Hostname: page-component-586b7cd67f-dlnhk Total loading time: 0 Render date: 2024-12-02T18:08:49.241Z Has data issue: false hasContentIssue false

Bone histology of the ichthyosaurs: comparative data and functional interpretation

Published online by Cambridge University Press:  08 April 2016

Vivian de Buffrénil
Affiliation:
Equipe “Formations Squelettiques” (Unité Associée au CNRS n°1137), Laboratoire d’Anatomie Comparée, Muséum National d'Histoire Naturelle, 55 rue Buffon 75005 Paris, FRANCE
Jean-Michel Mazin
Affiliation:
Unité Associée au CNRS n°720, Laboratoire de Paléontologie des Vertébrés et de Paléontologie Humaine, Université Paris 6, 4 place Jussieu 75252 Paris cedex 05, FRANCE

Abstract

The periosteal cortex in the shaft of limb bones is described histologically in three ichthyosaurian genera, Omphalosaurus, Stenopterygius, and Ichthyosaurus. The primary periosteal deposits are composed of typical woven-fibered tissue that was accreted as spongy bone in young individuals, and more or less compact bone in older individuals. During growth, the bone tissue was extensively remodeled with a quantitative imbalance between resorption and redeposition. As a result, the cortex was made cancellous, if previously compact, or still more spongy, if already cancellous. This pattern of remodeling explains why compact cortices are generally lacking in the long bones of ichthyosaurs. The presence of woven-fibered tissue strongly suggests that the limb bones, and probably also the body as a whole, had a rapid postnatal growth in ichthyosaurs, that might have been related to a high, “endotherm-like” metabolic rate. This hypothesis bears on the ecological interpretation of the ichthyosaurs: they could have been capable of sustained, fast swimming and long-range movements, rather than being slow-moving creatures as commonly supposed.

Type
Research Article
Copyright
Copyright © The Paleontological Society 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Literature Cited

Amprino, R. 1947. La structure du tissu osseux envisagée comme l'expression de différences dans la vitesse de l'accroissement. Archives de Biologie 58:315330.Google Scholar
Birkenmeier, E. 1971. Juvenile leathery turtles, Dermochelys coriacea (Linnaeus), in captivity. Brunei Museum Journal 2:160172.Google Scholar
Braun, J., and Reif, W.-E. 1985. A survey of aquatic locomotion in fishes and tetrapods. Neues Jahrbüch Geologie Paläontologie Abhandlungen 169:307332.Google Scholar
Brodie, P. F. 1977. Form, function and energetics of Cetacea: A discussion. Pp. 4558. In Harrisson, R. J. (ed.): Functional anatomy of marine mammals, vol. 3. Academic Press; New York.Google Scholar
Buffrénil, V. de. 1980. Mise en évidence de l'incidence des conditions de milieu sur la croissance de Crocodylus siamensis (Schneider, 1801) et valeur des marques de croissance squelettiques pour l'évaluation de l'âge. Archives de Zoologie Expérimentale et Générale 121:6376.Google Scholar
Buffrénil, V. de, and Schoevaert, D. 1988. On how the periosteal bone of the delphinid humerus becomes cancellous: ontogeny of an histological specialization. Journal of Morphology 198:149164.Google Scholar
Buffrénil, V. de, and Schoevaert, D. 1989. Données quantitatives et observations histologiques sur la pachyothose du squelette du Dugong (Dugong dugon) (Müller) (Sirenia, Dugongidae). Canadian Journal of Zoology 67(9):21072119.Google Scholar
Buffrénil, V. de, Collet, A., and Pascal, M. 1985. Ontogenetic development of skeletal weight in a small delphinid, Delphinus delphis L. Zoomorphology 105:336344.Google Scholar
Buffrénil, V. de, Sire, J.-Y., and Schoevaert, D. 1986. Comparaison de la structure et du volume squelettiques entre un delphinidé (Delphinus delphis L.) et un mammifère terrestre (Panthera leo L.). Canadian Journal of Zoology 64:17501756.Google Scholar
Buffrénil, V. de, Mazin, J.-M., and de Ricqlès, A. 1987. Caractères structuraux et mode de croissance du fémur d'Omphalosaurus nisseri, ichthyosaurien du Trias moyen du Spitsberg. Annales de Paléontologie (Vertébrés) 73:195216.Google Scholar
Carey, F. D., Teal, J. M., Kanwisher, J. W., Lawson, K. D., and Beckett, J. S. 1971. Warm-bodied fishes. American Zoologist 11:137145.Google Scholar
Carey, F. D., and Lawson, K. D. 1973. Temperature regulation in free-swimming bluefin tuna. Comparative Biochemistry and Physiology 44A:375392.CrossRefGoogle Scholar
Carroll, R. L. 1985. Evolutionary constraints in aquatic diapsid reptiles. Special Papers in Paleontology 33:145155.Google Scholar
Castanet, J. 1982. Recherches sur la croissance du tissu osseux des Reptiles. Applications: la méthode squelettochronologique. Unpublished thesis, Paris 7 University; Paris, France.Google Scholar
Castanet, J., Meunier, F. J., and de Ricqlès, A. 1977. L'enregistrement de la croissance cyclique par le tissu osseux chez les vertébrés poikilothermes: données comparatives et essai de synthèse. Bulletin Biologique de la France et de la Belgique 3:183202.Google Scholar
Enlow, D. H. 1963. Principles of Bone Remodeling. C. C. Thomas; Springfield, Massachusetts.Google Scholar
Enlow, D. H. 1969. The bone of reptiles. Pp. 4580. In Gans, C., and Bellairs, A. (eds.), Biology of the Reptilia. Morphology, Volume 1. Academic Press; New York.Google Scholar
Enlow, D. H., and Brown, S. O. 1957. A comparative histological study of fossil and recent bone tissues. Part 2. Texas Journal of Science 9:186214.Google Scholar
Fawcett, D. W. 1942. The amedullary bones of the Florida manatee (Trichechus latirostris). American Journal of Anatomy 71:271309.CrossRefGoogle Scholar
Felts, W.J.L. 1966. Some functional and structural characteristics of cetacean flippers and flukes. Pp. 255276. In Norris, K. S. (ed.), Whales, Dolphins and Porpoises. University of California Press; Berkeley, California.Google Scholar
Felts, W.J.L., and Spurrell, F. A. 1965. Structural orientation and density in cetacean humeri. American Journal of Anatomy 116:171203.Google Scholar
Felts, W.J.L., and Spurrell, F. A. 1966. Some structural and developmental characteristics of cetacean (Odontocete) radii. A study of adaptative osteogenesis. American Journal of Anatomy 118:103134.Google Scholar
Frair, W., Ackman, R. G., and Mrosowski, N. 1972. Body temperature of Dermochelys coriacea: warm turtle from cold water. Science 117:791793.CrossRefGoogle Scholar
Freytey, J. 1978. Mensurations de tortues-luths femelles adultes, Dermochelys coriacea (Linné), en Guyane française. Bulletin de la Société Zoologique de France 103:518523.Google Scholar
Frost, H. M. 1960. Observations on fibrous and lamellar bone. Henry Ford Hospital Medical Bulletin 8:199207.Google Scholar
Greer, A. E., Lazell, J. D. Jr. and Wright, R. M. 1973. Anatomical evidence for a counter-current heat exchanger in the leatherback turtle (Dermochelys coriacea). Nature 244:181.Google Scholar
Gross, W. 1934. Die Typen des mikroskopischen Knochenbaues bei fossilen Stegocephalen and Reptilien. Zeitschrift für Anatomie 103:731764.Google Scholar
Kiprijanoff, A. V. 1881–1883. Studien über die fossilen Reptilien Russlands. Mémoires de l'Académie Impériale des Sciences de St. Petersbourg, 7ème séries Volumes 28–31.Google Scholar
Lighthill, M. J. 1969. Hydromechanics of aquatic animal propulsion: a survey. Annual Review of Fluid Mechanics 1:413446.Google Scholar
Lindsey, C. C. 1978. Form, function and locomotory habits in fish. Pp. 1100. In Hoar, W. S., and Randall, D. J. (eds.), Fish Physiology, Volume 7: Locomotion. Academic Press; London and New York.Google Scholar
Magnusson, J. J. 1978. Locomotion by Scombroid fishes: hydromechanics, morphology, and behaviour. Pp. 240315. In Hoar, W. S., and Randall, D. J. (eds.), Fish Physiology, Volume 7: Locomotion. Academic Press; London and New York.Google Scholar
Massare, J. A. 1988. Swimming capabilities of Mesozoic marine reptiles: implications for methods of predation. Paleobiology 14:187205.CrossRefGoogle Scholar
Mazin, J.-M. 1983. Omphalosaurus nisseri (Wiman 1981), un ichthyopterygien à denture broyeuse du Trias moyen du Spitsberg. Bulletin du Muséum National d'Histoire Naturelle de Paris, 4ème séries 5:242263.Google Scholar
Mazin, J.-M., and Bucher, H. 1987. Omphalosaurus nettarhynchus, une nouvelle espèce d'Omphalosauridé (Reptilia, Ichthyopterygia) du Spathien de la Humboldt Range (Nevada, USA). Comptes-rendus de l'Académie des Sciences (Paris), Série II. 305:823828.Google Scholar
McGowan, C. 1973. Differential growth in three ichthyosaurs: Ichthyosaurus communis, I. breviceps and Stenopterygius quadriscissus (Reptilia, Ichthyosauria). Life Sciences Contributions of the Royal Ontario Museum 93:121.Google Scholar
McGowan, C. 1979. A revision of the lower Jurassic ichthyosaurs of Germany, with descriptions of two new species. Paleontographica 166:93135.Google Scholar
Murray, P.D.F. 1985. Bones. Second Edition. Cambridge University Press; Cambridge.Google Scholar
Nemerski, J., Harsanyi, L., and Ascadi, G. 1960. Methoden zur Diagnose des Lebensaltens von Skelettfunden. Anthropologische Anzeiger 24:7095.Google Scholar
Nopcsa, F. von, and Heidsieck, E. 1934. Ueber eine pachyostotische Rippe aus der Kreide Rügens. Acta Zoologica 15:431455.Google Scholar
Oemichen, E. 1938. Essai sur la dynamique des ichthyosauriens Longipinnati et particulièrement d'Ichthyosaurus burgundiae (Gaud.). Annales de Paléontologie 27:90114.Google Scholar
Paladino, F. V., O'Connor, M. P., and Spotila, J. R. 1990. Metabolism of leatherback turtles, gigantothermy, and thermoregulation of dinosaurs. Nature 344:858860.Google Scholar
Peabody, F. E. 1961. Annual growth zones in living and fossil vertebrates. Journal of Morphology 108:1162.Google Scholar
Pritchard, J. J. 1956. General anatomy and histology of bone. Pp. 125. In Bourne, C. G. (ed.), The Biochemistry and Physiology of Bone, Volume 1. Academic Press; London and New York.Google Scholar
Quenstedt, F. A. 1858. Der Jura. Laupp; Tübingen, Germany.Google Scholar
Rhodin, A.G.J. 1985. Comparative chondro-osseous development and growth of marine turtles. Copeia 1985:752771.Google Scholar
Rhodin, A.G.J., Ogden, J. A., and Conlogue, G. J. 1981. Chondro-osseous morphology of Dermochelys coriacea, a marine reptile with mammalian skeletal features. Nature 290:244246.CrossRefGoogle Scholar
Ricqlès, A. de. 1969. L'histologie osseuse envisagée comme indicateur de la physiologie thermique chez les tétrapodes fossiles. Comptes rendus de l'Académie des Sciences (Paris), Série D 268:782785.Google Scholar
Ricqlès, A. de. 1972. Vers une histoire de la physiologie thermique. Les données histologiques et leur interprétation fonctionnelle. Compte Rendus de l'Académie des Sciences (Paris), Série D 275:17451748.Google Scholar
Ricqlès, A. de. 1974. Evolution of endothermy: histological evidence. Evolution Theory 1:5180.Google Scholar
Ricqlès, A. de. 1975. Recherches paléohistologiques sur les os longs des Tétrapodes. VII. Sur la classification, la signification fonctionnelle et l'histoire des tissus osseux des Tétrapodes (première partie). Annales de Paléontologie (Vertébrés) 61:51129.Google Scholar
Ricqlès, A. de. 1976a. On bone histology of fossil and living reptiles, with comments on its functional and evolutionary significance. Pp. 123150. In Bellairs, A., and Cox, C. B. (eds.), Morphology and Biology of Reptiles. Linnean Society Symposium Series 33. Academic Press; London and New York.Google Scholar
Ricqlès, A. de. 1976b. Recherches paléohistologiques sur les os longs des Tétrapodes. VII. Sur la classification, la signification fonctionnelle et l'histoire des tissus osseux des Tétrapodes (deuxième partie). Annales de Paléontologie (Vertébrés) 62:71126.Google Scholar
Ricqlès, A. de. 1977. Recherches paléohistologiques sur les os longs des Tétrapodes: sur la classification; la signification fonctionnelle et l'histoire des tissus osseux des Tétrapodes (deuxième partie, suite). Annales de Paléontologie (Vertébrés) 63:3356, 133–160.Google Scholar
Ricqlès, A. de. 1978. Recherches paléohistologiques sur les os longs des Tétrapodes. VII. Evolution des tissus osseux des Tétrapodes. Annales de Paléontologie (Vertébrés) 64:85111, 153–184.Google Scholar
Ricqlès, A. de. 1979. Quelques remarques sur l'histoire évolutive des tissus squelettiques chez les Vertébrés et plus particulièrement chez les Tétrapodes. Année Biologique 18:135.Google Scholar
Ricqlès, A. de. 1989. Les mécanismes hétérochroniques dans le retour des Tétrapodes au milieu aquatique. Geobios, Mémoire Spécial 12:337348.Google Scholar
Riess, J. 1984. Biomechanics of ichthyosaurs. Pp. 199205. In Reif, W. E., and Westphal, F. (eds.), Third Symposium on Mesozoic Terrestrial Ecosystems. Attempto Verlag; Tübingen, Germany.Google Scholar
Riess, J. 1986. Fortbewegunsweise, Schwimmbiophysic und Phylogenie der Ichthyosaurier. Palaeontographica A 192:93155.Google Scholar
Seitz, A. L. 1907. Vergleichende Studien über den mikroscopischen Knochenbau fossilen und rezenten Reptilien. Nova Acta Kaiser Leop.-Carol. Deutschen Akademie für Naturforschung 37:230370.Google Scholar
Stevens, E., and Neill, W. H. 1978. Body temperature relations of tunas, especially Skipjack. Pp. 316360. In Hoar, W. S., and Randall, D. J. (eds.), Fish Physiology, Volume 7: Locomotion. Academic Press; London and New York.Google Scholar
Warren, J. W. 1963. Growth zones in the skeleton of recent and fossil vertebrates. Unpublished Ph. D. Thesis, University of California, Los Angeles.Google Scholar
Webb, P. W., and Skadsen, J. M. 1979. Reduced skin mass: an adaptation for acceleration in some teleost fishes. Canadian Journal of Zoology 57:15701575.Google Scholar
Wiman, C. 1910. Ichthyosaurier aus der Trias Spitsbergens. Bulletin of the Geological Institute of the University of Upsala 10:124148.Google Scholar
Witham, R. 1977. Dermochelys coriacea in captivity. Marine Turtle Newsletter 3:6.Google Scholar