Hostname: page-component-cd9895bd7-8ctnn Total loading time: 0 Render date: 2024-12-24T02:37:42.913Z Has data issue: false hasContentIssue false
  • English
  • Français

Three-Dimensional Synchrotron Virtual Paleohistology: A New Insight into the World of Fossil Bone Microstructures

Published online by Cambridge University Press:  02 October 2012

Sophie Sanchez ,
Per E. Ahlberg ,
Katherine M. Trinajstic ,
Alessandro Mirone  and
Paul Tafforeau
Sophie Sanchez*
Affiliation:
European Synchrotron Radiation Facility, BP220, 6 rue Jules Horowitz, 38043 Grenoble Cedex, France Department of Organismal Biology, Uppsala University, Norbyvägen 18A, 752 36 Uppsala, Sweden
Per E. Ahlberg
Affiliation:
Department of Organismal Biology, Uppsala University, Norbyvägen 18A, 752 36 Uppsala, Sweden
Katherine M. Trinajstic
Affiliation:
Department of Chemistry, Curtin University, Bentley Campus, GPO Box U1987 Perth, Western Australia 6845, Australia Department of Earth and Planetary Sciences, Western Australian Museum, Perth, Western Australia 6000, Australia
Alessandro Mirone
Affiliation:
European Synchrotron Radiation Facility, BP220, 6 rue Jules Horowitz, 38043 Grenoble Cedex, France
Paul Tafforeau
Affiliation:
European Synchrotron Radiation Facility, BP220, 6 rue Jules Horowitz, 38043 Grenoble Cedex, France
*
*Corresponding author. E-mail: [email protected]
Get access

Abstract

The recent developments of phase-contrast synchrotron imaging techniques have been of great interest for paleontologists, providing three-dimensional (3D) tomographic images of anatomical structures, thereby leading to new paleobiological insights and the discovery of new species. However, until now, it has not been used on features smaller than 5–7 μm voxel size in fossil bones. Because much information is contained within the 3D histological architecture of bone, including an ontogenetic record, crucial for understanding the paleobiology of fossil species, the application of phase-contrast synchrotron tomography to bone at higher resolutions is potentially of great interest. Here we use this technique to provide new 3D insights into the submicron-scale histology of fossil and recent bones, based on the development of new pink-beam configurations, data acquisition strategies, and improved processing tools. Not only do the scans reveal by nondestructive means all of the major features of the histology at a resolution comparable to that of optical microscopy, they provide 3D information that cannot be obtained by any other method.

Keywords

X-ray imagingphase contrastbonepaleontologybiology
Type
Biological Applications
Information
Microscopy and Microanalysis , Volume 18 , Issue 5 , October 2012 , pp. 1095 - 1105
Copyright
Copyright © Microscopy Society of America 2012

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Agassiz, L. (1833–1843). Recherches sur les poissons fossiles. Neuchatel, Switzerland: Imprimerie de Petitpierre.CrossRefGoogle Scholar
Ager, D.V. (1965). Serial grinding techniques. In Pages Handbook of Paleontological Techniques, Kummel, B. & Raup, D. (Eds.), pp. 212–224. New York: W.H. Freeman.Google Scholar
Amprino, R. (1947). La structure du tissu osseux envisagée comme expression de différences dans la vitesse de l'accroissement. Arch Biol 58, 315–330.Google Scholar
Anderson, J.S. (2007). Incorporating ontogeny into the matrix: A phylogenetic evaluation of developmental evidence for the origin of modern amphibians. In Major Transitions in Vertebrate Evolution, Anderson, J.S. & Sues, H.-D. (Eds.), pp. 182–227. Bloomington, IN: Indiana University Press.Google Scholar
Andrews, S.M. & Westoll, T.S. (1970). The postcranial skeleton of Eusthenopteron foordi Whiteaves. T RSE Earth 68, 207–329.Google Scholar
Bromage, T.G., Goldman, H.M., McFarlin, S.C., Perez-Ochoa, A. & Boyde, A. (2009). Confocal scanning optical microscopy of a 3-million-year-old Australopithecus afarensis femur. Scanning 31, 1–10.CrossRefGoogle ScholarPubMed
Carlson, K.J., Stout, D., Jashashvili, T., Ruiter, D.J. de, Tafforeau, P., Carlson, K. & Berger, L.R. (2011). The Endocast of MH1, Australopithecus sediba . Science 333, 1402–1407.CrossRefGoogle ScholarPubMed
Castanet, J., Francillon-Vieillot, H., Meunier, F.-J. & Ricqlès, A. de. (1993). Bone and individual aging. In Bone, vol. 7: Bone Growth-B, Hall, B.K. (Ed.), pp. 245–283. Boca Raton, FL: CRC Press.Google Scholar
Cloetens, P., Ludwig, W., Baruchel, J., Van Dyck, D., Van Landuyt, J., Guigay, J.P. & Schlenker, M. (1999). Holotomography: Quantitative phase tomography with micrometer resolution using hard synchrotron radiation X rays. Appl Phys Lett 75, 2912–2914.CrossRefGoogle Scholar
Croft, W.N. (1950). A parallel grinding instrument for the investigation of fossils by serial sections. J Paleontol 24, 693–698.Google Scholar
Currey, J.D. (2002). Bones: Structure and Mechanics. Princeton, NJ: Princeton University Press.CrossRefGoogle Scholar
Dierolf, M., Menzel, A., Thibault, P., Schneider, P., Kewish, C.M., Wepf, R., Bunk, O. & Pfeiffer, F. (2010). Ptychographic X-ray computed tomography at the nanoscale. Nature 467, 436–440.CrossRefGoogle ScholarPubMed
Dupret, V., Sanchez, S., Goujet, D., Tafforeau, P. & Ahlberg, P.E. (2010). Bone vascularization and growth in placoderms (Vertebrata): The example of the premedian plate of Romundina stellina Ørvig, 1975. CR Palevol 9, 369–375.CrossRefGoogle Scholar
Erickson, G.M., Makovicky, P.J., Currie, P.J., Norell, M.A., Yerby, S.A. & Brochu, C.A. (2004). Gigantism and comparative life-history parameters of tyrannosaurid dinosaurs. Nature 430, 772–775.CrossRefGoogle ScholarPubMed
Ford, B.J. (2001). The Royal Society and the microscope. Notes Rec Roy Soc 55, 29–49.CrossRefGoogle Scholar
Francillon-Vieillot, H., Buffrenil, V. de, Castanet, J., Géraudie, J., Meunier, F.J., Sire, J.-Y., Zylberberg, L. & Ricqlès, A. de. (1990). Microstructure and mineralization of vetebrate skeletal tissues. In Skeletal Biomineralization: Patterns, Processes and Evolutionary Trends: Volume I, Carter, J.G. (Ed.), pp. 471–530. New York: Van Nostrand Reinhold.Google Scholar
Gross, W. (1956). Über Crossopterygier und Dipnoer aus dem baltischen Oberdevon im Zusammenhang einer vergleichenden Untersuchung des Porenkanalsystems paläozoischer Agnathen und Fische. Kungl. Svenska vetenskapsakademiens Handlingar 5, 1–140.Google Scholar
Guigay, P., Langer, M., Boistel, R. & Cloetens, P. (2007). Mixed transfer function and transport of intensity approach for phase retrieval in the Fresnel region. Opt Lett 32, 1617–1619.CrossRefGoogle ScholarPubMed
Hieronymus, T.L. (2006). Quantitative microanatomy of jaw muscle attachment in extant diapsids. J Morphol 267, 954–967.CrossRefGoogle ScholarPubMed
Irvine, S.C., Morgan, K.S., Suzuki, Y., Uesugi, K., Takeuchi, A., Paganin, D.M. & Siu, K.K.W. (2010). Assessment of the use of a diffuser in propagation-based X-ray phase contrast imaging. Opt Express 18, 13478–13491.CrossRefGoogle ScholarPubMed
Janvier, P. (1996). Early Vertebrates. Oxford, UK: Clarendon Press.CrossRefGoogle Scholar
Jarvik, E. (1980). Basic Structure and Evolution of Vertebrates. London, UK: Academic Press.Google Scholar
Kiprijanoff, A.V. (1881–1883). Studien über die fossilien Reptilien Russlands. Mémoires de l'Académie Impériale des Sciences de St Petersbourg 7, 28–31.Google Scholar
Klembara, J. & Meszároš, S. (1992). New finds of Discosauriscus austriacus (Makowsky 1876) from the Lower Permian of Boskovice Furrow (Czecho-Slovakia). Geol Carpath 43, 305–312.Google Scholar
Lak, M., Néraudeau, D., Nel, A., Cloetens, P., Perrichot, V. & Tafforeau, P. (2008). Phase contrast X-ray synchrotron imaging: Opening access to fossil inclusions in opaque amber. Microsc Microanal 14, 251–259.CrossRefGoogle ScholarPubMed
Laurin, M., Meunier, F.J., Germain, D. & Lemoine, M. (2007). A microanatomical and histological study of the paired fin skeketon of the Devonian sarcopterygian Eusthenopteron foordi . J Paleontol 81, 143–153.CrossRefGoogle Scholar
Leeuwenhoek, A. van. (1674). Microscopical observations from Mr. Leeuwenhoek, about blood, milk, bones, the brain, spitle, cuticula, sweat, fatt, teares; communicated in two letters to the publisher. Philos T R Soc 9, 121–131.Google Scholar
Long, J.A., Trinajstic, K. & Johanson, Z. (2009). Devonian arthrodire embryos and the origin of internal fertilization in vertebrates. Nature 457, 1124–1127.CrossRefGoogle ScholarPubMed
Margerie, E. de, Tafforeau, P. & Rakotomanana, L. (2006). In silico evolution of functional morphology: A test on bone tissue biomechanics. J R Soc Interface 3, 679–687.CrossRefGoogle Scholar
Matzke-Karasz, R., Smith, R.J., Symonova, R., Miller, C.G. & Tafforeau, P. (2009). Sexual intercourse involving giant sperm in Cretaceous ostracode. Science 324, 1535.CrossRefGoogle ScholarPubMed
Meunier, F.J. & Laurin, M. (2010). A microanatomical and histological study of the fin long bones of the Devonian sarcopterygian Eusthenopteron foordi . Acta Zool 81, 143–153.Google Scholar
Organ, C.L., Shedlock, A.M., Meade, A., Pagel, M. & Edwards, S.V. (2007). Origin of avian genom size and structure in non-avian dinosaurs. Nature 446, 180–184.CrossRefGoogle Scholar
Owen, R. (1840–1845). Odontography, or a Treatise on the Comparative Anatomy of the Teeth, Their Physiological Relations, Mode of Development and Microscopic Structure, in the Vertebrate Animals. London, UK: Hippoly Bailliere.Google Scholar
Paganin, D., Mayo, S.C., Gureyev, T.E., Miller, P.R. & Wilkins, S.W. (2002). Simultaneous phase and amplitude extraction from a single defocused image of a homogeneous object. J Microsc 206, 33–40.CrossRefGoogle ScholarPubMed
Peyrin, F. (2009). Investigation of bone synchrotron radiation imaging: From micro to nano. Osteoporosis Int 20, 1057–1063.CrossRefGoogle ScholarPubMed
Poplin, C. & Ricqlès, A. de. (1970). A technique of serial sectionning for the study of the undecalcified fossils. Curator 13, 7–20.CrossRefGoogle Scholar
Pradel, A., Langer, M., Maisey, J., Geffard-Kuriyama, D., Cloetens, P., Janvier, P. & Tafforeau, P. (2009). Skull and brain of a 300 million-year-old chimaeroid fish revealed by synchrotron holotomography. P Natl Acad Sci 106, 5224–5228.CrossRefGoogle ScholarPubMed
Ricqlès, A. de, Castanet, J. & Francillon-Vieillot, H. (2004). The “message” of bone tissue in paleoherpetology. Ital J Zool 71(Suppl 1), 3–12.CrossRefGoogle Scholar
Rücklin, M., Giles, S., Janvier, P. & Donoghue, P.C.J. (2011). Teeth before jaws? Comparative analysis of the structure and development of the external and internal scales in the extinct jawless vertebrate Loganellia scotica. Evol Dev 13, 523–532.CrossRefGoogle ScholarPubMed
Ruta, M. & Coates, M.I. (2007). Dates, nodes and character conflict: Addressing the Lissamphibian origin problem. J Syst Paleontol 5, 69–122.CrossRefGoogle Scholar
Sansom, I.J., Smith, M.M. & Smith, P. (1996). Scales of thelodont and shark-like fishes from the Ordovician of Colorado. Nature 379, 628–630.CrossRefGoogle Scholar
Smith, T.M., Olejniczak, A.J., Kupczik, K., Lazzari, V., Vos, J. de, Kullmer, O., Schrenk, F., Hublin, J.-J., Jacob, T. & Tafforeau, P. (2009). Taxonomic assessment of the trinil molars using non-destructive 3D structural and development analysis. PaleoAnthropology 2009, 117–129.Google Scholar
Smith, T.M. & Tafforeau, P. (2008). New visions of dental tissue research: Tooth development, chemistry, and structure. Evol Anthropol 17, 213–226.CrossRefGoogle Scholar
Smith, T.M., Tafforeau, P., Reid, D.J., Grün, R., Eggins, S., Boutakiout, M. & Hublin, J.-J. (2007). Earliest evidence of modern human life history in North African early Homo sapiens . P Natl Acad Sci 104, 6128–6133.CrossRefGoogle ScholarPubMed
Smith, T.M., Tafforeau, P., Reid, D.J., Pouech, J., Lazzari, V., Zermeno, J.P., Guatelli-Steinberg, D., Olejniczak, A.J., Hoffman, A., Radovcic, J., Makaremi, M., Tousaint, M., Stringer, C. & Hublin, J.-J. (2010). Dental evidence for ontogenetic differences between modern humans and Neanderthals. P Natl Acad Sci 107, 20923–20928.CrossRefGoogle ScholarPubMed
Sollas, W.J. (1904). A method for the investigation of fossils by serial sections. T Roy Soc London B 196, 259–265.Google Scholar
Tafforeau, P., Bentaleb, I., Jaeger, J.-J. & Martin, C. (2007). Nature of laminations and mineralization in rhinoceros enamel using histology and X-ray synchrotron microtomography: Potential implications for palaeoenvironmental isotopic studies. Palaeogeogr Palaeocl 246, 206–227.CrossRefGoogle Scholar
Tafforeau, P., Boistel, R., Boller, E., Bravin, A., Brunet, M., Chaimanee, Y., Cloetens, P., Feist, M., Hoszowska, J., Jaeger, J.-J., Kay, R.F., Lazzari, V., Marivaux, L., Neil, A., Nemoz, C., Thibault, X., Vignaud, P. & Zabler, S. (2006). Applications of X-ray synchrotron microtomography for non-destructive 3D studies of paleontological specimens. Appl Phys A-Mater 83, 195–202.CrossRefGoogle Scholar
Tafforeau, P. & Smith, T.M. (2008). Nondestructive imaging of hominoid dental microstructure using phase contrast X-ray synchrotron microtomography. J Hum Evol 54, 272–278.CrossRefGoogle ScholarPubMed
Witham, H.T.M. (1831). Observations on Fossil Vegetables. Edinburgh, UK: Blackwood.Google Scholar
Supplementary material: PDF

Sophie Sanchez et al. Supplementary Material

Appendix

Download Sophie Sanchez et al. Supplementary Material(PDF)
PDF 1.9 MB