title: Bone cells in birds show exceptional surface area, a characteristic tracing back to saurischian dinosaurs of the late Triassic.
abstract: BACKGROUND
  Dinosaurs are unique among terrestrial tetrapods in their body sizes, which range from less than 3 gm in hummingbirds to 70,000 kg or more in sauropods. Studies of the microstructure of bone tissue have indicated that large dinosaurs, once believed to be slow growing, attained maturity at rates comparable to or greater than those of large mammals. A number of structural criteria in bone tissue have been used to assess differences in rates of osteogenesis in extinct taxa, including counts of lines of arrested growth and the density of vascular canals.
  
  
  RESULTS
  Here, we examine the density of the cytoplasmic surface of bone-producing cells, a feature which may set an upper limit to the rate of osteogenesis. Osteocyte lacunae and canaliculi, the cavities in bone containing osteocytes and their extensions, were measured in thin-sections of primary (woven and parallel fibered) bone in a diversity of tetrapods. The results indicate that bone cell surfaces are more densely organized in the Saurischia (extant birds, extinct Mesozoic Theropoda and Sauropodomorpha) than in other tetrapods, a result of denser branching of the cell extensions. The highest postnatal growth rates among extant tetrapods occur in modern birds, the only surviving saurischians, and the finding of exceptional cytoplasmic surface area of the cells that produce bone in this group suggests a relationship with bone growth rate. In support of this relationship is finding the lowest cell surface density among the saurischians examined in Dinornis, a member of a group of ratites that evolved in New Zealand in isolation from mammalian predators and show other evidence of lowered maturation rates.
authors.affiliation: Department of Earth and Space Sciences, University of Washington, Seattle, Washington, United States of America.
authors.forename: John M
authors.initials: JM
authors.lastname: Rensberger
authors.affiliation: Museo de Ciencias Naturales, Universidad Nacional de San Juan, San Juan, Argentina.
authors.forename: Ricardo N
authors.initials: RN
authors.lastname: Martínez
mesh_terms: D000818:Animals; D001717:Birds / Q000254:growth & development*; D049628:Body Size; D001842:Bone and Bones / Q000166:cytology*; D003593:Cytoplasm / Q000378:metabolism; D025061:Dinosaurs / Q000254:growth & development*; D010012:Osteogenesis; D013499:Surface Properties
references.citation: Nature. 2012 Jul 19;487(7407):358-61
references.pmid: 22763443
references.citation: Nature. 2000 Aug 10;406(6796):619-22
references.pmid: 10949300
references.citation: Bone. 2013 Nov;57(1):300-10
references.pmid: 23954754
references.citation: J Biophys Biochem Cytol. 1961 Dec 1;11(3):627-49
references.pmid: 19866598
references.citation: Nature. 2005 Jun 16;435(7044):940-3
references.pmid: 15959513
references.citation: Biol Rev Camb Philos Soc. 2014 Feb;89(1):24-47
references.pmid: 23647662
references.citation: J Biomech. 1995 Nov;28(11):1281-97
references.pmid: 8522542
references.citation: J Morphol. 2002 Dec;254(3):232-46
references.pmid: 12386894
references.citation: Nature. 1977 Sep 1;269(5623):80-2
references.pmid: 895891
references.citation: BMC Biol. 2012 Dec 14;10:101
references.pmid: 23241366
references.citation: Proc Natl Acad Sci U S A. 2007 Oct 2;104(40):15941-6
references.pmid: 17895377
references.citation: Am J Med Sci. 1998 Sep;316(3):189-95
references.pmid: 9749561
references.citation: C R Acad Sci III. 2000 Jun;323(6):543-50
references.pmid: 10923210
references.citation: C R Acad Sci III. 1996 Apr;319(4):301-8
references.pmid: 8762980
references.citation: Bone. 1985;6(5):335-7
references.pmid: 4096865
references.citation: J Biomech. 1987;20(3):261-70
references.pmid: 3584151
references.citation: Cell Tissue Res. 1986;246(1):125-31
references.pmid: 3779795
references.citation: Science. 1999 Jun 25;284(5423):2137-47
references.pmid: 10381873
references.citation: J Biomech. 2000 Feb;33(2):247-54
references.pmid: 10653041
references.citation: J Bone Joint Surg Am. 1984 Mar;66(3):397-402
references.pmid: 6699056
references.citation: J Exp Biol. 2004 Feb;207(Pt 5):869-79
references.pmid: 14747417
references.citation: J Biomech. 1994 Mar;27(3):339-60
references.pmid: 8051194
references.citation: Nature. 2001 Jul 26;412(6845):429-33
references.pmid: 11473315
references.citation: Calcif Tissue Int. 2009 May;84(5):388-404
references.pmid: 19234658
references.citation: Ital J Anat Embryol. 1998 Oct-Dec;103(4):145-55
references.pmid: 9882957
references.citation: J Cell Biol. 1963 Oct;19:19-32
references.pmid: 14069793
references.citation: Trends Ecol Evol. 2005 Apr;20(4):180-6
references.pmid: 16701366
references.citation: J Bone Miner Res. 1995 Feb;10(2):231-42
references.pmid: 7754802
references.citation: C R Biol. 2002 Mar;325(3):221-30
references.pmid: 12017770
references.citation: J Biomech Eng. 2000 Aug;122(4):387-93
references.pmid: 11036562
references.citation: Nature. 2004 Aug 12;430(7001):772-5
references.pmid: 15306807
references.citation: Ann Biomed Eng. 1994 May-Jun;22(3):280-92
references.pmid: 7978549
references.citation: Anat Rec A Discov Mol Cell Evol Biol. 2004 Jun;278(2):505-13
references.pmid: 15164337
references.citation: Nature. 2007 Mar 8;446(7132):180-4
references.pmid: 17344851
references.citation: J Biomech. 2000 Mar;33(3):317-25
references.pmid: 10673115
references.citation: Calcif Tissue Int. 2006 Nov;79(5):340-53
references.pmid: 17115241
references.citation: Ital J Anat Embryol. 1999 Jul-Sep;104(3):121-31
references.pmid: 10575824