Skip to main content
×
Home
    • Aa
    • Aa

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)
Abstract
Abstract

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.

Copyright
Linked references
Hide All

This list contains references from the content that can be linked to their source. For a full set of references and notes please see the PDF or HTML where available.

A. Ascenzi , and E. Bonucci . 1967. The tensile properties of single osteons. Anatomical Record 158:375386.

A. Ascenzi , and E. Bonucci . 1968. The compressive properties of single osteons. Anatomical Record 161:377391.

V. Bentolila , T. M. Boyce , D. P. Fyhrie , R. Drumb , T. M. Skerry , and M. B. Schaffler . 1998. Intracortical remodeling in adult rat long bones after fatigue loading. Bone 23:275281.

L. F. Bonewald 2011. The amazing osteocyte. Journal of Bone and Mineral Research 26:229238.

M. F. Bonnan 2004. Morphometric analysis of humerus and femur shape in Morrison sauropods: implications for functional morphology and paleobiology. Paleobiology 30:444470.

H. M. Britz , C. D. L. Thomas , J. G. Clement , and D. M. Cooper . 2009. The relation of femoral osteon geometry to age, sex, height and weight. Bone 45:7783.

D. B. Burr , R. Martin , M. B. Schaffler , and E. L. Radin . 1985. Bone remodeling in response to in vivo fatigue microdamage. Journal of Biomechanics 18:189200.

D. B. Burr , C. B. Ruff , and D. D. Thompson . 1990. Patterns of skeletal histologic change through time: comparison of an archaic Native American population with modern populations. Anatomical Record 226:307313.

P. Bybee , A. Lee , and E. Lamm . 2005. Sizing the Jurassic theropod dinosaur Allosaurus: assessing growth strategy and evolution of ontogenetic scaling of limbs. Journal of Morphology 267:347359.

N. E. Campione , and D. C. Evans . 2012. A universal scaling relationship between body mass and proximal limb bone dimensions in quadrupedal terrestrial tetrapods. BMC Biology 10:122.

J. Castanet 1994. Age estimation and longevity in reptiles. Gerontology 40:174192.

J. Company 2011. Bone histology of the titanosaur Lirainosaurus astibiae (Dinosauria: Sauropoda) from the latest Cretaceous of Spain. Naturwissenschaften 98:6778.

J. D. Currey 2011. The structure and mechanics of bone. Journal of Materials Science 47:4154.

K. Curry 1999. Ontogenetic histology of Apatosaurus (Dinosauria: Sauropoda): new insights on growth rates and longevity. Journal of Vertebrate Paleontology 19:654665.

K. Curry Rogers , M. Whitney , M. D’Emic , and B. Bagley . 2016. Precocity in a tiny titanosaur from the Cretaceous of Madagascar. Science 352:450453.

M. Ericksen 1991. Histologic estimation of age at death using the anterior cortex of the femur. American Journal of Physical Anthropology 84:171179.

G. M. Erickson 2005. Assessing dinosaur growth patterns: a microscopic revolution. Trends in Ecology and Evolution 20:677684.

G. M. Erickson , P. J. Makovicky , P. J. Currie , M. A. Norell , S. A. Yerby , and C. A. Brochu . 2004. Gigantism and comparative life-history parameters of tyrannosaurid dinosaurs. Nature 430:772775.

H. M. Frost 1969. Tetracycline-based histological analysis of bone remodeling. Calcified Tissue Research 3:211237.

R. A. García , L. Salgado , M. S. Fernández , I. A. Cerda , A. P. Carabajal , A. Otero , R. A. Coria , and L. E. Fiorelli . 2015. Paleobiology of titanosaurs: reproduction, development, histology, pneumaticity, locomotion and neuroanatomy from the South American fossil record. Ameghiniana 52:2968.

A. M. Ghilardi , T. Aureliano , R. R. C. Duque , M. A. Fernandes , A. M. F. Barreto , and A. Chinsamy . 2016. A new titanosaur from the Lower Cretaceous of Brazil. Cretaceous Research 67:1624.

E. M. Griebeler , N. Klein , and P. M. Sander . 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.

L. M. Havill 2003. Osteon remodeling dynamics in Macaca mulatta: normal variation with regard to age, sex, and skeletal maturity. Calcified Tissue International 74:95102.

S. Hayashi , K. Carpenter , and D. Suzuki . 2009. Different growth patterns between the skeleton and osteoderms of Stegosaurus (Ornithischia: Thyreophora). Journal of Vertebrate Paleontology 29:123131.

M. L. Hillier , and L. S. Bell . 2007. Differentiating human bone from animal bone: a review of histological methods. Journal of Forensic Sciences 52:249263.

J. R. Horner , and K. Padian . 2004. Age and growth dynamics of Tyrannosaurus rex . Proceedings of the Royal Society B 271:18751880.

J. R. Horner , A. de Ricqlès , and K. Padian . 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.

E. R. Kerley 1965. The microscopic determination of age in human bone. American Journal of Physical Anthropology 23:149163.

E. R. Kerley , and D. H. Ubelaker . 1978. Revisions in the microscopic method of estimating age at death in human cortical bone. American Journal of Physical Anthropology 49:545546.

N. Klein , and P. M. Sander . 2008. Ontogenetic stages in the long bone histology of sauropod dinosaurs. Paleobiology 34:247263.

N. Klein , P. M. Sander , K. Stein , J. Le Loeuff , J. L. Carballido , and E. Buffetaut . 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.

D. E. Lieberman , O. M. Pearson , J. D. Polk , B. Demes , and A. W. Crompton . 2003. Optimization of bone growth and remodeling in response to loading in tapered mammalian limbs. Journal of Experimental Biology 206:31253138.

R. Martin 2000. Toward a unifying theory of remodeling. Bone 26:16.

J. Mitchell , and P. M. Sander . 2014. The three-front model: a developmental explanation of long bone diaphyseal histology of Sauropoda. Biological Journal of the Linnean Society 112:765781.

S. Mori , and D. Burr . 1993. Increased intracortical remodeling following fatigue damage. Bone 14:103109.

D. M. Mulhern , and D. H. Ubelaker . 2003. Histologic examination of bone development in juvenile chimpanzees. American Journal of Physical Anthropology 122:127133.

D. J. Ortner 1975. Aging effects on osteon remodeling. Calcified Tissue Research 18:2736.

K. Padian , S. Werning , and J. R. Horner . 2016. A hypothesis of differential secondary bone formation in dinosaurs. Comptes Rendus Palevol 15:4048.

A. M. Parfitt 1994. Osteonal and hemi-osteonal remodeling: the spatial and temporal framework for signal traffic in adult human bone. Journal of Cellular Biochemistry 55:273286.

S. Pfeiffer , R. Lazenby , and J. Chiang . 1995. Cortical remodeling data are affected by sampling location. American Journal of Physical Anthropology 96:8992.

E. Richman , D. Ortner , and F. Schulter-Ellis . 1979. Differences in intracortical bone remodeling in three aboriginal American populations: possible dietary factors. Calcified Tissue International 28:209214.

A. G. Robling , A. B. Castillo , and C. H. Turner . 2006. Biomechanical and molecular regulation of bone remodeling. Annual Review of Biomedical Engineering 8:455498.

P. M. Sander 1999. Life history of Tendaguru sauropods as inferred from long bone histology. Fossil Record 2:103112.

P. M. Sander 2000. Longbone histology of the Tendaguru sauropods: implications for growth and biology. Paleobiology 26:466488.

P. M. Sander 2013. An evolutionary cascade model for sauropod dinosaur gigantism—overview, update and tests. PLoS ONE 8:e78573. http://dx.doi.org/10.1371/journal.pone.0078573.

P. M. Sander , and C. Tückmantel . 2003. Bone lamina thickness, bone apposition rates, and age estimates in sauropod humeri and femora. Paläontologische Zeitschrift 77:161172.

P. M. Sander , O. Mateus , T. Laven , and N. Knötschke . 2006. Bone histology indicates insular dwarfism in a new Late Jurassic sauropod dinosaur. Nature 441:739741.

I. J. Singh , and D. L. Gunberg . 1970. Estimation of age at death in human males from quantitative histology of bone fragments. American Journal of Physical Anthropology 33:373381.

K. Stein , and E. Prondvai . 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.

K. Stein , Z. Csiki , K. C. Rogers , D. B. Weishampel , R. Redelstorff , J. L. Carballido , and P. M. Sander . 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.

M. Stein , S. Hayashi , and P. M. Sander . 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.

S. D. Stout , and R. R. Paine . 1994. Bone remodeling rates: a test of an algorithm for estimating missing osteons. American Journal of Physical Anthropology 93:123129.

M. Streeter 2010. A four-stage method of age at death estimation for use in the subadult rib cortex. Journal of Forensic Sciences 55:10191024.

M. P. Taylor 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.

C. D. L. Thomas , M. S. Stein , S. A. Feik , J. D. Wark , and J. G. Clement . 2000. Determination of age at death using combined morphology and histology of the femur. Journal of Anatomy 196:463471.

D. D. Thompson 1979. The core technique in the determination of age at death of skeletons. Journal of Forensic Sciences 24:902915.

E. Tschopp , O. Mateus , and R. B. J. Benson . 2015. A specimen-level phylogenetic analysis and taxonomic revision of Diplodocidae (Dinosauria, Sauropoda). PeerJ 3:e857. doi: 10.7717/peerj.857.

R. F. van Oers , R. Ruimerman , E. Tanck , P. A. Hilbers , and R. Huiskes . 2008. A unified theory for osteonal and hemi-osteonal remodeling. Bone 42:250259.

D. J. Varricchio 1993. Bone microstructure of the Upper Cretaceous theropod dinosaur Troodon formosus . Journal of Vertebrate Paleontology 13:99104.

R. A. Walker , C. O. Lovejoy , and R. S. Meindl . 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.

K. Waskow , and P. M. Sander . 2014. Growth record and histological variation in the dorsal ribs of Camarasaurus sp. (Sauropoda). Journal of Vertebrate Paleontology 34:852869.

S. Werning 2012. The ontogenetic osteohistology of Tenontosaurus tilletti . PLoS ONE 7:e33539. doi.org/10.1371/journal.pone.0033539.

J. Wilson 2002. Sauropod dinosaur phylogeny: critique and cladistic analysis. Zoological Journal of the Linnean Society 136:215275.

H. N. Woodward , and T. M. Lehman . 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.

K. Wu , K. E. Schubeck , H. M. Frost , and A. Villanueva . 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.

Recommend this journal

Email your librarian or administrator to recommend adding this journal to your organisation's collection.

Paleobiology
  • ISSN: 0094-8373
  • EISSN: 1938-5331
  • URL: /core/journals/paleobiology
Please enter your name
Please enter a valid email address
Who would you like to send this to? *
×

Metrics

Altmetric attention score

Full text views

Total number of HTML views: 8
Total number of PDF views: 84 *
Loading metrics...

Abstract views

Total abstract views: 1137 *
Loading metrics...

* Views captured on Cambridge Core between 6th February 2017 - 29th April 2017. This data will be updated every 24 hours.