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Echinoderms: Hierarchically Organized Light Weight Skeletons

  • James H. NebelsickEmail author
  • Janina F. Dynowski
  • Jan Nils Grossmann
  • Christian Tötzke
Chapter
Part of the Biologically-Inspired Systems book series (BISY, volume 6)

Abstract

Echinoderm skeletons are described within a hierarchical framework ranging from complete organisms to the ultrastructural level. They consist of numerous elements which can be isolated, connected by soft tissue or locked together in rigid structures. The top level considers skeletons as a whole with all associated elements and the basic symmetry of the echinoderms. The next level deals with the structural analysis and modeling of echinoids with respect to the growth parameters and stress resistance of the corona. The flexibility and movement has also been studied for the stalks and arms of recent and fossil crinoids. The next level deals with the elaborate morphology and types of symmetry found in single skeletal elements. The numerous types of stereom architectures found within the elements of all echinoderms are highly correlated to specific functions. A high number of recent studies concern the last hierarchical level on ultrastructure and biomineralization. Lightweight aspects of the skeleton are especially present at the level of conjoined plates, single elements and the stereom.

Keywords

Echinoderms Skeletal Structures Lightweight Design Hierarchical Framework Morphology Symmetry Ultrastructure Biomineralisation Stereom 

Notes

Acknowledgments

Funding provided by the Stiftung Baden-Württemberg, the DAAD and the German Science Foundation (DFG Project NE 537/24-1). Macroscopic photographs by Wolfgang Gerber, Tübingen. REM images of Figs. 8.5 and 8.6 by Susanne Leidenroth, SMNS.

References

  1. Albeck S, Addadi I, Weiner S (1996) Regulation of calcite crystal morphology by intracrystalline acidic proteins and glycoproteins. Connect Tissue Res 35:365–370CrossRefGoogle Scholar
  2. Ameye L, Compere Ph, Dille J, Dubois Ph (1998) Ultrastructure of the early calcification site and of its mineralizing organic matrix in Paracentrotus lividus (Echinodermata: Echinoidea). Histochem Cell Biol 110:285–294CrossRefGoogle Scholar
  3. Ameye L, Hermann R, Dubois P (2000) Ultrastructure of sea urchin calcified tissues after high-pressure freezing and freeze substitution. J Struct Biol 131:116–125CrossRefGoogle Scholar
  4. Baumiller TK (2008) Crinoid ecological morphology. Annu Rev Earth Planet Sci 36:221–249CrossRefGoogle Scholar
  5. Baumiller TK, Ausich WI (1996) Crinoid stalk flexibility: theoretical predictions and fossil stalk postures. Lethaia 29:47–59CrossRefGoogle Scholar
  6. Baumiller TK, LaBarbera M (1993) Mechanical properties of the stalk and cirri of the sea lily Cenocrinus asterius. Comp Biochem Physiol 106A:91–95CrossRefGoogle Scholar
  7. Baumiller TK, Messing CG (2007) Stalked crinoid locomotion, and its ecological and evolutionary implications. Palaeont Electr 10(2A):10pGoogle Scholar
  8. Berman A, Addadi L, Weiner S (1988) Interactions of sea-urchin skeleton macromolecules with growing calcite crystals—a study of intracrystalline proteins. Nature 331:546–548CrossRefGoogle Scholar
  9. Birenheide R, Motokawa T (1994) Morphological basis and mechanics of arm movement in the stalked crinoid Metacrinus rotundus (Echinodermata, Crinoidea). Mar Biol 121:273–283CrossRefGoogle Scholar
  10. Birenheide R, Motokawa T (1996) Contractile connective tissue in crinoids. Biol Bull 191:1–4CrossRefGoogle Scholar
  11. Birenheide R, Motokawa T (1997) Morphology of Skeletal Cortex in the Arms of Crinoids (Echinodermata: Crinoidea). Zool Sci 14:753–761CrossRefGoogle Scholar
  12. Blake DF, Peacor DR, Allard LF (1984) Ultrastructural and microanalytical results from echinoderm calcite: implications for biomineralization and diagenesis of skeletal material. Micron Microscopica Acta 15:85–90CrossRefGoogle Scholar
  13. Burkhardt A, Hansmann W, Märkel K, Niemann HJ (1983) Mechanical design in spines of diadematoid echinoids (Echinodermata, Echinoidea). Zoomorphology 102:189–203CrossRefGoogle Scholar
  14. Chakra MA, Stone JR (2011) Classifying echinoid skeleton models: testing ideas about growth and form. Paleobiology 37:686–695CrossRefGoogle Scholar
  15. Coppard SE, Campbell AC (2004) Taxonomic significance of spine morphology in the echinoid genera Diadema and Echinothrix. Invertebr Biol 123:357–371CrossRefGoogle Scholar
  16. Cowen R (1981) Crinoids arms and banana plantations: an economic harvesting analogy. Paleobiology 7:332–343Google Scholar
  17. Currey JD (1975) A comparson of the strength of echinoderm spines and mollusc shells. J Mar Biol Ass UK 55:419–424CrossRefGoogle Scholar
  18. Dafni J (1986) Echinoid Skeletons as Pneu Structures. Konzepte SFB 230, Universität Tübingen und Stuttgart. Stuttgart 13:9–96Google Scholar
  19. Dafni J (1988) A biomechanical approach to the ontogeny and phylogeny of echinoids. In: Paul CRC, Smith AB (eds) Echinoderm phylogeny and evolutionary biology. Oxford University Press, Oxford, pp 175–188Google Scholar
  20. David B, Stock SR, De Carlo F, Hétérier V, De Ridder C (2009) Microstructures of Antarctic cidaroid spines: diversity of shapes and ectosymbiont attachments. Mar Biol 156:1559–1572CrossRefGoogle Scholar
  21. Dynowski JF (2012) Echinoderm remains in shallow-water carbonates at Fernandez Bay, San Salvador Island, Bahamas. Palaios 27:183–191CrossRefGoogle Scholar
  22. Dynowski JF, Nebelsick JH (2011) Ecophenotypic variations of Encrinus liliiformis (Echinodermata: Crinoidea) from the middle Triassic Muschelkalk of Southwest Germany. Swiss J Palaeont 130:53–67CrossRefGoogle Scholar
  23. Ebert TA (1975) Growth and morallity of post-larval echinoids. Am Zool 15:755–775CrossRefGoogle Scholar
  24. Ebert TA (1985) The non-periodic nature of growth rings in echinoid spines. In: Keegan BF, O’Connor BDS (eds) Echinodermata: proceedings of the International Echinoderm Conference, Galway, A.A. Balkema, Rotterdam, pp 261–267, 24–29 Sept 1984Google Scholar
  25. Ebert TA (1986) A new theory to explain the origin of growth lines in sea urchin spines. Mar Ecol Prog Ser 34:197–199CrossRefGoogle Scholar
  26. Ellers O, Telford M (1992) Causes and consequences of fluctuating coelomic pressure in sea urchins. Biol Bull 182:424–434CrossRefGoogle Scholar
  27. Ellers O, Johnson AS, Moberg PF (1998) Structural strengthening of urchin skeletons by collagenous sutural ligaments. Biol Bull 195:136–144CrossRefGoogle Scholar
  28. Emlet R (1982) Echinoderm calcite: a mechanical analysis from larval spicules. Biol Bull 163:264–275CrossRefGoogle Scholar
  29. Gilbert PUPA, Weiner S (2009) The grinding tip of the sea urchin tooth exhibits exquisite control over calcite crystal orientation and Mg distribution. Proc Natl Acad Sci USA 106:6048–6053CrossRefGoogle Scholar
  30. Gilbert PUPA, Wilt FH (2011) Molecular aspects of biomineralization of the echinoderm endoskeleton. Prog Mol Subcell Biol 52:199–223CrossRefGoogle Scholar
  31. Grossmann JN, Nebelsick JH (2013a) Stereom Differentiation in spines of Plococidaris verticillata, Heterocentrotus mammillatus and other regular sea urchins. In: Johnson C (ed) Echinoderms in a changing World. Proceedings of the 13th International Echinoderm Conference, Tasmania, CRC Press, London, pp 97–104Google Scholar
  32. Grossmann JN, Nebelsick JH (2013b) Comparative morphological and structural analysis of selected cidaroid and camarodont sea urchin spines. Zoomorph 132:301–315Google Scholar
  33. Hidaka M, Takahashi K (1983) Fine structure and mechanical properties of the catch apparatus of the sea-urchin spine, a collagenous connective tissue with muscle-like holding capacity. J Exp Biol 103:1–14Google Scholar
  34. Hotchkiss, FHC (1998) A “rays-as-appendages” model of the origin of pentamerism in echinoderms. Paleobiology 24(2):200–214.Google Scholar
  35. Johnson AS, Ellers O, Lemire J, Minor M, Leddy HA (2002) Sutural loosening and skeletal flexibility during growth: determination of drop-like shapes in sea urchins. Proc R Soc Lond B 269:215–220CrossRefGoogle Scholar
  36. Killian CE, Wilt FH (2008) Molecular aspects of biomineralization of the echinoderm endoskeleton: Chem Rev 108:4463–4474CrossRefGoogle Scholar
  37. Killian CE, Metzler RA, Gong YT, Churchill TH, Olson IC, Trubetskoy V, Christensen MB, Fournelle JH, De Carlo F, Cohen S, Mahamid J, Scholl A, Young A, Doran A, Wilt FH, Coppersmith SN, Gilbert PUPA (2011) Self-Sharpening Mechanism of the Sea Urchin Tooth. Adv Funct Mater 21:682–690CrossRefGoogle Scholar
  38. Kniprath E (1974) Ultrastructure and growth of the sea urchin tooth. Calc Tiss Res 14:211–228CrossRefGoogle Scholar
  39. Kroh A, Nebelsick JH (2010) Echinoderms and Oligo-Miocene carbonate systems: potential applications in sedimentology and environmental reconstruction. Int Assoc Sedimentol Spec Publ 42:201–228Google Scholar
  40. Kroh A, Smith AB (2010) The phylogeny and classification of post-Palaeozoic echinoids. J Syst Palaeont 8(2):147–212CrossRefGoogle Scholar
  41. Laurin B, David B (1990) Mapping morphological changes in the spatagoid Echinocardium: applications to ontogeny and interspcific comparisons. In: De Ridder C, Dubois P, Lahaye MC, Jangoux M (eds) Echinoderm research. Rotterdam, Balkema, pp 739–745Google Scholar
  42. Laurin B, Marchand D, Thierry J (1979) Variations morphologiques du test chez Echinocardium cordatum (Pennant): étude qualitative et quantitative de cinq échantillons de Bretagne et de Normandie. Bull Soc Geol Normandie 65:895–906Google Scholar
  43. Lawrence JM, Pomory CM, Sonnenholzner J, Chao C-M (1998) Bilateral symmetry of the petals in Melitta tenuis, Encope micropora, and Arachnoides placenta (Echinodermata: Clypeasteroida). Invertebr Biol 17:94–100CrossRefGoogle Scholar
  44. MacKenzie CR, Wilbanks SM, Barker MF, McGrath KM (2001) Biomineralisation in echinoderms: identification of occluded proteins. In: Barker M (ed) Echinoderms 2000. Swets & Zeitlinger, Lisse, pp 499–504Google Scholar
  45. Mann K, Poustka AJ, Mann M (2010a) Phosphoproteomes of Strongylocentrotus purpuratus shell and tooth matrix: identification of a major acidic sea urchin tooth phosphoprotein, phosphodontin. Proteome Sci 8:6CrossRefGoogle Scholar
  46. Mann K, Wilt FH, Proustka A (2010b) Proteomic analysis of sea urchin (Strongylocentrotus purpuratus) spicule matrix. Proteome Sci 8:33CrossRefGoogle Scholar
  47. Märkel K, Gorny P (1973) Zur funktionellen Anatomie der Seeigelzähne (Echinodermata, Echinoidea). Zoomorph 75:223–242Google Scholar
  48. Märkel K, Röser U (1983) Calcite-resorption in the spine of the echinoid Eucidaris tribuloides. Zoomorph 103:43–58CrossRefGoogle Scholar
  49. Märkel K, Kubanek F, Willgallis A (1971) Polykristalliner Calcit bei Seeigeln (Echinodermata, Echinoidea). Cell Tissue Res 119:355–377Google Scholar
  50. Märkel K, Röser U, Mackenstedt U, Klostermann M (1986) Ultrastructure investigation of matrix-mediated biomineralization in echinoids (Echinodermata, Echinoidea). Zoomorph 106:232–243CrossRefGoogle Scholar
  51. Matranga V, Bonaventura R, Costa C, Karakostis K, Pinsino A, Russo R, Zito F (2011) Echinoderms as blueprints for biocalcification: Regulation of skeletogenic genes and matrices. Mol Biomin 52:225–248CrossRefGoogle Scholar
  52. Mihaljević M, Jerjen I, Smith AB (2011) The test architecture of Clypeaster (Echinoidea, Clypeasteroida) and its phylogenetic significance. ZooTaxa 2983:21–38Google Scholar
  53. Morris, VB (2007) Origins of radial symmetry identified in an echinoderm during adult development and the inferred axes of ancestral bilateral symmetry. Proc R Soc B 294:1511–1516CrossRefGoogle Scholar
  54. Moss ML, Meehan MM (1968) Growth of the echinoid test. Acta Anat 69:409–444CrossRefGoogle Scholar
  55. Motokawa T, Osamu S, Birenheide R (2004) Contraction and stiffness changes in collagenous arm ligaments of the stalked crinoid Metacrinus rotundus (Echinodermata). Biol Bull 206:4–12CrossRefGoogle Scholar
  56. Moureaux C, Pérez-Huerta A, Compère P, Zhu W, Leloup T, Cusack M, Dubois P (2010) Structure, composition and mechanical relations to function in sea urchin spine. J Struct Biol 170:41–49CrossRefGoogle Scholar
  57. Nebelsick JH (1992) Echinoid distribution by fragment identification in the Northern Bay of Safaga, Red Sea. Palaios 7:316–328CrossRefGoogle Scholar
  58. Pearse JS, Pearse VB (1975) Growth zones in echinoids skeleton. Am Zool 15:731–753CrossRefGoogle Scholar
  59. Peled-Kamar M, Hamilton P, Wilt FH (2002) Spicule matrix protein LSM34 is essential for biomineralization of the sea urchin spicule. Exp Cell Res 272:56–61CrossRefGoogle Scholar
  60. Phillipi U, Nachtigall W (1996) Functional morphology of regular echinoid tests (Echinodermata, Echinoida): a finite element study. Zoomorph 116:35–50CrossRefGoogle Scholar
  61. Politi Y, Arad T, Klein E, Weiner S, Addadi L (2004) Sea Urchin Spine Calcite Forms via a Transient Amorphous Calcium Carbonate Phase. Science 306:1161–1164CrossRefGoogle Scholar
  62. Politi Y, Metzler RA, Abrecht M, Gilbert B, Wilt FH, Sagi I, Addadi L, Weiner S, Gilbert PU (2008) Transformation mechanism of amorphous calcium carbonate into calcite in the sea urchin larval spicule. Proc Natl Acad Sci USA 105:17362–17366CrossRefGoogle Scholar
  63. Presser V, Kohler C, Zivcová Z, Berthold C, Nickel KG, Schultheiß S, Gregorová E, Pabst W (2009) Sea urchin spines as a model-system for permeable, light-weight ceramics with graceful failure behavior. Part II. Mechanical behavior of sea urchin spine inspired porous aluminum oxide ceramics under compression. J Bionic Engin 6:357–364CrossRefGoogle Scholar
  64. Raup DM (1966) The endoskeleton. In: Boolotian RA (ed) Physiology of Echinodermata. Wiley, New York, pp 379–395Google Scholar
  65. Raup DM (1968) Theoretical morphology of echinoid growth. J. Paleont 42:50–63Google Scholar
  66. Robach JS, Stock SR, Veis A (2009) Structure of first- and second-stage mineralized elements in teeth of the sea urchin Lytechinus variegatus. J Struct Biol 168:452–466CrossRefGoogle Scholar
  67. Seilacher A (1979) Constructional morphology of sand dollars. Paleobiology 5:191–221Google Scholar
  68. Smith AB (1978) A functional classification of the coronal pores of regular echinoids. Palaeontology 21:759–789Google Scholar
  69. Smith AB (1980a) The structure, function and evolution of tube feet and ambulacral pores in irregular echinoids. Palaeontology 23:39–84Google Scholar
  70. Smith AB (1980b) The structure and arrangement of echinoid tubercles. Phil Trans Roy Soc Lond B 289:1–54CrossRefGoogle Scholar
  71. Smith AB (1980c) Stereom microstructure of the echinoid test. Spec Pap Palaeont 25:1–83Google Scholar
  72. Smith AB (1990) Biomineralization in Echinoderms. In: Carter JG (ed) Skeletal biomineralization: Patterns, process and evolutionary trends vol I. Van Nostrand Rheinhold, New York, pp 413–443Google Scholar
  73. Smith AB (1997) Echinoderm larvae and phylogeny. Annual Rev Ecol Syst 28:219–241CrossRefGoogle Scholar
  74. Smith AB (2005a) The pre-radial history of echinoderms. Geol J 40:255–280CrossRefGoogle Scholar
  75. Smith AB (2005b) Growth and form in echinoids: The evolutionary interplay of plate accretion and plate addition. In: Briggs DEG (ed) Evolving form and function: fossils and development: proceedings of a symposium honoring Adolf Seilacher for his contributions to paleontology in celebration of his 80th Birthday. New Haven. Peabody museum of Natural History, Yale University, pp 181–193Google Scholar
  76. Smith DS, del Castillo J, Morales M, Luke B (1990) The attachment of collagenous ligament to stereom in primary spines of the sea-urchin Eucidaris tribuloides. Tissue Cell 22:157–176CrossRefGoogle Scholar
  77. Smith AB, Peterson KJ, Wray G, Littlewood DTJ (2004) From bilateral symmetry to pentaradiality. The phylogeny of hemichordates and echinoderms. In: Cracraft J, Donoghue MJ (eds) Addembling the Tree of Life. Oxford University Press, New York, pp 365–383Google Scholar
  78. Stock SR, Nagaraja S, Barss J, Dahl T, Veis A (2003) X-ray microCT study of pyramids of the sea urchin Lytechinus variegatus. J Struct Biol 141:9–21CrossRefGoogle Scholar
  79. Strathmann RR (1981) The role of spines in preventing structural damage to echinoid tests. Paleobiology 7:400–406Google Scholar
  80. Telford M (1985) Domes, arches und urchins: the skeletal architecture of echinoids (Echinodermata). Zoomorph 105:114–124CrossRefGoogle Scholar
  81. Towe, KM (1967) Echinoderm calcite: Single crystal or polycrystalline aggregate. Science 157:1048–1050CrossRefGoogle Scholar
  82. Tsafnat N, Fitz Gerald JD, Le HN, Stachurski ZH (2012) Micromechanics of sea urchin spines. PLoS One 7(9):e44140. doi:10.1371/journal.pone.0044140CrossRefGoogle Scholar
  83. Tsipursky SJ, Buseck PR (1993) Structure of magnesian calcite from sea urchins. Am Min 78:775–781Google Scholar
  84. Veis A (2011) Organic matrix-related mineralization of sea urchin spicules, spines, test and teeth. Front Biosci 17:2540–2560CrossRefGoogle Scholar
  85. Veis A, Stock SR, Alvares K, Lux E (2011) On the formation and functions of high and very high magnesium calcites in the continuously growing teeth of the echinoderm Lytechinus variegatus: Development of crystallinity and protein involvement. Cells Tissues Organs 194:131–137CrossRefGoogle Scholar
  86. Wang RZ, Addadi L, Weiner S (1997) Design strategies of sea urchin teeth: structure, composition and micromechanical relations to function. Phil Trans R Soc Lond B Biol Sci 352(1352):469–480CrossRefGoogle Scholar
  87. Weber JN (1969) The incorporation of magnesium onto the skeletal calcite of echinoderms. Am J Sci 267:537–566CrossRefGoogle Scholar
  88. Wilt FH (1999) Matrix and mineral in the sea urchin larval skeleton. J Struct Biol 126:216–226CrossRefGoogle Scholar
  89. Wilt FH (2002) Biomineralization of the spicules of sea urchin embryos. Zool Sci 19:253–261CrossRefGoogle Scholar
  90. Wilt FH, Killian CE, Hamilton P, Croker L (2008) The dynamics of secretion during sea urchin embryonic skeleton formation. Exp Cell Res 314:1744–1752CrossRefGoogle Scholar
  91. Zachos LG (2009) A new computational growth model of sea urchin skeletons. J Theor Biol 259:646–657CrossRefGoogle Scholar
  92. Zamora S, Rahman I, Smith AB (2012) Plated Cambrian bilaterians reveal the earliest stages of echinoderm evolution. PLoS One 7(6):e38296CrossRefGoogle Scholar
  93. Ziegler A, Stock SR, Menze BH, Smith AB (2012) Macro- and microstructural diversity of sea urchin teeth revealed by large-scale micro-computed tomography survey. In Stock SR (ed) Developments in X-Ray tomography VIII. Proceedings of SPIE 8506, 85061GGoogle Scholar

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© Springer Science+Business Media Dordrecht 2015

Authors and Affiliations

  • James H. Nebelsick
    • 1
    Email author
  • Janina F. Dynowski
    • 2
    • 3
  • Jan Nils Grossmann
    • 4
    • 5
  • Christian Tötzke
    • 6
  1. 1.Department of GeosciencesUniversity of TübingenTübingenGermany
  2. 2.Stuttgart State Museum of Natural HistoryStuttgartGermany
  3. 3.Department of GeosciencesUniversity of TübingenTübingenGermany
  4. 4.Institute of Zoology, Graduate Program: Bionics-Interactions across Boundaries to the Environment, University of BonnBonnGermany
  5. 5.Zentrum für Wissenschafts- und TechnologietransferHochschule Bonn-Rhein-Sieg, University of Applied SciencesSankt AugustinGermany
  6. 6.Helmholtz-Zentrum Berlin for Materials and EnergyBerlinGermany

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