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Can secondary osteons be used as ontogenetic indicators in sauropods? Extending the histological ontogenetic stages into senescence

  • Jessica Mitchell (a1), P. Martin Sander (a1) and Koen Stein (a2)

Sauropod bone histology has provided a great deal of insight into the life history of these enormous animals. However, because of high growth rates, annual growth rings are not common in sauropod long bones, so directly measuring growth rates and determining sexual maturity require alternative measures. Histological ontogenetic stages (HOS) have been established to describe the changes in bone histology through development for basal Macronaria and Diplodocoidea, and subsequently for Titanosauria. Despite this, the current HOS model is not able to discriminate bone tissues in late ontogeny, when sauropods had reached asymptotic size and continued to live into senescence but their long bones became extensively remodeled by secondary osteons and all primary bone was destroyed. Here we establish remodeling stages (RS) to characterize the Haversian bone development through ontogeny in eight sauropod taxa (Apatosaurinae, Giraffatitan brancai, Camarasaurus spp., Dicraeosaurus spp., Ampelosaurus atacis, Phuwiangosaurus sirindhornae, Magyarosaurus dacus, and Alamosaurus sanjuanensis) and find significant correlation of RS with corresponding femur length (CFL) for the studied taxa, with the exception of Dicraeosaurus and Magyarosaurus. Remodeling stages are based on the maximum number of observable generations of crosscutting osteons from the innermost, mid-, and outermost part of the cortex. The correlation with CFL indicates that secondary osteons present an ontogenetic signal that could extend the histological ontogenetic stages. Remodeling stages also provide additional insight into the changes in histology through ontogeny for Sauropoda. This method has the potential to be used in other taxa, such as thyreophorans and many ornithischians, that develop Haversian tissue through development.

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Ahlqvist J., and Damsten O.. 1969. A modification of Kerley’s method for the microscopic determination of age in human bone. Journal of Forensic Sciences 14:205212.
Amprino R., and Marotti G.. 1964. A topographic quantitative study of bone formation and reconstruction. Bone and Tooth Symposium 1:2133.
Ascenzi A., and Bonucci E.. 1967. The tensile properties of single osteons. Anatomical Record 158:375386.
Ascenzi A., and Bonucci E.. 1968. The compressive properties of single osteons. Anatomical Record 161:377391.
Bentolila V., Boyce T. M., Fyhrie D. P., Drumb R., Skerry T. M., and Schaffler M. B.. 1998. Intracortical remodeling in adult rat long bones after fatigue loading. Bone 23:275281.
Bonewald L. F. 2011. The amazing osteocyte. Journal of Bone and Mineral Research 26:229238.
Bonnan M. F. 2004. Morphometric analysis of humerus and femur shape in Morrison sauropods: implications for functional morphology and paleobiology. Paleobiology 30:444470.
Britz H. M., Thomas C. D. L., Clement J. G., and Cooper D. M.. 2009. The relation of femoral osteon geometry to age, sex, height and weight. Bone 45:7783.
Burr D. B., Martin R., Schaffler M. B., and Radin E. L.. 1985. Bone remodeling in response to in vivo fatigue microdamage. Journal of Biomechanics 18:189200.
Burr D. B., Ruff C. B., and Thompson D. D.. 1990. Patterns of skeletal histologic change through time: comparison of an archaic Native American population with modern populations. Anatomical Record 226:307313.
Bybee P., Lee A., and Lamm E.. 2005. Sizing the Jurassic theropod dinosaur Allosaurus: assessing growth strategy and evolution of ontogenetic scaling of limbs. Journal of Morphology 267:347359.
Campione N. E., and Evans D. C.. 2012. A universal scaling relationship between body mass and proximal limb bone dimensions in quadrupedal terrestrial tetrapods. BMC Biology 10:122.
Castanet J. 1994. Age estimation and longevity in reptiles. Gerontology 40:174192.
Castrogiovanni P., Imbesi R., Fisichella M., and Mazzone V.. 2011. Osteonic organization of limb bones in mammals, including humans, and birds: a preliminary study. Italian Journal of Anatomy and Embryology 116:3037.
Cerda I. A., Chinsamy A., Pol D., Otero A., Powell J. A., and Martinez R.. 2016. Novel insight into the growth dynamics of sauropodomorph dinosaurs. Eleventh International Congress of Vertebrate Morphology, Washington, D.C. Anatomical Record Special Feature 299:75.
Chinsamy A. 1990. Physiological implications of the bone histology of Syntarsus rhodesiensis (Saurischia: Theropoda). Palaeontologia Africana 27:7782.
Chinsamy A. 1993. Bone histology and growth trajectory of the prosauropod dinosaur Massospondylus carinatus Owen. Modern Geology 18:319329.
Chinsamy A., and Raath M.. 1992. Preparation of fossil bone for histological examination. Palaeontologia Africana 29:3944.
Chinsamy-Turan A. 2005. The microstructure of dinosaur bone: deciphering biology with fine-scale techniques. Johns Hopkins University Press, Baltimore, Md.
Company J. 2011. Bone histology of the titanosaur Lirainosaurus astibiae (Dinosauria: Sauropoda) from the latest Cretaceous of Spain. Naturwissenschaften 98:6778.
Currey J. D. 1964. Some effects of ageing in human Haversian systems. Journal of Anatomy 98:6975.
Currey J. D. 2011. The structure and mechanics of bone. Journal of Materials Science 47:4154.
Curry K. 1999. Ontogenetic histology of Apatosaurus (Dinosauria: Sauropoda): new insights on growth rates and longevity. Journal of Vertebrate Paleontology 19:654665.
Curry Rogers K., Whitney M., D’Emic M., and Bagley B.. 2016. Precocity in a tiny titanosaur from the Cretaceous of Madagascar. Science 352:450453.
D’Emic M., and Wilson J. A.. 2012. Bone histology of a dwarf sauropod dinosaur from the latest Cretaceous of Jordan and a possible biomechanical explanation for “titanosaur-type” bone histology. Journal of Vertebrate Paleontology 32(Suppl. to Vol. 3), A83.
Enlow D., and Brown S.. 1956. A comparative histological study of fossil and recent bone tissues. Part I. Texas Journal of Science 8:405443.
Ericksen M. 1991. Histologic estimation of age at death using the anterior cortex of the femur. American Journal of Physical Anthropology 84:171179.
Erickson G. M. 2005. Assessing dinosaur growth patterns: a microscopic revolution. Trends in Ecology and Evolution 20:677684.
Erickson G. M., Makovicky P. J., Currie P. J., Norell M. A., Yerby S. A., and Brochu C. A.. 2004. Gigantism and comparative life-history parameters of tyrannosaurid dinosaurs. Nature 430:772775.
Francillon-Vieillot H., de Buffrénil V., Castanet J., Géraudie J., Meunier F. J., Sire J. Y., Zylberberg L., and de Ricqlès A.. 1990. Microstructure and mineralization of vertebrate skeletal tissues. Pp. 471530 in J. G. Carter, ed. Skeletal Biomineralization: Patterns, Processes and Evolutionary Trends Vol. 1 Van Nostrand Reinhold, New York.
Frost H. M. 1969. Tetracycline-based histological analysis of bone remodeling. Calcified Tissue Research 3:211237.
García R. A., Salgado L., Fernández M. S., Cerda I. A., Carabajal A. P., Otero A., Coria R. A., and Fiorelli L. E.. 2015. Paleobiology of titanosaurs: reproduction, development, histology, pneumaticity, locomotion and neuroanatomy from the South American fossil record. Ameghiniana 52:2968.
Ghilardi A. M., Aureliano T., Duque R. R. C., Fernandes M. A., Barreto A. M. F., and Chinsamy A.. 2016. A new titanosaur from the Lower Cretaceous of Brazil. Cretaceous Research 67:1624.
Griebeler E. M., Klein N., and Sander P. M.. 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. doi: 10.1371/journal.pone.0067012.
Gross W. 1934. Die Typen des mikroskopischen Knochenbaues bei fossilen Stegocephalen und Reptilien. Anatomy and Embryology 103:731764.
Ham A. 1953. Histology. Lippincott, Philadelphia.
Havill L. M. 2003. Osteon remodeling dynamics in Macaca mulatta: normal variation with regard to age, sex, and skeletal maturity. Calcified Tissue International 74:95102.
Hayashi S., Carpenter K., and Suzuki D.. 2009. Different growth patterns between the skeleton and osteoderms of Stegosaurus (Ornithischia: Thyreophora). Journal of Vertebrate Paleontology 29:123131.
Hillier M. L., and Bell L. S.. 2007. Differentiating human bone from animal bone: a review of histological methods. Journal of Forensic Sciences 52:249263.
Horner J. R., and Padian K.. 2004. Age and growth dynamics of Tyrannosaurus rex . Proceedings of the Royal Society B 271:18751880.
Horner J. R., de Ricqlès A., and Padian K.. 2000. Long bone histology of the hadrosaurid dinosaur Maiasaura peeblesorum: growth dynamics and physiology based on an ontogenetic series of skeletal elements. Journal of Vertebrate Paleontology 20:115129.
Jaworski Z. F., Duck B., and Sekaly G.. 1981. Kinetics of osteoclasts and their nuclei in evolving secondary Haversian systems. Journal of Anatomy 133:397.
Kerley E. R. 1965. The microscopic determination of age in human bone. American Journal of Physical Anthropology 23:149163.
Kerley E. R., and Ubelaker D. H.. 1978. Revisions in the microscopic method of estimating age at death in human cortical bone. American Journal of Physical Anthropology 49:545546.
Kilbourne B. M., and Makovicky P. J.. 2010. Limb bone allometry during postnatal ontogeny in non-avian dinosaurs: postnatal allometry of dinosaur limb bones. Journal of Anatomy 217:135152.
Klein N., and Sander P. 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). Special Papers in Palaeontology 77:169.
Klein N., and Sander P. M.. 2008. Ontogenetic stages in the long bone histology of sauropod dinosaurs. Paleobiology 34:247263.
Klein N., Sander P. M., and Suteethorn V.. 2009. Bone histology and its implications for the life history and growth of the Early Cretaceous titanosaur Phuwiangosaurus sirindhornae. Geological Society London Special Publication 315:217–228.
Klein N., Sander P. M., Stein K., Le Loeuff J., Carballido J. L., and Buffetaut E.. 2012. Modified laminar bone in Ampelosaurus atacis and other titanosaurs (Sauropoda): implications for life history and physiology. PLoS ONE 7:e36907. doi: 10.1371/journal.pone.0036907.
Lieberman D. E., Pearson O. M., Polk J. D., Demes B., and Crompton A. W.. 2003. Optimization of bone growth and remodeling in response to loading in tapered mammalian limbs. Journal of Experimental Biology 206:31253138.
Martin R. 2000. Toward a unifying theory of remodeling. Bone 26:16.
Martin R., Pickett J., and Zinaich S.. 1980. Studies of skeletal remodeling in aging men. Clinical Orthopaedics and Related Research 149:268.
Mitchell J., and Sander P. M.. 2014. The three-front model: a developmental explanation of long bone diaphyseal histology of Sauropoda. Biological Journal of the Linnean Society 112:765781.
Mori S., and Burr D.. 1993. Increased intracortical remodeling following fatigue damage. Bone 14:103109.
Mulhern D. M., and Ubelaker D. H.. 2003. Histologic examination of bone development in juvenile chimpanzees. American Journal of Physical Anthropology 122:127133.
Ortner D. J. 1975. Aging effects on osteon remodeling. Calcified Tissue Research 18:2736.
Padian K., Werning S., and Horner J. R.. 2016. A hypothesis of differential secondary bone formation in dinosaurs. Comptes Rendus Palevol 15:4048.
Parfitt A. M. 1994. Osteonal and hemi-osteonal remodeling: the spatial and temporal framework for signal traffic in adult human bone. Journal of Cellular Biochemistry 55:273286.
Pfeiffer S., Lazenby R., and Chiang J.. 1995. Cortical remodeling data are affected by sampling location. American Journal of Physical Anthropology 96:8992.
R Core Team 2015. R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria
Richman E., Ortner D., and Schulter-Ellis F.. 1979. Differences in intracortical bone remodeling in three aboriginal American populations: possible dietary factors. Calcified Tissue International 28:209214.
Ricqlès A. de. 1968a. Quelques observations paléohistologiques sur le dinosaurien sauropode Bothriospondylus . Annales de l’Université de Madagascar 6:157209.
Ricqlès A. de 1968b. Recherches paléohistologiques sur les os longs des tétrapodes: origine du tissu osseux plexiforme des dinosauriens sauropodes. Annales de Paléontologie 54:133145.
Ricqlès A. de 1980. Tissue structures of dinosaur bone: functional significance and possible relation to dinosaur physiology. A cold look at the warm-blooded dinosaurs. AAAS Selected Symposium 28:103139.
Ricqlès A. de 1983. Cyclical growth in the long limb bones of a sauropod dinosaur. Acta Palaeontologica Polonica 28:225232.
Robling A. G., Castillo A. B., and Turner C. H.. 2006. Biomechanical and molecular regulation of bone remodeling. Annual Review of Biomedical Engineering 8:455498.
Samson C., and Branigan K.. 1987. A new method of estimating age at death from fragmentary and weathered bone. Pages 101108 in A. Boddington, A. N. Garland, and R. C. Janaway, eds. Death, decay and reconstruction: approaches to archaeology and forensic science. Manchester University Press, Manchester.
Sander P. M. 1999. Life history of Tendaguru sauropods as inferred from long bone histology. Fossil Record 2:103112.
Sander P. M. 2000. Longbone histology of the Tendaguru sauropods: implications for growth and biology. Paleobiology 26:466488.
Sander P. M. 2013. An evolutionary cascade model for sauropod dinosaur gigantism—overview, update and tests. PLoS ONE 8:e78573.
Sander P. M., and Tückmantel C.. 2003. Bone lamina thickness, bone apposition rates, and age estimates in sauropod humeri and femora. Paläontologische Zeitschrift 77:161172.
Sander P. M., Klein N., Stein K., and Wings O.. 2011. Sauropod bone histology and implications for sauropod biology. Pp. 276302 in N. Klein, K. Remes, C. T. Gee, and P. M. Sander, eds. Biology of the Sauropod Dinosaurs. Understanding the Life of Giants. Indiana University Press, Bloomington.
Sander P. M., Mateus O., Laven T., and Knötschke N.. 2006. Bone histology indicates insular dwarfism in a new Late Jurassic sauropod dinosaur. Nature 441:739741.
Singh I. J., and Gunberg D. L.. 1970. Estimation of age at death in human males from quantitative histology of bone fragments. American Journal of Physical Anthropology 33:373381.
Stein K., and Prondvai E.. 2014. Rethinking the nature of fibrolamellar bone: an integrative biological revision of sauropod plexiform bone formation. Biological Reviews of the Cambridge Philosophical Society 89:2447.
Stein K., and Sander P. M.. 2009. Histological core drilling: a less destructive method for studying bone histology. Pp. 6980 in M. A. Brown, J. F. Kane, and W. G. Parker, eds. Methods in Preparation. Proceedings of the First Annual Fossil Preparation and Collections Symposium.
Stein K., Csiki Z., Rogers K. C., Weishampel D. B., Redelstorff R., Carballido J. L., and Sander P. M.. 2010. Small body size and extreme cortical bone remodeling indicate phyletic dwarfism in Magyarosaurus dacus (Sauropoda: Titanosauria). Proceedings of the National Academy of Sciences USA 107:92589263.
Stein M., Hayashi S., and Sander P. M.. 2013. Long bone histology and growth patterns in ankylosaurs: implications for life history and evolution. PLoS ONE 8:e68590. doi: 10.1371/journal.pone.0068590.
Stout S. 1989. The use of cortical bone histology to estimate age at death. Pp. 195207 in M. Y. Icscan, ed. Age markers in the human skeleton. Charles C. Thomas, Springfield, Illinois.
Stout S. D., and Paine R. R.. 1994. Bone remodeling rates: a test of an algorithm for estimating missing osteons. American Journal of Physical Anthropology 93:123129.
Streeter M. 2010. A four-stage method of age at death estimation for use in the subadult rib cortex. Journal of Forensic Sciences 55:10191024.
Taylor M. P. 2009. A re-evaluation of Brachiosaurus altithorax Riggs 1903 (Dinosauria, Sauropoda) and its generic separation from Giraffatitan brancai Janensch 1914. Journal of Vertebrate Paleontology 29:787806.
Thomas C. D. L., Stein M. S., Feik S. A., Wark J. D., and Clement J. G.. 2000. Determination of age at death using combined morphology and histology of the femur. Journal of Anatomy 196:463471.
Thompson D. D. 1979. The core technique in the determination of age at death of skeletons. Journal of Forensic Sciences 24:902915.
Tschopp E., Mateus O., and Benson R. B. J.. 2015. A specimen-level phylogenetic analysis and taxonomic revision of Diplodocidae (Dinosauria, Sauropoda). PeerJ 3:e857. doi: 10.7717/peerj.857.
van Oers R. F., Ruimerman R., Tanck E., Hilbers P. A., and Huiskes R.. 2008. A unified theory for osteonal and hemi-osteonal remodeling. Bone 42:250259.
Varricchio D. J. 1993. Bone microstructure of the Upper Cretaceous theropod dinosaur Troodon formosus . Journal of Vertebrate Paleontology 13:99104.
Walker R. A., Lovejoy C. O., and Meindl R. S.. 1994. Histomorphological and geometric properties of human femoral cortex in individuals over 50: implications for histomorphological determination of age-at-death. American Journal of Human Biology 6:659667.
Waskow K., and Sander P. M.. 2014. Growth record and histological variation in the dorsal ribs of Camarasaurus sp. (Sauropoda). Journal of Vertebrate Paleontology 34:852869.
Werning S. 2012. The ontogenetic osteohistology of Tenontosaurus tilletti . PLoS ONE 7:e33539.
Wilson J. 2002. Sauropod dinosaur phylogeny: critique and cladistic analysis. Zoological Journal of the Linnean Society 136:215275.
Wilson J., Leiggi P., and May P.. 1994. Histological techniques. Vertebrate Paleontological Techniques 1:205234.
Wings O., Sander P. M., Tütken T., Fowler D., and Sun G.. 2007. Growth and life history of Asia’s largest dinosaur. Journal of Vertebrate Paleontology 27:167A.
Woodward H. N., and Lehman T. M.. 2009. Bone histology and microanatomy of Alamosaurus sanjuanensis (Sauropoda: Titanosauria) from the Maastrichtian of Big Bend National Park, Texas. Journal of Vertebrate Paleontology 29:807821.
Wu K., Schubeck K. E., Frost H. M., and Villanueva A.. 1970. Haversian bone formation rates determined by a new method in a mastodon, and in human diabetes mellitus and osteoporosis. Calcified Tissue Research 6:204219.
Yee T. W. 2016. VGAM: vector generalized linear and additive models. R package, Version 1:01.
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