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The long-term ecology and evolution of marine reptiles in a Jurassic seaway

Nature Ecology & Evolution volume 2, pages 1548–1555 (2018)Cite this article

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Abstract

Marine reptiles flourished in the Mesozoic oceans, filling ecological roles today dominated by crocodylians, large fish, sharks and cetaceans. Many groups of these reptiles coexisted for over 50 million years (Myr), through major environmental changes. However, little is known about how the structure of their ecosystems or their ecologies changed over millions of years. We use the most common marine reptile fossils—teeth—to establish a quantitative system that assigns species to dietary guilds and then track the evolution of these guilds over the roughly 18-million-year history of a single seaway, the Jurassic Sub-Boreal Seaway of the United Kingdom. Groups did not significantly overlap in guild space, indicating that dietary niche partitioning enabled many species to live together. Although a highly diverse fauna was present throughout the history of the seaway, fish and squid eaters with piercing teeth declined over time while hard-object and large-prey specialists diversified, in concert with rising sea levels. High niche partitioning and spatial variation in dietary ecology related to sea depth also characterize modern marine tetrapod faunas, indicating a conserved ecological structure of the world’s oceans that has persisted for over 150 Myr.

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Fig. 1: Morphospace plots showing the distribution of marine reptile specimens based on tooth morphology.
Fig. 2: Morphospace plots showing the distribution of marine reptile clades based on tooth morphology through time.
Fig. 3: Partial disparity of Jurassic Sub-Boreal Seaway marine reptiles, mapped against global sea level.

References

  1. Pyenson, N. D., Kelley, N. P. & Parham, J. F. Marine tetrapod macroevolution: physical and biological drivers on 250 Ma of invasions and evolution in ocean ecosystems. Palaeogeogr. Palaeoclimatol. Palaeoecol. 400, 1–8 (2014).

    Article  Google Scholar 

  2. Kelley, N. P. & Pyenson, N. D. Evolutionary innovation and ecology in marine tetrapods from the Triassic to the Anthropocene. Science 348, aaa3716 (2015).

    Article  CAS  PubMed  Google Scholar 

  3. Benson, R. B. J., Butler, R. J., Lindgren, J. & Smith, A. S. Mesozoic marine tetrapod diversity: mass extinctions and temporal heterogeneity in geological megabiases affecting vertebrates. Proc. R. Soc. B 277, 829–834 (2010).

    Article  PubMed  Google Scholar 

  4. Ciampaglio, C. N., Wray, G. A. & Corliss, B. H. A toothy tale of evolution: convergence in tooth morphology among marine Mesozoic–Cenozoic sharks, reptiles, and mammals. Sediment. Rec. 3, 4–8 (2005).

    Article  Google Scholar 

  5. Andrews, C. W. A Descriptive Catalogue of the Marine Reptiles of the Oxford Clay: Part I (British Museum (Natural History), London, 1909).

  6. Andrews, C. W. A Descriptive Catalogue of the Marine Reptiles of the Oxford Clay: Part II (British Museum (Natural History), London, 1913).

  7. Massare, J. A. Tooth morphology and prey preference of Mesozoic marine reptiles. J. Vertebr. Paleontol. 7, 121–137 (1987).

    Article  Google Scholar 

  8. Massare, J. A. Swimming capabilities of Mesozoic marine reptiles: implications for method of predation. Paleobiology 14, 187–205 (1988).

    Article  Google Scholar 

  9. Buchy, M.-C. Morphologie dentaire et régime alimentaire des reptiles marins du Mésozoïque: revue critique et réévaluation. Oryctos 9, 49–82 (2010).

    Google Scholar 

  10. Chiarenza, A. A. et al. The youngest record of metriorhynchid crocodylomorphs, with implications for the extinction of Thalattosuchia. Cretaceous Res. 56, 608–616 (2015).

    Article  Google Scholar 

  11. Stubbs, T. L. & Benton, M, J. Ecomorphological diversifications of Mesozoic marine reptiles: the roles of ecological opportunity and extinction. Paleobiology 42, 547–573 (2016).

    Article  Google Scholar 

  12. Fischer, V., Bardet, N., Benson, R. J. B., Arkhangelsky, M. S. & Friedman, M. Extinction of fish-shaped marine reptiles associated with reduced evolutionary rates and global environmental volatility. Nat. Commun. 7, 10825 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Kelley, N. P. & Motani, R. Trophic convergence drives morphological convergence in marine tetrapods. Biol. Lett. 11, 20140709 (2015).

    Article  PubMed  PubMed Central  Google Scholar 

  14. Young, M. T. et al. The cranial osteology and feeding ecology of the metriorhynchid crocodylomorph genera Dakosaurus and Plesiosuchus from the Late Jurassic of Europe. PLoS ONE 7, e44985 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Young, M. T., Brusatte, S. L., Andrade, M. B., Beatty, L. & Desojo, J. B. Tooth-on-tooth interlocking occlusion suggests macrophagy in the Mesozoic marine crocodylomorph Dakosaurus. Anat. Rec. 295, 1147–1158 (2012).

    Article  Google Scholar 

  16. Benson, R. B. J. & Druckenmiller, P. S. Faunal turnover of marine tetrapods during the Jurassic–Cretaceous transition. Biol. Rev. 89, 1–23 (2014).

    Article  PubMed  Google Scholar 

  17. Young, M. T. Filling the ‘Corallian Gap’: re-description of a metriorhynchid crocodylomorph from the Oxfordian (Late Jurassic) of Headington, England. Hist. Biol. 26, 80–90 (2014).

    Article  Google Scholar 

  18. Fischer, V. et al. Peculiar macrophagous adaptations in a new Cretaceous pliosaurid. R. Soc. Open Sci. 2, 150552 (2015).

    Article  PubMed  PubMed Central  Google Scholar 

  19. Fischer, V. et al. Plasticity and convergence in the evolution of short-necked plesiosaurs. Curr. Biol. 27, 1667–1676 (2017).

    Article  CAS  PubMed  Google Scholar 

  20. Cox, B. M. in British Upper Jurassic Stratigraphy (eds Wright, J. K. & Cox, B. M.) Ch. 1, 3–10 (Geological Conservation Review Series 21, Joint Nature Conservation Committee, Peterborough, 2001).

  21. Cope, J. C. in The Geology of England and Wales 2nd edn (eds Brenchley, P. J. & Rawson, P. F.) 325–364 (Geological Society, London, 2006).

  22. Foffa, D., Young, M. T. & Brusatte, S. L. Filling the Corallian gap: new information on Late Jurassic marine reptile faunas from England. Acta Palaeontol. Pol. 63, 287–313 (2018).

    Article  Google Scholar 

  23. Cecca, F., Garin, B. M., Marchand, D., Lathuiliere, B. & Bartolini, A. Paleoclimatic control of biogeographic and sedimentary events in Tethyan and peri-Tethyan areas during the Oxfordian (Late Jurassic). Palaeogeogr. Palaeoclimatol. Palaeoecol. 222, 10–32 (2005).

    Article  Google Scholar 

  24. Armstrong, H. A. et al. Hadley circulation and precipitation changes controlling black shale deposition in the Late Jurassic Boreal Seaway. Paleoceanography 31, 1041–1053 (2016).

    Article  Google Scholar 

  25. Cox, B. M., Hudson, J. D. & Martill, D. M. Lithostratigraphic nomenclature of the Oxford Clay (Jurassic). Proc. Geol. Assoc. 103, 343–345 (1992).

    Article  Google Scholar 

  26. Mettam, C., Johnson, A. L. A., Nunn, E. V. & Schӧne, B. R. Stable isotope (δ18O and δ13C) sclerochronology of Callovian (Middle Jurassic) bivalves (Gryphaea (Bilobissa) dilobotes) and belemnites (Cylindroteuthis puzosiana) from the Peterborough Member of the Oxford Clay Formation (Cambridgeshire, England): evidence of palaeoclimate, water depth and belemnite behaviour. Palaeogeogr. Palaeoclimatol. Palaeoecol. 399, 187–201 (2014).

    Article  Google Scholar 

  27. Dromart, G. et al. Perturbation of the carbon cycle at the Middle–Late Jurassic transition: geological and geochemical evidence. Am. J. Sci. 303, 667–707 (2003).

    Article  CAS  Google Scholar 

  28. Dromart, G. et al. Ice age at the Middle–Late Jurassic transition? Earth Planet. Sci. Lett. 213, 205–220 (2003).

    Article  CAS  Google Scholar 

  29. Gallois, R. W. The Kimmeridge Clay: the most intensively studied formation in Britain. J. Open Univ. Geol. Soc. 25, 33–38 (2004).

    Google Scholar 

  30. Haq, B. U., Hardenbol, J. & Vail, P. R. in Sea Level Changes—An Integrated Approach (eds Wilgus, C. K. et al.) 71–108 (Special Publication 42, SEPM, Tulsa, 1988).

  31. Pauly, D., Trites, A. W., Capuli, E. & Christensen, V. Diet composition and trophic levels of marine mammals. ICES J. Mar. Sci. 55, 467–481 (1998).

    Article  Google Scholar 

  32. Esteban, R. et al. Identifying key habitat and seasonal patterns of a critically endangered population of killer whales. J. Mar. Biol. Assoc. UK 94, 1317–1325 (2013).

    Article  Google Scholar 

  33. Forney, K. A. Environmental models of cetacean abundance: reducing uncertainty in population trends. Conserv. Biol. 14, 1271–1286 (2000).

    Article  Google Scholar 

  34. Yen, P. P. W., Sydeman, W. J. & Hyrenbach, K. D. Marine birds and cetacean associations with bathymetric habitats and shallow-water topographies: implications for trophic transfer and conservation. J. Mar. Syst. 50, 79–99 (2004).

    Article  Google Scholar 

  35. Balance, L. T., Pitman, R. L. & Fiedler, P. C. Oceanographic influences on seabirds and cetaceans in the eastern tropical Pacific: a review. Prog. Oceanogr. 69, 360–390 (2006).

    Article  Google Scholar 

  36. MacLoed, C. D., Weit, C. R., Pierpoint, C. & Harland, E. J. The habitat preferences of marine mammals west of Scotland (UK). J. Mar. Biol. Assoc. UK 87, 157–164 (2007).

    Article  Google Scholar 

  37. Spitz, J. et al. Prey preferences among the community of deep-diving odontocetes from the Bay of Biscay, Northeast Atlantic. Deep Sea Res. Pt I 58, 273–282 (2011).

    Article  Google Scholar 

  38. Weir, C. R., MacLeod, C. D. & Pierce, G. J. Habitat preferences and evidence for niche partitioning amongst cetaceans in the waters between Gabon and Angola, eastern tropical Atlantic. J. Mar. Biol. Assoc. UK 92, 1735–1749 (2012).

    Article  Google Scholar 

  39. Roberts, J. J. et al. Habitat-based cetacean density models for the U.S. Atlantic and Gulf of Mexico. Sci. Rep. 6, 22615 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Fossete, S. et al. Resource partitioning facilitates coexistence in sympatric cetaceans in the California Current. Ecol. Evol. 7, 9085–9097 (2017).

    Article  Google Scholar 

  41. Larson, D. W., Brown, C. M. & Evans, D. C. Dental disparity and ecological stability in bird-like dinosaurs prior to the end-Cretaceous mass extinction. Curr. Biol. 26, 1325–1333 (2016).

    Article  CAS  PubMed  Google Scholar 

  42. Smith, J. B., Vann, D. R. & Dodson, P. Dental morphology and variation in theropod dinosaurs: implications for the taxonomic identification of isolated teeth. Anat. Rec. Pt A 285, 699–736 (2005).

    Article  Google Scholar 

  43. Noè, L. F. A Taxonomic and Functional Study of the Callovian (Middle Jurassic) Pliosauroidea (Reptilia, Sauropterygia). PhD thesis, Univ. Derby (2001).

  44. Sassoon, J., Foffa, D. & Marek, R. Dental ontogeny and replacement in Pliosauridae. R. Soc. Open Sci. 2, 150384 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Foffa, D., Young, M. T., Brusatte, S. L., Graham, M. R. & Steel, L. A new metriorhynchid crocodylomorph from the Oxford Clay Formation (Middle Jurassic) of England, with implications for the origin and diversification of Geosaurini. J. System. Palaeontol. 16, 1123–1143 (2018).

    Article  Google Scholar 

  46. Young, M. T., Hastings, A. K., Allain, R. & Smith, T. J. Revision of the enigmatic crocodyliform Elosuchus felixi de Lapparent de Broin, 2002 from the Lower–Upper Cretaceous boundary of Niger: potential evidence for an early origin of the clade Dyrosauridae. Zool. J. Linn. Soc. 179, 377–403 (2017).

    Google Scholar 

  47. Schneider, C. A., Rasband, W. S. & Eliceiri, K. W. NIH Image to ImageJ: 25 years of image analysis. Nat. Methods 9, 671–675 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. Anderson, P. S. L., Friedman, M., Brazeau, M. D. & Rayfield, E. J. Initial radiation of jaws demonstrated stability despite faunal and environmental change. Nature 476, 206–209 (2011).

    Article  CAS  PubMed  Google Scholar 

  49. Gower, J. C. A general coefficient of similarity and some of its properties. Biometrics 27, 857–871 (1971).

    Article  Google Scholar 

  50. Hammer, Ø, Harper, D. A. T. & Ryan, P. D. PAST: paleontological statistics software package for education and data analysis. Palaeontol. Electron 4, 1–9 (2001).

    Google Scholar 

  51. Anderson, M. J. A new method for non-parametric multivariate analysis of variance. Austral Ecol. 26, 32–46 (2001).

    Google Scholar 

  52. R Development Core Team. R: A Language and Environment for Statistical Computing (R Foundation for Statistical Computing, 2012).

  53. Benjamini, Y. & Hochberg, Y. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J. R. Stat. Soc. B. 57, 289–300 (1995).

    Google Scholar 

  54. Wills, M. A., Briggs, D. E. G. & Fortey, R. A. Disparity as an evolutionary index: a comparison of Cambrian and recent arthropods. Paleobiology 20, 93–130 (1994).

    Article  Google Scholar 

  55. Guillerme, T. dispRity: a modular R package for measuring disparity. Methods Ecol. Evol. 9, 1755–1763 (2018).

    Article  Google Scholar 

  56. Brusatte, L. S., Lloyd, G. T., Wang, S. C. & Norell, M. A. Gradual assembly of avian body plan culminated in rapid rates of evolution across the dinosaur–bird transition. Curr. Biol. 20, 2386–2392 (2014).

    Article  CAS  Google Scholar 

  57. Foote, M. Contributions of individual taxa to overall morphological disparity. Paleobiology 19, 403–419 (1993).

    Article  Google Scholar 

  58. Navarro, N. MDA: a MATLAB-based program for morphospace-disparity analysis. Comput. Geosci. 29, 655–664 (2003).

    Article  Google Scholar 

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Acknowledgements

We thank D. Hutchinson and I. Gladstone (BRSMG), M. Riley (CAMSM), P. Tomlinson (DORCM), N. Clark (GLAHM), S. Etches (MJML), L. Steel (NHMUK), E. Howlett and H. Ketchum (OUMNH), and E. Jarvis, S. King and S. Ogilvy (YORYM) for access and guidance during D.F.’s visits to the museum collections. D.F.’s museum visits were funded by the Small Grant Scheme ‘2015 Wood Award’ (PASW201402), Systematics Research Fund and Richard Owen Research Fund by the Palaeontographical Society. M.T.Y. and S.L.B. are supported by a Leverhulme Trust Research Project grant (RPG-2017-167), and S.L.B. is supported by a Marie Curie Career Integration Grant (630652). We thank P. dePolo for comments on the manuscript, and M. Puttick and T. Guillerme for discussion and technical support.

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Authors and Affiliations

  1. School of GeoSciences, Grant Institute, University of Edinburgh, Edinburgh, UK

    Davide Foffa, Mark T. Young, Kyle G. Dexter & Stephen L. Brusatte

  2. School of Earth Sciences, University of Bristol, Bristol, UK

    Thomas L. Stubbs

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Contributions

D.F. led the project, conceived the study and wrote the initial draft manuscript. M.T.Y. and S.L.B. helped develop the project, edited drafts and provided guidance on the statistical analyses. S.L.B. wrote the final manuscript, which was revised by all authors. D.F. designed and performed the analyses with technical support from T.L.S. and K.G.D.

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Correspondence to Davide Foffa.

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Supplementary Datasets 1-4

Specimen-character matrix; non-parametric MANOVA tests results; results of LDA group classifications; sensitivity analyses of guild groupings

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Foffa, D., Young, M.T., Stubbs, T.L. et al. The long-term ecology and evolution of marine reptiles in a Jurassic seaway. Nat Ecol Evol 2, 1548–1555 (2018). https://doi.org/10.1038/s41559-018-0656-6

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