Environmental Biology of Fishes

, Volume 63, Issue 3, pp 309–319 | Cite as

Teeth of Embryos in Lamniform Sharks (Chondrichthyes: Elasmobranchii)

  • Kenshu ShimadaEmail author


The dentitions of lamniform sharks possess a unique heterodonty, the lamnoid tooth pattern. However, in embryos, there are 'embryonic' and 'adult' dentitions. The teeth in the embryonic dentition are peg-like and appear to be attached to the jaw in an acrodont fashion. The adult dentition is characterized by the presence of replacement tooth series with the lamnoid tooth pattern. The embryonic–adult transition in dentitions appears at around 30–60 cm TL. Tooth replacement generally begins before birth in embryos with adult dentitions. The adult dentition becomes functional just before or after parturition. An embryo of one species (Lamna nasus) shows a tooth directly on the symphysis of the upper jaws, marking the first record of a medial tooth for the order Lamniformes.

lamnoid dentition dental pattern tooth replacement 


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References cited

  1. Abe, T., S. Isokawa, K. Aoki, T. Kishimoto, Y. Shimma & H. Shimma. 1969. Notes on some members of osteodonti (class Chondrichthyes) – II. Bull. Tokai Regional Fish. Res. Lab. 56: 1–6.Google Scholar
  2. Allen, G.R. & D.R. Robertson. 1994. Fishes of the tropical eastern Pacific. University of Hawaii Press, Honolulu. 332 pp.Google Scholar
  3. Applegate, S.P. 1965. Tooth terminology and variation in sharks with special reference to the sand shark, Carcharias taurus Rafinesque. Los Angeles Co. Mus. Contr. Sci. 86: 1–18.Google Scholar
  4. Bass, A.J. 1986a. Family no. 14: Lamnidae. pp. 98–100. In: M.M. Smith & P.C. Heemstra (ed.) Smiths' Sea Fishes, Springer-Verlag, Berlin.Google Scholar
  5. Bass, A.J. 1986b. Family no. 16: Alopiidae. pp. 101–102. In: M.M. Smith & P.C. Heemstra (ed.) Smiths' Sea Fishes, Springer-Verlag, Berlin.Google Scholar
  6. Bass, A.J., J.D. D'Aubrey & N. Kistnasamy. 1975. Sharks of the east coast of southern Africa: part IV, the families Odontaspididae, Scapanorhynchidae, Isuridae, Cetorhinidae, Alopiidae, Orectolobidae and Rhiniodontidae. Oceanogr. Res. Inst., Invest. Rep. 39: 1–102.Google Scholar
  7. Bigelow, H.B. & W.C. Schroeder. 1948. Sharks. pp. 59–546. In: Fishes of the western North Atlantic, Part I, Sears Foundation for Marine Research, New Haven.Google Scholar
  8. Bigelow, H.B. & W.C. Schroeder. 1953. Fishes of the Gulf of Maine. Fish. Bull. Fish and Wildlife Service 53: 1–577.Google Scholar
  9. Bigelow, H.B. & W.C. Schroeder. 1958. A large white shark, Carcharodon carcharias, taken in Massachusetts Bay. Copeia 1958: 54–55.Google Scholar
  10. Blagoderov, A.I. 1994. Seasonal distribution and some notes on the biology of salmon shark (Lamna ditropis) in the northwestern Pacific Ocean. J. Ichthyol. 34: 115: 121.Google Scholar
  11. Burgess, R.F. 1970. The sharks. Doubleday and Company, Garden City. 160 pp.Google Scholar
  12. Cadenat, J. 1956. Remarques biologiques sur le requin-sable Carcharias (Odontaspis) taurus Rafinesque 1810. Bull. Inst. Fran. Af. Noire, Ser. A 18: 1249–1256.Google Scholar
  13. Cadenat, J. & J. Blache. 1981. Requins de Mediterranee et d'Atlantique (plus particulierement de la Cote Occidentale d'Afrique). Collection Faune Tropicale (Editions de l'Office de la Recherche Scientifique et Technique Outer-Mer) 21: 1–330.Google Scholar
  14. Cailliet, G.M., L.K. Martin, J.T. Harvey, D. Kusher & B.A. Welden. 1983. Preliminary studies on the age and growth of blue, Prionace glauca, common thresher, Alopias vulpinus, and shortfin mako, Isurus oxyrinchus, sharks from California waters. NOAA Tech. Rep., NMFS Circ. 8: 179–188.Google Scholar
  15. Castro, J.I. 1983. The sharks of North American waters. Texas A&M University Press, College Station. 180 pp.Google Scholar
  16. Castro, J.I., E. Clark, K. Yano & K. Nakaya. 1997. The gross anatomy of the female reproductive tract and associated organs of the Fukuoka megamouth shark (Megachasma pelagios). pp. 33–37. In: K. Yano, J.F. Morrissey, Y. Yabumoto & K. Nakaya (ed.) Biology of Megamouth Shark, Tokai University Press, Tokyo.Google Scholar
  17. Chen, C.-T., K.-M. Liu & Y.-C. Chang. 1997. Reproductive biology of the bigeye thresher shark, Alopias superciliosus (Lowe, 1839) (Chondrichthyes: Alopiidae), in the northwestern Pacific. Ichthyol. Res. 44: 227–320.Google Scholar
  18. Cigala-Fulgosi, F. 1992. Addition to the fish fauna of the Italian Miocene. The occurrence of Pseudocarcharias (Chondrichthyes, Pseudocarchariidae) in the lower Serravallian of Parma Province. Tertiary Res. 14: 51–60.Google Scholar
  19. Compagno, L.J.V. 1984. FAO species catalogue. Sharks of the world. An annotated and illustrated catalogue of shark species known to date. FAO Fish. Synop. 125, 4: 1–655.Google Scholar
  20. Compagno, L.J.V. 1988. Sharks of the order Carcharhiniformes. Princeton University Press, Princeton. 486 pp.Google Scholar
  21. Compagno, L.J.V. 1990. Relationships of the megamouth shark, Megachasma pelagios (Lamniformes: Megachasmidae), with comments on its feeding habits. NOAA Tech. Rep. NMFS 90: 357–379.Google Scholar
  22. Compagno, L.J.V. 1999. Checklist of living elasmobranchs. pp. 471–498. In: W.C. Hamlett (ed.) Sharks, Skates, and Rays: the Biology of Elasmobranch Fishes, Johns Hopkins University Press, Baltimore.Google Scholar
  23. Duhamel, G. & C. Ozouf-Costaz. 1982. Presence de Lamna nasus (Bonnaterre, 1788) aux iles Kerguelen. Cybium 6(4): 15–18.Google Scholar
  24. Ellis, R. & J.E. McCosker. 1991. Great white shark. Stanford University Press, Palo Alto. 270 pp.Google Scholar
  25. Eschmeyer, W.N. & E.S. Herald. 1983. A field guide to Pacific coast fishes of North America from the Gulf of Alaska to Baja California. Houghton Mifflin Company, Boston. 336 pp.Google Scholar
  26. Follett, W.I. 1966. Man-eater of the California coast. Pacific Discovery 19: 18–22.Google Scholar
  27. Fowler, H.W. 1936. The marine fishes of west Africa based on the collection of the American Museum Congo Expedition, 1909–1915 (Part I). Bull. Amer. Mus. Nat. Hist. 70: 1–605.Google Scholar
  28. Francis, M.P. 1996. Observations on a pregnant white shark with a review of reproductive biology. pp. 157–172. In: A.P. Klimley & D.G. Ainley (ed.) Great White Sharks: the Biology of Carcharodon carcharias, Academic Press, San Diego.Google Scholar
  29. Francis, M.P. & J.D. Stevens. 2000. Reproduction, embryonic development, and growth of the porbeagle shark, Lamna nasus, in the southwest Pacific Ocean. U.S. Fish. Bull. 98: 41–63.Google Scholar
  30. Fries, B., C.U. Ekstrom & C. Sundevall. 1895. A history of Scandinavian fishes. P.A. Norstedt and Soner, Stockholm. 1240 pp.Google Scholar
  31. Fujita, K. 1981. Oviphagous embryos of the pseudocarchariid shark, Pseudocarcharias kamoharai, from the Central Pacific. Japan. J. Ichthyol. 28: 37–44.Google Scholar
  32. Garrick, J.A.F. 1967. Revision of sharks of genus Isurus with description of a newspecies (Galeoidea, Lamnidae). Proc. U.S. Nat. Mus. 118(3537): 663–690.Google Scholar
  33. Gauld, J.A. 1989. Records of porbeagles landed in Scotland, with observations on the biology, distribution and exploitation of the species. Scottish Fish. Res. Rep. 45: 1–15.Google Scholar
  34. Gilmore, R.G. 1983. Observations on the embryos of the longfin mako, Isurus paucus, and the bigeye thresher, Alopias superciliosus. Copeia 1983: 375–382.Google Scholar
  35. Gilmore, R.G. 1993. Reproductive biology of lamnoid sharks. Env. Biol. Fish. 38: 95–114.Google Scholar
  36. Gilmore, R.G., J.W. Dodrill & P.A. Linley. 1983. Reproduction and embryonic development of the sand tiger shark, Odontaspis taurus (Rafinesque). U.S. Fish. Bull. 81: 201–225.Google Scholar
  37. Gomes, U.L. & M.A.F. dos Reis. 1990. Observacoes sobre a heterodontia ontogenetica em Eugomphodus taurus (Rafinesque, 1809) – (Lamniformes, Odontaspididae). Anales del Sociedad Nordest de Zoologia 3: 315–330.Google Scholar
  38. Gottfried, M.D. & M.P. Francis. 1996. Developmental changes in white shark tooth morphology: implications for studies on fossil sharks. J. Vert. Paleont. 16(Supp. to No. 3): 38A.Google Scholar
  39. Gruber, S.H. & L.J.V. Compagno. 1981. Taxonomic status and biology of the bigeye thresher, Alopias superciliosus. U.S. Fish. Bull. 79: 617–640.Google Scholar
  40. Gruber, S.H. & R.S. Keyes. 1981. Keeping sharks for research. pp. 373–402. In: A.D. Hawkins (ed.) Aquarium Systems, Academic Press, New York.Google Scholar
  41. Gubanov, Y.P. 1978. The reproduction of some species of pelagic sharks from the equatorial zone of the Indian Ocean. J. Ichthyol. 18: 781–792.Google Scholar
  42. Guitart-Manday, D. 1975. Las presquerias pelagico-oceanicas de corto radio de accion en la region noroccidental de Cuba. Serie Oceanologica, Academia de Ciencias de Cuba 31: 1–41.Google Scholar
  43. Hildebrand, M. 1988. Analysis of vertebrate structure, 3rd edn., John Wiley and Sons, New York. 701 pp.Google Scholar
  44. Irvine, F.R. 1947. The fishes and fisheries of the Gold Coast. Cambridge University Press, Cambridge. 352 pp.Google Scholar
  45. Jordan, D.S. 1898. Description of a species of fish (Mitsukurina owstoni) from Japan, the type of a distinct family of lamnoid sharks. Proc. Calif. Acad. Sci. (Zool.), Ser. 3 1(6): 199–202.Google Scholar
  46. Kajiura, S.M. & T.C. Tricas. 1996. Seasonal dynamics of dental sexual dimorphism in the Atlantic stingray Dasyatis sabina. J. Exp. Biol. 199: 2297–2306.Google Scholar
  47. Kakizawa, Y. 1984. On the teeth of salmon shark, Lamna ditropis Hubbs and Follett. Nihon Univ. Dent. J. 58: 59–69.Google Scholar
  48. Kato, S., S. Springer & M.H. Wagner. 1967. Field guide to eastern Pacific and Hawaiian sharks. U.S. Fish and Wildlife Service, Circ. 271: 1–47.Google Scholar
  49. Klimley, A.P. 1985. The areal distribution and autoecology of the white shark, Carcharodon carcharias, off the west coast of North America. Mem. So. Calif. Acad. Sci. 9: 15–40.Google Scholar
  50. Last, P.R. & J.D. Stevens. 1994. Sharks and rays of Australia. Commonwealth Scientific and Industrial Research Organization, Australia. 513 pp.Google Scholar
  51. Liu, K.-M., C.-T. Chen, T.-H. Liao & S.-J. Joung. 1999. Age, growth, and reproduction of the pelagic thresher shark, Alopias pelagicus in the northwestern Pacific. Copeia 1999: 68–74.Google Scholar
  52. Lohberger, J. 1910. Über zwei riesige Embryonen von Lamna. Abhandlungen der math.-phys. Klasse der K. Bayer, Akademie der Wissenschaften 4(Supp. to No. 2): 1–45.Google Scholar
  53. Lucifora, L.O. & R.C. Menni. 1998. First record of a porbeagle shark, Lamna nasus, in brackish waters of Mar Chiquita Lagoon, Argentina. Cybium 22(1): 87–88.Google Scholar
  54. Lucifora, L.O., R.C. Menni & A.H. Escalante. 2001. Analysis of dental insertion angles in the sand tiger shark Carcharias taurus (Chondrichthyes: Lamniformes). Cybium 25(1): 23–31.Google Scholar
  55. Maul, G.E. 1955. Five species of rare sharks new for Madeira including two new to science. Notulae Naturae of the Academy of Natural Sciences of Philadelphia 279: 1–13.Google Scholar
  56. McKenzie, R.A. & S.N. Tibbo. 1964. Amorphometric description of porbeagle (Lamna nasus) from Canadian Atlantic waters. J. Fish. Res. Board Can. 21: 863–864.Google Scholar
  57. Mochizuki, K. & Y. Noze. 1986. Catalogue of the pisces specimens preserved in the Department of Fisheries, the University Museum, the University of Tokyo (I). Material Report, University Museum, University of Tokyo 14: 1–123.Google Scholar
  58. Mollet, H.F., G. Cliff, H.L. Pratt, Jr. & J.D. Stevens. 2000. Reproductive biology of the female shortfin mako, Isurus oxyrinchus Rafinesque, 1810, with comments on the embryonic development of lamnoids. U.S. Fish. Bull. 98: 299–318.Google Scholar
  59. Moreno, J.A. & J. Moron. 1992. Reproductive biology of the bigeye thresher shark, Alopias superciliosus (Lowe, 1839). Aust. J. Mar. Freshwater Res. 43: 77–86.Google Scholar
  60. Moreno, J.A., J.I. Parajua & J. Moron. 1989. Biologia reproductiva y fenologia de Alopias vulpinus (Bonnaterre, 1788) (Squaliformes: Alopiidae) en el Atlantico nor-oriental y Mediterraneo occidental.Scientia Marina 53: 37–46.Google Scholar
  61. Murru, F.L. 1990. The care and maintenance of elasmobranchs in controlled environments. NOAA Tech. Rep. NMFS 90: 203–209.Google Scholar
  62. Nakamura, H. 1935. On the two species of the thresher shark from Formosanwaters. Mem. Fac. Sci. Agri., Taihoku Imperial University 14: 1–6.Google Scholar
  63. Nakaya, K. 1982. Alopias superciliosus (Lowe). pp. 40–41. In: O. Okamura, K. Amaoka & H. Mitani (ed.) Fishes of the Kyushu-Palau Ridge and Tosa Bay, Japan Fisheries Resource Conservation Association, Tokyo.Google Scholar
  64. Otake, T. & K. Mizue. 1981. Direct evidence for oophagy in thresher shark, Alopias pelagicus. Japan. J. Ichthyol. 28: 171–172.Google Scholar
  65. Ray, L.L. 1928. Fauna Iberica: pesces (tomo primero). Museo Nacional de Ciencias Naturales, Madrid. 692 pp.Google Scholar
  66. Reif, W.E. 1976. Morphogenesis, pattern formation and function of the dentition of Heterodontus (Selachii). Zoomorphologie 83: 1–47.Google Scholar
  67. Reif, W.E. 1984. Pattern regulation in shark dentitions. pp. 603–621. In: G.M. Malacinski & S.V. Bryant (ed.) Pattern Formation: a Primer in Developmental Biology, Macmillan Publishing Company, New York.Google Scholar
  68. Reif, W.E., D. McGill & P. Motta. 1978. Tooth replacement rate of the sharks Triakis semifasciata and Ginglymostoma cirratum. Zool. Jahrb. Anat. 99: 151–156.Google Scholar
  69. Sadowsky, V. 1970. On the dentition of the sand shark, Odontaspis taurus, from the vicinity of Cananeia, Brazil. Boletim do Instituto Oceanografico, Sao Paulo 18: 37–44.Google Scholar
  70. Scattergood, L.W. 1962. White sharks, Carcharodon carcharias, in Maine, 1959–1960. Copeia 1962: 446–447.Google Scholar
  71. Scott, W.B. & M.G. Scott. 1988. Atlantic fishes of Canada. Can. Bull. Fish. Aqua. Sci. 219: 1–731.Google Scholar
  72. Seret, B. 1995. Premiere capture d'un requin grande gueule (Chondrichthyes, Megachasmidae) dans l'Atlantique, au large du senegal. Cybium 19: 425–427.Google Scholar
  73. Shann, E.W. 1923. The embryonic development of the porbeagle shark, Lamna cornubica. Proc. Zool. Soc. London 11: 161–171.Google Scholar
  74. Shimada, K. 2001. Dental homologies in lamniform sharks (Chondrichthyes: Elasmobranchii). J. Morphol. (in press).Google Scholar
  75. Smith, J.L.B. 1951. A juvenile of the man-eater, Carcharodon carcharias Linn. Ann. Mag. Nat. Hist., Ser. 12 4: 729–736.Google Scholar
  76. Smith, M.F.L. 1992. Capture and transportation of elasmobranchs, with emphasis on the gray nurse shark (Carcharias taurus). Aust. J. Mar. Freshwater Res. 43: 325–343.Google Scholar
  77. Springer, S. 1948. Oviphagous embryos of the sand shark, Carcharias taurus. Copeia 1948: 153–157.Google Scholar
  78. Springer, S. 1966. A review of Western Atlantic cat sharks, Scyliorhinidae, with descriptions of a new genus and five new species. U.S. Fish Wildlife Service, Fish. Bull. 65: 581–624.Google Scholar
  79. Springer, S. 1990. Alopiidae. p. 85. In: J.C. Quero, J.C. Hureau, C. Karrer, A. Post & L. Saldanha (ed.) Check-list of the Fishes of the Eastern Tropical Atlantic, Volume 1, Junta Nacional de Investigacao Cientifica e Tecnologica, Lisbon.Google Scholar
  80. Stead, D.G. 1963. Sharks and rays of Australian seas. Angus and Robertson, London. 211 pp.Google Scholar
  81. Stevens, J.D. 1983. Observations on reproduction in the shortfin mako Isurus oxyrinchus. Copeia 1983: 126–130.Google Scholar
  82. Stevens, J.D. 1987. Shark biology. pp. 50–75. In: J.D. Stevens (ed.) Sharks, Facts on File Publications, New York.Google Scholar
  83. Stevens, J.E. 1995. The delicate art of shark keeping. Sea Frontiers 14: 34–41 & 61.Google Scholar
  84. Swenander, G. 1907. Über die Ernahrung des Embryos der Lamna cornubica. Zoologiska Studier Tillagn T. Tullberg, Uppsala, pp. 283–288.Google Scholar
  85. Templeman, W. 1963. Distribution of sharks in the Canadian Atlantic (with special reference to Newfoundlandwaters). Bull. Fish. Res. Board Can. 140: 1–77.Google Scholar
  86. Uchida, S., M. Toda, K. Teshima & K. Yano. 1996. Pregnant white sharks and full-term embryos from Japan. pp. 139–155. In: A.P. Klimley & D.G. Ainley (ed.) Great White Sharks: The Biology of Carcharodon carcharias, Academic Press, San Diego.Google Scholar
  87. Uyeno, T. & Y. Matsushima. 1979. Comparative study of teeth from Naganuma Formation of Middle Pleistocene and Recent specimens of the great white shark, Carcharodon carcharias from Japan. Bull. Kanagawa Pref. Mus. 11: 11–30.Google Scholar
  88. Villavicencio-Garayzar, C.V. 1996. The ragged-tooth shark, Odontaspis ferox (Risso, 1810), in the Gulf of California. Calif. Fish Game 82: 195–196.Google Scholar
  89. Welton, B.J. & R.F. Farish. 1993. The collector's guide to fossil sharks and rays from the Cretaceous of Texas. Before Time, Lewisville. 204 pp.Google Scholar
  90. Wheeler, A. 1969. The fishes of the British Isles and north-west Europe. Macmillan and Company, London. 613 pp.Google Scholar
  91. Wourms, J.P., B.D. Grove & J. Lombardi. 1988. The maternal–embryonic relationship in viviparous fishes. pp. 1–134. In: W.S. Hoar & D.J. Randall (ed.) Fish Physiology, Vol. 11b, Academic Press, San Diego.Google Scholar

Copyright information

© Kluwer Academic Publishers 2002

Authors and Affiliations

  1. 1.Environmental Science Program and Department of Biological SciencesDePaul UniversityChicagoU.S.A.
  2. 2.Department of Biological SciencesUniversity of Illinois at ChicagoChicagoU.S.A.

Personalised recommendations