Zoomorphology

, Volume 127, Issue 3, pp 143–159

Muscular systems in gymnolaemate bryozoan larvae (Bryozoa: Gymnolaemata)

Original Paper

Abstract

Gymnolaemate bryozoan species exhibit larval forms that can either be planktotrophic cyphonautes or one of the several types of lecithotrophic larvae. Due to the lack of both a phylogenetic system of the Bryozoa and detailed information about larval morphology for many species, it is difficult to elaborate hypotheses about the evolution of larval forms in this group at the moment. In this study, phalloidin staining and confocal laser scanning microscopy are used to provide detailed morphological descriptions of the three-dimensional structure of muscular systems in the larvae of Flustrellidra hispida, Alcyonidium gelatinosum, Membranipora membranacea, Bugula fulva and Bowerbankia gracilis. A comparison to the available data from the literature is added. The results show muscular systems to be much more complex than previously recognized. In all but one species, an anterior median muscle inserts with one end at the basal side of the apical organ and with its other end at the papilla of the pyriform organ. This muscle can be paired or unpaired and was referred to as “neuromuscular strand” in earlier descriptions. All species except Bugula fulva exhibit a coronal ring muscle running concentric to the larva’s main locomotory ciliary band. Lateral muscle strands that connect the pallial epithelium to either the corona or oral epithelium are found mainly in the cyphonautes and pseudocyphonautes larvae and, in modified shape though, also in some coronate larvae. Transversal or shell adductor muscles can be shown to co-occur with lateral muscles and possibly originate from the same source. The findings are in accordance with the idea of a multiple origin of lecithotrophic forms within gymnolaemate Bryozoa.

Keywords

Bryozoa Gymnolaemata Larva Musculature Morphology Evolution 

References

  1. Atkins D (1955) The cyphonautes larvae of the Plymouth area and the metamorphosis of Membranipora membranacea. J Marine Biol Assoc UK 34:441–449CrossRefGoogle Scholar
  2. Barrois J (1877) Recherches sur l’ embryologie des Bryozoaires. Travaux de l’institut zoologique de Lille Fasc. 1:1–307 + 16 plsGoogle Scholar
  3. Boardman RS, Cheetham AH, Blake DB, Utgaard J, Karklins OL, Cook PL, Sandberg PA, Lutaud G, Wood TS (1983) Bryozoa. Treatise on invertebrate palaeontology, part G. Geological Society of America and University of Kansas Press, KansasGoogle Scholar
  4. Braem F (1897) Die geschlechtliche Entwicklung von Plumatella fungosa. Zoologica 10:1–96Google Scholar
  5. Braem F (1908) Die geschlechtliche Entwicklung von Fredericella sultana. Zoologica 52:1–37Google Scholar
  6. Calvet L (1900) Contribution à l’histoire naturelle des bryozoaires ectoproctes marins. Trav Inst Zool Univ Montpellier 8:1–488Google Scholar
  7. de Pinna MCC (1991) Concepts and tests of homology in the cladistic paradigm. Cladistics 7:367–394CrossRefGoogle Scholar
  8. d`Hondt JL (1973a) La musculature de la larve d’Alcyonidium polyoum (Hassall), Bryozoaire Cténostome. Comparaison avec la musculature larvaire d’autres Bryozoaires Eurystomes. C R Acad Sci (Paris) Ser D 276:1449–1452Google Scholar
  9. d`Hondt JL (1973b) Etude anatomique, histologique, et cytologique de la larve d’Alcyonidium polyoum (Hassal, 1841). Arch Zool Exp Gén 114:537–602Google Scholar
  10. d`Hondt JL (1975) La metamorphose larvaire et la realisation du “cystide” chez Alcyonidium polyoum (Hassal 1841). Arch Zool Exp Gén 115:577–605Google Scholar
  11. d`Hondt JL (1977a) Structure larvaire et histogenèse post-larvaire chez Crisia denticulata (Lamarck) (Bryozoa, Cyclostomata, Articulata). Zool Scr 6:55–60CrossRefGoogle Scholar
  12. d`Hondt JL (1977b) Structure larvaire et histogenese postlarvaire chez Bowerbankia imbricata (Adams 1798). Arch Zool Exp Gén 118:211–243Google Scholar
  13. d`Hondt JL (1977c) Larval structure and post-larval organogenesis of Flustrellidra hispida (Fabricius, 1780), Bryozoa, Ctenostomata. Zoomorphologie 87:165–189CrossRefGoogle Scholar
  14. Ernst A, Schäfer P (2006) Palaeozoic vs. post-palaeozoic Stenolaemata: phylogenetic relationship or morphological convergence? Courier Forsch -Inst Senckenberg 257:49–63Google Scholar
  15. Franzén Å, Sensenbaugh T (1983) Fine structure of the apical plate in the larva of the freshwater Bryozoan Plumatella fungosa (Pallas) (Bryozoa: Phylactolaemata). Zoomorphology 102:87–98CrossRefGoogle Scholar
  16. Fuchs J, Bright M, Funch P, Wanninger A (2006) Immunocytochemistry of the neuromuscular systems of Loxosomella vivipara and L. parguerensis (Entoprocta: Loxosomatidae). J Morphol 267:866–883PubMedCrossRefGoogle Scholar
  17. Haszprunar G, Wanninger A (2000) Molluscan muscle systems in development and evolution. J Zool Syst Evol Res 38:157–163CrossRefGoogle Scholar
  18. Haszprunar G, Wanninger A (2008) On the fine structure of the creeping larva of Loxosomella murmanica: additional evidence for a clade of Kamptozoa (Entoprocta) and Mollusca. Acta Zool (in press)Google Scholar
  19. Hayward PJ (1985) Ctenostome bryozoans. Brill/Backhuys, LondonGoogle Scholar
  20. Hayward PJ, Ryland JS (1998) Cheilostomatous bryozoa. Field Studies Council, ShrewsburyGoogle Scholar
  21. Hill SD, Boyer BC (2001) Phalloidin labeling of developing muscle in embryos of the polychaete Capitella sp I. Biol Bull 201:257–258PubMedCrossRefGoogle Scholar
  22. Jenner RA, Schram FR (1999) The grand game of metazoan phylogeny: rules and strategies. Biol Rev 74:121–142CrossRefGoogle Scholar
  23. Kupelwieser H (1905) Untersuchungen über den feineren Bau und die Metamorphose des Cyphonautes. Zoologica 47:1–50Google Scholar
  24. Lacalli TC, West JE (1985) The nervous-system of a pilidium larva—evidence from electron-microscope reconstructions. Can J Zool 63:1909–1916CrossRefGoogle Scholar
  25. Leasi F, Rothe BH, Schmidt-Rhaesa A, Todaro MA (2006) The musculature of three species of gastrotrichs surveyed with confocal laser scanning microscopy (CLSM). Acta Zool 87:171–180CrossRefGoogle Scholar
  26. Marcus E (1926) Sinnesphysiologie und Nervensystem der Larve von Plumatella fungosa (Pall.). Verh Dtsch Zool Ges 31:86–90Google Scholar
  27. McDougall C, Chen WC, Shimeld SM, Ferrier DE (2006) The development of the larval nervous system, musculature and ciliary bands of Pomatoceros lamarckii (Annelida): heterochrony in polychaetes. Front Zool 3:16PubMedCrossRefGoogle Scholar
  28. McKinney FK, Jackson JBC (1989) Bryozoan life histories. In: Bryozoan evolution. Unwin Hyman, Boston, pp 97–118Google Scholar
  29. Müller MCM, Worsaae K (2005) CLSM Analysis of the phalloidin-stained muscle system in Nerilla antennata, Nerillidium sp. and Trochonerilla mobilis (Polychaeta; Nerillidae). J Morphol 267:885–896CrossRefGoogle Scholar
  30. Nielsen C (1970) On metamorphosis and ancestrula formation in cylostomatous bryzoans. Ophelia 7:217–256Google Scholar
  31. Nielsen C (1971) Entoproct life-cycles and the entoproct/ectoproct relationship. Ophelia 9:209–341Google Scholar
  32. Nielsen C, Haszprunar G, Ruthensteiner B, Wanninger A (2007) Early development of the aplacophoran mollusc Chaetoderma. Acta Zool 88:231–247CrossRefGoogle Scholar
  33. Pace RM (1906) On the early stages in the development of Flustrella hispida (Fabricius), and on the existence of a -yolk nucleus- in the egg of this form. Q J Microsc Sci 50:435–478 + 4 plsGoogle Scholar
  34. Passamaneck YJ, Halanych KM (2004) Evidence from Hox genes that bryozoans are lophotrochozoans. Evol Dev 6:275–281PubMedCrossRefGoogle Scholar
  35. Passamaneck YJ, Halanych KM (2006) Lophotrochozoan phylogeny assessed with LSU and SSU data: evidence of lophophorate polyphyly. Mol Phylogenet Evol 40:20–28PubMedCrossRefGoogle Scholar
  36. Philippe H, Lartillot N, Brinkmann H (2005) Multigene analyses of bilaterian animals corroborate the monophyly of Ecdysozoa, Lophotrochozoa and Protostomia. Mol Biol Evol 22:1246–1253PubMedCrossRefGoogle Scholar
  37. Prouho H (1890) Recherches sur la larve de Flustrellidra hispida: Structure et metamorphose. Arch Zool Exp Gén 8(2. Ser.):409–459Google Scholar
  38. Prouho H (1892) Conribution a l’histoire des bryozoaires. Arch Zool Exp Gén 10(2.Ser.):557–656Google Scholar
  39. Purschke G, Müller MCM (2006) Evolution of body wall musculature. Integr Comp Biol 46:497–507CrossRefGoogle Scholar
  40. Reed CG (1980) The reproductive biology, larval morphology, and metamorphosis of the marine bryozoan, Bowerbankia gracilis (Vesicularioidea, Ctenostomata). PhD Thesis, University of Washington, Seattle, WA, USAGoogle Scholar
  41. Reed CG (1985) The many motors of morphogenesis. The roles of muscles, cilia, and microfilaments in the metamorphosis of marine bryozoans. In: Sawyer RH, Showman RM (eds) The cellular and molecular biology of invertebrate development. University of South Carolina Press, Columbia, pp 197–219Google Scholar
  42. Reed CG (1991) Bryozoa. In: Giese AC, Pearse JS, Pearse VB (eds) Reproduction of marine invertebrates VI echinoderms and lophophorates. Boxwood Press, Pacific Groove, pp 85–245Google Scholar
  43. Reed CG, Cloney RA (1982a) The larval morphology of the marine bryozoan Bowerbankia gracilis (Ctenostomata: Vesicularioidea). Zoomorphology 100:23–54CrossRefGoogle Scholar
  44. Reed CG, Cloney RA (1982b) The settlement and metamorphosis of the marine bryozoan Bowerbankia gracilis (Ctenostomata: Vesicularioidea). Zoomorphology 101:103–132CrossRefGoogle Scholar
  45. Reed CG, Woollacott RM (1982) Mechanisms of rapid morphogenetic movements in the metamorphosis of the bryozoan Bugula neritina (Cheilostomata, Cellularioidea) I. Attachment to the substratum. J Morphol 172:335–348CrossRefGoogle Scholar
  46. Reed CG, Woollacott RM (1983) Mechanisms of rapid morphogenetic movements in the metamorphosis of the bryozoan Bugula neritina (Cheilostomata, Cellularioidea) II. The role of dynamic assembages of microfilaments in the pallial epithelium. J Morphol 177:127–143CrossRefGoogle Scholar
  47. Repiachoff W (1878) Zur Embryologie der Bowerbankia. Zool Anz 1–4Google Scholar
  48. Rogick M (1939) Studies on fresh-water Bryozoa VIII. Larvae of Hyalinella punctata Trans Am Microsc Soc 58: 199–209CrossRefGoogle Scholar
  49. Ryland JS, Porter JS (2003) The identity of Alcyonidium gelatinosum (Linnaeus, 1761) (Bryozoa : Ctenostomatida). J Nat Hist 37:2179–2189CrossRefGoogle Scholar
  50. Ryland JS, Porter JS (2006) The identification, distribution and biology of encrusting species of Alcyonidium (Bryozoa, Ctenostomatida) around the coast of Ireland. Biol Environ 106B:19–33Google Scholar
  51. Santagata S, Zimmer RL (2002) Comparison of the neuromuscular systems among actinotroch larvae: systematic and evolutionary implications. Evol Dev 4:43–55PubMedCrossRefGoogle Scholar
  52. Santagata S (2008) The morphology and evolutionary significance of the ciliary fields and musculature among marine bryozoan larvae. J Morph (in press)Google Scholar
  53. Schmidt-Rhaesa A (2007) The evolution of organ systems. Oxford University Press, New YorkGoogle Scholar
  54. Schmidt-Rhaesa A, Kulessa J (2007) Muscular architecture of Milnesium tardigradum and Hypsibius sp. (Eutardigrada, Tardigrada) with some data on Ramazottius oberhaeuseri. Zoomorphology 126:265–281CrossRefGoogle Scholar
  55. Seeliger O (1906) Über die Larven und Verwandschaftsbeziehungen der Bryozoen. Z Wiss Zool 84:1–78Google Scholar
  56. Strathmann RR (1978) The evolution and loss of feeding larval stages of marine invertebrates. Evolution 32:894–906CrossRefGoogle Scholar
  57. Stricker SA (1988) Metamorphosis of the marine bryozoan Membranipora membranacea: an ultrastructural study of rapid morphogenetic movements. J Morphol 196:53–72CrossRefGoogle Scholar
  58. Stricker SA, Reed CG, Zimmer RL (1988a) The cyphonautes larva of the marine bryozoan Membranipora membranacea. I. General morphology, body wall, and gut. Can J Zool 66:368–383Google Scholar
  59. Stricker SA, Reed CG, Zimmer RL (1988b) The cyphonautes larva of the marine bryozoan Membranipora membranacea. II. Internal sac, musculature, and pyriform organ. Can J Zool 66:384–398Google Scholar
  60. Ström R (1977) Brooding patterns of bryozoans. In: Woollacott RM, Zimmer RL (eds) Biology of bryozoans. Academic Press, New York, pp 23–55Google Scholar
  61. Taylor PD (1988) Major radiations of Cheilostome Bryozoans: triggered by a new larval type? Hist Biol 1:45–64Google Scholar
  62. Temkin MH (1994) Gamete spawning and fertilization in the gymnolaemate bryozoan Membranipora membranacea. Biol Bull 187:143–155PubMedCrossRefGoogle Scholar
  63. Temkin MH (1996) Comparative fertilization biology of gymnolaemate bryozoans. Mar Biol 127:329–339CrossRefGoogle Scholar
  64. Todd JA (2000) The central role of ctenostomes in bryozoan phylogeny. In: Herrera-Cubilla A, Jackson JBC (eds) Proceedings of the 11th International Bryozoology Association conference. Smithsonian Tropical Research Institute, Balboa, pp 105–135Google Scholar
  65. Waeschenbach A, Telford MJ, Porter JS, Littlewood DTJ (2006) The complete mitochondrial genome of Flustrellidra hispida and the phylogenetic position of Bryozoa among the Metazoa. Mol Phylogenet Evol 40:195–207PubMedCrossRefGoogle Scholar
  66. Wanninger A (2004) Myo-anatomy of juvenile and adult loxosomatid entoprocta and the use of muscular body plans for phylogenetic inferences. J Morphol 261:249–257PubMedCrossRefGoogle Scholar
  67. Wanninger A, Haszprunar G (2002) Chiton myogenesis: perspectives for the development and evolution of larval and adult muscle systems in molluscs. J Morphol 251:103–113PubMedCrossRefGoogle Scholar
  68. Wanninger A, Koop D, Bromham L, Noonan E, Degnan BM (2005) Nervous and muscle system development in Phascolion strombus (Sipuncula). Dev Genes Evol 215:509–518PubMedCrossRefGoogle Scholar
  69. Wanninger A, Ruthensteiner B, Lobenwein S, Salvenmoser W, Dictus WJAG, Haszprunar G (1999) Development of the musculature in the limpet Patella (Mollusca, Patellogastropoda). Dev Genes Evol 209:226–238PubMedCrossRefGoogle Scholar
  70. Zimmer RL, Woollacott RM (1977) Structure and classification of gymnolaemate larvae. In: Woollacott RM, Zimmer RL (eds) Biology of bryozoans. Academic Press, New York, pp 57–89Google Scholar
  71. Zimmer RL, Woollacott RM (1989) Larval morphology of the bryozoan Watersipora arcuata (Cheilostomata: Ascophora). J Morphol 199:125–150CrossRefGoogle Scholar
  72. Zimmer RL, Woollacott RM (1993) Anatomy of the larva of Amathia vidovici (Bryozoa: Ctenostomata) and phylogenetic significance of vesiculariform larva. J Morphol 215:1–29CrossRefGoogle Scholar
  73. Zimmer RL, Reed CG (1994) Morphology and ultrastructure of the larva of the bryozoan Tanganella muelleri (Ctenostomata: Victorellidae). In: Wilson WH (ed) Reproduction and development of marine invertebrates: papers from a symposium held at Friday Harbor Laboratories of the University of Washington, 9–11 June. Johns Hopkins University Press, Baltimore, pp 224–245Google Scholar

Copyright information

© Springer-Verlag 2008

Authors and Affiliations

  1. 1.Systematik und Evolution der Tiere, Institut für Biologie Freie Universität BerlinBerlinGermany

Personalised recommendations