Protein-sparing effect of carbohydrate in diets for juvenile turbot <i>Scophthalmus maximus</i> reared at different salinities -- Journal of Oceanology and Limnology,2015,33(1):57-69

	Cite this paper:
	ZENG Lin, LEI Jilin, AI Chunxiang, HONG Wanshu, LIU Bin. Protein-sparing effect of carbohydrate in diets for juvenile turbot Scophthalmus maximus reared at different salinities[J]. Journal of Oceanology and Limnology, 2015, 33(1): 57-69

Protein-sparing effect of carbohydrate in diets for juvenile turbot Scophthalmus maximus reared at different salinities

ZENG Lin^1,2,3, LEI Jilin^1,2,3, AI Chunxiang¹, HONG Wanshu¹, LIU Bin^2,3

1 College of Ocean and Earth Sciences, Xiamen University, Xiamen 361005, China;
2 National Technology System for Flatfish Culture Industry, Chinese Ministry of Agriculture, Qingdao 266071, China;
3 Qingdao Key Laboratory for Marine Fish Breeding and Biology, Yellow Sea Fisheries Research Institute, Chinese Academy of Fishery Sciences, Qingdao 266071, China

Abstract:

The aim of the present study was to investigate the protein-sparing effect of carbohydrate in diets for juvenile turbot (Scophthalmus maximus) reared at five salinities (12, 18, 24, 30, and 36). The fish were fed three isocaloric and isolipidic diets for 60 days. The results show that specific growth rate (SGR) and feed conversion efficiency (FCE) were higher in fish reared at salinities of 18 and 36, but lower at 12. Fish fed with diet C25P40 (25% carbohydrate and 40% protein) had lower SGR and FCE values compared with those fed with the C5P52 (5% carbohydrate and 52% protein) and C15P46 (15% carbohydrate and 46% protein) diets; however, there was no statistical difference between diet C5P52 and C15P46. SGR and FCE values were unaffected by diet composition in fish reared at salinity 36. Hepatic lipogenic enzyme activities were higher in fish reared at 18 and 36, but lower at 12, while glucokinase (GK) activity was higher in fish reared at 12, and lower at 18 and 36. Dietary starch enhanced GK activity while depressing lipogenic enzyme activity. However, lipogenic enzyme activity increased with increasing dietary starch in fish reared at 36. It is recommended that salinity should be maintained >12 in the farming of juvenile turbot. In addition, an increase in gelatinized starch from 5% to 15% could spare 6% dietary protein in fish reared at salinities of 18-30, while higher salinity (36) could improve dietary carbohydrate use and enhance the protein-sparing effect, which is linked with the induction of lipogenic capacities.

Key words: Scophthalmus maximus|carbohydrate|salinity|protein-sparing effect|hepatic glycometabolism

Received: 2014-03-19 Revised: 2014-04-28

Tools

PDF (303 KB) Free

Print this page

Add to favorites

Email this article to others

Authors

Articles by ZENG Lin

Articles by LEI Jilin

Articles by AI Chunxiang

Articles by HONG Wanshu

Articles by LIU Bin

References:
Alegre M, Ciudad C J, Fillat C, Guinovart J J. 1988. Determination of glucose-6-phosphatase activity using the glucose dehydrogenase-coupled reaction. Anal. Biochem., 173 (1): 185-189.
Almeida D V, Martins C, Figueiredo M, Lanes C F, Bianchini A, Marins L F. 2013. Growth hormone transgenesis affects osmoregulation and energy metabolism in zebrafish (Danio rerio). Transgenic. Res., 22 (1): 75-88.
AOAC. 2000. Official Methods of Analysis. In: International A ed. Association of Official Analytical Chemists. 17 th edn. Arlington, VA, America. p.1-45.
Barton B A. 2002. Stress in fishes: a diversity of responses with particular reference to changes in circulating corticosteroids. Integr. Comp. Biol., 42 (3): 517-525.
Bautista J M, Garrido-Pertierra A, Soler G. 1988. Glucose-6- phosphate dehydrogenase from Dicentrarchus labrax liver: kinetic mechanism and kinetics of NADPH inhibition. Biochim. Biophys. Acta, 967 (3): 354-363.
Björnsson B T, Johansson V, Benedet S, Einarsdottir I E, Hildahl J, Agustsson T, Jönsson E. 2002. Growth hormone endocrinology of salmonids: regulatory mechanisms and mode of action. Fish Physiol. Biochem., 27 (3-4): 227- 242.
Bolasina S N, Tagawa M, Yamashita Y. 2007. Changes on cortisol level and digestive enzyme activity in juveniles of Japanese flounder, Paralichthys olivaceus, exposed to different salinity regimes. Aquaculture, 266 (1): 255-261.
Boujard T, Médale F. 1994. Regulation of voluntary feed intake in juvenile rainbow trout fed by hand or by selffeeders with diets containing two different protein/energy ratios. Aquat. Living Resour., 7 (3): 211-215.
Bradford M M. 1976. A rapid and sensitive method for quantitation of microgram quantities of protein utilizing principle of protein-dye binding. Anal. Biochem., 72 (1): 248-254.
Bureau D P, Kirkland J B, Cho C Y. 1998. In: McCracken K J ed. Energy Metabolism of Farm Animals. CAB International Press, Wallingford, UK. p.163-166.
Caceres-Martinez C, Cadena-Roa M, Métailler R. 1984. Nutritional requirements of turbot (Scophthalmus maximus) I. A preliminary study of protein and lipid utilization. J. World Maricult. Soc., 15 (1-4): 191-202.
Chakrabarty K, Leveille G A. 1969. Acetyl-CoA carboxylase and fatty acid synthetase activities in liver and adipose tissue of meal-fed rats. Proc. Soc. Exp. Biol. Med., 131 (3): 1 051-1
054. Elo B, Villano C M, Govorko D, White L A. 2007. Larval zebrafish as a model for glucose metabolism: expression of phosphoenolpyruvate carboxykinase as a marker for exposure to anti-diabetic compounds. J. Mol. Endocrinol., 38 (4): 433-440.
Enes P, Panserat S, Kaushik S, Oliva-Teles A. 2009. Nutritional regulation of hepatic glucose metabolism in fish. Fish. Physiol. Biochem., 35 (3): 519-539.
Evans D H, Piermarini P M, Choe K P. 2005. The multifunctional fish gill: dominant site of gas exchange, osmoregulation, acid-base regulation, and excretion of nitrogenous waste. Physiol. Rev., 85 (1): 97-177.
Evans D H. 2008. Teleost fish osmoregulation: what have we learned since August Krogh, Homer Smith, and Ancel Keys. Am. J. Physiol - Reg. I., 295 (2): R704-R713.
Felip O, Ibarz A, Fernandez-Borras J, Beltran M, Martin-Perez M, Planas J, Blasco J. 2012. Tracing metabolic routes of dietary carbohydrate and protein in rainbow trout (Oncorhynchus mykiss) using stable isotopes ([ ¹³ C]starch and [ ¹⁵ N]protein): effects of gelatinisation of starches and sustained swimming. Br. J. Nutr., 107 (1): 834-844.
Fernandez F, Miquel A G, Cordoba M, Varas M, Meton I, Caseras A, Baanante I V. 2007. Effects of diets with distinct protein-to-carbohydrate ratios on nutrient digestibility, growth performance, body composition and liver intermediary enzyme activities in gilthead sea bream (Sparus aurata, L.) fingerlings. J. Exp. Mar. Biol. Ecol., 343 (1): 1-10.
Foster G D, Moon T W. 1986. Enzyme activities in the Atlantic hagfish, Myxine glutinosa: changes with captivity and food deprivation. Can. J. Zool., 64 (5): 1 080-1 085.
Friedrichsen M, Mortensen B, Pehmøller C, Birk J B, Jørgen F P, Wojtaszewski J. 2013. Exercise-induced AMPK activity in skeletal muscle: role in glucose uptake and insulin sensitivity. Mol. Cell. Endocrinol., 366 (2): 204-214.
Fuentes E N, Einarsdottir I E, Valdes J A, Alvarez M, Molina A, Björnsson B T. 2012. Inherent growth hormone resistance in the skeletal muscle of the fine flounder is modulated by nutritional status and is characterized by high contents of truncated GHR, impairment in the JAK2/ STAT5 signaling pathway, and low IGF-I expression. Endocrinology, 153 (1): 283-294.
Garcia-Riera M P, Hemre G I. 1996. Glucose tolerance in turbot, Scophthalmus maximus (L.). Aquacult. Nutr., 2 (2): 117-120.
Gatlin D M, Barrows F T, Brown P, Dabrowski K, Gaylord T G, Hardy R W, Herman E, Hu G, Krogdahl A, Nelson R, Overturf K, Rust M, Sealey W, Skonberg D, Souza E J, Stone D, Wilson R, Wurtele E. 2007. Expanding the utilization of sustainable plant products in aquafeeds: a review. Aquac ult. Res., 38 (6): 551-579.
Gaumet F, Boeuf G, Severe A, Roux L, Mayer-Gostan N. 1995. Effects of salinity on the ionic balance and growth of juvenile turbot. J. Fish. Biol., 47 (5): 865-876.
Hardy R W. 2010. Utilization of plant proteins in fish diets: effects of global demand and supplies of fishmeal. Aqua cult. Res., 41 (5): 770-776.
Imsland A K, Foss A, Gunnarsson S, Berntssen M H G, FitzGerald R, Bonga S W, Ham E V, Nævdal G, Stefansson S O. 2001. The interaction of temperature and salinity on growth and food conversion in juvenile turbot (Scophthalmus maximus). Aquaculture, 198 (3): 353-367.
Imsland A K, Gunnarsson S, Foss A, Stefansson S O. 2003. Gill Na⁺, K ⁺ -ATPase activity, plasma chloride and osmolality in juvenile turbot (Scophthalmus maximus) reared at different temperatures and salinities. Aquaculture, 218 (3): 671-683.
Imsland A K, Gustavsson A, Gunnarsson S, Foss A, Arnason J, Arnarson I, Jonsson A F, Smaradottir H, Thorarensen H. 2008. Effects of reduced salinities on growth, feed conversion efficiency and blood physiology of juvenile Atlantic halibut (Hippoglossus hippoglossus L.). Aquaculture, 274 (2): 254-259.
Keppler D, Decker K. 1974. Glycogen. Determination with amyloglucosidase. In: Bergmeyer H U ed. Methods of Enzymatic Analysis. Academic Press, New York. p.1 127- 1 131.
Klover P J, Mooney R A. 2004. Hepatocytes: critical for glucose homeostasis. Int. J. Biochem. Cell Biol., 36 (5): 753-758.
Krogdahl A, Sundby A, Olli J J. 2004. Atlantic salmon (Salmo salar) and rainbow trout (Oncorhynchus mykiss) digest and metabolize nutrients differently. Effects of water salinity and dietary starch level. Aquaculture, 229 (1): 335-360.
Lee J K, Cho S H, Park S U, Kim K D, Lee S M. 2003a. Dietary protein requirement for young turbot (Scophthalmus maximus L.). Aquacult. Nutr., 9 (4): 283-286.
Lee S M, Kim K D, Lall S P. 2003b. Utilization of glucose, maltose, dextrin and cellulose by juvenile flounder (Paralichthys olivaceus). Aquaculture, 221 (1): 427-438.
Lovell R T. 1989. Nutrition and Feeding of Fish. Van Nostrand Reinhold, New York. Mayzaud P, Conover R J. 1988. O:N atomic ratio as a tool to describe zooplankton metabolism. Mar. Ecol. Prog. Ser., 45 (3): 289-302.
McCormick S D, Bradshaw D. 2006. Hormonal control of salt and water balance in vertebrates. Gen. Comp. Endocr., 147 (1): 3-8.
McCormick S D, Regish A, O'Dea M F, Shrimpton J M. 2008. Are we missing a mineralocorticoid in teleost fish? Effects of cortisol, deoxycorticosterone and aldosterone on osmoregulation, gill Na⁺, K⁺ -ATPase activity and isoform mRNA levels in Atlantic salmon. Gen. Comp. Endocr., 157 (1): 35-40.
Meton I, Mediavilla D, Caseras A, Canto E, Fernandez F, Baanante I V. 1999. Effect of diet composition and ration size on key enzyme activities of glycolysisgluconeogenesis, the pentose phosphate pathway and amino acid metabolism in liver of gilthead sea bream (Sparus aurata). Br. J. Nutr., 82 (3): 223-232.
Mol K A, Van Der Geyten S, Burel C, Kuhn E R, Boujard T, Darras V M. 1998. Comparative study of iodothyronine outer ring and inner ring deiodinase activities in five teleostean fishes. Fish Physiol. Biochem., 18 (3): 253-266.
Mommsen T P, Vijayan M M, Moon T W. 1999. Cortisol in teleosts: dynamics, mechanisms of action, and metabolic regulation. Rev. Fish Biol. Fish., 9 (3): 211-268.
Moon T W. 2001. Glucose intolerance in teleost fish: fact or fiction? Comp. Biochem. Physiol. B, 129 (2): 243-249.
Nagel F, Danwitz A V, Tusche K, Kroeckel S, Bussel C G J, Schlachter M, Adem H, Tressel R P, Schulz C. 2012. Nutritional evaluation of rapeseed protein isolate as fish meal substitute for juvenile turbot (Psetta maxima L.) — Impact on growth performance, body composition, nutrient digestibility and blood physiology. Aquaculture, 3 (1): 357-364.
Paspatis M, Boujard T. 1996. A comparative study of automatic feeding and selffeeding in juvenile Atlantic salmon (Salmo salar) fed diets of different energy levels. Aquaculture, 145 (1): 245-257.
Polakof S, Mommsen T P, Soengas J L. 2011. Glucosensing and glucose homeostasis: from fish to mammals. Comp. Biochem. Physiol. B, 160 (4): 123-149.
Polakof S, Panserat S, Soengas J L, Moon T W. 2012. Glucose metabolism in fish: a review. J. Comp. Physiol. B, 182 (8): 1 015-1 045.
Ricker W E. 1979. Growth rates and models. In: Hoar W S ed. Bioenergetics and Growth, Fish Physiology. Academic Press, London. p.677-743.
Ruohonen K, Simpson S J, Raubenheimer D. 2007. A new approach to diet optimisation: a re-analysis using European whitefish (Coregonus lavaretus). Aquaculture, 267 (1): 147-156.
Sangiao-Alvarellos S, Arjona F J, Martín del Río M P, Míguez J M, Mancera J M, Soengas J L. 2005. Time course of osmoregulatory and metabolic changes during osmotic acclimation in Sparus auratus. J. Exp. Biol., 208 (22): 4 291-4 304.
Sangiao-Alvarellos S, Laiz-Carrión R, Guzmán J M, Martin del Río M P, Miguez J M, Mancera J M, Soengas J L. 2003. Acclimation of S. aurata to various salinities alters energy metabolism of osmoregulatory and nonosmoregulatory organs. Am. J. Physiol. Regul. Integr. Comp. Physiol., 285 (4): R897-R907.
Scholz S, Braumbeck T, Segner H. 1998. Viability and differential function of rainbow trout liver cells in primary culture: coculture with two permanent fish cells. In Vitro Cell. Dev. Anim., 34 (10): 762-771.
Soengas J L, Barciela P, Fuentes J, Otero J, Andres M D, Aldegunde M. 1993. Changes in muscle carbohydrate metabolism in domesticated rainbow trout (Oncorhynchus mykiss) after transfer to seawater. Comp. Biochem. Physiol. B, 105 (3): 173-179.
Stone D A J. 2003. Dietary carbohydrate utilization by fish. Rev. Fish Sci., 11 (4): 337-369.
Thivend P, Mercier C, Guilbot A. 1972. Determination of starch with glucoamylase. In: Whistler R L ed. Methods in Carbohydrate Chemistry. Academic Press, New York. p.100-105.
Tranulis M A, Dregni O, Christophersen B, Krogdahl A, Borrebaek B. 1996. A glucokinase-like enzyme in the liver of Atlantic salmon (Salmo salar). Comp. Biochem. Physiol. B, 114 (1): 35-39.
Tseng Y C, Hwang P P. 2008. Some insights into energy metabolism for osmoregulation in fish. Comp. Biochem. Physiol. C, 148 (4): 419-429.
Vielma J, Koskela J, Ruohonen K, Jokinen I, Kettunen J. 2003. Optimal diet composition for European whitefish (Coregonus lavaretus): carbohydrate stress and immune parameter responses. Aquaculture, 225 (1): 3-16.
Wendelaar Bonga S E. 2011. Hormonal responses to stress. In: Farrell A P ed. Encyclopedia of Fish Physiology: From Genome to Environment. Academic Press, San Diego. p.1 515-1 524.
Wilson R P. 1994. Utilization of dietary carbohydrate by fish. Aquaculture, 124 (1): 67-80.
Zang X N, Zhang X C, Mu X S, Liu B. 2013. Optimization of the purification methods for recovery of recombinant growth hormone from Paralichthys olivaceus. Acta Oceanol. Sin., 12 (1): 169-174.
Zhang Y J, Mai K S, Ma H M, Ai Q H, Zhang W B, Xu W. 2011. Rearing in intermediate salinity enhances immunity and disease-resistance of turbot (Scophthalmus maximus L.). Acta Oceanol. Sin., 30 (4): 122-128.