Hostname: page-component-cd9895bd7-mkpzs Total loading time: 0 Render date: 2024-12-26T03:20:31.855Z Has data issue: false hasContentIssue false
  • English
  • Français

Hierarchical fibre composite structure and micromechanical properties of phosphatic and calcitic brachiopod shell biomaterials — an overview

Published online by Cambridge University Press:  05 July 2018

W. W. Schmahl ,
E. Griesshaber ,
C. Merkel ,
K. Kelm ,
J. Deuschle ,
R. D. Neuser ,
A. J. Göetz ,
A. Sehrbrock  and
W. Mader
W. W. Schmahl*
Affiliation:
GeoBioCentre and Department of Earth and Environmental Sciences, LMU Munich, Theresienstrasse 41, 80333 Munich, Germany
E. Griesshaber
Affiliation:
GeoBioCentre and Department of Earth and Environmental Sciences, LMU Munich, Theresienstrasse 41, 80333 Munich, Germany
C. Merkel
Affiliation:
GeoBioCentre and Department of Earth and Environmental Sciences, LMU Munich, Theresienstrasse 41, 80333 Munich, Germany
K. Kelm
Affiliation:
Institut für Anorganische Chemie, Römerstraβe 164, Universität Bonn, D-53117 Bonn, Germany
J. Deuschle
Affiliation:
Max Planck Institut für Metallforschung, Heisenbergstrasse 3, 70569 Stuttgart, Germany
R. D. Neuser
Affiliation:
Institut für Geologie, Mineralogie und Geophysik, Ruhr-Universität Bochum, Universitätsstrasse 150, 44801 Bochum, Germany
A. J. Göetz
Affiliation:
GeoBioCentre and Department of Earth and Environmental Sciences, LMU Munich, Theresienstrasse 41, 80333 Munich, Germany
A. Sehrbrock
Affiliation:
Forschungszentrum CAESAR, Ludwig-Erhard-Allee 2, 53175 Bonn, Germany
W. Mader
Affiliation:
Institut für Anorganische Chemie, Römerstraβe 164, Universität Bonn, D-53117 Bonn, Germany
*
*E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

Brachiopods are a phylum of shell-forming sessile marine invertebrates which have existed since the early Cambrian. Two very different biomaterial design strategies for their shells evolved early in their history. Both strategies use hybrid fibre composites, however, one is based on mineral fibres embedded in ~2 wt.% of organic biopolymer sheaths and the inorganic fibres are calcite single crystals. In the second strategy the fibres are biopolymers and are reinforced with Ca-phosphate nanoparticles to form a fibrous nanocomposite. Here the organic component (chitin) dominates. The Ca-phosphate nanoparticle-reinforcement strategy is not unlike that in vertebrate bone, however, the microscale structure is laminated with alternating laminae which have a different degree of mineralization.

The calcitic shells feature an outer compact layer of calcite micro- and nanoparticles protecting the inner fibrous layer from the outside. Transmission electron microscopy of the fibrous layer reveals intercrystalline and intracrystalline biopolymers. The calcitic shell material is stiff with nano-indentation E-moduli of 63±8 GPa and relatively hard (Vickers microhardness up to 400 HV 0.0005/10 and nanohardness 4±0.5 GPa). Compared to inorganic calcite the microhardness is doubled and the nanohardness increases by 60%. We attribute this increased hardness to intracrystalline biopolymers. The nano-indentation E-moduli of the chitinophosphatic shells range from 3 to 55 GPa as a result of the varying degree of mineralization between their laminae, and similarly their nanohardness varies between 0.1 and 3 GPa. For brachiopods burrowing inside the sediment, the alternation of non-mineralized laminae with thin, more strongly mineralized laminae provides abrasion-resistance, hardness and longitudinal stiffness while it preserves the flexibility provided by the organic component for bending movements.

Keywords

biomineralizationhierarchical architecturenano-indentationEBSDamorphous calciumphosphateACPhydroxylapatiteHAPnacrepalaeoclimate
Type
Research Article
Information
Mineralogical Magazine , Volume 72 , Issue 2 , April 2008 , pp. 541 - 562
Copyright
Copyright © The Mineralogical Society of Great Britain and Ireland 2008

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

Alexander, R.R. (2001) Functional morphology and biomechanics of articulate shells. Pp. 17–145 in: Brachiopods Ancient and Modern — A Tribute to G. A. Cooper (Carlson, S.J. and White, R.D., editors). The Paleontological Society Papers, 7, Yale University, New Haven, CT, USA.Google Scholar
Barthelat, F. and Espinosa, H.D. (2007) An experimental investigation of deformation and fracture of nacre-mother of pearl. Experimental Mechanics, 47, 311–324.CrossRefGoogle Scholar
Brand, U., Logan, A., Hiller, N. and Richardson, J. (2003) Geochemistry of modern brachiopods: applications and implications for oceanography and paleoceanography. Chemical Geology, 198, 305–334.CrossRefGoogle Scholar
Carpenter, SJ. and Lohmann, K.C. (1995) 518O and 5 C values of modern brachiopod shells. Geochimica et Cosmochimica Ada, 59, 3749–3764.CrossRefGoogle Scholar
Currey, J.D. (1977) Mechanical properties of mother of pearl in tension. Proceedings of the Royal Society of London, 196, 443—463. Currey, J.D. (1990) Biomechanics in mineralized skeletons. Pp. 11–25 in: Skeletal Biomineralization: Patterns, Processes and Evolutionary Trends (Carter, J.G., editor). Van Nostrand Reinhold, New York.Google Scholar
Currey, J.D. (1999) The design of mineralised hard tissues for their mechanical functions. Journal of Experimental Biology, 202, 3285–3294.Google ScholarPubMed
Currey, J.D. (2006) Bones: Structure and Mechanics. Princeton University Press, Princeton, New Jersey, 456 pp.Google Scholar
Currey, J.D. and Taylor, J.D. (1974) The mechanical behaviour of some molluscan hard tissues. Journal of Zoology (London), 173, 395–406.CrossRefGoogle Scholar
Gao, H.J. (2006) Application of fracture mechanics concepts to hierarchical biomechanics of bone and bone-like materials. International Journal of Fracture, 138, 101–137.CrossRefGoogle Scholar
Gay, D. and Hoa, V.S. (2007) Composite Materials: Design and Applications. CRC Press (London), 548 pp.Google Scholar
Gotz, A., Griesshaber, E., Schmahl, W.W., Neuser, R.D., Litter, C, Hiihner, M. and Harper, E.M. (submitted) The texture and hardness distribution pattern in recent brachiopods — a comparative study of Kakanuiella chathamensis, Liothyrella uva and Liothyrella neozelanica. European Journal of Mineralogy. Google Scholar
Griesshaber, E., Schmahl, W.W., Neuser, R.D., Job, R., Bluem, M. and Brand, U. (2005) Microstructure of brachiopod shells — an inorganic/organic fibre composite with nanocrystalline protective layer. MRS Symposium Proceedings Series, 844, 99–104.Google Scholar
Griesshaber, E., Kelm, K., Icnieps, M., Schmahl, W.W., Job, R. and Mader, W. (2006) The ultrastructure of brachiopod shells — A mechanically optimized material with hierarchical architecture. Materials Research Society Symposium Proceedings, 989E, 0898-L12–01.Google Scholar
Griesshaber, E., Schmahl, W.W., Neuser, R., Pettke, Th., Blum, M., Mutterlose, J. and Brand, U. (2007) Crystallographic texture and microstructure of terebratulid brachiopod shell calcite: An optimized materials design with hierarchical architecture. American Mineralogist, 92, 722–734.CrossRefGoogle Scholar
Grossmann, E.L., Mii, H.-S., Zhang, C. and Yancey, T. (1996) Chemical variation in Pennsylvanian brachiopod shells — diagenetic, taxonomic, microstructural and seasonal effects. Journal of Sedimentary Research, 66, 1011–1022.Google Scholar
Jackson, A.P., Vincent, J.F.V. and Turner, R.M. (1988) The mechanical design of nacre. Proceedings of the Royal Society of London, 234, 415–440.Google Scholar
Kamat, S., Su, X., Ballarini, R. and Heuer, A. (2000) Structural basis for the fracture toughness of the shell of the conch Strombus gigas. Nature, 405, 1036–1040.CrossRefGoogle Scholar
Katti, K., Katti, D.R., Tang, J., Pradhan, S. and Sarikaya M. (2005) Modeling mechanical responses in a laminated biocomposite. Part II. Nonlinear responses and nuances of nanostructure. Journal of Materials Science, 40, 1749–1755.CrossRefGoogle Scholar
Li, X.D., Chang, W.C., Chao, Y.J., Wang, R.Z. and Chang, M. (2004) Nanoscale structural and mechanical characterization of a natural nanocomposite material: the shell of red abalone. Nano Letters, 4, 613–617.CrossRefGoogle Scholar
Lowenstam, H.A. (1961) Mineralogy, 18O/16O ratios, and strontium and magnesium contents of recent and fossil brachiopods and their bearing on the history of oceans. Journal of Geology, 69, 241–260.CrossRefGoogle Scholar
Lowenstam, H.A. (1981) Minerals formed by Organisms. Science, 211, 1126–1131.CrossRefGoogle ScholarPubMed
Mayer, G. and Sarikaya, M. (2002) Rigid biological composite materials: Structural examples for biomi-metic design. Experimental Mechanics, 42, 395–403.CrossRefGoogle Scholar
Merkel, C, Griesshaber, E., Kelm, K., Neuser, R., Jordan, G., Logan, A., Mader, W. and Schmahl, W.W. (2007) Micromechanical properties and structural characterization of modern inarticulated brachiopod shells. Journal of Geophysical Research, 111, G02008, doi:10.1029/2006JG000253.Google Scholar
Okumura, K. and de Gennes, P.G. (2001) Why is nacre strong? Elastic theory and fracture mechanics for biocomposites with stratified structures. European Physical Journal E - Soft Matter, 4, 121–127.CrossRefGoogle Scholar
Oliver, W.C. and Pharr, G.M. (1992) An improved technique for determining hardness and elastic modulus using load and displacement sensing indentation experiments. Journal of Materials Research, 6, 1564–1583.CrossRefGoogle Scholar
Parkinson, D., Curry, G.B., Cusack, M. and Fallick, A.E. (2005) Shell structure, patterns and trends of oxygen and carbon stable isotopes in modern brachiopod shells. Chemical Geology, 219, 193–235.CrossRefGoogle Scholar
Perez-Huerta, A., Cusack, M., Zhu, W., England, J. and Hughes, J. (2007) Material properties of brachiopod shell ultrastructure by nanoindentation. Journal of the Royal Society Interface, 4, 33–39.CrossRefGoogle ScholarPubMed
Randle, V. and Engler, O. (2000) Introduction to Texture Analysis. CRC Press, Amsterdam, 408 pp.CrossRefGoogle Scholar
Reindl, S., Salvenmoser, W. and Haszprunar, G. (1995) Fine-structural and immunocytochemical investigations of the Ceca of Argyrotheca-cordata and Argyrotheca-cuneata (Brachiopoda, Terebratulida, Terebratellacea). Journal of Submicroscopic Cytology and Pathology, 27, 543–556.Google Scholar
Rowell, A. and Grant, R. (1987) Phylum Brachiopoda. Pp. 445–497 in: Fossil Invertebrates (Bradman, R.S., Cheetham, A.H. and Rowell, A.J., editors). Blackwell Scientific Publications, Oxford, UK.Google Scholar
Rudwick, M.J.S. (1970) Living and Fossil Brachiopods. Hutchinson and Co. LTD, London, 199 pp.Google Scholar
Samtleben, C, Munnecke, A. and Bickert, T. (2001) Shell succession, assemblage and species dependent effects on the C/O-isotopic composition of brachio-pods — examples from the Silurian of Gotland. Chemical Geology, 175, 61–107.CrossRefGoogle Scholar
Sarikaya, M. and Aksay, LA. (Eds) (1995) Biomimetics, Design and Processing of Materials. Woodbury, NY.Google Scholar
Schmahl, W.W., Griesshaber, E., Neuser, R.D., Lenze, A., Job, R. and Brand, U. (2004) The microstructure of the fibrous layer of terebratulide brachiopod shell calcite. European Journal of Mineralogy, 16, 693–697.CrossRefGoogle Scholar
Schmidt, N.H. and Olesen, N.O. (1989) Computer-aided determination of crystal-lattice orientation from electron channeling patterns in the SEM. The Canadian Mineralogist, 27, 15–22.Google Scholar
Song, F. and Bai, Y. (2002) Nanostructure of nacre and its mechanical effects. International Journal of Nonlinear Science and Numerical Simulations, 3, 257–260.Google Scholar
Thayer, C.W. and Steele-Petrovic, H.M. (1975) Burrowing of the lingulid brachiopod Glottidia pyramidata: its ecologic and paleoecologic significance. Lethaia, 8, 209–221.CrossRefGoogle Scholar
Taylor, W. (1949) Correlation of the Mohs's scale of hardness with the Vickers's hardness numbers. American Mineralogist, 28, 718–721.Google Scholar
Veizer, J., Ala, D. and Azmy, K. (1999) 87Sr/86Sr, 513C and 518O evolution of Phanerozoic seawater. Chemical Geology, 161, 59–88.CrossRefGoogle Scholar
Weiner, S., Traub, W. and Wagner, H.D. (1999) Lamellar bone: Structure-function relations. Journal of Structural Biology, 126, 241–255.CrossRefGoogle ScholarPubMed
Williams, A. (1968) Evolution of the shell structure of articulate brachiopods. Special Papers in Paleontology, 2, 1–55.Google Scholar
Williams, A. and Cusack, M. (1999) Evolution of a rhythmic lamination in the organophosphatic shells of brachiopods. Journal of Structural Biology, 126, 227–240.CrossRefGoogle ScholarPubMed
Williams, A., Mackay, S. and Cusack, M. (1992) Structure of the organo-phosphatic shell of the brachiopod Discina. Philosophical Transactions of the Royal Society, B337, 83–104.Google Scholar
Williams, A., Cusack, M. and Mackay, S. (1994) Collagenous chitinophosphatic shell of the brachiopod Lingula. Philosophical Transactions of the Royal Society, B346, 223–266.Google Scholar
Williams, A., Cusack, M., Buckman, J. and Stachel, T. (1998a) Siliceous tablets in the larval shells of apatitic discinid brachiopods. Science, 279, 2094–2096.CrossRefGoogle Scholar
Williams, A., Cusack, M. and Buckmann, J. (19986) Chemico-structural phylogeny of the discinoid brachiopod shell. Philosophical Transactions of the Royal Society, B353, 2005–2038.Google Scholar
Williams, A., Carlson, SJ. and Brunton, C.H.C. (2000) Brachiopod classification. Pp. 1–27 in: Treatise on Invertebrate Paleontology, Part H, Brachiopoda (revised) (A. Williams, C.H.C. Brunton, and Carlson, SJ., editors). Vol. 2. Geological Society of America, The University of Kansas Press, Lawrence, Kansas, USA.Google Scholar