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Tooth histology, attachment, and replacement in the Ichthyopterygia reviewed in an evolutionary context

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Abstract

Ichthyosaurs, an extinct group of Mesozoic marine diapsids, show a relatively small range of tooth crown morphologies. With few exceptions, members of the group bear a large number of conical teeth and show only minor heterodonty within a jaw. This uniformity in gross morphology masks a high degree of variation in both the quantity and arrangement of the mineralized tooth tissues. Here, we describe tooth tissue structure and distribution in derived ichthyosaurs. We synthesize these new observations with the historical literature, to map changes in the quantity and arrangement of tooth tissues. These changes affected tooth attachment, tooth replacement, plicidentine morphology, and the amount and distribution of cellular cementum. The amount of variation detected in features relating to ichthyosaurian dentition is not surprising given the geological longevity and morphological disparity of the group, but does emphasize the importance of extensive taxon sampling in studies of tooth histology and evolution. This study is important in that it incorporates morphological and histological information in a phylogenetic and developmental context, something that is rarely done for marine reptile dentitions.

Kurzfassung

Die Ichthyosaurier, eine ausgestorbene Gruppe von mesozoischen marinen Diapsiden, zeigen nur geringe morphologische Unterschiede der Zahnkronen. Die Mitglieder der Gruppe tragen, mit wenigen Ausnahmen, eine große Anzahl von konischen Zähnen, und zeigen nur geringfügige Heterodontie innerhalb eines Kiefers. Diese Einheitlichkeit in der Gesamtmorphologie verbirgt ein großes Ausmaß an Variation, sowohl was die Anzahl als auch die Anordnung der mineralisierten Zahngewebe betrifft. In der vorliegenden Arbeit beschreiben wir die Struktur und Verteilung des Zahngewebes bei Ichthyosauriern. Wir vergleichen diese neuen Beobachtungen mit solchen aus der Literatur, um Veränderungen der Zahngewebe bei Ichthyosauriern darzustellen. Diese Veränderungen betrafen Zahnbefestigung, Zahnersatz, Plicidentin-Morphologie und die Menge und Verteilung von zellulärem Zement. Der Grad an Variabilität, der bei den Merkmalen des Ichthyosauriergebisses festgestellt wurde, ist in Anbetracht der geologische Langlebigkeit und der morphologischen Unterschiede der Gruppe nicht überraschend, unterstreicht aber die Bedeutung der umfangreichen Probenahme an Taxa bei Untersuchungen der Zahnhistologie und -entwicklung. Diese Studie ist im Hinblick darauf wichtig, dass sie morphologische und histologische Informationen in einen phylogenetischen Zusammenhang und einen Entwicklungszusammenhang setzt, was sonst nur selten bei Gebissen von Meeresreptilien getan wird.

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Abbreviations

AM:

Australian Museum

ROM:

Royal Ontario Museum

UALVP:

University of Alberta Vertebrate Paleontology

References

  • Andrews, C.W. 1910. A descriptive catalogue of the marine reptiles of the Oxford Clay. London: British Museum of Natural History.

    Google Scholar 

  • Bardet, N. 1990. Dental cross-sections in Cretaceous Ichthyopterygia: Systematic implications. Geobios 23(2): 169–172.

    Article  Google Scholar 

  • Bauer, F. 1898. Die Ichthyosaurier des oberen weissen Jura. Palaeontographica 44: 283–328.

    Google Scholar 

  • Besmer, A. 1947. Die Triasfauna der Tessiner Kalkalpen XVI. Beiträge zur Kenntnis des Ichthyosauriergebisses. Schweizerische Palaeontologische Abhandlungen 65: 1–21.

    Google Scholar 

  • Bosshardt, D.D. 2005. Are cementoblasts a subpopulation of osteoblasts or a unique phenotype? Journal of Dental Research 84(5): 390–406.

    Article  Google Scholar 

  • Caldwell, M.W. 2007. Ontogeny, anatomy and attachment of the dentition in mosasaurs (Mosasauridae: Squamata). Zoological Journal of the Linnean Society 149: 687–700.

    Article  Google Scholar 

  • Caldwell, M.W., L.A. Budney, and D.O. Lamoureux. 2003. Histology of tooth attachment tissues in the Late Cretaceous mosasaurid Platecarpus. Journal of Vertebrate Paleontology 23(3): 622–630.

    Article  Google Scholar 

  • Camp, C.L. 1980. Large ichthyosaurs from the Upper Triassic of Nevada. Palaeontographica Abt. A 170(4–6): 139–200.

    Google Scholar 

  • Davit-Béal, T. 2009. Loss of teeth and enamel in tetrapods: fossil record, genetic data and morphological adaptations. Journal of Anatomy 214: 477–501.

    Article  Google Scholar 

  • de Buffrénil, V., and J.-M. Mazin. 1990. Bone histology of the ichthyosaurs: comparative data and functional interpretation. Paleobiology 16(4): 435–447.

    Google Scholar 

  • de Ricqlès, A., and J.R. Bolt. 1983. Jaw growth and tooth replacement in Captorhinus aguti (Reptilia: Captorhinomorpha): A morphological and histological analysis. Journal of Vertebrate Paleontology 3(1): 7–24.

    Article  Google Scholar 

  • Delgado, S., T. Davit-Béal, F. Allizard, and J.-Y. Sire. 2005. Tooth development in a scincid lizard, Chalcides viridanus (Squamata), with particular attention to enamel formation. Cell and Tissue Research 319: 71–89.

    Article  Google Scholar 

  • Diekwisch, T.G.H. 2001. Developmental biology of cementum. International Journal of Developmental Biology 45: 695–706.

    Google Scholar 

  • Edmund, A.G. 1960. Tooth replacement phenomena in the lower vertebrates. Life Sciences Contributions, Royal Ontario Museum 52: 1–190.

    Google Scholar 

  • Erickson, G.M. 1996a. Daily deposition of dentine in juvenile Alligator and assessment of tooth replacement rates using incremental line counts. Journal of Morphology 228: 189–194.

    Article  Google Scholar 

  • Erickson, G.M. 1996b. Incremental lines of von Ebner in dinosaurs and the assessment of tooth replacement rates using growth line counts. Proceedings of the National Academy of Sciences USA 93: 14623–14627.

    Article  Google Scholar 

  • Fraas, E. 1891. Ichthyosaurier der süddeutschen Trias- und Jura-Ablagerungen. Tübingen: H. Laupp.

    Google Scholar 

  • Kear, B.P. 2005. Cranial morphology of Platypterygius longmani Wade, 1990 (Reptilia: Ichthyosauria) from the Lower Cretaceous of Australia. Zoological Journal of the Linnean Society 145: 583–622.

    Article  Google Scholar 

  • Kieser, J.A., C. Klapsidis, L. Law, and M. Marion. 1993. Heterodonty and patterns of tooth replacement in Crocodylus niloticus. Journal of Morphology 218: 195–201.

    Article  Google Scholar 

  • Kiprijanoff, W. 1881. Studien über die fossilen Reptilien Russlands. Theil 1. Gattung Ichthyosaurus König aus dem Sewerischen Sandstein oder Osteolith der Kreide-Gruppe. Mémoires de l’Académie Impériale des Sciences de Saint-Pétersbourg 28: 1–103.

    Google Scholar 

  • Kozawa, Y., H. Chisaka, Y. Iwasa, R. Yokota, K. Suzuki, and H. Yamamoto. 2005. Origin and evolution of cementum as tooth attachment complex. Journal of Oral Biosciences 47(1): 25–32.

    Article  Google Scholar 

  • Luan, X., C. Walker, S. Dangaria, Y. Ito, R. Druzinsky, K. Jarosius, H. Lesot, and O. Rieppel. 2009. The mosasaur tooth attachment apparatus as paradigm for the evolution of the gnathostome periodontium. Evolution and Development 11(3): 247–259.

    Article  Google Scholar 

  • Maisch, M.W., and A.T. Matzke. 2000. The Ichthyosauria. Stuttgarter Beiträge zur Naturkunde Serie B (Geologie und Paläontologie) 298: 1–159.

    Google Scholar 

  • Maisch, M.W., and A.T. Matzke. 2002. Observations on Triassic ichthyosaurs. Part IX. The first associated skeletal remains of Pessopteryx n.g. (Ichthyosauria, Lower Triassic) and their bearing on the systematic position of the Omphalosauria. Neues Jahrbuch für Geologie und Paläontologie Abhandlungen 226(1): 59–94.

    Google Scholar 

  • Massare, J.A. 1987. Tooth morphology and prey preference of Mesozoic marine reptiles. Journal of Vertebrate Paleontology 7(2): 121–137.

    Article  Google Scholar 

  • Maxwell, E.E. 2010. Generic reassignment of an ichthyosaur from the Queen Elizabeth Islands, Northwest Territories, Canada. Journal of Vertebrate Paleontology 30(2): 403–415.

    Article  Google Scholar 

  • Maxwell, E.E., and M.W. Caldwell. 2006. A new genus of ichthyosaur from the Lower Cretaceous of Western Canada. Palaeontology 49: 1043–1052.

    Article  Google Scholar 

  • Maxwell, E.E., M.W. Caldwell, and D.O. Lamoureux. 2011. Tooth histology in the Cretaceous ichthyosaur Platypterygius australis, and its significance for the conservation and divergence of mineralized tooth tissues in amniotes. Journal of Morphology 272(2): 129–135.

    Article  Google Scholar 

  • Mazin, J.-M. 1981. Grippia longirostris Wiman, 1929, un Ichthyopterygia primitif du Trias inférieur du Spitsberg. Bulletin du Muséum National d’Histoire Naturelle 4: 317–340.

    Google Scholar 

  • Mazin, J.-M. 1983. L’implantation dentaire chez les Ichthyopterygia (Reptilia). Neues Jahrbuch für Geologie und Paläontologie. Monatschefte 1983(7): 406–418.

    Google Scholar 

  • Mazin, J.-M. 1988. Le crâne d’Ichthyosaurus tenuirostris Conybeare, 1822 (Toarcien, La Caîne, Normandie, France). Bulletin de la Société Linnéenne de Normandie 112–113: 121–132.

    Google Scholar 

  • McGowan, C., and R. Motani. 2003. Ichthyopterygia. München: Verlag Dr. Friedrich Pfeil.

    Google Scholar 

  • McIntosh, J.E., X. Anderton, L. Flores-de-Jacoby, D.S. Carlson, C.F. Shuler, and T.G.H. Diekwisch. 2002. Caiman periodontium as an intermediate between basal vertebrate ankylosis-type attachment and mammalian “true” periodontium. Microscopy Research and Technique 59: 449–459.

    Article  Google Scholar 

  • Merriam, J.C. 1908. Triassic Ichthyosauria with special reference to the American forms. Memoirs of the University of California 1: 1–196.

    Google Scholar 

  • Motani, R. 1996. Redescription of the dental features of an Early Triassic ichthyosaur, Utatsusaurus hataii. Journal of Vertebrate Paleontology 16(3): 396–402.

    Article  Google Scholar 

  • Motani, R. 1997a. Temporal and spatial distribution of tooth implantation in ichthyosaurs. In Ancient marine reptiles, ed. J.M. Callaway, and E.L. Nicholls, 81–103. London: Academic.

    Chapter  Google Scholar 

  • Motani, R. 1997b. Redescription of the dentition of Grippia longirostris (Ichthyosauria) with a comparison with Utatsusaurus hataii. Journal of Vertebrate Paleontology 17(1): 39–44.

    Article  Google Scholar 

  • Motani, R. 1999. Phylogeny of the Ichthyopterygia. Journal of Vertebrate Paleontology 19: 472–495.

    Google Scholar 

  • Nanci, A. 2008. Ten Cate’s oral histology: Development, structure, and function. St. Louis: Mosby Elsevier.

    Google Scholar 

  • Nicholls, E.L., and M. Manabe. 2001. A new genus of ichthyosaur from the Late Triassic Pardonet Formation of British Columbia: Bridging the Triassic-Jurassic gap. Canadian Journal of Earth Sciences 38: 983–1002.

    Article  Google Scholar 

  • Ogg, J.G., G. Ogg, and F.M. Gradenstein. 2008. The concise geologic time scale. Cambridge: Cambridge University Press.

    Google Scholar 

  • Owen, R. 1840–1845. Odontography; or a treatise on the comparative anatomy of the teeth; their physiological relations, mode of development, and microscopic structure in the vertebrate animals. London: Bailliere.

  • Owen, R. 1851. Monograph on the fossil Reptilia of the Cretaceous formations. London: Palaeontological Society.

    Google Scholar 

  • Peyer, B. 1968. Comparative odontology. Chicago: University of Chicago Press.

    Google Scholar 

  • Rieppel, O. 2001. Tooth implantation and replacement in Sauropterygia. Paläontologische Zeitschrift 75(2): 207–217.

    Google Scholar 

  • Rieppel, O., and M. Kearney. 2005. Tooth replacement in the Late Cretaceous mosasaur Clidastes. Journal of Herpetology 39(4): 688–692.

    Article  Google Scholar 

  • Sander, P.M. 1999. The microstructure of reptilian tooth enamel: terminology, function, and phylogeny. Münchner Geowissenschaftliche Abhandlungen (A) 38: 1–102.

    Google Scholar 

  • Sander, P.M. 2000a. Ichthyosauria: Their diversity, distribution and phylogeny. Paläontologische Zeitschrift 74(1/2): 1–35.

    Google Scholar 

  • Sander, P.M. 2000b. Prismless enamel in amniotes: Terminology, function and evolution. In Development, function and evolution of teeth, ed. M.F. Teaford, M.M. Smith, and M.W.J. Ferguson, 92–106. Cambridge: Cambridge University Press.

    Chapter  Google Scholar 

  • Sander, P.M., and C. Faber. 2003. The Triassic marine reptile Omphalosaurus: Osteology, jaw anatomy, and evidence for ichthyosaurian affinities. Journal of Vertebrate Paleontology 23(4): 799–816.

    Article  Google Scholar 

  • Scanlon, J.D., and M.S.Y. Lee. 2002. Varanoid-like dentition in primitive snakes (Madtsoiidae). Journal of Herpetology 36(1): 100–106.

    Google Scholar 

  • Schultze, H.-P. 1969. Die Faltenzähne der Rhipidistiiden Crossopterygier, der Tetrapoden und der Actinopterygier-Gattung Lepisosteus; nebst einer Beschreibung der Zahnstruktur von Onychodus (Struniiformer Crossopterygier). Palaeontographica Italica, New Series 35 65: 63–137.

  • Sereno, P.C., J.A. Wilson, L.M. Witmer, J.A. Whitlock, A. Maga, O. Ide, and T.A. Rowe. 2007. Structural extremes in a Cretaceous dinosaur. PLoS ONE 2(11): e1230.

    Article  Google Scholar 

  • Shimada, K., I. Sato, and H. Moriyama. 1992. Morphology of the tooth of the America alligator (Alligator mississippiensis): The fine structure and elemental analysis of the cementum. Journal of Morphology 211: 319–329.

    Article  Google Scholar 

  • Sire, J.-Y., P.C.J. Donoghue, and M.K. Vickaryous. 2009. Origin and evolution of the integumentary skeleton in non-tetrapod vertebrates. Journal of Anatomy 214: 409–440.

    Article  Google Scholar 

  • Warren, A., and S. Turner. 2006. Tooth histology patterns in early tetrapods and the presence of ‘dark dentine’. Transactions of the Royal Society of Edinburgh: Earth Sciences 96: 113–130.

    Google Scholar 

  • Westergaard, B., and M.W.J. Ferguson. 1987. Development of the dentition in Alligator mississippiensis. Later development in the lower jaws of embryos, hatchlings and young juveniles. Journal of Zoology, London 212: 191–222.

    Article  Google Scholar 

  • Westergaard, B., and M.W.J. Ferguson. 1990. Development of the dentition in Alligator mississippiensis: Upper jaw dental and craniofacial development in embryos, hatchlings, and young juveniles, with a comparison to lower jaw development. American Journal of Anatomy 187: 393–421.

    Article  Google Scholar 

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Acknowledgments

We would like to thank D. Evans (Royal Ontario Museum), R. Jones (Australian Museum, Sydney), and J. McNamara (South Australia Museum, Adelaide) for access to specimens. Thanks are due to B. Barr for discussions and comments during manuscript preparation, P. Druckenmiller and M. Zammit provided helpful reviews. K. Wolkenstein and R. Böttcher assisted with abstract translation. Financial support was provided by an I.W. Killam Memorial Postdoctoral Fellowship to E.E.M., and a Natural Sciences and Engineering Research Council (NSERC) Discovery Grant (#238458-01) and University of Alberta Chair’s Research Allowance to M.W.C.

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Maxwell, E.E., Caldwell, M.W. & Lamoureux, D.O. Tooth histology, attachment, and replacement in the Ichthyopterygia reviewed in an evolutionary context. Paläontol Z 86, 1–14 (2012). https://doi.org/10.1007/s12542-011-0115-z

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