Skeletal microstructures of cheilostome bryozoans (phylum Bryozoa, class Gymnolaemata): crystallography and secretion patterns

Abstract

Gymnolaemata bryozoans produce CaCO₃ skeletons of either calcite, aragonite, or both. Despite extensive research, their crystallography and biomineralization patterns remain unclear. We present a detailed study of the microstructures, mineralogy, and crystallography of eight extant cheilostome species using scanning electron microscopy, electron backscatter diffraction, atomic force microscopy, and micro-computed tomography. We distinguished five basic microstructures, three calcitic (tabular, irregularly platy, and granular), and two aragonitic (granular-platy and fibrous). The calcitic microstructures consist of crystal aggregates that transition from tabular or irregularly platy to granular assemblies. Fibrous aragonite consists of fibers arranged into spherulites. In all cases, the crystallographic textures are axial, and stronger in aragonite than in calcite, with the c-axis as the fiber axis. We reconstruct the biomineralization sequence in the different species by considering the distribution and morphology of the growth fronts of crystals and the location of the secretory epithelium. In bimineralic species, calcite formation always predates aragonite formation. In interior compound walls, growth proceeds from the cuticle toward the zooecium interior. We conclude that, with the exception of tabular calcite, biomineralization is remote and occurs within a relatively wide extrapallial space, which is consistent with the inorganic-like appearance of the microstructures. This biomineralization mode is rare among invertebrates.

Keywords

Biomineralization / Bryozoan / Skeleton / Calcite / Aragonite / Electron backscatter diffraction

References

[] Bader B, Schäfer P. Skeletal morphogenesis and growth check lines in the Antarctic bryozoan Melicerita obliqua. J Nat Hist, 2004, 38: 2901-2922

[] Benedix G, Jacob DE, Taylor PD. Bimineralic bryozoan skeletons: a comparison of three modern genera. Facies, 2014, 60: 389-403

[] Boardman RS, Cheetham AH. Skeletal growth, intracolony variation, and evolution in Bryozoa: a review. J Paleontol, 1969, 43: 205-233

[] Bøggild OB. The shell structure of the mollusks. Kongel Danske Vidensk Selsk Skr Naturvidensk Math Afd, 1930, 9: 231-326

[] Checa AG. Remote biomineralization in divaricate ribs of Strigilla and Solecurtus (Tellinoidea: Bivalvia). J Molluscan Stud, 2000, 66: 457-466

[] Checa AG. Physical and biological determinants of the fabrication of molluscan shell microstructures. Front Mar Sci, 2018, 5: 353

[] Checa AG, Salas C, Harper EM, de Bueno-Pérez JD. Early stage biomineralization in the periostracum of the ‘living fossil’ bivalve Neotrigonia. PLoS ONE, 2014, 9, pmcid: 3934977

[] Checa AG, Linares F, Grenier C, Griesshaber E, Rodríguez-Navarro AB, Schmahl WW. The argonaut constructs its shell via physical self-organization and coordinated cell sensorial activity. iScience, 2021, 24: 103288, pmcid: 8571729

[] Cheetham AH, Rucker JB, Carver RE. Wall structure and mineralogy of the cheilostome bryozoan Metrarabdotos. J Paleontol, 1969, 43: 129-135

[] Chinzei K, Seilacher A. Remote biomineralization I: fill skeletons in vesicular oyster shells. N Jb Geol Paläontol Abh, 1993, 190: 185-197

[] Coronado I, Fine M, Bosellini FR, Stolarski J. Impact of ocean acidification on crystallographic vital effect of the coral skeleton. Nat Commun, 2019, 10: 2896, pmcid: 6603003

[] Crippa G, Griesshaber E, Checa AG, Harper EM, Roda MS, Schmahl WW. Orientation patterns of aragonitic crossed-lamellar, fibrous prismatic and myostracal microstructures of modern Glycymeris shells. J Struct Biol, 2020, 212,

[] Currey JD. Mechanical properties of mother of pearl in tension. Proc R Soc Lond B, 1977, 196: 443-463

[] Currey JD, Taylor JD. The mechanical behaviour of some molluscan hard tissues. J Zool, 1974, 173: 395-406

[] Dick MH, Lidgard S, Gordon DP, Mawatari SF. The origin of ascophoran bryozoans was historically contingent but likely. Proc R Soc B, 2009, 276: 3141-3148, pmcid: 2817133

[] Gabitov RI, Sadekov A, Leinweber A. Crystal growth rate effect on Mg/Ca and Sr/Ca partitioning between calcite and fluid: An in situ approach. Chem Geol, 2014, 367: 70-82

[] Grant HE, Ostrovsky AN, Jenkins HL, Vieira LM, Gordon DP, Foster PG, Kotenko ON, Smith AM, Berning B, Porter JS, Souto J, Florence WK, Tilbrook KJ, Waeschenbach A. Multiple evolutionary transitions of reproductive strategies in a phylum of aquatic colonial invertebrates. Proc R Soc B, 2023, 290: 20231458,

[] Grenier C, Griesshaber E, Schmahl WW, Checa AG. Microstructure and crystallographic characteristics of stenolaemate bryozoans (phylum Bryozoa and class Stenolaemata). Cryst Growth Des, 2023, 23: 965-979

[] Grigor’ev DP (1965) Ontogeny of minerals. Israel Program for Scientific Translations, Jerusalem

[] Hageman SJ, Lukasik J, McGowran B, Bone Y. Paleoenvironmental significance of Celleporaria (Bryozoa) from modern and Tertiary cool-water carbonates of southern Australia. Palaios, 2003, 18: 510-527

[] Hincke MT, Nys Y, Gautron J, Mann K, Rodríguez-Navarro AB, McKee MD. The eggshell: structure, composition and mineralization. Front Biosci, 2012, 17: 1266-1280

[] Jablonski D, Lidgard S, Taylor PD. Comparative ecology of bryozoan radiations: origin of novelties in cyclostomes and cheilostomes. Palaios, 1997, 12: 505-523

[] Jacob DE, Ruthensteiner B, Trimby P, Henry H, Martha SO, Leitner J, Otter LM, Scholz J. Architecture of Anoteropora latirostris (Bryozoa, Cheilostomata) and implications for their biomineralization. Sci Rep, 2019, 9: 11439, pmcid: 6685955

[] Kuklinski P, Taylor PD. Mineralogy of Arctic bryozoan skeletons in a global context. Facies, 2009, 55: 489-500

[] Lombardi C, Kuklinski P, Spirandelli E, Bruzzone G, Raiteri G, Bordone A, Mazzoli C, López Correa M, van Geldern R, Plasseraud L. Antarctic bioconstructional bryozoans from Terra Nova Bay (Ross Sea): morphology, skeletal structures and biomineralization. Minerals, 2023, 13: 246

[] Lowenstam HA. Factors affecting the aragonite: calcite ratios in carbonate-secreting marine organisms. J Geol, 1954, 62: 284-322

[] Lowenstam HA. Minerals formed by organisms. Science, 1981, 211: 1126-1131,

[] Lowenstam HA, Weiner S. . On biomineralization, 1989 New York, USA Oxford University Press

[] Mann S (1983) Mineralization in biological systems. In: Inorganic Elements in Biochemistry. Structure and Bonding, vol 54. Springer, Berlin, Heidelberg, pp 125–174.

[] McKinney FK. Competitive interactions between related clades: evolutionary implications of overgrowth interactions between encrusting cyclostome and cheilostome bryozoans. Mar Biol, 1992, 114: 645-652

[] Nielsen C, Pedersen KJ. Cystid structure and protrusion of the polypide in Crisia (Bryozoa, Cyclostomata). Acta Zool, 1979, 60: 65-88

[] Nielsen MR, Sand KK, Rodriguez-Blanco JD, Bovet N, Generosi J, Dalby KN, Stipp SLS. Inhibition of calcite growth: combined effects of Mg²⁺ and SO₄ ^2–. Cryst Growth Des, 2016, 16: 6199-6207

[] O’Dea A, Håkansson E, Taylor PD, Okamura B. Environmental change prior to the K-T boundary inferred from temporal variation in the morphology of cheilostome bryozoans. Palaeogeogr Palaeoclimatol Palaeoecol, 2011, 308: 502-512

[] Orr RJS, Di Martino E, Ramsfjell MH, Gordon DP, Berning B, Chowdhury I, Craig S, Cumming RL, Figuerola B, Florence W, Harmelin J-G, Hirose M, Huang D, Jain SS, Jenkins HL, Kotenko ON, Kuklinski P, Lee HE, Madurell T, Mccann L, et al.. Paleozoic origins of cheilostome bryozoans and their parental care inferred by a new genome-skimmed phylogeny. Sci Adv, 2022, 8: eabm7452, pmcid: 8967238

[] Palmer AR. Relative cost of producing skeletal organic matrix versus calcification: evidence from marine gastropods. Mar Biol, 1983, 75: 287-292

[] Palmer AR. Calcification in marine molluscs: how costly is it?. Proc Natl Acad Sci USA, 1992, 89: 1379-1382, pmcid: 48454

[] Rodríguez-Navarro A, García-Ruiz JM. Model of textural development of layered crystal aggregates. Eur J Mineral, 2000, 12: 609-614

[] Ryland JS. Physiology and ecology of marine bryozoans. Adv Mar Biol, 1977, 14: 285-443

[] Sandberg PA. Scanning electron microscopy of cheilostome bryozoan skeletons; techniques and preliminary observations. Micropaleontology, 1971, 17: 129-151

[] Sandberg PA. Woollacott RM, Zimmer RL. Ultrastructure, mineralogy, and development of bryozoan skeletons. Biology of bryozoans, 1977 New York Academia Press 43-181

[] Schack CR, Gordon DP, Ryan KG. Modularity is the mother of invention: a review of polymorphism in bryozoans. Biol Rev, 2019, 94: 773-809,

[] Schoeppler V, Gránásy L, Reich E, Poulsen N, De Kloe R, Cook P, Rack A, Pusztai T, Zlotnikov I. Biomineralization as a paradigm of directional solidification: a physical model for molluscan shell ultrastructural morphogenesis. Adv Mater, 2018, 30: 1803855

[] Schoeppler V, Lemanis R, Reich E, Pusztai T, Gránásy L, Zlotnikov I. Crystal growth kinetics as an architectural constraint on the evolution of molluscan shells. Proc Natl Acad Sci USA, 2019, 116: 20388-20397, pmcid: 6789867

[] Simonet Roda M, Griesshaber E, Ziegler A, Rupp U, Yin X, Henkel D, Häussermann V, Laudien J, Brand U, Eisenhauer A, Checa AG, Schmahl WW. Calcite fibre formation in modern brachiopod shells. Sci Rep, 2019, 9: 598, pmcid: 6345923

[] Simonet Roda M, Griesshaber E, Angiolini L, Rollion-Bard C, Harper EM, Bitner MA, Milner Garcia S, Ye F, Henkel D, Häussermann V, Eisenhauer A, Gnägi H, Brand U, Logan A, Schmahl WW. The architecture of Recent brachiopod shells: diversity of biocrystal and biopolymer assemblages in rhynchonellide, terebratulide, thecideide and craniide shells. Mar Biol, 2022, 169: 4

[] Smith AM, Girvan E. Understanding a bimineralic bryozoan: skeletal structure and carbonate mineralogy of Odontionella cyclops (Foveolariidae: Cheilostomata: Bryozoa) in New Zealand. Palaeogeogr Palaeoclimatol Palaeoecol, 2010, 289: 113-122

[] Smith AM, Key MM Jr, Gordon DP. Skeletal mineralogy of bryozoans: taxonomic and temporal patterns. Earth Sci Rev, 2006, 78: 287-306

[] Stevens K, Griesshaber E, Schmahl W, Casella LA, Iba Y, Mutterlose J. Belemnite biomineralization, development, and geochemistry: the complex rostrum of Neohibolites minimus. Palaeogeogr Palaeoclimatol Palaeoecol, 2017, 468: 388-402

[] Tavener-Smith R, Williams A. The secretion and structure of the skeleton of living and fossil Bryozoa. Philos Trans R Soc, 1972, 264: 97-160

[] Taylor PD. An early cheilostome bryozoan from the Upper Jurassic of Yemen. N Jb Geol Palaeontol Abh, 1994, 191: 331-344

[] Taylor PD, Allison PA. Bryozoan carbonates through time and space. Geology, 1998, 26: 459-462

[] Taylor PD, Weedon MJ. Skeletal ultrastructure and phylogeny of cyclostome bryozoans. Zool J Linn Soc, 2000, 128: 337-399

[] Taylor PD, Waeschenbach A. Phylogeny and diversification of bryozoans. Palaeontology, 2015, 58: 585-599

[] Taylor PD, Kudryavtsev AB, Schopf JW. Calcite and aragonite distributions in the skeletons of bimineralic bryozoans as revealed by Raman spectroscopy. Invertebr Biol, 2008, 127: 87-97

[] Taylor PD, James NP, Bone Y, Kuklinski P, Kyser TK. Evolving mineralogy of cheilostome bryozoans. Palaios, 2009, 24: 440-452

[] Taylor PD, Lombardi C, Cocito S. Biomineralization in bryozoans: present, past and future. Biol Rev, 2015, 90: 1118-1150,

[] Taylor PD (2020) Bryozoan paleobiology. Wiley Blackwell, Oxford, pp320

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

[] Weedon MJ, Taylor PD (2000) Skeletal ultrastructure of primitive cheilostome bryozoans. In: Proceedings of the 11th International Bryozoology Association Conference. Smithsonian Tropical Research Institute, Balboa, Panama, pp 400–411

[] Williams A. Spiral growth of the laminar shell of the brachiopod Crania. Calcif Tissue Res, 1970, 6: 11-19,

[] WoRMS Editorial Board (2024) World Register of Marine Species. Available from https://www.marinespecies.org at VLIZ Accessed: 2024–01–22 doi:https://doi.org/10.14284/170

[] Yin X, Griesshaber E, Checa A, Nindiyasari-Behal F, Sánchez-Almazo I, Ziegler A, Schmahl WW. Calcite crystal orientation patterns in the bilayers of laminated shells of benthic rotaliid foraminifera. J Struct Biol, 2021, 213,

Funding

Universidad de Granada