Abstract
The ventral musculature of Convolutriloba longifissura (Acoela) has been studied using electron microscopy and fluorescently labeled whole mounts to demonstrate filamentous actin. Attention was directed to the reorganization and renewal of musculature during asexual reproduction and the adaptation of muscle sets for special predatory behavior. Three ventral subepidermal muscle layers could be distinguished in adult C. longifissura: (1) outer circular muscles that encircle the body, (2) intermediate modified longitudinal muscles with concentric pattern around the mouth and V-shaped orientation in the posterior part of the animal, and (3) inner special pore muscles with radial alignment fanning out from the mouth. Additionally, a few very fragile muscles were found at the anterior margin of the animal. The anterior ventral muscle system built a funnel with the mouth opening as organizing center. The special radial muscles and the antagonistically concentric muscles are perfectly adapted to catch prey in such a way that the funnel is put over the prey to press it through the mouth into the digestive syncytium. Convolutriloba longifissura shows a unique way of asexual reproduction by a two-step fission which results in three individuals. Immediately after separation from the mother animal, daughter individuals are missing the concentric and the radial muscle sets around the mouth completely, but within 30 h these sets are renewed for the most part. Two to three days after separation, the mouth opening is visible and the animals move for capturing prey. The peculiar course of longitudinal muscles in C. longifissura with concentric rings anteriorly and a V-shape muscle layer posteriorly shows that the pattern of body-wall musculature in such basal Plathelminthes as the Acoela may be highly modified from the original pattern of longitudinal and circular muscles.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Abildgaard PC (1806) Zoologica danica seu animalium Danicae et Norwegiae rariorum ac mines notorum descriptorum et historia aus O.F Mueller. Zool Dan 4:1–26
Adoutte A, Balavoine G, Lartillot N, Lesinet O, Prud'homme B, Rosa R de (2000) The new animal phylogeny: reliability and implications. Proc Natl Acad Sci USA 97:4453–4456
Åkesson B, Hendelberg J (1989) Nutrition and asexual reproduction in Convolutriloba retrogemma, an acoelous turbellarian in obligate symbiosis with algal cells. In: Ryland JS, Tyler PA (eds) Reproduction, genetics and distributions of marine organisms, 23rd European Marine Biology Symposium. Olsen and Olsen, Fredensborg, pp 13–21
Åkesson B, Gschwentner R, Hendelberg J, Ladurner P, Müller J, Rieger R (2001) Fission in Convolutriloba longifissura: asexual reproduction in acoelous turbellarians revisited. Acta Zool 82:231–239
Antonius A (1968) Faunistische Studien am Roten Meer im Winter 1961/62, Teil IV. Neue Convolutidae und eine Bearbeitung des Verwandtschaftskreises Convoluta (Turbellaria, Acoela). Zool Jahrb Syst Bd 95:297–394
Ax P (1961) Verwandtschaftsbeziehungen und Phylogenie der Turbellarien. Ergebn Biol 24:1–68
Ax P (1987) The phylogenetic system. Wiley, Chichester
Bartolomaeus T, Balzer I (1997) Convolutriloba longifissura, nov. spec. (Acoela): first case of longitudinal fission in Plathelminthes. Microfauna Mar 11:7–18
Berney C, Pawlowski J, Zaninetti L (2000) Elongation factor 1-alpha sequences do not support an early divergence of the Acoela. Mol Biol Evol 17:1032–1039
Böhmig L (1895) Die Turbellaria Acoela der Plankton-Expedition. In: Hensen V (ed) Ergebnisse der Plankton-Expedition der Humboldt-Stiftung, vol 2. Lipsius and Tischer, Keil, pp 1–48
Brusca RC, Brusca GJ (1990) Invertebrates. Sinauer, Sunderland, Mass, p 922
Dörjes J (1968) Die Acoela (Turbellaria) der deutschen Nordseeküste und ein neues System der Ordnung. Z Zool Syst Evolutionsforsch 6:56–452
Graff L von (1891) Die Organisation der Turbellaria Acoela. Engelmann, Leipzig
Gschwentner R, Ladurner P, Salvenmoser W, Rieger R, Tyler S (1999) Fine structure and evolutionary significance of sagittocysts of Convolutriloba longifissura (Acoela, Platyhelminthes). Invert Biol 118:332–345
Gschwentner R, Ladurner P, Rieger R (2001) Stem cells in a basal bilaterian: S-phase and mitotic cells in Convolutriloba longifissura (Acoela, Platyhelminthes). Cell Tissue Res 304:401–408
Hendelberg J, Åkesson B (1988) Convolutriloba retrogemma gen. et sp.n., a turbellarian (Acoela, Platyhelminthes) with reversed polarity of reproductive buds. Fortschr Zool 36:321–327
Hendelberg J, Åkesson B (1991) Studies of the budding process in Convolutriloba retrogemma (Acoela, Platyhelminthes). Hydrobiologia 227:11–17
Hooge MD (2001) Evolution of body-wall musculature in the Platyhelminthes (Acoelomorpha, Catenulida, Rhabditophora). J Morphol 249:171–194
Hooge MD, Tyler S (1999) Body-wall musculature of Praeconvoluta tornuva n. sp. (Acoela, Platyhelminthes) and the use of muscle patterns in taxonomy. Invert Biol 118:8–17
Hooge MD, Tyler S (2003) Acoels (Platyhelminthes, Acoela) from the Atlantic coast of North America. Meiofauna Mar (in press)
Ladurner P, Rieger R (2000) Embryonic muscle development of Convoluta pulchra (Turbellaria-Acoelomorpha, Platyhelminthes). Dev Biol 222:359–375
Luther A (1955) Die Dalyelliiden (Turbellaria Neorhabdocoela), eine Monographie. Acta Zool Fenn 87:1–337
Marcus E (1949) Turbellaria Brasileiros (7). Bol Fac Filos Ciênc Letr Sao Paulo Zool 14:7–155
Rieger RM, Weyrer S (1998) The evolution of the lower Metazoa: evidence from the phenotype. Prog Mol Subcell Biol 21:21–43
Rieger RM, Tyler S, Smith JPS III, Rieger GE (1991) Platyhelminthes: Turbellaria. In: Harrison FW, Bogitsh BJ (eds) Microscopic anatomy of invertebrates, vol 3. Wiley-Liss, New York, pp 7–140
Rieger RM, Salvenmoser W, Legniti A, Tyler S (1994) Phalloidin-rhodamine preparations of Macrostomum hystricinum marinum (Plathelminthes): morphology and post embryonic development of the musculature. Zoomorphology 114:133–147
Ruiz-Trillo I, Riutort M, Littlewood DTJ, Herniou EA, Bagua J (1999) Acoel flatworms: earliest extant bilaterian metazoans, not members of Platyhelminthes. Science 283:1919–1923
Smith JPS, Bush L (1991) Convoluta pulchra, n. sp., (Turbellaria: Acoela) from the east coast of North America. Trans Am Microsc Soc 110:12–26
Spurr AR (1969) A low-viscosity epoxy resin embedding medium for electron microscopy. J Ultrastruct Res 26:31–43
Steinböck O (1963a) Regeneration experiments and phylogeny. In: Dougherty EL (ed) The lower Metazoa. University of California Press, Berkeley, pp 108–112
Steinböck O (1963b) Regeneration- und Konplantationsversuche an Amphiscolops spec. (Turbellaria Acoela). Roux Arch Entwick 154:308–353
Steinböck O (1967) Regenerationsversuche mit Hofstenia giselae Steinb. (Turbellaria Acoela). Wilh Roux's Arch Entwicklungsmech 158:394–458
Tyler S, Hyra SG (1998) Patterns of musculature as taxonomic characters for the Turbellaria Acoela. Hydrobiologia 383:51–59
Tyler S, Rieger RM (1999) Functional morphology of musculature in the acoelomate worm, Convoluta pulchra (Plathelminthes). Zoomorphology 119:127–141
Acknowledgements
This work was supported by an FWF grant. We thank family Matiasch (Maishofen, Austria) for specimens of Convolutriloba longifissura, Willi Salvenmoser, Karl Schatz, and Konrad Eller for photographic and technical assistance, and Gunde Rieger for suggestions. LSM 510 was used with courtesy of Professor Pelster, Institute of Zoology and Limnology, University of Innsbruck.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Gschwentner, R., Mueller, J., Ladurner, P. et al. Unique patterns of longitudinal body-wall musculature in the Acoela (Plathelminthes): the ventral musculature of Convolutriloba longifissura . Zoomorphology 122, 87–94 (2003). https://doi.org/10.1007/s00435-003-0074-3
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00435-003-0074-3