The three-front model: A developmental explanation of long bone diaphyseal histology of Sauropoda

Biological Journal of the Linnean Society

Volumn 112, Issue 4, 2014, Pages 765-781

  Mitchell, Jessica ^a   Sander, P Martin ^a  

^a UNIVERSITY OF BONN   (Germany)

Author keywords

Apposition front; Haversian substitution front; Palaeohistology; Resorption front

Indexed keywords

EID: 84904577449     PISSN: 00244066     EISSN: 10958312     Source Type: Journal    
DOI: 10.1111/bij.12324     Document Type: Article

References (62)

1. Aguirre JI, Plotkin LI, Stewart SA, Weinstein RS, Parfitt AM, Manolagas SC, Bellido T. 2006. Osteocyte apoptosis is induced by weightlessness in mice and precedes osteoclast recruitment and bone loss. Journal of Bone and Mineral Research 21: 605-615.
2. Amprino R. 1947. La structure du tissu osseux envisagée comme expression de différences dans la vitesse de l'accroissement. Archives de Biologie 58: 317-330.
3. Ascenzi A, Bonucci E. 1967. The tensile properties of single osteons. The Anatomical Record 158: 375-386.
4. Burr DB, Martin RB. 1989. Errors in bone remodeling: toward a unified theory of metabolic bone disease. American Journal of Anatomy 186: 186-216.
5. Burr DB, Martin RB, Schaffler MB, Radin EL. 1985. Bone remodeling in response to in vivo fatigue microdamage. Journal of Biomechanics 18: 189-200.
6. Carballido JL, Sander PM. 2013. Postcranial axial skeleton of Europasaurus holgeri (Dinosauria, Sauropoda) from the Upper Jurassic of Germany: implications for sauropod ontogeny and phylogenetic relationships of basal Macronaria. Journal of Systematic Palaeontology 12: 335-387.
7. Cardoso L, Herman BC, Verborgt O, Laudier D, Majeska RJ, Schaffler MB. 2009. Osteocyte apoptosis controls activation of intracortical resorption in response to bone fatigue. Journal of Bone and Mineral Research 24: 597-605.
8. Castanet J, Curry Rogers K, Cubo J, Boisard J. 2000. Periosteal bone growth rates in extant ratites (ostriche and emu). Implications for assessing growth in dinosaurs. Comptes Rendus de l'Académie des Sciences-Séries III-Sciences de la Vie 323: 543-550.
9. Castanet J, Francillon-Vieillot H, Meunier FJ, de Ricqlès A. 1993. Bone and individual aging. In: Hall BK, ed. Bone, Vol. 7: bone growth. London: CRC Press, 245-283.
10. Chinsamy A, Raath MA. 1992. Preparation of fossil bone for histological examination. Palaeontologia africana 29: 39-44.
11. Cope ED. 1877. On a gigantic saurian from the Dakota Epoch of Colorado. Palaeontological Bulletin 25: 5-10.
12. Cubo J, Le Roy N, Martinez-Maza C, Montes L. 2012. Paleohistological estimation of bone growth rate in extinct archosaurs. Paleobiology 38: 335-349.
13. Currey JD. 1959. Differences in the tensile strength of bone of different histological types. Journal of Anatomy 93: 87-95.
14. Currey JD. 1962. Stress concentrations in bone. Quarterly Journal of Microscopical Science 3: 111-133.
15. Currey JD. 2002. Bones: structure and mechanics. Princeton, NJ: Princeton University Press.
16. Curry K. 1999. Ontogenetic histology of Apatosaurus (Dinosauria: Sauropoda): new insights on growth rates and longevity. Journal of Vertebrate Paleontology 19: 654-665.
17. Enlow DH, Brown SO. 1956. A comparative histological study of fossil and recent bone tissues. Part I. Texas. Journal of Science 8: 405-443.
18. Erickson GM. 2005. Assessing dinosaur growth patterns: a microscopic revolution. Trends in Ecology & Evolution 20: 677-684.
19. Francillon-Vieillot H, Buffrénil V de, Castanet J, Géraudie J, Meunier FJ, Sire JY, Zylberberg L, Ricqlès A de. 1990. Microstructure and mineralization of vertebrate skeletal tissues. In: Carter JG, ed. Skeletal biomineralization: patterns, processes and evolutionary trends. New York, NY: Van Nostrand Reinhold, 471-529.
20. Frost HM. 1969. Tetracycline-based histological analysis of bone remodeling. Calcified Tissue International 3: 211-237.
21. Gillooly JF, Allen AP, Charnov EL. 2006. Dinosaur fossils predict body temperatures. PLoS Biology 4: 1467-1469.
22. Griebeler EM, Klein N, Sander PM. 2013. Aging, maturation and growth of sauropodomorph dinosaurs as deduced from growth curves using long bone histological data: an assessment of methodological constraints and solutions. PLoS ONE 8: e67012.
23. Ham AW. 1953. Histology. Philadelphia, PA: Lippincott Company.
24. Hayashi S, Carpenter K, Suzuki D. 2009. Different growth patterns between the skeleton and osteoderms of Stegosaurus (Ornithischia: Thyreophora). Journal of Vertebrate Paleontology 29: 123-131.
25. Hedgecock NL, Hadi T, Chen AA, Curtiss SB, Martin RB, Hazelwood SJ. 2007. Quantitative regional associations between remodeling, modeling, and osteocyte apoptosis and density in rabbit tibial midshafts. Bone 40: 627-637.
26. Horner JR, de Ricqlès A, Padian K. 1999. Variation in dinosaur skeletochronology indicators: implications for age assessment and physiology. Paleobiology 25: 295-304.
27. Huttenlocker AK, Woodward HN, Hall BK. 2013. The biology of bone. In: Padian K, Lamm ET, eds. Bone histology of fossil tetrapods. Advancing methods, analysis, and interpretation. Berkeley, CA: University of California Press, 13-34.
28. Janensch W. 1914. Übersicht über die Wirbeltierfauna der Tendaguruschichten, nebst einer kurzer Charakterisierung der neu aufgeführten Arten von Sauropoden. Archiv für Biontologie 3: 81-110.
29. Klein N, Sander PM. 2007. Bone histology and growth of the prosauropod dinosaur Plateosaurus engelhardti von Meyer, 1837 from the Norian bonebeds of Trossingen (Germany) and Frick (Switzerland). Special Papers in Palaeontology 77: 169-206.
30. Klein N, Sander PM. 2008. Ontogenetic stages in the long bone histology of sauropod dinosaurs. Paleobiology 34: 247-263.
31. Klein N, Sander PM, Stein K, Le Loeuff J, Carballido JL, Buffetaut E. 2012. Modified laminar bone in Ampelosaurus atacis and other titanosaurs (Sauropoda): implications for life history and physiology. PLoS ONE 7: e36907.
32. Köhler M, Marín-Moratalla N, Jordana X, Aanes R. 2012. Seasonal bone growth and physiology in endotherms shed light on dinosaur physiology. Nature 487: 358-361.
33. Köhler M, Moyà-Solà S. 2004. Reduction of brain and sense organs in the fossil insular bovid Myotragus. Brain, Behavior and Evolution 63: 125-140.
34. Köhler M, Moyà-Solà S. 2009. Physiological and life history strategies of a fossil large mammal in a resource-limited environment. Proceedings of the National Academy of Sciences of the United States of America 106: 20354-20358.
35. Lee AH, Huttenlocker AK, Padian K, Woodward HN. 2013. Analysis of growth rates. In: Padian K, Lamm ET, eds. Bone histology of fossil tetrapods. Advancing methods, analysis, and interpretation. Berkeley, CA: University of California Press, 217-251.
36. Lehman TM, Woodward HN. 2008. Modeling growth rates for sauropod dinosaurs. Paleobiology 34: 264-281.
37. Linnaeus C. 1758. Systema naturæ per regna tria naturæ, secundum classes, ordines, genera, species, cum characteribus, differentiis, synonymis, locis. Stockholm: Salvius.
38. le Loeuff J. 1995. Ampelosaurus atacis (nov. gen., nov. sp.), a new titanosaurid (Dinosauria, Sauropoda) from the Late Cretaceous of the Upper Aude Valley (France). Comptes Rendus de l'Académie des Sciences - Série IIa - Sciences de la Terre et des planètes 321: 693-699.
39. de Margerie E, Cubo J, Castanet J. 2002. Bone typology and growth rate: testing and quantifying 'Amprino's rule' in the mallard (Anas platyrhynchos). Comptes Rendus Biologies 325: 221-230.
40. de Margerie E, Robin JP, Verrier D, Cubo J, Groscolas R, Castanet J. 2004. Assessing a relationship between bone microstructure and growth rate: a fluorescent labelling study in the king penguin chick (Aptenodytes patagonicus). Journal of Experimental Biology 207: 869-879.
41. Marsh OC. 1877. Notice of new dinosaurian reptiles from the Jurassic Formation. American Journal of Science XIV: 514-516.
42. Martin RB. 2003. Fatigue microdamage as an essential element of bone mechanics and biology. Calcified Tissue International 73: 101-107.
43. Mitchell J. 2012. Bone remodeling in sauropod dinosaurs: using secondary osteons as ontogenetic indicators. Master's Thesis, University of Bonn.
44. Mori S, Burr D. 1993. Increased intracortical remodeling following fatigue damage. Bone 14: 103-109.
45. Nopcsa F. 1914. Über das Vorkommen der Dinosaurier in Siebenbürgen. Verhandlungen der Zoologisch-Botanischen Gesellschaft Wien 54: 12-14.
46. van Oers RFM, Ruimerman R, Tanck E, Hilbers PAJ, Huiskes R. 2008. A unified theory for osteonal and hemi-osteonal remodeling. Bone 42: 250-259.
47. Padian K, Horner JR, de Ricqlès A. 2004. Growth in small dinosaurs and pterosaurs: the evolution of archosaurian growth strategies. Journal of Vertebrate Paleontology 24: 555-571.
48. Parfitt AM. 1981. Integration of skeletal and mineral homeostasis. In: Deluca H, Frost HM, Jee W, Johnston C, Parfitt A, eds. Osteoporosis. Recent advances in pathogenesis and treatment. Baltimore, MD: University Park Press, 115.
49. Parfitt AM. 2002. Targeted and nontargeted bone remodeling: relationship to basic multicellular unit origination and progression. Bone 30: 5-7.
50. Reid REH. 1987. Bone and dinosaurian 'endothermy'. Modern Geology 11: 133-154.
51. de Ricqlès A. 1968. Recherches paléohistologiques sur les os longs des tétrapodes: origine du tissu osseux plexiforme des dinosauriens sauropodes. Annales de Paléontologie 54: 133-145.
52. de Ricqlès A. 1975. Recherches paléohistologiques sur les os longs des tétrapodes VII.Sur la classification, la signification fonctionnelle et l'histoire des tissus osseux des tétrapodes. Annales de Paléontologie 61: 51-129.
53. Sander PM. 2000. Longbone histology of the Tendaguru sauropods: implications for growth and biology. Paleobiology 26: 466-488.
54. Sander PM, Andrassy P. 2006. Lines of arrested growth and long bone histology in Pleistocene large mammals from Germany: what do they tell us about dinosaur physiology? Palaeontographica Abteilung A 277: 143-159.
55. Sander PM, Klein N, Stein K, Wings O. 2011. Sauropod bone histology and implications for sauropod biology. In: Klein N, Remes K, Gee CT, Sander PM, eds. Biology of the sauropod dinosaurs. Understanding the life of giants. Bloomington, IN: Indiana University Press, 276-302.
56. Sander PM, Mateus O, Laven T, Knötschke N. 2006. Bone histology indicates insular dwarfism in a new Late Jurassic sauropod dinosaur. Nature 441: 739-741.
57. Starck JM, Chinsamy A. 2002. Bone microstructure and developmental plasticity in birds and other dinosaurs. Journal of Morphology 254: 232-246.
58. Stein K, Csiki Z, Rogers KC, Weishampel DB, Redelstorff R, Carballido JL, Sander PM. 2010. Small body size and extreme cortical bone remodeling indicate phyletic dwarfism in Magyarosaurus dacus (Sauropoda: Titanosauria). Proceedings of the National Academy of Sciences of the United States of America 107: 9258-9263.
59. Stein K, Prondvai E. 2013. Rethinking the nature of fibrolamellar bone: an integrative biological revision of sauropod plexiform bone formation. Biological Reviews 89: 24-47.
60. Stein K, Sander PM. 2009. Histological core drilling: a less destructive method for studying bone histology. In: Brown MA, Kane JF, Parker WG, eds. Methods in fossil prepraration: proceedings of the first annual fossil preparation and collections symposium, 69-80.
61. Werning S. 2012. The ontogenetic osteohistology of Tenontosaurus tilletti. PLoS ONE 7: e33539.
62. Wilson JW, Leiggi P, May P. 1994. Histological techniques. Vertebrate Paleontological Techniques 1: 205-234.