[en] The larval development of Myzostoma cirriferum is described by means of SEM, TEM, and cLSM. It is similar to that of other myzostomids and includes three stages: the protrochophore, the trochophore, and the metatrochophore. The protrochophore is a ball-shaped larva present in culture from 18-48 h after egg laying. It has no internal organs and its body is made of three cell types: covering cells and ciliated cells that are external and surrounded by a cuticle, and resting cells that fill the blastocoel. The trochophore is a pear-shaped larva that develops 20-72 h after egg laying; the body includes the same three cell types as the previous stage. The metatrochophore is a pear-shaped larva that develops between 40 h and 14 days and is characterized by the presence of two bundles of four chaetae. When fully developed, the metatrochophore has a digestive system (made of a pharynx, an esophagus, and a blind digestive pouch), two pairs of protonephridia, and a nervous system composed of a supraesophageal ganglion, circumesophageal connectives, and dorsal and ventral nerves. Metamorphosis generally occurs 7 days after egg laying. At that time, the metatrochophore loses its chaetae and becomes pleated ventrally. This ultrastructural analysis suggests that chaetae and the five ventral longitudinal nerve cords of M. cirriferum metatrochophores are homologous structures to those observed in some polychaete trochophores. Coupled with recent phylogenetic analyses, where the Myzostomida are placed outside the Annelida, homologies between myzostomid and polychaete larvae support the view that a trochophore appeared early during the spiralian evolution
Disciplines :
Veterinary medicine & animal health
Author, co-author :
Eeckhaut, I.; Université de Mons-Hainaut - UMH > Marine Biology Laboratory, Natural Sciences Building
Fievez, Laurence ; Université de Liège - ULiège > Département de sciences fonctionnelles > GIGA-R : Biochimie et biologie moléculaire
Muller, M. C.; Universität Osnabrück, Osnabrück, Germany > Spezielle Zoologie, Fachbereich Biologie/Chemie
Language :
English
Title :
Larval development of Myzostoma cirriferum (Myzostomida)
Publication date :
2003
Journal title :
Journal of Morphology
ISSN :
0362-2525
eISSN :
1097-4687
Publisher :
Wiley Liss, Inc., New York, United States - New York
Volume :
258
Pages :
269-283
Peer reviewed :
Peer Reviewed verified by ORBi
Funders :
Fonds de la Recherche Scientifique (Communauté française de Belgique) - FNRS; Grant Number: 2.4.505.98.f
Åkesson B. 1962. The embryology of Tomopteris helgolandica (Polychaeta). Acta Zool 43:135-199.
Anderson DT. 1966. The comparative embryology of the Polychaeta. Acta Zool 47:1-42.
Bartolomaeus T. 1989. Larvale Nierenorgane bei Lepidochiton cinereus (Polyplacophora) und Aeolida papillosa (Gastropoda). Zoomorphology 109:15-32.
Bartolomaeus T. 1998. Head kidney in hatchlings of Scoloplos armiger (Annelida: Orbiniida): implications for the occurrence of protonephridia in lecithotrophic larvae. J Morphol 78:183-192.
Beard J. 1898. The sexual condition of Myzostoma glabrum (F.S. Leuckart). Mitt Zool Stat Neapel 13:293-324.
Budelmann BU, Schipp R, von Boletsky S. 1997. Cephalopoda. In: Harrison FW, Kohn AJ, editors. Microscopic anatomy of invertebrates, vol. 6A. Mollusca II. New York: John Wiley & Sons. p 119-414.
Bullock TH, Horridge GA. 1965. Structure and function in the nervous system of invertebrates, vol. I, II. San Francisco: Freeman.
Bristol CL. 1898. The metamerism of Nephelis. A contribution to the morphology of the nervous system, with a description of Nephelis lateralis. J Morphol 15:17-72.
Eeckhaut I. 1998. Mycomyzostoma calcidicola gen. nov., sp. nov., the first extant parasitic myzostome infesting crinoid stalks, with a nomenclatural appendix by M.J. Grygier. Species Diversity 3:89-103
Eeckhaut I, Jangoux M. 1992. Development and behaviour of Myzostoma alatum and Pulvinomyzostomum pulvinar, two myzostomid symbiotes of the comatulid Leptometra phalangium (Echinodermata). In: Scalera-Liaci L, Canicatti C, editors. Echinoderm research 1991. Rotterdam: Balkema. p 229-236.
Eeckhaut I, Jangoux M. 1993a. Life cycle and mode of infestation of Myzostoma cirriferum (Annelida), a symbiotic myzostomid of the comatulid crinoid Antedon bifida (Echinodermata). Dis Aquat Org 15:207-217.
Eeckhaut I, Jangoux M. 1993b. Integument and epidermal sensory structures of Myzostoma cirriferum (Myzostomida). Zoomorphology 113:33-46.
Eeckhaut I, McHugh D, Mardulyn P, Tiedemann R, Monteyne D, Jangoux M, Milinkovitch MC. 2000. Myzostomida: a link between trochozoans and flatworms? PRS London B 267:1383-1392.
Fauchald K, Rouse GW. 1997. Polychaete systematics: past and present. Zool Scr 26:71-138.
Fransen ME. 1980. Ultrastructure of coelomic organization in annelids. I. Archiannelids and other small polychaetes. Zoomorphologie 95:235-249.
Fransen ME. 1987. Coelomic and vascular systems. In: Westheide W, Hermans CO, editors. The ultrastructure of polychaeta. Stuttgart: Gustav Fischer, p 199-214.
Gardiner SL 1992. External anatomy. In: Harrison FW, Gardiner SL, editors. Microscopic anatomy of invertebrates, vol. 7. Annelida. New York: John Wiley & Sons, p 11-18.
Grygier MJ. 2000. Class Myzostomida. In: Beesley PL, Ross GJB, Glasby, editors. Polychaetes and allies: the southern synthesis. Fauna of Australia, vol. 4A. Polychaeta, Myzostomida, Pogonophora, Echiura, Sipuncula. Melbourne: CSIRO Publishing, p 297-330.
Gustus RM, Cloney RA. 1972. Ultrastructural similarities between setae of brachiopods and polychaetes. Acta Zool 53:229-233.
Hanström B. 1968. Vergleichende Anatomie des Nervensystems der wirbellosen Tiere. Amsterdam: Asher.
Haszprunar G. 1996. The Mollusca: coelomate turbellarians or mesenchymate annelids? In: Taylor JD, editor. Origin and evolutionary radiation of the Mollusca. Oxford: Oxford University Press, p 3-28
Hatschek B. 1878. Studien über Entwicklungsgeschichte der Anneliden. Ein Beitrag zur Morphologie der Bilaterien. Arbeiten aus dem Zoologischen Institute der Universität Wien und der Zoologischen Station in Triest 3:277-404.
Heimler W. 1987. Larvae. In: Westheide W, Hermans CO, editors. The ultrastructure of Polychaeta. Stuttgart: Gustav Fischer. p 353-372.
Jägersten G. 1936. Zur Kenntnis der Parapodialborsten bei Myzostomum. Zool Bidr Uppsala 16:238-299.
Jägersten G. 1939. Zur Kenntnis der Larventwicklung bei Myzostomum. Arkiv Zool 31:1-21.
James MA. 1997. Brachiopoda: internal anatomy, embryology, and development. In: Harrison FW, Woollacott RM, editors. Microscopic anatomy of invertebrates, vol. 13. Lophophorates, Entoprocta, and Cycliophora. New York: John Wiley & Sons, p 297-408.
Jangoux M. 1990. Diseases of Echinodermata. In: Kinne O, editor. Diseases of marine animals, vol. 3. Hamburg: Biologische Anstalt Helgoland, p 439-467.
Kato K. 1952. On the development of myzostome. Sci Rep Saitama Univ (B) 1:1-16.
McHugh D. 1997. Molecular evidence that echiurans and pogonophorans are derived annelids. Proc Nat Acad Sci USA 94:8006-8009.
McHugh D. 2000. Molecular phylogeny of the Annelida. Can J Zool 78:1873-1884.
Meyer DL, Ausich W. 1983. Biotic interactions among recent and among fossil crinoids. In: Tevesz MJS, McCall PL, editors. Biotic interactions in Recent and fossil benthic communities. New York: Plenum. p 377-427.
Müller MC. 1999. Das Nervensystem der Polychaeten: Immunohistochemische Untersuchungen an ausgewählen Taxa. PhD thesis, University of Osnabrück.
Müller MC, Westheide W. 1997. Das Nervensystem parapodienloser Polychaeten: Orthogonale Strukturen des Nervensystems juveniler Stadien und progenetischer Arten. Verh Dtsch Zool Ges 92:43.
Müller MC, Westheide W. 2000. Structure of the nervous system of Myzostoma cirriferum (Annelida) as revealed by immunohistochemistry and cLSM analyses. J Morphol 245:87-98.
Müller MC, Westheide W. 2002. Comparative analysis of the nervous systems in presumptive progenetic dinophilid and dorvilleid polychaetes (Annelida) by immunohistochemistry and cLSM. Acta Zool 83:33-48.
Newby WW. 1940. The embryology of the echiuroid worm Urechis caupo. Mem Am Philos Soc 16:1-219.
Nielsen C. 1995. Animal evolution. Oxford: Oxford University Press.
Orrhage L. 1973. Light and electron microscope studies of some brachiopod and pogonophoran setae. Zeitsch Morphol Oekol Tiere 74:253-270.
Orrhage L. 1995. On the innervation and homologues of the anterior end appendages of the eunicea (Polychaeta), with a tentative outline of the fundamental constitution of the cephalic nervous system of the polychaetes. Acta Zool (Stockh) 76:229-248.
Pietsch A, Westheide W. 1987. Protonephridial organs in Myzostoma cirriferum (Myzostomida). Acta Zool 68:195-203.
Reuter M, Mantyla K, Gustafsson MKS. 1998. Organization of the orthogon - main and minor nerve cords. Hydrobiologia 383:175-182.
Rieger RM. 1986. Über den Ursprung der Bilateria: die Bedeutung der Ultrastrukturforshung für ein neues Verstehen der Metazoenevolution. Verh Dtsch Zool Ges 79:31-50.
Rouse GW. 1999. Trochophore concepts: ciliary bands and the evolution of larvae in spiralian Metazoa. J Linnean Soc 66:411-464.
Rouse GW, Fauchald K. 1997. Cladistics and polychaetes. Zool Scr 26:139-204.
Ruppert EE. 1978. A review of metamorphosis of turbellarian larvae. In: Chia F-S, Rice ME, editors. Settlement and metamorphosis of marine invertebrate larvae. New York: Elsevier. p 65-81.
Salvini-Plawen LV. 1980. Was ist eine Trochophora? (What is a Trochophora?). Zool Jahrb Anat 103:354-373.
Smith PR. 1992. Excretory system. In: Harrison FW, Gardiner SL, editors. Microscopic anatomy of invertebrates, vol. 7. Annelida. New York: John Wiley & Sons, p 71-108.
Smith PR, Lombardi J, Rieger RM. 1986. Ultrastructure of the body cavity lining in a secondary acoelomate, Microphtalmus cf. listensis Westheide (Polychaeta: Hesionidae). J Morphol 188: 257-271
Specht A. 1987. Chaetae. In: Westheide W, Hermans CO, editors. The ultrastructure of Polychaeta. Stuttgart: Gustav Fischer. p 45-60.
Strathmann RR. 1993. Hypotheses on the origins of marine larvae. Annu Rev Ecol System 24:89-117.
Warn JM. 1974 Presumed myzostomid infestation of an Ordovician crinoid. J Paleont 48:506-513
Zrzavy J, Mihulka S, Kepka P, Bezdek A, Tietz D. 1998. Phylogeny of the metazoa based on morphological and 18S ribosomal DNA evidence. Cladistics 14:249-285.
Zrzavy J, Hypsa V, Tietz DF. 2001. Myzostomida are not annelids: molecular and morphological support for a clade of animals with anterior sperm flagella. Cladistics 17:1-29.
