Fish Physiology and Biochemistry

, Volume 44, Issue 2, pp 527–542 | Cite as

Effects of long-term feed deprivation on body weight loss, muscle composition, plasma metabolites, and intermediate metabolism of meagre (Argyrosomus regius) under different water temperatures

  • Stavros Chatzifotis
  • Sofia Clavero
  • Christiana Kounna
  • Alexandros Soumalevris
  • Konstantinos Feidantsis
  • Efthimia Antonopoulou


The effect of feed deprivation at four water temperatures (17, 20, 23, 26 °C) was investigated in meagre (Argyrosomus regius) of initial mean weight ± SD, 116.16 ± 4.74 g, in triplicate groups. Fish were deprived of feed for a period of 60 days and sampled on days 0, 14, 41, and 60, during which body weight, specific growth rate, somatic indices, muscle proximate composition, plasma metabolite levels (total lipids, proteins, cholesterol, triglycerides, glucose), and liver and muscle enzymatic activities [L-lactate dehydrogenase (L-LDH), citrate synthase (CS), malate dehydrogenase (MDH)] were evaluated. Long-term feed deprivation resulted in a significant decrease in body weight, condition factor (CF), hepatosomatic index (HSI), muscle lipids, and plasma metabolites (all except proteins) and increase in muscle moisture. Plasma glucose concentration decreased with time and became significantly lower at 41 and 60 days. Glucose concentration and weight loss expressed a different response in the short term (14 days) than in the long term (14 and 60 days) of feed deprivation, suggesting a change in glucose metabolic profile. After 60 days of feed deprivation, there was an increase in the L-LDH activity in the liver at all temperature levels, which reflects a rising glycolytic potential by activating the carbohydrate metabolism and an ATP-dependent demand. MDH activity increased in the liver and muscle, except at 17 °C in the muscle, which indicates aerobic glycolysis and lipolysis. CS activity in the liver increased after the 60 days, whereas that in the muscle decreased, indicating the muscle is less dependent on aerobic oxidation for energy reserves.


Argyrosomus regius Feed deprivation Fasting Starvation Metabolism Temperature 


Funding information

Financial support for this study has been provided by the Ministry of Education, Lifelong Learning and Religious Affairs, General Secretariat for Research and Technology, Greece, under the call “Cooperation” of the National Strategic Reference Framework 2007–2013 (SYN09-24-424) to Dr. Constantinos C. Mylonas, titled “Development of methods for re-production and rearing of meagre (Argyrosomus regius) as a means for the enhancement of the competitiveness of aquaculture, with the introduction of new species.”

Compliance with ethical standards

HCMR installations at Crete are licensed facilities for operations of breeding and experimentation use of fish issued by the region of Crete, General Directorate of Agricultural and Veterinary, under the updated license no. 3989/01.03.2017. Experimental protocols of starvation as well as surgery and sacrifice conditions were approved under the license numbers EL91-BIO-03 and EL91-BIO-04, following the Greek Presidential Degree No. 56/2013 and Official Journal of the Greek Government No. 106/30 April 2013 on the protection of animals used for scientific purposes.


  1. Abolfathi M, Hajimoradloo A, Ghorban R, Zamani A (2012) Effect of starvation and refeeding on digestive enzyme activities in juvenile roach, Rutilus rutilus caspicus. Comp Biochem Physiol 161(2):166–173. CrossRefGoogle Scholar
  2. Alliot E, Pastoureaud A, Thebault H (1983) Influence de la temperature et de la salinite sur la croissance et la composition corporelle d’alevins de Dicentrarchus labrax. Aquaculture 31(2-4):181–194. CrossRefGoogle Scholar
  3. Alliot E, Djabali M, Pastoureaud A, Thebault H (1984) Changes in the biochemical composition of tissues in juvenile sea bass during forced starvation. Biochem Syst Ecol 12(2):209–213. CrossRefGoogle Scholar
  4. Aranda A, Sanchez-Vazquez FJ, Madrid JA (2001) Effect of short-term fasting on macronutrient self-selection in sea bass. Physiol Behav 73(1-2):105–109. CrossRefPubMedGoogle Scholar
  5. Bar N (2014) Physiological and hormonal changes during prolonged starvation in fish. Can J Fish Aquat Sci 71(10):1447–1458. CrossRefGoogle Scholar
  6. Bar N, Volkoff H (2012) Adaptation of the physiological, endocrine and digestive system functions to prolonged food deprivation in fish. In: McCue MD (ed) Comparative physiology of fasting, starvation and food limitation. Springer, Heidelberg, pp 69–89. CrossRefGoogle Scholar
  7. Basu N, Todgham AE, Ackerman PA, Bibeau MR, Nakano K, Schulte PM, Iwama GK (2002) Heat shock protein genes and their functional significance in fish. Gene 295(2):173–183. CrossRefPubMedGoogle Scholar
  8. Beamish FWH (1964) Influence of starvation on standard and routine oxygen consumption. Trans Am Fish Soc 93(1):103–107.[103:IOSOSA]2.0.CO;2 CrossRefGoogle Scholar
  9. Binner M, Kloas W, Hardewig I (2008) Energy allocation in juvenile roach and burbot under different temperature and feeding regimes. Fish Physiol Biochem 34(2):103–106. CrossRefPubMedGoogle Scholar
  10. 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(4):469–479. CrossRefGoogle Scholar
  11. Bond CE (1996) Nervous and endocrine systems. In: Bond CE (ed) Biology of fishes. Saunders College Publishing, FortWorth, pp 241–258Google Scholar
  12. Brett JR, Shelbourn JE, Shoop CT (1969) Growth rate and body composition of fingerling sockeye salmon, Oncorhynchus nerka, in relation to temperature and ration size. J Fish Res Board Can 26(9):2363–2394. CrossRefGoogle Scholar
  13. Buckley BA, Hofmann EG (2004) Magnitude and duration of thermal stress determine kinetics of hsp gene regulation in the goby Gillicthys mirabilis. Physiol Biochem Zool 77(4):570–581. CrossRefPubMedGoogle Scholar
  14. Buentello JA, Gatlin DM III, Neill WH (2000) Effects of water temperature and dissolved oxygen on daily feed consumption, feed utilization and growth of channel catfish (Ictalurus punctatus). Aquaculture 182(3-4):339–352. CrossRefGoogle Scholar
  15. Chatzifotis S, Panagiotidou M, Papaioannou N, Pavlidis M, Nengas I, Mylonas CC (2010) Effect of dietary lipid levels on growth, feed utilization, body composition and serum metabolites of meagre (Argyrosomus regius) juveniles. Aquaculture 307(1-2):65–70. CrossRefGoogle Scholar
  16. 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(1-4):53–59. CrossRefGoogle Scholar
  17. Chatzifotis S, Santos-Rodríguez L, Mastoraki M, Antonopoulou E (2015) Effect of temperature and feeding level on energy and nutrient efficiency of meagre (Argyrosomus regius). Paper presented at the AE2015 Annual Meeting of the European Aquaculture Society, Rotterdam, pp 147–148Google Scholar
  18. Cho CY, Kaushik SJ (1990) Nutritional energetics in fish: energy and protein utilization in rainbow trout (Salmo gairdneri). World Rev Nutr Diet 61:132–172CrossRefPubMedGoogle Scholar
  19. Collins AL, Anderson TA (1995) The regulation of endogenous energy stores during starvation and refeeding in the somatic tissues of the golden perch. J Fish Biol 47(6):1004–1015. CrossRefGoogle Scholar
  20. Cordiner S, Egginton S (1997) Effects of seasonal temperature acclimatization on muscle metabolism in rainbow trout, Oncorhynchus mykiss. Fish Physiol Biochem 16(4):333–343. CrossRefGoogle Scholar
  21. Costas B, Aragão C, Ruiz-Jarabo I, Vargas-Chacoff L, Arjona FJ, Dinis MT, Mancera JM, Conceição LEC (2011) Feed deprivation in Senegalese sole (Solea senegalensis Kaup, 1858) juveniles: effects on blood plasma metabolites and free amino acid levels. Fish Physiol Biochem 37(3):495–504. CrossRefPubMedGoogle Scholar
  22. Couto A, Enes P, Peres H, Oliva-Teles A (2008) Effect of water temperature and dietary starch on growth and metabolic utilization of diets in gilthead sea bream (Sparus aurata) juveniles. Comp Biochem Physiol, Part A 151(1):45–50. CrossRefGoogle Scholar
  23. van Dijk PLM, Staaks G, Hardewig I (2002) The effect of fasting and refeeding on temperature preference, activity and growth of roach, Rutilus rutilus. Oecologia 130(4):496–504. CrossRefPubMedGoogle Scholar
  24. van Dijk PLM, Hardewig I, Hölker F (2005) Energy reserves during food deprivation and compensatory growth in juvenile roach: the importance of season and temperature. J Fish Biol 66(1):167–181. CrossRefGoogle Scholar
  25. Driedzic WR, Almeida-Val VMF (1996) Enzymes of cardiac energy metabolism in Amazonian teleosts and the fresh-water stingray (Potamotrygon hystrix). J Exp Zool 274(6):327–333.<327::AID-JEZ1>3.0.CO;2-Q CrossRefGoogle Scholar
  26. Echevarría G, Martínez-Bebiá M, Zamora S (1997) Evolution of biometric indices of plasma metabolites during prolonged starvation in European sea bass (Dicentrarchus labrax, L). Comp Biochem Physiol 118(1):111–123. CrossRefGoogle Scholar
  27. Elliot JM (1976) Body composition of brown trout (Salmo trutta L) in relation to temperature and ration size. J Anim Ecol 45(1):273–289. CrossRefGoogle Scholar
  28. Enes P, Panserat S, Kaushik S, Oliva-Teles A (2008) Hepatic glucokinase and glucose-6-phosphatase responses to dietary glucose and starch in gilthead sea bream (Sparus aurata) juveniles reared at two temperatures. Comp Biochem Physiol A 149(1):80–86. CrossRefGoogle Scholar
  29. Estévez A, Treviño L, Kotzamanis Y, Karacostas I, Tort L, Gisbert E (2010) Effects of different levels of plant proteins on the ongrowing of meagre (Argyrosomus regius) juveniles at low temperatures. Aquac Nutr 17:e572–e582CrossRefGoogle Scholar
  30. Feidantsis K, Pörtner HO, Lazou A, Kostoglou B, Michaelidis B (2009) Metabolic and molecular stress responses of the gilthead sea bream Sparus aurata during long term exposure to increasing temperatures. Mar Biol 156(4):797–809. CrossRefGoogle Scholar
  31. Figueiredo-Garutti ML, Navarro I, Capilla E, Souza R, Moraes G, Gutiérrez J, Vicentini-Paulinoe ML (2002) Metabolic changes in Brycon cephalus (Teleostei, Characidae) during post-feeding and fasting. Comp Biochem Physiol A 132(2):467–476. CrossRefGoogle Scholar
  32. Folch J, Less M, Sloane Stanley GH (1957) A simple method for the isolation and purification of total lipides from animal tissues. J Biol Chem 226(1):497–509PubMedGoogle Scholar
  33. Food and Agriculture Organization of the United Nations (2017) Cultured aquatic species information programme meagre (Argyrosomus regius) (Asso, 1801) In: Cultured Aquatic Species Information Programme Available via http://www.faoorg/fishery/culturedspecies/Argyrosomus_regius/en
  34. Furné M, Morales AE, Trenzado CE, García-Gallego M, Hidalgo MC, Domezain A, Sanz-Rus A (2012) The metabolic effects of prolonged starvation and refeeding in sturgeon and rainbow trout. J Comp Physiol B 182(1):63–76. CrossRefPubMedGoogle Scholar
  35. Gao Y, Wang Z, Hur J-W, Lee J-Y (2015) Body composition and compensatory growth in Nile tilapia Oreochromis niloticus under different feeding intervals. Chin J Oceanol Limnol 33(4):945–956. CrossRefGoogle Scholar
  36. Gillis TE, Ballantyne JS (1996) The effects of starvation on plasma free amino acid and glucose concentrations in lake sturgeon. J Fish Biol 49(6):1306–1316. CrossRefGoogle Scholar
  37. Grigorakis K, Alexis MN (2005) Effects of fasting on the meat quality and fat deposition of commercial-size farmed gilthead sea bream (Sparus aurata, L) fed different dietary regimes. Aquac Nutr 11(5):341–344. CrossRefGoogle Scholar
  38. Guderley H (1998) Temperature and growth rates as modulators of the metabolic capacities of fish muscle. In: Pörtner HO, Playle RC (eds) Cold Ocean Physiology SEB Sem Ser: 66. Cambridge University Press, Cambridge, pp 58–87CrossRefGoogle Scholar
  39. Guderley H, Dutil JD, Pelletier D (1996) The physiological status of Atlantic cod, Gadus morhua, in the wild and the laboratory: estimates of growth rates under field conditions. Can J Fish Aquat Sci 53(3):550–557. CrossRefGoogle Scholar
  40. Guderley H, Lapointe D, Bédard M, Dutil J-D (2003) Metabolic priorities during starvation: enzyme sparing in liver and white muscle of Atlantic cod, Gadus morhua L. Comp Biochem Physiol A 135(2):347–356. CrossRefGoogle Scholar
  41. Gunasekera RM, De Silva SS, Ingram BA (2001) Chemical changes in fed and starved larval trout cod, Maccull Chella macquarensis during early development. Fish Physiol Biochem 25(4):255–268. CrossRefGoogle Scholar
  42. 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(2):107–112. CrossRefPubMedGoogle Scholar
  43. Hemre G-I, Lie O, Sundby A (1993) Dietary carbohydrate utilization in cod (Gadus morhua): metabolic responses to feeding and fasting. Fish Physiol Biochem 10(6):455–463. CrossRefPubMedGoogle Scholar
  44. Hidalgo F, Alliot E (1988) Influence of water temperature on protein requirement and protein utilization in juvenile sea bass, Dicentrarchus labrax. Aquaculture 72(1-2):115–129. CrossRefGoogle Scholar
  45. Hidalgo F, Alliot E, Thebault H (1987) Influence of water temperature on food intake, food efficiency and gross composition of juvenile sea bass, Dicentrarchus labrax. Aquaculture 64(3):199–207. CrossRefGoogle Scholar
  46. Hölker F, Volkmann S, Wolter C, van Dijk PLM, Hardewig I (2004) Colonization of the freshwater environment by a marine invader: how to cope with warm summer temperatures? Evol Ecol Res 6:1123–1144Google Scholar
  47. 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(1-4):357–363. CrossRefGoogle Scholar
  48. Ince BW, Thorpe A (1976) The effects of starvation and force-feeding on the metabolism of the northern pike, Esox lucius L. J Fish Biol 8(1):79–88. CrossRefGoogle Scholar
  49. Jobling M (1980) Effects of starvation on proximate chemical composition and energy utilization of plaice, Pleuronectes platessa L. J Fish Biol 17(3):325–334. CrossRefGoogle Scholar
  50. Koch F, Wieser W, Niederstätter H (1992) Interactive effects of season and temperature on enzyme activities, tissue and whole animal respiration in roach, Rutilus rutilus. Environ Biol Fish 33(1-2):73–85. CrossRefGoogle Scholar
  51. Lanning G, Eckerle LG, Serendero I, Sartoris FJ, Fischer T, Knust R, Johansen T, Pörtner HO (2003) Temperature adaptation in eurythermal cod (Gadus morhua): a comparison of mitochondrial enzyme capacities in boreal and Arctic populations. Mar Biol 142(3):589–599. CrossRefGoogle Scholar
  52. Lauff RF, Wood CM (1996) Respiratory gas exchange, nitrogenous waste excretion, and fuel usage during starvation in juvenile rainbow trout, Oncorhynchus mykiss. J Comp Physiol 165B:542–551CrossRefGoogle Scholar
  53. Love RM (1970) The chemical biology of fishes. Academic Press, New York, p 547Google Scholar
  54. Luo Z, Tan XY, Wang WM, Fan QX (2009) Effects of long-term starvation on body weight and body composition of juvenile channel catfish, Ictalurus punctatus, with special emphasis on amino acid and fatty acid changes. J Appl Ichthyol 25(2):184–189. CrossRefGoogle Scholar
  55. Mancera JM, Vargas-Chacoff L, García-López A, Kleszczynska A, Kalamarz H, Martínez-Rodríguez G, Kulczykowska E (2008) High density and food deprivation affect arginine vasotocin, isotocin and melatonin in gilthead sea bream (Sparus aurata). Comp Biochem Physiol A 149(1):92–97. CrossRefGoogle Scholar
  56. Martínez FJ, García MP, Canteras M, De Costa J, Zamora S (1992) Effect of simultaneous variation of weight, density, temperature, and O2 concentration on rainbow trout (Oncorhynchus mykiss) body composition. Reprod Nutr Dev 32(2):105–112. CrossRefPubMedGoogle Scholar
  57. Martinez-Llorens S, Espert J, Moya J, Cerdá MJ, Tomás-Vidal A (2011) Growth and nutrient efficiency of meagre (Argyrosomus regius, Asso1801) fed extruded diets with different protein and lipid levels. Int J Fish Aquac 3:195–203Google Scholar
  58. McCarthy I, Houlihan D (1997) The effect of temperature on protein metabolism in fish: the possible consequences for wild Atlantic salmon (Salmo salar L.) stocks in Europe as a result of global warming. In: Wood C, McDonald D (eds) Global warming: implications for freshwater and marine fish. Cambridge University Press, Cambridge, number 61 in Society of Experimental Biology Seminar Series, pp 51–77Google Scholar
  59. Médale F, Aguirre P, Kaushik SJ (1991) Utilization of dietary carbohydrates by rainbow trout at two water temperatures. In: Wenk, C, Boessinger, M (Eds), Energy metabolism of farm animals. EAAP Publication (European Association for Animal Production). Presented at 12. Symposium EAAP, Kartause Ittigen, SWZ (1991-09-01–1991-09-07). Institut fur Nutztierwissenschaften, Zurich, 58: 392–395.
  60. Médale F, Poli JM, Vallée F, Blanc D (1999) Comparaison de l’utilisation digestive et métabolique d’un régime riche en glucides par la carpe à 18 °C et 25 °C. Cybium 23:139–152Google Scholar
  61. Mehner T, Wieser W (1994) Energetics and metabolic correlates of starvation in juvenile perch (Perca fluviatilis). J Fish Biol 45(2):325–333. CrossRefGoogle Scholar
  62. Méndez G, Wieser W (1993) Metabolic responses to food deprivation and refeeding in juveniles of Rutilus rutilus (Teleostei: Cyprinidae). Environ Biol Fish 36(1):73–81. CrossRefGoogle Scholar
  63. Moon TW, Mommsen TP (1987) Enzymes of intermediary metabolism in tissues of the little skate, Raja erinacea. J Exp Zool 244(1):9–15Google Scholar
  64. Moreira IS, Peres H, Couto A, Enes P, Oliva-Teles A (2008) Temperature and dietary carbohydrate level effects on performance and metabolic utilisation of diets in European sea bass (Dicentrarchus labrax) juveniles. Aquaculture 274(1):153–160. CrossRefGoogle Scholar
  65. Navarro I, Gutiérrez J (1995) Fasting and starvation. In: Hochachka P, Mommsen TP (eds) Biochemistry and molecular biology of fishes, metabolic biochemistry, vol 4. Elsevier, Amsterdam, pp 393–434Google Scholar
  66. Olivereau M, Olivereau JM (1997) Long-term starvation in the European eel: general effects and responses of pituitary growth hormone-(GH) and somatolactin-(SL) secreting cells. Fish Physiol Biochem 17(1/6):261–269. CrossRefGoogle Scholar
  67. Panepucci L, Fernades MN, Sanches JR, Rantin FT (2000) Changes in lactate dehydrogenase and malate dehydrogenase activities during hypoxia and after temperature acclimation in the armored fish, Rhinelepis strigosa (Siluriformes, Loricariidae). Rev Bras Biol 60(2):353–360. CrossRefPubMedGoogle Scholar
  68. Panepucci RA, Panepucci L, Fernandes MN, Sanches JR, Rantin FT (2001) The effects of hypoxia and recuperation on carbohydrate metabolism in pacu (Piaractus mesopotamicus). Braz J Biol 61(4):547–554. CrossRefPubMedGoogle Scholar
  69. Pereira C, Vijayan MM, Moon TW (1995) In vitro hepatocyte metabolism of alanine and glucose and the response to insulin in fed and fasted rainbow trout. J Exp Zool A 271(6):425–431. CrossRefGoogle Scholar
  70. Peres H, Oliva-Teles A (1999) Influence of temperature on protein utilization in juvenile European sea bass (Dicentrarchus labrax). Aquaculture 170(3-4):337–348. CrossRefGoogle Scholar
  71. Peres H, Oliva-Teles A (2001) Effect of dietary protein and lipid level on metabolic utilization of diets by european sea bass (Dicentrarchus labrax) juveniles. Fish Physiol Biochem 25(4):269–275. CrossRefGoogle Scholar
  72. 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(1-4):325–335. CrossRefGoogle Scholar
  73. Pérez-Jiménez A, Cardenete G, Hidalgo MC, García-Alcázar G, Abellán E, Morales AE (2012) Metabolic adjustments of Dentex dentex to prolonged starvation and refeeding. Fish Physiol Biochem 38(4):1145–1157. CrossRefPubMedGoogle Scholar
  74. Person-Le Ruyet J, Mahè K, Le Bayon N, Le Delliou H (2004) Effects of temperature on growth and metabolism in a Mediterranean population of European sea bass, Dicentrarchus labrax. Aquaculture 237(1-4):269–280. CrossRefGoogle Scholar
  75. Polakof S, Arjona FJ, Sangiao-Alvarellos S, Míguez JM, Martín del Río MP, Mancera JM, Soengas JL (2006) Food deprivation alters osmoregulatory and metabolic responses to salinity acclimation in gilthead sea bream Sparus aurata. J Comp Physiol B 176(5):441–452. CrossRefPubMedGoogle Scholar
  76. Polakof S, Panserat S, Soengas JL, Moon TW (2012) Glucose metabolism in fish: a review. J Comp Physiol B 182(8):1015–1045. CrossRefPubMedGoogle Scholar
  77. Poli BM, Parisi G, Zampacavallo G, Lurzan F, Mecatti M, Lupi P, Bonelli A (2003) Preliminary results on quality and quality changes in reared meagre (Argyrosomus regius): body and fillet traits and freshness changes in refrigerated commercial-size fish. Aquac Int 11(3):301–311. CrossRefGoogle Scholar
  78. Power DM, Melo J, Santos CRA (2000) The effect of food deprivation and refeeding on the liver, thyroid hormones and transthyretin in sea bream. J Fish Biol 56(2):374–387. CrossRefGoogle Scholar
  79. Quéméner L, Suquet M, Mero D, Gaignon JL (2002) Selection method of new candidates for finfish aquaculture: the case of the French Atlantic, the channel and the North Sea coasts. Aquat Living Resour 15(5):293–302. CrossRefGoogle Scholar
  80. Rawles SD, Gaylord TG, Snyder GS, Freeman DW (2010) The influence of protein and energy density in commercial diets on growth, body composition and nutrient retention of sunshine bass, Morone chrysops ♀ × Morone saxatilis ♂, reared at extreme temperature. J World Aquacult Soc 41:165–178. CrossRefGoogle Scholar
  81. Rios FS, Kalinin AL, Rantin FT (2002) The effects of long-term food deprivation on respiration and haematology of the neotropical fish Hoplias malabaricus. J Fish Biol 61(1):85–95. CrossRefGoogle Scholar
  82. Rios FS, Kalinin AL, Fernandes MN, Rantin FT (2004) Changes in gut gross morphometry of traìra, Hoplias malabaricus (Teleostei, Erythrinidae) during long-term starvation and after refeeding. Braz J Biol 64(3b):683–689. CrossRefPubMedGoogle Scholar
  83. Rueda FM, Martinez FJ, Zamora S, Kentouri M, Divanach P (1998) Effect of fasting and reefeding on growth and body composition of red porgy, Pagrus pagrus L. Aquac Res 29:447–452Google Scholar
  84. Russel NR, Fish JD, Wootton RJ (1996) Feeding and growth of juvenile sea bass: effect of ration and temperature on growth rate and efficiency. J Fish Biol 49(2):206–220. CrossRefGoogle Scholar
  85. Sangiao-Alvarellos S, Guzmán JM, Laiz-Carrión R, Míguez JM, Martín del Río MP, Mancera JM, Soengas JL (2005) Interactive effects of high stocking density and food deprivation on carbohydrate metabolism in several tissues of gilthead sea bream Sparus aurata. J Exp Zool A 303:761–775CrossRefGoogle Scholar
  86. Santulli A, Messina CM, D’Amelio V (1997) Variations of lipid and apolipoprotein content in lipoproteins during fasting in European sea bass (Dicentrarchus labrax L). Comp Biochem Physiol, A 118(4):1233–1239. CrossRefGoogle Scholar
  87. 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(3):473–483. CrossRefPubMedGoogle Scholar
  88. Shimeno S, Kheyvyali D, Takeda M (1990) Metabolic adaptation to prolonged starvation in carp. Nippon Suisan Gakkaishi 56(1):35–41. CrossRefGoogle Scholar
  89. Shimeno S, Shikata T, Hosokawa H, Masumoto T, Kheyyali D (1997) Metabolic response to feeding rates in common carp, Cyprinus carpio. Aquaculture 151(1-4):371–377. CrossRefGoogle Scholar
  90. Sidell BD, Driedzic WR, Stowe DB, Johnston IA (1987) Biochemical correlations of power development and metabolic fuel preferenda in fish hearts. Physiol Zool 60(2):221–232Google Scholar
  91. Sidell BD, Moerland TS (1989) Effects of temperature on muscular function and locomotory performance in teleost fish. Adv Comp Environ Physiol 5:115–155. CrossRefGoogle Scholar
  92. Singer TD, Ballantyne JS (1989) Absence of extrahepatic lipid oxidation in a fresh-water elasmobranch, the dwarf stingray potamotrygon-magdalenae - evidence from enzyme-activities. J Exp Zool 251(3):355–360Google Scholar
  93. 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(6):491–511. CrossRefPubMedGoogle Scholar
  94. Stirling HP (1976) Effects of experimental feeding and starvation on the proximate composition of the European bass Dicentrarchus labrax. Mar Biol 34(1):85–91. CrossRefGoogle Scholar
  95. Takeuchi T, Watanabe T (1982) The effects of starvation and environmental temperature on proximate and fatty acid composition of carp and rainbow trout. Bull Jpn Soc Sci Fish 48(9):1307–1316. CrossRefGoogle Scholar
  96. Thibault M, Blier PU, Guderley H (1997) Seasonal variation of muscle metabolic organization in rainbow trout (Oncorhynchus mykiss). Fish Physiol Biochem 16(2):139–155. CrossRefGoogle Scholar
  97. Vigliano FA, Quiroga MI, Nieto JM (2002) Adaptaciones metabólicas al ayuno y realimentación en peces. Revista de Ictiología 10:79–108Google Scholar
  98. Walsh PJ, Foster GD, Moon TW (1983) The effects of temperature on metabolism of the American eel Anguilla rostrata (LeSueur). Physiol Zool 56(4):532–540. CrossRefGoogle Scholar
  99. Watt PW, Marshall PA, Heap SP, Loughna PT, Goldspink G (1988) Proteins synthesis in tissues of fed and starved carp, acclimated to different temperatures. Fish Physiol Biochem 4(4):165–176. CrossRefPubMedGoogle Scholar
  100. Weatherley AH, Gill HS (1981) Recovery growth following periods of restricted rations and starvation in rainbow trout Salmo gairdneri Richardson. J Fish Biol 18(2):195–208. CrossRefGoogle Scholar
  101. Weatherley AH, Gill HS (1983) Protein, lipid, water and caloric contents of immature rainbow trout, Salmo gairdneri Richardson. J Fish Biol 23(6):653–673. CrossRefGoogle Scholar
  102. Wilkins NP (1967) Starvation of the herring Clupea harengus L survival and some gross biochemical changes. Comp Biochem Physiol 23(2):503–518. CrossRefPubMedGoogle Scholar
  103. Zammit VA, Newsholme EA (1979) Activities of enzymes of tat and ketone-body metabolism and effects of starvation on blood concentrations of glucose and fat fuels in teleost and elasmobranch fish. Biochem J 184(2):313–322. CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer Science+Business Media B.V., part of Springer Nature 2017

Authors and Affiliations

  • Stavros Chatzifotis
    • 1
  • Sofia Clavero
    • 1
  • Christiana Kounna
    • 1
  • Alexandros Soumalevris
    • 2
  • Konstantinos Feidantsis
    • 2
  • Efthimia Antonopoulou
    • 2
  1. 1.Hellenic Centre for Marine Research (HCMR)Institute of Marine Biology Biotechnology and AquacultureHeraklionGreece
  2. 2.Laboratory of Animal Physiology, Department of Zoology, School of Biology, Faculty of ScienceAristotle University of ThessalonikiThessalonikiGreece

Personalised recommendations