Mass mortalities of Pacific oysters Crassostrea gigas reflect infectious diseases and vary with farming practices in the Mediterranean Thau lagoon, France

Aquaculture Environment Interactions

Volumn 2, Issue 3, 2012, Pages 215-237

  Pernet, Fabrice ^a   Barret, Jean ^a   Le Gall, Patrik ^a   Corporeau, Charlotte ^b   Dégremont, Lionel ^a   Lagarde, Franck ^a   Pépin, Jean François ^a   Keck, Nicolas ^c  

^a IFREMER   (France)

^b TECHNOPÔLE BREST IROISE   (France)

^c Laboratoire Départemental Vétérinaire   (France)

Author keywords

Disease; Energetic; Farming practices; Hydrodynamics; Mortality; Pacific oyster

Indexed keywords

BACTERIA (MICROORGANISMS); CRASSOSTREA GIGAS; HERPESVIRIDAE; OSTREID HERPESVIRUS 1; OSTREIDAE; VIBRIO; VIBRIO SPLENDIDUS;

EID: 84868098776     PISSN: 1869215X     EISSN: 18697534     Source Type: Journal    
DOI: 10.3354/aei00041     Document Type: Article

References (76)

1. Bacca H (2007) Étude des voies métaboliques des sucres chez l'huître creuse Crassostrea gigas. Implication dans les mortalités estivales. PhD thesis, Université de Rennes I, Rennes
2. Barnabé G, Doumenge F (2001) Mariculture of Mediterranean species. In: John HS (ed) Encyclopedia of ocean sciences. Academic Press, Oxford, p 1567-1572
3. Bédier E (2010) Observatoire national Conchylicole. Rapport 2009, Ifremer, La Trinité
4. Berthelin C, Kellner K, Mathieu M (2000) Storage metabolism in the Pacific oyster (Crassostrea gigas) in relation to summer mortalities and reproductive cycle (West coast of France). Comp Biochem Physiol B Biochem Mol Biol 125:359-369
5. Bouquet AL, Mille D, Blachier P, Oudot G and others (2011) Recherche de solutions zootechniques pour limiter les surmortalités-bilan des suivis 2010. Centre Régional d'Expérimentation et d'Application Aquacole, Le Château d'Oléron
6. Childress JJ, Somero GN (1979) Depth-related enzymic activities in muscle, brain and heart of deep-living pelagic marine teleosts. Mar Biol 52:273-283
7. Corporeau C, Groisillier A, Jeudy A, Barbeyron T and others (2011) A functional study of transforming growth factorbeta from the gonad of Pacific oyster Crassostrea gigas. Mar Biotechnol (NY) 13:971-980
8. Côté J, Himmelman JH, Claereboudt MR (1994) Separating effects of limited food and space on growth of the giant scallop Placopecten magellanicus in suspended culture. Mar Ecol Prog Ser 106:85-91
9. 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 106:179-191
10. Dégremont L (2011) Evidence of herpesvirus (OsHV-1) resistance in juvenile Crassostrea gigas selected for high resistance to the summer mortality phenomenon. Aquaculture 317:94-98
11. Dégremont L, Bédier E, Boudry P (2010a) Summer mortality of hatchery-produced Pacific oyster spat (Crassostrea gigas). II. Response to selection for survival and its influence on growth and yield. Aquaculture 299:21-29
12. Dégremont L, Boudry P, Ropert M, Samain JF, Bédier E, Soletchnik P (2010b) Effects of age and environment on survival of summer mortality by two selected groups of the Pacific oyster Crassostrea gigas. Aquaculture 299: 44-50
13. Delaporte M, Soudant P, Lambert C, Moal J, Pouvreau S, Samain JF (2006) Impact of food availability on energy storage and defense related hemocyte parameters of the Pacific oyster Crassostrea gigas during an experimental reproductive cycle. Aquaculture 254:571-582
14. DuBois M, Gilles KA, Hamilton JK, Rebers PA, Smith F (1956) Colorimetric method for determination of sugars and related substances. Anal Chem 28:350-356
15. Floreto EAT, Bayer R, Brown PB (2000) The effect of soybean-based diets, with and without amino-acid supplementation, on growth and biochemical composition of juvenile American lobster, Homarus americanus. Aquaculture 189:211-235
16. Flye-Sainte-Marie J, Pouvreau S, Paillard C, Jean F (2007) Impact of brown ring disease on the energy budget of the Manila clam Ruditapes philippinarum. J Exp Mar Biol Ecol 349:378-389
17. Folch J, Lees M, Sloane-Stanlez GH (1957) A simple method for the isolation and purification of total lipids from animal tissues. J Biol Chem 226:497-509
18. Forrest BM, Keeley NB, Hopkins GA, Webb SC, Clement DM (2009) Bivalve aquaculture in estuaries: review and synthesis of oyster cultivation effects. Aquaculture 298: 1-15
19. Fréchette M, Butman CA, Geyer WR (1989) The importance of boundary-layer flows in supplying phytoplankton to the benthic suspension feeder, Mytilus edulis L. Limnol Oceanogr 34:19-36
20. 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
21. Gangnery A, Chabirand J-M, Lagarde F, Gall PL, Oheix J, Bacher C, Buestel D (2003) Growth model of the Pacific oyster, Crassostrea gigas, cultured in Thau Lagoon (Méditerranée, France). Aquaculture 215:267-290
22. Garnier M, Labreuche Y, Garcia C, Robert A, Nicolas JL (2007) Evidence for the involvement of pathogenic bacteria in summer mortalities of the Pacific oyster Crassostrea gigas. Microb Ecol 53:187-196
23. Gay M, Renault T, Pons AM, Le Roux F (2004) Two Vibrio splendidus related strains collaborate to kill Crassostrea gigas: taxonomy and host alterations. Dis Aquat Org 62:65-74
24. Genard B, Pernet F, Lemarchand K, Boudry P, Moraga D, Tremblay R (2011) Physiological and biochemical changes associated with massive mortality event occurring during premetamorphic development of American oyster Crassostrea virginica. Aquat Living Resour 24:247-260
25. Greenway SC, Storey KB (1999) The effect of prolonged anoxia on enzyme activities in oysters (Crassostrea virginica) at different seasons. J Exp Mar Biol Ecol 242: 259-272
26. Gustafson LL, Ellis SK, Beattie MJ, Chang BD and others (2007) Hydrographics and the timing of infectious salmon anemia outbreaks among Atlantic salmon (Salmo salar L.) farms in the Quoddy region of Maine, USA and New Brunswick, Canada. Prev Vet Med 78:35-56
27. Harvell CD, Kim K, Burkholder JM, Colwell RR and others (1999) Emerging marine diseases-climate links and anthropogenic factors. Science 285:1505-1510
28. Harvell CD, Mitchell CE, Ward JR, Altizer S, Dobson AP, Ostfeld RS, Samuel MD (2002) Climate warming and disease risks for terrestrial and marine biota. Science 296:2158-2162
29. Holliday JE, Maguire GB, Nell JA (1991) Optimum stocking density for nursery culture of Sydney rock oysters (Saccostrea commercialis). Aquaculture 96:7-16
30. Hurlbert SH (1984) Pseudoreplication and the design of ecological field experiments. Ecol Monogr 54:187-211
31. Kristoffersen AB, Viljugrein H, Kongtorp RT, Brun E, Jansen PA (2009) Risk factors for pancreas disease (PD) outbreaks in farmed Atlantic salmon and rainbow trout in Norway during 2003-2007. Prev Vet Med 90: 127-136
32. Krkošek M (2010) Host density thresholds and disease control for fisheries and aquaculture. Aquacult Environ Interact 1:21-32
33. Lafferty KD, Porter JW, Ford SE (2004) Are diseases increasing in the ocean? Annu Rev Ecol Evol Syst 35:31-54
34. Laing I (2009) Oysters-shellfish farming. In: John HS, Karl KT, Steve AT (eds) Encyclopedia of ocean sciences, 2nd edn. Academic Press, Oxford, p 274-286
35. Le Deuff RM, Renault T, Gérard A (1996) Effects of temperature on herpes-like virus detection among hatcheryreared larval Pacific oyster Crassostrea gigas. Dis Aquat Org 24:149-157
36. Lightner DV (2011) Virus diseases of farmed shrimp in the Western Hemisphere (the Americas): a review. J Invertebr Pathol 106:110-130
37. Lynch SA, Carlsson J, Culloty SC (2011) Investigation into the involvement of ostreid herpes virus 1 (OsHV-1) in summer mortalities of pacific oyster, Crassostrea gigas, spat and market sized adults in Ireland. J Shellfish Res 30:528-529
38. Maguire JA, Burnell GM (2001) The effect of stocking density in suspended culture on growth and carbohydrate content of the adductor muscle in two populations of the scallop (Pecten maximus L.) in Bantry Bay, Ireland. Aquaculture 198:95-108
39. Martenot C, Oden E, Travaillé E, Malas JP, Houssin M (2011) Detection of different variants of ostreid herpesvirus 1 in the Pacific oyster, Crassostrea gigas between 2008 and 2010. Virus Res 160:25-31
40. Mazón-Suástegui JM, Ruíz-Ruíz KM, Parres-Haro A, Saucedo PE (2008) Combined effects of diet and stocking density on growth and biochemical composition of spat of the Cortez oyster Crassostrea corteziensis at the hatchery. Aquaculture 284:98-105
41. McCallum HI, Kuris A, Harvell CD, Lafferty KD, Smith GW, Porter J (2004) Does terrestrial epidemiology apply to marine systems? Trends Ecol Evol 19:585-591
42. Meyer E, Green A, MooreM, Manahan D (2007) Food availability and physiological state of sea urchin larvae (Strongylocentrotus purpuratus). Mar Biol 152:179-191
43. Montagnani C, Tirapé A, Boulo V, Escoubas JM (2005) The two Cg-timp mRNAs expressed in oyster hemocytes are generated by two gene families and differentially expressed during ontogenesis. Dev Comp Immunol 29: 831-839
44. Moran AL, Manahan DT (2004) Physiological recovery from prolonged 'starvation' in larvae of the Pacific oyster Crassostrea gigas. J Exp Mar Biol Ecol 306:17-36
45. Murray AG, Peeler EJ (2005) A framework for understanding the potential for emerging diseases in aquaculture. Prev Vet Med 67:223-235
46. Mydlarz LD, Jones LE, Harvell CD (2006) Innate immunity environmental drivers and disease ecology of marine and freshwater invertebrates. Annu Rev Ecol Evol Syst 37: 251-288
47. Nell JA (2002) Farming triploid oysters. Aquaculture 210: 69-88
48. Normand J, Le Pennec M, Boudry P (2008) Comparative histological study of gametogenesis in diploid and triploid Pacific oysters (Crassostrea gigas) reared in an estuarine farming site in France during the 2003 heatwave. Aquaculture 282:124-129
49. Normand J, Ernande B, Haure J, McCombie H, Boudry P (2009) Reproductive effort and growth in Crassostrea gigas: comparison of young diploid and triploid oysters issued from natural crosses or chemical induction. Aquat Biol 7:229-241
50. Oberbeckmann S, Wichels A, Wiltshire KH, Gerdts G (2011) Occurrence of Vibrio parahaemolyticus and Vibrio alginolyticus in the German Bight over a seasonal cycle. Antonie van Leeuwenhoek 100:291-307
51. Oden E, Martenot C, Berthaux M, Travaillé E, Malas JP, Houssin M (2011) Quantification of ostreid herpesvirus 1 (OsHV-1) in Crassostrea gigas by real-time PCR: determination of a viral load threshold to prevent summer mortalities. Aquaculture 317:27-31
52. Parrish CC (1999) Determination of total lipid, lipid classes, and fatty acids in aquatic samples. In: Arts MT, Wainman BC (eds) Lipids in freshwater ecosystems. Springer-Verlag, New York, NY, p 5-20
53. Peeler EJ, Taylor NGH (2011) The application of epidemiology in aquatic animal health-opportunities and challenges. Vet Res 42:94
54. Pepin JF, Riou A, Renault T (2008) Rapid and sensitive detection of ostreid herpesvirus 1 in oyster samples by real-time PCR. J Virol Methods 149:269-276
55. Pernet F, Bricelj VM, Cartier S (2006) Lipid class dynamics during larval ontogeny of sea scallops, Placopecten magellanicus, in relation to metamorphic success and response to antibiotics. J Exp Mar Biol Ecol 329:265-280
56. Pernet F, Barret J, Marty C, Moal J, Le Gall P, Boudry P (2010) Environmental anomalies, energetic reserves and fatty acid modifications in oysters coincide with an exceptional mortality event. Mar Ecol Prog Ser 401: 129-146
57. Plana S, Sinquin G, Maes P, Paillard C, Le Pennec M (1996) Variations in biochemical composition of juvenile Ruditapes philippinarum infected by a Vibrio sp. Dis Aquat Org 24:205-213
58. Repamo (2009) Bilan 2009 du réseau Repamo. Rapport in terne Ifremer. http://wwz.ifremer.fr/repamo/content/download/32431/445002/file/If_Rapport_REPAMO_2009.pdf Accessed December 20 2011
59. Repamo (2010) Bilan 2010 du réseau Repamo. Rapport interne Ifremer. wwz.ifremer.fr/repamo/content/download/45379/641129/file/IF_Rapport%20REPAMO%202010.pdf. Accessed December 20, 2011
60. Salama NKG, Murray AG (2011) Farm size as a factor in hydrodynamic transmission of pathogens in aquaculture fish production. Aquacult Environ Interact 2:61-74
61. Samain JF, McCombie H (2008) Summer mortality of Pacific oyster Crassostrea gigas: the Morest Project. Ifremer/Quæ Editions, Versailles
62. Saulnier D, De Decker S, Haffner P (2009) Real-time PCR assay for rapid detection and quantification of Vibrio aestuarianus in oyster and seawater: a useful tool for epidemiologic studies. J Microbiol Methods 77:191-197
63. Saulnier D, De Decker S, Haffner P, Cobret L, Robert M, Garcia C (2010) A large-scale epidemiological study to identify bacteria pathogenic to Pacific oyster Crassostrea gigas and correlation between virulence and metalloprotease-like activity. Microb Ecol 59:787-798
64. Sauvage C, Pépin JF, Lapègue S, Boudry P, Renault T (2009) Ostreid herpes virus 1 infection in families of the Pacific oyster, Crassostrea gigas, during a summer mortality outbreak: differences in viral DNA detection and quantification using real-time PCR. Virus Res 142:181-187
65. Schikorski D, Faury N, Pépin JF, Saulnier D, Tourbiez D, Renault T (2011a) Experimental ostreid herpesvirus 1 infection of the Pacific oyster Crassostrea gigas: kinetics of virus DNA detection by q-PCR in seawater and in oyster samples. Virus Res 155:28-34
66. Schikorski D, Renault T, Saulnier D, Faury N, Moreau P, Pépin JF (2011b) Experimental infection of Pacific oyster Crassostrea gigas spat by ostreid herpesvirus 1: demonstration of oyster spat susceptibility. Vet Res 42:27
67. Segarra A, Pépin JF, Arzul I, Morga B, Faury N, Renault T (2010) Detection and description of a particular ostreid herpesvirus 1 genotype associated with massive mortality outbreaks of Pacific oysters, Crassostrea gigas, in France in 2008. Virus Res 153:92-99
68. Soletchnik P, Razet D, Geairon P, Faury N, Goulletquer P (1997) Ecophysiology of maturation and spawning in oyster (Crassostrea gigas): metabolic (respiration) and feeding (clearance and absorption rates) responses at different maturation stages. Aquat Living Resour 10: 177-185
69. Soletchnik P, Faury N, Goulletquer P (2006) Seasonal changes in carbohydrate metabolism and its relationship with summer mortality of Pacific oyster Crassostrea gigas (Thunberg) in Marennes-Oléron bay (France). Aquaculture 252:328-338
70. Stuck KC, Overstreet RM (1994) Effect of Baculovirus penaei on growth and survival of experimentally infected postlarvae of the Pacific white shrimp, Penaeus vannamei. J Invertebr Pathol 64:18-25
71. Stuck KC, Stuck LM, Overstreet RM, Wang SY (1996) Relationship between BP (Baculovirus penaei) and energy reserves in larval and postlarval Pacific white shrimp Penaeus vannamei. Dis Aquat Org 24:191-198
72. Taylor JJ, Rose RA, Southgate PC, Taylor CE (1997) Effects of stocking density on growth and survival of early juvenile silver-lip pearl oysters, Pinctada maxima (Jameson), held in suspended nursery culture. Aquaculture 153: 41-49
73. Thompson JR, Randa MA, Marcelino LA, Tomita-Mitchell A, Lim E, Polz MF (2004) Diversity and dynamics of a North Atlantic coastal Vibrio community. Appl Environ Microbiol 70:4103-4110
74. Tirapé A, Bacque C, Brizard R, Vandenbulcke F, Boulo V (2007) Expression of immune-related genes in the oyster Crassostrea gigas during ontogenesis. Dev Comp Immunol 31:859-873
75. Viljugrein H, Staalstrøm A, Molvær J, Urke HA, Jansen PA (2009) Integration of hydrodynamics into a statistical model on the spread of pancreas disease (PD) in salmon farming. Dis Aquat Org 88:35-44
76. Webb SC, Fidler A, Renault T (2007) Primers for PCR-based detection of ostreid herpes virus-1 (OsHV-1): application in a survey of New Zealand molluscs. Aquaculture 272:126-139