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Scanning electron microscope examination of the dental enameloid of the Cretaceous durophagous shark Ptychodus supports neoselachian classification

Published online by Cambridge University Press:  01 August 2016

Brian L. Hoffman Open the ORCID record for Brian L. Hoffman [Opens in a new window] ,
Scott A. Hageman  and
Gregory D. Claycomb
Brian L. Hoffman
Affiliation:
Department of Natural and Applied Sciences, Park University, Parkville, Missouri 64152, USA 〈brian.hoffman@park.edu〉, 〈shageman@park.edu〉, 〈gclaycomb@park.edu〉
Scott A. Hageman
Affiliation:
Department of Natural and Applied Sciences, Park University, Parkville, Missouri 64152, USA 〈brian.hoffman@park.edu〉, 〈shageman@park.edu〉, 〈gclaycomb@park.edu〉
Gregory D. Claycomb
Affiliation:
Department of Natural and Applied Sciences, Park University, Parkville, Missouri 64152, USA 〈brian.hoffman@park.edu〉, 〈shageman@park.edu〉, 〈gclaycomb@park.edu〉
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Abstract

Although Ptychodus teeth are well known in Late Cretaceous marine deposits in North America and Europe and a few specimens with jaw elements have been discovered, the taxonomic position of the shark genus Ptychodus is enigmatic due to the lack of preservation of diagnostic material other than teeth. These sharks possessed a pavement dentition suited to a diet of hard-shelled macroinvertebrates (durophagy), leading several studies to variously describe Ptychodus as a batoid, a hybodont shark, or a selachimorph. Members of the Selachimorpha share one dental synapomorphy, a triple-layered enameloid (TLE) consisting of an outer shiny-layered enameloid (SLE) of randomly oriented hydroxyapatite crystallites, a middle layer of parallel-bundled enameloid (PBE), and an inner layer of tangled-bundled enameloid (TBE). Batoids and hybodonts both have teeth with single crystallite enameloid (SCE). We examined teeth from Ptychodus collected from the Lincoln Limestone of the Greenhorn Formation of Barton County, Kansas, and compared their enameloid ultrastructure with that of a Carboniferous hybodontiform and the Cretaceous lamniform shark Squalicorax curvatus Williston, 1900. Scanning electron microscopic examination of Ptychodus shows that crystallite bundling in the form of a TLE is evident in these teeth. The PBE is most apparent at transverse enameloid ridges of Ptychodus teeth. Columns of dentine penetrate into the tooth enameloid, and the crystallites near the dentine are randomly oriented. These observations bolster the argument that Ptychodus is a genus of highly specialized selachimorph shark, rather than a hybodont or batoid.

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Articles
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Journal of Paleontology , Volume 90 , Issue 4 , July 2016 , pp. 741 - 762
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Copyright © 2016, The Paleontological Society 

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References

Agassiz, L., 1833–1844, Recherches sur les Poissons Fossiles [5 volumes]: Neuchâtel, Imprimerie de Petitpierre, 1420 p.Google Scholar
Andreev, P.S., 2010, Enameloid microstructure of the serrated cutting edges in certain fossil carchariniform and lamniform sharks: Microscopy Research and Technique, v. 73, p. 704–713.Google Scholar
Andreev, P.S., and Cuny, G., 2012, New Triassic stem selachimorphs (Chondrichthyes, Elasmobranchii) and their bearing on the evolution of dental enameloid in Neoselachii: Journal of Vertebrate Paleontology, v. 32, p. 255–266.Google Scholar
Bendix-Almgreen, S.E., 1983, Carcharodon megalodon from the Upper Miocene of Denmark, with comments on elasmobranch tooth enameloid: Coronoïn: Bulletin of the Geological Society of Denmark, v. 32, p. 1–32.Google Scholar
Berg, L.S., 1937, A classification of fish-like vertebrates: Bulletin de l’Académie des Sciences de l’URSS, v. 1937, p. 1277–1280 [in Russian with English summary].Google Scholar
Bonaparte, C.L., 1838, Selachorum tabula analytica: Nuovi Annali della Scienze Naturali, Bologna, v. 1, p. 195–214.Google Scholar
Brito, P.M., and Janvier, P., 2002, A ptychodontid (Chondrichthyes, Elasmobranchii) from the Upper Cretaceous of South America: Geodiversitas, v. 24, p. 785–790.Google Scholar
Canavari, M., 1916, Descrizione di um notevole esemplare di Ptychodus Agassiz trovato nel calcare bianco della Creta superior di Gallio nei Sette Comuni (Veneto): Palaeontographica Italica, v. 22, p. 35–102.Google Scholar
Cappetta, H., 2012, Chondrichthyes—Mesozoic and Cenozoic Elasmobranchii: Teeth. Handbook of Paleoichthyology, v. 3E: Munich, Verlag Dr. Friedrich Pfeil, 512 p.Google Scholar
Cappetta, H., and Case, G.R., 1999, Additions aux faunes de sélachiens du Crétaché du Texas (Albian supérieur-Campanien): Paleo Ichthyologica, v. 9, p. 5–111.Google Scholar
Casier, E.N., 1947, Constitution et évolution de la racine dentaire des Euselachii. II-Etude comparative des types: Bruxelles Bull. Mus. r. Hist. nat. Belg, v. 23, no. 4, p. 1–32.Google Scholar
Coates, M.I., and Gess, R.W., 2007, A new reconstruction of Onychoselache traquairi, comments on early chondrichthyan pectoral girdles and hybodontiform phylogeny: Palaeontology, v. 50, p. 1421–1446.Google Scholar
Compagno, L.J.V., 1977, Phyletic relationships of living sharks and rays: American Zoologist, v. 17, p. 303–322.CrossRefGoogle Scholar
Conybeare, W.D., and Phillips, W., 1822, Outlines of the Geology of England and Wales. Part I, London, William Phillips, 477 p.Google Scholar
Cumbaa, S.L., Schröder-Adams, C., Day, R.G., and Phillips, A.J., 2006, Cenomanian bonebed faunas from the northeastern margin, Western Interior Seaway, Canada: New Mexico Museum of Natural History and Science Bulletin, v. 35, p. 139–155.Google Scholar
Cuny, G., 2008, Mesozoic hybodont sharks from Asia and their relationships to the genus Ptychodus : Acta Geologica Polonica, v. 58, p. 211–216.Google Scholar
Cuny, G., and Risnes, S., 2005, The enameloid microstructure of the teeth of synechodontiform sharks (Chondrichthyes: Neoselachii): PalArch Foundation Journal of Vertebrate Palaeontology, v. 3, p. 8–19.Google Scholar
Cuny, G., Srisuk, P., Khamha, S., Suteethorn, V., and Tong, H., 2009, A new elasmobranch fauna from the middle Jurassic of southern Thailand: Geological Society, London, Special Publications, v. 315, p. 97–113.CrossRefGoogle Scholar
David, M.L., 1996, Dental histology of Ptychodus and its implications in the phylogeny of the Ptychodontidae: Journal of Vertebrate Paleontology, v. 16, no. 3 (supplement), p. 30A.Google Scholar
David, M.L., 1999, A histological and mechanical description of Ptychodus [M.S. thesis]: Hays, Fort Hays State University, 44 p.Google Scholar
Dick, J.R.F., 1978, On the Carboniferous shark Tristychius arcuatus from Scotland: Transactions of the Royal Society of Edinburgh, v. 70, no. 4, p. 63–109.Google Scholar
Dick, J.R.F., and Maisey, J.G., 1980, The Scottish lower Carboniferous shark Onychoselache traquairi : Palaeontology, v. 23, p. 363–374.Google Scholar
Douady, C., Dosay, M., Shivji, M.S., and Stanhope, M.J., 2003, Molecular phylogenetic evidence refuting the hypothesis of Batoidea (rays and skates) as derived sharks: Molecular Phylogenetics and Evolution, v. 26, p. 215–221.CrossRefGoogle ScholarPubMed
Ebert, D.A., and Stehmann, M.F.W., 2013, Sharks, batoids and chimaeras of the North Atlantic, Rome, FAO Species Catalogue for Fishery Purposes, no. 7, 523 p.Google Scholar
Elder, W.P., 1987, The paleoecology of Cenomanian-Turonian (Cretaceous) boundary extinctions at Black Mesa, Arizona: PALAIOS, v. 2, no. 1, p. 24–40.Google Scholar
Enault, S., Cappetta, H., and Adnet, S., 2013, Simplification of the enameloid microstructure of large stingrays (Chondricthyes: Myliobatiformes): A functional approach: Zoological Journal of the Linnean Society, v. 169, p. 144–155.CrossRefGoogle Scholar
Enault, S., Guinot, G., Koot, M.B., and Cuny, G., 2015, Chondrichthyan tooth enameloid: Past, present, and future: Zoological Journal of the Linnean Society, v. 174, p. 549–570.Google Scholar
Enax, J., Janus, A.M., Raabe, D., Epple, M., and Fabritius, H.-O., 2014, Ultrastructural organization and micromechanical properties of shark tooth enameloid: Acta Biomateriala, v. 10, p. 3959–3968.CrossRefGoogle ScholarPubMed
Everhart, M.J., 2005, The Oceans of Kansas: A Natural History of the Western Interior Sea, Bloomington, Indiana University Press, 344 p.Google Scholar
Everhart, M.J., 2013, “The Palate Bones of a Fish?”—The first specimen of Ptychodus mortoni (Chondrichthyes; Elasmobranchii) from Alabama: Bulletin of the Alabama Museum of Natural History, v. 31, p. 98–104.Google Scholar
Everhart, M.J., and Caggiano, T., 2004, An associated dentition and calcified vertebral centra of the Late Cretaceous elasmobranch, Ptychodus anonymus Williston 1900: Paludicola, no. 4, 125–136.Google Scholar
Gallardo, C., Shimada, K., and Schumacher, B.A., 2013, A new Late Cretaceous marine vertebrate assemblage from the Lincoln Limestone Member of the Greenhorn Limestone in southeastern Colorado: Kansas Academy of Science, Transactions, v. 115, no. 3/4, p. 107–116.Google Scholar
Gillis, J.A., and Donoghue, P.C.J., 2007, The homology and phylogeny of chondrichthyan tooth enameloid: Journal of Morphology, v. 268, p. 33–49.CrossRefGoogle ScholarPubMed
Ginter, M., Hampe, O., and Duffin, C., 2010, Chondrichthyes—Paleozoic Elasmobranchii: Teeth. Handbook of Paleoichthyology, v. 3D: Munich, Verlag Dr. Friedrich Pfeil, 168 p.Google Scholar
Goto, M., 1991, Evolutionary trends of the tooth structure in Chondrichthyes, in Suga, S., and Nakahara, H., eds., Mechanisms and Phylogeny of Mineralization in Biological Systems: Biomineralization ’90: Tokyo, Springer-Verlag, p. 447–452.Google Scholar
Guinot, G., and Cappetta, H., 2011, Enameloid microstructure of some Cretaceous Hexanchiformes and Synechodontiformes (Chondrichthyes: Neoselachii): New structures and systematic implications: Microscopy Research and Technique, v. 74, p. 196–205.CrossRefGoogle ScholarPubMed
Guinot, G., Adnet, S., Cavin, L., and Cappetta, H., 2013, Cretaceous stem chondrichthyans survived the end-Permian mass extinction: Nature Communications, doi:10.1038/ncomms3669.CrossRefGoogle Scholar
Hamm, S.A., 2008, Systematic, stratigraphic, geographic and paleoecological distribution of the Late Cretaceous shark genus Ptychodus within the Western Interior Seaway [M.S. thesis]: Dallas, University of Texas-Dallas, 434 p.Google Scholar
Hamm, S.A., 2010, The Late Cretaceous shark, Ptychodus rugosus, (Ptychodontidae) in the Western Interior Sea: Kansas Academy of Science, Transactions, v. 113, no. 1/2, p. 44–55.Google Scholar
Hamm, S.A., 2015, Paraptychodus washitaensis n. gen. et n. sp., of Ptychodontid shark from the Albian of Texas, USA: Cretaceous Research, v. 54, p. 60–67.CrossRefGoogle Scholar
Hansen, M.C., 1986, Microscopic chondrichthyan remains from Pennsylvanian marine rocks of Ohio and adjacent areas [Ph.D. dissertation], Columbus, The Ohio State University, 536 p.Google Scholar
Hattin, D.E., 1975, Stratigraphy and depositional environment of Greenhorn Limestone (Upper Cretaceous) of Kansas: Bulletin of Kansas Geological Survey, no. 209, 128 p.Google Scholar
Hawkins, A., 1819, Kingsbridge and Salcombe, with an Intermediate Estuary, Historically and Topographically Depicted, London, R. Southwood, 210 p.Google Scholar
Hay, O.P., 1902, Bibliography and catalogue of fossil Vertebrata of North America: United States Geological Survey Bulletin, v. 179, 868 p.Google Scholar
Hodnett, J.-P., Elliot, D.K., Olson, T.J., and Wittke, J.H., 2012, Ctenacanthiform sharks from the Permian Kaibab Formation, northern Arizona: Historical Biology, v. 24, p. 381–395.Google Scholar
Huxley, T.H., 1880, On the application of the laws of evolution to the arrangement of the Vertebrata and more particularly the Mammalia: Proceedings of the Zoological Society of London, v. 1880, p. 649–662.Google Scholar
Jaekel, O.M.J., 1898, Die Selachier aus dem oberen Muschelkalk Lothringens. Abhandteilung Geologische Spezialk: Elasass-Lothringen, Series 3, no. 4, p. 273–332.Google Scholar
Kauffman, E.G., 1972, Ptychodus predation upon a Cretaceous Inoceramus : Journal of Paleontology, v. 15, p. 439–444.Google Scholar
Kauffman, E.G., 1977, Geological and biological overview: Western Interior Cretaceous basin: The Mountain Geologist, v. 14, no. 3/4, p. 75–99.Google Scholar
Kauffman, E.G., Sageman, B.B., Kirkland, J.I., Elder, W.P., Harries, P.J., and Villamil, T., 1993, Molluscan biostratigraphy of the Cretaceous Western Interior Basin, North America, in Caldwell, W.G.E., and Kauffman, E.G., eds., Evolution of the Western Interior Basin: Geological Association of Canada, Special Paper no. 39, p. 397–434.Google Scholar
Landman, N.H., and Klofak, S.M., 2012, Anatomy of a concretion: Life, death and burial in the Western Interior Seaway: PALAIOS, v. 27, no. 10, p. 671–692.Google Scholar
Leidy, J., 1868, Notice of American species of Ptychodus : Proceedings of the Academy of Natural Sciences of Philadelphia, v. 20, p. 205–208.Google Scholar
Macleod, N., 1982, The first North American occurrence of the Late Cretaceous elasmobranch Ptychodus rugosus : Journal of Paleontology, v. 56, p. 403–409.Google Scholar
Maisey, J.G., 1975, The interrelationships of phalacanthous selachians: Neues Jahrbüch für Geologie and Paläontologie Monatschefte, v. 1975, no. 9, p. 553–567.Google Scholar
Maisey, J.G., 1982, The anatomy and interrelationships of Mesozoic hybodont sharks: American Museum Novitates, v. 2724, p. 1–48.Google Scholar
Maisey, J.G., Naylor, G.J.P., and Ward, D.J., 2004, Mesozoic elasmobranchs, neoselachian phylogeny, and the rise of modern neoselachian diversity, in Arratia, G., and Tintori, A., eds., Mesozoic Fishes 3—Systematics, Paleoenvironments and Biodiversity, Munich, Verlag Dr. Friedrich Pfeil, p. 17–56.Google Scholar
Mantell, G.A., 1822, Fossils of the South Downs, or, Illustrations of the geology of Sussex, London, Lupton Relfe, 320 p.Google Scholar
McKirahan, J., Goldstein, R.H., and Franseen, E.K., 2000, Sequence stratigraphy of the Lane-Island Creek Shales and the Farley Limestone in northeastern Kansas and geologic factors affecting the quality of limestone aggregates: Kansas Department of Transportation Report, no. K-TRAN: KU-97-1, p. 6–70.Google Scholar
Morton, S.G., 1834, Synopsis of the Organic Remains of the Cretaceous Group of the United States, Philadelphia, Key and Biddle, 89 p.Google Scholar
Mutter, R.J., Itturalde-Vinent, M., and Carmona, J.F., 2005, The first Mesozoic Caribbean shark is from the Turonian of Cuba: Ptychodus cyclodontis sp. nov. (?Neoselachii): Journal of Vertebrate Paleontology, v. 25, p. 976–978.Google Scholar
Myers, C.E., and Lieberman, B.S., 2011, Sharks that pass in the night: Using geographical information systems to investigate competition in the Western Interior Seaway: Proceedings of the Royal Academy of Sciences B, v. 278, p. 681–689.CrossRefGoogle ScholarPubMed
Patterson, C., 1966, British Wealden sharks: Bulletin of the British Museum (Natural History) Geology, v. 11, p. 283–350.CrossRefGoogle Scholar
Preuschoft, H., Reif, W.E., and Muller, W.H., 1974, Funktionsanpassungen in form und struktur an haifischzähnen: Zeitschrift für Anatomie und Entwicklungsgeschichte, v. 143, p. 315–344.Google Scholar
Rees, J., 2008, Interrelationships of Mesozoic hybodont sharks as indicated by dental morphology—preliminary results: Acta Geologica Polonica, v. 58, p. 217–221.Google Scholar
Rees, J., and Underwood, C.T., 2002, The status of the genus Lissodus Brough, 1935, and the position of the nominal Lissodus species within the Hybodontoidea (Selachii): Journal of Vertebrate Paleontology, v. 22, p. 471–478.Google Scholar
Reif, W., 1973, Morphologie und Skulptür der Haifisch-Zähnkronen: Neues Jahrbüch für Geologie and Paläontologie Abhandlungen, v. 143, p. 39–55.Google Scholar
Reif, W., 1977, Tooth enameloid as taxonomic criterion: 1. A new euselachian shark from the Rhaetic-Liassic boundary: Neues Jahrbüch für Geologie and Paläontologie Monatschefte, v. 1977, p. 565–576.Google Scholar
Rocco, L., Liguori, I., Costagliola, D., Morescalchi, M.A., Tintl, F., and Stingo, V., 2007, Molecular and karyological aspects of Batoidea (Chondrichthyes: Elasmobranchii) phylogeny: Gene, v. 389, p. 80–86.Google Scholar
Schmeisser McKean, R.L., and Gillette, D.D., 2015, Taphonomy of large marine vertebrates in the Upper Cretaceous (Cenomanian-Turonian) tropic shale of southern Utah: Cretaceous Research, v. 56, p. 278–292.CrossRefGoogle Scholar
Schultze, H.-P., and Chorn, J., 1988, The Upper Pennsylvanian vertebrate fauna of Hamilton, Kansas, in Mapes, G., and Mapes, R.H., eds., Regional Geology and Paleontology of Upper Paleozoic Hamilton Quarry Area in Southeastern Kansas: Kansas Geological Survey Guidebook, no. 6, p. 147–154.Google Scholar
Shimada, K., and Cicimurri, D.J., 2006, The oldest record of the Late Cretaceous anacoracid shark Squalicorax pristodontus (Agassiz), from the Western Interior, with comments on Squalicorax phylogeny, in Lucas, S.G., and Sullivan, R.M., eds., Late Cretaceous Vertebrates from the Western Interior: New Mexico Museum of Natural History and Science Bulletin, no. 35, p. 177–184.Google Scholar
Shimada, K., Schumacher, B.A., Parkin, J.A., and Palermo, J.M., 2006, Fossil marine vertebrates from the Lowermost Greenhorn Limestone (Upper Cretaceous: Middle Cenomanian) in Southeastern Colorado: Journal of Paleontology, v. 80 (supplement to no. 2), Memoir 63.Google Scholar
Shimada, K., Rigby, C.J., and Kim, S.H., 2009, Partial skull of Late Cretaceous durophagous shark Ptychodus occidentalis (Elasmobranchii: Ptychodontidae), from Nebraska, U.S.A: Journal of Vertebrate Paleontology, v. 29, p. 336–349.Google Scholar
Siverson, M., Lindquist, J., and Kelly, L.S., 2007, Anacoracid sharks from the Albian (Lower Cretaceous) Pawpaw Shale of Texas: Palaeontology, v. 50, p. 939–950.Google Scholar
Stewart, J.D., 1980, Reevaluation of the phylogenetic position of the Ptychodontidae: Kansas Academy of Science, Transactions, v. 83, no. 3, p. 154.Google Scholar
Stewart, J.D., 1988, Paleoecology and the first West Coast record of the shark genus Ptychodus : Journal of Vertebrate Paleontology, v. 8, no. 3 (supplement) p. 27A.Google Scholar
Stromer, E., 1927, Prof. E. Stromers in den Wüsten Ägyptens. II. Wirbeltier-Reste der Baharije-Stufe (Unterstes Cenoman). 9. Die Plagiostomen mit einem Anhang über käno- und mesozoische Rückenflossenstacheln von Elasmobranchiern: Abhandlungen der Bayerischen Akademie der Wissenschaften, Mathematisch-naturwissenschaftliche Abteilung, Neue Funde, 31, p. 1–64.Google Scholar
Underwood, C.J., and Cumbaa, S.L., 2010, Chondrichthyans from a Cenomanian (Late Cretaceous) bonebed, Saskatchewan, Canada: Paleontology, v. 53, p. 903–944.Google Scholar
Whitenack, L.B., Simpkins, D.C. Jr., Motta, P.J., Hirai, M., and Kumar, A., 2010, Young’s modulus and hardness of shark tooth biomaterials: Archives of Oral Biology, v. 55, p. 203–209.Google Scholar
Whitenack, L.B., Simpkins, D.C. Jr., and Motta, P.J., 2011, Biology meets engineering: The structural mechanics of fossil and extant shark teeth: Journal of Morphology, v. 272, p. 169–179.Google Scholar
Whitley, G.P., 1939, Taxonomic notes on sharks and rays: Australian Zoologist, v. 9, no. 3, p. 227–262.Google Scholar
Williamson, T.E., Kirkland, J.I., and Lucas, S.G., 1991, The Cretaceous elasmobranch Ptychodus decurrens Agassiz from North America: Geobios, v. 24, p. 595–599.Google Scholar
Williston, S.W., 1900, Some fish teeth from the Kansas Cretaceous: Kansas University Quarterly, v. 9, p. 27–42.Google Scholar
Winchell, C.J., Martin, A.P., and Mallat, J., 2004, Phylogeny of elasmobranchs based on LSU and SSU ribosomal RNA genes: Molecular Phylogenetics and Evolution, v. 31, p. 214–224.Google Scholar
Woodward, A.S., 1887, On the dentition and affinities of the selachian genus Ptychodus Agassiz: Quarterly Journal of the Geological Society, London, v. 43, p. 121–131.Google Scholar
Woodward, A.S., 1889, Catalogue of the Fossil Fishes in the British Museum, London, British Museum of Natural History, 474 p.Google Scholar
Woodward, A.S., 1904, The jaws of Ptychodus from the Chalk: Quarterly Journal of the Geological Society, London, v. 60, p. 133–135.Google Scholar
Zangerl, R., 1981, Chondrichthyes I: Paleozoic Elasmobranchii. Handbook of Paleoichthyology, v. 3A: Stuttgart, Gustav Fischer, 115 p.Google Scholar