Hostname: page-component-745bb68f8f-grxwn Total loading time: 0 Render date: 2025-01-11T07:08:07.910Z Has data issue: false hasContentIssue false
  • English
  • Français

The biology and functional morphology of Modiolarca subpicta (Bivalvia: Mytilidae: Musculinae), epizoically symbiotic with Ascidiella aspersa (Urochordata: Ascidiacea), from the Kattegat, northern Jutland, Denmark

Published online by Cambridge University Press:  15 December 2010

Brian Morton  and
Grete E. Dinesen
Brian Morton*
Affiliation:
Department of Zoology, The Natural History Museum, Cromwell Road, London SW7 5BD, United Kingdom
Grete E. Dinesen
Affiliation:
Coastal Ecology Section, National Institute of Aquatic Resources, Technical University of Denmark, Charlottenlund Castle, Jægersborg Allé 1, DK-2920 Charlottenlund, Denmark Invertebrate Section, Zoological Museum, Natural History Museum of Denmark, University of Copenhagen, Universitetsparken 15, 2100 Copenhagen, Denmark
*
Correspondence should be addressed to: B. Morton, Department of Zoology, The Natural History Museum, Cromwell Road, London SW7 5BD, United Kingdom email: prof_bmorton@hotmail.co.uk
Get access Rights & Permissions [Opens in a new window]

Abstract

This study of the little known north-eastern Atlantic mytilid Modiolarca subpicta suggests a more intimate relationship with ascidians and, especially, Ascidiella aspersa, than has hitherto been appreciated. Both live for ~18 months and the reproductive cycle of both is approximately co-ordinated so that juvenile ascidians become available as hosts to the settling spat of the symbiotically epizoic M. subpicta each summer. Settling spat of M. subpicta are thought to be attracted to the exhalant flow from the ascidian's anal siphon. After the ascidian's death, the liberated mussels may adopt a wandering, free-living, lifestyle they have occasionally been reported to pursue. Anatomically, M. subpicta is of the typical mytilid plan, albeit simplified commensurate upon its normal lifestyle of protective envelopment within the host's tunic. The foot, however, is highly mobile and in addition to being used for locomotion, especially in juveniles, is responsible for the planting of byssal threads, typically dorsally above the shell, so that each individual stimulates the ascidian to produce an epidermal pocket into which it manœuvres itself and reposes, securely attached, but dorsal side down Modiolarca subpicta, epizoic in the tests of ascidians, could have evolved from a more isomyarian, equivalve, ancestor via a nestling, epibyssate, Trichomusculus-like shaped intermediary with ventral flattening and, hence, stability characteristic of the more familiar heteromyarian mytilids of rocky shores and lotic freshwaters being achieved through living dorsal side down.

Keywords

MytilidaeBivalviaModiolarca subpictacommensalAscidiella aspersaUrochordataAscidiaceaDenmark
Type
Research Article
Information
Journal of the Marine Biological Association of the United Kingdom , Volume 91 , Issue 8 , December 2011 , pp. 1637 - 1649
Copyright
Copyright © Marine Biological Association of the United Kingdom 2010

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

Andrews, J. (1981) Texas shells. Austin, TX: University of Texas Press, pp. i–xxvi & 1–175.Google Scholar
Beedham, G.E. (1958) Observations on the non-calcareous component of the shell of the Lamellibranchia. Quarterly Journal of Microscopical Science 99, 341–357.Google Scholar
Bodger, P.M. and Allen, J.A. (2008) The ecology and life cycle of a population of Modiolarca tumida (Hanley, 1843) (Bivalvia: Mytilidae) off the coast of north-eastern England. Journal of Molluscan Studies 74, 97–101.Google Scholar
Bourdillon, A. (1950) Note sur le commensalisme de Modiolaria et des ascidies. Vie et Milieu 1, 198–199.Google Scholar
Carlton, J.T. (2003) Community assembly and historical biogeography in the North Atlantic Ocean: the potential role of human-mediated dispersal vectors. Hydrobiologia 503, 1–8.Google Scholar
Cantraine, F.J. (1835) Diagnoses ou descriptions succinctes de quelques espèces nouvelles de mollusques. Bulletins de l'Académie des Sciences et Belles-lettres de Bruxelles 2, 380–411.Google Scholar
Collin, J. (1880) Faunula Molluscorum Marinorum Hellebækiana: Oversigt over den marine bløddyrfauna ved Hellebæk. Kjøbenhavn: Thieles Bogtrykkeri. Naturhistorisk Tidskrift 3, R. 12, Volume 1880, 1–169.Google Scholar
Collin, J. (1884) Om Limfjordens tidligere og nuværende marine fauna, med særligt hensyn til bløddyrfaunaen. Kjøbenhavn: Gyldendalske Boghandels Forlag, pp. 1–169.Google Scholar
Dando, P.R., O'Hara, S.C.M., Schuster, U., Taylor, L.J., Clayton, C.J., Baylis, S. and Laier, T. (1994) Gas seepage from a carbonate cemented sandstone reef on the Kattegat coast of Denmark. Marine and Petroleum Geology 11, 182–189.CrossRefGoogle Scholar
Dodge, H. (1952) A historical review of the mollusks of Linnaeus. Part 1. The classes Loricata and Pelecypoda. Bulletin of the American Museum of Natural History 100, 1–263.Google Scholar
Fleming, C.A. (1959) Notes on New Zealand recent and tertiary mussels (Mytilidae). Transactions of the Royal Society of New Zealand 87, 172–173.Google Scholar
Forbes, E. (1838) Malacologia Monensis: a catalogue of the Mollusca inhabiting the Isle of Man and the neighbouring sea. Edinburgh: J. Carfrae and Son, pp. xii, 1–63 & 3 plates.Google Scholar
Forbes, E. and Hanley, S. (1853) A history of British Mollusca and their shells. Volume 2. London: John van Voorst, 557 pp.Google Scholar
de Frias Martins, A.M., Borges, J.P., Ávila, S.P., Costa, A.C., Madeira, P. and Morton, B. (2009) Illustrated checklist of the infralittoral Mollusca off Vila Franco do Campo. Açoreana Supplement 6, 15–103.Google Scholar
Gray, J.E. (1840) Synopsis of the contents of the British Museum. 42nd edition. London: British Museum, 370 pp.Google Scholar
Gray, J.E. (1842) Synopsis of the contents of the British Museum. 44th edition. London: British Museum, 92 pp.Google Scholar
Gray, J.E. (1843) Catalogue of the species of Mollusca found at New Zealand, with the description of some lately discovered species. In Dieffenback, E. (ed.) Travels in New Zealand; with contributions to the geography, geology, botany, and natural history of that country. Volume 2. London: John Murray, pp. 1–396.Google Scholar
Gray, J.E. (1847) A list of the genera of Recent Mollusca, their synonyma and types. Proceedings of the Zoological Society of London for 1847 [15] 178, 129–219.Google Scholar
Hanley, S. (1843) An illustrated and descriptive catalogue of recent shells. Part 2. London: W. Wood, pp. 33–272.Google Scholar
Hansson, H.G. (1998) Sydskandinaviska marine flercelliga evertebrater. 2nd edition. Tjärnö Marinbiologiska Laboratorium, Länsstyrelsen Västra Götland 1998, pp. 1–294.Google Scholar
Hayward, P.J. and Ryland, J.S. (eds) (1995) Handbook of the marine fauna of north-west Europe. Oxford: Oxford University Press.Google Scholar
Højsæter, T. (1986) An annotated check-list of marine mollusks of the Norwegian Coast and adjacent waters. Sarsia 71, 73–145.CrossRefGoogle Scholar
Iredale, T. (1914) On some invalid molluscan generic names. Proceedings of the Malacological Society of London 11, 170–178.Google Scholar
Iredale, T. (1915) A commentary on Suter's ‘Manual of the New Zealand Mollusca’. Transactions and Proceedings of the New Zealand Institute 47, 417–497.Google Scholar
Jeffreys, J.G. (1863) British conchology. Volume 2. Marine shells. London: John van Voorst, pp. 1–465 & 8 plates.Google Scholar
Jensen, A.D.S. and Spärck, R. (1934) Bløddyr Volume 2, Saltvandsmuslinger. Danmarks Fauna. København: G.E.C. Gads Forlag, pp. 1–208.Google Scholar
Jensen, K.R. and Knudsen, J. (1995) Annotated checklist of recent marine mollusks of Danish waters. Copenhagen: H.C.Ø. Tryk, pp. 1–73.Google Scholar
Jensen, P., Aagard, I., Burke, R.A. Jr, Dando, P.R., Jørgensen, N.O., Kuijpers, A., Laier, T., O'Hara, S.C.M. and Schmalljohan, R. (1992) ‘Bubbling reefs’ in the Kattegat: submarine landscapes of carbonate-cemented rocks support a diverse ecosystem at methane seeps. Marine Ecology Progress Series 83, 103–112.Google Scholar
Kott, P.A. (1985) The Australian Ascidiacea. Part 1. Phlebobranchia and Stolidobranchia. Memoirs of the Queensland Museum 23, 1–440.Google Scholar
Larsen, J.B., Frischer, M.E., Ockelmann, K.W., Rasmussen, L.J. and Hansen, B.W. (2007) Temporal occurrence of planktotrophic bivalve larvae identified morphologically and by single step nested multiplex PCR. Journal of Plankton Research 29, 423–436.Google Scholar
Leach, W.E. (1815) The zoological miscellany, being descriptions of new or interesting animals. Illustrated with coloured illustrations. Volume 2. London: E. Nodder & Son.Google Scholar
List, T. (1902) Fauna und Flora des Golfes von Neapel und der angrenzenden Meeres-Abschnitte, I. Die Mytiliden. Mittheilungen aus der Zoologischen Station zu Neapel 27, 1–312.Google Scholar
Lovén, S. (1846) Index Molluscorum, litora Scandinaviæ occidentalia habitantium. Faunæ prodromum. Öfversigt af Kongeliga Vetenskaps-Akademiens Handlinger för år 1846, 1–50.Google Scholar
Lovén, S. (1848) Bidrag til kännedomen om utvecklingen af Mollusca Acephala Lamellibranchiata. Öfversigt af Kongeliga Vetenskaps-Akademiens Handlinger för år 1848, 1–117.Google Scholar
McKay, D.W. and Smith, S.M. (1979) Marine Mollusca of East Scotland. Edinburgh: Royal Scottish Museum.Google Scholar
Meissner, A. (1893) Das Einnisten der Crenella marmorata in den Mantel der Ascidiella virginia. Sitzungsberichte der Gesellschaft Naturforschende Freunde zu Berlin 1893, 259–260.Google Scholar
Merrill, A.S. and Turner, R.D. (1963) Nest building in the bivalve mollusk genera Musculus and Lima. Veliger 6, 55–59.Google Scholar
Millar, R.H. (1952) The annual growth and reproductive cycle of four ascidians. Journal of the Marine Biological Association of the United Kingdom 31, 41–61.Google Scholar
Millar, R.H. (1971) The biology of ascidians. Advances in Marine Biology 9, 1–100.CrossRefGoogle Scholar
Morton, B. (1973) Some aspects of the biology, population dynamics and functional morphology of Musculista senhausia Benson (Bivalvia: Mytilacea). Pacific Science 28, 19–33.Google Scholar
Morton, B. (1980) The biology and some aspects of the functional morphology of Arcuatula elegans (Mytilacea: Crenellinae). In Morton, B. (ed.) Proceedings of the First International Workshop on the Malacofauna of Hong Kong and Southern China, Hong Kong, 1977. Hong Kong: Hong Kong University Press, pp. 331–345.Google Scholar
Morton, B. (1982) The mode of life and functional morphology of Gregariella coralliophaga (Gmelin 1791) (Bivalvia: Mytilacea) with a discussion on the evolution of the boring Lithophaginae and adaptive radiation in the Mytilidae. In Morton, B. and Tseng, C.K. (eds) Proceedings of the First International Marine Biological Workshop: the marine flora and fauna of Hong Kong and southern China, Hong Kong, 1980. Hong Kong: Hong Kong University Press, pp. 875–895.Google Scholar
Morton, B. (1988) Partnerships in the sea: Hong Kong's marine symbioses. Hong Kong: Hong Kong University Press, pp. i–xv & 1–124.Google Scholar
Morton, B. (1990) Corals and their bivalve borers—the evolution of a symbiosis. In Morton, B. (ed.) The Bivalvia. Proceedings of a Memorial Symposium in Honour of Sir Charles Maurice Yonge, Edinburgh, 1986. Hong Kong: Hong Kong University Press, pp. 11–46.Google Scholar
Morton, B. (1992) The evolution and success of the heteromyarian form in the Mytiloidea. In Gosling, E.M. (ed.) The mussel Mytilus: ecology, physiology, genetics and culture. Developments in aquaculture and fisheries 25. Amsterdam: Elsevier, pp. 21–52.Google Scholar
Morton, B. (1995) The biology and functional morphology of Trichomusculus semigranatus (Bivalvia: Mytiloidea) from the Azores. In de Frias Martins A.M. (ed.) The marine flora and fauna of the Azores. Proceedings of the Second International Workshop of Malacology and Marine Biology, Sao Miguel, Azores, 1991. Açoreana Supplement 4, 279–295.Google Scholar
Morton, B. and Dinesen, G.E. (2010) Colonization of Asian freshwaters by the Mytilidae (Bivalvia): and a comparison of Sinomytilus harmandi from the Tonle-Sap River, Phnom Penh, Cambodia, with Limnoperna fortunei. Molluscan Research 30, 57–74.CrossRefGoogle Scholar
Niermann-Kerkenberg, E. and Hofmann, D.K. (2006) Fertilization and normal development in Ascidiella aspersa (Tunicata) studied with Nomarski-optics. Helgoland Marine Research 43, 245–258.Google Scholar
Ockelmann, K.W. (1965) Developmental types in marine bivalves and their distribution along the Atlantic coast of Europe. In Cox, L.R. and Peake, J.F. (eds) Proceedings of the 1st European Malacological Congress, 1962. Conchological Society of Great Britain and Ireland and Malacological Society of London, pp. 25–33.Google Scholar
Ong Che, R.G. and Morton, B. (1992) Structure and seasonal variations in abundance of the macro-invertebrate community associated with Septifer virgatus (Bivalvia: Mytilidae) at Cape d'Aguilar, Hong Kong. Asian Marine Biology 9, 217–233.Google Scholar
Poppe, G.T. and Goto, Y. (1993) European seashells. Volume 2 (Scaphopoda, Bivalvia, Cephalopoda). Wiesbaden: Verlag Christa Hemmen, pp. 1–221.Google Scholar
Roberts, D. and Breen, J.P. (1985) The biology and functional anatomy of Modiolarca tumida (Musculus marmoratus) Bivalvia: Mytilidae. Journal of Zoology, London (Series A) 205, 435–443.Google Scholar
Rodríguez, R.G. and Sánchez, J.M.P. (1997) Moluscos Bivalvos de Canarias. Las Palmas de Gran Canaria: Ediciones del Cabildo Insular de Gran Canaria, pp. 1–425.Google Scholar
Seed, R., Richardson, C.A. and Smith, K. (2000) Marine mussels, their evolutionary success, ecological significance and use as chronometers of environmental change. In Harper, E.M., Taylor, J.D. and Crame, J.A. (eds) The evolutionary biology of the Bivalvia. London: Geological Society, Special Publications 177, pp. 465–478.Google Scholar
Service, M. and Magorrian, B.H. (1997) The extent and temporal variation of distubance to epibenthic communities in Strangford Lough, Northern Ireland. Journal of the Marine Biological Association of the United Kingdom 77, 1151–1164.Google Scholar
Soot-Ryen, T. (1955) A report on the family of Mytilidae (Pelecypoda). Allan Hancock Pacific Expedition 20, 1–174.Google Scholar
Soot-Ryen, T. (1963) Some nomenclatural changes in the family Mytilidae. Proceedings of the Malacological Society of London 35, 127–128.Google Scholar
Soot-Ryen, T. (1969) Mytilidae. In Moore, R.C. (ed.) Treatise on invertebrate paleontology, Mollusca 6, Bivalvia, Part N, Volume 1. Lawrence, KS: Geological Society of America and University of Kansas Press, pp. N271–278.Google Scholar
Svavarsson, J. (1990) Population dynamics and life cycle of the symbiotic copepod Lichomolgus canui Sars, associated with the ascidian Halocynthia pyriformis (Rathke). Journal of Experimental Marine Biology and Ecology 142, 1–12.Google Scholar
Svavarsson, J., Svane, I. and Helgason, G.V. (1993) Population biology of Doropygus pulex and Gunenotophorus globularis (Copepoda), symbionts within the ascidian Polycarpa pomaria (Savigny). Journal of Crustacean Biology 13, 532–537.Google Scholar
Tebble, N. (1966) British bivalve seashells. London: Trustees of the British Museum (Natural History), pp. 1–212.Google Scholar
Tendal, O.S. and Dinesen, G.E. (2005) Biogenic sediments, substrates and habitats of the Faroese shelf and slope. BIOFAR Proceedings 2005—Annales Societas Scientarium Færoenses Supplementum 41, 224–242.Google Scholar
Thiele, J. (1934) Handbuch der systematischen Weichtierkunde, Part III (Scaphopoda, Bivalvia, Cephalopoda). Family Mytilidae. Jena: Verlag von Gustav Fisher, pp. 797–801.Google Scholar
Thorson, G. (1946) Reproduction and larval development of Danish marine bottom invertebrates, with special references to the planktonic larvae of the Sound (Øresund). Meddelselser fra Kommissionen for Danmarks Fiskeri-og Havundersøgelser, serie Plankton 4, 1–523.Google Scholar
Van Dover, C.L. (2002) Community structure of mussel beds at deep-sea hydrothermal vents. Marine Ecology Progress Series 230, 137–158.Google Scholar
Vokes, H.E. (1980) Genera of the Bivalvia: a systematic and bibliographic catalogue. Revised and Updated. Ithaca, NY: Paleontological Research Institute, pp. 1–307.Google Scholar
White, K.M. (1949) Musculus lebourae, new species. Proceedings of the Malacological Society 28, 46–49.Google Scholar
Yonge, C.M. (1976) The ‘mussel’ form and habitat. In Bayne, B.L. (ed.) Marine mussels: their ecology and physiology. International Biological Programme 10. Cambridge: Cambridge University Press, pp. 1–23.Google Scholar
Yonge, C.M. and Campbell, J.I. (1968) On the heteromyarian condition in the Bivalvia with special reference to Dreissena polymorpha and certain Mytilacea. Transactions of the Royal Society of Edinburgh 68, 21–43.Google Scholar