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Temperature and seston quantity and quality effects on field reproduction of farmed oysters, Crassostrea gigas, in Bourgneuf Bay, France

Published online by Cambridge University Press:  23 October 2009

Mickaël Dutertre ,
Peter G. Beninger ,
Laurent Barillé ,
Mathias Papin ,
Philippe Rosa ,
Anne-Laure Barillé  and
Joël Haure
Mickaël Dutertre
Affiliation:
Université de Nantes, Nantes Atlantique Universités, Équipe Mer-Molécules-Santé EA 2160, Faculté des Sciences et des Techniques, 2 rue de la Houssinière, BP 92208, 44322 Nantes, France
Peter G. Beninger
Affiliation:
Université de Nantes, Nantes Atlantique Universités, Équipe Mer-Molécules-Santé EA 2160, Faculté des Sciences et des Techniques, 2 rue de la Houssinière, BP 92208, 44322 Nantes, France
Laurent Barillé
Affiliation:
Université de Nantes, Nantes Atlantique Universités, Équipe Mer-Molécules-Santé EA 2160, Faculté des Sciences et des Techniques, 2 rue de la Houssinière, BP 92208, 44322 Nantes, France
Mathias Papin
Affiliation:
IFREMER, Laboratoire conchylicole des Pays de la Loire, Polder des Champs, 85230 Bouin, France
Philippe Rosa
Affiliation:
Université de Nantes, Nantes Atlantique Universités, Équipe Mer-Molécules-Santé EA 2160, Faculté des Sciences et des Techniques, 2 rue de la Houssinière, BP 92208, 44322 Nantes, France
Anne-Laure Barillé
Affiliation:
BIO-LITTORAL, Faculté des Sciences et des Techniques, 2 rue de la Houssinière, BP 92208, 44322 Nantes, France
Joël Haure
Affiliation:
IFREMER, Laboratoire conchylicole des Pays de la Loire, Polder des Champs, 85230 Bouin, France
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Abstract

The proliferation of the voluntarily-introduced cupped oyster, Crassostrea gigas, has attained the proportions of species invasion in many intertidal habitats in Europe, presumably resulting from successful reproduction of farmed individuals. It is thus imperative to better understand the reproductive characteristics of farmed oysters, since they are directly under human control. We quantified the dry tissue mass (DTM), gametosomatic index (GSI), and reproductive cycle of farmed oysters at two sites in Bourgneuf Bay, France, in relation to environmental parameters using continuously-recording probes in 2005 and 2006. The GSI was developed for this study, based on the actual area occupied by gametes, rather than the area of the gonad previously used for quantitative histological estimation of reproductive effort. The two sites, intermediate – (IT) and high-turbidity (HT), differed markedly in the amount and quality of particulate suspended matter, and also in fine-scale temperature variations. Oysters at both sites presented two spawning periods in both 2005 and 2006; Bourgneuf Bay is thus near the northernmost European limit for a 2-spawning cycle in Crassostrea gigas. Gonad maturation was initiated when spring water temperature reached 8–10 °C, and gamete atresia occurred when water temperatures transiently dipped to 15–18 °C. Spawns, which occurred above 18 °C, were timed by fine-scale water temperature variations. Particulate organic matter quality peaks, coinciding with gonad maturation, were related to DTM variations before spawning periods, for the IT oysters in both years, and for the HT oysters in 2006. The reproductive effort (GSI) of oysters was similar at both sites; however, the fates of the gametes differed according to site. At the first spawning, the IT oyster gamete emissions were +1 month delayed, as were peak water temperatures greater than 18 °C, and more pronounced, compared to the HT site. Although the second spawning showed high proportions of atretic oocytes at both sites in both years, the IT oysters evacuated twice as many gametes as the HT oysters in 2005. The IT conditions therefore appear more suited to Crassostrea gigas gamete evacuation than the HT conditions.

Keywords

ReproductionTemperatureTurbidityOocytesAtresiaBiological invasionGametosomatic indexBivalveOyster farmingCrassostrea gigasAtlantic Ocean
Type
Research Article
Information
Aquatic Living Resources , Volume 22 , Issue 3 , July 2009 , pp. 319 - 329
Copyright
© EDP Sciences, IFREMER, IRD, 2009

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References

Anderson, T.J., Pejrup, M., 2001, Suspended sediment transport on a temperate, microtidal mudflat, the Danish Wadden Sea. Mar. Geol. 173, 69–85. CrossRef
Andrews J.D., 1979, Pelecypoda:Ostreidae. In: Giese A.C., Pearse J.S. (Eds.), Reproduction of Marine Invertebrates. Molluscs: Pelecypods and lesser classes. Academic Press, New York, pp. 293–341.
Arakawa, K.Y., 1990, Natural spat collecting in the Pacific oyster Crassostrea gigas (Thunberg). Mar. Behav. Physiol. 17, 95–128. CrossRef
Barber, B.J., Getchell, R., Shumway, S., Schick, D., 1988, Reduced fecundity in a deep-water population of the giant scallop Placopecten magellanicus in the gulf of Maine, USA. Mar. Ecol. Prog. Ser. 42, 207–212. CrossRef
Barillé, L., Haure, J., Cognie, B., Leroy, A., 2000, Variations in pallial organ and eulatero-frontal cirri in response to high particulate matter concentrations in the oyster Crassostrea gigas. Can. J. Fish. Aquat. Sci. 57, 837–843. CrossRef
Barillé, L., Prou, J., Héral, M., Razet, D., 1997, Effects of high natural seston concentration on the feeding, selection and absorption of the oyster Crassostrea gigas. J. Exp. Mar. Biol. Ecol. 212, 149–172. CrossRef
Barillé-Boyer, A.-L., Barillé, L., Massé, H., Razet, D., Héral, M., 2003, Correction for particulate organic matter as estimated by loss on ignition in estuarine ecosystems. Estuar. Coast. Shelf Sci. 58, 147–153. CrossRef
Beninger, P.G., 1987, A qualitative and quantitative study of the reproductive cycle of the giant scallop, Placopecten magellanicus, in the Bay of Fundy (New Brunswick, Canada). Can. J. Zool. 65, 495–498. CrossRef
Beninger, P.G., Cannuel, R., Blin, J.-L., Pien, S., Richard, O., 2001, Reproductive characteristics of the archaeogastropod Megathura crenulata. J. Shellfish Res. 20, 301–307.
Beninger, P.G., Lucas, A., 1984, Seasonal variations in condition, reproductive activity, and gross biochemical composition of two species of adult clam reared in a common habitat: Tapes decussatus L. (Jeffreys) and Tapes philippinarum (Adams and Reeve). J. Exp. Mar. Biol. Ecol. 79, 19–37. CrossRef
Beninger, P.G., Valdizan, A., Decottignies, P., Cognie, B., 2008, Impact of seston characteristics on qualitative particle selection sites and efficiencies in the pseudolamellibranch bivalve Crassostrea gigas. J. Exp. Mar. Biol. Ecol. 360, 9–14. CrossRef
Berg, J.A., Newell, R.I.E., 1986, Temporal and spatial variations of seston available to the suspension feeder Crassostrea virginica. Estuar. Coast. Shelf Sci. 23, 375–386. CrossRef
Bourlès Y., Alunno-Bruscia M., Pouvreau S., Tollu G., Leguay D., Arnaud C., Goulletquer P., Kooijman S.A.L.M., 2009, Modelling growth and reproduction of the Pacific oyster Crassostrea gigas: Advances in the oyster-DEB model through application to a coastal pond. J. Sea Res. 62, in press.
Brandt, G., Wehrmann, A., Wirtz, K.W., 2008, Rapid invasion of Crassostrea gigas into the German Wadden Sea dominated by larval supply. J. Sea Res. 59, 279–296. CrossRef
Cardoso, J.F.M.F., Langlet, D., Loff, J.F., Martins, A.R., Witte, J.I.J., Santos, P.T., van der Veer, H.W., 2007, Spatial variability in growth and reproduction of the Pacific oyster Crassostrea gigas (Thunberg, 1793) along the west European coast. J. Sea Res. 57, 303–315. CrossRef
Chávez-Villalba, J., Barret, J., Mingant, C., Cochard, J.C., Le Pennec, M., 2002, Autumn conditioning of the oyster Crassostrea gigas: A new approach. Aquaculture 210, 171–186. CrossRef
Chávez-Villalba, J., Cochard, J.C., Le Pennec, M., Barret, J., Enríquez-Díaz, M., Cáceres-Martínez, C., 2003, Effects of temperature and feeding regimes on gametogenesis and larval production in the oyster Crassostrea gigas. J. Shellfish Res. 22, 721–731.
Chávez-Villalba, J., Mingant, C., Cochard, J.C., Le Pennec, M., 2001, Gamétogenèse chez l'huître Crassostrea gigas de l'Aber Benoît (Bretagne, France), à la limite nord de son aire de reproduction. Haliotis 30, 1–12.
Cognie, B., Haure, J., Barillé, L., 2006, Spatial distribution in a temperate coastal ecosystem of the wild stock of the farmed oyster Crassostrea gigas (Thunberg). Aquaculture 259, 249–259. CrossRef
Conover W.J. 1999, Practical nonparametric statistics. 3rd edition, John Wiley & Sons, Inc., New York.
DeVlaming, V., Grossman, G., Chapman, F., 1982, On the use of the gonadosomatic index. Comp. Biochem. Physiol. A 73A, 31–39. CrossRef
Diederich, S., 2006, High survival and growth rates of introduced Pacific oysters may cause restrictions on habitat use by native mussels in the Wadden Sea. J. Exp. Mar. Biol. Ecol. 328, 211–227. CrossRef
Diederich, S., Nehls, G., van Beusekom, J.E.E., Reise, K., 2005, Introduced Pacific oysters (Crassostrea gigas) in the northern Wadden Sea: invasion accelerated by warm summers? Helgol. Mar. Res. 59, 97–106.
Dorange, G., Le Pennec, M., 1989, Ultrastructural study of oogenesis and oocytic degeneration in Pecten maximus from the Bay of St Brieuc. Mar. Biol. 103, 339–348. CrossRef
Drinkwaard, A.C., 1999, Introductions and developments of oysters in the North Sea area: a review. Helgol. Meeresunters 52, 301–308. CrossRef
Dupont, C., Gruet, Y., 2005, Malacofaune et crustacés marins des amas coquilliers mésolithiques de Beg-an-Dorchenn (Plomeur, Finistère) et de Beg-er-Vil (Quiberon, Morbihan). In : Marchand G., Tresset A., Unité et diversité des processus de néolithisation sur la façade atlantique de l'Europe (6e–4e millénaires avant J.-C.). Mém. Soc. Préhist. Française 36, 139–161.
Dutertre M., Beninger P.G., Barillé L., Papin M., Haure J., 2009, Rising water temperatures, reproduction and recruitment of an invasive oyster, Crassostrea gigas, on the French Atlantic coast. Mar. Environ. Res. 68.
Enríquez-Díaz M., Pouvreau S., Chávez-Villalba J., Le Pennec M., 2009, Gametogenesis, reproductive investment, and spawning behavior of the Pacific giant oyster Crassostrea gigas: evidence of an environment-dependant strategy. Aquacult. Int. 17.
Fabioux, C., Huvet, A., Le Souchu, P., Le Pennec, M., Pouvreau, S., 2005, Temperature and photoperiod drive Crassostrea gigas reproductive internal clock. Aquaculture 250, 458–470. CrossRef
Fegley, S.R., MacDonald, B.A., Jacobsen, T.R., 1992, Short-term variation in the quantity and quality of seston available to benthic suspension feeders. Estuar. Coast. Shelf Sci. 34, 393–412. CrossRef
Flassch, J.P., Leborgne, Y., 1992, Introduction in Europe, from 1972 to 1980, of the Japanese Manila clam (Tapes philippinarum) and effects on aquaculture production and natural settlement. ICES J. Mar. Sci. 194, 92–96.
Gosling E., 2003 (Ed.), Bivalve molluscs: biology, ecology and culture. Fishing News Books, Blackwell Science, Oxford.
Grizel H., Héral M., 1991, Introduction into France of the Japanese oyster (Crassostrea gigas). J. Cons. Int. Explor. Mer, 47, 399–403.
Kobayashi, M., Hofmann, E.E., Powell, E.N., Klinck, J.M., Kusaka, K., 1997, A population dynamics model for the Japanese oyster, Crassostrea gigas. Aquaculture 149, 285–321. CrossRef
Kochmann, J., Bushbaum, C., Volkenborn, N., Reise, K., 2008, Shift from native mussels to alien oysters: Differential effects of ecosystem engineers. J. Exp. Mar. Biol. Ecol. 364, 1–10. CrossRef
Lango-Reynoso, F., Chávez-Villalba, J., Cochard, J.C., Le Pennec, M., 2000, Oocyte size, a means to evaluate the gametogenic development of the Pacific oyster, Crassostrea gigas (Thunberg). Aquaculture 190, 183–199. CrossRef
Le Pennec, M., Beninger, P.G., Dorange, G., Paulet, Y.M., 1991, Trophic sources and pathways to the developing gametes of Pecten maximus (Bivalvia: Pectinidae). J. Mar. Biol. Assoc. UK 71, 451–463. CrossRef
Lorenzen, C.J., 1967, Determination of chlorophyll and pheo-pigments: spectrophotometric equations. Limnol. Oceanogr. 12, 343–346. CrossRef
Lubet, P., Besnard, J.Y., Faveris, R., 1987, Compétition énergétique entre tissu musculaire et gonadique chez la coquille St-Jacques (Pecten maximus L.). Haliotis 16, 173–180.
Lucas, A., 1982, La nutrition des larves de bivalves. Océanis 8, 363–388.
Mann, R., 1979, Some biochemical and physiological aspects of growth and gametogenesis in Crassostrea gigas and Ostrea edulis grown at sustained elevated temperatures. J. Mar. Biol. Assoc. UK 59, 95–110. CrossRef
Martoja R., Martoja-Pierson M., 1967, Initiation aux techniques de l'histologie animale. Masson & Cie (Eds.), Paris.
Morales-Alamo, R., Mann, R., 1989, Anatomical features in histological sections of Crassostrea virginica (Gmelin, 1791) as an aid in measurements of gonad area for reproductive assessment. J. Shellfish Res. 8, 71–82.
Morvan, C., Ansell, A.D., 1988, Stereological methods applied to reproductive cycle of Tapes rhomboides. Mar. Biol. 97, 355–364. CrossRef
Paulet, Y.M., Lucas, A., Gerard, A., 1988, Reproduction and larval development in two Pecten maximus (L.) populations from Brittany. J. Exp. Mar. Biol. Ecol. 119, 145–156. CrossRef
Pazos, A.J., Román, G., Acosta, C.P., Abad, M., Sánchez, J.L., 1996, Stereological studies on the gametogenic cycle of the scallop, Pecten maximus, in suspended culture in Ria de Arousa (Galicia, NW Spain). Aquaculture 142, 119–135. CrossRef
Pejrup, M., 1986, Parameters affecting fine-grained suspended sediment concentrations in a shallow micro-tidal estuary, Ho Bugt. Estuar. Coast. Shelf Sci. 22, 241–254. CrossRef
Pipe, R.K., 1987, Oogenesis in the marine mussel Mytilus edulis: an ultrastructural study. Mar. Biol. 95, 405–414. CrossRef
Reise, K., Gollasch, S., Wolff, W., 1999, Introduced marine species of the North Sea coasts. Helgol. Mar. Res. 52, 219–234.
Rico-Villa, B., Pouvreau, S., Robert, R., 2009, Influence of food density and temperature on ingestion, growth and settlement of Pacific oyster larvae, Crassostrea gigas. Aquaculture 287, 395–401. CrossRef
Robinson, W.E., Wehling, W.E., Morse, M.P., McLeod, G.C., 1981, Seasonal changes in soft-body component indices and energy reserves in the Atlantic deep-sea scallop, Placopecten magellanicus. Fish. Bull. 79, 449–458.
Ruesink, J.L., Lenihan, H.S., Trimble, A.C., Heiman, K.W., Micheli, F., Byers, J.E., Kay, M.C., 2005, Introduction of non-native oysters: ecosystem effects and restoration implications. Annu. Rev. Ecol. Evol. Syst. 36, 643–689. CrossRef
Ruiz, C., Abad, M., Sedano, F., Garcia-Martin, L.O., Sánchez-López, J.L., 1992, Influence of seasonal environmental changes on the gamete production and biochemical composition of Crassostrea gigas (Thunberg) in suspended culture in El Grove, Galicia, Spain. J. Exp. Mar. Biol. Ecol. 155, 249–262. CrossRef
Sastry A.N., 1979, Pelecypoda (excluding Ostreidae). In: Giese A.C., Pearse J.S. (Eds.), Reproduction of Marine Invertebrates. Molluscs: Pelecypods and lesser classes. Academic Press, New York, pp. 113–292.
Seno, H., Hori, J., Kusakabe, D., 1926, Effects of temperature and salinity on the development of the eggs of the common Japanese oyster, Ostrea gigas Thunberg. J. Imp. Fish. Inst. 22, 41–47.
Shatkin, G., Shumway, S.E., Hawes, R., 1997, Considerations regarding the possible introduction of the Pacific oyster (Crassostrea gigas) to the Gulf of Maine: a review of global experience. J. Shellfish Res. 16, 463–477.
Shpigel, M., 1989, Gametogenesis of the european flat oyster (Ostrea edulis) and pacific oyster (Crassostrea gigas) in farm water in Israel. Aquaculture 80, 343–349. CrossRef
Smaal, A., van Stralen, M., Craeymeersch, J., 2005, Does the introduction of the Pacific oyster Crassostrea gigas lead to species shifts in the wadden sea? In: Dame R.F., Olenin S. (Eds.) The Comparative Roles of Suspension-Feeders in Ecosystems. Dordrecht, Kluwer (NATO Science Series IV). Earth Environ. Sci. 47, 277–289.
Steele, S., Mulcahy, M.F., 1999, Gametogenesis of the oyster Crassostrea gigas in southern Ireland. J. Mar. Biol. Assoc. UK 79, 673–686. CrossRef
Thompson, R.J., 1977, Blood chemistry, biochemical composition, and the annual reproductive cycle in the giant scallop, Placopecten magellanicus, from southeast Newfoundland. J. Fish. Res. Board Can. 34, 2104–2116. CrossRef
Thresher, R., Grewe, P., Patil, J.G., Whyard, S., Templeton, C.M., Chaimongol, A., Hardy, C.M., Hinds, L.A., Dunham, R., 2009, Development of repressible sterility to prevent the establishment of feral populations of exotic and genetically modified animals. Aquaculture 290, 104–109. CrossRef
Troost, K., Gelderman, E., Kamermans, P., Smaal, A.C., Wolff, W.J., 2009, Effects of an increasing filter feeder stock on larval abundance in the Oosterschelde estuary (SW Netherlands). J. Sea Res. 61, 153–164. CrossRef
van der Meer, J., 2006, An introduction to Dynamic Energy Budget (DEB) models with special emphasis on parameter estimation. J. Sea Res. 56, 85–102. CrossRef
Ventilla, R.F., 1984, Recent developments in the Japanese oyster culture industry. Adv. Mar. Biol. 21, 1–57. CrossRef
Wehrmann, A., Herlyn, M., Bungenstock, F., Hertweck, G., Millat, G., 2000, The distribution gap is closed-first record of naturally settled Pacific oysters (Crassostrea gigas) in the East Frisian Wadden Sea, North Sea. Senckenb. Marit. 30, 153–160. CrossRef