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Physiological basis of extreme growth rate differences in the spat of oyster (Crassostrea gigas)

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Abstract

Juvenile oysters (Crassostrea gigas) (produced in November 2009) reared under uniform hatchery conditions for 4 months were selected for extreme growth rate differences by repeatedly taking larger and smaller individuals to achieve weight differences >30× between fast (F) and slow (S) growers. The physiological basis of differential growth was analyzed in experiments in June 2010, where components of energy gain (clearance and ingestion rates and absorption efficiency), energy loss (metabolic rates) and resulting scope for growth (J h−1) were compared for groups of F and S oysters fed three different ration levels (≈0.5, 1.5 and 3.0 mg of total particulate matter L−1). In both F and S oysters, a higher food ration promoted asymptotic increases in energy gain rates through regulatory adjustments to clearance rates, which maintained similar absorption efficiencies across the food concentrations. No significant differences were found between growth groups in mass-specific physiological rates (i.e., per unit of body mass). However, the scaling of these rates to a common size in both groups using allometric coefficients derived for C. gigas revealed higher energy gain rates coupled with lower metabolic costs of growth in fast growers. Thus, appropriate size-standardization is essential in accounting for observed differences in growth rate. Present results are in accordance with previous reports on other bivalve species on the physiological processes underlying endogenous growth differences, suggesting that the same interpretation can be applied to the extremes of these differences.

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References

  • Barillé L, Prou J, Héral M, Razet D (1997) Effects of high natural seston concentrations on the feeding, selection, and absorption of the oyster Crassostrea gigas (Thunberg). J Exp Mar Biol Ecol 212:149–172

    Article  Google Scholar 

  • Batista F, Leitão A, Fonseca V, Ben-Hamadou R, Ruano F, Henriques M, Guedes-Pinto H, Boudry P (2007) Individual relationship between aneuploidy of gill cells and growth rate in cupped oysters Crassostrea angulata, C. gigas and their reciprocal hybrids. J Exp Mar Biol Ecol 352:226–233

    Article  Google Scholar 

  • Bayne BL (1999) Physiological components of growth differences between individual oysters (Crassostrea gigas) and a comparison with Saccostrea commercialis. Physiol Biochem Zool 72(6):705–713

    Article  CAS  Google Scholar 

  • Bayne BL (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

    Article  Google Scholar 

  • Bayne BL (2004) Phenotypic flexibility and physiological tradeoffs in the feeding and growth of marine bivalve molluscs. Integr Comp Biol 44:425–432

    Article  Google Scholar 

  • Bayne BL, Hawkins AJS (1997) Protein metabolism, the costs of growth, and genomic heterozygosity: experiments with the mussel Mytilus galloprovincialis Lmk. Physiol Zool 70:391–402

    Article  CAS  Google Scholar 

  • Bayne BL, Newell RC (1983) Physiological energetics of marine molluscs. In: Salenium ASM, Wilbur KM (eds) The mollusca, Academic Press, New York, 4(1) pp 407–515

  • Bayne BL, Hedgecock D, McGoldrick D, Rees R (1999a) Feeding behaviour and metabolic efficiency contribute to growth heterosis in Pacific oysters [Crassostrea gigas (Thunberg)]. J Exp Mar Biol Ecol 233:115–130

    Article  Google Scholar 

  • Bayne BL, Svensson S, Nell JA (1999b) The physiological basis for faster growth in the Sydney rock oyster, Saccostrea commercialis. Biol Bull 197:377–387

    Article  Google Scholar 

  • Bougrier S, Geairon P, Deslous-Paoli JM, Bacher C, Jonquières G (1995) Allometric relationships and effects of temperature on clearance and oxygen consumption rates of Crassostrea gigas (Thunberg). Aquaculture 134:143–154

    Article  Google Scholar 

  • Brown JR (1988) Multivariate analyses of the role of environmental factors and seasonal and site-related growth variation in the Pacific oyster, Crassostrea gigas. Mar Ecol Progr Ser 45:225–236

    Article  Google Scholar 

  • Conover RJ (1966) Assimilation of organic matter by zooplankton. Limnol Oceanogr 11:338–354

    Article  Google Scholar 

  • Crisp DJ (1971) Energy flow measurements. In: Holme NA, Mc Intyre AD (eds) Methods for the study of marine benthos, (IBP nº 16). Blackwell, Oxford, p 197–323

  • Dickie LM, Boudreau PR, Freeman KR (1984) Influence of stock and site on growth and mortality in the blue mussel (Mytilus edulis). Can J Fish Aquat Sci 41:134–140

    Article  Google Scholar 

  • Evans S, Langdon C (2006) Direct and indirect responses to selection on individual body weight in the pacific oyster (Crassostrea gigas). Aquaculture 261:546–555

  • Gaffney PM, Scott TM, Koehn RK, Diehl WJ (1990) Interrelationships of heterozygosity, growth rate and heterozygote deficiencies in the coot clam, Munilia lateralis. Genetics 124:687–699

    CAS  Google Scholar 

  • Garton DW, Koehn RK, Scott TM (1984) Multiple-locus heterozygosity and the physiological energetics of growth in the coot clam, Mulinia lateralis, from a natural population. Genetics 108:445–455

    CAS  Google Scholar 

  • Genard B, Miner P, Nicolas J-L, Moraga D, Boudry P, Pernet F, Tremblay R (2013) Integrative study of physiological changes associated with bacterial infection in Pacific oyster larvae. PLoS One 8(5):e64534. doi:10.1371/journal.pone.0064534

    Article  CAS  Google Scholar 

  • Gnaiger E (1983) Heat dissipation and energetic efficiency in animal anoxibiosis: economy contra power. J Exp Zool 228:471–490

    Article  CAS  Google Scholar 

  • Haure J, Huvet A, Palvadeau H, Nourry M, Penisson C, Martin JLY, Boudry P (2003) Feeding and respiratory time activities in the cupped oysters Crassostrea gigas, Crassostrea angulata and their hybrids. Aquaculture 218:539–551

    Article  Google Scholar 

  • Hawkins AJS (1995) Effects of temperature change on ectotherm metabolism and evolution: metabolic and physiological interrelations underlying the superiority of multi-locus heterozygotes in heterogeneous environments. J Therm Biol 2:23–33

    Article  Google Scholar 

  • Hawkins AJS, Day AJ (1996) The metabolic basis of genetic differences in growth efficiency among marine animals. J Exp Mar Biol Ecol 203:93–115

    Article  CAS  Google Scholar 

  • Hawkins AJS, Bayne BL, Day AJ (1986) Protein turnover, physiological energetics and heterozygosity in the blue mussel Mytilus edulis: the basis of variable age-specific growth. Proc R Soc Lond 229B:161–176

    Article  Google Scholar 

  • Hawkins AJS, Widdows J, Bayne BL (1989a) The relevance of whole-body protein metabolism to measured costs of maintenance and growth in Mytilus edulis. Physiol Zool 62:745–763

    Google Scholar 

  • Hawkins AJS, Bayne BL, Day AJ, Rusin J, Worrall CM (1989b) Genotype-dependent interrelations between energy metabolism, protein metabolism and fitness. In: Ryland JS, Tyler PA (eds) Reproduction, genetics and distribution of marine organisms. Olsen and Olsen, Fredensborg, pp 283–292

    Google Scholar 

  • Hedgecock D, McGoldrick DJ, Manahan DT, Vavra J, Appelmans N, Bayne BL (1995) Quantitative and molecular genetic analyses of heterosis in bivalve molluscs. J Exp Mar Biol Ecol 203:49–59

    Article  Google Scholar 

  • Hedgecock D, Lin JZ, DeCola S, Haudenschild CD, Meyer E, Manahan DT, Bowen B (2007) Transcriptomic analysis of growth heterosis in larval Pacific oysters (Crassostrea gigas). Proc Natl Acad Sci USA 104:2313–2318

    Article  CAS  Google Scholar 

  • Ibarrola I, Larretxea X, Navarro E, Iglesias JIP, Urrutia MB (2008) Effects of body-size and season on digestive organ size and the energy balance of cockles fed with a constant diet of phytoplankton. J Comp Physiol B 178:501–514

    Article  CAS  Google Scholar 

  • Ibarrola I, Arambalza U, Navarro JM, Urrutia MB, Navarro E (2012) Allometric relationships in feeding and digestion in the Chilean mytilids Mytilus chilensis (Hupé), Choromytilus chorus (Molina) and Aulacomya ater (Molina): a comparative study. J Exp Mar Biol Ecol 426:18–27

    Article  Google Scholar 

  • Jenny MJ, Chapman RW, Annalaura M et al (2007) A cDNA microarray for Crassostrea virginica and C. gigas. Mar Biotech 9:577–591

    Article  CAS  Google Scholar 

  • Koehn RK, Gaffney PM (1984) Genetic heterozygosity and growth rate in Mytilus edulis. Mar Biol 82:1–7

    Article  Google Scholar 

  • Launey S, Hedegecock D (2001) High genetic load in the Pacific oyster Crassostrea gigas. Genetics 159:255–265

    CAS  Google Scholar 

  • Leitão A, Boudry P, Thiriot-Quiévreux C (2001) Negative correlation between aneuploidy and growth in the Pacific oyster Crassostrea gigas: ten years of evidence. Aquaculture 193:39–48

    Article  Google Scholar 

  • Mallet AL, Haley LH (1983) Growth rate and survival in pure population mating and crosses of the oyster Crassostrea virginica. Can J Fish Aquat Sci 40:948–954

    Article  Google Scholar 

  • Meyer E, Manahan DT (2010) Gene expression profiling of genetically determined growth variation in bivalve larvae (Crassostrea gigas). J Exp Biol 213:749–758

    Article  CAS  Google Scholar 

  • Morgan IJ, McCarthy ID, Metcalfe NB (2000) Life-history strategies and protein metabolism in overwintering juvenile Atlantic salmon: growth is enhanced in early migrants through lower protein turnover. J Fish Biol 56:637–647

    Article  Google Scholar 

  • Myrand B, Tremblay R, Sevigny JM (2009) Decreases in multi-locus heterozygosity in suspension-cultured mussels (Mytilus edulis) through loss of the more heterozygous individuals. Aquac 295:188–194

    Article  CAS  Google Scholar 

  • Newkirk GF (1980) Review of the genetics and the potential for selective breeding of commercially important bivalves. Aquaculture 19:209–228

    Article  Google Scholar 

  • Pace DA, Marsh AG, Leong PK, Green AJ, Hedgecock D, Manahan DT (2006) Physiological bases of genetically determined variation in growth of marine invertebrate larvae: a study of growth heterosis in the bivalve Crassostrea gigas. J Exp Mar Biol Ecol 335:188–209

    Article  Google Scholar 

  • Parry GD (1983) The influence of the costs of growth on ectotherm metabolism. J Theor Biol 101:453–477

    Article  CAS  Google Scholar 

  • Pernet F, Tremblay R, Redjah I, Sévigny JM, Gionet C (2008) Physiological and biochemical traits correlate with differences in growth rate and temperature adaptation among groups of the eastern oyster Crassostrea virginica. J Exp Biol 211:969–977

    Article  Google Scholar 

  • Riisgård HU (1988) Efficiency of particle retention and filtration rate in 6 species of Northeast American bivalves. Mar Ecol Prog Ser 45:217–223

    Article  Google Scholar 

  • Riisgård HU (1998) No foundation of a “3/4 power scaling law” for respiration in biology. Ecol Lett 1:71–73

    Article  Google Scholar 

  • Riisgård HU, Egede PP, Saavedra IB (2011) Feeding behaviour of the mussel, Mytilus edulis: new observations, with mini-review of current knowledge. J Mar Biol 2011:1–13. doi:10.1155/2011/312459

  • Ropert M, Goulletquer P (2000) Comparative physiological energetics of two suspension feeders: polychaete annelid Lanice conchilega (Pallas 1766) and Pacific cupped oyster Crassostrea gigas (Thunberg 1795). Aquaculture 181:171–189

    Article  Google Scholar 

  • Sheridan AK (1997) Genetic improvement of oyster production—a critique. Aquaculture 153:165–179

    Article  Google Scholar 

  • Tamayo D, Ibarrola I, Urrutia MB, Navarro E (2011) The physiological basis for inter-individual growth variability in the spat of clams (Ruditapes philippinarum). Aquaculture 321:113–120

    Article  Google Scholar 

  • Tamayo D, Ibarrola I, Navarro E (2013) Thermal dependence of clearance and metabolic rates in slow- and fast-growing spats of manila clam Ruditapes philippinarum. J Comp Physiol B 183:893–904

    Article  CAS  Google Scholar 

  • Tanguy A, Bierne N, Saavedra C et al (2008) Increasing genomic information in bivalves through new EST collections in four species: development of new genetic markers for environmental studies and genome evolution. Gene 408:27–36

    Article  CAS  Google Scholar 

  • Teixeira de Sousa J, Matias D, Joaquim S, Ben-Hamadou R, Leitão A (2011) Growth variation in bivalves: new insights into growth, physiology and somatic aneuploidy in the carpet shell Ruditapes decussatus. J Exp Mar Biol Ecol 406:46–53

    Article  Google Scholar 

  • Thiriot-Quièvreux C, Pogson GH, Zouros E (1992) Genetics of growth rate variation in bivalves: aneuploidy and heterozygosity effects in a Crassostrea gigas family. Genome 35:39–45

    Article  Google Scholar 

  • Toro JE, Vergara AM (1998) Growth and heterozygosity in a 12-month-old cohort of Ostrea chilensis obtained by mass spawning in laboratory. Mar Ecol 19:311–323

    Article  Google Scholar 

  • Toro JE, Vergara AM, Gallegillos R (1996) Multiple-locus heterozygosity and growth at two different stages in the life cycle of the Chilean oyster Ostrea chilensis. Mar Ecol Prog Ser 134:151–158

    Article  Google Scholar 

  • Vladimirova IG, Kleimenov SY, Radzinskaya LI (2003) The relation of energy metabolism and body weight in bivalves. Biol Bull 30:392–399

    Article  Google Scholar 

  • Whyte J (1987) Biochemical composition and energy content of six species of phytoplankton used in mariculture of bivalves. Aquaculture 60:231–241

    Article  CAS  Google Scholar 

  • Zar JH (1984) Bioestatistical analysis, 3rd edn. Prentice-Hall, Englewood Cliffs

    Google Scholar 

  • Zhang G, Fang X, Guo X et al (2012) The oyster genome reveals stress adaptation and complexity of shell formation. Nature 490(7418):49–54

    Article  CAS  Google Scholar 

  • Zhao X, Yu H, Kong L, Li Q (2012) Transcriptomic responses to salinity stress in the Pacific oyster Crassostrea gigas. PLoS One 7(9):e46244. doi:10.1371/journal.pone.0046244

    Article  CAS  Google Scholar 

  • Zouros E, Thiriot-Quièvreux C, Kotulas G (1996) The negative correlation between somatic aneuploidy and growth in the oyster Crassostrea gigas and implications for the effects of induced polyploidization. Genet Res 68:109–116

    Article  Google Scholar 

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Acknowledgments

This study was funded through the project AGL2009-09981 of the Spanish Ministry of Science and Innovation. D.T. was funded by a FPI grant from the Basque Government. Thanks are given to Juan Cigarría (Tinamenor S.L.) for providing selected specimens of oysters. Technical and human support provided by SGIker (UPV/EHU), MICINN, GV/EJ, ERDF and ESF is gratefully acknowledged. Comments and suggestions of two anonymous reviewers have greatly improved the manuscript.

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Correspondence to David Tamayo.

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Communicated by J. Grassle.

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Tamayo, D., Ibarrola, I., Urrutxurtu, I. et al. Physiological basis of extreme growth rate differences in the spat of oyster (Crassostrea gigas). Mar Biol 161, 1627–1637 (2014). https://doi.org/10.1007/s00227-014-2447-1

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  • DOI: https://doi.org/10.1007/s00227-014-2447-1

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