Hostname: page-component-848d4c4894-cjp7w Total loading time: 0 Render date: 2024-07-08T00:09:55.902Z Has data issue: false hasContentIssue false
  • English
  • Français

Review and perspectives of physiological mechanisms underlying genetically-based resistance of the Pacific oyster Crassostrea gigas to summer mortality

Published online by Cambridge University Press:  27 September 2011

Jean-François Samain
Jean-François Samain*
Affiliation:
Ifremer, Centre de Brest, BP 70, 29280 Plouzané, France
*
aCorresponding author: [email protected]
Get access

Abstract

French oyster farming has been subject to severe mortalities during the summer months. Results from the research program “Morest”, which ran from 2000 to 2006 and examined the possible causes of these mortalities, led to the construction of a model to explain the interaction between environmental factors, oyster physiology and different opportunistic pathogens underlying oyster summer mortality. Temperature, food, reproduction and stress were the main factors required for oyster mortality. Genetically-based resistance (“R” oysters) or susceptibility (“S” oysters) to summer mortality was revealed by divergent selection. Building on these results, a literature search was made in 2007 on the molecular origin of genetic resistance to such a complex mortality risk. The objectives were to lay a foundation for the preparation and orientation of future research directions and to improve understanding of the underlying physiological mechanism leading to summer mortality. Three years later, the resulting conceptual analysis reported here was presented as an introductory lecture to Physiomar 2010, a conference where many new results contributing to this research field were also reported. The literature review highlighted two major review articles: the first dealing with nutrition and reproduction (Schneider 2004), the second with reproduction, temperature, oxidative stress and mortality (Heineinger 2002). The effect of nutrition level on energy orientation to growth or reproduction is controlled by endocrine factors. Among these, neuropeptide Y (NPY), ghrelin and leptin neuropeptides appeared to be potential candidates involved in germ-soma orientation in relation to trophic conditions. Depending on reproductive effort and temperature, a metabolic stress resulting from the germ-soma conflict can appear, characterized by mitochondrial reactive oxygen species (ROS) production. Such an excess of ROS induces perturbations in mitochondrial activity leading to cell death. Many organisms, such as annual plants or the Pacific salmon, do not survive their first reproduction. In contrast, others increase stress resistance by selection of antioxidant processes (superoxide dismutase SOD, catalase, etc.) through evolution, and survive first reproduction. A similar difference was observed in the comparison made between R and S oysters, which differed in ROS production, SOD and catalase levels. Such factors controlling reproduction and ROS detoxification processes could therefore provide new markers for selection of oysters with better resistance to non-specific pathogens, complementing other classic selection approaches against specific pathogens or for improved immunity. This antioxidant defence mechanism is found in many organisms including vertebrates and in some invertebrates, including oysters. Its role needs to be considered in pathology events involving other aquaculture species and it may also contribute to explaining the increase in marine pathologies under anthropogenic environmental changes.

Keywords

ImmunityAntibacterial activityHost defenceEnvironmental stressCrassostrea gigas
Type
Research Article
Information
Aquatic Living Resources , Volume 24 , Issue 3: Physiomar10 , July 2011 , pp. 227 - 236
Copyright
© EDP Sciences, IFREMER, IRD 2011

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

Abele, D., Strahl, J., Brey, T., Philipp, E.E.R., 2008, Imperceptible senescence: Ageing in the ocean quahog Arctica islandica. Free Radical Res. 42, 474–480. CrossRefGoogle ScholarPubMed
Allen, S.K, Downing, S.L., 1986, Performance of triploid Pacific oysters, Crassostrea gigas (Thunberg). I. Survival, growth, glycogen content, and sexual maturation in yearlings. J. Exp. Mar. Biol. Ecol. 102, 197–208. CrossRefGoogle Scholar
Barja, G., 2000, The flux of free radical attack through mitochondrial DNA is related to aging rate. Aging Clin. Exp. Res. 12, 342–355. CrossRefGoogle ScholarPubMed
Bayne B.L., Newell R.C., 1983, Physiological energetics of marine molluscs. In: Wilbur K.M., Saleuddin A.S. (Eds.), The Mollusca, Vol. 4. Academic Press, New York, pp. 407–515
Boudry P., Dégremont L., Haffray P., 2008, The genetic basis of summer mortality in Pacific oyster spat and potential for improving survival by selective breeding in France. In: Samain J.F., McCombie H. (Eds.) Summer mortality of Pacific oyster Crassostrea gigas. The Morest Project. Quae, Versailles, pp. 153–196.
Buttemer, W.A., Abele, D., Costantini, D., 2010, The ecology of antioxidants and oxidative stress in animals. From bivalves to birds: oxidative stress and longevity. Funct. Ecol. 24, 971–983. Google Scholar
da Silva, P.M., Fuentes, J., Villalba, A., 2009, Differences in gametogenic cycle among strains of the European flat oyster Ostrea edulis and relationship between gametogenesis and bonamiosis. Aquaculture 287, 253–265. CrossRefGoogle Scholar
De Decker, S., Normand, J., Saulnier, D., Pernet, F., Castagnet, S., Boudry, P., 2011, Responses of diploid and triploid Pacific oysters Crassostrea gigas to Vibrio infection in relation to their reproductive status. J. Invertebr. Pathol. 106, 179–19. CrossRefGoogle ScholarPubMed
Dégremont L., 2003, Etude des bases génétiques de la mortalité estivale et des relations avec la croissance chez les juvéniles de l’huître creuse Crassostrea gigas. Thèse Doctorat Univ. Caen.
Dégremont, L., Ernande, B., Bedier, E., Boudry,, P., 2007, Summer mortality of hatchery-produced Pacific oyster spat (Crassostrea gigas). I. Estimation of genetic parameters for survival and growth. Aquaculture 262, 41–53. CrossRefGoogle Scholar
Delaporte, M., Soudant, P., Lambert, C., Jegaden, M., Moal, J., Pouvreau, S., Degremont, L., Boudry, P., Samain, J.F., 2007, Characterisation of physiological and immunological differences between Pacific oysters (Crassostrea gigas) genetically selected for high or low survival to summer mortalities and fed different rations under controlled conditions. J. Exp. Mar. Biol. Ecol. 353, 45–57. CrossRefGoogle Scholar
Duchemin, M.B., Fournier, M., Auffret, M., 2006, Seasonal variations of immune parameters in diploid and triploid Pacific oysters, Crassostrea gigas (Thunberg). Aquaculture 264, 73–81. CrossRefGoogle Scholar
Duperthuy, M., Schmitt, P., Garzon, E., Caro, A., Rosa, R.D., Le Roux, F., Lautredou-Audouy, N., Got, P., Romestand, B., de Lorgeril, J., Kieffer-Jaquinod, S., Bachère, E., Destoumieux-Garzon, D., 2011, Use of OmpU porins for attachment and invasion of Crassostrea gigas immune cells by the oyster pathogen Vibrio splendidus. Proc. Nat. Acad. USA 108, 2993–2998. CrossRefGoogle ScholarPubMed
Fabioux, C., Corporeau, C., Quillien, V., Favrel, P., Huvet, A., 2009, In vivo RNA interference in oyster vasa silencing inhibits germ cell development. FEBS J. 276, 2566–2573. CrossRefGoogle ScholarPubMed
Fabioux, C., Pouvreau, S., Le Roux, F., Huvet, A., 2004, The oyster vasa-like gene: a specific marker of the germ line in Crassostrea gigas. Biochem. Biophys. Res. Comm. 315, 897–904. CrossRefGoogle ScholarPubMed
Fleury, E., Fabioux, C., Lelong, C., Favrel, P., Huvet, A., 2008, Characterization of a gonad-specific transforming growth factor-beta superfamily member differentially expressed during the reproductive cycle of the oyster Crassostrea gigas. Gene 410, 187–196. CrossRefGoogle ScholarPubMed
Fleury, E., Huvet, A., Lelong, C., de Lorgeril, J., Boulo, V., Gueguen, Y., Bachère, E., Tanguy, A., Moraga, D., Fabioux, C., Lindeque, P., Shaw, J., Reinhardt, R., Prunet, P., Davey, G., Lapegue, S., Sauvage, C., Corporeau, C., Moal, J., Gavory, F., Wincker, P., Moreews, F., Klopp, C., Mathieu, M., Boudry, P., Favrel, P., 2009, Generation and analysis of a 29 745 unique expressed sequence tags from the Pacific oyster (Crassostrea gigas) assembled into a publicly accessible database: the Gigas Database. BMC Genomics 10, 341. CrossRefGoogle ScholarPubMed
Fleury, E., Moal, J., Boulo, V., Daniel, J.Y., Mazurais, D., Hénaut, A., Corporeau, C., Boudry, P., Favrel, P., Huvet, A., 2010, Microarray-based identification of gonad transcripts differentially expressed between lines of Pacific oyster selected to be resistant or susceptible to summer mortality. Mar. Biotechnol. 12, 326–339. CrossRefGoogle Scholar
Fleury E., Huvet A., 2011, Microarray analysis highlights immune response of Pacific oysters as a determinant of resistance to summer mortality syndrome. Mar. Biotechnol. in press DOI: 10.1007/s10126-011-9403-6.
Franco A., Kellner K., Mathieu M., Lelong C., Goux D., Heude- Berthelin C., 2011, Male germ cells of the Pacific oyster Crassostrea gigas: flow cytometry analysis, cell sorting and molecular expression. Aquat.Living Resour. 24.
Gabitta, S.P., Butterfield, D.A., Hensley, K., Shaw, W., Carney, J.M., 1997, Aging and caloric restriction affect mitochondrial respiration and lipid membrane status: an electron paramagnetic resonance investigation. Free Radic. Biol. Med. 23, 191–201. CrossRefGoogle Scholar
Gaikwad, A., Biju, K.C., Saha, S.G., Subhedar, N., 2004, Neuropeptide Y in the olfactory system, forebrain and pituitary of the teleost, Clarias batrachus. J. Chem. Neuroanat. 27, 55–70. CrossRefGoogle ScholarPubMed
Gagnaire, B., Soletchnik, P., Madec, P., Geairon, P., Le Moine, O., Renault, T., 2006, Diploid and triploid Pacific oysters, Crassostrea gigas (Thunberg), reared at two heights above sediment in Marennes-Oleron Basin, France: difference in mortality, sexual maturation and hemocyte parameters. Aquaculture 254, 606–616. CrossRefGoogle Scholar
Gonzalez, M., Gueguen, Y., Desserre, G., de Lorgeril, J., Romestand, B., Bachère, E., 2007, Molecular characterization of two isoforms of defensin from hemocytes of the oyster Crassostrea gigas. Dev. Comp. Immunol. 31, 332–339. CrossRefGoogle ScholarPubMed
Grangere, K., Menesguen, A., Lefebvre, S., Bacher, C., Pouvreau, S., 2009, Modelling the influence of environmental factors on the physiological status of the Pacific oyster Crassostrea gigas in an estuarine embayment; The Baie des Veys (France). J. Sea Res. 62 Special Issue, 147–158. CrossRefGoogle Scholar
Guderley, H., Brokordt, K., Pérez Cortés, H.M., Marty, Y., Kraffe, E., 2011, Diet and performance in the scallop, Argopecten purpuratus: force production during escape responses and mitochondrial oxidative capacities. Aquat.Living Resour. 24, 3. CrossRefGoogle Scholar
Gueguen, Y., Bernard, B., Fievet, J., Schmitt, P., Destoumieux-Garzón, D., Vandenbulcke, F., Bulet, P., Bachère, E., 2009, Oyster hemocytes express a proline-rich peptide displaying synergistic antimicrobial activity with a defensin. Mol. Immunol. 46, 516–522. CrossRefGoogle Scholar
Gueguen, Y., Cadoret, J.P., Flament, D., Barreau-Roumiguière, C., Girardot, A.L., Garnier, J., Hoareau, A., Bachère, E., Escoubas, J.M., 2003, Immune gene discovery by expressed sequence tags generated from hemocytes of the bacteria-challenged oyster Crassostrea gigas. Gene 303, 139–145. CrossRefGoogle ScholarPubMed
Guo X., DeBrosse G.A., Allen S.K., 1996, All-triploid Pacific oysters (Crassostrea gigas Thunberg) produced by mating tetraploids and diploids. Aquaculture 149–161.
Handley, S.J., 1997, Optimizing subdital oyster production, Marlborough Sounds, New Zealand: spionid polychaete infestations, water depth and spat stunting. J. Shellfish Res. 16, 143–150. Google Scholar
Heininger, K., 1999, A unifiying hypothesis of Alzheimer’s disease. I. Ageing sets the stage. Hum. Psychopharmacol. Clin. Exp. 14, 363–414. 3.0.CO;2-R>CrossRefGoogle Scholar
Heininger, K., 2001, The deprivation syndrome is the driving force of phylogeny, ontogeny and oncogeny. Rev. Neurosci. 12, 217–287. CrossRefGoogle ScholarPubMed
Heininger, K., 2002, Aging is a deprivation syndrome driven by a germ-soma conflict. Ageing Res. Rev. 1, 481–536. CrossRefGoogle ScholarPubMed
Hewes, R.S., Taghert, P.H., 2001, Neuropeptides and neuropeptide receptors in the Drosophila melanogaster genome. Genome Res. 11, 1126–1142. CrossRefGoogle ScholarPubMed
Hosono, R., Nishimoto, S., Kuno, S., 1989, Alteration of life span in the nematode Caenorhabditis elegans under monoxenic culture conditions. Exp. Gerontol. 24, 251–264. CrossRefGoogle ScholarPubMed
Huvet, A., Normand, J., Fleury, E., Quillien, V., Fabioux, C., Boudry, P., 2010, Reproductive effort of Pacific oysters: a trait associated with susceptibility to summer mortality. Aquaculture 304, 95–99. CrossRefGoogle Scholar
Huvet A., Royer J., Moal J., Burgeot T., Lapègue S., Boulo V., Nicolas J.L., Lambert C., Van Wormhoudt A., Samain J.F., 2008, Phenotypic characteristics of “R” and “S” oysters lines, selected for resistance or susceptibility to summer mortality In: Samain J.F., McCombie H. (Eds.), Summer mortality of Pacific oyster Crassostrea gigas. The Morest Project, Quae, Versailles, pp. 197–241.
Jeschke J.M., Gabriel W., Kokko H., 2008, r-Strategist/K-Strategists. In: Jørgensen S.E., Fath B.D. (Eds.). Encyclopedia of Ecology, pp. 3113–3122.
Jiang H., Ren F., Sun J., He L., Li W., 2010, Molecular cloning and gene expression analysis of the leptin receptor in the Chinese mitten crab Eriocheir sinensis. PLoSone 5(6), e11175. doi:10.1371/journal.pone.0011175.
Johnson, R.M., Johnson, T.M., Londraville, R.L., 2000, Evidence for leptin expression in fishes. J. Exp. Zool. 286, 718–724. 3.0.CO;2-I>CrossRefGoogle ScholarPubMed
de Jong-Brink, M., 2001, NPY in invertebrates: molecular answers to altered functions during evolution. Peptides 22, 309–315. CrossRefGoogle ScholarPubMed
Jouaux, A., Heude-Berthelin, C., Sourdaine, P., Mathieu, M., Kellner, K., 2010, Gametogenic stages in triploid oysters Crassostrea gigas: J. Exp. Mar. Biol. Ecol. 395, 162–170. CrossRefGoogle Scholar
Katayama K., Ikeda Z., Shinohara M., 1979, The growth and survival of the seed oyster Crassostrea gigas with different hardening effects. Bull. Fish. Exp. Stn. Okayama Prefect., pp. 176–180.
Kiris, I., Eroldogan, O., Kir, M., Kumlu, M., 2004, Influence of neuropeptide Y (NPY) on food intake and growth of penaeid shrimps and Marsupenaeus japonicus and Paneaus semisulcatus (Decapoda: Penaeidae). Comp. Biochem. Physiol. Part A Mol. Integr. Physiol. 139, 239–244. CrossRefGoogle Scholar
Kirkwood, T.B.L., Kowald, A., 1997, Network theory of aging. Exp. Gerontol. 32, 395–399. CrossRefGoogle Scholar
Kooijman S.A.L.M., 2000, Dynamic energy and mass budgets in biological systems. Cambridge University Press, Cambridge, UK.
Kuzmin, E.V., Karpora, O.V., Elthon, T.E., Newton, K.J., 2004, Mitochondrial respiratory deficiencies signal up-regulation of genes of heat shock proteins. J. Biol. Chem. 279, 20672–20677. CrossRefGoogle ScholarPubMed
Lambert C., Moal J., Le Moullac, Pouvreau S., 2008, Mortality risks associated with physiological traits of oysters during reproduction. In: Samain J.F., McCombie H. (Eds.), Summer mortality of Pacific oyster Crassostrea gigas. The Morest Project, Quae, Versailles, pp. 63–106.
Larsson, T.A., Larson, E.T., Fredriksson, R., Conlon, J.M., Larhammar, D., 2006, Characterization of NPY receptor subtypes Y2 and Y7 in rainbow trout Oncorhynchus mykiss. Peptides 27, 1320–1327. CrossRefGoogle Scholar
Lin, S.J., Defossez, P.A., Guarente, L., 2000, Requirements of NAD and SIR2 for life span extension by caloric restriction in Saccharomyces cerevisiae. Science 289, 2126–2128. CrossRefGoogle Scholar
MacArthur R.H., Wilson E.O., 1967, The theory of island biogeography. Princeton University Press, Princeton.
Masoro, E.J., 1998, Influence of caloric intake on aging and on the response to stressors. J. Toxicol. Environ. Health. Part B, 1, Crit. Rev. 1, 243–257. Google Scholar
Mateo, D.R., Greenwood, S.J., Araya, M.T., Berthe, F.C.J., Johnson, G.R., Siah, A., 2010, Differential gene expression of gamma-actin, Toll-like receptor 2 (TLR-2) and interleukin-1 receptor-associated kinase 4 (IRAK-4) in Mya arenaria haemocytes induced by in vivo infections with two Vibrio splendidus strains. Dev. Comp. Immunol. 34, 710–714. CrossRefGoogle Scholar
Mori, K., 1979, Effects of artificial eutrophication on the metabolism of the Japanese oyster Crassostrea gigas. Mar. Biol. 53, 361–369 CrossRefGoogle Scholar
Na, G.H., Lee, C.S., Choi, W.J., 1991, The effect of dissolved oxygen on the estival mass mortality of sea squirt Halocynthia roretzi. Bull. Korean Fish. Soc. 24, 52–58. Google Scholar
Pouvreau, S., Bourlès, Y., Lefèbvre, S., Gangnery, A., Alunno-Bruscia, M., 2006, Application of a dynamic energy budget model to the Pacific oyster, Crassostrea gigas, reared under various environmental conditions. J. Sea Res. 56, 156–167. CrossRefGoogle Scholar
Rao, G., Xia, E., Nadakavukaren, M.J., Richardson, A., 1990, Effect of dietary restriction on the age-dependent changes in the expression of antioxidant enzymes in rat liver. J. Nutr. 120, 602–609. Google ScholarPubMed
Renault, T., Faury, N., Barbosa-Solomieu, V., Moreau, K., 2011, Suppression substractive hybridisation (SSH) and real time PCR reveal differential gene expression in the Pacific cupped oyster, Crassostrea gigas, challenged with Ostreid herpesvirus 1. Dev. Comp. Immunol. 35, 725–735. CrossRefGoogle Scholar
Risby, T.H., Jiang, L., Stoll, S., Ingram, D., Spankler, E., Heim, J., Cutler, R., Roth, G.S., Rifkind, J.M., 1999, breath ethane as a marker of reactive oxygen species during manipulation of diet and oxygen tension in rats. J. Appl. Physiol. 86, 617–622. Google ScholarPubMed
Samain, J.F., Dégremont, L., Soletchnik, P., Haure, J., Bédier, E., Ropert, M., Moal, J., Huvet, A., Bacca, H., Van Wormhoudt, A., Delaporte, M., Costil, K., Pouvreau, S., Lambert, C., Boulo, V., Soudant, P., Nicolas, J.L., Le Roux, F., Renault, T., Gagnaire, B., Geret, F., Boutet, I., Burgeot, T., Boudry, P., 2007, Genetically based resistance to summer mortality in the Pacific oyster (Crassostrea gigas) and its relationship with physiological, immunological characteristics and infection processes. Aquaculture 268, 227–243. CrossRefGoogle Scholar
Samain J.F., McCombie, H., 2008, Summer mortality of Pacific oyster Crassostrea gigas. The Morest Project. Quae, Versailles.
Samain J.F., Ropert M., Bédier E., Soletchnik P., Mazurié J., Le Coz F., Blin J.L., Costil K., Mille D., Trintignac P., Boudry P., Haffray P., Bacher C., Grangeré K., Pouvreau S., Bourles Y. , Sylvand B., Misko P., Gohin F., Woerther P., 2008, A synthesis of the Morest project and recommendations for forecasting and managing oyster summer mortalities. In: Samain, J.F., McCombie H. (Eds.), Summer mortality of Pacific oyster Crassostrea gigas. The Morest Project, Quae, Versailles, pp. 307–348.
Saraiva, S., van der Meer, J., Kooijman, S.A.L.M., Sousa, T., 2011, Modelling feeding processes in bivalves: a mechanistic approach. Ecol. Model. 222, 514–523. CrossRefGoogle Scholar
Schneider, J.E., 2004, Energy balance and reproduction. Physiol. Behav. 81, 289–317. CrossRefGoogle ScholarPubMed
Segarra, A., Pépin, J.F., Arzul, I., Morga, B., Faury, N., Renault, T., 2010, Detection and description of a particular Ostreid herpes virus 1 genotype associated with massive mortality outbreaks of Pacific oysters, Crassostrea gigas, in France in 2008. Virus Res. 153, 92–99. CrossRefGoogle Scholar
Singru, P.S., Mazumdar, M., Barsagade, V., Lechan, R.M., Thim, L., Clausen, J.T., Subhedar, N., 2008, Association of cocaine- and amphetamine-regulated transcript and neuropeptide Y in the forebrain and pituitary of the catfish, Clarias batrachus: a double immuno fluorescentlabeling study. J. Chem. Neuroanat. 36, 239–50. CrossRefGoogle Scholar
Sohal, R.S., Weindruch, R., 1996, Oxidative stress, caloric restriction, and aging. Science 273, 59–63. CrossRefGoogle ScholarPubMed
Strahl, J., Abele, D., 2010, Cell turnover in tissues of the long-lived ocean quahog Arctica islandica and the short-lived scallop Aequipecten opercularis. Mar. Biol. 157, 1283–1292. CrossRefGoogle Scholar
Sussarellu, R., Fabioux, C., Le Moullac, G., Fleury, E., Moraga, D., 2010, Transcriptomic response of the Pacific oyster Crassostrea gigas to hypoxia. Mar. Genom. 3, 133–143. CrossRefGoogle ScholarPubMed
Tensen, C.P., Cox, K.J., Burke, J.F., Leurs, R., van der Schors, R.C., Geraerts, W.P., Vreugdenhil, E., Heerikhuizen, H., 1998, Molecular cloning and characterization of an invertebrate homologue of a neuropeptide Y receptor. Eur. J. Neurosci. 10, 3409–3416. CrossRefGoogle ScholarPubMed
Terashima, S., Katayama, K., Shinohara, M., Ikeda, Z., 1978, Hardening methods of the seed oyster, Crassostrea gigas for the culture of the oyster. Bull. Fish. Exp. Stn. Okayama Prefect. 3, 150–156. Google Scholar
Travers, M.A., Le Goïc, N., Huchette, S., Koken, M., Paillard, C., 2008, Summer immune depression associated with increased susceptibility of the European abalone, Haliotis tuberculata to Vibrio harveyi infection. Fish Shellfish Immunol. 25, 800–808. CrossRefGoogle ScholarPubMed
Unniappan, S., Peter, R.E., 2005, Structure, distribution and physiological functions of ghrelin in fish. Comp. Biochem.Physiol. Part A Mol. Integr. Physiol. 140, 396–408. CrossRefGoogle Scholar
Wanagat J., Weindruch R., 2000, Caloric restriction and aging : studies in rodent and primates. In: Morley J.E., Armbrecht H.T., Coe R.M., Vellas B. (Eds.), The sciences of geriatrics. Serdi Publisher, Paris, pp. 153–165.
Warren C.E., Davis G.E., 1967, Laboratory studies on the feeding, bioenergetics and growth of fishes. In: Gerking S.D. (Ed.), The Biological Basis of Freshwater Fish Production. Blackwell Scientific Publications, Oxford, pp. 175–214.
Weindruch R., Walford R.L., 1988, The retardation of aging and disease by dietary restriction. Thomas C.C. (Ed.) Springfield IL.
Widdows, J., Johnson, D., 1988, Physiological energetics of Mytilus edulis: scope for growth. Mar. Ecol. Prog. Ser. 46, 113–12. CrossRefGoogle Scholar
Xiao, J., Ford, S.E., Yang, H., Zhang, G., Zhang, F., Guo, X., 2005, Studies on mass summer mortality of cultured zhikong scallops (Chlamys farreri Jones et Preston) in China. Aquaculture 250, 602–615.CrossRefGoogle Scholar