Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Letter
  • Published:

Self-similar mesostructure evolution of the growing mollusc shell reminiscent of thermodynamically driven grain growth

Abstract

Significant progress has been made in understanding the interaction between mineral precursors and organic components leading to material formation and structuring in biomineralizing systems1,2,3,4,5. The mesostructure of biological materials, such as the outer calcitic shell of molluscs, is characterized by many parameters and the question arises as to what extent they all are, or need to be, controlled biologically. Here, we analyse the three-dimensional structure of the calcite-based prismatic layer of Pinna nobilis6,7,8, the giant Mediterranean fan mussel, using high-resolution synchrotron-based microtomography. We show that the evolution of the layer is statistically self-similar and, remarkably, its morphology and mesostructure can be fully predicted using classical materials science theories for normal grain growth9,10,11,12,13,14,15,16. These findings are a fundamental step in understanding the constraints that dictate the shape of these biogenic minerals and shed light on how biological organisms make use of thermodynamics to generate complex morphologies.

This is a preview of subscription content, access via your institution

Access options

Buy this article

Prices may be subject to local taxes which are calculated during checkout

Figure 1: The microstructure of the prismatic layer of P. nobilis.
Figure 2: Mesostructure characterization based on mean field considerations.
Figure 3: Mesostructure characterization based on topological considerations.

Similar content being viewed by others

References

  1. Weiner, S. & Addadi, L. Crystallization pathways in biomineralization. Annu. Rev. Mater. Res. 41, 21–40 (2011).

    Article  CAS  Google Scholar 

  2. Nudelman, F. & Sommerdijk, N. Biomineralization as an inspiration for materials chemistry. Angew. Chem. Int. Ed. 51, 6582–6596 (2012).

    Article  CAS  Google Scholar 

  3. Schenk, A. S. et al. Systematic study of the effects of polyamines on calcium carbonate precipitation. Chem. Mater. 26, 2703–2711 (2014).

    Article  CAS  Google Scholar 

  4. Gower, L. B. Biomimetic model systems for investigating the amorphous precursor pathway and its role in biomineralization. Chem. Rev. 108, 4551–4627 (2008).

    Article  CAS  Google Scholar 

  5. Schenk, A. S. et al. Hierarchical calcite crystals with occlusions of a simple polyelectrolyte mimic complex biomineral structures. Adv. Funct. Mater. 22, 4668–4676 (2012).

    Article  CAS  Google Scholar 

  6. Marin, F., Narayanappa, P. & Motreuil, S. in Molecular Biomineralization Vol. 52 (ed. Müller, W. E. G.) Ch. 13, 353–395 (Springer, 2011).

    Book  Google Scholar 

  7. Taylor, J. & Layman, M. The mechanical properties of bivalve (Mollusca) shell structures. Palaeontology 15, 73–87 (1972).

    Google Scholar 

  8. Marin, F. & Luquet, G. Molluscan biomineralization: The proteinaceous shell constituents of Pinna nobilis L. Mater. Sci. Eng. C 25, 105–111 (2005).

    Article  Google Scholar 

  9. Atkinson, H. V. Theories of normal grain growth in pure single phase systems. Acta Metall. 36, 469–491 (1988).

    Article  CAS  Google Scholar 

  10. Hillert, M. On the theory of normal and abnormal grain growth. Acta Metall. 13, 227–238 (1965).

    Article  CAS  Google Scholar 

  11. Mullins, W. W. Two-dimensional motion of idealized grain boundaries. J. Appl. Phys. 27, 900–904 (1956).

    Article  Google Scholar 

  12. Von Neumann, J. in Metal Interfaces (ed Herring, C.) 108–110 (American Society of Metals, 1952).

    Google Scholar 

  13. Burke, J. & Turnbull, D. Recrystallization and grain growth. Prog. Met. Phys. 3, 220–244 (1952).

    Article  CAS  Google Scholar 

  14. Srolovitz, D. J., Anderson, M. P., Crest, G. S. & Sahni, P. S. Computer simulation of grain growth-II. Grain size distribution, topology, and local dynamics. Acta Metall. 32, 793–802 (1984).

    Article  CAS  Google Scholar 

  15. Smith, C. S. Some elementary principles of polycrystalline microstructure. Metall. Rev. 9, 1–48 (1964).

    CAS  Google Scholar 

  16. Smith, C. S. Structure, substructure, and superstructure. Rev. Mod. Phys. 36, 524–532 (1964).

    Article  Google Scholar 

  17. Fratzl, P. & Weinkamer, R. Nature’s hierarchical materials. Prog. Mater. Sci. 52, 1263–1334 (2007).

    Article  CAS  Google Scholar 

  18. Dauphin, Y. et al. In situ mapping of growth lines in the calcitic prismatic layers of mollusc shells using X-ray absorption near-edge structure (XANES) spectroscopy at the sulphur K-edge. Mar. Biol. 142, 299–304 (2003).

    Article  Google Scholar 

  19. Pokroy, B., Fitch, A. & Zolotoyabko, E. The microstructure of biogenic calcite: A view by high-resolution synchrotron powder diffraction. Adv. Mater. 18, 2363–2368 (2006).

    Article  CAS  Google Scholar 

  20. Dauphin, Y. Comparison of the soluble matrices of the calcitic prismatic layer of Pinnanobilis (Mollusca, Bivalvia, Pteriomorpha). Comp. Biochem. Physiol. A 132, 577–590 (2002).

    Article  CAS  Google Scholar 

  21. Olson, I. C. et al. Crystal nucleation and near-epitaxial growth in nacre. J. Struct. Biol. 184, 454–463 (2013).

    Article  CAS  Google Scholar 

  22. Checa, A. G., Rodríguez-Navarro, A. B. & Esteban-Delgado, F. J. The nature and formation of calcitic columnar prismatic shell layers in pteriomorphian bivalves. Biomaterials 26, 6404–6414 (2005).

    Article  CAS  Google Scholar 

  23. Thompson, C. V. Grain growth in thin films. Annu. Rev. Mater. Sci. 20, 245–268 (1990).

    Article  CAS  Google Scholar 

  24. Barmak, K. et al. Grain growth and the puzzle of its stagnation in thin films: The curious tale of a tail and an ear. Prog. Mater. Sci. 58, 987–1055 (2013).

    Article  CAS  Google Scholar 

  25. Beck, P. Annealing of cold worked metals. Adv. Phys. 3, 245–324 (1954).

    Article  Google Scholar 

  26. Mullins, W. W. The statistical self-similarity hypothesis in grain growth and particle coarsening. J. Appl. Phys. 59, 1341–1349 (1986).

    Article  CAS  Google Scholar 

  27. Elsey, M., Esedoglu, S. & Smereka, P. Large-scale simulation of normal grain growth via diffusion-generated motion. Proc. R. Soc. A 467, 381–401 (2010).

    Article  Google Scholar 

  28. Fayad, W., Thompson, C. V. & Frost, H. J. Steady-state grain-size distributions resulting from grain growth in two dimensions. Scripta Mater. 40, 1199–1204 (1999).

    Article  CAS  Google Scholar 

  29. Zöllner, D. & Rios, P. R. Investigating the von Neumann–Mullins relation under triple junction dragging. Acta Mater. 70, 290–297 (2014).

    Article  Google Scholar 

  30. Weitkamp, T., Haas, D., Wegrzynek, D. & Rack, A. ANKAphase: Software for single-distance phase retrieval from inline X-ray phase-contrast radiographs. J. Synchrotron Radiat. 18, 617–629 (2011).

    Article  CAS  Google Scholar 

  31. Schneider, C. A, Rasband, W. S. & Eliceiri, K. W. NIH Image to ImageJ: 25 years of image analysis. Nature Methods 9, 671–675 (2012).

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We acknowledge the European Synchrotron Radiation Facility for provision of synchrotron radiation facilities on ID19. Project supported in part by the German Science Foundation DFG, project FR 2190/4-1 (Leibniz Prize to P.F.).

Author information

Authors and Affiliations

Authors

Contributions

B.B. prepared the samples for the tomography experiments. B.B., I.Z., P.Z. and A.R. performed the synchrotron-based microtomography experiments. P.Z. and A.R. performed the data processing. B.B., P.F. and I.Z. performed image and data analysis. Y.D. supplied the samples. B.B., P.F. and I.Z. wrote the manuscript. I.Z. conceived the project. All authors commented on the manuscript.

Corresponding author

Correspondence to Igor Zlotnikov.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Supplementary information

Supplementary Information

Supplementary Movie S1 (AVI 4759 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Bayerlein, B., Zaslansky, P., Dauphin, Y. et al. Self-similar mesostructure evolution of the growing mollusc shell reminiscent of thermodynamically driven grain growth. Nature Mater 13, 1102–1107 (2014). https://doi.org/10.1038/nmat4110

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nmat4110

This article is cited by

Search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing