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Subaqueous foraging among carnivorous dinosaurs - Nature.com

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Abstract

Secondary aquatic adaptations evolved independently more than 30 times from terrestrial vertebrate ancestors1,2. For decades, non-avian dinosaurs were believed to be an exception to this pattern. Only a few species have been hypothesized to be partly or predominantly aquatic3,4,5,6,7,8,9,10,11. However, these hypotheses remain controversial12,13, largely owing to the difficulty of identifying unambiguous anatomical adaptations for aquatic habits in extinct animals. Here we demonstrate that the relationship between bone density and aquatic ecologies across extant amniotes provides a reliable inference of aquatic habits in extinct species. We use this approach to evaluate the distribution of aquatic adaptations among non-avian dinosaurs. We find strong support for aquatic habits in spinosaurids, associated with a marked increase in bone density, which precedes the evolution of more conspicuous anatomical modifications, a pattern also observed in other aquatic reptiles and mammals14,15,16. Spinosaurids are revealed to be aquatic specialists with surprising ecological disparity, including subaqueous foraging behaviour in Spinosaurus and Baryonyx, and non-diving habits in Suchomimus. Adaptation to aquatic environments appeared in spinosaurids during the Early Cretaceous, following their divergence from other tetanuran theropods during the Early Jurassic17.

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Fig. 1: Osteohistology and ecological variation among amniotes, including the analysed spinosaurid taxa.
Fig. 2: Relationship between midshaft density of femur, diameter and major lifestyle among amniotes including Spinosauridae.
Fig. 3: Relationship between dorsal ribs density, diameter and major lifestyle among amniotes including Spinosauridae.

Data availability

All data described and used in this manuscript are freely available. The measurements and provenance information for fossil specimens can be found in the extended data figures and in the Supplementary Dataset. The phylogenetic datasets and the R coding are available as Supplementary Material. The CT scan datasets collected for this study are available in Morphosource (specific links for each taxon can be found in the Supplementary Dataset).

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Acknowledgements

We acknowledge P. Barrett and S. Chapman for access to the holotype of Baryonyx at the Natural History Museum, London, J. Scannella for access to thin sections of Tyrannosaurus housed at the Museum of the Rockies, and M. Fox and J. Gauthier for access to Poposaurus at the Yale Peabody Museum. The Moroccan Ministry of Energy, Mines, and the Environment is thanked for providing fieldwork permits to N. I. Members of the 2015–2019 expedition seasons are thanked for their assistance in the field. We thank J. Choiniere, P. Falkingham, S. Nesbitt and the other, anonymous, reviewer for constructive comments that improved the manuscript. Funding was received from the European Union’s Horizon 2020 research and innovation program 2014–2018, starting grant (R. B. J. B., 677774); a National Geographic Society grant (N.I., CP-143R-170); a National Geographic Emerging Explorer Grant (N.I.); the Jurassic Foundation (M.F.); the Paleontological Society grant (M.F.), as well as the Explorers Club (grant awarded to M.F.). The Lokschuppen (Rosenheim, Germany) and J. Pfauntsch provided additional financial support for fieldwork led by N.I. in Morocco.

Author information

Affiliations

  1. Negaunee Integrative Research Center, Field Museum of Natural History, Chicago, IL, USA

    Matteo Fabbri & Jingmai O’Connor

  2. Department of Earth Sciences, University of Cambridge, Cambridge, UK

    Guillermo Navalón

  3. Department of Earth Sciences, University of Oxford, Oxford, UK

    Guillermo Navalón, Roger B. J. Benson & Andrew Orkney

  4. Unidad de Paleontología, Departamento de Biología, Universidad Autónoma de Madrid, Madrid, Spain

    Guillermo Navalón

  5. CONICET, Museo Paleontológico Egidio Feruglio, Trelew, Argentina

    Diego Pol

  6. Department of Earth and Planetary Sciences and Peabody Museum of Natural History, Yale University, New Haven, CT, USA

    Bhart-Anjan S. Bhullar

  7. Department of Biological Science, Florida State University, Tallahassee, FL, USA

    Gregory M. Erickson

  8. Division of Vertebrate Paleontology, American Museum of Natural History, New York, NY, USA

    Mark A. Norell

  9. Section of Vertebrate Paleontology, Carnegie Museum of Natural History, Pittsburgh, PA, USA

    Matthew C. Lamanna

  10. Department of Geology and Health and Environment Laboratory, Hassan II University of Casablanca, Casablanca, Morocco

    Samir Zouhri

  11. Department of Biology, University of Detroit Mercy, Detroit, MI, USA

    Justine Becker & Amanda Emke

  12. Department of Physician Assistant Studies, Wayne State University, Detroit, MI, USA

    Amanda Emke

  13. Sezione di Paleontologia dei Vertebrati, Museo di Storia Naturale di Milano, Milan, Italy

    Cristiano Dal Sasso, Gabriele Bindellini, Simone Maganuco & Marco Auditore

  14. Dipartimento di Scienze della Terra ‘A. Desio’, Università degli Studi di Milano, Milan, Italy

    Gabriele Bindellini

  15. Associazione Paleontologica Paleoartistica Italiana, Parma, Italy

    Simone Maganuco

  16. School of the Environment, Geography and Geosciences, University of Portsmouth, Portsmouth, UK

    Nizar Ibrahim

Authors
  1. Matteo Fabbri
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  2. Guillermo Navalón
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  4. Diego Pol
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Contributions

Conceptualization: M.F. Data collection and curation: all authors. Data quantification: M.F. Methodology: M.F., G.N. and R.B.J.B. Formal analysis: M.F., G.N. and R.B.J.B. Resources: all authors. Writing, original draft preparation: M.F. Writing, review and editing: all authors. Visualization: M.F. and G.N.; Supervision: M.F., G.N., R.B.J.B. and N.I. Funding acquisition: M.F., R.B.J.B. and N.I.

Corresponding authors

Correspondence to Matteo Fabbri, Guillermo Navalón or Roger B. J. Benson.

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Competing interests

The authors declare no competing interests.

Peer review

Peer review information

Nature thanks Jonah Choiniere, Peter Falkingham, Sterling Nesbitt and the other, anonymous, reviewers for their contribution to the peer review of this work. Peer review reports are available.

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Extended data figures and tables

Extended Data Fig. 1 Comparative array of archosaurian femoral diaphysis included in the dataset.

Numerical values represent the bone density quantified for each taxon. Asterisks indicate femoral diaphysis that were retro-deformed before quantification of bone density due to taphonomic deformation and/or fragmentation present in the fossil.

Extended Data Fig. 2 Comparative array of non-avian and avian femoral diaphysis included in the dataset.

Numerical values represent the bone density quantified for each taxon.

Extended Data Fig. 3 Comparative array of avian and lepidosaur femoral diaphysis included in the dataset.

Numerical values represent the bone density quantified for each taxon.

Extended Data Fig. 4 Comparative array of amniote femoral diaphysis included in the dataset.

Numerical values represent the bone density quantified for each taxon.

Extended Data Fig. 5 Comparative array of mammalian femoral diaphysis included in the dataset.

Numerical values represent the bone density quantified for each taxon.

Extended Data Fig. 6 Comparative array of archosaurian dorsal rib cross sections included in the dataset.

Numerical values represent the bone density quantified for each taxon.

Extended Data Fig. 7 Comparative array of amniote dorsal rib cross sections included in the dataset.

Numerical values represent the bone density quantified for each taxon.

Extended Data Fig. 8

Bone density and femur diameter phylogenetic distribution plotted on the informal consensus tree used for discriminant analyses representing the phylogenetic relationships of the taxa included in our study.

Extended Data Fig. 9

Bone density and dorsal rib diameter phylogenetic distribution plotted on the informal consensus tree used for discriminant analyses representing the phylogenetic relationships of the taxa included in our study.

Extended Data Fig. 10 Qualitative comparison of bone compactness in selected skeletal elements between osteosclerotic spinosaurids and other non-avian dinosaurs.

Baryonyx and Spinosaurus possess dense, compact bone throughout the postcranial skeleton, namely in the neural spines, ribs, scapula, ilium, pubis, ischium, femur, and fibula. Increased bone density is found in postcranial elements of Spinosaurus as well; a reduced medullary cavity is present in the ribs, dorsal and caudal neural spines, manual phalanges, femur, tibia, and fibula. Abbreviations: bd=bone density.

Supplementary information

Supplementary Information

This file contains Supplementary Figs. 1–3 and Tables 1–10

Reporting Summary

Peer Review File

Supplementary Dataset

This folder contains the list of taxa analysed in this study; R coding; phylogenetic dataset from Malafaia et al. (2020) and phylogenetic dataset from Rauhut & Pol (2019)

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Fabbri, M., Navalón, G., Benson, R.B.J. et al. Subaqueous foraging among carnivorous dinosaurs. Nature (2022). https://ift.tt/7gA3hky

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