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Biomineral structure and crystallographic arrangement of cerioid and phaceloid growth in corals belonging to the Syringoporicae (Tabulata, Devonian–Carboniferous): a genetic reflection

Published online by Cambridge University Press:  01 February 2016

ISMAEL CORONADO*
Affiliation:
Departamento de Paleontología, Universidad Complutense de Madrid. C/ José Antonio Nováis 12, Ciudad Universitaria. E-28040 Madrid. Spain
SERGIO RODRÍGUEZ
Affiliation:
Departamento de Paleontología, Universidad Complutense de Madrid. C/ José Antonio Nováis 12, Ciudad Universitaria. E-28040 Madrid. Spain Instituto de Geociencias (IGEO. CSIC-UCM). C/ José Antonio Nováis 2, Ciudad Universitaria. E-28040 Madrid. Spain
*
Author for correspondence: [email protected]

Abstract

An extensive study of the microstructure, nanostructrure and crystallographic properties of six taxa belonging to four different genera of Devonian and Carboniferous Syringoporicae showing dense phaceloid (Pleurosiphonella), pseudocerioid (Neomultithecopora) and cerioid growth patterns (Roemeria and Roemeripora) has been done in order to disclose the similarities and differences in the growth processes at the biomineral scale and understand the growth processes that provide organisms with an evolutionary advantage to colonize different habitats. All the skeletons have similarities regarding the biocrystallization process, showing that the Syringoporicae skeletons are a product of matrix-mediated biocrystallization. Micro- and nanotextural features are common in all of the skeletons studied, showing that they were composed of hierarchical structures. All studied taxa possess a complex nanostructure composed of co-oriented rounded nanocrystals with different sizes and morphologies, depending on the taxon. The identified microstructures include granules, lamellae, fibres and hyaline elements. The crystallographic techniques demonstrate that all of them except the hyaline elements are biogenic in origin. Granules could be aborted fibres during the growth of two corallites in contact. On the other hand, the study of the biomineral properties suggests that the skeleton structure is a reflection of the genetic code. The median lamina was formed by the joint crystallization of both polyps at the same time. The variation in the internal structural organization (phaceloid, pseudocerioid or cerioid) was conditioned by the environment (stressful situations or feeding strategies); on the contrary, the final structure is controlled by genetics and their crystallographic properties are characteristic for each internal structural organization.

Type
Original Articles
Copyright
Copyright © Cambridge University Press 2016 

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References

Balthasar, U., Cusack, M., Faryma, L., Chung, P., Holmer, L. E., Jin, J., Percival, I. G. & Popov, L. E. 2011. Relic aragonite from Ordovician–Silurian brachiopods: implications for the evolution of calcification. Geology 39, 967–70.CrossRefGoogle Scholar
Barbin, V., Ramseyer, K. & Elfman, M. 2008. Biological record of added manganese in seawater: a new efficient tool to mark in vivo growth lines in the oyster species Crassostrea gigas . International Journal of Earth Sciences 97, 193–99.CrossRefGoogle Scholar
Baronnet, A., Cuif, J. P., Dauphin, Y., Farre, B. & Nouet, J. 2008. Crystallization of biogenic Ca-carbonate within organo-mineral micro-domains. Structure of the calcite prisms of the Pelecypod Pinctada margaritifera (Mollusca) at the submicron to nanometre ranges. Mineralogical Magazine 72, 617–26.CrossRefGoogle Scholar
Barret, S. 1997. Image analysis and the internet. Scientific Data Management 1, 1825.Google Scholar
Berman, A. 2010. Biomineralization of calcium carbonate. The interplay with biosubstrates. In Biomineralization: From Nature to Application. Metal Ions in Life Sciences, Vol. 4 (eds Sigel, A., Sigel, H. & Sigel, R. K. O.), pp. 167205. Chichester: John Wiley & Sons, Ltd.Google Scholar
Brood, K. 1978. Skeletal structures of Silurian auloporid corals. Geologiska Föreningen i Stockholm Förhandlingar 100, 5363.Google Scholar
Checa, A. G., Mutvei, H., Osuna-Mascaró, A. J., Bonarski, J. T., Faryna, M., Berent, K., Pina, C. M., Rousseau, M. & Macías-Sánchez, E. 2013. Crystallographic control on the substructure of nacre tablets. Journal of Structural Biology 183, 368–76.Google Scholar
Coronado, I., Pérez-Huerta, A. & Rodríguez, S. 2013. Primary biogenic skeletal structures in Multithecopora (Tabulata, Pennsylvanian). Palaeogeography, Palaeoclimatology, Palaeoecology 386, 286–99.Google Scholar
Coronado, I., Pérez-Huerta, A. & Rodríguez, S. 2015 a. Computer-integrated polarisation (CIP) in the analysis of fossils: a case of study in a Palaeozoic coral (Sinopora, Syringoporicae, Carboniferous). Historical Biology 27, 1098–112.Google Scholar
Coronado, I., Pérez-Huerta, A. & Rodríguez, S. 2015 b. Crystallographic orientations of structural elements in skeletons of Syringoporicae (tabulate corals, Carboniferous): implications for biomineralization processes in Palaeozoic corals. Palaeontology 58, 111–32.CrossRefGoogle Scholar
Coronado, I. & Rodríguez, S. 2014. Carboniferous auloporids from the Iberian Peninsula: palaeocology, diversity, and spatio-temporal distribution. Journal of Iberian Geology 40, 6185.CrossRefGoogle Scholar
Cuif, J. P., Dauphin, Y., Farre, B., Nehrke, G., Nouet, J. & Salomé, M. 2008. Distribution of sulphated polysaccharides within calcareous biominerals suggests a widely shared two-step crystallization process for the microstructural growth units. Mineralogical Magazine 72, 233–7.Google Scholar
Cuif, J. P., Dauphin, Y. & Gautret, P. 1999. Compositional diversity of soluble mineralizing matrices in some recent coral skeletons compared to fine-scale growth structures of fibres: discussion of consequences for biomineralization and diagenesis. International Journal of Earth Sciences 88, 582–92.CrossRefGoogle Scholar
Cuif, J.-P., Dauphin, Y., Nehrke, G., Nouet, J. & Perez-Huerta, A. 2012. Layered growth and crystallization in calcareous biominerals: impact of structural and chemical evidence on two major concepts in invertebrate biomineralization studies. Minerals 2, 1139.Google Scholar
Cuif, J.-P., Dauphin, Y. & Sorauf, J. E. 2011. Biominerals and Fossils Through Time. Cambridge, New York: Cambridge University Press. 504 pp.Google Scholar
Cusack, M., Dauphin, Y., Chung, P., Pérez-Huerta, A. & Cuif, J. P. 2008. Multiscale structure of calcite fibres of the shell of the brachiopod Terebratulina retusa . Journal of Structural Biology 164, 96100.Google Scholar
Dauphin, Y. 2002. Fossil organic matrices of the Callovian aragonitic ammonites from Lukow (Poland): location and composition. International Journal of Earth Sciences 91, 1071–80.CrossRefGoogle Scholar
de Fromentel, E. 1861. Introduction à l’Étude des Éponges Fossiles. Hardel: Caen, Typ. de A. Google Scholar
Falini, G., Manara, S., Fermani, S., Roveri, N., Goisis, M., Manganelli, G. & Cassar, L. 2007. Polymeric admixtures effects on calcium carbonate crystallization: relevance to cement industries and biomineralization. CrystEngComm 9, 1162–70.Google Scholar
Frýda, J., Klicnarova, K., Frydova, B. & Mergl, M. 2010. Variability in the crystallographic texture of bivalve nacre. Bulletin of Geosciences 85, 645–62.Google Scholar
Gibson, L. J. & Ashby, M. F. 1997. Cellular Solids: Structure and Properties. Cambridge: Cambridge University Press. 532 pp.Google Scholar
Goffredo, S., Vergni, P., Reggi, M., Caroselli, E., Sparla, F., Levy, O., Dubinsky, Z. & Falini, G. 2011. The skeletal organic matrix from Mediterranean coral Balanophyllia europaea influences calcium carbonate precipitation. PLoS ONE 6 (7), e22338. doi: 10.1371/journal.pone.0022338.Google Scholar
Goldfuss, G. A. 1829. Petrefacta Germaniae, I. Düsseldorf: Arnz & Co.Google Scholar
Gorzelak, P., Stolarski, J., Mazur, M. & Meibom, A. 2013. Micro- to nanostructure and geochemistry of extant crinoidal echinoderm skeletons. Geobiology 11, 2943.CrossRefGoogle ScholarPubMed
Hammer, O. 1998. Regulation of astogeny in halysitid tabulates. Acta Palaeontologica Polonica 43, 635–51.Google Scholar
Heilbronner, R. 2000. Automatic grain boundary detection and grain size analysis using polarization micrographs or orientation images. Journal of Structural Geology 22, 969–81.Google Scholar
Heilbronner, R. & Barret, S. 2014. Image Analysis in Earth Sciences – Microstructures and Textures of Earth Materials. London: Springer. 520 pp.Google Scholar
Heilbronner, R. P. & Pauli, C. 1993. Integrated spatial and orientation analysis of quartz c-axes by computer-aided microscopy. Journal of Structural Geology 15, 369–82.Google Scholar
Hill, D. 1981. Rugosa and Tabulata. In Treatise on Invertebrate Paleontology, Part F [Coelenterata], Supplement 1 (ed. Teichert C, C.). Lawrence, Kansas: University of Kansas Press & Boulder, Colorado: Geological Society of America. 762 pp.Google Scholar
Horcas, I., Fernández, R., Gómez-Rodríguez, J. M., Colchero, J., Gómez-Herrero, J. & Baro, A. 2007. WSXM: a software for scanning probe microscopy and a tool for nanotechnology. Review of Scientific Instruments 78, 8.Google Scholar
Lafuste, J. 1970. Lames ultra-minces a faces polies. Procede et applicationa la microstructure des Madreporaires fossiles. Comptes Rendus Hebdomadaires des Seances de l’Academie des Sciences Paris 270, 679–81.Google Scholar
Lafuste, J. 1978. Modalites de passage des lamelles aux fibres dans la muraillede tabules (Micheliniidae) du Devonien et du Permien. Geobios 11, 405–8.Google Scholar
Lafuste, J. 1981. Structure et microstructure de Dendropora Michelin 1846 (Tabulata, Devonien). Bulletin de la Societe geologique de France 23, 271–7.Google Scholar
Lafuste, J. 1983. Passage des microlamelles aux fibres dans le squelette d’un Tabulé “michelinimorphe” du Viséen du Sahara algérien. Geobios 16, 755–61.CrossRefGoogle Scholar
Lafuste, J., Fernández-Martínez, E. & Tourneur, F. 1992. Parastriatopora (Tabulata) de las Calizas del Lorito (Devónico Inferior, provincia de Córdoba). Revista Española de Paleontología 7, 312.Google Scholar
Lafuste, J. & Plusquellec, Y. 1985. Attribution de ‘Michelinia’ compressa Michelin, 1847 au genre Yavorskia Fomitchev (Tabule, Tournaisien). Geobios 18, 381–7.Google Scholar
Lafuste, J. & Plusquellec, Y. 1986. Les caulicules, éléments nouveaux de l’axe des trabécules du Tabulé dévonien Ligulodictyum Plusquellec 1973. Comptes rendus de l’Académie des sciences. Série 2, Mécanique, Physique, Chimie, Sciences de l’univers, Sciences de la Terre 303, 761–4.Google Scholar
Lafuste, J. & Tourneur, F. 1988 a. Précisions sur la structure et la microstructure du genre Roemeria Milne-Edwards & Haime 1851 (Tabulata, Dévonien moyen d’Allemagne et de Belgique). Paläontologische Zeitschrift 62, 1148.Google Scholar
Lafuste, J. & Tourneur, F. 1988 b. Dendropora Michelin, 1846, et le nouveau genre dendroporimorphe Senceliaepora du Givétien et du Frasnien de la Belgique et du Boulonnais (France). Bulletin du Museum National d’Histoire Naturelle. Section C, Sciences de la terre, paléontologie, géologie, minéralogie 10, 307–41.Google Scholar
Lafuste, J. & Tourneur, F. 1990. Structure et microstructure du genre Kiaerites Stasińska, 1967 (Tabulata, Silurien de Norvège). Geobios 23, 655–69.CrossRefGoogle Scholar
Lafuste, J. & Tourneur, F. 1991. Biocristaux et éléments foncés de la muraille chez Thamnopora Steininger, 1831 (Tabulata, Dévonien). Annales de Paléontologie 77, 320.Google Scholar
Lowenstam, H. & Weiner, S. 1989. On Biomineralization. New York: Oxford University Press. 336 pp.Google Scholar
Mann, S. 2001. Biomineralization: Principles and Concepts in Bioinorganic Materials Chemistry. Oxford: Oxford University Press. 198 pp.CrossRefGoogle Scholar
Marin, F., Le Roy, N., Marie, B., Ramos-Silva, P., Bundeleva, I., Guichard, N. & Immel, F. 2014. Metazoan calcium carbonate biomineralizations: macroevolutionary trends – challenges for the coming decade. Bulletin de la Societe geologique de France 185, 217–32.Google Scholar
Mistiaen, B. 1988. Tabulés Auloporida du Givetien et du Frasnien de Ferques (Boulonnais — France). In Le Dévonien de Ferques. Bas-Boulonnais (N. France) (ed. Brice, D.), pp. 197230. Brest: Universite de Bretagne occidentale.Google Scholar
Moreno-Azanza, M., Mariani, E., Bauluz, B. & Canudo, J. I. 2013. Growth mechanisms in dinosaur eggshells: an insight from electron backscatter diffraction. Journal of Vertebrate Paleontology 33, 121–30.Google Scholar
Nicholson, H. A. 1879. On the Structure and Affinities of the “Tabulate Corals” of the Palaeozoic Period: With Critical Descriptions of Illustrative Species. Edinburgh: William Blackwood and Sons.Google Scholar
Nindiyasari, F., Fernández-Díaz, L., Griesshaber, E., Astilleros, J. M., Sánchez-Pastor, N. & Schmahl, W. W. 2014. Influence of gelatin hydrogel porosity on the crystallization of CaCO3 . Crystal Growth & Design 14, 1531–42.Google Scholar
Nowinski, A. 1991. Late Carboniferous to Early Permian Tabulata from Spitsbergen. Palaeontologia Polonica 51, 374.Google Scholar
Pérez-Huerta, A., Cusack, M. & England, J. 2007. Crystallography and diagenesis in fossil craniid brachiopods. Palaeontology 50, 757–63.Google Scholar
Pérez-Huerta, A., Cusack, M. & Méndez, C. A. 2012. Preliminary assessment of the use of electron backscatter diffraction (EBSD) in conodonts. Lethaia 45, 253–8.Google Scholar
Plusquellec, Y. 1976. Les polypiers. Tabulata. Les Schistes et Calcaires de l´Armorique (Dévonien inférieur, Massif Armorican, France). Sédimentologie, paléontologie, stratigraphie. In Mémoires de la Societé géologique et mineraligique de Bretagne 19 (ed. Lardeux, H.), pp. 183215.Google Scholar
Plusquellec, Y. & Tchudinova, I. I. 1977. The microstrucuture of Parastriatopora Sokolov, 1949 (Siluro-Devonian Tabulata). Annales de la Société géologique du nord 97, 127–30.Google Scholar
Počta, P. 1902. Anthozoaires et Alcyonaire. In Système Silurien du Centre de la Bohême. Première Partie: Recherches Paléontologiques VIII (ed. Barrande, J.), p. 347. Prague: Musée Boliême.Google Scholar
Poty, E. 2010. Morphological limits to diversification of the rugose and tabulate corals. Palaeoworld 19, 389400.Google Scholar
Rodríguez, S. 1989. Lamellar microstructure in Palaeozoic corals: origin and use in taxonomy. Memoirs of the Association of Australasian Palaentologists 8, 157–68.Google Scholar
Rodríguez, S. & Ramírez, C. 1987. Los siringopóridos de la Seccion de la Playa de la Huelga (Carbonífero, Asturias, NW de España). Boletín de la Real Sociedad Española de Historia Natural (Geologia) 83 (1–4), 5782.Google Scholar
Scrutton, C. T. 1998. The Palaeozoic corals, II: structure, variation and palaeoecology. Proceedings of the Yorkshire Geological Society 52, 157.Google Scholar
Semenoff-Tian-Chansky, P. 1984. Microstructure of Siphonodendron (Lithostrotionidae). Palaeontographica Americana 54, 489500.Google Scholar
Sorauf, J. E. 1984. Upper Permian corals from Timor and diagenesis. Palaeontographica Americana 54, 294302.Google Scholar
Stolarski, J. 2000. Origin and phylogeny of Guyniidae (Scleractinia) in the light of microstructural data. Lethaia 33, 1338.Google Scholar
Stolarski, J., Meibom, A., Przenioslo, R. & Mazur, M. 2007. A Cretaceous Scleractinian coral with a calcitic skeleton. Science 318, 92–4.Google Scholar
Taylor, P. D., Kudryavtsev, A. B. & Schopf, J. W. 2008. Calcite and aragonite distributions in the skeletons of bimineralic bryozoans as revealed by Raman spectroscopy. Invertebrate Biology 127 (1), 8797.Google Scholar
Tchudinova, I. I. 1970. Novyye tabulyaty iz paelzoya Zakav-kaz’ya [New tabulate corals from the Paleozoic of Transcaucasia]. In Novyye Vidy Paleozoiskikh Mshanok i Korallov [New Species of Paleozoic Bryozoa and Corals] (eds Astrova, G. G. & Tchudinova, I. I.), pp. 97111. Moscow: Akademia Nauka SSSR.Google Scholar
Tchudinova, I. I. 1980. Morphogenesis of Syringoporida. Acta Palaeontologica Polonica 25, 505–11.Google Scholar
Tchudinova, I. I. 1986. Composition, system and phylogeny of fossil corals. Order Syringoporida. Trudy Paleontologicheskogo Instituta Akademia Nauka SSSR 216, 377.Google Scholar
Tourneur, F. & Lafuste, J. 1991. Précisions sur la structure et la microstructure de Roemeria bohemica Počta 1902, espèce-type du genre Roemeripora Kraicz 1934 (Tabulata, Dévonien inférieur de Bohême). Paläontologische Zeitschrift 65, 77103.Google Scholar
Trimby, P. W. & Prior, D. J. 1999. Microstructural imaging techniques: a comparison between light and scanning electron microscopy. Tectonophysics 303, 7181.Google Scholar
Wang, H. C. 1950. A revision of the zoantharia rugosa in the light of their minute skeletal structures. Philosophical Transactions of the Royal Society of London B Biological Sciences 234, 175246.Google ScholarPubMed
Young, G. A. & Scrutton, C. T. 1991. Growth form in Silurian heliolitid corals: the influence of genetics and environment. Paleobiology 17, 369–87.Google Scholar
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