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The biology and functional morphology of Mytilaster minimus (Bivalvia: Mytiloidea: Mytilidae) from the intertidal dinaric karst of Croatia (Adriatic Sea)

Published online by Cambridge University Press:  22 August 2017

Brian Morton  and
Sanja Puljas
Brian Morton*
Affiliation:
School of Biological Sciences, The University of Hong Kong, Hong Kong SAR, China
Sanja Puljas
Affiliation:
Department of Biology, Faculty of Science, University of Split, Teslina 12/III Split, Croatia
*
Correspondence should be addressed to: B. Morton, School of Biological Sciences, The University of Hong Kong, Hong Kong SAR, China email: prof_bmorton@hotmail.co.uk
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Abstract

Mytilaster minimus is widely distributed along the rocky intertidal of much of the Mediterranean's coastline and the Adriatic Sea. Populations are, however, threatened by the Lessepsian invader Brachidontes pharaonis that occupies the same habitat and is more tolerant of environmental extremes. This is the first study of the anatomy of M. minimus in relation to its evolution and adaptations towards an intertidal life on the karsted limestone shores that characterize much of the Mediterranean. In most anatomical respects M. minimus is a typical mytilid but is small (<16 mm shell length) and, post-juvenile, greatly deformed concomitant with its niche of colonizing pits in the karsted rocks. It is thus generally squatter, that is, dorso-ventrally flattened, laterally expanded and antero-posteriorly foreshortened in comparison with M. galloprovincialis. A pair of statocysts has been identified in the visceral mass. Most interest, however, resides in the fact the posterior byssal retractor muscles, like the shell, are foreshortened to comprise one paired block and the posterior pedal retractor muscles are situated beneath these not anterior to them as in other mytilids. These adaptations equip M. minimus for a compressed, squat, life in the intertidal karst. In addition to competition from the introduced B. pharaonis in the Mediterranean, M. minimus is facing competitive exclusion from the native Mytilus galloprovincialis that, as a result of intensive and increasing mariculture, is coming to dominate Croatian shorelines. This study is, therefore, prescient in laying the foundations for future research on what is becoming a threatened native Mediterranean species.

Keywords

Heteromyarian formshell deformitiesmusculaturestatocystsevolution
Type
Research Article
Information
Journal of the Marine Biological Association of the United Kingdom , Volume 98 , Special Issue 8: Special Section: European Marine Biology Symposium Papers 2018 , December 2018 , pp. 1999 - 2016
Copyright
Copyright © Marine Biological Association of the United Kingdom 2017 

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References

REFERENCES

Antiti, M., Daoulatli, A., Rueda, J.L. and Salas, C. (2013) Temporal variation of the algae-associated molluscan assemblage of artificial substrata in the Bay of Tunis (Tunisia). Mediterranean Marine Science 14, 390–402.Google Scholar
Atkins, D. (1937) On the ciliary mechanisms and interrelationships of lamellibranchs. Part III. Types of lamellibranch gills and their food currents. Quarterly Journal of Microscopical Science 79, 375–421.Google Scholar
Atkins, D. (1938) On the ciliary mechanisms and interrelationships of lamellibranchs. Part VII. Laterofrontal cilia of the gill filaments and their phylogenetic value. Quarterly Journal of Microscopical Science 80, 346–430.Google Scholar
Bacallardo, J.J. and collaborators (1984) Estudio de Bentos Marino del Archipiélago Canario. Gobierno de Canarias: Consejeria de Agricultura y Pesca.Google Scholar
Barbieri, L., Urgu, F., Maltagliati, G., Di Giuseppe, C., Lardicci, A. and Castelli, M. (2011) Genetic divergence between marine and brackishwater individuals of Mytilaster minimus (Mollusca, Bivalvia). Biologia Marina Mediterranea 18, 234–235.Google Scholar
Barić, A., Gačić, M., Grbec, B., Margeta, J., Miloš, B., Onofri, I. and Veldić, V. (1996) Implications of expected climatic changes on Kaštela Bay. In Jeftić, L., Kečkeš, S. and Pernetta, C. (eds) Climatic change and the Mediterranean: environmental and societal impacts of climatic change and sea-level rise in the Mediterranean region, Volume II. London: Edward Arnold, pp. 143–249.Google Scholar
Bayne, B.L., Widdows, J. and Thompson, R.J. (1976) Physiology: II. In Bayne, B.L. (ed.) Marine mussels: their ecology and physiology. International Biological Programme 10. Cambridge: Cambridge University Press, pp. 207–260.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
Board, P. (1983) The settlement of post larval Mytilus edulis. Journal of Molluscan Studies 49, 53–60.Google Scholar
Brown, C.H. (1952) Some structural proteins of Mytilus edulis. Quarterly Journal of Microscopical Science 93, 487–502.Google Scholar
Cannicci, S., Gomei, M., Dahdouh-Guebas, F., Rorandelli, R. and Terlizzi, A. (2007) Influence of seasonal food abundance and quality on the feeding habits of an opportunistic feeder, the intertidal crab Pachygrapsus marmoratus. Marine Biology 151, 1331–1342.Google Scholar
Colgan, D.J. and da Costa, P. (2013) Invasive and non-invasive lineages in Xenostrobus (Bivalvia: Mytilidae). Molluscan Research 33, 272–280.Google Scholar
Comeau, L.A. and Babarro, J.M.F. (2014) Narrow valve gaping in the invasive mussel Limnoperna securis: implications for competition with the indigenous mussel Mytilus galloprovincialis in NW Spain. Aquaculture International 22, 1215–1227.Google Scholar
d'Angelo, G. and Garguillo, S. (1978) Guida alle Conchigliie Mediterranée. Milano: Ed. Fabbri, 224 pp.Google Scholar
Darrigran, G. and Pastorino, G. (1995) The recent introduction of Asiatic bivalve, Limnoperna fortunei (Mytilidae) into South America. The Veliger 38, 183–187.Google Scholar
Dinesen, G.E. and Morton, B. (2014) Review of the functional morphology, biology and perturbation impacts on the circum-boreal, habitat-forming horse mussel Modiolus modiolus (Bivalvia: Mytilidae). Marine Biology Research 10, 845–870.Google Scholar
Dogan, A., Sezgin, M., Katagan, T. and Önen, M. (2015) Crustacea associated with Mytilus galloprovincialis Lamarck, 1819 and Mytilaster minimus (Poli, 1795) (Mollusca, Bivalvia) beds from Izmir Bay, Aegean Sea, Turkey. Crustaceana 88, 857–866.Google Scholar
Fankboner, P.V. (1971) The ciliary currents associated with feeding, digestion and sediment removal in Adula (Botula) falcata Gould 1851. Biological Bulletin 140, 28–45.Google Scholar
Fernandez-Trujillo, J.B. and Fernandez, A.R. (1992) Fauna Marina Amenazada en Las Islas Canarias. Icona: Colección Técnica, pp. 296.Google Scholar
Fischer, P. (1899) Manuel de conchyliologie et de paleontologie conchyliologique: ou, Histoire naturelle des mollusques vivants et fossiles. Suivi d'un appendice sur les brachiopodes par D. P. Œhlert. Avec 23 planches contenant 600 figures dessinées par S. P. Woodward. Paris: F. Savy.Google Scholar
Fishelson, L. (2000) Marine animal assemblages along the littoral of the Israeli Mediterranean seashore: the Red-Mediterranean Seas communities of species. Italian Journal of Zoology 67, 393–415.Google Scholar
Galil, B.S. (2007a) Seeing red: alien species along the Mediterranean coast of Israel. Aquatic Invasions 2, 281–312.Google Scholar
Galil, B.S. (2007b) Loss or gain? Invasive aliens and biodiversity in the Mediterranean Sea. Marine Pollution Bulletin 55, 314–322.Google Scholar
Gestoso, I., Olabarria, C. and Arenas, F. (2012) The invasive mussel Xenostrobus securis along the Galician Rias Baixas (NW of Spain): status of invasion. Cahiers de Biologie Marine 53, 391–396.Google Scholar
Giacoletti, A., Rinaldi, A., Mercurio, M., Mirto, S. and Sarà, G. (2016) Local consumers are the first line to control biological invasions: a case of study with the whelk Stramonita haemastoma (Gastropoda: Muricidae). Hydrobiologia 772, 117–129. doi: 10.1007/s10750-016-2645-6.Google Scholar
Giusti, F. (1971) The fine structure of the style sac and intestine in Mytilus galloprovincialis Lam. Proceedings of the Malacological Society of London 39, 95–104.Google Scholar
Gofas, S., Le Renard, J. and Bouchet, P. (2001) Mollusca. In Costello, M.J., Emblow, C.S. and White, R. et al. (eds) European register of marine species: a check-list of the marine species in Europe and a bibliography of guides to their identification. Paris: Muséum national d’Histoire naturelle: Collection. Patrimoines Naturels, 50, 180–213.Google Scholar
Gosling, E.M. (ed.) (1992) The mussel Mytilus. Amsterdam: Elsevier Science.Google Scholar
Hanley, S. (1843) An illustrated and descriptive catalogue of Recent bivalve shells with 960 figures by Wood and Sowerby, forming an appendix to the Index Testaceologicus. London: W. Wood, pp. 33–272 + Plates 9–13.Google Scholar
Hernández, J.M., Rolán, E., Swinnen, F., Gómez, R. and Pérez, J.M. (2011) Moluscos y conchas marinas de Canarias. Hackenheim: Conchbooks.Google Scholar
Huber, M. (2010) Compendium of bivalves. A full-color guide to 3,300 of the world's marine bivalves. A status on Bivalvia after 250 years of research. Hackenheim: ConchBooks.Google Scholar
Kellogg, J.L. (1915) Ciliary mechanisms of lamellibranches with descriptions of anatomy. Journal of Morphology 26, 625–701.Google Scholar
Klobučar, G.I.V., Štambuk, A., Hylland, K. and Pavlica, M. (2008) Detection of DNA damage in Mytilus galloprovincialis in the coastal ecosystems of Kaštela and Trogir bays, Croatia. Science of the Total Environment 405, 330–337.Google Scholar
Kršinić, F. (2012) Zooplankton. U: Početna procjena stanja i opterećenja morskog okoliša hrvatskog dijela Jadrana (koordinator: N. Krstulović), pp. 144–172.Google Scholar
List, T. (1902) Fauna und Flora des Golfes von Neapel und der angrenzenden den Meeres-Abschnitte. 1. Die Mytiliden des Golfes von Neapel und der angrenzenden den Meeres-Abschnitte. Mitteilungen aus der Zoologischen Station zu Neapel 27, 1–312.Google Scholar
Manachini, B., Arizza, V., Rinaldi, A., Montalto, V. and Sarà, G. (2013) Eco-physiological response of two marine bivalves to acute exposition to commercial Bt-based pesticide. Marine Environmental Research 83, 29–37.Google Scholar
Marina, P., Urra, J., Rueda, J.L. and Salas, C. (2012) Composition and structure of the molluscan assemblage associated with a Cymodocea nodosa bed in south-eastern Spain: seasonal and diel variation. Helgoland Marine Research 66, 585–599.Google Scholar
Mistri, M, Fano, E.A. and Rossi, R. (2001) Redundancy of macrobenthos from lagoonal habitats in the Adriatic Sea. Marine Ecology Progress Series 215, 289–296.Google Scholar
Morton, B. (1980) Anatomy of the ‘living fossil’ Pholadomya candida Sowerby 1823 (Bivalvia: Anomalodesmata: Pholadomyacea). Videnskabelige Meddelelser fra Dansk naturhistorik Forening i Kjøbenhavn 142, 7–101.Google Scholar
Morton, B. (1985) Statocyst structure in the Anomalodesmata (Bivalvia). Journal of Zoology, London 206, 23–34.Google Scholar
Morton, B. (1988) The population dynamics and reproductive cycle of Brachidontes variabilis (Bivalvia: Mytilidae) in a Hong Kong mangrove. Malacological Review 21, 1–9.Google Scholar
Morton, B. (1992) The evolution and success of the heteromyarian form in the Mytiloida. In Gosling, E.M. (ed.) The mussel mytilus. Amsterdam: Elsevier Science, pp. 21–52.Google Scholar
Morton, B. (1995) The population dynamics and reproductive cycle of Septifer virgatus (Bivalvia: Mytilidae) on an exposed rocky shore in Hong Kong. Journal of Zoology, London 235, 485–500.Google Scholar
Morton, B. (1999) Competitive grazers and the predatory whelk Lepsiella flindersi (Gastropoda: Muricidae) structure a mussel bed (Xenostrobus pulex) on a southwest Australian shore. Journal of Molluscan Studies 65, 435–452.Google Scholar
Morton, B. (2004) Predator-prey interactions between Lepsiella vinosa (Gastropoda: Muricidae) and Xenostrobus inconstans (Bivalvia: Mytilidae) in a southwest Australian marsh. Journal of Molluscan Studies 70, 237–245.Google Scholar
Morton, B. (2012) A significant and un-appreciated intertidal mytiloidean genus: the biology and functional morphology of Brachidontes puniceus (Bivalvia: Mytilidae) from the Cape Verde Islands. African Journal of Marine Science 34, 71–80.Google Scholar
Morton, B. (2015a) The biology and anatomy of Limnoperna fortunei, a significant freshwater bio-invader: blueprints for success. In Boltovskoy, D. (ed.) Limnoperna fortunei: the ecology, distribution and control of a swiftly spreading invasive fouling mussel. Invading Nature – Springer Series in Invasion Ecology, Volume 10. Cham: Springer International Publishing, pp. 3–41.Google Scholar
Morton, B. (2015b) The evolution, adaptive radiation and classification of the Mytiloidea (Bivalvia): clues from the pericardial – posterior byssal retractor muscles complex. Molluscan Research 35, 1–19.Google Scholar
Morton, B. (2016) The biology and functional morphology of the predatory septibranch Cardiomya costellata (Bivalvia: Anomalodesmata: Cuspidariidae) from the Mid-Atlantic Ridge at the Açores. Survival at the edge. Journal of the Marine Biological Association of the United Kingdom 96, 1347–1361.Google Scholar
Morton, B., Britton, J.C. and de Frias-Martins, A.M. (1998) Coastal ecology of the Açores. Ponta Delgada, Sao Miguel, Açores: Sociedade Afonso Chaves.Google Scholar
Morton, B. and Dinesen, G. (2010) Colonization of Asian freshwaters by the Mytilidae (Bivalvia): a comparison of Sinomytilus harmandi from the Tonle-Sap River, Phnom Penh, Cambodia, with Limnoperna fortunei. Molluscan Research 30, 57–72.Google Scholar
Morton, B. and Leung, K.F. (2015) Introduction of the alien Xenostrobus securis (Bivalvia: Mytilidae) into Hong Kong, China: interactions with and impacts upon native species and the earlier introduced Mytilopsis sallei (Bivalvia: Dreissenidae). Marine Pollution Bulletin 92, 134–142.Google Scholar
Nicolaidou, A. (2007) Lack of temporal variability in the benthos of a coastal brackish water lagoon in Greece. Mediterranean Marine Science 8, 5–17.Google Scholar
Ockelmann, K. (1995) Ontogenetic characters of mytilaceans. Phuket Marine Biological Center, Special Publication 15, 85–88.Google Scholar
Ockelmann, K.W. (1983) Descriptions of mytilid species and definition of the Dacrydiinae n. sub. fam. (Mytilacea – Bivalvia). Ophelia 22, 81–123.Google Scholar
Ockelmann, K.W. and Dinesen, G.E. (2009) Systematic relationship of the genus Adula and its descent from a Mytilus-like ancestor (Bivalvia, Mytilidae, Mytilinae). Steenstrupia 30, 141–152.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
Owen, G. (1974) Studies on the gill of Mytilus edulis: the eu-latero-frontal cirri. Proceedings of the Royal Society of London, Series B 187, 83–91.Google Scholar
Owen, G. (1978) Classification and the bivalve gill. Philosophical Transactions of the Royal Society of London, Series B 284, 377–386.Google Scholar
Owen, G., Trueman, E.R. and Yonge, C.M. (1953) The ligament in the Lamellibranchia. Nature, London 171, 1–6.Google Scholar
Pallary, P. (1920) Exploration scientifique du Maroc organisée par la Société de Géographie de Paris et continuée par la Société des Sciences Naturelles du Maroc. Deuxième fascicule. Malacologie (1912). Larose, Rabat et Paris, pp. 108, 1 pl., 1 map.Google Scholar
Poppe, G.T. and Goto, Y. (1993) European seashells, Volume II. (Scaphopoda, Bivalvia, Cephalopoda). Wiesbaden: Verlag, pp. 221.Google Scholar
Pujol, J.P. (1967) Formation of the byssus in the common mussel (Mytilus edulis L.). Nature 214, 204–205.Google Scholar
Ridewood, W.G. (1903) On the structure of the gill of the Lamellibranchia. Philosophical Transactions of the Royal Society, Series B 195, 147–284.Google Scholar
Riggio, S., D'Anna, G. and Sparla, M.P. (1992) Coastal eutrophication and settlement of mussel beds in NW Sicily: remarks on their significance. In Ceccherelli V.U. and Rossi R. (eds) Marine eutrophication and population dynamics. Proceedings of 25th European Marine Biology Symposium 1990. Fredensborg: Olsen and Olsen, pp. 117–120.Google Scholar
Rilov, G., Benayahu, Ya. and Gasith, A. (2004) Prolonged lag in population outbreak of an invasive mussel: a shifting-habitat model. Biological Invasions 6, 347–364.Google Scholar
Rodríguez, R.G. and Sánchez, J.M.P. (1997) Moluscos Bivalvos de Canarias. Las Palmas: Ediciones del Cabildo Insular de Gran Canaria, 425 pp.Google Scholar
Rolan Mosquera, E., Otero Schmitt, J. and Rolan Alvarez, E. (1990) Moluscos de la Ria de Vigo. 2. Poliplacoforos, Bivalvos, Escafopodos, Cefalopodos. Thalassas, Annex 2, 1–276.Google Scholar
Safriel, U.N., Gilboa, A. and Felsenburg, T. (1980) Distribution of rocky intertidal mussels in the Red Sea coasts of Sinai, the Suez Canal and the Mediterranean coast of Israel, with special reference to recent colonizers. Journal of Biogeography 7, 39–62.Google Scholar
Safriel, U.N. and Sasson-Frosting, Z. (1988) Can colonising mussel outcompete indigenous mussel? Journal of Experimental Marine Biology and Ecology 117, 211–226.Google Scholar
Sarà, G. and de Pirro, M. (2011) Heart beat rate adaptations to varying salinity of two intertidal Mediterranean bivalves: the invasive Brachidontes pharaonis and the native Mytilaster minimus. Italian Journal of Zoology 78, 193–197.Google Scholar
Sarà, G., Milanese, M., Prusina, I., Sarà, A., Angel, D.L., Glamuzina, B., Nitzan, T., Freeman, S., Rinaldi, A., Palmeri, V., Montalto, V., Martire, M.L., Gianguzza, P., Arizza, V., Brutto, S.L., De Pirro, M., Helmuth, B., Murray, J., De Cantis, S. and Williams, G.A. (2014) The impact of climate change on Mediterranean intertidal communities: losses in coastal ecosystem integrity and services. Regional Environmental Change 14 (Suppl. 1), S5–S17.Google Scholar
Sarà, G., Romano, C., Caruso, M. and Mazzola, A. (2000) The new Lessepsian entry Brachidontes pharaonis (Fischer P., 1870) (Bivalvia, Mytilidae) in the western Mediterranean: a physiological analysis under varying natural conditions. Journal of Shellfish Research 19, 967–977.Google Scholar
Seed, R. (1969) The ecology of Mytilus edulis L. (Lamellibranchiata) on exposed rocky shores. 2. Growth and mortality. Oecologia 3, 317–350.Google Scholar
Šiletić, T. (2006) Marine fauna of Mljet National Park (Adriatic Sea, Croatia). 5. Mollusca: Bivalvia. Natura Croatica 15, 109–169.Google Scholar
Štambuk, A., Šrut, M., Šatović, Z., Tkalec, M. and Klobučar, G.I.V. (2013) Gene flow vs pollution pressure: genetic diversity of Mytilus galloprovincialis in eastern Adriatic. Aquatic Toxicology 136–137, 22–31.Google Scholar
Stasek, C.R. (1963) Synopsis and discussion of the association of ctenidia and labial palps in the bivalved Mollusca. The Veliger 6, 91–97.Google Scholar
Taylor, J.D., Kennedy, W.J. and Hall, A. (1969) The shell structure and mineralogy of the Bivalvia. Introduction. Nuculacae-Trigonacae. Bulletin of the British Museum, Natural History (Zoology) Supplement 3, 1–125.Google Scholar
Trueman, E.R. (1950) Observations on the ligament of Mytilus edulis. Quarterly Journal of Microscopical Science 91, 225–235.Google Scholar
White, K.M. (1937) Mytilus. Liverpool Marine Biological Committee Memoirs on Typical British Marine Plants and Animals 31, 1–117.Google Scholar
Wilson, B.R. (1967) A new generic name for three recent and one fossil species of Mytilidae (Mollusca: Bivalvia) in southern Australasia, with re-descriptions of the species. Proceedings of the Malacological Society of London 37, 279–295.Google Scholar
Wright, M.M. and Francis, L. (1984) Predator deterrence by flexible shell extensions of the horse mussel Modiolus modiolus. The Veliger 27, 140–142.Google Scholar
Yonge, C.M. (1948) Formation of siphons in Lamellibranchia. Nature species. Part I- Bivalvia. Proceedings of the United States National Museum 20, 775–901.Google Scholar
Yonge, C.M. (1955) Adaptation of rockboring in Botula and Lithophaga (Lamellibranchia, Mytilidae), with a discussion on the evolution of this habit. Quarterly Journal of Microscopical Science 96, 383–410.Google Scholar
Yonge, C.M. (1957) Mantle fusion in the Lamellibranchia. Pubblicazioni della Stazione Zoologica di Napoli 29, 151–171.Google Scholar
Yonge, C.M. (1976) The ‘mussel’ form and habit. In Bayne, B.L. (ed.) Marine mussels: their ecology and physiology. International Biological Programme 10. Cambridge: Cambridge University Press, pp. 1–12.Google Scholar
Yonge, C.M. (1978) Significance of the ligament in the classification of the Bivalvia. Proceedings of the Royal Society of London, Series B 202, 231–248.Google Scholar
Yonge, C.M. (1982) Mantle margins with a revision of siphonal types in the Bivalvia. Journal of Molluscan Studies 48, 102–103.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
Zamouri-Langar, N., Chouba, L., Ajjabi Chebil, L., Mrabet, R. and El Abed, A. (2011) Les coquillages bivalves des côtes tunisiennes. Institut National des Sciences et Technologies de la Mer: Salammbô. ISBN 978-9938-9512-0-2, 128 pp.Google Scholar
Zenetos, A., Vardala-Theodorou, E. and Alexandrakis, C. (2005) Update of the marine Bivalvia Mollusca checklist in Greek waters. Journal of the Marine Biological Association of the United Kingdom 85, 4798/1–6.Google Scholar