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Food regime modulates physiological processes underlying size differentiation in juvenile intertidal mussels Mytilus galloprovincialis

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Abstract

Feeding and growth experiments were conducted to test the hypothesis that physiological attributes responsible for size differentiation among bivalves likely vary with environmental conditions. Juvenile mussels (Mytilus galloprovincialis) were collected from an intertidal population in Biscay, Spain (43°24′42,462″N02°56′43,659″W), in January 2007 and 2009. These mussels were maintained in the laboratory under either restrictive or optimal feeding conditions until fast- and slow-growing individuals on each maintenance regime could be identified. After fast- and slow-growing individuals were identified, the components of energy balance responsible for such growth rate differences were measured. The analysis of physiological traits indicates that under optimal food supply conditions, the capacity to ingest and absorb food and associated costs of growth are the main factors underlying growth rate differences. The set of physiological differences changed when size differentiation took place under restrictive food conditions. Higher rates of absorption coupled with reduced rates of metabolism accounted for faster growth in this case, especially under low food rations.

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References

  • Alvarez G, Zapata C, Amaro R, Guerra A (1989) Multilocus heterozygosity at protein loci and fitness in the European oyster, Ostrea edulis L. Heredity 63:359–372

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Bayne BL (2000) Relations between variable rates of growth, metabolic costs and growth efficiencies in individual Sydney rock oysters (Saccostrea comercialis). J Exp Mar Biol Ecol 251:185–203

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

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

  • Bayne BL, Thompson RJ, Widdows J (1973) Some effects of temperature and food on the rate of oxygen consumption by Mytilus edulis L. In: Wieser W (ed) Effects of temperature on ectothermic organisms. Springer, Berlin, pp 181–193

    Chapter  Google Scholar 

  • Bayne BL, Hawkins AJS, Navarro E, Iglesias JIP (1989) Effects of seston concentration on feeding, digestion and growth in the mussel Mytilus edulis. Mar Ecol Prog Ser 55:47–54

    Article  Google Scholar 

  • 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 

  • 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 Inture AD (eds) Methods for the study of marine benthos, (IBP no 16). Blackwell, Oxford, pp 197–323

    Google Scholar 

  • David P (1998) Heterozygosity—fitness correlations: new perspectives on old problems. Heredity 80:531–537

    Article  Google Scholar 

  • David P, Delay B, Berthou P, Jarne P (1995) Alternative models for allozyme-associated heterosis in the marine bivalve Spisula ovalis. Genetics 139:1719–1726

    CAS  Google Scholar 

  • Diehl WJ, Koehn RK (1985) Multiple-locus heterozygosity, mortality and growth in a cohort of Mytilus edulis. Mar Biol 88:256–271

    Article  Google Scholar 

  • Diehl WJ, Gaffney PM, Koehn RK (1986) Physiological and genetic aspects of growth in the mussel Mytilus edulis. I. Oxygen consumption, growth and weight loss. Physiol Zool 59:201–211

    Article  Google Scholar 

  • Garton DW (1984) Relationship between multiple locus heterozygosity and physiological energetics of growth in the estuarine gastropod Thais haemastoma. Physiol Zool 57:530–543

    Article  Google Scholar 

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

    CAS  Google Scholar 

  • Gentili MR, Beaumont AR (1988) Environmental stress, heterozygosity, and growth rate in Mytilus edulis L. J Exp Mar Biol Ecol 120:145–153

    Article  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 

  • 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 (1989) The relevance of whole-body protein metabolism to measured costs of maintenance and growth in Mytilus edulis. Physiol Zool 62:745–763

    Article  Google Scholar 

  • Holey ME, Foltz DW (1987) Effect of multiple-locus heterozygosity and salinity on clearance rate in a brackish water clam, Rangia cuneata (sowerby). J Exp Mar Biol Ecol 111:121–131

    Article  Google Scholar 

  • Hulbert AJ, Else PL (2005) Membranes and the setting of energy demand. J Exp Biol 208:1593–1599

    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 

  • Koehn RK, Diehl WJ, Scott TM (1988) The differential contribution by individual enzymes of glycolysis and protein catabolism to the relationship between heterozygosity and growth rate in the coot clam, Mulinia lateralis. Genetics 118:121–130

    CAS  Google Scholar 

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

    CAS  Google Scholar 

  • LeBlanc N, Tremblay R, Davidson J, Landry T, McNiven M (2008) The effect of selection treatments on Mytilus edulis, modifications of genetic and physiological characteristics. Mar Biol 153:1141–1152

    Article  CAS  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 

  • Pace DA, Marsh AG, Leong Patrick K, 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 

  • 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  Google Scholar 

  • Tamayo D, Ibarrola I, Urrutxurtu I, Navarro E (2014) Physiological basis of extreme growth rate differences in the spat of oyster (Crassostrea gigas). Mar Biol 161:1627–1637

    Article  Google Scholar 

  • Tamayo D, Ibarrola I, Navarro E (2015) The effects of food conditioning on feeding and growth responses to variable rations in fast and slow growing spat of the Manila clam (Ruditapes philippinarum). J Exp Mar Biol Ecol 471:92–103

    Article  Google Scholar 

  • Thompson RJ, Bayne BL (1974) Some relationships between growth, metabolism and food in the mussel Mytilus edulis. Mar Biol 27:317–326

    Article  CAS  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. P S Z N Mar Ecol 19:311–323

    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 

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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. Authors are indebted to two referees for valuable comments and suggestions. Finally, Tamayo D. wants to thank, in particular, the invaluable support received from Muguruza C. over the years. Will you marry me?

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Authors and Affiliations

  1. Departamento GAFFA (Animal Physiology), Facultad de Ciencia y Tecnología, Universidad del País Vasco/Euskal Herriko Unibertsitatea, Apartado 644, 48080, Bilbao, Spain

    David Tamayo, Katerin Azpeitia, Pablo Markaide, Enrique Navarro & Irrintzi Ibarrola

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  1. David Tamayo
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  2. Katerin Azpeitia
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  3. Pablo Markaide
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  4. Enrique Navarro
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  5. Irrintzi Ibarrola
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Correspondence to David Tamayo.

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Responsible Editor: J. Grassle.

Reviewed by H. Guderley and an undisclosed expert.

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Tamayo, D., Azpeitia, K., Markaide, P. et al. Food regime modulates physiological processes underlying size differentiation in juvenile intertidal mussels Mytilus galloprovincialis . Mar Biol 163, 131 (2016). https://doi.org/10.1007/s00227-016-2905-z

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  • DOI: https://doi.org/10.1007/s00227-016-2905-z

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