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Biochemical and genetic characteristics of suspension-cultured mussels (Mytilus edulis) in relation to byssal thread production and losses by fall-off

Published online by Cambridge University Press:  14 June 2011

Andrée-Anne Lachance
Affiliation:
Institut des sciences de la mer, Université du Québec à Rimouski, 310 allée des Ursulines, Rimouski, Québec, G5L 3A1, Canada
Remy Hennebicq
Affiliation:
Institut des sciences de la mer, Université du Québec à Rimouski, 310 allée des Ursulines, Rimouski, Québec, G5L 3A1, Canada
Bruno Myrand
Affiliation:
Centre maricole des Îles-de-la-Madeleine, MAPAQ, 107-125 chemin du Parc, Cap-aux-Meules, Québec, G4T 1B3, Canada
Jean-Marie Sévigny
Affiliation:
Pêches et Océans Canada, Institut Maurice-Lamontagne, 850 route de la mer, C.P. 1000 Mont-Joli, Québec, G5H 3Z4, Canada
Edouard Kraffe
Affiliation:
CEMCA UMR CNRS 6521, Université de Bretagne occidentale, CS 93837, 29238 Brest Cedex 3, France
Yanic Marty
Affiliation:
CEMCA UMR CNRS 6521, Université de Bretagne occidentale, CS 93837, 29238 Brest Cedex 3, France
Isabelle Marcotte
Affiliation:
Département de chimie, Université du Québec à Montréal, C.P. 8888, Succursale Centre-ville, Montréal, Québec, H3C 3P8, Canada
Réjean Tremblay*
Affiliation:
Institut des sciences de la mer, Université du Québec à Rimouski, 310 allée des Ursulines, Rimouski, Québec, G5L 3A1, Canada
*
aCorresponding author: rejean_tremblay@uqar.qc.ca
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Abstract

Mussel culture relies on the mussel self-attachment capacity through byssus production. By doing so, no cages or containment devices are needed. It has been previously suggested that thread production requires a non-negligible part of the energy expenditure in blue mussels Mytilus edulis. Therefore our work investigates the relationships between byssal thread production, mussels energetic reserves and phospholipids profiles in the foot. The relationship between thread production and heterozygosity was also examined. The study was realized in a small lagoon of the Îles-de-la-Madeleine, southern Gulf of St. Lawrence, Canada, on four sampling dates between June and September encompassing the pre- to post-spawning periods. Our results show a significant relationship between the thread numbers and attachment strength. However, no correlations were found between energy reserves, phospholipids composition of the foot or heterozygosity level and byssal production. Our results suggest that mussels in suspension culture in this lagoon were not energy-limited so that the energy reserves did not influence the byssal thread production.

Type
Research Article
Copyright
© EDP Sciences, IFREMER, IRD 2011

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References

Alfaro, A.C., 2005, Effect of water flow and oxygen concentration on early settlement of the New Zealand green-lipped mussel, Perna canaliculus. Aquaculture 246, 285294. CrossRefGoogle Scholar
Alfaro, A.C., 2006, Byssal attachment of juvenile mussels, Perna canaliculus, affected by water motion and air bubbles. Aquaculture 255, 357361. CrossRefGoogle Scholar
Babarro, J., Reiriz, M., 2010, Secretion of byssal threads in Mytilus galloprovincialis: quantitative and qualitative values after spawning stress. J. Comp. Physiol. 180, 95104. CrossRefGoogle ScholarPubMed
Bairati, A., Vitellaro-Zuccarello, L., 1976, The ultrastructure of the byssal apparatus of Mytilus galloprovincialis. IV. Observations by transmission electron microscopy. Cell Tissue Res. 166, 219234. CrossRefGoogle ScholarPubMed
Bayne B.L., Newell R.C., 1983, Physiological energetics of marine molluscs. In: Saleuddin A.S.M., Wilbur K.M. (Eds.), The Mollusca. London, Academic Press, pp. 407–515.
Bayne, B.L., Widdows, J., 1978, The physiological ecology of two populations of Mytilus edulis L. Oecologia 37, 137162. CrossRefGoogle ScholarPubMed
Belkhir K., Borsa P., Goudet J., Chikhi L., Bonhomme F., 1998, Genetix, logiciel sous WindowTM pour la génétique des populations, Laboratoire génome et populations, CNRS UPR 9060, Université de Montpellier II, Montpellier.
Bell, E.C., Gosline, J.M., 1996, Mechanical design of mussel byssus: Material yield enhances attachment strength. J. Exp. Biol. 199, 10051017. Google ScholarPubMed
Bell, E.C., Gosline, J.M., 1997, Strategies for life in flow: tenacity, morphometry, and probability of dislodgment of two Mytilus species. Mar. Ecol. Prog. Ser. 159, 197208. CrossRefGoogle Scholar
Benedict, C., Waite, J.H., 1986, Composition and ultrastructure of the byssus of Mytilus edulis. J. Morphol. 189, 261270. CrossRefGoogle ScholarPubMed
Blanco, S.L., Suárez, M.P., San Juan, F., 2006, Seasonal changes of nucleotides in mussel (Mytilus galloprovincialis) mantle tissue. Comp. Biochem. Physiol. 143B, 384390. CrossRefGoogle Scholar
Bourque F., Myrand B., 2006, Étude descriptive du dégrappage en milieu lagunaire aux Îles-de-la-Madeleine, MAPAQ, DIT, Rapport de R-D. No. 152.
Calder, P.C., Yaqoob, P., 2007, Lipid rafts – Composition, characterization, and controversies. J. Nutr. 137, 545547. Google Scholar
Carrington, E., 2002, Seasonal variation in the attachment strength of blue mussels: causes and consequences. Limnol. Oceanogr. 47, 17231733. CrossRefGoogle Scholar
Cartier, S., Pellerin, J., Fournier, M., Tamigneaux, E., Girault, L., Lemaire, N., 2004, Use of an index based on the blue mussel (Mytilus edulis and Mytilus trossulus) digestive gland weight to assess the nutritional quality of mussel farm sites. Aquaculture 241, 633654. CrossRefGoogle Scholar
Clarke K.R., Warwick R.M., 2001, Change in marine communities: an approach to statistical analysis and interpretation, 2nd edn. PRIMER-E, Plymouth.
Clarke, M., 1999, The effect of food availability on byssogenesis by the zebra mussel (Dreissena polymorpha Pallas). J. Mollusc. Stud. 65, 329333. CrossRefGoogle Scholar
Coyne, K.J., Qin, X.X., Waite, J.H., 1997, Extensible collagen in mussel byssus: A natural block copolymer. Science 277, 18301832. CrossRefGoogle ScholarPubMed
Dolmer, P., Svane, I., 1994, Attachment and orientation of Mytilus edulis L. in flowing water. Ophelia 40, 6374. CrossRefGoogle Scholar
Epp, J., Bricelj, V.M., Malouf, R.E., 1988, Seasonal partitioning and utilization of energy reserves in two age classes of the bay scallop Argopecten irradians irradians (Lamarck). J. Exp. Mar. Biol. Ecol. 121, 113136. CrossRefGoogle Scholar
Folch, J., Lees, M., Sloane-Stanlez, G.H., 1957, A simple method for the isolation and purification of total lipids from animal tissues. J. Biol. Chem. 226, 497509. Google ScholarPubMed
Fréchette, M., Bergeron, P., Gagnon, P., 1996, On the use of self-thinning relationships in stocking experiments. Aquaculture 145, 91112. CrossRefGoogle Scholar
Freites, L., Fernandez-Reiriz, M.J., Labarta, U., 2002, Lipid classes of mussel seeds Mytilus galloprovincialis of subtidal and rocky shore origin. Aquaculture 207, 97111. CrossRefGoogle Scholar
Gentili, M.R., Beaumont, A.R., 1988, Environmental stress, heterozygosity, and growth rate in Mytilus edulis L. J. Exp. Mar. Biol. Ecol. 120, 145153. CrossRefGoogle Scholar
Gosling E.M., 1992, Genetics of Mytilus, The mussel Mytilus: ecology, physiology, genetics, Developments in aquaculture and fisheries science, Elsevier, Amsterdam, pp. 309–380.
Goudet, J., 2001, FSTAT, a program to estimate and test gene diversities andfixation indices (version 2.9.3.2), Updated from Goudet 1995, FSTAT version 1.2: acomputer program to calculate F-statistics. J. Hered. 86, 485486. CrossRefGoogle Scholar
Hawkins, A.J.S., 1985, Relationships between the synthesis and breakdown of protein, dietary absorption and turnovers of nitrogen and carbon in the blue mussel, Mytilus edulis L. Oecologia 66, 4249. CrossRefGoogle ScholarPubMed
Hawkins, A.J.S., Bayne, B.L., 1991, Nutririon of marine mussels: factors influencing the relative utilizations of protein and energy. Aquaculture 94, 177196. CrossRefGoogle Scholar
Hawkins, A.J.S., Day, A.J., 1996, The metabolic basis of genetic differences in growth efficiency among marine animals. J. Exp. Mar. Biol. Ecol. 203, 93115. CrossRefGoogle Scholar
Hazel, J.R., Williams, E.E., 1990, The role of alterations in membrane lipid composition in enabling physiological adaptation of organisms to their physical environment. Prog. Lipid Res. 29, 167227. CrossRefGoogle Scholar
Holten-Andersen, N., Harrington, M.J., Birkedal, H., Lee,, B.P., Messersmith, P.B., Lee, K.Y.C., Waite, J.H., 2011, pH-induced metal-ligand cross-links inspired by mussel yield self-healing polymer networks with near-covalent elastic moduli. Proc. Nat. Acad. Sci. USA 108, 26512655. CrossRefGoogle ScholarPubMed
Hulbert, A.J., Else, P.L., 1999, Membranes as possible pacemakers ofmetabolism. J. Theor. Biol. 199, 257274. CrossRefGoogle Scholar
Hulbert, A.J., 2003, Life, death and membrane bilayers. J. Exp. Biol. 206, 23032311. CrossRefGoogle ScholarPubMed
Hunt, H.L., Scheibling, R.E., 2001, Predicting wave dislodgment of mussels: variation in attachment strength with body size, habitat, and season. Mar. Ecol. Prog. Ser. 213, 157164. CrossRefGoogle Scholar
Hunt, H.L., Sheibling, R.E., 2002, Movement and wave dislodgment of mussels on a wave-exposed rocky shore. Veliger 45, 273277. Google Scholar
Kraffe, E., Soudant, P., Marty, Y., 2004, Fatty acids of serine, ethanolamine, and choline plasmalogens in some marine bivalves. Lipids 39, 5966. CrossRefGoogle Scholar
Kraffe, E., Tremblay, R., Belvin, S., LeCoz, J.-R., Marty, Y., Guderley, H., 2008, Effect of reproduction on escape responses, metabolic rates and muscle mitochondrial properties in the scallop Placopecten magellanicus. Mar. Biol. 156, 2538. CrossRefGoogle Scholar
Lachance, A.A., Myrand, B., Tremblay, R., Koutitonsky, V., Carrington, E., 2008, Biotic and abiotic factors influencing attachment strength of blue mussels Mytilus edulis in suspended culture. Aquat. Biol. 2, 119129. CrossRefGoogle Scholar
Le Grand, F., Kraffe, E., Marty, Y., Donaghy, L., Soudant, P., 2011, Membrane phospholipid compositions of hemocytes in the Pacific oyster Crassostrea gigas and the Manila clam Ruditapes philippinarum. Comp. Biochem. Physiol. 159, 383391. CrossRefGoogle ScholarPubMed
LeBlanc, N., Tremblay, R., Davidson, J., Landry, T., McNiven, M., 2008, The effect of selection treatments on Mytilus edulis, modifications of genetic and physiological characteristics. Mar. Biol. 153, 11421152. CrossRefGoogle Scholar
Lee, C.Y., Shirley, S., Lim, L., Owen, M.D., 1990, The rate and strength of byssal reattachment by blue mussels (Mytilus edulis L.). Can. J. Zool. 68, 20052009. CrossRefGoogle Scholar
Lemaire, N., Pellerin, J., Fournier, M., Girault, L., Tamigneaux, E., Cartier, S., Pelletier, E., 2006, Seasonal variations of physiological parameters in the blue mussel Mytilus spp. from farm sites of eastern Quebec. Aquaculture 261, 729751. CrossRefGoogle Scholar
Mahéo, R., 1968, Observations sur l’anatomie et le fonctionnement du complexe byssogène de Chlamys varia L. Cah. Biol. Mar. 9, 373379. Google Scholar
Mallet A., Myrand B., 1995, The culture of the blue mussel in Atlantic Canada. In: Boghen A.D. (Ed.), Cold-Water Aquaculture in Atlantic Canada, 2nd edn. Moncton, Canada, Canadian Institute for Research on Regional Development, pp. 255–296.
Marty, Y., Delaunay, F., Moal, J., Samain, J.-F., 1992, Changes in the fatty acid composition of Pecten maximus (L.) during larval development. J. Exp. Mar. Biol. Ecol. 163, 221234. CrossRefGoogle Scholar
Monahan, J., Wilker, J.J., 2004, Cross-linking the protein precursor of marine mussel adhesives: bulk measurements and reagents for curring. Langmuir 20, 37243729. CrossRefGoogle Scholar
Myrand, B., Guderley, H., Himmelman, J.H., 2000, Reproduction and summer mortality of blue mussels Mytilus edulis in the Magdalen Islands, southern Gulf of St. Lawrence. Mar. Ecol. Prog. Ser. 197, 193207. CrossRefGoogle Scholar
Myrand, B., Tremblay, R., Sévigny, J.-M., 2002, Selection against blue mussels (Mytilus edulis L.) homozygotes under various stressful conditions. J. Hered. 93, 238248. CrossRefGoogle ScholarPubMed
Myrand, B., Tremblay, R., Sévigny, J.-M., 2009a, Decreases in multi-locus heterozygosity in suspension-cultured mussels (Mytilus edulis) through loss of the more heterozygous individuals. Aquaculture 295, 188194. CrossRefGoogle Scholar
Myrand, B., Tremblay, R., Sévigny, J.-M., 2009b, Impact of suspension culture using mesh sleeves on genetic characteristics of Mytilus edulis L. in Canada. Aquaculture 291, 147153. CrossRefGoogle Scholar
Parrish, C., 1987, Separation of aquatic lipid classes by chromarod thin-layer chromatography with measurement by Iatroscan Flame Ionization detection. Can. J. Fish. Aquat. Sci. 44, 722731. CrossRefGoogle Scholar
Pernet, F., Tremblay, R., Comeau, L., Guderley, H., 2007, Temperature adaptation in two bivalve species from different thermal habitat: energetic and remodeling of membrane lipids. J. Exp. Biol. 210, 29993014. CrossRefGoogle Scholar
Phillips, R., Ursell, T., Wiggins, P., Sens, P., 2009, Emerging roles for lipids in shaping membrane-protein function. Nature 459, 379385. CrossRefGoogle ScholarPubMed
Pieters, H., Kluytmans, J.H., Zandee, D.I., Cadee, G.C., 1980, Tissue composition and reproduction of Mytilus edulis in relation to food availability. Neth. J. Sea Res. 14, 349361. CrossRefGoogle Scholar
Racotta, I.S., Ramirez, J.L., Ibarra, A.M., Rodriguez-Jaramillo, M.C., Carreno, D., Palacios, E., 2003, Growth and gametogenesis in the lion-paw scallop Nodipecten (Lyropecten) subnodosus. Aquaculture 217, 335349. CrossRefGoogle Scholar
Rodhouse, P.G., Roden, C.M., Hensey, M.P., Ryan, T.H., 1984, Ressource allocation in Mytilus edulis on the shore and in suspended culture. Mar. Biol. 84, 2734. CrossRefGoogle Scholar
Scott, T.M., Koehn, R.K., 1990, The effect of environmental stress on the relationship of heterozygosity to growth rate in the coot clam Mulinia lateralis (Say). J. Exp. Biol. Ecol. 135, 109116. CrossRefGoogle Scholar
Seed, R., Richardson, C.A., 1999, Evolutionary traits in Perna viridis (Linnaeus) and Septifer virgatus (Wiegmann) (Bivalvia: Mytilidae). J. Exp. Mar. Biol. Ecol. 239, 273287. CrossRefGoogle Scholar
Sénéchal, J., Grant, J., Archambault, M.-C., 2008, Experimental manipulation of suspended culture socks: growth and behavior juvenile mussels (Mytilus spp.). J. Shellfish Res. 27, 811826. CrossRefGoogle Scholar
Soo Hwang, D., Zeng, H., Masic, A., Harrington, M.J., Israelachvili, J.N., Waite, J.H., 2010, Protein- and metal-dependent interactions of a prominent protein in mussel adhesive plaques. J. Biol. Chem. 285, 2585025858. CrossRefGoogle Scholar
Stuart, J.A., Gillis, T.E., Ballantyne, J.S., 1998, Compositional correlates of metabolic depression in the mitochondrial membranes of estivating snails. Am. J. Physiol. Regul. Integr. Comp. Physiol. 44, R1977R1982. Google Scholar
Thieltges, D.W., Buschbaum, C., 2007, Mechanism of an epibiont burden: Crepidula fornicata increases byssus thread production by Mytilus edulis. J. Mollusc. Stud. 73, 7577. CrossRefGoogle Scholar
Tremblay, R., Myrand, B., Sevigny, J.-M., 1998a, Genetic characterization of wild and suspension-cultured blue mussels (Mytilus edulis Linneaus, 1758) in the Magdalen Islands (southern Gulf of St. Lawrence, Canada). J. Shellfish Res. 17, 11911202. Google Scholar
Tremblay, R., Myrand, B., Sévigny, J.-M., Blier, P., Guderley, H., 1998b, Bioenergetic and genetic parameters in relation to susceptibility of blue mussels, Mytilus edulis (L.) to summer mortality. J. Exp. Mar. Biol. Ecol. 221, 2758. CrossRefGoogle Scholar
Waite, J.H., 2002, Adhésion à la moule. Int. Comp. Biol. 42, 11721180. CrossRefGoogle ScholarPubMed
Weir, B.S., Cockerham, C.C., 1984, Estimating F-statistics for the analysis of population structure. Evolution 38, 13581370. Google ScholarPubMed
Young, G.A., 1985, Byssus-thread formation by the mussel Mytilus edulis: effects of environmental factors. Mar. Ecol. Prog. Ser. 24, 261271. 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, 155163. CrossRefGoogle Scholar
Zehmer, J.K., Hazel, J.R., 2005, Thermally induced changes in lipid composition of raft and non-raft regions of hepatocyte plasma membranes of rainbow trout. J. Exp. Biol. 208, 42834290. CrossRefGoogle ScholarPubMed