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Variability in the Crystallographic Texture of Bivalve Nacre Variability in the crystallographic texture of bivalve nacre JIØÍ FRÝDA, MAGDALENA KLICNAROVÁ, BARBORA FRÝDOVÁ & MICHAL MERGL 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 plate- lets. The texture strength of a-axes (direction parallel to growth lines) is always weaker than that of b- and c-axes. Ob- served 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. • Key words: Bivalvia, nacre, crystallographic texture, phylogeny. FRÝDA, J., KLICNAROVÁ, K., FRÝDOVÁ,B.&MERGL, M. 2010. Variability in the crystallographic texture of bivalve nacre. Bulletin of Geosciences 85(4), 645–662 (9 figures). Czech Geological Survey, Prague. ISSN 1214-1119. Manu- script received October 18, 2010; accepted in revised form December 6, 2010; published online December 13, 2010; is- sued December 20, 2010. Jiří Frýda, Czech Geological Survey, P.O.B. 85, 118 21 Prague 1, and Faculty of Environmental Sciences, Czech Uni- versity of Life Sciences Prague, Kamýcká 129, 165 21 Praha 6 – Suchdol, Czech Republic; [email protected] • Magdalena Klicnarová, Faculty of Environmental Sciences, Czech University of Life Sciences Prague, Kamýcká 129, 165 21 Praha 6 – Suchdol, Czech Republic • Barbora Frýdová, VÚRV v.v.i., Research Institute, Drnovská 507, 161 06 Prague – Ruzyně, Czech Republic • Michal Mergl, University of West Bohemia, Faculty of Education, Department of Bi- ology, Klatovská 51, 306 19 Plzeň, Czech Republic; [email protected] The study of biologically controlled mineralization is one make preparation of new nanocomposites possible in the of topics connecting scientists with quite different metho- future. dological approaches, such as material physicists, zoolo- The molecular mechanism determining the shape and gists, molecular biologists, paleontologists and medical orientation of individual calcium carbonate crystals in mol- doctors. The fact that molecular mechanisms in some or- luscan shells is very complex and still not well understood ganisms may control and produce at low temperature per- even though it had been intensively studied during the last fectly organized structures on a nanoscale is a great inspi- three decades. Recent studies showed that molluscan shell ration for material scientists. The formation of molluscan mineralization is a very complex process in which different shells is one of the most studied cases of biologically con- shell proteins play a very important role (e.g., Marin & trolled mineralization. Molluscan shells consist mainly of Luquet 2004; Marie et al. 2008, 2009; Ouhenia et al. calcium carbonate crystals (aragonite and/or calcite, ra- 2008b; see excellent review by Marin et al. 2008). Bio- rely vaterite) with a small amount of other organic subs- chemical studies produced evidence of the active role of tances. The carbonate mono- or polycrystals forming some macromolecules in control of the polymorphism of these shells are organized into many different microstruc- calcium carbonate. It was shown that macromolecules ex- tures and textures (see Carter 1990a, b). It has been shown tracted from the aragonite shell layer induced the growth of several times that the style of nanoscale organization of aragonite in vitro on a substrate of polysaccharide b-chitin inorganic and organic components of the molluscan shells and hydrophobic silk protein (e.g., Falini et al. 1996). Re- considerably changes their physical properties (e.g., Ber- cently a team of Japanese scientists (Suzuki et al. 2009) toldi et al. 2008, Denkena et al. 2010, Ouhenia et al. reported a discovery of two novel proteins, named Pif80 2008a, Chateigner et al. 2010). Understanding of the bio- and Pif97, which seem to be the key players in controlling mineralization processes on a molecular level should the crystal structure of nacre in pearl-forming oysters. DOI 10.3140/bull.geosci.1217 645 Bulletin of Geosciences Vol. 85, 4, 2010 During the last decades, biochemical studies have thus Channel coast near Brighton, England, and from (2) the produced many significant insights into the mechanisms of North Sea, Slemmestad near Oslo, Sweden], Mytilus gal- shell formation on the molecular level. As has been previ- loprovincialis Lamarck, 1819, from the Adriatic Sea near ously shown, that each particular shell microstructure is the town of Rabac, Istria, Croatia, and Mytilus california- very complex nanocomposite which is also the product of a nus (Conrad, 1837), from the coast of the Pacific Ocean very complex molecular mechanism. Because of this a par- near the town of Brookings, SW Oregon, U.S.A. The genus allel development of shell layer with the same micro- Modiolus Lamarck, 1799, is represented by the species structure and texture is highly unlikely. Better understand- Modiolus barbatus (Linnaeus, 1758), from the Adriatic ing of the relationships between particular molecular Sea near the village of Izola, Slovenia, and the genus Bra- processes on the one hand and microstructure and texture chidontes Swainson, 1840, by the species Brachidontes of individual shell layers on the other hand will thus pro- rostratus (Dunker, 1857), from Brouler Beach near Syd- duce a new data source for understanding the long evolu- ney, NSW, Australia. Two species of genera Pinctada Ro- tion of molluscs. Inorganic and organic components of ding, 1798, and Pinna Linnaeus, 1758 from the order Pteri- molluscan shells and their functions may be studied only in ida were studied: Pinctada radiata (Leach, 1814), from the living molluscs. However the extremely rich and diverse Mediterranean Sea, Karpathos island, Greece, and Pinna fossil record of molluscan evolution gives the chance to nobilis (Linnaeus, 1758), from two localities [(1) the coast study only inorganic biomineralization products, i.e., mol- of the Mediterranean Sea near Dénia, 80 km SE of Valen- luscan shells. Individual molluscan shell layers may be cia, Spain, and (2) the Adriatic Sea near the village of Izola, characterized by their shell microstructure, phase composi- Slovenia]. Three freshwater species of unionid genera, Am- tion, and crystallographic texture. The shell micro- blema Rafinesque, 1820, Leptodea Rafinesque, 1820, and structure, characterizing the shape of biocrystals, has been Quadrula Rafinesque, 1820, were selected to characterize the most studied property of molluscan shells. On the other the superorder Heteroconchia Cox, 1960: Amblema plicata hand, there are almost no data on crystallographic textures (Say, 1817), Leptodea fragilis (Rafinesque, 1820), and Qua- of particular shell layers of living as well as fossil molluscs. drula apiculata (Say, 1829), all coming from NW Texas. The crystallographic texture describing the arrangement of Bivalve shells selected for crystallographic texture crystal axes of individual biocrystals thus provides non-re- analysis were gently broken to preserve information on the dundant characteristics of a particular shell layer. biological orientation of each which may be valuable in fu- In this short paper we present the results of crystallo- ture research. Several shell fragments of each species were graphic texture analysis of nacre in eleven bivalve species studied under SEM (Figs 1–3) and special attention was belonging to three different superorders. The main goal of paid to lateral thickness variability of the nacreous layer. this short study was to test how variable are the crystallo- Fragments with the thickest nacreous layer were used for graphic texture characteristics of bivalve nacre (i.e., quan- crystallographic texture analysis and separately embedded titatively evaluate texture pattern of the bivalve nacre and in epoxy resin. The biological orientation of each shell percentage of twinning of nacreous platelets). fragment was marked on the surface of the surrounding ep- oxy resin block. Subsequently, each shell fragment was polished using a progressively finer polishing medium Material and methods (down to 5 μm grit SiC followed by several minutes with 3 μm diamond, 1 μm diamond, 0.25 μm diamond, and 5 The present study is based on crystallographic texture ana- minutes with 0.05 μm colloidal silica). Each shell fragment lysis of nacre in eleven bivalve species belonging to supe- was polished parallel to the inner shell surface and to a rorders Opponobranchia Giribet, 2008, Pteriomorpha Be- level cutting roughly to the middle of the nacreous shell urlen, 1944, and Paleoheterodonta Newell, 1965, all of layer (i.e., area having the same distance from inner surface which develope a nacreous layer in their
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