Adequately Defining the Amino Acid Requirements of Fish: The Case Example of Lysine
Abstract
A critical review of the literature highlights significant discrepancies in the estimates and modes of expression of
amino acid requirements. Using lysine as a case example, this paper highlights some of these discrepancies and
potential limitations of current approaches.
Published estimates of lysine requirements for rainbow trout varied from 1.3 – 2.9 % of the diet and NRC (1993)
estimated lysine requirement at 1.8% of the diet. Results from recent studies and detailed data analysis suggest that
lysine requirement to maximize weight gain is about 2.3% of the diet in rainbow trout, where requirement to
maximize protein gain of this species appears to be closer to 2.7% of the diet. These estimates are significantly
higher and appear more appropriate (robust) than the lysine requirement proposed by NRC (1993).
Different modes of expression of lysine requirement are used, often interchangeably, in the literature. It is important
to understand that these different modes of expression are based on different assumptions and that the use of
different modes of expression will result in dramatically different recommendations, especially since aquaculture
feeds are formulated to widely different nutritional specifications (protein, energy, etc.). Studies suggest that
expressing lysine requirement as a function of digestible energy or protein contents of the diet is not appropriate.
Studies have also indicated that “newer” approaches of estimating amino acid requirements (e.g., factorial amino
acid requirement, ideal protein concept), widely used in poultry and swine nutrition, may have significant pitfalls
when used in fish nutrition.
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References
Abboudi, T., Rollin, X., Larondelle, Y., 2002. Lysine and nitrogen requirement for maintenance and protein
accretion of Atlantic salmon (Salmo salar) fry. In: 10th International Symposium on Nutrition & Feeding in
Fish. 2-7 June, Rhodes Greece. (Abst.).
Adeola, O., 1995. Dietary lysine and threonine utilization by young pigs: Efficiency for carcass growth. Can. J.
Anim. Sci. 75, 445-452.
Aragão, C., Conceição, L.E.C., Martins, D., Ronnestad, I., Gomes, E., Dinis, M.T., 2004. A Balanced dietary amino
acid profile improves amino acid retention in post-larval Senegalese sole (Solea senegalensis).
Aquaculture. 233, 293-304.
Baker, D. H., 1991. Partitioning nutrients for growth and other metabolic functions: efficiency and priority
considerations. Poult. Sci. 70, 1797-1805.
Baker, D. H., Fernandez, S.R., Parsons, Edwards III, H.M., Emmert, J.L., Webel, D.M., 1996. Maintenance
requirements for valine and efficiency of its use above maintenance for accretion of whole body valine and
protein in young chicks. J. Nutr. 126, 1844-1851.
Batterham, E. S., 1984. Utilization of free lysine by pigs. Pig News. Info 5, 85-86.
Batterham, E. S., 1992. Availability and utilization of amino acids for growing pigs. J. Nutr. Res. Rev 5, 1-18.
Batterham, E. S., Murison, R. D., 1981. Utilization of free lysine by growing pigs. Br. J. Nutr. 46, 87-92.
Boujard, T. & Medale, F., 1994. Regulation of voluntary feed intake in juvenile rainbow trout fed by hand or by
self-feeders with diets containing two different protein/energy ratios. Aquatic Living Resources. &, 211-
Boorman, K.N. and Ellis. 1996. Maximum nutritional response to poor-quality protein and amino acid utilization.
Br. Poult. Sci. 37, 145-156.
Brown, P.B., 1995. Using whole body amino acid patterns and quantitative requirements to rapidly develop diets for
new species such as striped bass (Morone saxatilis). J. Appl. Ichtyol. 11, 342-246.
Bureau, D.P. and Cho, C.Y. 2000. Complementarity of corn gluten meal and soybean meal as protein sources in the
diet of young Atlantic salmon, Salmo salar. IX International Symposium on Nutrition and Feeding of Fish,
-25 May 2000, Miyazaki, Japan.
Chen, H. Y., Leu, Y. T., Roclants, I., 1992. Effective supplementation of arginine in the diets of juvenile marine
shrimp. Penaeus monodon. Aquaculture 108, 87-95.
Cheng, Z.J., Hardy, R.W., Usry, J.L., 2003. Plant protein ingredients with lysine supplementation reduce dietary
protein level in rainbow trout (Oncorhynchus mykiss) diets, and reduce ammonia nitrogen and soluble
phosphorus excretion. Aquaculture. 218, 553-565.
Cowey, C.B., 1994. Amino acid requirements of fish: a critical appraisal of present values. Aquaculture. 124, 1-11.
Cowey, C. B., Walton, M. J., 1988. Studies on the uptake of 14C-amino acids derived from both dietary 14C-protein
and dietary 14C-amino acids by rainbow trout. J. Fish. Biol 33, 293–305.
Cowey, C.B. and Walton, M. J., 1989. Intermediary catabolism. In: Fish Nutrition (Halver, J. E., Ed). 2nd Ed.
Academic Press, San Diego, CA. pp 259-329.
Cowey, C.B. & Cho, C.Y., 1993. Nutritional requirements of fish. Proceedings of the Nutrition Society. 52:417-426.
Conceição, L.E.C., Grasdalen, H., Rønnestad, I. (2003) Amino acid requirements of fish larvae and post-larvae: new
tools and recent findings. Aquaculture 227, 221-232.
Davis, S.J. and Morris, P.C., 1997. Influence of multiple amino acid supplementation on the performance of rainbow
trout, Oncorhynchus mykiss (Walbaum), fed soya based diets. Aquaculture Research. 28, 65-74.
D’Mello, 1994. Amino acid imbalances, antagonisms and toxicities. In: Amino acids in farm animal nutrition. J.P.F.
D’Mello (Ed). CAB International. Wallingford. UK. pp. 63-97.
Edwards, H.M., III, Fernandez, S.R., Baker, D.H., 1999. Maintenance lysine requirements and efficiency of using
lysine for accretion of whole-body lysine and protein in young chicks. Poult. Sci. 78, 1412-1417.
Elharoun E.R. and D.P. Bureau. 2006. Effect of increasing digestible energy of feeds by increasing digestible
protein using protein sources with different amino acid profiles on growth and feed efficiency of rainbow
trout (Oncorhynchus mykiss). XII International Symposium on Fish Nutrition & Feeding May 28th – June
st 2006, Biarritz, France.
Elharoun, E.R. and D.P. Bureau 2004. Assessing bioavailability of lysine in different blood meals using a slope-ratio
assay with rainbow trout. Aquaculture Association of Canada Annual Meeting, 16-20 October 2004,
Quebec, Canada.
Encarnação P. 2005. Effect of Diet Composition on Lysine Requirement and Utilization in Rainbow trout
(Oncorhynchus mykiss).PhD Thesis, University of Guelph, Ontario, Canada.
Encarnação P., Bureau D.P., 2001 Amino acid requirements: A matter of controversy. International Aqua Feed. 1,
-24.
Encarnação, P., deLange, C. Rodehutscord, M., Hoehler, D., Bureau, W., Bureau, D.P. 2004. Diet digestible energy
content affects lysine utilization, but not dietary lysine requirements of rainbow trout (Oncorhynchus
mykiss) for maximum growth. Aquaculture 235, 569-586.
Encarnação, P., C.F.M. de Lange, and D. P. Bureau. 2006. Diet energy source affect lysine utilization for protein
deposition in rainbow trout (Oncorhynchus mykiss). Aquaculture (in press).
Espe, M., Lied, E., Torrissen, K.R., 1993. Changes in plasma and muscle free amino acids in Atlantic salmon
(Salmo salar) during absorption of diets containing different amounts of hydrolysed cod muscle protein.
Comp. Biochem. Physiol., 105(A), 555-562.
Espe, M. & Lied, E., 1994. Do Atlantic salmon (Salmo salar) utilize mixtures of free amino acids to the same extent
as intact protein sources for muscle protein synthesis? Comp. Biochem. Physiol. 107A:249-254.
Fox, J. M., Lawrence, A. L., Li-Chan, E., 1995. Dietary requirement for lysine by juvenile Penaeus vannamei using
intact and free amino acid sources. Aquaculture 131, 279-290.
Fuller, M. F., 1994. Amino acid requirements for maintenance, body protein accretion and reproduction in pigs. In
Amino acids in farm animal nutrition. Ed. J.P.F. D’Mello. CAB International.Edinburgh.UK. 418 pp.
Fuller, M. F., McWilliam, R., Wang, T.C., Giles, L.R., 1989. The optimum dietary amino acid pattern fro growing
pigs 2. Requirements for maintenance and tissue protein accretion. Brit. J. Nutr. 62, 255-267.
Fuller, M.F., Garthwaite, P., 1993. The form of response of body protein accretion to dietary amino acid supply. J.
Nutr. 123, 957-963.
Gahl, M.J., Finke, M.D, Crenshaw, T.D., Benavenga, N.J., 1991. Use of four-parameter logistic equation to evaluate
the response of growing rats to ten levels of each indispensable amino acid. J. Nutr. 121, 1720-1729.
Gahl, M.J., Finke, M.D, Crenshaw, T.D., Benavenga, N.J., 1995. Diminishing returns in weight, nitrogen, and lysine
gain of pigs fed six levels of lysine from three supplemental sources. J. Anim. Sci. 73, 3177-3187.
Gahl, M.J., Finke, M.D, Crenshaw, T.D., Benavenga, N.J., 1997. Efficiency of lysine or threonine retention in
growing rats fed diets limiting in either lysine or threonine. J. Nutr. 126, 3090-3099.
Green, J.A., Hardy, R.W., 2002a. The optimum dietary essential amino acid pattern for rainbow trout
(Oncorhynchus mykiss), to maximize nitrogen retention and minimize nitrogen excretion. Fish Physiology
and Biochemistry. 27, 97-108.
Green, J.A., Hardy, R.W., Brannon, E.L., 2002b. The optimum dietary essential: nonessential amino acid ratio for
rainbow trout (Oncorhynchus mykiss), which maximizes nitrogen retention and minimizes nitrogen
excretion. Fish Physiology and Biochemistry. 27, 109-115.
Harper, A., Leung, E., Yoshida, P., Rogers, Q.R., 1964. Some new thoughts on amino acid balance. Fed. Proc., 23,
-1096.
Hauler, R., Carter, C., 2001a. Reevaluation of the quantitative dietary lysine requirement of fish. Rev. Fish. Sci.
,133-163.
Hauler, R., Carter, C., 2001b. Lysine deposition responds linearly to marginal lysine intake in Atlantic salmon
(Salmo salar L) parr. Aquacult. Res.. 32 (suppl. 1),147-156.
Jobling, M. & Wandsvik, A., 1983. An investigation of factors contributing to the control of food intake in Artic
charr, Salvelinus alpinus? J. Fish Biol. 43, 487-489.
Kaushik, S. J., Dabrowski, K., 1983. Nitrogen and energy utilization in juvenile carp fed casein, amino acids or a
protein-free diet. Reprod. Nutr. Dev 23, 741–754.
Kaushik, S.J. & Luquet, P., 1979. Influence of dietary amino acid patterns on the free amino acid contents of blood
and muscle of rainbow trout Salmo gairdneri. Comp. Biochem. Physiol. 64B, 175-180.
Kaushik, S.J. & Medale, F., 1994. Energy requirements, utilization and dietary supply to salmonids. Aquaculture
, 81-97.
Ketola, H.G., 1982. Amino acid nutrition of fishes: Requirements and supplementation of diets. Comp. Biochem.
Physiol. 73(B), 1-17.
Ketola, H.G., 1983. Requirements for dietary lysine and arginine by fry of rainbow trout. J. Anim. Sci. 56, 101-107.
Kim, K., 1997. Re-evaluation of protein and amino acid requirements of rainbow trout (Oncorhynchus mykiss).
Aquaculture 151, 3-7.
Kim, K.I., Kayes, T.B., 1982. Test diet development and lysine requirement of rainbow trout. Fed. Proc. Fed. Am.
Soc. Exp Biol. 42:677
Kim, K.I., Kayes, T.B., Amundson, C.H., 1987. Effects of dietary tryptophan levels on growth, feed/gain, carcass
composition and liver glutamate dehydrogenase activity in rainbow trout (Salmo gairdneri). Comp.
Biochem. Physiol. 88B, 737-741.
Kim, K.I., Kayes, T.B., Amundson, C.H., 1991. Purified diet development and re-evaluation of the dietary protein
requirement of fingerling rainbow trout (Oncorhynchus mykiss). Aquaculture. 96, 57-67.
Kim, K.I., Kayes, T.B., Amundson, C.H., 1992a. Requirements for lysine and arginine by rainbow trout
(Oncorhynchus mykiss). Aquaculture 106,333-344.
Lobley, G.E., Lapierre, H., 2003. Post-absorptive metabolism of amino acids. Progress in research on energy and
protein metabolism. International Symposium, Rostock-Warnemünde, Germany, 13-18 September, pp.
-756.
Mambrini, M., Kaushik, S.J., 1994. Partial replacement of dietary protein nitrogen with dispensable amino acids in
diets of Nile tilapia, Oreochromis niloticus. Comp. Biochem. Physiol. 109A, 469-477.
Mambrini, M., Kaushik, S.J., 1995. Indispensable amino acid requirements of fish: correspondence between
quantitative data and amino acid profiles of tissue proteins. J. Appl. Ichthyol. 11, 240-247.
Mambrini, M. and Guillaume, J., 1999. Nutrition protéique. In: Guillaume, J., Kaushik, S.J., Bergot, P. & Métailler,
R. (Eds) Nutrition et alimentation des poissons et des crustacés. Collections Du Labo au Terrain. Éditions
INRA, Paris, France.
Mercer, L.P., May, H.E. Dodds, S.J., 1989. The determination of nutritional requirements in rats: mathematical
modeling of sigmoidal, inhibited nutrient-response curves. J. Nutr. 119, 1465-1471.
Moehn, S., Ball, R.O., Fuller, M.F., Gillis, A.M., de Lange, C.F.M., 2004. Growth potential, but not body weight or
moderate limitation of lysine intake, affects inevitable lysine catabolism in growing pigs. J. Nutr. 134,
-2292.
Mohn, S. and de Lange, C.F.M., 1998. The effect of body weight on the upper limit to protein deposition in a
defined population of growing gilts. J. Anim. Sci. 76, 124-133.
Mohn, S., Gillis, A.M., Moughan, P.J., de Lange, C.F.M., 2000. Influence of dietary lysine and energy intakes on
body protein deposition and lysine utilization in the growing pig. J. Anim. Sci., 78:1510-1519.
Morris, T.R. Gous, R.M., Fisher, C., 1999. An analysis of the hypothesis that amino acid requirements for chicks
should be stated as a proportion of dietary protein. World’s Poultry Sci. J. 55, 7-22.
Moughan, P.J., 1989. Simulation of the daily partitioning of lysine in the 50 kg live-weight pig – A factorial
approach to estimating amino acid requirements for growth and maintenance. Research and Development
in Agriculture. 6, 7-14.
Murai, T., Ogata, H., Hirasawa, Y., Akiyama, T. and Nose, T., 1987. Portal absorption and hepatic uptake of amino
acids in rainbow trout force fed complete diets containing casein or crystalline amino acids. Nippon Suisan
Gakkaishi, 53: 1847-1859.
Nose, T., 1973. Changes in pattern of free plasma amino acid in rainbow trout after feeding. Bull. Freshwater fish.
Res. Rab. 22(2):137-144.
National Research Council (NRC), 1993. Nutrient requirements of fish. National Academy Press. Washington, DC.
Oldham, J.D., Emmans, G.C., Kyriazakis, I., 1997. Symposium on ‘Regulation of nitrogen retention in farm
animals’ Limits and limitations to nitrogen use in farm animals. Proc. Nutr. Soc. 56,525-534.
Pfeffer, E., Al-Sabty, H., Heverkanp, R., 1992. Studies on lysine requirements of rainbow trout (Oncorhynchus
mykiss) fed wheat gluten as only source of dietary protein. J. Anim. Physiol. A. Anim. Nutr. 67,74-82.
Rezaei, M. , Nassiri, Moghaddam, N.H., Reza, J.P. and Kermanshahi, H. 2004. The effects of dietary protein and
lysine levels on broiler performance, carcass characteristics and N excretion. International Journal of
Poultry Science 3, 148-152
Robbins, K.R., Norton, H.W., Baker, D.H., 1979. A flexible growth function for empirical use. J. Expt. Bot. 10,
-300.
Robinson, E.H., Poe, W.E., Wilson, R.P., 1984. Effects of feeding diets containing an imbalance of branched-chain
amino acids on fingerling channel catfish. Aquaculture. 37, 51-62.
Rodehutscord, M., Jacobs, S., Pack, M., Pfeffer, E., 1995a. Response of rainbow trout (Oncorhynchus mykiss)
growing from 50 to 150 g to supplements of DL-methionine in a semipurified diet containing low or high
levels of cysteine. J. Nutr. 125, 964-969.
Rodehutscord, M., M. Pack, S. Jacobs and E. Pfeffer. 1995b. Free amino acids can replace protein-bound amino
acids in test diets for studies in Rainbow trout (Oncorhynchus mykiss). J. Nutr.125: 956-963.
Rodehutscord, M., Becker, A., Pack, M. and Pfeffer, E., 1997. Response of rainbow trout (Oncorhynchus mykiss) to
supplements of individual essential amino acids in a semipurified diet, including an estimate of the
maintenance requirement for essential amino acids. J. Nutr. 127, 1166-1175.
Rodehutscord, M. & Pack, M., 1999. Estimates of essential amino acid requirements from dose-response studies
with rainbow trout and broiler chicken: effect of mathematical model. Arch. Anim. Nutr. 52, 223-244.
Rodehutscord, M., Borchert, F., Gregus, Z., Pack, M., Pfeffer, E., 2000. Availability and utilization of free lysine in
rainbow trout (Oncorhynchus mykiss) 1. Effect of dietary crude protein level. Aquaculture. 187,163-176.
Rollin, X., Mambrini, M., Abboudi, Larondelle, Y. , Kaushik, S. J., 2003. The optimum dietary indispensable
amino acid pattern for growing Atlantic salmon (Salmo salar L.) fry. Brit. J. Nutr. 90 (5), 865-876.
Rolls, B. A., Porter, J. W. G., Westgarth, D. R., 1972. The course of digestion of different feed proteins in the rats:
the absorption of proteins given alone and with supplements of their limiting amino acids. Br. J. Anim.
Nutr 28, 283-293.
Schumacher, A., Wax, C., Gropp, J. M., 1997. Plasma amino acids in rainbow trout fed intact protein or crystalline
amino acids. Aquaculture 151, 15-28.
Segovia-Quintero, M.S., Reigh, R.C., 2004. Coating crystalline methionine with tripalmitin-polyvinyl alcohol slows
its absorption in the intestine of Nile tilapia, Oreochromis niloticus Aquaculture. 238, 355-367
Schinckel, A.P., deLange, C.F.M., 1996. Characterization of growth parameters needed as inputs for pig growth
models. J. Anim. Sci. 74, 2021-2036.
Shuhmacher, A., Goldberg, M., Schon, J., Wax, C., Groop, J.M., 1993. Plasma amino acid levels in rainbow trout
(O. Mykiss). EIFAC Workshop on Methodology for Determination of Nutrient Requirements in Fish. 29,
June-1 July. Eichenau, Germany.
Shuhmacher, A., Wax, C., Groop, J.M., 1997. Plasma amino acids in rainbow trout (Oncorhynchus mykiss) fed
intact protein or crystalline amino acid diet. Aquaculture. 151, 15-28.
Susenbeth, A., 1995. Factors affecting lysine utilization in growing pigs: an analysis of literature data. Livestock
Prod. Sci. 43,193-204.
Susenbeth, A., Dickel, T., Diekenhorst, A., Hohler, D., 1999. The effect of energy intake, genotype, and body
weight on protein retention in pigs when dietary lysine is the first-limiting factor. J. Anim. Sci. 77,2985-
Tacon, A.G.J., 1995. Application of nutrient requirement data under practical conditions: special problems of
intensive and semi-intensive fish farming systems. J. Appl. Ichthyol. 11:205-214.
Tacon, A.G.J. & Cowey, C.B., 1985. Protein and amino acid requirements. In: Fish Energetics New Perspectives.
Tytler, P. & Calow, P. (Eds.). The Johns Hoptkins University Press, Baltimore, MD. Pp. 155-183.
Tantikitti, C., March, B. E., 1995. Dynamics of plasma free amino acids in rainbow trout (Oncorhynchus mykiss)
under variety of dietary conditions. Fish Physiology and Biochemistry 14, 179-194.
Teshima, S., Kanazawa, A., Koshio, S., 1990. Effects of methionine enriched plastein supplemented to soybeanprotein
based diets on common carp and tilapia. In: The Second Asian Fisheries Forum (Hirano, R. and
Hanyu, I. eds), pp. 279-282. Asian Fisheries Society Manila, Philippines.
Teshima, S., Kanazawa, A., Koshio, S., 1992. Supplemental effects of methionine-enriched plastein in penaus
japonicus diets. Aquaculture 101, 85-93.
Tibaldi E., Kaushik S.J., 2002. Amino acid requirements of Mediterranean fish species. Workshop on Mediterrarean
Fish Nutrition. Rhodes (Grece). 1-2 June. pp. 8-10.
Walton, M.J., Cowey, C.B., Adron, J.W., 1984. The effect of dietary lysine levels on growth and metabolism of
rainbow trout. Br. J. Nutr. 52, 115-122.
Walton, M.J., Wilson. R.W., 1986. Postprandial changes in plasma and liver free amino acids of rainbow trout fed
complete diets containing casein. Aquaculture. 51:105-115.
Wang, T.C., Fuller, M.F., 1989. The optimum dietary amino acid pattern for growing pigs 1. Experiments by amino
acid deletion. Brit. J. Nutr. 62, 77-89.
Webb, K.A. and Gatlin III, D.M., 2002. Nutrition of red drum Sciaenops ocellatus: effects of dietary protein on
requirement estimates and ammonia excretion. In: 10th International Symposium on Nutrition & Feeding in
Fish. 2-7 June, Rhodes Greece. (Abst.).
Williams, K., Barlow, C., Rodgers, L., 2001. Efficacy of crystalline and protein-bound amino acids for amino acid
enrichment of diets for barramundi/Asian seabass (Lates calcarifer Bloch). Aquaculture Research. 32, 415-
Wilson, R.P., 1985. Amino Acid and Protein requirement of fish. In C.B. Cowey, A.M. Mackie, and J.G. Bell (Ed.)
Nutrition and Feeding in Fish, Academic Press, Orlando.Fl. p. 1-16.
Wilson, R.P., 1989. Protein and amino acid requirements of fishes. Progress in Fish Nutrition. Proceeding of the fish
nutrition symposium. Shi-Yen Shiau (ed.) Marine Food Science Series. no 9. pp. 51-77.
Wilson, R.P., 1993. Amino acid nutrition of fish: A new method aof estimating requirement values. Proceeding of
the 20th US-Japan Symposium on Aquaculture Nutrition. Newport, Oregon. 28-39 October 1991. Collie,
M.R. & McVey, J.P. (Eds.). pp. 49-54.
Wilson, R.P., 1994. Amino acids requirements of finfish. In: Amino acids in farm animal nutrition. J.P.F. D’Mello
(Ed.). CAB International. Wallingford. UK. 418 pp.
Wilson, R.P., 2002. Amino acid and Proteins. In: Fish nutrition. (Halver, J.E. and Hardy, R.W., Eds) 2rd Edition.
Academic Press. San Diego. CA. pp. 144-179.
Wilson, R.P., Harding, D.E., Garling, D.L., 1977. Effect of dietary pH on amino acid utilization and the lysine
requirement of fingerling channel catfish. J. Nutr. 107, 166-170.
Yamada, S., Tanaka, Y., Katayama, T., 1981a. Feeding experiments with carp fry fed an amino acid diet by
increasing the number of feedings per day. Bull. Jpn. Soc. Sci. Fish. 47 (9), p. 1247.
Yamada, S., Simpson, K., Tanaka, Y., Katayama, T., 1981b. Plasma amino acid changes in rainbow trout force-fed
casein and corresponding amino acid mixture. Bull. Jpn. Soc. Sci. Fish., 47:1035-1040.
Yamamoto, T., Unuma, T., Akiyama, T., 1998a. Postprandial changes in plasma free amino acid concentrations of
rainbow trout fed diets containing different protein sources. Fisheries Science. 64 (3): 474-481.
Yamamoto, T., Unuma, T., Akiyama, T., 2000a. The influence of dietary protein and fat levels on tissue free acid
levels of fingerling rainbow trout (Oncorhynchus mykiss). Aquaculture. 182:353-372.
Yamamoto, T., Shima, T., Furuita, H., Shiraishi, M., Sánchez-Vásques, F.J., Tabata, M., 2000b. Self-selection of
diets with different amino acid profiles by rainbow trout (Oncorhynchus mykiss). Aquaculture. 187, 375-
Yamamoto, T., Shima, T., Furuita, H., 2004. Antagonistic effects of branched-chain amino acids induced by excess
protein-bound leucine in diets for rainbow trout (Oncorhynchus mykiss). Aquaculture. 232, 539-550.
Yamamoto, T., Sugita, T., Furuita, H., 2005. Essential amino acid supplementation to fish meal-based diets with low
protein to energy ratios improves the protein utilization in juvenile rainbow trout Oncorhynchus mykiss.
Aquaculture. 246, 379-391
Zarate, D.D., Lovell, R.T., 1997. Free lysine (L-lysine HCl) is utilized for growth less efficiently than protein-bound
lysine (soybean meal) in practical diets by young channel catfish (Ictalurus punctatus).Aquaculture.
:87-100.
Zarate, D. D., Lovell, R. T., Payne, M., 1999. Effects of feeding frequency and rate of stomach evacuation on
utilization of dietary free and protein bound-lysine for growth by channel catfish. Aquac. Nutr. 5, 17-22.
