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Structural commonalities and deviations in the hierarchical organization of crossed-lamellar shells: A case study on the shell of the bivalve Glycymeris glycymeris

Published online by Cambridge University Press:  11 March 2016

Corinna F. Böhm ,
Benedikt Demmert ,
Joe Harris ,
Tobias Fey ,
Frédéric Marin  and
Stephan E. Wolf
Corinna F. Böhm
Affiliation:
Department of Materials Science and Engineering, Chair for Glass and Ceramics, Friedrich-Alexander-University Erlangen-Nürnberg, 91058 Erlangen, Germany
Benedikt Demmert
Affiliation:
Department of Materials Science and Engineering, Chair for Glass and Ceramics, Friedrich-Alexander-University Erlangen-Nürnberg, 91058 Erlangen, Germany
Joe Harris
Affiliation:
Department of Materials Science and Engineering, Chair for Glass and Ceramics, Friedrich-Alexander-University Erlangen-Nürnberg, 91058 Erlangen, Germany
Tobias Fey
Affiliation:
Department of Materials Science and Engineering, Chair for Glass and Ceramics, Friedrich-Alexander-University Erlangen-Nürnberg, 91058 Erlangen, Germany
Frédéric Marin
Affiliation:
UMR CNRS 6282 Biogéosciences, Université de Bourgogne Franche-Comté, 21000 Dijon, France
Stephan E. Wolf*
Affiliation:
Department of Materials Science and Engineering, Chair for Glass and Ceramics, Friedrich-Alexander-University Erlangen-Nürnberg, 91058 Erlangen, Germany
*
a) Address all correspondence to this author. e-mail: stephan.e.wolf@fau.de
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Abstract

The structural organization of the palliostracum—the dominant part of the shell which is formed by the mantle cells—of Glycymeris glycymeris (Linné 1758) is comprised of five hierarchical levels with pronounced structural commonalities and deviations from other crossed-lamellar shells. The hierarchical level known as second order lamellae, present within other crossed-lamellar shells, is absent highlighting a short-coming of the currently used nomenclature. On the mesoscale, secondary microtubules penetrate the palliostracum and serve as crack arrestors. Moreover, the growth lamellae follow bent trajectories possibly impacting crack propagation, crack deflection, and energy dissipation mechanisms whilst circumventing delamination. Finally, at least two structural elements are related to external circatidal and circaanular stimuli. This emphasizes that endogeneous rhythms may contribute and (co-)control the self-organization of a complex mineralized tissue and that it is insufficient to rely fully on a reductionistic approach when studying biomineralization.

Keywords

biomimetic (assembly)crystal growthtoughness
Type
Biomineralization and Biomimetics Articles
Information
Journal of Materials Research , Volume 31 , Issue 5 , 14 March 2016 , pp. 536 - 546
Copyright
Copyright © Materials Research Society 2016 

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References

REFERENCES

Wegst, U.G.K., Bai, H., Saiz, E., Tomsia, A.P., and Ritchie, R.O.: Bioinspired structural materials. Nat. Mater. 14, 23–36 (2014).CrossRefGoogle ScholarPubMed
Wolf, S.E., Böhm, C., Harris, J., Hajir, M., Mondeshki, M., and Marin, F.: Single nanogranules preserve intracrystalline amorphicity in biominerals. Key Eng. Mater. 672, 47–59 (2015).Google Scholar
Tai, K., Ulm, F.J., and Ortiz, C.: Nanogranular origins of the strength of bone. Nano Lett. 6, 2520–2525 (2006).CrossRefGoogle ScholarPubMed
Li, X., Xu, Z-H., and Wang, R.: In situ observation of nanograin rotation and deformation in nacre. Nano Lett. 6, 2301–2304 (2006).CrossRefGoogle ScholarPubMed
Gao, H., Ji, B., Jager, I.L., Arzt, E., and Fratzl, P.: Materials become insensitive to flaws at nanoscale: lessons from nature. Proc. Natl. Acad. Sci. U. S. A. 100, 5597–5600 (2003).CrossRefGoogle ScholarPubMed
Jacob, D.E., Soldati, A., Wirth, R., Huth, J., Wehrmeister, U., and Hofmeister, W.: Nanostructure, composition and mechanisms of bivalve shell growth. Geochim. Cosmochim. Acta 72, 5401–5415 (2008).Google Scholar
Huang, Z. and Li, X.: Origin of flaw-tolerance in nacre. Sci. Rep. 3, 1693 (2013).Google Scholar
Barthelat, F., Li, C., Comi, C., and Espinosa, H.D.: Mechanical properties of nacre constituents and their impact on mechanical performance. J. Mater. Res. 21, 1977–1986 (2006).Google Scholar
Checa, A.G., Cartwright, J.H.E., and Willinger, M-G.: The key role of the surface membrane in why gastropod nacre grows in towers. Proc. Natl. Acad. Sci. U. S. A. 106, 38–43 (2009).CrossRefGoogle ScholarPubMed
Cartwright, J.H.E. and Checa, A.G.: The dynamics of nacre self-assembly. J. R. Soc., Interface 4, 491–504 (2007).CrossRefGoogle ScholarPubMed
Currey, J.D. and Taylor, J.D.: The mechanical behaviour of some molluscan hard tissues. J. Zool. 173, 395–406 (1974).Google Scholar
Burghard, Z., Zini, L., Srot, V., Bellina, P., Van Aken, P.A., and Bill, J.: Toughening through nature-adapted nanoscale design. Nano Lett. 9, 4103–4108 (2009).Google Scholar
Kamat, S., Su, X., Ballarini, R., and Heuer, A.H.: Structural basis for the fracture toughness of the shell of the conch Strombus gigas . Nature 405, 1036–1040 (2000).Google Scholar
Kuhn-Spearing, L.T., Kessler, H., Chateau, E., Ballarini, R., Heuer, A.H., and Spearing, S.M.: Fracture mechanisms of the Strombus gigas conch shell: implications for the design of brittle laminates. J. Mater. Sci. 31, 6583–6594 (1996).Google Scholar
Pokroy, B. and Zolotoyabko, E.: Microstructure of natural plywood-like ceramics: a study by high-resolution electron microscopy and energy-variable X-ray diffraction. J. Mater. Chem. 13, 682–688 (2003).Google Scholar
Weiner, S., Addadi, L., and Wagner, H.D.: Materials design in biology. Mater. Sci. Eng., C 11, 1–8 (2000).Google Scholar
Fleischli, F.D., Dietiker, M., Borgia, C., and Spolenak, R.: The influence of internal length scales on mechanical properties in natural nanocomposites: a comparative study on inner layers of seashells. Acta Biomater. 4, 1694–1706 (2008).CrossRefGoogle ScholarPubMed
Yang, W., Zhang, G., Liu, H., and Li, X.: Microstructural Characterization and Hardness Behavior of a Biological Saxidomus purpuratus Shell. J. Mater. Sci. Technol. 27, 139–146 (2011).CrossRefGoogle Scholar
Oliver, P.G. and Holmes, A.M.: The Arcoidea (Mollusca: Bivalvia): a review of the current phenetic-based systematics. Zool. J. Linn. Soc. 148, 237–251 (2006).CrossRefGoogle Scholar
Oberling, J.J.: Observations on some structural features of the pelecypod shell. Mitt. Naturforsch. Ges. Bern Neue Folge 20, 1–63 (1962).Google Scholar
Dame, R.: Ecology of Marine Bivalves: An Ecosystem Approach (CRC Press, Boca Raton, 1996).Google Scholar
Morvan, C.: Cycle de reproduction et fécondité de deux espéces de bivalves dans le golfe Normand-Breton. Ph.D Thesis, Université de Bretagne Occidentale, 1987.Google Scholar
Taylor, J.D., Kennedy, W.J., and Hall, A.: The shell structure and mineralogy of the Bivalvia. Nuculacea—Trigonacea. Bull. Br. Mus. 3, 1–125 (1969).Google Scholar
Yahyazadehfar, M., Bajaj, D., and Arola, D.D.: Hidden contributions of the enamel rods on the fracture resistance of human teeth. Acta Biomater. 9, 4806–4814 (2013).Google Scholar
Cuif, J-P., Dauphin, Y., and Sorauf, J.E.: Biominerals and Fossils Through Time (Cambridge University Press, New York, 2011).Google Scholar
Clark, G.R.: Growth Lines in Invertebrate Skeletons. Annu. Rev. Earth Planet. Sci. 2, 77–99 (1974).Google Scholar
Rhoads, D.C. and Lutz, R.A.. Growth Patterns within the Molluscan Shell: An overview. In Skeletal Growth of Aquatic Organisms: Biological Records of Environmental Change, Rhoads, D.C. and Lutz, R.A., eds. (Plenum Press: New York, 1980); pp. 203–255.Google Scholar
Jackson, A.P., Vincent, J.F.V., and Turner, R.M.: Comparison of nacre with other ceramic composites. J. Mater. Sci. 25, 3173–3178 (1990).Google Scholar
Younis, S., Kauffmann, Y., Pokroy, B., and Zolotoyabko, E.: Atomic structure and ultrastructure of the Murex troscheli shell. J. Struct. Biol. 180, 539–545 (2012).Google Scholar
Barthelat, F., Rim, J.E., and Espinosa, H.D.: A Review on the Structure and Mechanical Properties of Mollusk Shells - Perspectives on Synthetic Biomimetic Materials. In Applied Scanning Probe Methods XIII, Biomimetics and Industrial Applications, Bhushan, B. and Fuchs, H., eds. (Springer: New York, 2009); pp. 17–41.Google Scholar
Kobayashi, I. and Akai, J.: Twinned aragonite crystals found in the bivalvian crossed lamellar shell structure. J. Geol. Soc. Jpn. 100, 177–180 (1994).Google Scholar
Wolf, S.E., Böhm, C.F., Harris, J., Demmert, B., Jacob, D., Mondeshki, M., Ruiz-Agudo, E., and Navarro, C.R.: Nonclassical Crystallization in vivo et in vitro (I): Process-Structure-Property relationships of nanogranular biominerals. J. Struct. Biol. (2016). In review.Google Scholar
Wolf, S.E., Lieberwirth, I., Natalio, F., Bardeau, J-F., Delorme, N., Emmerling, F., Barrea, R., Kappl, M., and Marin, F.: Merging models of biomineralisation with concepts of nonclassical crystallisation: is a liquid amorphous precursor involved in the formation of the prismatic layer of the Mediterranean Fan Mussel Pinna nobilis? Faraday Discuss. 159, 433 (2012).Google Scholar
Gal, A., Kahil, K., Vidavsky, N., DeVol, R.T., Gilbert, P.U.P.A., Fratzl, P., Weiner, S., and Addadi, L.: Particle Accretion Mechanism Underlies Biological Crystal Growth from an Amorphous Precursor Phase. Adv. Funct. Mater. 24, 5420–5426 (2014).CrossRefGoogle Scholar
Gal, A., Habraken, W., Gur, D., Fratzl, P., Weiner, S., and Addadi, L.: Calcite Crystal Growth by a Solid-State Transformation of Stabilized Amorphous Calcium Carbonate Nanospheres in a Hydrogel. Angew. Chem., Int. Ed. 125, 4967–4970 (2013).Google Scholar
Ihli, J., Wong, W.C., Noel, E.H., Kim, Y-Y., Kulak, A.N., Christenson, H.K., Duer, M.J., and Meldrum, F.C.: A critical analysis of calcium carbonate mesocrystals. Nat. Commun. 5, 3169 (2014).CrossRefGoogle Scholar
Jacob, D.E., Wirth, R., Soldati, A., Wehrmeister, U., and Schreiber, A.: Amorphous calcium carbonate in the shells of adult Unionoida. J. Struct. Biol. 173, 241–249 (2011).CrossRefGoogle ScholarPubMed
Hovden, R., Wolf, S.E., Holtz, M.E., Marin, F., Muller, D.A., and Estroff, L.A.: Nanoscale assembly processes revealed in the nacroprismatic transition zone of Pinna nobilis mollusc shells. Nat. Commun. 6, 10097 (2015).Google Scholar
Dauphin, Y.: The nanostructural unity of Mollusc shells. Miner. Mag. 72, 243–246 (2008).Google Scholar
Sethmann, I.: Observation of nano-clustered calcite growth via a transient phase mediated by organic polyanions: A close match for biomineralization. Am. Miner. 90, 1213–1217 (2005).Google Scholar
Sethmann, I., Hinrichs, R., Wörheide, G., and Putnis, A.: Nano-cluster composite structure of calcitic sponge spicules–a case study of basic characteristics of biominerals. J. Inorg. Biochem. 100, 88–96 (2006).Google Scholar
Araujo, R., Ramos, M.A., and Bedoya, J.: Microtubules in the shell of the invasive bivalve Corbicula fluminea. J. Molluscan Stud. 60, 406–413 (1994).CrossRefGoogle Scholar
Hallett, P.D., Dexter, A.R., and Seville, J.P.K.: Identification of pre-existing cracks on soil fracture surfaces using dye. Soil Tillage Res. 33, 163–184 (1995).CrossRefGoogle Scholar
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