Variability in the crystallographic texture of bivalve nacre


Authors: Frýda J, Klicnarová K, Frýdová B, Mergl M

Published in: Bulletin of Geosciences, volume 85, issue 4; pages: 645 - 662; Received 18 October 2010; Accepted in revised form 6 December 2010; Online 13 December 2010

Keywords: Bivalvia, nacre, crystallographic texture, phylogeny,

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The crystallographic texture of nacre in eleven bivalve species belonging to the superorders Opponobranchia, Pteriomorpha, and Paleoheterodonta, was studied. Our analysis confirmed a uniform orientation of the crystallographic c-axes of aragonite platelets in all the species studied, but a variable arrangement of a- and b-axes. New data suggest that the rate of alignment of a- and b-axes from girdle-like (unordered nacre) to a single crystal-like texture (ordered nacre) differs considerably among the analyzed species. Numerical evaluation of the data obtained from species with ordered nacre also revealed systematic differences in texture strength among the main crystallographic axes of aragonite platelets. The texture strength of a-axes (direction parallel to growth lines) is always weaker than that of b- and c-axes. Observed differences in shape of the growth lines on the surface of nacreous platelets, in twinning percentage as well as in rate of alignment of a- and b-axes suggest variations in nacre growth process in individual phylogenetic lineages of the Class Bivalvia. These facts may imply not only evolutionary changes in microstructure and crystallographic texture of the nacre but also in molecular mechanisms driving its production during the long molluscan evolution.


Addadi, L., Joester, D., Nudelman, F. & Weiner, S. 2006. Mollusk Shell Formation: A Source of New Concepts for Understanding Biomineralization Processes. Chemistry - A European Journal 12, 980-987.View article

Aktipis, S.W., Giribet, G., Lindberg, D.R. & Ponder, W.F. 2008. Gastropoda - an overview and analysis, 201-237. In Ponder, W. & Lindberg, D.L. (eds) Phylogeny and Evolution of the Mollusca. 488 pp. University of California Press, Berkeley and Los Angeles, California.

Bandel, K. 1982. Morphologie und Bildung der fruhontogenetischen Gehause bei conchiferen Mollusken. Fazies 7, 1-198.

Bandel, K. 1993. Evolutionary history of sinistral archaeogastropods with and without slit (Cirroidea, Vetigastropoda). Freiberger Forschungshefte, Paläontologie C450, 41-82.

Bandel, K. 1997. Higher classification and pattern of evolution of the Gastropoda. Courier Forschungsinstitut Senckenberg 201, 57-81.

Bandel, K. & Geldmacher, W. 1996. The structure of the shell of Patella crenata connected with suggestions to the classification and evolution of the Archaeogastropoda. Freiberger Forschungsheft C 464, 1-71.

Bandel, K., Nützel, A. & Yancey, T.E. 2002. Larval shells and shell microstructures of exceptionally well-preserved Late Carboniferous gastropods from the Buckhorn Asphalt Deposit (Oklahoma, USA). Senckenbergiana lethaea 82(2), 639-689.View article

Batten, R.L. 1972. The ultrastructure of five common Pennsylvanian pleurotomarian gastropod species of Eastern United States. American Museum Novitates 2501, 1-34.

Bertoldi, K., Bigoni, D. & Drugan, W.J. 2008. Nacre: An orthotropic and bimodular elastic material. Composites Science and Technology 68, 1363-1375.View article

Beurlen, K. 1944. Beitrage zur Stammesgeschichte der Muscheln. München Akademie Sitzungsberichte 11, 113-131.

Bieler, R. & Mikkesen, P. 2006. Bivalvia - a look at the branches. Zoological Journal of the Linnean Society 148(3), 223-235.View article

Bieler, R., Carter, J.G. & Coan, E.V. 2010. Classification of bivalve families, 113-133. In Bouchet, P. & Rocroi, J.-P. Nomenclator of bivalve families. Malacologia 52(2), 1-184.

Bouchet, P. & Rocroi, J.-P. 2010. Nomenclator of bivalve families with a classification of bivalve families by R. Bieler, J.G. Carter & E.V. Coan. Malacologia 52(2), 1-184.View article

Bouchet, P., Rocroi, J.-P., Frýda, J., Hausdorf, B., Ponder, W., Valdes, A. & Warén, A. 2005. Classification and nomenclator of gastropod families. Malacologia 47(1-2), 1-368.

Bragg, W.L. 1924. The structure of aragonite. Proceedings of the Royal Society of London, Series A105, 16-37.View article

Carter, J.G. 1990a. Evolutionary significance of shell microstructure in the Palaeotaxodonta, Pteriomorphia and isofilibranchia (Bivalvia: Mollusca), 136-296. In Carter, J.G. (ed.) Skeletal Biomineralisation: Patterns, Processes and evolutionary trends. Vol. II. Atlas and Index. 832 pp. Van Nostrand Reinhold, New York.

Carter, J.G. 1990b. Shell microstructural data for the Bivalvia, 297-412. In Carter, J.G. (ed.) Skeletal Biomineralisation: Patterns, Processes and evolutionary trends. Vol. II. Atlas and Index. 832 pp. Van Nostrand Reinhold, New York. Cartwright, J.H.E. & Checa, A.G. 2007. The dynamics of nacre self-assembly. Journal of the Royal Society Interface 4, 491-504.View article

Chateigner, D., Hedegaard, C. & Wenk, H.-R. 2000. Mollusc shell microstructures and crystallographic textures. Journal of Structural Geology 22, 1723-1735.View article

Chateigner, D., Ouhenia, S., Krauss, C., Belkhir, M. & Morales, M. 2010. Structural distortion of biogenic aragonite in strongly textured mollusc shell layers. Nuclear Instruments and Methods in Physics Research B 268, 341-345.View article

Checa, A.G.,Okamoto, T. & Ramirez, J. 2006. Organization pattern of nacre in Pteriidae (Bivalvia: Mollusca) explained by crystal competition. Proceedings of the Royal Society B 273, 1329-1337.View article

Checa, A.G., Ramírez-Rico, J., González-Segura, A. & Sánchez-Navas, A. 2008. Nacre and false nacre (foliated aragonite) in extant monoplacophorans (= Tryblidiida: Mollusca). Naturwissenschaften, 111-122.View article

Checa, A.G. & Rodríguez-Navarro, A.B. 2000. Geometrical and crystallographic constraints determine the self-organization of shell microstructures in Unionidae (Bivalvia: Mollusca). Proceedings of the Royal Society of London, Series B 268, 771-778.View article

Checa, A.G. & Rodríguez-Navarro, A.B. 2005. Self-organisation of nacre in the shells of Pterioida (Bivalvia: Mollusca). Biomaterials 26, 1071-1079.View article

Conrad, T.A. 1837. Descriptions of new marine shells, from Upper California. Journal of the Academy of Natural Sciences of Philadelphia 7, 227-268.

Cox, L.R. 1960. Thoughts on the classification of the Bivalvia. Proceedings of the Malacological Society of London 34, 60-80.

Dall, W.H. 1889. On the hinge of pelecypods and its development, with an attempt toward a better subdivision of the group. American Journal of Science, Ser. 3, 38(228), 445-462.

Dauphin, Y., Ball, A.D., Cotte, M., Cuif, J.-P., Meibom, A., Salome, M., Susini, J. & Williams, C.T. 2008. A microstructural, mineralogical, and chemical study of the nacre-prisms boundary in the shells of Pinctada margaritifera (Mollusca, Bivalvia). Analytical and Bioanalytical Chemistry 390, 1659-1669.View article

Denkena, B., Koehler, J. & Moral, A. 2010. Ductile and brittle material removal mechanisms in natural nacre - A model for novel implant materials. Journal of Materials Processing Technology 210, 1827-1837.View article

Dunker, W. 1857. Mytilacea nova collectionis Cumingianae. Proceedings of the Zoological Society of London 24, 358-366.

Dunker, W. 1872. Die Gattung Avicula in Abbildungennach der Natur mit Beschreibungen. In Kuster, H.C. (ed.) Systematisches Conchylien-Cabinet von Martini und Chemnitz, vol. 7. Bauer & Raspe, Nurnberg.

Falini, G., Shira Albeck, S., Weiner, S. & Addadi, L. 1996. Control of Aragonite or Calcite Polymorphism by Mollusk Shell Macromolecules. Science 271(5245), 67-69.View article

Feng, W. & Sun, W. 2003. Phosphate replicated and replaced microstructure of molluscan shells from the earliest Cambrian of China. Acta Palaeontologica Polonica 48(1), 21-30.

Ferussac, A.E.J.P.J.F. d’Audebard de 1822. Tableaux systématiques des animaux mollusques classés en familles naturelles, dans lesquels on a établi la concordance de tous les systemes; suivis d’un prodrome général pour tous les mollusques terrestres ou fluviatiles, vivants ou fossiles. 110 pp. Paris.

Frýda, J. 1997. Oldest representatives of the superfamily Cirroidea (Vetigastropoda) with notes on their early phylogeny. Journal of Paleontology 71(5), 839-847.

Frýda, J., Bandel, K. & Frýdova, B. 2009a. Crystallographic texture of Late Triassic gastropod nacre: evidence of longterm stability of the mechanism controlling its formation. Bulletin of Geosciences 84(4), 747-756.View article

Frýda, J. & Blodgett, R.B. 1998. Two new cirroidean genera (Vetigastropoda, Archaeogastropoda) from the Emsian (late Early Devonian) of Alaska with notes on the early phylogeny of Cirroidea. Journal of Paleontology 72(2), 265-273.

Frýda, J. & Blodgett, R.B. 2004. New Emsian (late Early Devonian) gastropods from Limestone Mountain, Medfra B-4 quadrangle, west-central Alaska (Farewell terrane), and their paleobiogeographic affinities and evolutionary significance. Journal of Paleontology 78(1), 111-132.View article

Frýda, J. & Farrell, J.R. 2005. Systematic position of two Early Devonian gastropods with sinistrally heterostrophic shells from the Garra Limestone, Larras Lee, New South Wales. Alcheringa 29, 229-240.View article

Frýda, J., Nützel, A. & Wagner, P.J. 2008. Paleozoic gastropods, 237-268. In Ponder, W. & Lindberg, D.L. (eds) Phylogeny and Evolution of the Mollusca. 466 pp. University of California Press, Berkeley & Los Angeles, California.

Frýda, J., Racheboeuf, P.R., Frýdová, B., Ferrová, L., Mergl, M. & Berkyová, S. 2009b. Platyceratid gastropods - stem group of patellogastropods, neritimorphs or something else? Bulletin of Geosciences 84(1), 107-120.View article

Frýda, J. & Rohr, D.M. 2006. Shell heterostrophy in Early Ordovician Macluritella Kirk, 1927, and its implications for phylogeny and classification of Macluritoidea (Gastropoda). Journal of Paleontology 80(2), 264-271.View article

Fuchigami, T. & Sasaki, T. 2005. The shell structure of the Recent Patellogastropoda (Mollusca: Gastropoda). Palaeontological Research 9, 143-168.View article

Gauldie, R.W. 1999. Ultrastructure of lamellae, mineral and matrix components of fish otolith twinned aragonite crystals: implications for estimating age in fish. Tissue Cell 31(2), 138-153.View article

Gauldie, R.W. & Nelson, D.G.A. 1988. Aragonite twinning and neuroprotein secretion are the cause of daily growth rings in fish otoliths. Comparative Biochemistry and Physiology Part A, Physiology 90(3), 501-509.View article

Geiger, D.L., Nützel, A. & Sasaki, T. 2008. Vetigastropoda, 297-330. In Ponder, W. & Lindberg, D.L. (eds) Phylogeny and Evolution of the Mollusca. 488 pp. University of California Press, Berkeley & Los Angeles, California.

Giribet, G. 2008. Bivalvia, 105-141. In Ponder, W.F. & Lindberg, D.R. (eds) Phylogeny and Evolution of the Mollusca. University of California Press, Berkeley.

Hedegaard, C., Lindberg, D.R. & Bandel, K. 1997. Shell microstructure of a Triassic patellogastropod limpet. Lethaia 30, 331-335.View article

Hedegaard, C. & Wenk, H.-R. 1998. Microstructure and texture patterns of mollusc shells. Journal of Molluscan Studies 64, 133-136.View article

Jackson, D., McDougall, C., Woodcroft, B., Moase, P., Rose, R., Kube, M., Reinhardt, R., Rokhsar, D., Montagnani, C., Joubert, C., Piquemal, D. & Degnan, B.M. 2010. Parallel Evolution of Nacre Building Gene Sets in Molluscs. Molecular biology and evolution 27(3), 591-608.View article

Kiel, S. & Frýda, J. 2004. Shell structure of Late Cretaceous Sensuitrochus ferreri (Cirridae, Gastropoda). Journal of Paleontology 78(4), 795-797.View article

Klug, C., Kroger, B., Kiessling, W.,Mullins, G.L., Servais, T., Frýda, J., Korn, D. & Turner, S. 2010. The Devonian Nekton Revolution. Lethaia 43, 465-477.View article

Kouchinsky, A. 2000. Shell microstructures in Early Cambrian molluscs. Acta Palaeontologica Polonica 45(2), 119-150.

Kříž, J. 2007. Origin, evolution and classification of the new superorder Nepiomorphia (Mollusca, Bivalvia, Lower Paleozoic). Palaeontology 50(6), 1341-1365.View article

Kříž, J. 2008a. A new bivalve community from the lower Ludlow of the Prague Basin (Perunica, Bohemia). Bulletin of Geosciences 83(3), 237-280.View article

Kříž, J. 2008b. Algerina gen. nov. (Bivalvia, Nepiomorphia) from the Silurian of the North Gondwana margin (Algeria), peri-Gondwanan Europe (France, Italy), Perunica (Prague Basin, Bohemia) and the Siberian Plate (Tajmyr Basin, Russia). Bulletin of Geosciences 83(1), 79-84.View article

Kříž, J. & STEINOVÁ, M. 2009. Uppermost Ordovician bivalves from the Prague Basin (Hirnantian, Perunica, Bohemia). Bulletin of Geosciences 84(3), 409-436.View article

Lamarck, J.B.P.A. de Monet de 1799. Prodrome d’une nouvelle classification des coquilles, comprenant une redaction appropriée des caracteres generiques, et l’etablissement d’un grand nombre de genres nouveaux. Mémoires de la Société d’Histoire Naturelle de Paris 1 [an VII], 63-91.

Lamarck, J.P.B.A. de Monet de 1819. Histoire naturelle des animaux sans vertebres, présentant les caracteres généraux et particuliers de ces animaux, leur distribution, leurs classes, leurs familles, leurs genres, et la citation des principales especes qui s’y rapportent; précédée d’une introduction offrant la détermination des caracteres essentiels de l’animal, sa distinction du végétal et des autres corps naturels, enfin, l’exposition des principes fondamentaux de la zoologie. Tome sixieme. 343 pp. Paris.

Leach, W.E. 1814. The zoological miscellany; being descriptions of new, or interesting animals. Illustrated with coloured figures, drawn from nature, by R.P. Nodder. Vol. I. 144 pp. Nodder, London.

Lightfoot, J. 1786. Catalogue of the Portland Museum. 194 pp. London.

Linnaeus, C. 1758. Systema naturae per regna tria naturae: secundum classes, ordines, genera, species, cum characteribus, differentiis, synonymis, locis. Holmiae: Impensis Direct. 824 pp. Laurentii Salvii.

MacClintock, C. 1968. Shell structure of patelloid and bellerophontoid gastropods (Mollusca). Peabody Museum of Natural History Bulletin 22, 1-140.

Mann, S. 1983. Mineralization in biological systems. Structure and Bonding 54, 125-174.View article

Marie, B., Luquet, G., Bedouet, L., Milet, C., Guichard, N., Medakovic, D. & Marin, F. 2008. Nacre Calcification in the Freshwater Mussel Unio pictorum: Carbonic Anhydrase Activity and Purification of a 95 kDa Calcium-Binding Glycoprotein. ChemBioChem 9(15), 2515-2523.View article

Marie, B., Marin, F., Marie, A., Bedouet, L., Dubost, L., Alcaraz, G., Milet, C. & Luquet, G. 2009. Evolution of nacre: Biochemistry and proteomics of the shell organic matrix of the cephalopod Nautilus macromphalus. ChemBioChem 10(9), 1495-1506.View article

Marin, F. & Luquet, G. 2004. Molluscan shell proteins. Comptes Rendus Palevol 3, 469-492.View article

Marin, F., Luquet, G., Marie, B. & Medakovic, D. 2008. Molluscan Shell Proteins: Primary Structure, Origin, and Evolution. Current Topics in Developmental Biology 80, 210-277.

Mukai, H., Saruwatari, K., Nagasawa, H. & Kogure, T. 2010. Aragonite twinning in gastropod nacre. Journal of Crystal Growth 312(20), 3014-3019.View article

Mutvei, H. 1980. The nacreous layer in molluscan shells, 49-56. In Omori, M. & Watabe, N. (eds) The mechanisms of biomineralisation in animals and plants. Tokai University Press.

Newell, N.D. 1965. Classification of the Bivalvia. American Museum Novitates 2206, 1-25.

Nishiguchi, M. & Mapes, R.K. 2008. Cephalopoda, 163-199. In Ponder, W.F. & Lindberg, D.R. (eds) Phylogeny and Evolution of the Mollusca. University of California Press, Berkeley.

Nützel, A. & Frýda, J. 2003. Paleozoic plankton revolution: evidence from early gastropod ontogeny. Geology 31, 829-831.View article

Nützel, A., Lehnert, O. & Frýda, J. 2006. Origin of planktotrophy - evidence from early molluscs. Evolution and Development 8(4), 325-330.View article

Ouhenia, S., Chateigner, D., Belkhir, M. & Guilmeau, E. 2008a. Microstructure and crystallographic texture of Charonia lampas lampas shell. Journal of Structural Biology 163, 175-184.View article

Ouhenia, S., Chateigner, D., Belkhir, M., Guilmeau, E. & Krauss, C. 2008b. Synthesis of calcium carbonate polymorphs in the presence of polyacrylic acid. Journal of Crystal Growth 310, 2832-2841.View article

Parkhaev, P.Y. 2008. The Early Cambrian Radiation of Mollusca, 33-69. In Ponder, W.F. & Lindberg, D.R. (eds) Phylogeny and Evolution of the Mollusca. University of California Press, Berkeley.

Pokroy, B., Kapon, M., Marin, F., Adir, N. & Zolotoyabko, E. 2007. Protein-induced, previously unidentified twin form of calcite. Proceedings of the National Academy of Sciences of the United States of America 104(18), 7337-7341.View article

Ponder, W.F. & Lindberg, D.R. 1997. Towards a phylogeny of gastropod molluscs: an analysis using morphological characters. Zoological Journal of the Linnean Society 119, 83-265.View article

Rafinesque, C.S. 1820. Annals of nature or annual synopsis of new genera and species of animals, plants, &c. discovered in North America. First annual number for 1820. 16 pp. Lexington.

Roding, P.F. 1798. Museum Boltenianum sive catalogus cimeliorum e tribus regnis natura qua olim collegerat Joa. Fried Bolten, M. D. p. d. per XL. annos proto physicus Hamburgensis. Pars secunda continens conchylia sive testacea univalvia, bivalvia & multivalvia. 199 pp. Hamburgi.

Rohr, D.M., Blodgett, R.B. & Furnish, W.M. 1992. Maclurina manitobensis (Whiteaves) (Ordovician Gastropoda); the largest known Paleozoic gastropod. Journal of Paleontology 66, 880-884.

Rohr, D.M. & Gubanov, A.P. 1997. Macluritid opercula (Gastropoda) from the Middle Ordovician of Siberia and Alaska. Journal of Paleontology 71, 394-400.

Rousseau, M., Meibom, A., Geze, M., Bourrat, X., Angellier, M. & Lopez, E. 2009. Dynamics of sheet nacre formation in bivalves. Journal of Structural Biology 165, 190-195.View article

Runnegar, B. 1985. Shell microstructures of Cambrian molluscs replicated by phosphate. Alcheringa 9(3-4), 245-257.View article

Sasaki, T. 1998. Comparative anatomy and phylogeny of the Recent Archaeogastropoda. The University Museum, The University of Tokyo Bulletin 38, 1-223.

Saruwatari, K., Matsui, T., Mukai, H., Nagasawa, H. & Kogure, T. 2009. Nucleation and growth of aragonite crystals at the growth front of nacres in pearl oyster, Pinctada fucata. Biomaterials 30, 3028-3034.View article

Say, T. 1817. Descriptions of seven species of American fresh water and land shells, not noticed in the systems. Journal of the Academy of Natural Sciences of Philadelphia 1(1-2), 13-17.

Say, T. 1829. Descriptions of some new terrestrial and fluviatile shells of North America (cont.). The Disseminator of Useful Knowledge; containing hints to the youth of the U. States, from the School of Industry 2(17), 259-261.

Suzuki, M., Saruwatari, K., Kogure, T., Yamamoto, Y., Nishimura, T., Kato, T. & Nagasawa, H. 2009. An Acidic Matrix Protein, Pif, Is a Key Macromolecule for Nacre Formation. Science 325 (5946), 1388-1390.View article

Swainson, W. 1840. A treatise on malacology, or shells and shell-fish. 419 pp. London.

Ubukata, T. 1994. Architectural constraints on the morphogenesis of prismatic structure in Bivalvia. Palaeontology 37, 241-261.

Wada, K. 1972. Nucleation and growth of aragonite crystals in the nacre of some bivalve molluscs. Biomineralization 1972(4), 141-159.

Wagner, P.J. 1999. Phylogenetics of the earliest anisostrophically coiled gastropods. Smithsonian Contributions to Paleobiology 88, 1-132.

Wise, S.W. 1970. Microarchitecture and mode of formation of nacre (mother of pearl) in pelecypods, gastropods and cephalopods. Eclogae Geologicae Helvetiae 63, 775-797.

Woodcock, N.H. 1977. Specification of fabric shape using an eigenvalue method. Geological Society of America Bulletin 88, 1231-1236.View article

Woodcock, N.H. & Naylor, M.A. 1983. Randomness testing in three-dimensional orientation data. Journal of Structural Geology 5, 539-548.View article

Weiner, S. & Traub, W. 1980. X-ray diffraction study of the insoluble organic matrix of mollusk shells. FEBS Letters 111, 311-316.View article

Weiner, S. & Traub,W. 1984. Macromolecules in mollusc shells and their functions in biomineralization. Philosophical Transactions of the Royal Society of London, B 3042, 425-435.View article

Wise, S.W. 1970. Microarchitecture and mode of formation of nacre (mother of pearl) in pelecypods, gastropods and cephalopods. Eclogae Geologicae Helvetiae 63, 775-797.