全部 标题 作者
关键词 摘要

OALib Journal期刊
ISSN: 2333-9721
费用:99美元

查看量下载量

相关文章

更多...
PLOS ONE  2012 

Bone Histology in Dysalotosaurus lettowvorbecki (Ornithischia: Iguanodontia) – Variation, Growth, and Implications

DOI: 10.1371/journal.pone.0029958

Full-Text   Cite this paper   Add to My Lib

Abstract:

Background Dysalotosaurus lettowvorbecki is a small ornithopod dinosaur known from thousands of bones and several ontogenetic stages. It was found in a single locality within the Tendaguru Formation of southeastern Tanzania, possibly representing a single herd. Dysalotosaurus provides an excellent case study for examining variation in bone microstructure and life history and helps to unravel the still mysterious growth pattern of small ornithopods. Methodology/Principal Findings Five different skeletal elements were sampled, revealing microstructural variation between individuals, skeletal elements, cross sectional units, and ontogenetic stages. The bone wall consists of fibrolamellar bone with strong variability in vascularization and development of growth cycles. Larger bones with a high degree of utilization have high relative growth rates and seldom annuli/LAGs, whereas small and less intensively used bones have lower growth rates and a higher number of these resting lines. Due to the scarcity of annuli/LAGs, the reconstruction of the life history of Dysalotosaurus was carried out using regularly developed and alternating slow and fast growing zones. Dysalotosaurus was a precocial dinosaur, which experienced sexual maturity at ten years, had an indeterminate growth pattern, and maximum growth rates comparable to a large kangaroo. Conclusions/Significance The variation in the bone histology of Dysalotosaurus demonstrates the influence of size, utilization, and shape of bones on relative growth rates. Annuli/LAGs are not the only type of annual growth cycles that can be used to reconstruct the life history of fossil vertebrates, but the degree of development of these lines may be of importance for the reconstruction of paleobehavior. The regular development of annuli/LAGs in subadults and adults of large ornithopods therefore reflects higher seasonal stress due to higher food demands, migration, and altricial breeding behavior. Small ornithopods often lack regularly developed annuli/LAGs due to lower food demands, no need for migration, and precocial behavior.

References

[1]  Lehman TM (2007) Growth and population age structure in the horned dinosaur Chasmosaurus. In: Carpenter K, editor. Horns and beaks: ceratopsian and ornithopod dinosaurs. Bloomington: Indiana University Press. pp. 259–317.
[2]  Sampson SD, Ryan MJ, Tanke DH (1997) Craniofacial ontogeny in centrosaurine dinosaurs (Ornithischia: Ceratopsidae): taxonomic and behavioural implications. Zool J Linn Soc 121: 293–337.
[3]  Tumarkin-Deratzian AR (2003) Bone surface textures as ontogenetic indicators in extant and fossil archosaurs: Macroscopic and histological evaluations. 333 p. PhD Thesis. Philadelphia: University of Pennsylvania.
[4]  Tumarkin-Deratzian AR (2009) Evaluation of long bone surface textures as ontogenetic indicators in centrosaurine ceratopsids. Anat Rec 292: 1485–1500.
[5]  Castanet J, Francillon-Vieillot H, Meunier FJ, de Ricqlès A (1993) Bone and individual aging. In: Hall BK, editor. Bone. Volume 7: Bone growth - B. Boca Raton: CRC Press. pp. 245–283.
[6]  Chinsamy-Turan A (2005) The microstructure of dinosaur bone – Deciphering biology with fine-scale techniques. Baltimore/London: Johns Hopkins University Press. 195 p.
[7]  Erickson GM (2005) Assessing dinosaur growth patterns: a microscopic revolution. Trends Ecol Evol 20(12): 677–684.
[8]  Francillon-Vieillot H, de Buffrénil V, Castanet J, Géraudie J, Meunier FJ, et al. (1990) Microstructure and mineralization of vertebrate skeletal tissues. In: Carter JE, editor. Skeletal biomineralization: Patterns, processes and evolutionary trends. New York: Van Nostrand Reinhold. pp. 471–530.
[9]  Hübner TR (2011) Ontogeny in Dysalotosaurus lettowvorbecki. 318 p. PhD Thesis. Munich: Ludwig Maximilians Universit?t.
[10]  de Ricqlès A, Meunier FJ, Castanet J, Francillon-Vieillot H (1991) Comparative microstructure of bone. In: Hall BK, editor. Bone. Volume 3: Bone matrix and bone specific products. Boca Raton: CRC Press. pp. 1–78.
[11]  Janensch W (1914) Die Gliederung der Tendaguru-Schichten im Tendaguru-Gebiet und die Entstehung der Saurier-Lagerst?tten. Arch Biont 3(3): 227–261.
[12]  Maier G (2003) African Dinosaurs Unearthed. Bloomington: Indiana University Press. 512 p.
[13]  Bussert R, Heinrich W-D, Aberhan M (2009) The Tendaguru Formation (Late Jurassic to Early Cretaceous, southern Tanzania): definition, palaeoenvironments, and sequence stratigraphy. Fossil Record 12(2): 141–174.
[14]  Heinrich W-D (1999) The taphonomy of dinosaurs from the Upper Jurassic of Tendaguru (Tanzania) based on field sketches of the German Tendaguru Expedition (1909–1913). Mitt Mus Natkd Berl, Geowiss Reihe 2: 25–61.
[15]  Reck H (1925) Grabungen auf fossile Wirbeltiere in Deutsch-Ostafrika. Geol Char 31: 1–36.
[16]  Russell D, Beland F, McIntosh JS (1980) Paleoecology of the dinosaurs of Tendaguru (Tanzania). Mem Soc Geol France 59(139): 169–175.
[17]  Aberhan M, Bussert R, Heinrich W-D, Schrank E, Schultka S, et al. (2002) Paleoecology and depositional environments of the Tendaguru Beds (Late Jurassic to Early Cretaceous, Tanzania). Mitt Mus Natkd Berl, Geowiss Reihe 2: 201–205.
[18]  Chinsamy A (1995) Ontogenetic changes in the bone histology of the Late Jurassic ornithopod Dryosaurus lettowvorbecki. J Vert Pal 15(1): 96–104.
[19]  Galton P (1977) The ornithopod dinosaur Dryosaurus and a Laurasia-Gondwanaland connection in the Upper Jurassic. Nature 268: 230–232.
[20]  Hübner TR, Rauhut OWM (2010) A juvenile skull of Dysalotosaurus lettowvorbecki (Ornithischia: Iguanodontia), and implications for cranial ontogeny, phylogeny, and taxonomy in ornithopod dinosaurs. Zool J Linn Soc 160: 366–396.
[21]  Hutton JM (1986) Age determination of living Nile crocodiles from the cortical stratification of bone. Copeia 1986(2): 332–341.
[22]  Klevezal GA (1996) Recording structures of mammals: Determination of age and reconstruction of life history. Rotterdam: Balkema. 274 p.
[23]  Peabody FE (1961) Annual growth zones in living and fossil vertebrates. J Morph 108: 11–62.
[24]  Botha J, Chinsamy A (2000) Growth patterns from the bone histology of the cynodonts Diademodon and Cynognathus. J Vert Pal 20: 705–711.
[25]  Chinsamy A (1990) Physiological implications of the bone histology of Syntarsus rhodesiensis (Saurischia: Theropoda). Palaeont Afr 27: 77–82.
[26]  Erickson GM, Brochu CA (1999) How the “terror crocodile” grew so big. Nature 398: 205–206.
[27]  Erickson GM, Tumanova TA (2000) Growth curve of Psittacosaurus mongoliensis Osborn (Ceratopsia: Psittacosauridae) inferred from long bone histology. Zool J Linn Soc 130: 551–566.
[28]  Horner JR, Padian K (2004) Age and growth dynamics of Tyrannosaurus rex. Proc R Soc Lond B 271: 1875–1880.
[29]  Sander PM, Mateus O, Laven T, Kn?tschke N (2006) Bone histology indicates insular dwarfism in a new Late Jurassic sauropod dinosaur. Nature 441: 739–741.
[30]  Varricchio DJ (1993) Bone microstructures of the Upper Cretaceous theropod dinosaur Troodon formosus. J Vert Pal 13: 99–104.
[31]  Castanet J, Meunier FJ, de Ricqlès A (1977) L'enregistrement de la croissance cyclique par le tissu osseux chez les vertebres poikilothermes: donnees comparatives et essai de synthese. Bull Biol Fr Belg 111: 183–202.
[32]  Klein N (2004) Bone histology and growth of the prosauropod dinosaur Plateosaurus engelhardti Meyer 1837 from the Norian bonebeds of Trossingen (Germany) and Frick (Switzerland). 128 p. PhD Thesis. Bonn: Rheinische Friedrich-Wilhelms-Universit?t.
[33]  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). Spec Pap Pal 77: 169–206.
[34]  Werning S (2005) Long bone histology of Tenontosaurus tilletti Ostrom 1970 (Early Cretaceous, North America), with comments on ontogeny. 150 p. Master's Thesis. Norman: University of Oklahoma.
[35]  Chinsamy A (1993) Bone histology and growth trajectory of the prosauropod dinosaur Massospondylus carinatus Owen. Mod Geol 18: 319–329.
[36]  Horner JR, de Ricqlès A, Padian K (2000) Long bone histology of the hadrosaurid dinosaur Maiasaura peeblesorum: growth dynamics and physiology based on an ontogenetic series of skeletal elements. J Vert Pal 20(1): 115–129.
[37]  de Ricqlès A (1983) Cyclical growth in the long limb bones of a sauropod dinosaur. Acta Pal Pol 28: 225–232.
[38]  Horner JR, de Ricqlès A, Padian K (1999) Variation in dinosaur skeletochronology indicators: implications for age assessment and physiology. Paleobiology 25(3): 295–304.
[39]  Amprino R (1947) La structure du tissu osseux envisagèe comme expression de differences dans la vitesse de l' accroisement. Arch Biol 58: 315–330.
[40]  de Buffrenil V, Houssaye A, B?hme W (2008) Bone vascular supply in monitor lizards (Squamata: Varanidae): Influence of size, growth, and phylogeny. J Morph 269: 533–543.
[41]  Castanet J, Curry Rogers K, Cubo J, Boisard J-J (2000) Periosteal bone growth rates in extant ratites (ostriches and emu). Implications for assessing growth in dinosaurs. C R Acad Sci Paris, Sci Vie 323: 543–550.
[42]  Erickson GM, Makovicky PJ, Currie PJ, Norell MA, Yerby SA, et al. (2004) Gigantism and comparative life-history parameters of tyrannosaurid dinosaurs. Nature 430: 772–775.
[43]  Padian K, Horner JR, de Ricqlès A (2004) Growth in small dinosaurs and pterosaurs: the evolution of archosaurian growth strategies. J Vert Pal 24(4): 555–571.
[44]  Turvey ST, Green OR, Holdaway RN (2005) Cortical growth marks reveal extended juvenile development in New Zealand moa. Nature 435: 940–943.
[45]  Starck JM, Chinsamy A (2002) Bone microstructure and developmental plasticity in birds and other dinosaurs. J Morph 254: 232–246.
[46]  de Margerie E, Cubo J, Castanet J (2002) Bone typology and growth rate: Testing and quantifying “Amprino's rule” in the mallard (Anas platyrhynchos). C R Acad Sci Paris, Biol 325: 221–230.
[47]  de Margerie E, Robin J-P, Verrier D, Cubo J, Groscolas R, et al. (2004) Assessing the relationship between bone microstructure and growth rate: A fluorescent labelling study in the king penguin chick (Aptenodytes patagonicus). J Exp Biol 207: 869–879.
[48]  Chinsamy A, Rich T, Vickers-Rich P (1998) Polar dinosaur bone histology. J Vert Pal 18: 385–390.
[49]  Cooper LN, Lee AH, Taper ML, Horner JR (2008) Relative growth rates of predator and prey dinosaurs reflect effects of predation. Proc R Soc Lond B. doi:10.1098/rspb.2008.0912.
[50]  Horner JR, Currie PJ (1994) Embryonic and neonatal morphology and ontogeny of a new species of Hypacrosaurus (Ornithischia, Lambeosaurinae) from Montana and Alberta. In: Carpenter K, Hirsch KF, Horner JR, editors. Dinosaur eggs and babies. Cambridge: Cambridge University Press. pp. 312–336.
[51]  Horner JR, Padian K, de Ricqlès A (2001) Comparative osteohistology of some embryonic and perinatal archosaurs: developmental and behavioral implications for dinosaurs. Paleobiology 27: 39–58.
[52]  Horner JR, de Ricqlès A, Padian K, Scheetz RD (2009) Comparative long bone histology and growth of the ‘Hypsilophodontid” dinosaurs Orodromeus makelai, Dryosaurus altus, and Tenontosaurus tilletti (Ornithischia: Euornithopoda). J Vert Pal 29(3): 734–747.
[53]  Scheetz RD (1999) Osteology of Orodromeus makelai and the phylogeny of basal ornithopod dinosaurs. 186 p. PhD Thesis. Bozeman: Montana State University.
[54]  Cerda IA, Chinsamy-Turan A (2008) Bone histology of Gasparinisaura cincosaltensis, a basal ornithopod dinosaur from the Upper Cretaceous of Patagonia. Ameghiniana 45(4): 24R.
[55]  Winkler DA (1994) Aspects of growth in the Early Cretaceous Proctor Lake ornithopod. J Vert Pal 14(3): 53A.
[56]  Curry KA (1999) Ontogenetic histology of Apatosaurus (Dinosauria: Sauropoda): New insights on growth rates and longevity. J Vert Pal 19(4): 654–665.
[57]  Sander PM (2000) Long bone histology of the Tendaguru sauropods: implications for growth and biology. Paleobiology 26(3): 466–488.
[58]  Woodward HN, Lehman TM (2009) Bone histology and microanatomy of Alamosaurus sanjuanensis (Sauropoda: Titanosauria) from the Maastrichtian of Big Bend National Park, Texas. J Vert Pal 29(3): 807–821.
[59]  Lee AH (2004) Histological organization and its relationship to function in the femur of Alligator mississippiensis. J Anat 204: 197–207.
[60]  Chinsamy A, Tumarkin-Deratzian A (2009) Pathologic bone tissues in a turkey vulture and a nonavian dinosaur: Implications for interpreting endosteal bone and radial fibrolamellar bone in fossil dinosaurs. Anat Rec 292: 1478–1484.
[61]  Holmes JR (1958) Experimental transmission of avian osteopetrosis. J Comp Pathol 68: 439–451.
[62]  Lee AH, Werning S (2008) Sexual maturity in growing dinosaurs does not fit reptilian growth models. Proc Nat Acad Sci 105: 582–587.
[63]  Schweitzer MH, Wittmeyer JL, Horner JR (2005) Gender-specific reproductive tissue in ratites and Tyrannosaurus rex. Science 308: 1456–1460.
[64]  Anderson JF, Hall-Martin A, Russell DA (1985) Long-bone circumference and weight in mammals, birds and dinosaurs. J Zool Lond 207: 53–61.
[65]  Ray S, Chinsamy A (2004) Diictodon feliceps (Therapsida, Dicynodontia): Bone histology, growth, and biomechanics. J Vert Pal 24(1): 180–194.
[66]  Enlow DH, Brown SO (1958) A comparative histological study of fossil and recent bone tissues. Part III. Tex J Sci 10: 187–230.
[67]  de Ricqlès AJ, Padian K, Horner JR, Francillon-Vieillot H (2000) Palaeohistology of the bones of pterosaurs (Reptilia: Archosauria): anatomy, ontogeny, and biomechanical implications. Zool J Linn Soc 129(3): 349–385.
[68]  Bybee PJ, Lee AH, Lamm E-T (2006) Sizing the Jurassic theropod dinosaur Allosaurus: assessing growth strategy and evolution of ontogenetic scaling of limbs. J Morph 267(3): 347–359.
[69]  Botha J, Chinsamy A (2005) Growth patterns of Thrinaxodon liorhinus, a non-mammalian cynodont from the Lower Triassic of South Africa. Palaeontology 48(2): 385–394.
[70]  Ray R, Botha J, Chinsamy A (2004) Bone histology and growth patterns of some nonmammalian therapsids. J Vert Pal 24: 634–648.
[71]  Enlow DH (1962) A Study of the Post-Natal Growth and Remodeling of Bone. Am J Anat 110: 79–101.
[72]  Chinsamy A, Hurum JH (2006) Bone microstructure and growth patterns of early mammals. Acta Pal Pol 51(2): 325–338.
[73]  Reid REH (1984) The histology of dinosaurian bone, and its possible bearing on dinosaur physiology. Symp Zool Soc Lond 52: 629–662.
[74]  Currey JD (1984) Comparative Mechanical Properties and Histology of Bone. Am Zool 24: 5–12.
[75]  Erickson GM, Rogers KC, Varricchio DJ, Norell MA, Xu X (2007) Growth patterns in brooding dinosaurs reveals the timing of sexual maturity in non-avian dinosaurs and genesis of the avian condition. Biol Lett. doi:10.1098/rsbl.2007.0254.
[76]  Sander PM, Klein N, Buffetaut E, Cuny G, Suteethorn V, et al. (2004) Adaptive radiation in sauropod dinosaurs: bone histology indicates rapid evolution of giant body size through acceleration. Org Div Evol 4: 165–173.
[77]  Erickson GM, Curry Rogers K, Yerby SA (2001) Dinosaurian growth patterns and rapid avian growth rates. Nature 412: 429–433.
[78]  Lehman TM, Woodward HN (2008) Modeling growth rates for sauropod dinosaurs. Paleobiology 34(2): 264–281.
[79]  de Ricqlès AJ, Padian K, Horner JR (2003) On the bone histology of some Triassic pseudosuchian archosaurs and related taxa. Ann Paleontol 89: 67–101.
[80]  Case TJ (1978) Speculations on the growth rate and reproduction of some dinosaurs. Paleobiology 4: 320–328.
[81]  Klein N, Sander PM (2008) Ontogenetic stages in the long bone histology of sauropod dinosaurs. Paleobiology 34(2): 247–263.
[82]  de Ricqlès AJ (1976) On bone histology of fossil and living reptiles, with comments on its functional and evolutionary significance. In: Bellairs A d'A, Cox CB, eds. Morphology and Biology of Reptiles. Linn Soc Symp Ser 3: 123–150.
[83]  Castanet J, Croci S, Aujard F, Perret M, Cubo J, et al. (2004) Lines of arrested growth in bone and age estimation in a small primate: Microcebus murinus. J Zool Lond 263: 31–39.
[84]  Burr DB (1992) Estimated intracortical bone turnover in the femur of growing macaques: Implications for their use as models in skeletal pathology. Anat Rec 232: 180–189.
[85]  Mulhern DM, Ubelaker DH (2003) Histologic examination of bone development in juvenile chimpanzees. Am J Phys Anth 122: 127–133.
[86]  Singh IJ, Tonna EA, Gandel CP (1974) A comparative histological study of mammalian bone. J Morph 144: 421–431.
[87]  Horner JR, Weishampel DB (1988) A comparative embryological study of two ornithischian dinosaurs. Nature 332: 256–257.
[88]  Chure DJ, Turner C, Peterson F (1994) An embryo of Camptosaurus from the Morrison Formation (Jurassic, Middle Tithonian) in Dinosaur National Monument, Utah. In: Carpenter K, Hirsch KF, Horner JR, editors. Dinosaur eggs and babies. Cambridge: Cambridge University Press. pp. 298–310.
[89]  Andrews RM (1982) Patterns of growth in reptiles. In: Gans C, Pough FH, editors. Biology of the Reptilia. London: Academic Press. pp. 273–320.
[90]  Chinsamy A, Codorniu L, Chiappe L (2008) Developmental growth patterns of the filter-feeder pterosaur, Pterodaustro guinnazui. Biol Let 4: 282–285.
[91]  Erickson GM, Currie PJ, Inouye BD, Winn AA (2006) Tyrannosaur life tables: An example of nonavian dinosaur population biology. Science 313: 213–217.
[92]  Jarman PJ, Jarman MV (1973) Social behavior, population structure, and reproduction potential in impala. E Afr Wild J 11: 329–338.
[93]  Owen-Smith N (1993) Comparative mortality rates of male and female kudus: the costs of sexual size dimorphism. J Anim Ecol 62: 428–440.
[94]  Jorgenson JT, Festa-Bianchet M, Gaillard J-M, Wishart WD (1997) Effects of age, sex, disease, and density on survival of bighorn sheep. Ecology 78(4): 1019–1032.
[95]  Mihlbachler MC (2003) Demography of late Miocene rhinoceroses (Teleoceras proterum and Aphelops malacorhinus) from Florida: linking mortality and sociality in fossil assemblages. Paleobiology 29: 412–428.
[96]  Proaktor G, Coulson T, Milner-Gulland EJ (2008) The demographic consequences of the cost of reproduction in ungulates. Ecology 89(9): 2604–2611.
[97]  Rimblot-Baly F, de Ricqlès A, Zylberberg L (1995) Analyse paleohistologique d'une serie de croissance partielle chez Lapparentosaurus madagascariensis (Jurassique Moyen): Essai sur la dynamique de croissance d'un dinosaure sauropode. Ann Pal 81: 49–86.
[98]  Woodward HN, Rich TH, Chinsamy A, Vickers-Rich P (2011) Growth dynamics of Australia's polar dinosaurs. PLoS ONE 6(8): e23339. doi:10.1371/journal.pone.0023339.
[99]  Norman DB, Sues H-D, Witmer LM, Coria RA (2004) Basal Ornithopoda. In: Weishampel DB, Dodson P, Osmólska H, editors. The Dinosauria. Second edition. Berkeley: University of California Press. pp. 393–412.
[100]  Bell PR, Snively E (2008) Polar dinosaurs on parade: a review of dinosaur migration. Alcheringa 32: 271–284.
[101]  Carrano MT, Janis CM, Sepkoski JJ Jr (1999) Hadrosaurs as ungulate parallels: Lost lifestyles and deficient data. Acta Pal Pol 44(3): 237–261.
[102]  Norman DB, Weishampel DB (1985) Ornithopod feeding mechanisms: Their bearing on the evolution of herbivory. Am Nat 126: 151–164.
[103]  Forster CA (1990) Evidence for juvenile groups in the ornithopod dinosaur Tenontosaurus tilletti Ostrom. J Pal 64(1): 164–165.
[104]  Horner JR, Makela R (1979) Nest of juveniles provides evidence of family structure among dinosaurs. Nature 282(5736): 296–298.
[105]  Horner JR, Weishampel DB, Forster CA (2004) Hadrosauridae. In: Weishampel DB, Dodson P, Osmólska H, editors. The Dinosauria. Second edition. Berkeley: University of California Press. pp. 438–468.
[106]  Varricchio DJ, Martin AJ, Katsura Y (2007) First trace and body fossil evidence of a burrowing, denning dinosaur. Proc R Soc Lond B 274(1616): 1361–1368.
[107]  Huh M, Lee D-G, Kim J-K, Lim J-D, Godefroit P (2011) A new basal ornithopod dinosaur from the Upper Cretaceous of South Korea. N Jb Geol Pal?ont Abh 259(1): 1–24.
[108]  Redelstorff R, Csiki Z, Grigorescu D (2009) The heritage of Nopcsa: Dwarf status of Hateg ornithopods supported by the histology of long bones. J Vert Pal 29(3): 170A.
[109]  Klein N (2010) Long Bone Histology of Sauropterygia from the Lower Muschelkalk of the Germanic Basin Provides Unexpected Implications for Phylogeny. PLoS ONE 5(7): e11613. doi:10.1371/journal.pone.0011613.
[110]  Packard GC, Boardman TJ, Birchard GF (2009) Allometric equations for predicting body mass of dinosaurs. J Zool Lond 279: 102–110.
[111]  Cawley GC, Janacek GJ (2010) On allometric equations for predicting body mass of dinosaurs. J Zool Lond 280: 355–361.
[112]  Dodson P (1975) Functional and ecological significance of relative growth in Alligator. J Zool Lond 175: 315–355.
[113]  Carrier D, Leon LR (1990) Skeletal growth in the California gull (Larus californicus). J Zool Lond 222: 375–389.
[114]  Witmer LM (1995) The extant phylogenetic bracket and the importance of reconstructing soft tissues in fossils. In: Thomason JJ, editor. Functional morphology in vertebrate paleontology. Cambridge: Cambridge University Press. pp. 19–33.
[115]  Wells JW (1963) Coral growth and geochronometry. Nature 197: 948–950.

Full-Text

Contact Us

service@oalib.com

QQ:3279437679

WhatsApp +8615387084133