J. E. Jr) 24–26 (New Prairie, 2005).
Magee, L. R 2 measures based on Wald and likelihood ratio joint significance tests. Am. Stat. 44, 250–253 (1990).
Ye, H., Clark, A., Deyle, E., Keyes, O. & Sugihara, G. rEDM: Applications of empirical dynamic modeling from time series. R Package Version 0.5 7 (2017); https://CRAN.R-project.org/package=rEDM
Theiler, J., Eubank, S., Longtin, A., Galdrikian, B. & Farmer, J. D. Testing for nonlinearity in time series: the method of surrogate data. Physica D 58, 77–94 (1992).
Alroy, J. A more precise speciation and extinction rate estimator. Paleobiology 41, 633–639 (2015).
Sanders, H. L. Marine benthic diversity: a comparative study. Am. Nat. 102, 243–282 (1968).
Alroy, J. et al. Phanerozoic trends in the global diversity of marine invertebrates. Science 321, 97–100 (2008).
Cleveland, W. S., Grosse, E., Shyu, W. M., Chambers, J. M. & Hastie, J. T. in Statistical Models in S (ed. Hastie, J. T.) Ch. 8 (Routledge, 1992).
Kocsis, Á. T., Reddin, C. J., Alroy, J. & Kiessling, W. The R package divDyn for quantifying diversity dynamics using fossil sampling data. Methods Ecol. Evol. 10, 735–743 (2019).
This project was supported by the University of Plymouth (K.E., U.B., C.W.S. and J.S.), by the Trond Mohn Foundation (funding to K.A.H.) and by the Deutsche Forschungsgemeinschaft (KI 806/16-1, funding to W.K.). We thank all contributors to the PBDB, and D. Diego for discussions on pullback attractor formalism and CCM interpretations. We are grateful to J. Crampton and A. Hood for their comments on an earlier version of this manuscript. This is Paleobiology Database publication no. 344.
The authors declare no competing interests.
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Eichenseer, K., Balthasar, U., Smart, C.W. et al. Jurassic shift from abiotic to biotic control on marine ecological success. Nat. Geosci. 12, 638–642 (2019). https://doi.org/10.1038/s41561-019-0392-9
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