Evolution of a novel muscle design in sea urchins (echinodermata: Echinoidea)

PLoS ONE

Volumn 7, Issue 5, 2012, Pages

  Ziegler, Alexander ^a   Schröder, Leif ^b   Ogurreck, Malte ^c   Faber, Cornelius ^d   Stach, Thomas ^e  

^a HARVARD UNIVERSITY   (United States)

^b LEIBNIZ INSTITUT FÜR MOLEKULARE PHARMAKOLOGIE   (Germany)

^c INSTITUTE OF MATERIALS RESEARCH   (Germany)

^d UNIVERSITY HOSPITAL MÜNSTER   (Germany)

^e FREIE UNIVERSITÄT BERLIN   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL STRUCTURES; ANIMAL TISSUE; ARISTOTLE LANTERN; ARTICLE; ECHINODERM; ECHINOMETRIDAE; EVOLUTION; FLAT MUSCLE; HISTOLOGY; MASTICATORY MUSCLE; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; ONTOGENY; PERIPHARYNX COELOM; PROTRACTOR MUSCLE; SCANNING ELECTRON MICROSCOPY; SEA URCHIN; SPECIES COMPARISON; STRONGYLOCENTROTIDAE; TOXOPNEUSTIDAE; ULTRASTRUCTURE; ANIMAL; PHYSIOLOGY; SPECIES DIFFERENCE;

ECHINODERMATA; ECHINOIDA; ECHINOIDEA; ECHINOMETRIDAE; STRONGYLOCENTROTIDAE; TOXOPNEUSTIDAE;

ANIMALS; BIOLOGICAL EVOLUTION; HISTOLOGICAL TECHNIQUES; MAGNETIC RESONANCE IMAGING; MASTICATORY MUSCLES; MICROSCOPY, ELECTRON, SCANNING; SEA URCHINS; SPECIES SPECIFICITY;

EID: 84862060934     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0037520     Document Type: Article

References (83)

1. Tiedemann F, (1816) Anatomie der Röhren-Holothurie, des pomeranzfarbigen Seesterns und des Stein-Seeigels Landshut Joseph Thomann.
2. Valentin G, (1841) Anatomie du genre Echinus. In: Agassiz L, editors. Monographies d'echinodermes vivans et fossiles Neuchâtel Petitpierre.
3. Prouho H, (1888) Recherches sur le Dorocidaris papillata et quelques autres échinides de la Méditerranée Paris Hennuyer.
4. Cuénot L, (1891) Etudes morphologiques sur les echinodermes. In: van Beneden E, van Bambeke C, editors. Archives de Biologie, Tome XI Paris Masson.
5. Lovén S, (1892) Echinologica. Bih Kong Svensk Vetensk Akadem Handl 18: 1-74.
6. Jackson RT, (1912) Phylogeny of the Echini, with a revision of Palaeozoic species. Mem Bos Soc Nat Hist 7: 1-493.
7. Hyman LH, (1955) The invertebrates: Echinodermata. The coelomate Bilateria. Volume IV New York McGraw-Hill.
8. Lanzavecchia G, Candia Carnevali MD, Melone G, Celentano FC, Andrietti F, (1988) Aristotle's lantern in the regular sea urchin Paracentrotus lividus. I. Functional morphology and significance of bones, muscles and ligaments. In: Burke RD, Mladenov PV, Lambert P, Parsley R, editors. Echinoderm Biology Rotterdam Balkema pp. 649-662.
9. Candia Carnevali MD, Bonasoro F, Melone G, (1991) Microstructure and mechanical design in the lantern ossicles of the regular sea-urchin Paracentrotus lividus: a scanning electron microscope study. Boll Zool 58: 1-42.
10. Candia Carnevali MD, Wilkie IC, Lucca E, Andrietti F, Melone G, (1993) The Aristotle's lantern of the sea-urchin Stylocidaris affinis (Echinoida, Cidaridae): functional morphology of the musculo-skeletal system. Zoomorphology 113: 173-189.
11. Hoffmann CK, (1871) Zur Anatomie der Echinen und Spatangen. Niederl Arch Zool 1: 11-112.
12. Schick JM, (1983) Respiratory gas exchange in echinoderms. In: Jangoux M, Lawrence JM, editors. Echinoderm Studies 1 Rotterdam, Balkema pp. 67-110.
13. De Ridder C, (1988) Could the Stewart's organs of cidaroid echinoids be internal gills? In: Burke RD, Mladenov PV, Lambert P, Parsley R, editors. Echinoderm Biology Rotterdam Balkema pp. 675-681.
14. Birenheide R, (1992) The sea urchin lantern coelom: a circulatory system. In: Scalera-Liaci L, Canicatti C, editors. Echinoderm Research 1991 Rotterdam Balkema pp. 67-72.
15. Hill RB, (1993) Comparative physiology of echinoderm muscle. In: Jangoux M, Lawrence JM, editors. Echinoderm Studies 4 Rotterdam Balkema pp. 81-109.
16. Candia Carnevali MD, Lanzavecchia G, Melone G, Celentano FC, Andrietti F, (1988) Aristotle's lantern in the regular sea urchin Paracentrotus lividus. II. Biomechanical approach to the interpretation of movement. In: Burke RD, Mladenov PV, Lambert P, Parsley R, editors. Echinoderm Biology Rotterdam Balkema pp. 663-672.
17. Andrietti F, Candia Carnevali MD, Wilkie IC, Lanzavecchia G, Melone G, et al. (1990) Mechanical analysis of the sea-urchin lantern: the overall system in Paracentrotus lividus. J Zool 220: 345-366.
18. Andrietti F, Candia Carnevali MD, Wilkie IC, (1992) Mechanical analysis of the lantern movement in the cidarid sea-urchin Stylocidaris affinis (Phil.): comparison with a typical camarodont lantern. In: Scalera-Liaci L, Canicatti C, editors. Echinoderm Research 1991 Rotterdam Balkema pp. 95-98.
19. Wilkie IC, Candia Carnevali MD, Bonasoro F, (1998) Organization and mechanical behaviour of myocyte-ligament composites in a sea-urchin lantern: the compass depressors of Stylocidaris affinis (Echinodermata, Echinoida). Zoomorphology 118: 87-101.
20. Wilkie IC, Candia Carnevali MD, Andrietti F, (1998) Mechanical properties of sea-urchin lantern muscles: a comparative investigation of intact muscle groups in Paracentrotus lividus (Lam.) and Stylocidaris affinis (Phil.) (Echinodermata, Echinoidea). J Comp Phys B 168: 204-212.
21. Wilkie IC, Candia Carnevali MD, Bonasoro F, (1992) The compass depressors of Paracentrotus lividus (Echinodermata, Echinoida): ultrastructural and mechanical aspects of their variable tensility and contractility. Zoomorphology 112: 143-153.
22. McKew M, Wilkie IC, (1999) Organisation and pharmacology of the compass elevator muscles of the sea-urchin Echinus esculentus L. In: Candia Carnevali MD, Bonasoro F, editors. Echinoderm Research 1998 Rotterdam Balkema pp. 103-108.
23. Ellers O, Telford M, (1997) Muscles advance the teeth in sand dollars and other sea urchins. P Roy Soc Lond B Bio 264: 1525-1530.
24. Telford M, Ellers O, (1997) Tooth advancement muscles in the sand dollar Echinarachnius parma. Invertebr Biol 116: 255-261.
25. Wilkie IC, (1996) Mutable collagenous tissues: extracellular matrix as mechano-effector. In: Jangoux M, Lawrence JM, editors. Echinoderm Studies 5 Rotterdam Balkema pp. 61-102.
26. Wilkie IC, (2002) Is muscle involved in the mechanical adaptability of echinoderm mutable collagenous tissue? J Exp Biol 205: 159-165.
27. Ribeiro AR, Barbaglio A, Benedetto CD, Ribeiro CC, Wilkie IC, et al. (2011) New insights into mutable collagenous tissue: correlations between the microstructure and mechanical state of a sea-urchin ligament. PLoS ONE 6: e24822.
28. Buchanan JB, (1969) Feeding and the control of volume within the tests of regular sea-urchins. J Zool 159: 51-64.
29. Stauber M, (1993) The lantern of Aristotle: organization of its coelom and origin of its muscles (Echinodermata, Echinoida). Zoomorphology 113: 137-151.
30. Cavey MJ, Märkel K, (1994) Echinoidea. In: Harrison FW, Chia FS, editors. Microscopic Anatomy of Invertebrates, Volume 14: Echinodermata New York Wiley-Liss pp. 345-400.
31. Stauber M, Märkel K, (1988) Comparative morphology of muscle-skeleton attachments in the Echinodermata. Zoomorphology 108: 137-148.
32. Märkel K, Röser U, Stauber M, (1990) The interpyramidal muscle of Aristotle's lantern: its myoepithelial structure and its growth. Zoomorphology 109: 251-262.
33. Cobb JLS, Laverack MS, (1966) The lantern of Echinus esculentus (L.). I. Gross anatomy and physiology. P Roy Soc Lond B Bio 164: 624-640.
34. Wilkie IC, Candia Carnevali MD, Bonasoro F, (2000) A spicule-reinforced contractile mesentery: organisation and mechanical behaviour of the exterior coelomic septum of Stylocidaris affinis (Echinodermata, Echinoida). Zoomorphology 120: 119-133.
35. Candia Carnevali MD, Bonasoro F, Andrietti F, Melone G, Wilkie IC, (1990) Functional morphology of the peristomial membrane of regular sea-urchins: structural organization and mechanical properties in Paracentrotus lividus. In: De Ridder C, Dubois P, Lahaye MC, Jangoux M, editors. Echinoderm Research Rotterdam Balkema pp. 207-216.
36. Wilkie IC, Candia Carnevali MD, Andrietti F, (1993) Variable tensility of the peristomial membrane of the sea-urchin Paracentrotus lividus (Lamarck). Comp Biochem Phys A 105: 493-501.
37. Wilkie IC, Candia Carnevali MD, Andrietti F, (1994) Microarchitecture and mechanics of the sea-urchin peristomial membrane. Boll Zool 61: 39-51.
38. Bonasoro F, Candia Carnevali MD, Wilkie IC, (1995) The peristomial membrane of regular sea-urchins: functional morphology of the epidermis and coleomic lining in Paracentrotus lividus (Lamarck). B Zool 62: 121-135.
39. Lavallard R, Schlenz R, Balas G, (1965) Structures et ultrastructures du muscle protracteur de l'appareil masticateur chez Echinometra lucunter, L. Bol Fac Filos Cien Let Univ São Paulo Zool 25: 133-174.
40. Saita A, (1969) La morfologia ultrastrutturale dei muscoli della "Lanterna di Aristotele" di alcuni echinoidi. Rend Sci Ist Lomb B 103: 297-313.
41. Dolmatov IY, Mashanov VS, Zueva OR, (2007) Derivation of muscles of the Aristotle's lantern from coelomic epithelia. Cell Tissue Res 327: 371-384.
42. Meyer-Rochow VB, Fraile B, Paniagua R, Royuela M, (2003) First immunocytochemical study of echinoderm smooth muscle: the Antarctic cushionstar Odontaster validus Koehler (Echinodermata, Asteroidea). Protoplasma 220: 227-232.
43. Elphick M, Melarange R, (2001) Neural control of muscle relaxation in echinoderms. J Exp Biol 204: 875-885.
44. Cobb JLS, (1968) Observations on the electrical activity within the retractor muscles of the lantern of Echinus esculentus using extracellular recording electrodes. Comp Biochem Physiol 24: 311-315.
45. Boltt RE, Ewer DW, (1963) Studies on the myoneural physiology of Echinodermata. IV. The lantern retractor muscle of Parechinus: responses to stimulation by light. J Exp Biol 40: 713-726.
46. Cobb JLS, Laverack MS, (1966) The lantern of Echinus esculentus (L.). II. Fine structure of hyponeural tissue and its connexions. P Roy Soc Lond B Bio 164: 641-650.
47. Cobb JLS, Laverack MS, (1966) The lantern of Echinus esculentus (L.). III. The fine structure of the lantern retractor muscle and its innervation. P Roy Soc Lond B Bio 164: 651-658.
48. Birenheide R, Motokawa T, (1996) To be stiff or to be soft- the dilemma of the echinoid tooth ligament. I. Morphology. Biol Bull 190: 218-230.
49. Ziegler A, Ogurreck M, Steinke T, Beckmann F, Prohaska S, et al. (2010) Opportunities and challenges for digital morphology. Biol Direct 5: 45.
50. Ziegler A, Mueller S, (2011) Analysis of freshly fixed and museum invertebrate specimens using high-resolution, high-throughput MRI. Method Mol Biol 771: 633-651.
51. Ziegler A, Faber C, Mueller S, Bartolomaeus T, (2008) Systematic comparison and reconstruction of sea urchin (Echinoidea) internal anatomy: a novel approach using magnetic resonance imaging. BMC Biol 6: 33.
52. Ziegler A, Faber C, Bartolomaeus T, (2009) Comparative morphology of the axial complex and interdependence of internal organ systems in sea urchins (Echinodermata: Echinoidea). Front Zool 6: 10.
53. Ziegler A, Mooi R, Rolet G, De Ridder C, (2010) Origin and evolutionary plasticity of the gastric caecum in sea urchins (Echinodermata: Echinoidea). BMC Evol Biol 10: 313.
54. Ziegler A, (2013) Broad application of non-invasive imaging techniques to echinoids and other echinoderm taxa. In: Reich M, Kroh A, editors. Proceedings of the 7th European Conference on Echinoderms. Lecture Notes Proceedings Heidelberg Springer In press.
55. Hawkins HL, (1934) The lantern and girdle of some recent and fossil Echinoidea. Philos T Roy Soc B 223: 617-649.
56. Strenger A, (1973) Sphaerechinus granularis, Violetter Seeigel. Anleitung zur makroskopischen und mikroskopischen Untersuchung. Grosses Zoologisches Praktikum 18e Stuttgart Gustav Fischer.
57. Hamann O, (1887) Beiträge zur Histologie der Echinodermen. Anatomie und Histologie der Echiniden und Spatangiden. Jen Z Naturwiss 21: 87-266.
58. Ziegler A, Kunth M, Mueller S, Bock C, Pohmann R, et al. (2011) Application of magnetic resonance imaging in zoology. Zoomorphology 130: 227-254.
59. Holland ND, Ghiselin MT, (2009) Magnetic resonance imaging (MRI) has failed to distinguish between smaller gut regions and larger haemal sinuses in sea urchins (Echinodermata: Echinoidea). BMC Biol 7: 39.
60. Smith AB, (1980) Stereom microstructure of the echinoid test. Spec Pap Palaeontol 25: 1-80.
61. Smith AB, (1990) Biomineralization in echinoderms. In: Carter JG, editors. Skeletal biomineralization: patterns, processes and trends. Volume I New York Van Nostrand Reinhold pp. 413-443.
62. De Ridder C, Lawrence JM, (1982) Food and feeding mechanisms: Echinoidea. In: Jangoux M, Lawrence JM, editors. Echinoderm nutrition Rotterdam Balkema pp. 57-115.
63. Grünbaum H, Bergman G, Abbott DP, Ogden JC, (1978) Intraspecific agonistic behavior in the rock-boring sea urchin Echinometra lucunter (L.) (Echinodermata: Echinoidea). B Mar Sci 28: 181-188.
64. Asgaard U, Bromley RG, (2008) Echinometrid sea urchins, their trophic styles and corresponding bioerosion. In: Wisshak M, Tapanila L, editors. Current Developments in Bioerosion Heidelberg Springer pp. 279-303.
65. Mortensen T, (1943) A monograph of the Echinoidea. III. 2 Camarodonta. I. Orthopsidae, Glyphocyphidae, Temnopleuridae, and Toxopneustidae Copenhagen Reitzel.
66. Mortensen T, (1943) A monograph of the Echinoidea. III. 3 Camarodonta. II. Echinidae, Strongylocentrotidae, Parasaleniidae, Echinometridae Copenhagen Reitzel.
67. Kroh A, Smith AB, (2010) The phylogeny and classification of post-Palaeozoic echinoids. J Syst Palaeontol 8: 147-212.
68. Märkel K, (1979) Structure and growth of the cidaroid socket-joint lantern of Aristotle compared to the hinge-joint lanterns of non-cidaroid regular echinoids (Echinodermata, Echinoidea). Zoomorphology 94: 1-32.
69. Binyon J, (1972) Physiology of echinoderms Oxford Pergamon Press.
70. Farmanfarmaian A, (1966) The respiratory physiology of echinoderms. In: Boolootian RA, editors. Physiology of Echinodermata New York Interscience Publishers pp. 245-265.
71. Hanson JL, Gust G, (1986) Circulation of perivisceral fluid in the sea urchin Lytechinus variegatus. Mar Biol 92: 125-134.
72. Lawrence JM, (2001) Function of eponymous structures in echinoderms: a review. Can J Zool 79: 1251-1264.
73. Kier PM, (1974) Evolutionary trends and their functional significance in the post-Paleozoic echinoids. Palaeontol Soc Mem 5: 1-95.
74. Cobb JLS, Sneddon E, (1977) An ultra-structural study of the gills of Echinus esculentus. Cell Tissue Res 182: 265-274.
75. Littlewood DTJ, Smith AB, (1995) A combined morphological and molecular phylogeny for sea urchins (Echinoidea: Echinodermata). Philos T Roy Soc B 347: 213-234.
76. Littlewood DTJ, Smith AB, Clough KA, Emson RH, (1997) The interrelationships of the echinoderm classes: morphological and molecular evidence. Biol J Linn Soc 61: 409-438.
77. Smith AB, Pisani D, Mackenzie-Dodds JA, Stockley B, Webster BL, et al. (2006) Testing the molecular clock: molecular and paleontological estimates of divergence times in the Echinoidea (Echinodermata). Mol Biol Evol 23: 1832-1851.
78. Janies DA, Voight JR, Daly M, (2011) Echinoderm phylogeny including Xyloplax, a progenetic asteroid. Syst Biol 60: 420-438.
79. Emig CC, (1974) The systematics and evolution of the phylum Phoronida. Z Zool Syst Evol 12: 128-151.
80. Emig CC, (1985) Phylogenetic systematics in Phoronida (Lophophorata). Z Zool Syst Evol 23: 184-193.
81. Temereva EN, Malakhov VV, Yushin VV, (2001) Histology and ultrastructure of the body wall in the phoronid Phoronopsis harmeri. Russ J Mar Biol 27: 156-167.
82. Leydig F, (1854) Kleinere Mittheilungen zur thierischen Gewebelehre. In: Müller J, editors. Archiv für Anatomie, Physiologie und wissenschaftliche Medicin Berlin Veit et Compagnie pp. 296-348.
83. Kroh A, Mooi R, (2012) World Echinoidea Database. Available: http://marinespecies.org/echinoidea. Accessed 2012 Apr 27.