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Bone histology of the titanosaur Lirainosaurus astibiae (Dinosauria: Sauropoda) from the Latest Cretaceous of Spain

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Abstract

The titanosaur Lirainosaurus astibiae is the only sauropod species known from the Late Cretaceous of the Iberian Peninsula. Lirainosaurus did not reach a gigantic body size and is one of the smallest sauropods discovered to date. Histological analysis of Lirainosaurus bones, focused on diaphyseal transverse sections of appendicular elements, reveals that Lirainosaurus did not exhibit the osseous microstructure typical for large sauropods, but is comparable with that of the coeval titanosaurs Alamosaurus sanjuanensis, Ampelosaurus atacis, and Magyarosaurus dacus, and also shares histological traits with other small to medium-sized sauropodomorph dinosaurs. Lirainosaurus limb bones exhibit a laminar fibrolamellar bone microstructure interrupted by growth marks, fully obliterated in adulthood by intense secondary remodeling processes which tend to replace completely the primary cortex. Lirainosaurus attained smaller sizes than typical sauropods reducing the rate of primary periosteal osteogenesis and developing an extensive secondary remodeling well before the adult size was reached. Histological organization of Lirainosaurus long bones is more mature than observed in basal neosauropods at similar ontogenetic stage, documenting a case of peramorphosis by pre-displacement. This heterochronic growth would be a reversal of the accelerated pattern of bone deposition typical for the sauropod lineage.

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References

  • Alexander RM (1989) Dynamics of dinosaurs and other extinct giants. Columbia University Press, New York

    Google Scholar 

  • Benton MJ, Csiki Z, Grigorescu D, Redelstorff R, Sander PM, Stein K, Weishampel DB (2010) Dinosaurs and the island rule: the dwarfed dinosaurs from Haţeg Island. Palaeogeography. doi:10.1016/j.palaeo.2010.01.026

    Google Scholar 

  • Calvo JO, Porfiri JD, González-Riga BJ, ArWA K (2007) A new Cretaceous terrestrial ecosystem from Gondwana with the description of a new sauropod dinosaur. An Acad Bras Ciênc 79:529–541. doi:10.1590/S0001-37652007000300013

    Article  PubMed  Google Scholar 

  • Castanet J, Francillon-Vieillot H, Meunier F, De Ricqlès A (1993) Bone and individual aging. In: Hall BK (ed) Bone, volume VII. Bone growth. CRC, London, pp 245–283

    Google Scholar 

  • Chinsamy A (1993) Bone histology and growth trajectory of the prosauropod dinosaur Massospondylus carinatus Owen. Mod Geol 18:77–82

    Google Scholar 

  • Chinsamy-Turan A (2005) The microstructure of dinosaur bone: deciphering biology with fine-scale techniques. Johns Hopkins University Press, Baltimore

    Google Scholar 

  • Company J (2005) Longbone histology of Lirainosaurus astibiae (Sauropodomorpha: Titanosauria) from the Upper Campanian of Chera, Spain. Kaupia 14:76

    Google Scholar 

  • Company J, Pereda-Suberbiola X, Ruiz-Omeñaca JI (2009) Nuevos restos fósiles del dinosaurio Lirainosaurus (Sauropoda, Titanosauria) en el Cretácico superior (Campaniano-Maastrichtiano) de la Península Ibérica. Ameghiniana 46:391–405

    Google Scholar 

  • Cormack D (1987) Ham’s histology. Lippincott Williams & Wilkins, New York

    Google Scholar 

  • Csiki Z, Grigorescu D (2007) The “Dinosaur Island”. New interpretation of the Hateg Basin vertebrate fauna after 110 years. Acta Mus Dev Ser Sci Nat Deva XX, Sargetia, pp 5–26

    Google Scholar 

  • Csiki Z, Codrea V, Jipa-Murzea C, Godefroit P (2010) A partial titanosaur (Sauropoda, Dinosauria) skeleton from the Maastrichtian of Nălaţ-Vad, Haţeg Basin, Romania. N Jb Geol Paläont Abh. doi:10.1127/0077-7749/2010/0098

    Google Scholar 

  • Curry KA (1999) Ontogenetic histology of Apatosaurus (Dinosauria: Sauropoda): new insights on growth rates and longevity. J Vert Paleont 19:654–665

    Article  Google Scholar 

  • Curry-Rogers KA (2005) Titanosauria: a phyllogenetic overview. In: Curry-Rogers KA, Wilson JA (eds) The sauropods: evolution and paleobiology. University of California Press, Berkeley, pp 50–103

    Google Scholar 

  • Curry-Rogers KA, Erickson GM (2005) Sauropod histology. In: Curry-Rogers KA, Wilson JA (eds) The sauropods: evolution and paleobiology. University of California Press, Berkeley, pp 303–326

    Google Scholar 

  • de Ricqlès AJ (1983) Cyclical growth in the long limb bones of a sauropod dinosaur. Acta Paleontol Pol 28:225–232

    Google Scholar 

  • Erickson GM (2005) Assessing dinosaur growth patterns: a microscopic revolution. Trends Ecol Evolut. doi:10.1016/j.tree.2005.08.012

    Google Scholar 

  • Erickson GM, Makovicky PJ, Currie PJ, Norell MA, Yerby SA, Brochu CA (2004) Gigantism and comparative life-history parameters of tyrannosaurid dinosaurs. Nature 430:772–775. doi:10.1038/nature02699

    Article  CAS  PubMed  Google Scholar 

  • González-Riga BJ, Previtera E, Pirrone CA (2009) Malarguesaurus florenciae gen. et sp. nov., a new titanosauriform (Dinosauria, Sauropoda) from the Upper Cretaceous of Mendoza, Argentina. Cret Res 30:135–148

    Article  Google Scholar 

  • Jianu CM, Weishampel DB (1999) The smallest of the largest: a new look at possible dwarfing in sauropod dinosaurs. Geol Mijnbouw—N J G 78:335–343

    Article  Google Scholar 

  • Klein N, Sander M (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 Palaeontol 77:169–206

    Google Scholar 

  • Klein N, Sander M (2008) Ontogenetic stages in the long bone histology of sauropod dinosaurs. Paleobiology 34:247–263

    Article  Google Scholar 

  • Klein N, Sander M, Le Loeuff J (2006) An unusual bone histology and growth pattern in Ampelosaurus atacis, a titanosaurid sauropod from South France. J Vert Paleont 26(Suppl to No 3):85A

    Google Scholar 

  • Klein N, Sander M, Suteethorn V (2009) Bone histology and its implications for the life history and growth of the Early Cretaceous titanosaur Phuwiangosaurus sirindhornae. In: Buffetaut E, Cuny G, Le Loeuff J, Suteethorn V (eds) Late Palaeozoic and Mesozoic ecosystems in SE Asia. The Geological Society, London, Special Publications, 315, pp 217–228. doi:10.1144/SP315.15

  • Köler M, Moyà-Solà S (2009) Physiological and life history strategies of a fossil large mammal in a resource-limited environment. Proc Natl Acad Sci USA 106:20354–20358. doi:10.1073/pnas.0813385106

    Article  Google Scholar 

  • Le Loeuff J (2005) Romanian Late Cretaceous dinosaurs: big dwarfs or small giants? Hist Biol 17:15–17

    Google Scholar 

  • Lee AH, Werning S (2008) Sexual maturity in growing dinosaurs does not fit reptilian growth models. Proc Natl Acad Sci USA 105:582–587. doi:10.1073/pnas.0708903105ER

    Article  CAS  PubMed  Google Scholar 

  • Lehman TM (2007) Growth and population age structure in the horned dinosaur Chasmosaurus. In: Carpenter K (ed) Horns and beaks: ceratopsian and ornithopod dinosaurs. Indiana University Press, Bloomington, pp 259–317

    Google Scholar 

  • Lehman TM, Woodward HN (2008) Modeling growth rates for sauropod dinosaurs. Paleobiology 34:264–281

    Article  Google Scholar 

  • Martín-Chivelet M, Berásategui X, Rosales I et al (2002) Cretaceous. In: Gibbons W, Moreno MT (eds) The geology of Spain. The Geological Society, London, pp 255–256

    Google Scholar 

  • McNamara KJ (1986) A guide to the nomenclature of heterochrony. J Paleontol 60:4–13

    Google Scholar 

  • Nopcsa F (1914) Über das Vorkommen der Dinosaurier in Siebenbürgen. Verh Zool Bot Ges 54:12–14

    Google Scholar 

  • Padian K, Horner JR, De Ricqlès A (2004) Growth in small dinosaurs and pterosaurs: the evolution of archosaurian growth strategies. J Vert Paleont 24:555–571

    Article  Google Scholar 

  • Reid REH (1981) Lamellar–zonal bone with zones and annuli in the pelvis of a sauropod dinosaur. Nature 292:49–51

    Article  Google Scholar 

  • Reid REH (1990) Zonal “growth rings” in dinosaurs. Mod Geol 15:19–48

    Google Scholar 

  • Reid REH (1996) Bone histology of the Cleveland-Lloyd dinosaurs and of dinosaurs in general, Part I: Introduction: introduction to bone tissues. Bringham Young Univ Geol Stud 41:25–72

    Google Scholar 

  • Ricqlès AJ, Padian K, Knoll F, Horner JR (2008) On the origin of high growth rates in archosaurs and their ancient relatives: complementary histological studies on Triassic archosauriforms and the problem of a “phylogenetic signal” in bone histology. Ann Paleontol. doi:10.1016/j.annpal.2008.03.002

    Google Scholar 

  • Rimblot-Baly F, de Ricqlès A, Zylberberg L (1995) Analyse paléohistologique d’une série de croissance partielle chez Lapparentosaurus madagascariensis (Jurassique moyen): essai sur la dynamique de croissance d’un dinosaure sauropode. Ann Paleontol 81:49–86

    Google Scholar 

  • Sander PM (2000) Longbone histology of the Tendaguru sauropods: implications for growth and biology. Paleobiology 26:466–488

    Article  Google Scholar 

  • Sander PM, Clauss M (2008) Sauropod gigantism. Science 322:200–201

    Article  CAS  PubMed  Google Scholar 

  • Sander PM, Tückmantel C (2003) Bone lamina thickness, bone apposition rates, and age estimates in sauropod humeri and femora. Paläontol Zeit 77:161–172

    Google Scholar 

  • Sander PM, Klein N, Buffetaut E, Cuny G, Suteethorn V, Le Loeuff J (2004) Adaptive radiation in sauropod dinosaurs: bone histology indicates rapid evolution of giant body size through acceleration. Org Divers Evol 4:165–173. doi:10.1016/j.ode.2003.12.002

    Article  Google Scholar 

  • Sander PM, Mateus O, Laven T, Knötschke N (2006) Bone histology indicates insular dwarfism in a new Late Jurassic sauropod dinosaur. Nature 41:739–741

    Article  Google Scholar 

  • Sanz JL, Powell JE, Le Loeuff J, Martinez R, Pereda-Suberbiola X (1999) Sauropod remains from the Upper Cretaceous of Laño (northcentral Spain). Titanosaur phylogenetic relationships. Estud Mus Cienc Nat Alava 14(Núm Esp 1):235–255

    Google Scholar 

  • Stein K, Sander PM (2009) Quantifying growth rates in island dwarf sauropods. Darwin–Bernissart Meeting, Brussels, Programme and Abstracts 9–13

  • Stein K, Sander PM, Csiki Z, Curry-Rogers K, Weishampel, DB (2008). Nopcsa’s legacy supported: Magyarosaurus dacus (Sauropoda: Titanosauria) bone histology suggests dwarfism on a palaeo-island. Symposium of Palaeontological Preparation and Conservation Annual Meeting, Dublin, Programme and Abstracts 50–51

  • 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). PNAS 107(20):9258–9263. doi:10.1073/pnas.1000781107

    Article  CAS  PubMed  Google Scholar 

  • Turvey ST, Green OR, Holdaway RN (2005) Cortical growth marks reveal extended juvenile development in New Zealand moa. Nature 435:940–943, 10.1038/nature03635

    Article  CAS  PubMed  Google Scholar 

  • Upchurch P, Barrett PM, Dodson P (2004) Sauropoda. In: Weishampel DB, Dodson P, Osmólska H (eds) The Dinosauria, 2nd edn. University of California Press, Berkeley, pp 259–322

    Google Scholar 

  • Wilson JA (2002) Sauropod dinosaur phylogeny: critique and cladistic analysis. Zool J Linn Soc 136:217–276

    Article  Google Scholar 

  • Wilson JA, Carrano MT (1999) Titanosaurs and the origin of “wide-gauge” trackways: a biomechanical and systematic perspective on sauropod locomotion. Paleobiology 25:252–257

    Google Scholar 

  • 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 Paleont 29:807–821

    Article  Google Scholar 

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Acknowledgments

I am very grateful to Fabien Knoll (Museo Nacional de Ciencias Naturales, Madrid), Attila Ösi (Hungarian Natural History Museum, Budapest), Jeff Wilson (University of Michigan, Michigan), and Holly Woodward (Montana State University, Montana) for reading and commenting on an early version of the manuscript. Two anonymous reviewers also improved the manuscript with constructive reviews. Miquel De Renzi (University of Valencia, Valencia) helped with morphometric estimations. Xabier Pereda-Suberbiola and Verónica Díez (Universidad del País Vasco, Vizcaya) proportioned helpful measurements of specimens housed at MCNA (Vitoria, Spain) and MNHN (Paris, France). Finally, I would also to express my deepest gratitude to Thomas Lehman (Texas Tech University, Texas) for sharing with me his knowledge, for providing many helpful suggestions and for an exhaustive review of the manuscript. This research was partly supported by the Ministerio de Ciencia e Innovación (MICINN, project CGL2007-64061/BTE).

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Correspondence to Julio Company.

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Communicated by Robert Reisz

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Company, J. Bone histology of the titanosaur Lirainosaurus astibiae (Dinosauria: Sauropoda) from the Latest Cretaceous of Spain. Naturwissenschaften 98, 67–78 (2011). https://doi.org/10.1007/s00114-010-0742-3

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