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Ecophysiological responses of invasive and indigenous mytilidsin the Ría de Vigo (NW Spain)

Published online by Cambridge University Press:  27 September 2011

Jose M.F. Babarro  and
Malwenn Lassudrie
Jose M.F. Babarro*
Affiliation:
Instituto de Investigaciones Marinas, CSIC, Eduardo Cabello 6, 36208 Vigo, Spain
Malwenn Lassudrie
Affiliation:
Université de Bretagne Occidentale, Institut Universitaire Européen de la Mer (IUEM), 3 rue des Archives, CS 93837, 29238 Brest Cedex 3, France
*
aCorresponding author:[email protected]
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Abstract

The impact of an alien species is correlated with its abundance and potential to colonisenew environments. Consequently, the crucial aspects that give a mytilid species invasivepotential include its strength and capacity for adhesion to a wide variety of substratesand its ecological tolerance to environmental conditions. The alien black pygmy musselXenostrobus securis settles together with the indigenous and raftcultured mussel Mytilus galloprovincialis on hard substrates of the innercoastline of the Ría de Vigo (Atlantic Coast NW Spain). Key parameters for the ecologicalsuccess of these species could include their byssus structure and ecological plasticity.In this study, we assessed their comparative ability to attach to different substratesunder different environmental conditions, using both in situ and laboratory approaches.Byssus threads secreted by X. securis were found to be extremely thin andtheir thickness did not vary with mussel size. This thinness of byssus filaments inX. securis was compensated by the secretion of a huge number (up tothousand of byssus filaments). Although no increase in attachment strength was found withincreasing mussel size in this species, multiple byssus thread secretion might be a keyfactor in the successful invasion of inner areas of the estuary. Furthermore, X.securis exposes a much lower shell area to lift and drag forces in musselconglomerates. By contrast, the indigenous species M. galloprovincialissecretes thicker byssus threads, which provide stronger in situ attachmentdisplaying a linear increase in strength relative to the size of mussels. The exposure ofboth mytilid species to different abiotic factors in the laboratory confirmed the weakerbyssus secretion and limited variation in attachment strength in the alien species. On onehand, X. securis seemed to be better adapted to life on soft bottoms andnot capable of much plasticity when attached to different substrates. However, X.securis might be also well adapted to variable environmental conditions, e.g.,salinity fluctuations, with no need to modify its byssus properties to ensure secureattachment. Attachment strength of M. galloprovincialis was higher thanX. securis in all abiotic conditions tested. Results are discussed inrelation to the ecological tolerance and impact of these mytilid species.

Keywords

EcophysiologyInvasionAttachment strengthByssus secretionBivalvesXenostrobus securisMytilus galloprovincialis
Type
Research Article
Information
Aquatic Living Resources , Volume 24 , Issue 3: Physiomar10 , July 2011 , pp. 303 - 315
Copyright
© EDP Sciences, IFREMER, IRD 2011

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References

Ackerman, J.D., 1999, Effect of velocity on the filter feeding of dreissenid mussels (Dreissena polymorpha and Dreissena bugensis): implications for trophic dynamics. Can. J. Fish. Aquat. Sci. 56, 1551–1561. CrossRefGoogle Scholar
Allen, J.A., Cook, M., Jackson, D.J., Preston, S., Worth, E.M., 1976, Observations on the rate of production and mechanical properties of the byssus threads of Mytilus edulis L. J. Mollusc. Stud. 42, 279–289. Google Scholar
Babarro, J.M.F., Fernández-Reiriz, M.J., Labarta, U., 2000, Feeding behaviour of seed mussel Mytilus galloprovincialis: environmental parameters and seed origin. J. Shellfish Res. 145, 204–213. Google Scholar
Babarro, J.M.F., Fernández-Reiriz, M.J., 2010, Secretion of byssal threads in Mytilus galloprovincialis after spawning stress. J. Comp. Physiol. B 180, 95–104. CrossRefGoogle ScholarPubMed
Babarro, J.M.F., Carrington, E., 2011, Byssus secretion of Mytilus galloprovincialis: effect of site at macro- and micro-geographical scales within Ría de Vigo (NW Spain). Mar. Ecol. Prog. Ser. 435, 125–140. CrossRefGoogle Scholar
Bell, E.C., Gosline, J.M., 1996, Mechanical design of mussel byssus: material yield enhances attachment strength. J. Exp. Biol. 199, 1005–1017. Google ScholarPubMed
Bell, E.C., Gosline, J.M., 1997, Strategies for life in flow: tenacity, morphometry, and probability of dislodgement of two Mytilus species. Mar. Ecol. Prog. Ser. 159, 197–208. CrossRefGoogle Scholar
Bownes, S.J., McQuaid, D., 2010, Mechanisms of habitat segregation between an invasive (Mytilus galloprovincialis) and an indigenous (Perna perna) mussel: adult growth and mortality. Mar. Biol. 157, 1799–1810. CrossRefGoogle Scholar
Brazee, S.L., Carrington, E., 2006, Interspecific comparison of the mechanical properties of mussel byssus. Biol. Bull. 211, 263–274. CrossRefGoogle ScholarPubMed
Brenner, M., Buck, B.H., 2010, Attachment properties of blue mussel (Mytilus edulis L.) byssus threads on culture-based artificial collector substrates. Aquac. Eng. 42, 128–139. CrossRefGoogle Scholar
Braby, C.E., Somero, G.N., 2006, Following the heart: temperature and salinity effects on heart rate in native and invasive species of blue mussels (genus Mytilus). J. Exp. Biol. 209, 2554–2566. CrossRefGoogle Scholar
Brown, C.H., 1952, Some structural proteins of Mytilus edulis L. Quart. J. Microsc. Sci. 93, 487–502. Google Scholar
Buck, B.H., Buchholz, C.M., 2005, Response of offshore cultivated Laminaria saccharina to hydrodynamic forcing in the North Sea. Aquaculture 250, 674–691. CrossRefGoogle Scholar
Burkett, J.R., Wojtas, J.L., Cloud, J.L., Wilker, J.J., 2009, A method for measuring the adhesion strength of marine mussels, J. Adhesion 85, 601–615. CrossRefGoogle Scholar
Byers, J.E., 2000, Differential susceptibility to hypoxia aids estuarine invasion. Mar. Ecol. Prog. Ser. 203, 123–132. CrossRefGoogle Scholar
Carrington, E., 2002, Seasonal variation in the attachment strength of the blue mussel: causes and consequences. Limnol. Oceanogr. 47, 1723–1733. CrossRefGoogle Scholar
Carrington, E., Moeser, G.M., Thompson, S.B., Coutts, L.C., Craig, C.A., 2008, Mussel attachment on rocky shores: the effect of flow on byssus production. Int. Comp. Biol. 48, 801–807. CrossRefGoogle ScholarPubMed
Connell, J.H., 1961, The influence of interspecific competition and other factors on the distribution of the barnacle Chthamalus stellatus. Ecology 42, 710–723. CrossRefGoogle Scholar
Darrigran, G., 2002, Potential impact of filter-feeding invaders on temperate inland freshwater environments. Biol. Invasions 4, 145–156. CrossRefGoogle Scholar
Dayton, P.K., 1971, Competition, disturbance and community organization: the provision and subsequent utilization of space in a rocky shore intertidal community. Ecol. Monogr. 41, 351–389. CrossRefGoogle Scholar
Dutton, J.M., Hofmann, G.E., 2008, Spatial and temporal variation in distribution and protein ubiquitination for Mytilus congeners in the California hybrid zone. Mar. Biol. 154, 1067–1075. CrossRefGoogle Scholar
Filgueira, R., Peteiro, L.G., Labarta, U., Fernández-Reiriz, M.J., 2007, Assessment of spat collector ropes in Galician mussel farming. Aquac. Eng. 37, 195–201. CrossRefGoogle Scholar
Garci, M.E., Trigo, J.E., Pascual, S., Gonzalez, A.F., Rocha, F., Guerra, A., 2007, Xenostrobus securis (Lamarck, 1819) (Mollusca: Bivalvia): first report of an introduced species in Galician waters. Aquac. Int. 15, 19–24. CrossRefGoogle Scholar
Griffiths, C.L., Hockey, P.A.R., 1987, A model describing the interactive roles of predation, competition and tidal elevation in structuring mussel population. S. Afr. J. Mar. Sci. 5, 547–556. CrossRefGoogle Scholar
Harger, J.R., 1972, Competitive co-existence: maintenance of interacting associations of the sea mussel Mytilus edulis and Mytilus californianus. Veliger 14, 387–410. Google Scholar
Holt T.J., Rees E.I., Hawkins S.J., Seed R., 1998, Biogenic Reefs, Vol. 9: An Overview of Dynamic an Sensitivity Characteristics for Conservation Management of Marine SACs. Scottish Association of Marine Sciences/UK Marine SACs Project, Oban, Scotland.
Holway, D.A., 1999, Competitive mechanisms underlying the displacement of native ants by the invasive Argentine ant. Ecology 80, 238–251. CrossRefGoogle Scholar
Johnson, A.S., 2001, Drag, drafting, and mechanical interactions in canopies of the red alga Chondrus crispus. Biol. Bull. Mar. Biol. Lab. 201, 126–135. CrossRefGoogle ScholarPubMed
Kennedy, V.S., 2011, Biology of the uncommon dreissenid bivalve Mytilopsis leucophaeata (Conrand, 1831) in central Chesapeake Bay. J. Mollusc. Stud. 77, 154–164. CrossRefGoogle Scholar
Kohama, T., Montani, S., Kajiwara, Y., Yamada, M., 2001, Population dynamics of sessile bivalves Mytilus galloprovincialis and Xenostrobus securis in hyper eutrophicated bay, Japan. Bull. Jpn Soc. Fish Sci. 67, 664–671. CrossRefGoogle Scholar
Kimura T., 1994, The population dynamics of Musculista senhousia (Benson) and Limnoperna fortunei kikuchii Habe in Lake Hamana, especially the ecological study of larval recruitment. Ph.D. thesis, Mie University, Mie, Japan.
Kimura, T., Kakuta, T., Kurokura, H., 1995, Salinity tolerance and osmoregulation in freshwater and brackish water mytilids (Mytilidae: genus Limnoperna). Bull. Soc. Sea Water Scientist. Jpn 49, 148–152. Google Scholar
Kimura, T., Masaaki, T., Yasuhiro, S., 1999, Limnoperna fortunei kikuchii Habe, 1981 (Bivalvia: Mytilidae) is a synonym of Xenostrobus securis (Lamarck, 1918): introduction into Japan from Australia and/or New Zealand. Jpn J. Malacol. 58, 101–117. Google Scholar
Labarta U., Fernández-Reiriz M.J., Pérez-Camacho A., Pérez Corbacho E., 2004, Bateeiros, mar, mejillón. Una perspectiva bioeconómica. CIEF. Fundación Caixagalicia, Santiago de Compostela, ISBN 84-95491-69-9.
Lazzari, G., Rinaldi, E., 1994, Alcune considerazione sulla presenza di specie extra Mediterranee nelle lagune salmastre di Ravenna. Bull. Malacol. 30, 195–202. Google Scholar
Lekang, O.-I., Stevik, T.K., Borno, A.M., 2003, Evaluation of different combined collectors used in longlines for blue mussel farming. Aquac. Eng. 27, 89–104. CrossRefGoogle Scholar
Martella, T., 1974, Some factors influencing byssus thread production in Mytilus edulis (Mollusca: Bivalvia) Linnaeus, 1758. Water Air Soil Pollut. 3, 171–177. Google Scholar
Meadows, P.S., Shand, P., 1989, Experimental analysis of byssus thread production by Mytilus edulis and Modiolus modiolus in sediments. Mar. Biol. 101, 219–226. CrossRefGoogle Scholar
Míguez, B.M., Farina-Busto, L., Figueiras, F.G., Pérez, F.F., 2001, Succession of phytoplankton assemblages in relation to estuarine hydrodynamics in the Ría de Vigo: a box model approach. Sci. Mar. 65, 65–76. CrossRefGoogle Scholar
Nicastro, K.R., Zardi, G.I., Mcquaid, C.D., 2008, Movement behaviour and mortality in invasive and indigenous mussels: resilience and resistance strategies at different spatial scales. Mar. Ecol. Prog. Ser. 372, 119–126. CrossRefGoogle Scholar
Nicastro K.R., Zardi G.I., Mcquaid C.D., 2010, Differential reproductive investment, attachment strength and mortality of invasive and indigenous mussels across heterogeneous environments. Biol. Invasions, 12, 2165–2177.
Paini, D.R., Funderburk, J.E., Reitz, S.R., 2008, Competitive exclusion of a worldwide invasive pest by a native. Quantifying competition between two phytophagous insects on two host plant species. J. Anim. Ecol. 77, 184–190. Google ScholarPubMed
Pascual, S., Villalba, A., Abollo, E., Garci, M., González, A.F., Nombela, M., Posada, D., Guerra, A., 2010, The mussel Xenostrobus securis: a well-established alien invader in the Ria de Vigo (Spain, NE Atlantic). Biol. Invasions 12, 2091–2103. CrossRefGoogle Scholar
Pearce, T., LaBarbera, M., 2009, Biomechanics of byssal threads outside the Mytilidae: Atrina rigida and Ctenoides mitis. J. Exp. Biol. 212, 1449–1454. CrossRefGoogle ScholarPubMed
Petersen, J.K., Nielsen, T.G., van Duren, L., Maar, M., 2008, Depletion of plankton in a raft culture of Mytilus galloprovincialis in Ría de Vigo, NW Spain. I. Phytoplankton. Aquat. Biol. 4, 113–125. CrossRefGoogle Scholar
Price, H.A., 1982, An analysis of factors determining seasonal variation in the byssal attachment strength of Mytilus edulis L. J. Mar. Biol. Assoc. UK 62, 147–155. CrossRefGoogle Scholar
Price, H.A., 1983, Structure and formation of the byssus complex in Mytilus (Mollusca, Bivalvia). J. Mollusc. Stud. 49, 9–17. CrossRefGoogle Scholar
Rius, M., McQuaid, C.D., 2006, Wave action and competitive interaction between the invasive mussel Mytilus galloprovincialis and the indigenous Perna perna in South Africa. Mar. Biol. 150, 69–78. CrossRefGoogle Scholar
Sabelli, B., Speranza, S., 1994, Rinvenimento di Xenostrobus sp. (Bivalvia, Mytilidae) nella laguna di Venecia. Bull. Malacol. 29, 311–318. Google Scholar
Safriel, U.N., Sasson-Frostig, Z., 1988, Can colonizing mussel outcompete indigenous mussel? J. Exp. Mar. Biol. Ecol. 117, 211–226. CrossRefGoogle Scholar
Santaclara, F.J., Espiñeira, M., Vieites, J.M., 2007, Molecular Detection of Xenostrobus securis and Mytillus galloprovincialis Larvae in Galician Coast (Spain). Mar. Biotechnol. 9, 722–732. CrossRefGoogle Scholar
Sará, G., Romano, C., Widdows, J., Staff, F.J., 2008, Effect of salinity and temperature on feeding physiology and scope for growth of an invasive species (Brachidontes pharaonis – Mollusca: Bivalvia) within the Mediterranean sea. J. Exp. Mar. Biol. Ecol. 363, 130–136. CrossRefGoogle Scholar
Stanley, S.M., 1972, Functional morphology and evolution of byssally attached bivalve molluscs. J. Paleontol. 46, 165–212. Google Scholar
Steffani, C.N., Branch, G.M., 2005, Mechanisms and consequences of competition between an alien mussel, Mytilus galloprovincialis, and an indigenous limpet, Scutellastra argenvillei. J. Exp. Mar. Biol. Ecol. 317, 127–142. CrossRefGoogle Scholar
Suchanek, T.H., 1978, The ecology of Mytilus edulis L. in exposed rocky inertial communities. J. Exp. Mar. Biol. Ecol. 31, 105–120. CrossRefGoogle Scholar
Udhayakumar, M., Karande, A.A., 1989, Byssal threads of Mytilopsis sallei (Recluz) and their adhesive strength. Proc. Indian Acad. Sci. (Anim. Sci.) 98, 65–76. CrossRefGoogle Scholar
Van Erkom Schurink, C., Griffiths, C.L., 1990, Marine mussels of Southern Africa-their distribution patterns, standing stocks, exploitation and culture. J. Shellfish Res. 9, 75–85. Google Scholar
Van Winkle, W., 1970, Effect of environmental factors on byssal thread formation. Mar. Biol. 7, 143–148. CrossRefGoogle Scholar
Vogel, S., 1984, Drag and flexibility in sessile organisms. Am. Zool. 24, 37–44. CrossRefGoogle Scholar
Vogel S., 1994, Life in moving fluids, 2nd edn. Princeton University Press, Princeton, NJ.
Waite, J.H., 2002, Adhésion à la moule. Integr. Comp. Biol. 42, 1172–1180. CrossRefGoogle ScholarPubMed
Waite, J.H., Vaccaro, E., Sun, C., Lucas, J.M., 2002, Elastomeric gradients: a hedge against stress concentration in marine holdfasts? Phil. Trans. R. Soc. Lond. B. 357, 143–153. CrossRefGoogle Scholar
Walter, U., Liebezeit, G., 2003, Efficiency of blue mussel (Mytilus edulis) spat collectors in highly dynamic tidal environments of the Lower Saxonian coast (southern North Sea). Biomol. Eng. 20, 407–411. CrossRefGoogle Scholar
Widdows, J., Bayne, B.L., 1971, Temperature acclimation of Mytilus edulis with reference to its energy budget. J. Mar. Biol. Assoc. UK 51, 827–843. CrossRefGoogle Scholar
Wilson, B., 1968, Survival and reproduction of the mussel Xenostrobus securis (Lam.) (Mollusca-Bivalvia-Mytilidae) in a Western Australian estuary. I. Salinity tolerance. J. Nat. Hist. 2, 307–328. CrossRefGoogle Scholar
Yamamoto, H., 1995, Marine adhesive proteins and some biotechnological applications. Biotechnol. Genet. Eng. 13, 133–165. CrossRefGoogle ScholarPubMed
Yonge, C.M., 1962, On the primitive significance of the byssus in the Bivalvia and its effects in evolution. J. Mar. Biol. Assoc. UK 42, 113–125. CrossRefGoogle Scholar
Young, G.A., 1985, Byssus-thread formation by the mussel Mytilus edulis: effects of environmental factors. Mar. Ecol. Prog. Ser. 24, 261–271. CrossRefGoogle Scholar
Zardi, G.I., Nicastro, K.R., Mc Quaid, C.D., Rius, M., Porri, F., 2006, Hydrodynamic stress and habitat partitioning between indigenous (Perna perna) and invasive (Mytilus galloprovincialis) mussels: constraints of an evolutionary strategy. Mar. Biol. 150, 79–88. CrossRefGoogle Scholar
Zardi, G.I., McQuaid, C.D., Nicastro, K.R., 2007, Balancing survival and reproduction: seasonality of wave action, attachment strength and reproductive output in indigenous Perna perna and invasive Mytilus galloprovincialis mussels. Mar. Ecol. Prog. Ser. 334, 155–163. CrossRefGoogle Scholar
Zardi, G.I., Nicastro, K.R., Mc Quaid, C.D., Erlandsson, J., 2008, Sand and wave induced mortality in invasive (Mytilus galloprovincialis) and indigenous (Perna perna) mussels. Mar. Biol. 153, 853–858. CrossRefGoogle Scholar