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.
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References
Atkins D (1955) The cyphonautes larvae of the Plymouth area and the metamorphosis of Membranipora membranacea. J Marine Biol Assoc UK 34:441–449
Barrois J (1877) Recherches sur l’ embryologie des Bryozoaires. Travaux de l’institut zoologique de Lille Fasc. 1:1–307 + 16 pls
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, Kansas
Braem F (1897) Die geschlechtliche Entwicklung von Plumatella fungosa. Zoologica 10:1–96
Braem F (1908) Die geschlechtliche Entwicklung von Fredericella sultana. Zoologica 52:1–37
Calvet L (1900) Contribution à l’histoire naturelle des bryozoaires ectoproctes marins. Trav Inst Zool Univ Montpellier 8:1–488
de Pinna MCC (1991) Concepts and tests of homology in the cladistic paradigm. Cladistics 7:367–394
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 276:1449–1452
d`Hondt JL (1973b) Etude anatomique, histologique, et cytologique de la larve d’Alcyonidium polyoum (Hassal, 1841). Arch Zool Exp Gén 114:537–602
d`Hondt JL (1975) La metamorphose larvaire et la realisation du “cystide” chez Alcyonidium polyoum (Hassal 1841). Arch Zool Exp Gén 115:577–605
d`Hondt JL (1977a) Structure larvaire et histogenèse post-larvaire chez Crisia denticulata (Lamarck) (Bryozoa, Cyclostomata, Articulata). Zool Scr 6:55–60
d`Hondt JL (1977b) Structure larvaire et histogenese postlarvaire chez Bowerbankia imbricata (Adams 1798). Arch Zool Exp Gén 118:211–243
d`Hondt JL (1977c) Larval structure and post-larval organogenesis of Flustrellidra hispida (Fabricius, 1780), Bryozoa, Ctenostomata. Zoomorphologie 87:165–189
Ernst A, Schäfer P (2006) Palaeozoic vs. post-palaeozoic Stenolaemata: phylogenetic relationship or morphological convergence? Courier Forsch -Inst Senckenberg 257:49–63
Franzén Å, Sensenbaugh T (1983) Fine structure of the apical plate in the larva of the freshwater Bryozoan Plumatella fungosa (Pallas) (Bryozoa: Phylactolaemata). Zoomorphology 102:87–98
Fuchs J, Bright M, Funch P, Wanninger A (2006) Immunocytochemistry of the neuromuscular systems of Loxosomella vivipara and L. parguerensis (Entoprocta: Loxosomatidae). J Morphol 267:866–883
Haszprunar G, Wanninger A (2000) Molluscan muscle systems in development and evolution. J Zool Syst Evol Res 38:157–163
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)
Hayward PJ (1985) Ctenostome bryozoans. Brill/Backhuys, London
Hayward PJ, Ryland JS (1998) Cheilostomatous bryozoa. Field Studies Council, Shrewsbury
Hill SD, Boyer BC (2001) Phalloidin labeling of developing muscle in embryos of the polychaete Capitella sp I. Biol Bull 201:257–258
Jenner RA, Schram FR (1999) The grand game of metazoan phylogeny: rules and strategies. Biol Rev 74:121–142
Kupelwieser H (1905) Untersuchungen über den feineren Bau und die Metamorphose des Cyphonautes. Zoologica 47:1–50
Lacalli TC, West JE (1985) The nervous-system of a pilidium larva—evidence from electron-microscope reconstructions. Can J Zool 63:1909–1916
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 87:171–180
Marcus E (1926) Sinnesphysiologie und Nervensystem der Larve von Plumatella fungosa (Pall.). Verh Dtsch Zool Ges 31:86–90
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 3:16
McKinney FK, Jackson JBC (1989) Bryozoan life histories. In: Bryozoan evolution. Unwin Hyman, Boston, pp 97–118
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 267:885–896
Nielsen C (1970) On metamorphosis and ancestrula formation in cylostomatous bryzoans. Ophelia 7:217–256
Nielsen C (1971) Entoproct life-cycles and the entoproct/ectoproct relationship. Ophelia 9:209–341
Nielsen C, Haszprunar G, Ruthensteiner B, Wanninger A (2007) Early development of the aplacophoran mollusc Chaetoderma. Acta Zool 88:231–247
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 pls
Passamaneck YJ, Halanych KM (2004) Evidence from Hox genes that bryozoans are lophotrochozoans. Evol Dev 6:275–281
Passamaneck YJ, Halanych KM (2006) Lophotrochozoan phylogeny assessed with LSU and SSU data: evidence of lophophorate polyphyly. Mol Phylogenet Evol 40:20–28
Philippe H, Lartillot N, Brinkmann H (2005) Multigene analyses of bilaterian animals corroborate the monophyly of Ecdysozoa, Lophotrochozoa and Protostomia. Mol Biol Evol 22:1246–1253
Prouho H (1890) Recherches sur la larve de Flustrellidra hispida: Structure et metamorphose. Arch Zool Exp Gén 8(2. Ser.):409–459
Prouho H (1892) Conribution a l’histoire des bryozoaires. Arch Zool Exp Gén 10(2.Ser.):557–656
Purschke G, Müller MCM (2006) Evolution of body wall musculature. Integr Comp Biol 46:497–507
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, USA
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 197–219
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 85–245
Reed CG, Cloney RA (1982a) The larval morphology of the marine bryozoan Bowerbankia gracilis (Ctenostomata: Vesicularioidea). Zoomorphology 100:23–54
Reed CG, Cloney RA (1982b) The settlement and metamorphosis of the marine bryozoan Bowerbankia gracilis (Ctenostomata: Vesicularioidea). Zoomorphology 101:103–132
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 172:335–348
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 177:127–143
Repiachoff W (1878) Zur Embryologie der Bowerbankia. Zool Anz 1–4
Rogick M (1939) Studies on fresh-water Bryozoa VIII. Larvae of Hyalinella punctata Trans Am Microsc Soc 58: 199–209
Ryland JS, Porter JS (2003) The identity of Alcyonidium gelatinosum (Linnaeus, 1761) (Bryozoa : Ctenostomatida). J Nat Hist 37:2179–2189
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:19–33
Santagata S, Zimmer RL (2002) Comparison of the neuromuscular systems among actinotroch larvae: systematic and evolutionary implications. Evol Dev 4:43–55
Santagata S (2008) The morphology and evolutionary significance of the ciliary fields and musculature among marine bryozoan larvae. J Morph (in press)
Schmidt-Rhaesa A (2007) The evolution of organ systems. Oxford University Press, New York
Schmidt-Rhaesa A, Kulessa J (2007) Muscular architecture of Milnesium tardigradum and Hypsibius sp. (Eutardigrada, Tardigrada) with some data on Ramazottius oberhaeuseri. Zoomorphology 126:265–281
Seeliger O (1906) Über die Larven und Verwandschaftsbeziehungen der Bryozoen. Z Wiss Zool 84:1–78
Strathmann RR (1978) The evolution and loss of feeding larval stages of marine invertebrates. Evolution 32:894–906
Stricker SA (1988) Metamorphosis of the marine bryozoan Membranipora membranacea: an ultrastructural study of rapid morphogenetic movements. J Morphol 196:53–72
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 66:368–383
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 66:384–398
Ström R (1977) Brooding patterns of bryozoans. In: Woollacott RM, Zimmer RL (eds) Biology of bryozoans. Academic Press, New York, pp 23–55
Taylor PD (1988) Major radiations of Cheilostome Bryozoans: triggered by a new larval type? Hist Biol 1:45–64
Temkin MH (1994) Gamete spawning and fertilization in the gymnolaemate bryozoan Membranipora membranacea. Biol Bull 187:143–155
Temkin MH (1996) Comparative fertilization biology of gymnolaemate bryozoans. Mar Biol 127:329–339
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 105–135
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 40:195–207
Wanninger A (2004) Myo-anatomy of juvenile and adult loxosomatid entoprocta and the use of muscular body plans for phylogenetic inferences. J Morphol 261:249–257
Wanninger A, Haszprunar G (2002) Chiton myogenesis: perspectives for the development and evolution of larval and adult muscle systems in molluscs. J Morphol 251:103–113
Wanninger A, Koop D, Bromham L, Noonan E, Degnan BM (2005) Nervous and muscle system development in Phascolion strombus (Sipuncula). Dev Genes Evol 215:509–518
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 209:226–238
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 57–89
Zimmer RL, Woollacott RM (1989) Larval morphology of the bryozoan Watersipora arcuata (Cheilostomata: Ascophora). J Morphol 199:125–150
Zimmer RL, Woollacott RM (1993) Anatomy of the larva of Amathia vidovici (Bryozoa: Ctenostomata) and phylogenetic significance of vesiculariform larva. J Morphol 215:1–29
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 224–245
Acknowledgments
I am deeply grateful to Thomas Bartolomaeus (Berlin) for supporting my research as well as for advice and helpful discussions on the manuscript. Warm thanks also go to Björn Quast and Harald Hausen (Berlin) for numerous discussions and companionship in the lab, Anne Paasch (Berlin) for her support by translating french bryozoan papers, and Anja Jachmann (Helgoland) for her help with collecting animals. Suggestions by two anonymous reviewers substantially improved the manuscript.
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Gruhl, A. Muscular systems in gymnolaemate bryozoan larvae (Bryozoa: Gymnolaemata). Zoomorphology 127, 143–159 (2008). https://doi.org/10.1007/s00435-008-0059-3
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DOI: https://doi.org/10.1007/s00435-008-0059-3