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Nacre and false nacre (foliated aragonite) in extant monoplacophorans (=Tryblidiida: Mollusca)

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Abstract

Extant monoplacophorans (Tryblidiida, Mollusca) have traditionally been reported as having an internal nacreous layer, thus representing the ancestral molluscan condition. The examination of this layer in three species of Neopilinidae (Rokopella euglypta, Veleropilina zografi, and Micropilina arntzi) reveals that only V. zografi secretes an internal layer of true nacre, which occupies only part of the internal shell surface. The rest of the internal surface of V. zografi and the whole internal surfaces of the other two species examined are covered by a material consisting of lath-like, instead of brick-like, crystals, which are arranged into lamellae. In all cases examined, the crystallographic c-axis in this lamellar material is perpendicular to the surface of laths and the a-axis is parallel to their long dimension. The differences between taxa relate to the frequency of twins, which is much higher in Micropilina. In general, the material is well ordered, particularly towards the margin, where lamellae pile up at a small step size, which is most likely due to processes of crystal competition. Given its morphological resemblance to the foliated calcite of bivalves, we propose the name foliated aragonite for this previously undescribed biomaterial secreted by monoplacophorans. We conclude that the foliated aragonite probably lacks preformed interlamellar membranes and is therefore not a variant of nacre. A review of the existing literature reveals that previous reports of nacre in the group were instead of the aragonitic foliated layer and that our report of nacre in V. zografi is the first undisputed evidence of nacre in monoplacophorans. From the evolutionary viewpoint, the foliated aragonite could easily have been derived from nacre. Assuming that nacre represents the ancestral condition, as in other molluscan classes, it has been replaced by foliated aragonite along the tryblidiidan lineage, although the fossil record does not presently provide evidence as to when this replacement took place.

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References

  • Addadi L, Joester D, Nudelman F, Weiner S (2006) Mollusk shell formation: a source of new concepts for understanding biomineralization processes. Chem Eur J 12:980–987. doi:10.1002/chem.200500980

    Article  CAS  Google Scholar 

  • Bevelander G, Nakahara H (1969) An electron microscope study of the formation of the nacreous layer in the shell of certain bivalve molluscs. Calcif Tissue Res 3:84–92. doi:10.1007/BF02058648

    Article  PubMed  CAS  Google Scholar 

  • Cartwright JHE, Checa AG (2007) The dynamics of nacre self-assembly. J R Soc Interface 4:491–504. doi:10.1098/rsif.2006.0188

    Article  PubMed  CAS  Google Scholar 

  • Chateigner D, Hedegaard C, Wenk H-R (2000) Mollusc shell microstructures and crystallographic textures. J Struct Geol 22:1723–1735

    Article  Google Scholar 

  • Checa AG, Rodríguez-Navarro A (2001) Geometrical and crystallographic constraints determine the self-organization of shell microstructures in Unionidae (Bivalvia: Mollusca). Proc R Soc B 268:771–778. doi:10.1098/rspb.2000.1415

    Article  PubMed  CAS  Google Scholar 

  • Checa AG, Rodríguez-Navarro A (2005) Self-organisation of nacre in the shells of Pterioida. Biomaterials 26:1071–1079 . doi:10.1016/j.biomaterials.2004.04.007

    Article  PubMed  CAS  Google Scholar 

  • Checa AG, Esteban-Delgado FJ, Rodríguez-Navarro AB (2007) Crystallographic structure of the foliated calcite of bivalves. J Struct Biol 157:393–402. doi:10.1016/j.jsb.2006.09.005

    Article  PubMed  CAS  Google Scholar 

  • Cruz R, Weismüller G, Farina M (2003) Microstructure of Monoplacophora (Mollusca) shell examined by low-voltage field emission scanning electron and atomic force microscopy. Scanning 25:12–18. doi:10.1002/sca.4950250104

    PubMed  Google Scholar 

  • Erben K (1972) Über die Bildung und das Wachstum von Perlmutt. Biomineral Res Rep 4:15–46

    Google Scholar 

  • Erben HK, Flajs G, Siehl A (1968) Über die Schalenstruktur von Monoplacophoren. Akad Wiss Lit, Abh Math-Naturwiss Kl 1968:1–24

    Google Scholar 

  • Hedegaard C, Wenk H-R (1998) Microstructure and texture patterns of molluscan shells. J Moll Stud 64:133–136. doi:10.1093/mollus/64.1.133

    Article  Google Scholar 

  • Lemche H, Wingstrand KG (1959) The anatomy of Neopilina galatheae Lemche, 1957. In: Bruun AF, Greve S, Spärck R, Wolff T (eds) Scientific results of the Danish deep-sea expedition round the world 1950–52, Galathea Report, volume 3. Danish Science Press, Copenhagen, pp 9–71

    Google Scholar 

  • Levi-Kalisman Y, Falini G, Addadi L, Weiner S (2001) Structure of the nacreous organic matrix of a bivalve mollusc shell examined in the hydrated state using cryo-TEM. J Struct Biol 135:8–17. doi:10.1006/jsbi.2001.4372

    Article  PubMed  CAS  Google Scholar 

  • Lindberg DR, Ponder WF (1996) An evolutionary tree for the mollusca: branches or roots? In: Taylor JD (ed) Origin and evolutionary radiation of the mollusca. Oxford University Press, Oxford, pp 67–75

    Google Scholar 

  • Manne S, Zaremba CM, Giles R, Huggins L, Walters DA, Belcher A, Morse DE, Stucky GD, Didymus JM, Mann S, Hansma PK (1994) Atomic force microscopy of the nacreous layer in mollusk shells. Proc R Soc B 256:17–23

    Article  Google Scholar 

  • Meenakshi VR, Hare PE, Watabe N, Wilbur KM, Menzies RJ (1970) Ultrastructure, histochemistry, and amino acid composition of the shell of Neopilina. Anton Bruun Rep 2:3–12

    Google Scholar 

  • Mutvei H (1970) Ultrastructure of the mineral and organic components of molluscan nacreous layers. Biomineral Res Rep 2:47–72

    Google Scholar 

  • Mutvei H (1978) Ultrastructural characteristics of the nacre in some gastropods. Zool Scripta 7:287–296

    Article  Google Scholar 

  • Mutvei H (1980) The nacreous layer in molluscan shells. In: Omori M, Watabe N (eds) The mechanisms of biomineralization in animals and plants. Tokai University Press, Tokyo, pp 49–56

    Google Scholar 

  • Mutvei H (1991) Using plasma-etching and proteolytic enzymes in studies of molluscan shell ultrastructure. In: Suga S, Nakahara H (eds) Mechanisms and phylogeny of mineralization in biological systems. Springer, Tokyo, pp 157–160

    Google Scholar 

  • Nakahara H (1979) An electron microscope study of the growing surface of nacre in two gastropod species, Turbo cornutus and Tegula pfeifferi. Venus 38:205–211

    Google Scholar 

  • Nakahara H (1991) Nacre formation in bivalve and gastropod molluscs. In: Suga S, Nakahara H (eds) Mechanisms and phylogeny of mineralization in biological systems. Springer, Tokyo, pp 343–350

    Google Scholar 

  • Peel JS (1991) The Classes Tergomya and Helcionelloida, and early molluscan evolution. Bull Grønlands Geol Undersøgelse 161:11–65

    Google Scholar 

  • Runnegar B (1983) Molluscan phylogeny revisited. Mem Assoc Australasian Palaeontol 1:121–144

    Google Scholar 

  • Runnegar B (1985) Shell microstructures of Cambrian molluscs replicated by phosphate. Alcheringa 9:245–257

    Article  Google Scholar 

  • Schäffer TE, Ionescu-Zanetti C, Proksch R, Fritz M, Walters DA, Almquist N, Zaremba CM, Belcher AM, Smith BL, Stucky GD, Morse DE, Hansma PK (1997) Does abalone nacre form by heteroepitaxial nucleation or by growth through mineral bridges? Chem Mater 9:1731–1740. doi:10.1021/cm960429i

    Article  Google Scholar 

  • Schmidt WJ (1959) Bemerkungen zur Schalenstruktur von Neopilina galatheae. In: Bruun AF, Greve S, Spärck R, Wolff T (eds) Scientific results of the Danish deep-sea expedition round the world 1950–52, Galathea Report, volume 3. Danish Science Press, Copenhagen, pp 73–76

    Google Scholar 

  • Taviani M, Sabelli B, Candini F (1990) A fossil Cenozoic monoplacophoran. Lethaia 23:213–216. doi:10.1111/j.1502-3931.1990.tb01361.x

    Article  Google Scholar 

  • Travis DF, Gonsalves M (1969) Comparative ultrastructure and organization of the prismatic region of two bivalves and its possible relation to the chemical mechanism of boring. Am Zool 9:635–661. doi:10.1093/icb/9.3.635

    Google Scholar 

  • Ubukata T (1994) Architectural constraints on the morphogenesis of prismatic structure in Bivalvia. Palaeontology 37:241–261

    Google Scholar 

  • Urgorri V, García-Álvarez O, Luque A (2005) Laevipilina cachuchensis, a new neopilinid (Mollusca, Tryblidia) from off North Spain. J Moll Stud 71:59–66. doi:10.1093/mollus/eyi008

    Article  Google Scholar 

  • Wada K (1960) Crystal growth of the inner shell surface of Pinctada martensii (Dunker) I. J Electron Microsc Tokyo 9:21–23

    Google Scholar 

  • Wada K (1961) Crystal growth of molluscan shells. Bull Natl Pearl Res Lab Jpn 7:703–828

    Google Scholar 

  • Wada K (1972) Nucleation and growth of aragonite crystals in the nacre of some bivalve molluscs. Biomineral Res Rep 4:141–159

    Google Scholar 

  • Warén A, Gofas S (1996) A new species of Monoplacophora, redescription of the genera Veleropilina and Rokopella, and new information on three species of the class. Zool Scripta 25:215–232

    Article  Google Scholar 

  • Warén A, Hain S (1992) Laevipilina antarctica and Micropilina arntzi, two new monoplacophorans from the Antarctic. The Veliger 35:165–176

    Google Scholar 

  • Watabe N (1965) Studies on shell formation. XI. Crystal-matrix relationships in the inner layers of mollusk shells. J Ultrastruct Res 12:351–370

    Article  PubMed  CAS  Google Scholar 

  • Weiner S, Traub W (1981) Structural aspects of recognition and assembly. In: Balaban M, Sussman JL, Traub W, Yonath A (eds) Biological macromolecules. Balaban ISS, Philadelphia, pp 467–482

    Google Scholar 

  • Wise SW (1970) Microarchitecture and mode of formation of nacre (mother of pearl) in pelecypods, gastropods and cephalopods. Eclogae Geol Helv 63:775–797

    Google Scholar 

Download references

Acknowledgements

Serge Gofas (Departamento de Biología Animal, Universidad de Málaga), Anders Warén, and Karin Sindemark Kronestedt (Swedish Museum of Natural History) contributed in an essential manner by providing specimens. X-ray diffraction data of Fig. S2 are joint unpublished results of A.C. with Alejandro Rodríguez-Navarro (Departamento de Mineralogía y Petrología, Universidad de Granada). TEM sections of Fig. S3 are from the original material of the late Hiroshi Nakahara, kindly ceded by Mitsuo Kakei (School of Dentistry, Meikai University). J.R-R. is grateful to the Spanish Junta de Andalucía for his research grant. The study has been funded by Projects CGL2004-00802 and CGL2007-60549 (Ministerio de Educación y Ciencia) and by Research Group RMN190 (Junta de Andalucía).

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Authors and Affiliations

  1. Departamento de Estratigrafía y Paleontología, Facultad de Ciencias, Universidad de Granada, Avenida Fuentenueva s/n, 18071, Granada, Spain

    Antonio G. Checa

  2. Departamento de Física de la Materia Condensada, Facultad de Física, Universidad de Sevilla, Avenida Reina Mercedes s/n, 41012, Seville, Spain

    Joaquín Ramírez-Rico

  3. Centro de Instrumentación Científica, Universidad de Granada, Paseo del Profesor Juan Ossorio s/n, 18071, Granada, Spain

    Alicia González-Segura

  4. Departamento de Mineralogía y Petrología, Facultad de Ciencias, Universidad de Granada, Avenida Fuentenueva s/n, 18071, Granada, Spain

    Antonio Sánchez-Navas

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  1. Antonio G. Checa
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  3. Alicia González-Segura
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Correspondence to Antonio G. Checa.

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ESM Fig. S1

Nacre in bivalves (a, b), gastropods (c, d), and the cephalod Nautilus (e, f). a View of the growth surface of the bivalve Atrina pectinata; growth fronts are diffuse, i.e., they are composed by many crystals and different growth stages. b Semimature nacre in the bivalve Pinctada margaritifera; it is characterized by polygonal tablets. c Growth surface of the gastropod Perotrochus caledonicus, showing a characteristic tower-like growth. d Mature (fractured) nacre of the gastropod Bolma rugosa. e Growth surface of nacre of a juvenile specimen of Nautilus pompilius, close to the aperture; growth is towered, similar to gastropods. f Growth surface of the same specimen as in e, in a more internal location; growth is more similar to that of bivalves. Arrows indicate the growth direction of the shell (JPG 884 KB)

ESM Fig. S2

Pole figures for the bivalves Pteria hirundo (a), the cephalod Nautilus belauensis (b), and the gastropod B. rugosa (c) obtained by EBSD (a) and X-ray diffraction (b, c). In all three cases, the 001 pole figure implies that the c-axis is approximately perpendicular to the shell surface. The 010 pole figure in a and the 110 pole figure in b indicate that the b-axis is parallel to the growth direction of the shell (arrows), whereas the circular distribution in the 110 pole figure of c implies that crystals have their b-axis disoriented (JPG 348 KB)

ESM Fig. S3

TEM sections of the nacre of the gastropod Monodonta labio (a, b) and of the bivalve Pinctada radiata (c). a, b In gastropods, the interlamellar membranes extend between the boundaries of the plates of adjacent towers which are in a similar growth stage. c In bivalves, the interlamellar membranes on top of a given lamella of crystals extend freely beyond the edge of the biomineralization front, marked by the position of the last formed crystal (lfc); the adoral end of the interlamellar membrane (ime) is also indicated. Arrows indicate the growth direction (JPG 636 KB)

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Checa, A.G., Ramírez-Rico, J., González-Segura, A. et al. Nacre and false nacre (foliated aragonite) in extant monoplacophorans (=Tryblidiida: Mollusca). Naturwissenschaften 96, 111–122 (2009). https://doi.org/10.1007/s00114-008-0461-1

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