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The metabolic effects of prolonged starvation and refeeding in sturgeon and rainbow trout

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Abstract

The present study examines the particular metabolic strategies of the sturgeon Acipenser naccarii in facing a period of prolonged starvation (72 days) and subsequent refeeding (60 days) compared to the trout Oncorhynchus mykiss response under similar conditions. Plasma metabolites, endogenous reserves, and the activity of intermediate enzymes in liver and white muscle were evaluated. This study shows the mobilization of tissue reserves during a starvation period in both species with an associated enzymatic response. The sturgeon displayed an early increase in hepatic glycolysis during starvation. The trout preferentially used lactate for gluconeogenesis in liver and white muscle. The sturgeon had higher lipid-degradation capacity and greater synthesis of hepatic ketone bodies than the trout, although this latter species also showed strong synthesis of ketone bodies during starvation. During refeeding, the metabolic activity present before starvation was recovered in both fish, with a reestablishment of tissue reserves, plasmatic parameters (glucemia and cholesterol), and enzymatic activities in the liver and muscle. A compensatory effect in enzymes regarding lipids, ketone bodies, and oxidative metabolism was displayed in the liver of both species. There are metabolic differences between sturgeon and trout that support the contention that the sturgeon has common characteristics with elasmobranchs and teleosts.

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References

  • Agradi E, Abrami G, Serrini G, McKenzie D, Bolis C, Bronzi P (1993) The role of dietary n-3 fatty acid and vitamin E supplements in growth of sturgeon (Acipenser naccarii). Comp Biochem Physiol A 105:187–195

    Article  Google Scholar 

  • Ali M, Nicieza A, Wooton RJ (2003) Compensatory growth in fishes: a response to growth depression. Fish Fish 4:147–190

    Article  Google Scholar 

  • Barcellos LJG, Marqueze A, Trapp M, Quevedo RM, Ferreira D (2010) The effects of fasting on cortisol, blood glucose and liver and muscle glycogen in adult jundiá Rhamdia quelen. Aquaculture 300:231–236

    Article  CAS  Google Scholar 

  • Beaulieu MA, Guderley H (1998) Changes in qualitative composition of white muscle with nutritional status of Atlantic cod, Gadus morhua. Comp Biochem Physiol A 121:135–141

    Article  CAS  Google Scholar 

  • Black D, Love RM (1986) The sequential mobilisation and restoration of energy reserves in tissues of Atlantic cod during starvation and refeeding. J Comp Physiol B 156:469–479

    Article  CAS  Google Scholar 

  • Blasco J, Fernández J, Gutiérrez J (1992) Variations in tissue reserves, plasma metabolites and pancreatic hormones during fasting in immature carp (Cyprinus Carpio). Comp Biochem Physiol A 103:357–363

    Article  Google Scholar 

  • Böhm R, Hanke W, Segner H (1994) The sequential restoration of plasma metabolite levels, liver composition and liver structure in refed carp, Cyprinus carpio. J Comp Physiol B 164:32–41

    Article  Google Scholar 

  • Bond CE (1996) Nervous and endocrine systems. In: Bond CE (ed) Biology of fishes. Saunders College Publishing, FortWorth, pp 241–258

    Google Scholar 

  • Bradford M (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein using the principle of protein dye-binding. Anal Biochem 72:248–254

    Article  PubMed  CAS  Google Scholar 

  • Carmona R, García Gallego M, Sanz A, Domezain A, Ostos-Garrido MV (2004) Chloride cells and pavement cells in gill epithelia of Acipenser naccarii: ultrastructural modifications in seawater-acclimated specimens. J Fish Biol 64:553–556

    Article  Google Scholar 

  • Cataldi E, Ciccotti E, Di Marco P, Di Santo O, Bronzi P, Cataudella S (1995) Acclimation trials of juvenile Italian sturgeon to different salinities: morpho-physiological descriptors. J Fish Biol 47:609–618

    Article  Google Scholar 

  • Cataldi E, Barzaghi C, Di Marco P, Boglione C, Dini L, McKenzie DJ, Bronzi P, Cataudella S (1999) Some aspects of osmotic and ionic regulation in Adriatic sturgeon Acipenser naccarii. I: ontogenesis of salinity tolerance. J Appl Ichthyol 15:57–60

    Article  Google Scholar 

  • Cataldi E, Albano C, Boglione C, Dini L, Monaco G, Bronzi P, Cataudella S (2002) Acipenser naccarii: fine structure of the alimentary canal with references to its ontogenesis. J Appl Ichthyol 18:329–337

    Article  Google Scholar 

  • Chatzifotis S, Papadaki M, Despoti S, Roufidou C, Antonopoulou E (2011) Effect of starvation and re-feeding on reproductive indices, body weight, plasma metabolites and oxidative enzymes of sea bass (Dicentrarchus labrax). Aquaculture 316:53–59

    Article  CAS  Google Scholar 

  • Clementi M, Cataldi E, Capo C, Petruzzelli R, Tellone E, Giardina B (1999) Purification and characterization of the haemoglobin components from Adriatic sturgeon (Acipenser naccarii) blood. J Appl Ichthyol 15:78–80

    Article  CAS  Google Scholar 

  • Dave G, Johansson-Sjöbeck ML, Larsson A, Lewander K, Lidman U (1975) Effects of cortisol on the fatty acid composition of the total blood plasma lipids in the European eel, Anguilla anguilla L. Comp Biochem Physiol A 64:37–40

    Article  Google Scholar 

  • De la Herrán R, Robles F, Martínez-Espín E, Lorente JA, Ruiz Rejón C, Garrido-Ramos MA, Ruiz Rejón M (2004) Genetic identification of western Mediterranean sturgeons and its implications for conservation. Conserv Genet 5:545–551

    Article  Google Scholar 

  • de Roos R (1994) Plasma ketone, glucose, lactate, and alanine levels in the vascular supply to and from the brain of the spiny dogfish shark (Squalus acanthias). J Exp Zool 268:354–363

    Article  Google Scholar 

  • Duncan DB (1955) Multiple range and multiple F test. Biometrics 11:1–42

    Article  Google Scholar 

  • Ferguson RA, Storey KB (1991) Glycolytic and associated enzymes of rainbow trout (Oncorhynchus mykiss) red cells: in vitro and in vivo studies. J Exp Biol 155:469–485

    CAS  Google Scholar 

  • Figueiredo-Garutti ML, Navarro I, Capilla E, Souza R, Moraes G, Gutiérrez J, Vicentini-Paulinoe ML (2002) Metabolic changes in Brycoon cephalus (Teleostei, Characidae) during post-feeding and fasting. Comp Biochem Physiol A 132:467–476

    Article  CAS  Google Scholar 

  • Folch J, Lees M, Sloane-Stanley GM (1957) A simple method for the isolation and purification of total lipids from animal tissues. J Biol Chem 226:497–509

    PubMed  CAS  Google Scholar 

  • Foster GD, Moon TW (1991) Hypometabolism with fasting in the yellow perch (Perca flavescens): a study of enzymes, hepatocyte metabolism, and tissue size. Physiol Zool 64:259–275

    CAS  Google Scholar 

  • French CJ, Mommsen TP, Hochachka TP (1981) Amino acid utilization in isolated hepatocytes from rainbow trout. Eur J Biochem 113:311–317

    Article  PubMed  CAS  Google Scholar 

  • Furné M, Hidalgo MC, López A, García Gallego M, Morales AE, Domezain A, Domezain J, Sanz A (2005) Digestive enzyme activities in Adriatic sturgeon Acipenser naccarii and rainbow trout Oncorhynchus mykiss. A comparative study. Aquaculture 250:391–398

    Article  CAS  Google Scholar 

  • Furné M, García-Gallego M, Hidalgo MC, Morales AE, Domezain A, Domezain J, Sanz A (2008) Effect of starvation and refeeding on digestive enzyme in sturgeon (Acipenser naccarii) and trout (Oncorhynchus mykiss). Comp Biochem Physiol A 149:420–425

    Article  CAS  Google Scholar 

  • Furné M, García-Gallego M, Hidalgo MC, Morales AE, Domezain A, Domezain J, Sanz A (2009a) Oxidative stress parameters during starvation and refeeding periods in Adriatic sturgeon (Acipenser naccarii) and rainbow trout (Oncorhynchus mykiss). Aquacult Nutr 15:587–595

    Article  CAS  Google Scholar 

  • Furné M, Sanz A, García-Gallego M, Hidalgo MC, Domezain A, Domezain J, Morales AE (2009b) Metabolic organization of the sturgeon Acipenser naccarii. A comparative study with rainbow trout Oncorhynchus mykiss. Aquaculture 289:161–166

    Article  CAS  Google Scholar 

  • Garrido-Ramos MA, Soriguer MC, de la Herrán R, Jamilena M, Ruiz Rejón C, Domezain A, Hernando JA, Ruiz Rejón M (1997) Morphogenetic and genetic analysis as proof for the existence of two sturgeon species in the Guadalquivir river. Mar Biol 129:33–39

    Article  Google Scholar 

  • Gillis TE, Ballantyne JS (1996) The effects of starvation on plasma free amino acid and glucose concentrations in lake sturgeon Acipenser fulvescens. J Fish Biol 49:1306–1316

    Article  CAS  Google Scholar 

  • Grandi G, Chicca M (2004) Early development of the pituitary gland in Acipenser naccarii (Chondrostei, Acipenseriformes): an immunocytochemical study. Anat Embryol 208:311–321

    PubMed  CAS  Google Scholar 

  • Guderley H, Lapointe D, Bédard M, Dutil JD (2003) Metabolic priorities during starvation: enzyme sparing in liver and white muscle of Atlantic cod, Gadus morhua L. Comp Biochem Physiol A 135:347–356

    Article  CAS  Google Scholar 

  • Gutiérrez J, Pérez J, Navarro I, Zanuy S, Carrillo M (1991) Changes in plasma glucagon and insulin associated with fasting in sea bass (Dicentrarchus labrax). Fish Physiol Biochem 9:107–112

    Article  PubMed  Google Scholar 

  • Hernando JA, Vasiléva ED, Arlati G, Vasiléva YP, Santiago JA, Belysheva-Polyakova L, Domezain A, Soriguer MC (1999) New evidence for a wider historical area of two species of European sturgeons: Acipenser naccarii and Huso huso. J Ichthyol 39:803–806

    Google Scholar 

  • Hinch SG, Cooke SJ, Healey MC, Farrel AP (2005) Behavioural physiology of fish migrations: salmon as a model approach. Fish Physiol 24:239–295

    Article  Google Scholar 

  • Hung SSO, Liu W, Li H, Storebakken T, Cui Y (1997) Effect of starvation on some morphological and biochemical parameters in white sturgeon, Acipenser transmontanus. Aquaculture 151:357–363

    Article  Google Scholar 

  • Icardo JM, Guerrero A, Durán AC, Domezain A, Colvee E, Sans-Coma V (2004) The development of the sturgeon heart. Anat Embryol 208:439–449

    PubMed  Google Scholar 

  • Jürss K, Bittorf T, Vökler T (1986) Influence of salinity and food deprivation on growth, RNA/DNA ratio and certain enzyme activities in rainbow trout (Salmo gairdneri Richardson). Comp Biochem Physiol B 83:425–433

    Google Scholar 

  • Kirchner S, Seixas P, Kaushik S, Panserat S (2005) Effects of low protein intake on extra-hepatic gluconeogenic enzyme expression and peripheral glucose phosphorylation in rainbow trout (Oncorhynchus mykiss). Comp Biochem Physiol B 140:333–340

    Article  PubMed  CAS  Google Scholar 

  • Lim ALL, Ip YK (1989) Effect of fasting on glycogen metabolism and activities of glycolytic and gluconeogenic enzymes in the mudskipper Boleophthalmus boddaerti. J Fish Biol 34:349–367

    Article  CAS  Google Scholar 

  • Lin H, Romsos DR, Tack PI, Leville G (1977) Influence of dietary lipid on lipogenic enzyme activities in coho salmon Oncorhynchus kisutch (Walbaum). J Nutr 107:846–854

    PubMed  CAS  Google Scholar 

  • Lowery MS, Somero GN (1990) Starvation effects on protein synthesis in red and white muscle of the barred sand bass, Paralabrax nebulifer. Physiol Zool 63:630–648

    Google Scholar 

  • Machado CR, Garofalo MAR, Roselino JES, Kettelhut IC, Migliorini RH (1988) Effects of starvation, refeeding, and insulin on energy-linked metabolic processes in catfish (Rhamdia hilarii) adapted to a carbohydrate-rich diet. Gen Comp Endocrinol 71:429–437

    Article  PubMed  CAS  Google Scholar 

  • Martínez-Álvarez RM, Hidalgo MC, Domezain A, Morales AE, García-Gallego M, Sanz A (2002) Physiological changes of sturgeon Acipenser naccarii caused by increasing environmental salinity. J Exp Biol 205:3066–3079

    Google Scholar 

  • Martínez-Álvarez RM, Sanz A, García-Gallego M, Domezain A, Domezain J, Carmona R, Ostos-Garrido MV, Morales AE (2005) Adaptive branchial mechanisms in the sturgeon Acipenser naccarii during acclimation to salt water. Comp Biochem Physiol A 141:183–190

    Article  CAS  Google Scholar 

  • McKenzie DJ, Cataldi E, Di Marco P, Mandlich A, Romano P, Ansferri S, Bronzi P, Cataudella S (1999) Some aspects of osmotic and ionic regulation in Adriatic sturgeon Acipenser naccarii. II: morpho-physiological adjustments to hyperosmotic environments. J Appl Ichthyol 15:61–66

    Article  Google Scholar 

  • McKenzie DJ, Cataldi E, Romano P, Owen SF, Taylor EW, Bronzi P (2001a) Effects of acclimation to brackish water on the growth, respiratory metabolism, and swimming performance of young-of-the-year Adriatic sturgeon (Acipenser naccarii). Can J Fish Aquat Sci 58:1104–1112

    Article  Google Scholar 

  • McKenzie DJ, Cataldi E, Romano P, Taylor EW, Cataudella S, Bronzi P (2001b) Effects of acclimation to brackish water on tolerance of salinity challenge by young-of- the-year Adriatic sturgeon (Acipenser naccarii). Can J Fish Aquat Sci 58:1113–1121

    Article  Google Scholar 

  • Méndez G, Wieser W (1993) Metabolic responses to food deprivation and refeeding in juveniles of Rutilus rutilus (Teleostei: Cyprinidae). Environ Biol Fish 36:73–81

    Article  Google Scholar 

  • Metón I, Fernández F, Baanante IV (2003) Short- and long-term effects of refeeding on key enzyme activities in glicólisis-gluconeogenesis in the liver of gilthead seabream (Sparus aurata). Aquaculture 225:99–107

    Article  CAS  Google Scholar 

  • Miller KM, Schulze AD, Ginther N, Li S, Patterson DA, Farrell AP, Hinch SG (2009) Salmon spawning migration: metabolic shifts and environmental triggers. Comp Biochem Physiol 4D:75–89

    Article  CAS  Google Scholar 

  • Moon TW, Foster GD, Plisetskaya EM (1989) Changes in peptide hormones and liver enzymes in the rainbow trout deprived of food for 6 weeks. Can J Zool 67:2189–2193

    Google Scholar 

  • Morales AE, Pérez-Jiménez A, Hidalgo MC, Abellán E, Cardenete G (2004) Oxidative stress and antioxidant defences alter prolonged starvation in Dentex dentex liver. Comp Biochem Physiol C 139:153–161

    Google Scholar 

  • Moyes CD, Buck LT, Hochachka PW, Suárez RK (1989) Oxidative properties of carp red and white muscle. J Exp Biol 143:321–332

    PubMed  CAS  Google Scholar 

  • Navarro I, Gutiérrez J (1995) Fasting and starvation. In: Hochachka PW, Mommsen TP (eds) Biochemistry and molecular biology of fishes, metabolic biochemistry, vol 4. Elsevier, Amsterdam, pp 393–434

    Google Scholar 

  • Pérez-Jiménez A, Guedes MJ, Morales AE, Oliva-Teles A (2007) Metabolic responses to short starvation and refeeding in Dicentrarchus labrax. Effect of dietary composition. Aquaculture 265:325–335

    Article  CAS  Google Scholar 

  • Phan T, Bach A, Metais P (1974) Effects fasting on intermediate hepatic metabolism of rat. Arch Int Physiol Biochem 24:31–39

    Google Scholar 

  • Roehrig KL, Allred JB (1974) Direct enzymatic procedure for the determination of liver glycogen. Anal Biochem 58:414–421

    Article  PubMed  CAS  Google Scholar 

  • Salem M, Silverstein J, Rexroad CE, Yao J (2007) Effect of starvation on global gene expression and proteolysis in rainbow trout (Oncorhynchus mykiss). BMC Genomics 8:328–343

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Sheridan MA, Mommsen TP (1991) Effects of nutritional state on in vivo lipid and carbohydrate metabolism of coho salmon Oncorhynchus kisutch. Gen Comp Endocrinol 81:473–483

    Article  PubMed  CAS  Google Scholar 

  • Shimeno S, Kheyyali D, Takeda M (1990) Metabolic adaptation to prolonged starvation in carp. Nippon Suisan Gakk 56:35–41

    Article  CAS  Google Scholar 

  • Shimeno S, Duan-Cun-Ming y, Takeda M (1993) Regulation of carbohydrate metabolism in fish. XVI. Metabolic response to dietary carbohydrate to lipid ration Oreochromis niloticus. Nippon Suisan Gakk 59:827–833

    Article  CAS  Google Scholar 

  • Singer TD, Mahadevappa VG, Ballantyne JS (1990) Aspects of the energy metabolism of lake sturgeon, Acipenser fulvescens, with special emphasis on lipid and ketone body metabolism. Can J Fish Aquat Sci 47:873–881

    Article  CAS  Google Scholar 

  • Soengas JL, Strong EF, Fuentes J, Veira JAR, Andrés MD (1996) Food deprivation and refeeding in Atlantic salmon, Salmo salar: effects on brain and liver carbohydrate and ketone bodies metabolism. Fish Physiol Biochem 15:491–511

    Article  CAS  PubMed  Google Scholar 

  • Soriguer MC, Domezain A, Aragonés J, Domezain J, Hernando JA (2002) Feeding preference in juveniles of Acipenser naccarii Bonaparte 1836. J Appl Ichthyol 18:691–694

    Article  Google Scholar 

  • Trenzado C, Hidalgo MC, García-Gallego M, Morales AE, Furné M, Domezain A, Domezain J, Sanz A (2006) Antioxidant enzymes and lipid peroxidation in sturgeon Acipenser naccarii and trout Oncorhynchus mykiss. A comparative study. Aquaculture 254:758–767

    Article  CAS  Google Scholar 

  • Vázquez M, Rodríguez F, Domezain A, Salas C (2002) Development of the brain of the sturgeon Acipenser naccarii. J Appl Ichthyol 18:275–279

    Article  Google Scholar 

  • Wang T, Hung CCY, Randall DJ (2006) The comparative physiology of food deprivation: from feast to famine. Ann Rev Physiol 68:223–251

    Article  CAS  Google Scholar 

  • Zammit VA, Newsholme EA (1979) Activities of enzymes of fat and ketone-body metabolism and effects of starvation on blood concentrations of glucose and fat fuels in teleost and elasmobranch fish. Biochem J 184:313–322

    PubMed  CAS  PubMed Central  Google Scholar 

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Acknowledgments

This work was supported by the Spanish Ministerio de Educación y Ciencia, under the research project CGL2006/12193.

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Correspondence to Ana Sanz Rus.

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Communicated by G. Heldmaier.

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Furné, M., Morales, A.E., Trenzado, C.E. et al. The metabolic effects of prolonged starvation and refeeding in sturgeon and rainbow trout. J Comp Physiol B 182, 63–76 (2012). https://doi.org/10.1007/s00360-011-0596-9

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