Element contents
Series: Elements of Paleontology
Functional Micromorphology of the Echinoderm Skeleton
Published online by Cambridge University Press: 02 February 2021
Summary
Echinoderms elaborate a calcite skeleton composed of numerous plates with a distinct microstructure (stereom) that can be modelled into different shapes thanks to the use of a transient amorphous calcium carbonate (ACC) precursor phase and the incorporation of an intraorganic matrix during biomineralization. A variety of different types of stereom microarchitecture have been distinguished, each of them optimized for a specific function. For instance, a regular, galleried stereom typically houses collagenous ligaments, whereas an irregular, fine labyrinthic stereom commonly bears muscles. Epithelial tissues, in turn, are usually associated with coarse and dense stereom microfabrics. Stereom can be preserved in fossil echinoderms and a wide array of investigating methods are available. As many case studies have shown, a great deal of important paleobiological and paleoecological information can be decoded by studying the stereom microstructure of extinct echinoderms.
- Type
- Element
- Information
- Series: Elements of PaleontologyOnline ISBN: 9781108893886Publisher: Cambridge University PressPrint publication: 11 February 2021
References
Aizenberg, J., Hanson, J., Koetzle, T. F., Weiner, S., and Addadi, L. (1997). Control of macromolecule distribution within synthetic and biogenic single calcite crystals. Journal of the American Chemical Society, 119, 881–886.CrossRefGoogle Scholar
Aizenberg, J., Tkachenko, A., Weiner, S., Addadi, L., and Hendler, G. (2001). Calcitic microlenses as part of the photoreceptor system in brittlestars. Nature, 412, 819–822.Google Scholar
Alberic, M., Stifler, C., Zou, Z., et al. (2019). Growth and regrowth of adult sea urchin spines involve hydrated and anhydrous amorphous calcium carbonate precursors. Journal of Structural Biology, 1, 100004.Google ScholarPubMed
Ameye, L., (1999). Control of biomineralization in echinoderms: Ultrastructure and cytochemistry of the organic matrix. PhD thesis, Université Libre Bruxelles, Faculté des Sciences, Laboratorie de Biologie Marine.Google Scholar
Ameye, L, Compère, Ph., Dille, J., and Dubois, Ph. (1998). Ultrastructure and cytochemistry of the early calcification site and of its mineralization organic matrix in Paracentrotus lividus (Echinodermata: Echinoidea). Histochemistry and Cell Biology, 110, 285–294.Google Scholar
Ameye, L. De Becker, G., Killian, C., et al. (2001). Proteins and saccharides of the sea urchin organic matrix of mineralization: Characterization and localization in the spine skeleton. Journal of Structural Biology, 134, 56–66.CrossRefGoogle ScholarPubMed
Ausich, W. I. (1977). The functional morphology and evolution of Pisocrinus (Crinoidea: Silurian). Journal of Paleontology, 51, 672–686.Google Scholar
Ausich, W. I. (1983). Functional morphology and feeding dynamics of the Early Mississippian crinoid Barycrinus asteriscus. Journal of Paleontology, 57, 31–41.Google Scholar
Baumiller, T. K., and Hagdorn, H. (1995). Taphonomy as a guide to functional morphology of Holocrinus, the first post-Paleozoic crinoid. Lethaia, 28, 221–228.Google Scholar
Baumiller, T. K., Salamon, M. A., Gorzelak, P., Mooi, R., Messing, Ch. G., and Gahn, F. J. (2010). Post-Paleozoic crinoid radiation in response to benthic predation preceded the Mesozoic marine revolution. Proceedings of the National Academy of Sciences of USA, 107, 5893–5896.Google Scholar
Beniash, E., Addadi, L., and Weiner, S. (1999). Cellular control over spicule formation in sea urchin embryos: a structural approach. Journal of Structural Biology, 125, 50–62.CrossRefGoogle ScholarPubMed
Berg-Madsen, V. (1986). Middle Cambrian cystoid (sensu lato) stem columnals from 720 Bornholm, Denmark. Lethaia, 19, 67–80.CrossRefGoogle Scholar
Berman, A., Addaddi, A., and Weiner, S. (1988). Interactions of sea-urchin skeleton macromolecules with growing calcite crystals – a study of intracrystalline proteins. Nature, 331, 546–548.Google Scholar
Berman, A., Hanson, J., Leiserowitz, L., Koetzle, T. F., Weiner, S., and Addadi, L. (1993). Biological control of crystal texture: a widespread strategy for adapting crystal properties to function. Science, 259, 776–779.CrossRefGoogle ScholarPubMed
Bohatý, J. (2011). Revision of the flexible crinoid genus Ammonicrinus and a new hypothesis on its life mode. Acta Palaeontologica Polonica, 56, 615–639.CrossRefGoogle Scholar
Bottjer, D. J., Davidson, E. H., Peterson, K. J., and Cameron, R. A. (2006). Paleogenomics of echinoderms. Science, 314, 956–960.CrossRefGoogle ScholarPubMed
Brower, J. C. (1999). A new pleurocystitid rhombiferan echinoderm from the middle Ordovician Galena group of northern Iowa and southern Minnesota. Journal of Paleontology, 73, 129–153.Google Scholar
Carlson, S. J., and Fisher, D. C. (1981). Microstructural and morphologic analysis of a carpoid aulacophore. Geological Society of America, Abstracts with Programs, 13(7), 422.Google Scholar
Clark, E. G., Hutchinson, J. R., Bishop, P. J., and Briggs, D. E. G. (2020). Arm waving in stylophoran echinoderms: Three-dimensional mobility analysis illuminates cornute locomotion. Royal Society Open Science 7, 200191. http://dx.doi.org/10.1098/rsos.200191CrossRefGoogle ScholarPubMed
Clausen, S., and Smith, A. B. (2005). Palaeoanatomy and biological affinities of a Cambrian deuterostome (Stylophora). Nature, 438, 351–354.Google Scholar
Clausen, S., and Smith, A. B. (2008). Stem structure and evolution in the earliest pelmatozoan echinoderms. Journal of Paleontology, 82, 737–748.CrossRefGoogle Scholar
Cuif, J. P., Dauphin, Y., and Sorauf, J. E. (2011). Biominerals and fossils through time. Cambridge: Cambridge University Press.Google Scholar
David, B., Stock, S., De Carlo, F., Hétérier, V., and De Ridder, C. (2009). Microstructures of Antarctic cidaroid spines: Diversity of shapes and ectosymbiont attachments. Marine Biology, 156, 1559–1572.CrossRefGoogle Scholar
Dickson, J. A. D. (1966). Carbonate identification and genesis as revealed by staining. Journal of Sedimentary Research, 36(4), 491–505.Google Scholar
Donnay, G., and Pawson, D. L. (1969). X-ray diffraction studies of echinoderm plates. Science, 166, 1147–1150.CrossRefGoogle ScholarPubMed
Donovan, S. K. (1989). The improbability of a muscular crinoid column. Lethaia, 22, 307–315.CrossRefGoogle Scholar
Donovan, S. K., and Franzen-Bengtson, C. (1988). Myelodactylid crinoid columnals from the Lower Visby Beds (Llandoverian) of Gotland. GFF, 110, 69–79.Google Scholar
Dubois, Ph. (1991). Morphological evidence of coherent organic material within the stereom of postmetamorphic echinoderms. In Suga, S. and Nakahara, H., eds., Mechanisms and Phylogeny of Mineralization in Biological Systems. Tokyo: Springer-Verlag, pp.41–45.CrossRefGoogle Scholar
Dubois, Ph., and Chen, C. P. (1989). Calcification in Echinoderms. Echinoderm Studies, 3, 109–178.Google Scholar
Dubois, Ph., and Jangoux, M. (1990). Stereom morphogenesis and differentiation during regeneration of fractured adambulacral spines of Asterias rubens (Echinodermata, Asteroidea). Zoomorphology, 109, 263–272.Google Scholar
Gale, A. S. (1987). Phylogeny and classification of the Asteroidea (Echinodermata). Zoological Journal of the Linnean Society, 89, 107–132.CrossRefGoogle Scholar
Gorzelak, P. (2018). Microstructural evidence for stalk autotomy in Holocrinus: The oldest stem-group isocrinid. Palaeogeography, Palaeoclimatology, Palaeoecology, 506, 202–207.CrossRefGoogle Scholar
Gorzelak, P., Dery, A., Dubois, Ph., and Stolarski, J. (2017a). Sea urchin growth dynamics at microstructural length scale revealed by Mn-labeling and cathodoluminescence imaging. Frontiers in Zoology, 14, 42, doi:10.1186/s12983-017-0227-8.Google Scholar
Gorzelak, P., Kołbuk, D., Salamon, M., Łukowiak, M., Ausich, W., and Baumiller, T. (2020). Bringing planktonic crinoids back to the bottom: Reassessment of the functional role of scyphocrinoid loboliths. Paleobiology, 46(1), 104–122.Google Scholar
Gorzelak, P., Głuchowski, E., Brachaniec, T., Łukowiak, M., and Salamon, M. A. (2017b). Skeletal microstructure of uintacrinoid crinoids and inferences about their mode of life. Palaeogeography, Palaeoclimatology, Palaeoecology, 468, 200–207.CrossRefGoogle Scholar
Gorzelak, P., Głuchowski, E., and Salamon, M. A. (2014b). Reassessing the improbability of a muscular crinoid stem. Scientific Reports, 4, 6049.CrossRefGoogle ScholarPubMed
Gorzelak, P., Krzykawski, T., and Stolarski, J. (2016). Diagenesis of echinoderm skeletons: Constraints on paleoseawater Mg/Ca reconstructions. Global and Planetary Change, 144, 142–157.Google Scholar
Gorzelak, P., Rahman, I.A., Zamora, S., Gąsiński, A., Trzciński, J., Brachaniec, T., and Salamon, M. A. (2017c). Towards a better understanding of the origins of microlens arrays in Mesozoic ophiuroids and asteroids. Evolutionary Biology, 44, 339–346.CrossRefGoogle Scholar
Gorzelak, P., Stolarski, J., Dery, A., Dubois, Ph., Escrig, S., and Meibom, A. (2014a). Ultra- and micro-scale growth dynamics of the cidaroid spine of Phyllacanthus imperialis revealed by 26Mg labeling and NanoSIMS isotopic imaging. Journal of Morphology, 275(7), 788–796.CrossRefGoogle Scholar
Gorzelak, P., Stolarski, J., Dubois, P., Kopp, Ch., and Meibom, A. (2011). 26Mg labeling of the sea urchin regenerating spine: Insights into echinoderm biomineralization process. Journal of Structural Biology, 176, 119–126.CrossRefGoogle ScholarPubMed
Gorzelak, P., and Zamora, S. (2013). Stereom microstructures of Cambrian echinoderms revealed by cathodoluminescence (CL). Palaeontologia Electronica, 16 (3), 32A.Google Scholar
Gorzelak, P., and Zamora, S. (2016). Understanding form and function of the stem in early flattened echinoderms (pleurocystitids) using a microstructural approach. PeerJ, 4, e1820.Google Scholar
Grimmer, J. C., Holland, N. D., and Messing, C. G. (1984). Fine structure of the stalk of the bourgueticrinid sea lily Democrinus conifer (Echinodermata: Crinoidea). Marine Biology, 81, 163–176.CrossRefGoogle Scholar
Haude, R. (1972). Bau und Funktion der Scyphocrinites-Lobolithen. Lethaia, 5, 95–125.CrossRefGoogle Scholar
Heatfield, B. M. (1971). Growth of the calcareous skeleton during regeneration of spines of the sea urchin Strongylocentrotus purpuratus (Stimpson); a light and scanning electron microscope study. Journal of Morphology, 134, 57–90.Google Scholar
Hess., H. (1999). Uintacrinus beds of the Upper Cretaceous Niobrara formation, Kansas, USA. In Hess, H., Ausich, W. I., Brett, C. E., Simms, M. J., eds., Fossil Crinoids. Cambridge: Cambridge University Press, pp. 225–232.CrossRefGoogle Scholar
Hess, H., and Messing, Ch. (2011). Treatise on Invertebrate Paleontology. Part T, revised, Echinodermata 2, volume 3, Crinoidea Articulata. Lawrence, KS: Paleontological Institute, The University of Kansas.Google Scholar
Holland, N. D., Grimmer, J. C., and Wiegmann, K. (1991). The structure of the sea lily Calamocrinus diomedeae, with special reference to the articulations, skeletal microstructure, symbiotic bacteria, axial organs, and stalk tissues (Crinoidea, Millericrinida). Zoomorphology, 110, 115–132.Google Scholar
Kołbuk, D., Dubois, Ph., Stolarski, J., and Gorzelak, P. (2019). Effects of seawater chemistry (Mg2+/Ca2+ ratio) and diet on the skeletal Mg/Ca ratio in the common sea urchin Paracentrotus lividus. Marine Environmental Research, 145, 22–26.CrossRefGoogle Scholar
Kołbuk, D., Di Giglio, S., M’Zoudi, S., Dubois, P., Stolarski, J., Gorzelak, P. (2020). Effects of seawater Mg2+/Ca2+ ratio and diet on the biomineralization and growth of sea urchins and the relevance of fossil echinoderms to paleoenvironmental reconstructions. Geobiology, 18, 710–724.Google Scholar
Kroh, K., and Smith, A. B., ( 2010). The phylogeny and classification of post-Palaeozoic echinoids. Journal of Systematic Palaeontology, 8(2), 147–212.Google Scholar
Lapham, K. E., Ausich, W. I., and Lane, N. G. (1976). A technique for developing the stereom of fossil crinoid ossicles. Journal of Paleontology, 50, 245–248.Google Scholar
Lefebvre, B., Guensburg, T. E., Martin, E. L. O., et al. (2019). Exceptionally preserved soft parts in fossils from the Lower Ordovician of Morocco clarify stylophoran affinities within basal deuterostomes. Geobios, 52, 27–36.Google Scholar
Lowenstam, H. A., and Rossman, G. R., (1975). Amorphous, hydrous, ferric phosphatic dermal granules in Molpadia (Holothuroidea): Physical and chemical characterization, and ecologic implication of the bioinorganic fraction. Chemical Geology, 15, 15–51.Google Scholar
Ma, Y., Aichmayer, B., Paris, O., Fratzl, P., et al. (2009). The grinding tip of the sea urchin tooth exhibits exquisite control over calcite crystal orientation and Mg distribution. Proceedings of the National Academy of Sciences of USA, 106(15), 6048–6053.Google Scholar
Macurda, D. B., and Meyer, D. L. (1975). The microstructure of the crinoid endoskeleton. The University of Kansas Paleontological Contributions, 74, 1–22.Google Scholar
Macurda, D. B. (1976). Skeletal modifications related to food capture and feeding behavior of the basketstar. Astrophyton. Paleobiology, 2, 1–7.CrossRefGoogle Scholar
Märkel, K. (1986). Ultrastructural investigation of matrix-mediated biomineralization in echinoids (Echinodermata, Echinoidea). Zoomorphology, 106, 232–243.CrossRefGoogle Scholar
Márquez-Borrás, F., Solís-Marín, F. A., and Mejía-Ortíz, L. M. (2018). Troglomorphism in a brittlestar of the genus Ophionereis (Ophiuroidea: Ophionereididae) from Mexico. Abstracts of the 16th International Echinoderm Conference, Nagoya, Japan.Google Scholar
Martins, L., and Tavares, M. (2018). Ypsilothuria bitentaculata bitentaculata (Echinodermata: Holothuroidea) from the southwestern Atlantic, with comments on its morphology. Zoologia, 35, e24573.CrossRefGoogle Scholar
Medeiros-Bergen, D. E. (1996). On the stereom microstructure of ophiuroid teeth. Ophelia, 45, 211–222.CrossRefGoogle Scholar
Moureaux, C., Pérez-Huerta, A., Compère, P., et al. (2010). Structure, composition and mechanical relations to function in sea urchin spine. Journal of Structural Biology, 170, 41–49.CrossRefGoogle ScholarPubMed
Nissen, H. U. (1969). Crystal orientation and plate structure in echinoid skeletal units. Science, 166, 1150–1152.Google Scholar
Oaki, Y., and Imai, H. (2006). Nanoengineering in echinoderms: The emergence of morphology from nanobricks. Small, 2, 66–70.CrossRefGoogle ScholarPubMed
Okazaki, K. (1960). Skeleton formation of sea urchin larvae. II. Organic matrix of the spicule. Embryologia, 5, 283–320.Google Scholar
Paul, C. R. C. (1984). British Ordovician cystoids, part 2. Monograph of the Paleontographical Society, London, 136, 65–153.Google Scholar
Pisera, A. (1994). Echinoderms from the Mójcza Limestone. Palaeontologia Polonica, 53, 283–307.Google Scholar
Pearse, J. S., and Pearse, V. B. (1975). Growth zones in the echinoid skeleton. American Zoologist, 15, 731–753.Google Scholar
Polishchuk, I., Brach, A. A., Bloch, L., et al. (2017). Coherently aligned nanoparticles within a biogenic single crystal: A biological prestressing strategy. Science, 358(6368), 1294–1298.Google Scholar
Ribeiro, A. R., Barbaglio, A., Benedetto, C. D., et al. (2011). New insights into mutable collagenous tissue: Correlations between the microstructure and mechanical state of a sea-urchin ligament. PLoS ONE, 6 (9),e24822.CrossRefGoogle ScholarPubMed
Richter, D. K., Goette, T., Goetze, J., Neuser, R. D., and Neuser, R. D. (2003). Progress in application of cathodoluminescence (CL) in sedimentary petrology. Mineralogy and Petrology, 79, 127–166.Google Scholar
Riddle, S. W., Wulff, J. I., and Ausich, W. I. (1988). Biomechanics and stereomic microstructure of the Gilbertsocrinus tuberosus column. In Burke, R. D., Mladenov, P. V., Lambert, P. and Parsley, R. L., eds., Echinoderm Biology. Rotterdam: A.A. Balkema, pp. 641–648.Google Scholar
Reich, M. (2015). Different pathways in early evolution of the holothurian calcareous ring? In Zamora, S., and Rábano, I., eds., Progress in Echinoderm Palaeobiology. Madrid: Inst. Geol. España: Cuadenos del Museo Geominero, 19, pp. 137–145.Google Scholar
Roux, M. (1970). Introduction à l’étude des microstructures des tiges de crinoïdes. Geobios, 3, 79–98.Google Scholar
Roux, M. (1971). Recherches sur la microstructure des pédonculés de crinoides post Paléozoiques. Travaux du Laboratoire de paléontologie Orsay, 1–83.Google Scholar
Roux, M. (1974). Les principaux modes d’articulation des ossicules du squelette des Crinoïdes pédonculés actuels. Observations microstructurales et conséquences pour l’interprétation des fossiles. Compte Rendu de l’Académie des Sciences, Paris, 278, 2015–2018.Google Scholar
Roux, M. (1975). Microstructural analysis of the crinoid stem. The University of Kansas Paleontological Contributions, 75, 1–7.Google Scholar
Roux, M. (1977). The stalk-joints of Recent Isocrinidae (Crinoidea). Bulletin of the British Museum (Natural History). Zoology, 32, 45–64.Google Scholar
Roux, M., Messing, C. G., and Améziane, N. (2002). Artificial keys to the genera of living stalked crinoids (Echinodermata). Bulletin of Marine Science, 70, 799–830.Google Scholar
Salamon, M. A., Gorzelak, P., Hanken, N. M., Riise, H. E., and Ferré, B. (2015). Crinoids from Svalbard in the aftermath of the end: Permian mass extinction. Polish Polar Research, 36(3), 225–238.Google Scholar
Schroeder, J. H., Dwornik, E. J., and Papike, J. J. (1969). Primary protodolomite in echinoid skeletons. Geological Society of America Bulletin, 80, 1613–1618.Google Scholar
Seto, J., Ma, Y., Davis, S. A., et al. (2012). Structure-property relationships of a biological mesocrystal in the adult sea urchin spine. Proccedings of the National Academy of Sciences of USA, 10, 3699–3704.CrossRefGoogle Scholar
Sevastopulo, G. D., and Keegan, J. B. (1980). A technique revealing the stereom microstructure of fossil crinoids. Palaeontology, 23, 749–756.Google Scholar
Simms, M. J. (2011). Stereom microstructure of columnal latera: A character for assessing phylogenetic relationships in articulate crinoids. Swiss Journal of Palaeontology, 130, 143–154.CrossRefGoogle Scholar
Smith, A. B. (1978). A functional classification of the coronal pores of regular echinoids. Palaeontology, 21, 81–84.Google Scholar
Smith, A. B. (1980a). Stereom microstructure of the echinoid test. Special Paper in Palaeontogy, 25, 1–81.Google Scholar
Smith, A. B. (1980b). The structure, function, and evolution of tube feet and ambulacral pores in irregular echinoids. Palaeontology, 23, 39–83.Google Scholar
Smith, A. B. (1982). The affinities of the Middle Cambrian Haplozoa (Echinodermata). Alcheringa: An Australasian Journal of Palaeontology, 6(2), 93–99.Google Scholar
Smith, A. B. (1990). Biomineralization in echinoderms. In Carter, J. G., ed., Skeletal Biomineralization: Patterns, Processes, and Evolutionary Trends. New York: Van Nostrand Reinhold, pp. 413–443.Google Scholar
Sumner-Rooney, L. Rahman, I. A., Sigwart, J. D., and Ullrich-Lüter, E. (2018). Whole-body photoreceptor networks are independent of ‘lenses’ in brittle stars. Proceedings of the Royal Society B: Biological Sciences, 285 (1871), 20172590 doi: 10.1098/rspb.2017.2590Google ScholarPubMed
Sumner-Rooney, L., Kirwan, J. D., Lowe, E., and Ullrich- Lüter, E. (2020). Extraocular vision in a brittle star is mediated by chromatophore movement in response to ambient light. Current Biology, 30, 319–327.CrossRefGoogle Scholar
Sumrall, C. D. (2000). The biological implications of an edrioasteroid attached to a pleurocystitid rhombiferan. Journal of Paleontology, 74, 67–71Google Scholar
Weiner, S. (1985). Organic matrix-like macromolecules associated with the mineral phase of sea urchin skeletal plates and teeth. Journal of Experimental Zoology, 234, 7–15.Google Scholar
Weiner, S., and Addadi, L. (2011). Crystallization pathways in biomineralization. Annual Review of Materials Research, 41, 21–40.CrossRefGoogle Scholar
Wilt, F. H. (1999). Matrix and mineral in the sea urchin larval skeleton. Journal of Structural Biology, 126, 216–226.CrossRefGoogle ScholarPubMed
Vidavsky, N., Addadi, S., Mahamid, J., et al. (2014). Initial stages of calcium uptake and mineral deposition in sea urchin embryos. Proceedings of the National Academy of Sciences of USA, 111(1), 39–44.CrossRefGoogle ScholarPubMed
Vidavsky, N., Addadi, S., Schertel, A., et al. (2016). Calcium transport into the cells of the sea urchin larva in relation to spicule formation. Proceedings of the National Academy of Sciences of USA, 113(45), 12637–12642.Google Scholar
Yang, L., Killian, C. E., Kunz, M., Tamura, N., and Gilbert, P. U. P. A. (2011). Biomineral nanoparticles are space-filling. Nanoscale, 3, 603–609.Google Scholar
Zamora, S., Rahman, I. A., and Smith, A. B. (2013). The ontogeny of cinctans (stem-group Echinodermata) as revealed by a new genus, Graciacystis, from the middle Cambrian of Spain. Palaeontology, 56, 399–410.Google Scholar
Zapasnik, H. T., and Johnston, P. A. (1984). Replication in plastic of three-dimensional fossils preserved in indurated clastic sedimentary rocks. Science, 224, 1425–1427.Google Scholar
- 14
- Cited by