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Physiological responses of female and male black-lip pearl oysters (Pinctada margaritifera) to different temperatures and concentrations of food

Published online by Cambridge University Press:  05 August 2013

Jorge Chávez-Villalba ,
Claude Soyez ,
Hermann Aurentz  and
Gilles Le Moullac
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Abstract

This study was designed to measure responses of four-year-old black-lip pearl oysters (Pinctada margaritifera) to different temperatures and food concentrations and to identify the energy requirements of each sex. Oysters were fed a monospecific microalgal diet of Isochrysis affinis galbana (T-iso). Measurements of oxygen consumption and ingestion rates were carried out at 24 °C and 27 °C and at two algal (T-iso) concentrations: 5000 and 30 000 cell ml-1. Glycogen content in adductor muscle, absorption efficiency and scope for growth were also estimated. Females and males responded differently to environmental factors, with food level being the most influential parameter. Oxygen consumption and absorption efficiency were significantly higher in females than in males, but males had significantly higher glycogen content than females. At high food concentration, glycogen content, ingestion rate, oxygen consumption, and scope for growth were significantly higher than at the low food concentration. Only absorption efficiency was significantly higher at the low food concentration. Oxygen consumption was significantly higher at 27 °C than at 24 °C. These results indicate that females and males have different bioenergetic functioning and that energy demands for reproduction are higher in females.

Keywords

Food supplyIngestion rateGlycogenOxygen consumptionScope for growthPearl oyster
Type
Research Article
Information
Aquatic Living Resources , Volume 26 , Issue 3 , 2013 , pp. 263 - 271
Copyright
© EDP Sciences, IFREMER, IRD 2013

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References

Aldridge, D.W., Payne, B.S., Miller, A.C., 1995, Oxygen consumption, nitrogenous excretion, and filtration rates of Dreissena polymorpha at acclimation temperatures between 20 and 32 ° C. Can. J. Fish. Aquat. Sci. 52, 1761–1767. CrossRefGoogle Scholar
Bayne, B.L., Gabbott, P.A., Widdows, J., 1975, Some effects of stress in the adult on the eggs and larvae of Mytilus edulis L. J. Mar. Biol. Assoc. UK 55, 675–689. CrossRefGoogle Scholar
Bayne B.L., 1976, Aspects of the reproduction in bivalve mollusks of reproduction. In: Wiley M. (Ed.) Estuarine Processes, Vol. 1. London, Academic Press Inc., pp. 432–448.
Bayne B.L., Newell R.C., 1983, Physiological energetics of marine molluscs. In: Saleuddin A.S.M., Wilbur K.W. (Eds.) The Mollusca. Physiology Part I, New York, Academic Press Inc., pp. 407–515.
Bayne, B.L., Hawkins, A.J.S., Navarro, E., 1987, Feeding and digestion by the mussel Mytilus edulis L. (Bivalvia: Mollusca) in mixtures of silt and algal cells at low concentration. J. Exp. Mar. Biol. Ecol. 111, 1–22. CrossRefGoogle Scholar
Bayne, B.L., 2000, Relations between variable rates of growth, metabolic costs and growth efficiencies in individual Sydney rock oysters (Saccostrea commercialis). J. Exp. Mar. Biol. Ecol. 251, 185–203. CrossRefGoogle Scholar
Beninger, P., Le Pennec, M., 1997, Reproductive characteristics of a primitive bivalve from a deep-sea reducing environment: giant gametes and their significance in Acharaxalinae (Cryptodonta: Solemyidae). Mar. Ecol. Prog. Ser. 157, 195–206. CrossRefGoogle Scholar
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 125, 359–369. CrossRefGoogle Scholar
Bierbaum, R., Shumway, S., 1988, Filtration and oxygen consumption in mussels, Mytilus edulis with and without pea crabs, Pinnotheres maculatus. Estuaries 11, 264–271. CrossRefGoogle Scholar
Bougrier, S., Geairon, P., Deslous-Paoli, J.M., Bacher, C., Jonquières, G., 1995, Allometric relationships and effects of temperature on clearance and oxygen consumption of Crassostrea gigas (Thunberg). Aquaculture 134, 143–154. CrossRefGoogle Scholar
Bühringer, H., Danischewski, D., 2001, Laboratory studies on the scope for growth in blue mussels Mytilus edulis L. Arch. Fish. Mar. Res. 49, 61–68. Google Scholar
Chávez-Villalba, J., Soyez, C., Huvet, A., Gueguen, Y., Lo, C., Le Moullac, G., 2011, Determination of gender in the pearl oyster Pinctada margaritifera. J. Shellfish Res. 30, 231–240. CrossRefGoogle Scholar
Cochennec-Laureau, N., Montagnani, C., Saulnier, D., Fougerouse, A., Levy, P., Lo, C., 2010, A histological examination of grafting success in pearl oyster Pinctada margaritifera in French Polynesia. Aquat. Living Resour. 23, 131–140. CrossRefGoogle Scholar
Conover, R.J., 1966, Assimilation of organic matter by zooplankton. Oceanogr. 11, 338–345. Google Scholar
Delaporte, M., Soudant, P., Lambert, C., Moal, J., Pouvreau, S., Samain, J.F., 2006, Impact of food availability on energetic storage and related hemocyte parameters of the Pacific oysters Crassostrea gigas during an experimental reproductive cycle. Aquaculture 254, 571–582. CrossRefGoogle Scholar
Dubois, M., Gilles, K.A., Hamilton, J.K., Rebers, P.A., Smith, F., 1956, Colorimetric method for determination of sugars and related substances. Anal. Chem. 28, 350–356. CrossRefGoogle Scholar
Fournier J., Levesque E., Pouvreau S., Le Pennec M., Le Moullac G., 2012, Influence of plankton concentration on gametogenesis and spawning of the black lip pearl oyster Pinctada margaritifera in Ahe atoll lagoon (Tuamotu archipelago, French Polynesia). Mar. Pollut. Bull. 65, Spec. Issue, 463-470.
Gnaiger, E., 1983, Heat dissipation and energetic efficiency in animal anoxibiosis. Economy contra power. J. Exp. Zool. 228, 471–490. Google Scholar
Han, K.N., Lee, S.W., Wang, S.Y., 2008, The effect of temperature on the energy budget of the Manila clam, Ruditapes philippinarum. Aquac. Int. 16, 143–152. CrossRefGoogle Scholar
Hansen, B.W., Dolmer, P., Vismann, B., 2011, In situ method for measurements of community clearance rate on shallow water bivalve populations. Limnol. Oceanogr. Meth. 9, 454–459. CrossRefGoogle Scholar
Harrang, E., Lapegue, S., Morga, B., Bierne, N., 2013, A high load of non-neutral amino-acid polymorphisms explains high protein diversity despite moderate effective population size in a marine bivalve with sweepstakes reproduction. G3 Genes Genom. Genet. 3, 333–341. Google Scholar
Haure, J., Huvet, A., Palvadeau, H., Nourry, M., Penisson, C., Martin, J.L.Y., Boudry, P., 2003, Feeding and respiratory time activities in the cupped oysters Crassostrea gigas, Crassostrea angulata and their hybrids. Aquaculture 218, 539–551. CrossRefGoogle Scholar
Hawkins, A.J.S., Bayne, B.L., Bougrier, S., Héral, M., Iglesias, J.I.P., Navarro, E., Smith, R.F.M., Urrutia, M.B., 1998, Some general relationships in comparing the feeding physiology of suspension-feeding bivalve molluscs. J. Exp. Mar. Biol. Ecol. 219, 87–103. CrossRefGoogle Scholar
Hicks, D.W., McMahon, R.F., 2002, Temperature acclimation of upper and lower thermal limits and freeze resistance in the non-indigenous brown mussel, Perna perna (L.), from the Gulf of Mexico. Mar. Biol. 140, 1167–1179. Google Scholar
Honkoop, P.J.C., 2003, Physiological costs of reproduction in the Sydney rock oyster Saccostrea glomerata. How expensive is reproduction? Oecologia 135, 176–183. Google ScholarPubMed
Hui, B., Vonau, V., Moriceau, J., Tetumu, R., Vanaa, V., Demoy-Schneider, M., Suquet, M., Le Moullac, G., 2011, Hatchery-scale trials using cryopreserved spermatozoa of black-lip pearl oyster, Pinctada margaritifera. Aquat. Living Resour. 24, 219–223. CrossRefGoogle Scholar
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
Iglesias, J.I.P., Navarro, E., Alvarez-Jorna, P., Armentina, I., 1992, Feeding, particle selection and absorption in cockles Cerastoderma edule (L.) exposed to variable conditions of food concentration and quality. J. Exp. Mar. Biol. Ecol. 162, 177–198. CrossRefGoogle Scholar
Kesarcodi-Watson, A., Klumpp, D.W., Lucas, J.S., 2001, Comparative feeding and physiological energetics in diploid and triploid Sydney rock oysters (Saccostrea commercialis) - II. Influences of food concentration and tissue energy distribution. Aquaculture 203, 195–216. Google Scholar
Kong, L., Wang, Z., Yu, R., Li, Q., Wang, R., 2007, Seasonal variation of the glycogen enzyme activity in diploid and triploid Pacific oyster gonad during sexual maturation. J. Ocean. Univ. China (English edition) 6, 383–386. CrossRefGoogle Scholar
Laing, I., 2004, Filtration of king scallops (Pecten maximus). Aquaculture 240, 369–384. CrossRefGoogle Scholar
Lambert C., Moal J., Le Moullac G., Pouvreau S., 2007, 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. Quæ edn. Versailles, pp. 63–106.
Le Moullac, G., Goyard, E., Saulnier, D., Haffner, P., Thouard, E., Nedelec, G., Goguenheim, J., Rouxel, C., Cuzon, G., Aquacop, 2003, Recent improvements in broodstock management and larviculture in marine species in Polynesia and New Caledonia: genetic and health approaches. Aquaculture 227, 89–106. CrossRefGoogle Scholar
Le Moullac, G., Tiapari, J., Tessier, H., Martinez, E., Cochard, J.C., 2012, Growth and gonad development of the tropical blacklip pearl oyster, Pinctada margaritifera (L.), in the Gambier archipelago (French Polynesia). Aquac. Int. 20, 305–315. CrossRefGoogle Scholar
Le Moullac, G., Soyez, C., Sham-Koua, M., Levy, P., Moriceau, J., Vonau, V., Maihota, M., Cochard, J.C., 2013, Feeding the pearl oyster Pinctada margaritifera during reproductive conditioning. Aquac. Res. 44, 404–411. CrossRefGoogle Scholar
MacDonald B.A., Bricelj M., Shumway S.E., 2006, Physiology: Energy acquisition and utilisation. In: Shumway S.E., Parsons G.J. (Eds.) Scallops: biology, ecology and aquaculture. Amsterdam, Elsevier, pp. 417–492.
Marsden, I.D., Weatherhead, M.A., 1998, Effects of aerial exposure on oxygen consumption by the New Zealand mussel Perna canaliculus (Gmelin, 1791) from an intertidal habitat. J. Exp. Mar. Biol. Ecol. 230, 15–29. CrossRefGoogle Scholar
Palmer, R.E., 1980, Behavioral and rhythmic aspects of filtration in the bay scallop, Argopecten irradians concentricus (Say), and the oyster Crassostrea virginica (Gmelin). J. Exp. Mar. Biol. Ecol. 45, 273–295. CrossRefGoogle Scholar
Petersen, J.K., Bougrier, S., Smaal, A.C., Garen, P., Robert, S., Larsen, J.E.N., Brummelhuis, E., 2004, Intercalibration of mussel Mytilus edulis clearance rate measurements. Mar. Ecol. Prog. Ser. 267, 187–19. CrossRefGoogle Scholar
Pouvreau, S., Jonquières, G., Buestel, D., 1999, Filtration by the pearl oyster, Pinctada margaritifera, under conditions of low seston load and small particle size in a tropical lagoon habitat. Aquaculture 176, 295–314. CrossRefGoogle Scholar
Pouvreau, S., Bacher, C., Héral, M., 2000, Ecophysiological model of growth and reproduction of the black pearl oyster, Pinctada margaritifera: potential applications for pearl farming in French Polynesia. Aquaculture 186, 117–144. CrossRefGoogle Scholar
Rueda, J.L., Smaal, A.C., 2004, Variation of the physiological energetics of the bivalve Spisula subtruncata (da Costa, 1778) within an annual cycle. J. Exp. Mar. Biol. Ecol. 301, 141–157. CrossRefGoogle Scholar
Saraiva, S., van der Meera, J., Kooijman, S.A.L.M., Sousa, T., 2011, Modelling feeding processes in bivalves: A mechanistic approach. Ecol. Model. 222, 514–523. CrossRefGoogle Scholar
Saucedo, P.E., Ocampo, L., Monteforte, M., Bervera, H., 2004, Effect of temperature on oxygen consumption and ammonia excretion in the Calafia mother-of-pearl oyster, Pinctada mazatlanica (Hanley, 1856). Aquaculture 229, 377–387. CrossRefGoogle Scholar
Savina, M., Pouvreau, S., 2004, A comparative ecophysiological study of two infaunal filter-feeding bivalves: Paphia rhomboides and Glycymeris glycymeris. Aquaculture 239, 289–306. CrossRefGoogle Scholar
Shumway, S.E., 1982, Oxygen consumption in oysters: an overview. Mar. Biol. Lett. 3, 1–23. Google Scholar
Soletchnik, P., Razet, D., Geairon, P., Faury, N., Goulletquer, P., 1997, Ecophysiology of maturation and spawning in oyster (Crassostrea gigas): metabolic (respiration) and feeding (filtration and absorption rates) responses at different maturation stages. Aquat. Living Resour. 10, 177–185. CrossRefGoogle Scholar
Sugiyama, A., Tomori, A., 1988, Oxygen consumption of black-lip pearl oyster. Suisan Zoshoku 36, 121–125 (in Japanese). Google Scholar
Tankersley, R.A., Dimock, R.V., 1993, The effect of larval brooding on the respiratory physiology of the freshwater unionid mussel Pyganodon cataracta. Am. Midl. Nat. 130, 146–163. CrossRefGoogle Scholar
Tomaru, Y., Ebisuzaki, S., Kawabata, Z., Nakano, S., 2002, Respiration rates of the Japanese pearl oyster, Pinctada fucata martensii, feeding on Pavlova lutheri and Chaetoceros gracilis. Aquac. Res. 33, 33–36. CrossRefGoogle Scholar
Tran, D., Massabuau, J.C., Vercelli, C., 2008, Influence of sex and spawning status on oxygen consumption and blood oxygenation status in oysters Crassostrea gigas cultured in a Mediterranean lagoon (Thau, France). Aquaculture 277, 58–65. CrossRefGoogle Scholar
Tranter, D.J., 1958, Reproduction in Australian pearl oysters (Lamellibranchia). IV. Pinctada margaritifera (Linnaeus). Aust. J. Mar. Freshw. Res. 9, 511–525. Google Scholar
Tremblay, R., Myrand, B., Sévigny, J.M., Guderley, H., 1998, Bioenergetic and genetic parameters in relation to susceptibility of blue mussels, Mytilus edulis (L.) to summer mortality. J. Exp. Mar. Biol. Ecol. 221, 27–58. CrossRefGoogle Scholar
Vahl O., Sundet J.H., 1985, Is sperm really so cheap? In: Gray J.S., Christiansen M.E. (Eds.) Marine Biology and Polar Regions and Effects of Stress on Marine Organisms. New York, John Wiley and Sons, pp. 281–285.
Valenzuela, D.M., Murphy, A.J., Frendewey, D., Gale, N.W., Economides, A.N., Auerbach, W., Poueymirou, W.T., Adams, N.C., Rojas, J., Yasenchak, J. et al., 2003, High-throughput engineering of the mouse genome coupled with high-resolution expression analysis. Nat. Biotechnol. 21, 652–659. CrossRefGoogle ScholarPubMed
Velasco, L.A., 2007, Energetic physiology of the Caribbean scallops Argopecten nucleus and Nodipecten nodosus fed with different microalgal diets Aquaculture 270, 299–311. CrossRefGoogle Scholar
Wessa P., 2012, Box-Cox Normality Plot (v1.1.3) in Free Statistics Software (v1.1.23-r7), Office for Research Development and Education, URL http://www.wessa.net/rwasp_boxcoxnorm.wasp/
Winter, J.E., 1978, A review on the knowledge of suspension feeding in Lamellibranchiate bivalves, with special reference to artificial aquaculture systems. Aquaculture 13, l–33. CrossRefGoogle Scholar
Wright, W.G., 1988, Sex change in the mollusca. Trends Ecol. Evol. 3, 137–140. CrossRefGoogle ScholarPubMed
Yu, Z., Jiang, A., Wang, C., 2010, Oxygen consumption, ammonia excretion, and filtration rate of the marine bivalve Mytilus edulis exposed to methamidophos and omethoate. Mar. Freshw. Behav. Physiol. 43, 243–255. Google Scholar
Yukihira, H., Klumpp, D.W., Lucas, J.S., 1998, Effects of body size on suspension feeding and energy budgets of the pearl oysters Pinctada margaritifera and P. maxima. Mar. Ecol. Prog. Ser. 170, 119–130. CrossRefGoogle Scholar
Yukihira, H., Lucas, J.S., Klumpp, D.W., 2000, Comparative effects of temperature on suspension feeding and energy budgets of the pearl oysters Pinctada margaritifera and P. maxima. Mar. Ecol. Prog. Ser. 195, 179–188. CrossRefGoogle Scholar