Hostname: page-component-78c5997874-dh8gc Total loading time: 0 Render date: 2024-11-04T18:25:11.922Z Has data issue: false hasContentIssue false

Developmental studies of the enigmatic worm Caobangia billeti Giard, 1893 (Annelida; Sabellidae), a symbiont of freshwater snails

Published online by Cambridge University Press:  10 August 2017

Glafira D. Kolbasova*
Affiliation:
Pertsov White Sea Biological Station, Biological Faculty, Moscow State University, Moscow, 119234, Russia
Alexander B. Tzetlin
Affiliation:
Pertsov White Sea Biological Station, Biological Faculty, Moscow State University, Moscow, 119234, Russia Invertebrate Zoology Department, Biological Faculty, Moscow State University, Moscow, 119234, Russia
*
Correspondence should be addressed to: G.D. Kolbasova, Pertsov White Sea Biological Station, Biological Faculty, Moscow State University, Moscow, 119234, Russia email: [email protected]

Abstract

Caobangiids are an aberrant group of annelids with an unusual phoronid-like body plan. The most perceptible anatomical characteristic of caobangiids is the anal trunk, which is recurved outside the body and ends with an anal opening located near the head. So far neither the larval development nor the metamorphosis of these worms have been investigated thoroughly. This study describes the larval development and metamorphosis of Caobangia billeti, and focuses mainly on the formation of the alimentary tract. The trochophore has eight chaetigers. Embryogenesis includes the development of segmentally arranged bands of cilia and ventral ciliary fields, the development of chaetae and the early formation of anterior radioles. Upon exiting the larval duct, larvae have eyes with lenses, two pairs of rudimentary radioles on the prostomium, a pair of nephridia on the peristomium, and two capillary chaetae in each parapodium of segments 3–9; parapodia of the 10th segment also bear a row of palmate hooks. Metamorphosis takes about 20 h and involves dorso-ventral folding of the body and enlargement of the pygidium along the dorsal side of segments 5–8. Thus, the anus develops on the dorsal side of the 5th segment, the anal trunk forms from the projection of pygidium whereas the prepygidial growth zone appears posterior to the 8th body segment. After the completion of metamorphosis, the prostomial and peristomial segments are fused and reduced, eight full thoracic chaetigers derive from the larva's body. Abdominal chaetigers grow posteriorly from the prepygidial growth zone.

Type
Research Article
Copyright
Copyright © Marine Biological Association of the United Kingdom 2017 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Absolon, K. and Hrabě, S. (1930) Über einen neuen Süsswasser-Polychaeten aus den Höhlengewässern der Herzegowina. Zoologischer Anzeiger 88, 259264.Google Scholar
Anderson, D.T. (1965) The comparative embryology of the Polychaeta. Acta Zoologica 47, 142.CrossRefGoogle Scholar
Berrill, N.J. (1977) Functional morphology and development of segmental inversion in sabellid polychaetes. Biological Bulletin 153, 453467.Google Scholar
Berrill, N.J. (1978) Induced segmental reorganization in sabellid worms. Journal of Embryology and Experimental Morphology 47, 8596.Google Scholar
Bick, A. (1996) Reproduction and larval development of Manayunkia aestuarina (Bourne, 1883) (Polychaeta, Sabellidae) in a coastal region of the southern Baltic. Helgoländer Meeresuntersuchungen 50, 287298.Google Scholar
Blake, J.A. (1969) Systematics and ecology of shell-boring polychaetes from New England. American Zoologist 9, 813820.Google Scholar
Capa, M. (2007) Taxonomic revision and phylogenetic relationships of apomorphic sabellids (Polychaeta) from Australia. Invertebrate Systematics 21, 537567.Google Scholar
Chalmers, R. (2002) An investigation into the feeding biology and factors influencing the population dynamics of Terebrasabella heterouncinata (Polychaeta: Sabellidae), a problematic tube-dwelling polychaete in farmed abalone in South Africa . MSc thesis. Rhodes University, Grahamstown, 78118.Google Scholar
Chughtai, I. (1986) Fine structure of spermatozoa in Perkinsiana rubra and Pseudopotamilla reniformis (Sabellidae: Polychaeta). Acta Zoologica 67, 165171.Google Scholar
Chughtai, I. and Knight-Jones, E.W. (1988) Burrowing into limestone by sabellid polychaetes. Zoologica Scripta 17, 231238.Google Scholar
Fitzhugh, K. (1989) A systematic revision of the Sabellidae–Caobangiidae–Sabellongidae complex (Annelida: Polychaeta). Bulletin of the American Museum of the Natural History 192, 1104.Google Scholar
Fitzhugh, K. (1991) Further revisions of the Sabellidae subfamilies and cladistic relationships among the Fabriciinae (Annelida: Polychaeta). Zoological Journal of Linnean Society 102, 305322.Google Scholar
Fitzhugh, K. (1992) On the systematic position of Monroika africana (Monro) (Polychaeta: Sabellidae: Fabriciinae) and a description of a new fabriciin genus from Australia. Proceedings of the Biological Society of Washington 105, 116131.Google Scholar
Fitzhugh, K. (2003) A new species of Megalomma Johansson, 1927 (Polychaeta: Sabellidae: Sabellinae) from Taiwan, with comments on sabellid dorsal lip classification. Zoological Studies 42, 106134.Google Scholar
Fitzhugh, K. and Rouse, G.W. (1999) A remarkable new genus and species of fan worm (Polychaeta: Sabellidae: Sabellinae) associated with marine gastropods. Invertebrate Biology 118, 357390.Google Scholar
Giard, A. (1893) Sur un type nouveau et aberrant de la famille des Sabellides (Caobangia billeti). Comples Rendus Hebdomadaires des Séances et Mémoires de la Société de Biologie 9, 473476.Google Scholar
Glasby, C.J. and Timm, T. (2008) Global diversity of polychaetes (Polychaeta; Annelida) in freshwater. Hydrobiologia 595, 107115.Google Scholar
Grube, A.E. (1860) Beschreibung neuer oder wenig bekannter Anneliden. Archiv für Naturgeschichte 26, 71118.Google Scholar
Haigler, S.A. (1969) Boring mechanism of Polydora websteri inhabiting Crassostrea virginica . American Zoologist 9, 821828.Google Scholar
Hutchings, P. (2008) Role of polychaetes in bioerosion of coral substrates. In Wisshak, M. and Tapanila, L. (eds) Current developments in bioerosion. Berlin: Springer, pp. 249264.CrossRefGoogle Scholar
Jones, M.L. (1969) Boring of shell by Caobangia in freshwater snails of southeast Asia. American Zoologist 9, 829835.Google Scholar
Jones, M.L. (1974a) On the Caobangiidae, a new family of the Polychaeta, with a redescription of Caobangia billeti Giard. Smithson. Contributions on Zoology 175, 155.Google Scholar
Jones, M.L. (1974b) Brandtika asiatica new genus, new species, from southeastern Asia and a redescription of Monroika africana (Monro) (Polychaeta: Sabellidae). Proceedings of the Biological Society of Washington 87, 217230.Google Scholar
Knight-Jones, P. (1981) Behaviour, setal inversion and phylogeny of Sabellida (Polychaeta). Zoologica Scripta 10, 183202.Google Scholar
Knight-Jones, P. and Bowden, N. (1984) Incubation and scissiparity in Sabellidae (Polychaeta). Journal of the Marine Biological Association of the United Kingdom 64, 809818.Google Scholar
Kuris, A.M. and Culver, C.S. (1999) An introduced sabellid polychaete pest infesting cultured abalones and its potential spread to other California gastropods. Invertebrate Biology 118, 391403.Google Scholar
Langerhans, P. (1880) Die Wurmfauna Madeiras. Zeitschrift für wissenschaftliche Zoologie 33, 271316.Google Scholar
Leidy, J. (1883) Manayunkia speciosa . Proceedings of the Academy of Natural Sciences of Philadelphia 35, 204212.Google Scholar
Licciano, M., Murray, J.M., Watson, G.J. and Giangrande, A. (2012) Morphological comparison of the regeneration process in Sabella spallanzanii and Branchiomma luctuosum (Annelida, Sabellida). Invertebrate Biology 131, 4051.Google Scholar
Murray, J.M. (2010) Regeneration and reproduction in Sabella pavonina (Savigny), developing a novel method to culture marine ornamental sabellids . PhD thesis. University of Portsmouth, Portsmouth, UK, 274 pp.Google Scholar
Müller, O.F. (1771) Von Würmern des süssen und salzigen Wassers. Copenhagen: Heineck und Faber.Google Scholar
Nogueira, J.M.M., Fitzhugh, K. and Rossi, S.C.M. (2010) A new genus and new species of fan worms (Polychaeta: Sabellidae) from Atlantic and Pacific Oceans – the formal treatment of taxon names as explanatory hypotheses. Zootaxa 2603, 152.Google Scholar
Norf, H., Kniggendorf, L.G., Fischer, A., Arndt, H. and Kureck, A. (2010) Sexual and reproductive traits of Hypania invalida (Polychaeta, Ampharetidae), a remarkable invasive species in Central European waterways. Freshwater Biology 55, 25102520.CrossRefGoogle Scholar
Rouse, G.W. (1995) Is sperm ultrastructure useful in polychaete systematics? An example using 20 species of the Fabriciinae (Polychaeta, Sabellidae). Acta Zoologica (Stockholm) 76, 5774.Google Scholar
Rouse, G.W. (1996) New Fabriciola and Manayunkia species (Fabriciinae, Sabellidae, Polychaeta) from Papua New Guinea. Journal of Natural History 30, 17611778.Google Scholar
Rouse, G.W. (1999) Polychaete sperm, phylogenetic and functional considerations. In Dorresteijn, A.W.C. and Westheide, W. (eds) Reproductive strategies and developmental patterns in annelids. Dordrecht: Springer, pp. 215224.Google Scholar
Rouse, G.W. (2004) Annelida, Polychaeta. In Yule, C.M. and Yong, H.S. (eds) Freshwater invertebrates of the Malaysian region. Malaysia: Academy of Sciences, pp. 194206.Google Scholar
Rouse, G.W. and Fitzhugh, K. (1994) Broadcasting fables, is external fertilization really primitive? Sex, size and larvae in sabellid polychaetes. Zoologica Scripta 23, 271312.Google Scholar
Rouse, G.W., Kupriyanova, E.K. and Nishi, E. (2006) Sabellida. In Rouse, G.W. and Pleijel, F. (eds) Reproductive biology and phylogeny of Annelida. Enfield: Science Publishers, pp. 521563.Google Scholar
Rouse, G.W. and Pleijel, F. (2001) Polychaetes. Oxford: Oxford University Press.Google Scholar
Sato, M. (1999) Divergence of reproductive and developmental characteristics in Hediste (Polychaeta, Nereididae). Hydrobiologia 402, 129143.CrossRefGoogle Scholar