Abstract
A 9-week feeding trial was conducted to investigate the effects of dietary carbohydrate to lipid ratio (CHO:LIP) on the growth performance and feed utilization of juvenile turbot Scophthalmus maximus (initial body weight 8.75 g ± 0.04 g). Four isonitrogenous and isoenergetic low protein level (39%) diets were formulated with increasing ratios of dietary carbohydrate to lipid (2:18, 6:18, 18:12 and 28:6). A high protein level (50%) diet with the 2:12 ratio of carbohydrate to lipid was used as the control. Results showed that the survival rate, contents of moisture, crude protein and ash in muscle were not significantly affected by dietary treatments. With the dietary CHO:LIP ratio increased from 2:18 to 18:12, weight gain rate significantly increased (P < 0.05). Higher dietary CHO:LIP ratio (28:6) resulted in the significantly decreased weight gain rate (P < 0.05). Meanwhile, this treatment also resulted in the highest daily feed intake and liver glycogen content, as well as the lowest feed efficiency (P < 0.05). Muscle glycogen content in fish fed the diet with 2:12 or 2:18 CHO:LIP ratio was significantly lower than those fed with the other three diets (P < 0.05). The present results confirmed that the juvenile turbot can utilize carbohydrate. Furthermore, the appropriate ratio of dietary carbohydrate to lipid was important to the growth and feed utilization of turbot. The proper CHO:LIP ratio based on the growth performance in the present study was determined to be 18:12 when the dietary protein level was 39%.
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Abdel-Tawwab, M., Ahmad, M. H., Khattab, Y. A., and Shalaby, A. M., 2010. Effect of dietary protein level, initial body weight, and their interaction on the growth, feed utilization, and physiological alterations of Nile tilapia, Oreochromis niloticus (L.). Aquaculture, 298: 267–274.
Ali, A., and AL-Asgan, N. A., 2001. Effect of feeding different carbohydrate to lipid ratios on the growth performance and body composition of Nile tilapia (Oreochromis niloticus) fingerlings. Animal Research, 50: 91–100.
Association of Official Analytical Chemists (AOAC), 1995. Official Methods of Analysis of Official Analytical Chemists International. 16th edition. Association of Official Analytical Chemists, Arlington, VA,16–26.
Azaza, M. S., Khiari, N., Dhraief, M. N., Aloui, N., Kraiem, M. M., and Elfeki, A., 2015. Growth performance, oxidative stress indices and hepatic carbohydrate metabolic enzymes activities of juvenile Nile tilapia, Oreochromis niloticus L., in response to dietary starch to protein ratios. Aquaculture Research, 1: 14–27.
Bell, J. G., Strachan, F., Good, J. E., and Tocher, D. R., 2006. Effect of dietary echiumoil on growth, fatty acid composition and metabolism, gill prostaglandin production and macrophage activity in Atlantic cod (Gadus morhua L.). Aquaculture Research, 37: 606–617.
Borba, M. R., Fracalossi, D. M., and Pezzato, L. E., 2006. Dietary energy requirement of piracanjuba fingerlings, Brycon orbignyanus, and relative utilization of dietary carbohydrate and lipid. Aquaculture Nutrition, 12: 183–191.
Cowey, C. B., and Walton, M. J., 1989. Intermediary metabolism. In: Fish Nutrition. Halver, J. E., ed., San Diego, Academic Press, CA,260–321.
Ellis, A. E., 1981. Stress and the modulation of defence mechanisms in fish. In: Stress in Fish. Pickering, A. D., ed., Academic Press, London, New York, 147–169.
Enes, P., Panserat, S., Kaushik, S., and Oliva-Teles, A., 2006. Rapid metabolic adaptation in European sea bass (Dicentrarchus labrax) juveniles fed different carbohydrate sources after heat shock stress. Comparative Biochemistry and Physiology Part A, 145: 73–81.
Erfanullah, A. K., and Jafri, K., 1995. Protein sparing effect of dietary carbohydrate in diets for fingerlings Labeo rohita. Aquaculture, 136: 331–339.
Erfanullah, A. K., and Jafri, K., 1998. Effect of dietary carbohydrate-to-lipid ratio on growth and body composition of walking catfish (Clarias batrachus). Aquaculture, 161: 159–168.
FAO, 2014. Cultured aquatic species information programme Psetta maxima (Linnaeus, 1758). http://www.fao.org/fishery/culturedspecies/Psetta_maxima/en.
Garcia-riera, M. P., and Hemre, G. I., 1996. Glucose tolerance in turbot, Scophthalmus maximus (L). Aquaculture Nutrition, 2: 117–120.
Giovanni, V. M., Rodrigo, Y. C., Gilberto, M., and Debora, M. F., 2010. Dietary non-protein energy sources: Growth, digestive enzyme activities and nutrient utilization by the catfish jundiá, Rhamdia quelen. Aquaculture Research, 41: 394–400.
Hamre, K., Øfsti, A., Næss, T., Nortvedt, R., and Holm, J. C., 2003. Macronutrient composition of formulated diets for Atlantic halibut (Hippoglossus hippoglossus L.) juveniles. Aquaculture, 227: 233–244.
Hatlen, B., Grisdale-Helland, B., and Helland, S. J., 2005. Growth, feed utilization and body composition in two size groups of Atlantic halibut (Hippoglossus hippoglossus) fed diets differing in protein and carbohydrate content. Aquaculture, 249: 401–408.
Hedge, J. E., and Hofreiter, B. T., 1962. In: Carbohydrate Chemistry, Volume 17. Whistler, R. L., and BeMiller, J. N., eds., Academic Press, New York, 17–22.
Hemre, G. I., Lie, Ø., and Sundby, A., 1993. Dietary carbohydrate utilization in cod (Gadus morhua): Metabolic responses to feeding and fasting. Fish Physiology and Biochemistry, 10: 455–463.
Hemre, G. I., Mommsen, T. P., and Krogdahl, A., 2002. Carbohydrates in fish nutrition: Effects on growth, glucose metabolism and hepatic enzymes. Aquaculture Nutrition, 8: 175–194.
Hemre, G. I., Sandnes, K., Lie, Ø., and Waagbø, R., 1995. Blood chemistry and organ nutrient composition in Atlantic salmon, Salmo salar L., fed graded amounts of wheat starch. Aquaculture Nutrition, 1: 37–42.
Hutchins, C. G., Rawles, S. D., and Gatlin, D. M., 1998. Effects of dietary carbohydrate kind and level on growth, body composition and glycemic response of juvenile sunshine bass (Morone chrysops female × M. saxatilis male). Aquaculture, 161: 187–199.
Lee, J. K., Cho, S. H., Park, S. U., Kim, K.-D., and Lee, S.-M., 2003a. Dietary protein requirement for young turbot (Scophthalmus maximus L.). Aquaculture Nutrition, 9: 283–286.
Lee, S. M., Kim, K. D., and Lall, S. P., 2003b. Utilization of glucose, maltose, dextrin and cellulose by juvenile flounder (Paralichthys olivaceus). Aquaculture, 221: 427–438.
Liu, X. H., Ye, C. X., Ye, J. D., Shen, B. D., Wang, C. Y., and Wang, A. L., 2014. Effects of dietary amylose/amylopectin ratio on growth performance, feed utilization, digestive enzymes, and postprandial metabolic responses in juvenile obscure puffer Takifugu obscurus. Fish Physiology Biochemistry, 40: 1423–1436.
Maule, A. G., Tripp, R. A., Kaattari, S. L., and Schreck, C. B., 1989. Stress alters the immune function and disease resistance in Chinook salmon (Oncorhunchus tshawytscha). The Journal of Endocrinology, 120: 135–142.
Miao, S. Y., Miao, H. J., Nie, Q., Zhang, W. B., and Mai, K. S., 2013. Effects of different dietary carbohydrates on growth performance and metabolism response of juvenile turbot (Scophthalmus maximus). Journal of Fisheries of China, 37 (6): 910–919.
Ming, J., Xie, J., Xu, P., Ge, X., Liu, W., and Ye, J., 2012. Effects of emodin and vitamin C on growth performance, biochemical parameters and twoHSP70smRNAexpression of Wuchang bream (Megalobrama amblycephalaYih) under high temperature stress. Fish & Shellfish Immunology, 32: 651–661.
Mohanta, K. N., Mohanty, A. N., and Jena, J. K., 2007. Protein-sparing effect of carbohydrate in silver barb Puntius gonionotus fry. Aquaculture Nutrition, 13: 311–317.
Montero, D., Mathlouthi, F., Tort, L., Afonso, J. M., Torrecillas, S., Fernández-Vaquero, A., Negrin, D., and Izquierdo, M. S., 2010. Replacement of dietary fish oil by vegetable oils affects humoral immunity and expression of pro-inflammatory cytokines genes in gilthead sea bream Sparus aurata. Fish & Shellfish Immunology, 29 (6): 1073–1081.
Moon, T. W., 2001. Glucose tolerance in fish: Fact or fiction? Comparative Biochemistry and Physiology Part B, 129: 243–244.
Moreira, I. S., Peres, H., Couto, A., Enes, P., and Oliva-Teles, A., 2008. Temperature and dietarycarbohydrate level effects on performance and metabolic utilization of diets in European sea bass (Dicentrarchus labrax) juveniles. Aquaculture, 274: 153–160.
Nanton, D. A., Lall, S. P., and McNiven, M. A., 2001. Effects of dietary lipid level on liver and muscle lipid deposition in juvenile haddock, Melanogrammus aeglefinus. Aquaculture Research, 32 (Supplement s1): 225–234.
Nijhof, M., and Bult, T. P., 1994. Metabolizable energy from dietary carbohydrates in turbot, Scophthalmus maximus (C.). Aquaculture Research, 25: 319–327.
Peng, M., 2013. The effects of dietary lipid level and fatty acids composition on lipid deposition in juvenile turbot (Scophthalmus maximus L.). PhD thesis. Ocean University of China, Qingdao.
Pieper, A., and Pfeffer, E., 1980. Studies on the comparative efficiency of utilization of gross energy from some carbohydrates, proteins and fats by rainbow trout (Salmo gairdneri R.). Aquaculture, 20: 323–332.
Plummer, P., 1987. Glycogen Determination in Animal Tissues. An Introduction to Practical Biochemistry. 3rd edition. McGraw Hill Book, Maidenhead, 332pp.
Polakof, S., Panserat, S., Soengas, J. L., and Moon, T. W., 2012. Glucose metabolism in fish: A review. Comparative Biochemistry and Physiology Part B, 182: 1015–1045.
Regost, C., Arzel, J., Cardinal, M., Robin, J., Laroche, M., and Kaushik, S. J., 2001. Dietary lipid level, hepatic lipogenesis and flesh quality in turbot (Psetta maxima). Aquaculture, 193 (3-4): 291–309.
Rubio, V. C., Boluda Navarro, D., Madrid, J. A., and Sánchez-Vázquez, F. J., 2009. Macronutrient self-selection in Solea senegalensis fed macronutrient diets and challenged with dietary protein dilutions. Aquaculture, 291: 95–100.
Rueda-Jasso, R., Conceicão, L. E. C., Dias, J., De Coen, W., Gomes, E., Rees, J. F., Soares, F., Dinis, M. T., and Sorgeloos, P., 2004. Effect of dietary non-protein energy levels on condition and oxidative status of Senegalese sole (Solea senegalensis) juveniles. Aquaculture, 231 (1-4): 417–433.
Russell, P., Davies, S., Gouveia, A., and Tekinay, A., 2001. Influence of dietary starch source on liver morphology in juvenile cultured European sea bass (Dicentrarchus labrax L.). Aquaculture Research, 32: 306–314.
Shiau, S. Y., and Peng, C. Y., 1993. Protein-sparing effect by carbohydrates in diets for tilapia Oreochromis niloticus ×O. aureus. Aquaculture, 117: 327–334.
Suárez, M. D., Sanz, A., Bazoco, J., and García-Gallego, M., 2002. Metabolic effects of changes in the dietary protein: Carbohydrate ratio in eel (Angilla anguilla) and trout (Oncorhynchus mykiss). Aquaculture International, 10: 1–14.
Tan, Q., Wang, F., Xie, S., Zhu, X., Lei, W., and Shen, J., 2009. Effect of high dietary starch levels on the growth performance, blood chemistry and body composition of gibel carp (Carassius auratus var. gibelio). Aquaculture Research, 40: 1011–1018.
Webb, L. T., and Holt, G. J., 2010. Effects of dietary starches and the protein to energy ratio to growth and feed efficiency of juvenile cobia, Rachycentron canadum. Aquaculture Nutrition, 16: 447–456.
Wiik, R., Andersen, K., Ulgenes, I., and Egidius, E., 1989. Cortisolinduced increase in susceptibility of Atlantic salmon, Salmo salar, together with effects on the blood cell pattern. Aquaculture, 83: 201–215.
Wilson, R. P., 1994. Utilization of dietary carbohydrate by fish. Aquaculture, 124: 67–80.
Young, A., Morris, P. C., Huntingford, F. A., and Sinnott, R., 2006. Replacing fish oil with pre-extruded carbohydrate in diets for Atlantic salmon, Salmo salar, during their entire marine grow-out phase: Effects on growth, composition and colour. Aquaculture, 253: 531–546.
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Miao, S., Nie, Q., Miao, H. et al. Effects of dietary carbohydrate-to-lipid ratio on the growth performance and feed utilization of juvenile turbot (Scophthalmus maximus). J. Ocean Univ. China 15, 660–666 (2016). https://doi.org/10.1007/s11802-016-2934-8
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DOI: https://doi.org/10.1007/s11802-016-2934-8