Abstract
A 120-day feeding experiment was conducted to investigate the effects of partial replacement of brown fish meal (BFM) by fermented soybean meal (FSBM) in diets of Chinese soft-shelled turtle (Pelodiscus sinensis). The turtles (initial mean body weight, (115.52 ± 1.05) g) were fed with three experimental diets, in which 0%, 4.72% and 9.44% BFM protein was replaced by 0%, 3% and 6% FSBM, respectively. Results showed that the feeding rate (FR), specific growth rate (SGR) and feed efficiency ratio (FER) of turtles fed with the diet containing 3% FSBM were not significantly different from the control group (0% FSBM) (P > 0.05). However, FR, SGR and FER of turtles fed with the diet containing 6% FSBM were significantly lower than those of the control group (P < 0.05). No significant differences were observed in the activities of serum glutamic-oxalacetic transaminase and glutamic-pyruvic transaminase among dietary treatments (P > 0.05). However, the uric acid concentration in turtles fed with the diet containing 3% or 6% FSBM was significantly lower than that in the control group (P < 0.05). There were no significant differences in the activities of lysozyme, alkaline phosphatase and total superoxide dismutase among dietary treatments (P > 0.05). The results suggested that FSBM could replace 4.72% BFM protein in turtle diets without exerting adverse effects on turtle growth, feed utilization and measured immune parameters.
Article PDF
Similar content being viewed by others
Avoid common mistakes on your manuscript.
References
Adler-Nissen, J., 1979. Determination of the degree of hydrolysis of food protein hydrolysates by trinitrobenzenesulfonic acid. Journal of Agricultural and Food Chemistry, 27: 1256–1262.
Ai, Q., Mai, K., Tan, B., Xu, W., Duan, Q., Ma, H., and Zhang, L., 2006. Replacement of fish meal by meat and bone meal in diets for large yellow croaker, Pseudosciaena crocea. Aquaculture, 260(1–4): 255–263.
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, USA.
Bergmeyer, H. U., Scheibe, P., and Wahlefeld, A. W., 1978. Optimization of methods for asparate aminotransferase and alanine aminotrans ferase. Clinical Chemistry, 24(1): 58–61.
Biagini, G., Sala, D., and Zini, I., 1995. Diethyldithiocarbamate, a superoxide dismutase inhibitor, counteracts the maturation of ischemic-like lesions caused by endothelin-1 intrastriatal injection. Neuroscience Letters, 190(3): 212–216.
Bradford, M. M., 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry, 72: 248–254.
Burrells, C., Williams, P. D., Southgate, P. J., and Crampton, V. O., 1999. Immunological, physiological and pathological responses of rainbow trout (Oncorhynchus mykiss) to increasing dietary concentration of soybean proteins. Veterinary Immunology and Immunopathology, 72(3–4): 277–288.
Chen, J. H., 2006. Effects of fermentation, exogenous enzyme and feeding stimulants on utilization of soybean meal protein by Japanese flounder (Paralichthys olivaceus). Doctoral degree paper of Ocean University of China, Qingdao, China, 19–106 (in Chinse with English abstract).
Choi, S. M., Wang, X., Park, G. J., Lim, S. R., Kim, K. W., Bai, S. C., and Shin, I. S., 2004. Dietary dehulled soybean meal as a replacement for fish meal in fingerling and growing olive flounder Paralichthys olivaceus (Temminck et Schlegel). Aquaculture Research, 35(4): 410–418.
Delente, J. and Ladenburg, K., 1972. Quantitative determination of the oligosaccharides in defatted soybean meal by gas-liquid chromatography. Journal of Food Science, 37(3): 372–374.
Egounlety, M. and Aworh, O. C., 2003. Effect of soaking, dehulling, cooking and fermentation with Rhizopus oligosporus on the oligosaccharides, trypsin inhibitor, phytic acid and tannins of soybean (Glycine max Merr.), cowpea (Vigna unguiculata L.Walp) and groundbean (Macrotyloma geocarpa Harms). Journal of Food Engineering, 56(2–3): 249–254.
Ellis, R. and Morris, E. R., 1983. Improved ion-exchange phytate method. Cereal Chemistry, 60: 121–124.
Feng, J., Liu, X., Xu, Z. R., Wang, Y. Z., and Liu, J. X., 2007. Effects of fermented soybean meal on digestive enzyme activities and intestinal morphology in broilers. Poultry Science, 86(6): 1149–1154.
Førde-Skjærvik, O., Refstie, S., Aslaksen, M. A., and Skrede, A., 2006. Digestibility of diets containing different soybean meals in Atlantic cod (Gadus morhua); comparison of collection methods and mapping of digestibility in different sections of the gastrointestinal tract. Aquaculture, 261(1): 251–258.
Francis, G., Makkar, H. P. S., and Becker, K., 2001. Antinutritional factors present in plant-derived alternate fish feed ingredients and their effects in fish. Aquaculture, 199(3–4), 197–227.
Frias, J., Song, Y. S., Martínez-Villaluenga, C., de Meja, E. G., and Vidal-Valverde, C., 2008. Immunoreactivity and amino acid content of fermented soybean products. Journal of Agricultural and Food Chemistry, 56(1): 99–105.
Gallagher, M. L., 1994. The use of soybean meal as a replacement for fish meal in diets for hybrid striped bass (Morone saxatillis × M. chrysops). Aquaculture, 126: 119–127.
Gardner, W. S. and Miller, W. H., 1980. Reverse-phase liquid chromatography of amino acids after reaction with Ophthalaadehde. Analytical Biochemistry, 101: 61–70.
Gurfinkel, D. M. and Rao, A. V., 2002. Determination of saponins in legumes by directs densitometry. Journal of Agricultural and Food Chemistry, 50(3): 426–430.
Hachmeister, K. A. and Fung, D. Y., 1993. Tempeh: A mold-modified indigenous fermented food made from soybeans and/or cereal grains. Critical Reviews in Microbiology, 19(3): 137–188.
Hajen, W. E., Beames, R. M., Higgs, D. A., and Dosanjh, B. S., 1993. Digestibility of various feedstuffs by post-juvenile chinook salmon (Oncorhynchus tshawytscha) in sea water. 1. Validation of technique. Aquaculture, 112(4): 321–332.
Henry, R. J., Sobel, C., and Kim, J., 1957. A modified carbonate-phosphotungstate method for the determination of uric acid and comparison with the spectrophotometric uricase method. American Journal of Clinical Pathology, 28(2): 152–160.
Hernández, M. D., Martínez, F. J., Jover, M., and García García, B., 2007. Effects of partial replacement of fish meal by soybean meal in sharpsnout seabream (Diplodus puntazzo) diet. Aquaculture, 263(1–4): 159–167.
Hong, K. J., Lee, C. H., and Kim, S. W., 2004. Aspergillus oryzae GB-107 fermentation improves nutritional quality of food soybeans and feed soybean meals. Journal of Medicinal Food, 7(4): 430–435.
Hotz, C. and Gibson, R. S., 2007. Traditional food-processing and preparation practices to enhance the bioavailability of micronutrients in plant-based diets. Journal of Nutrition, 137(4): 1097–1100.
Hou, X., Liang, G. Y., Yang, H. J., Liu, Y. J., and Tian, L. X., 2009. Replacement of fish meal by fermented soybean meal and crystal amino acid in diets for hybrid tilapia. South China Fisheries Science, 5(2): 28–33 (in Chinse with English abstract).
Huang, C. H. and Lin, W. Y., 2002. Estimation of optimal dietary methionine requirement for softshell turtle, Pelodiscus sinensis. Aquaculture, 207(3–4): 281–287.
Huang, C. H., Lin, W. Y., and Chu, J. H., 2005. Dietary lipid level influences fatty acid profiles, tissue composition, and lipid peroxidation of soft-shelled turtle, Pelodiscus sinensis. Comparative Biochemistry and Physiology, Part A: Molecular and Integrative Physiology, 2: 383–388.
Huang, C. H., Lin, W. Y., and Wu, S. M., 2003. Effect of dietary calcium and phosphorus supplementation in fish meal-based diets on the growth of soft-shelled turtle Pelodiscus sinensis (Wiegmann). Aquaculture research, 4(10): 843–848.
Hultmark, D., Steiner, H., Rasmuson, T., and Boman, H. G., 1980. Insect immunity. Purification and properties of three inducible bactericidal proteins from hemolymph of immunized pupae of Hyalophora cecropia. European Journal of Biochemistry, 106(1): 7–16.
Iwabuchi, S. and Yamauchi, F., 1987. Determination of glycinin and beta-conglycinin in soybean proteins by immunological methods. Journal of Agricultural and Food Chemistry, 35(2): 200–205.
Jia, Y., Yang, Z., Hao, Y., and Gao, Y., 2005. Effects of animal-plant protein ratio in extruded and expanded feed on nitrogen and energy budgets of juvenile Chinese soft-shelled turtle (Pelodiscus sinensis Wiegmann). Aquaculture research, 36(1): 61–68.
Kakade, M. L., Simons, N., and Liener, I. E., 1969. An evaluation of natural versus synthetic substrates for measuring the antitryptic activity of soybean samples. Cereal Chemistry, 46: 518–526.
Kiers, J. L., Meijer, J. C., Nout, M. J. R., Rombouts, F. M., Nabuurs, M. J. A., and van der Meulen, J., 2003. Effect of fermented soya beans on diarrhoea and feed efficiency in weaned piglets. Journal of Applied Microbiology, 95(3): 545–552.
King, J., 1965. The hydrolases-acid and alkaline phosphatases. In: Practical Clinical Enzymology. Van, D. ed., Nostrand Company Limited, London, UK, 191–208.
Leng, X. J., Wang, W. L., Zhou, H. Q., and Liu, H., 2006. The use of various soybean products as partial substitute for fish meal in Diets for Penaeus vannaei (Boone). Freshwater Fisheries, 36(3): 47–49 (in Chinse with English abstract).
Leng, X. J., Wang, W. L., and Li, X. Q., 2007. Experiment on feeding Penaeus Vannamei Boones with fermented soybean meal as partial substitute for fish meal. Cereal and Feed Industry, (3): 40–41 (in Chinse with English abstract).
Li, X. L., Zhang, C. L., Fang, W. H., and Lin, F. C., 2008. White-spot disease of Chinese soft-shelled turtles (Trionyx sinens) caused by Paecilomyces lilacinus. Journal of Zhejiang University, 9(7): 578–581.
Lin, S. and Luo, L., 2011. Effects of different levels of soybean meal inclusion in replacement for fish meal on growth, digestive enzymes and transaminase activities in practical diets for juvenile tilapia, Oreochromis niloticus × O. aureus. Animal Feed Science and Technology, 168(1–2): 80–87.
Lindsay, R. C., 1994. Flavour of fish. In: Seafoods: Chemistry, Processing Technology and Quality. Shahidi, F. and Botta, J. R. eds., Blackie Academic and Professional, London, UK, 75–84.
Liu, K., Zhu, L., Lin, Q., and Cao, H., 2010a. Effect of isomaltose hypgather and yeast cell wall on immune function of soft-shelled turtle (Trionyx sinensis). Chinese Agricultural Science Bulletin, 26(9): 386–390 (in Chinese with English abstract).
Liu, X. W., Wang, H. L., Zhang, H. T., Jiang, Y. J., and Zhao, L. M., 2010b. Effects of fish meal in diets replaced by soybean meal and fermented soybean meal on growth performance and feed intake in Pompano. China Feed, 18: 27–36 (in Chinse with English abstract).
Long, L. Q., Bai, D. Q., Tang, B. G., and Liang, Y. G., 1997. Distribution of three major digestive enzymes of digestive tissue of Trionyx sinensis. Chinese Journal of zoology, 32(6): 23–26 (in Chinse with English abstract).
Lowry, O. H., Rosenbrough, N. J., Farr, A. L., and Randall, R. J., 1951. Protein measurement with the Folin phenol reagent. Journal of Biological Chemistry, 193(1): 265–275.
Luo, Z., Liu, Y. J., Mai, K. S., Tian, L. X., Liu, D. H., and Tan, X. Y., 2004. Partial replacement of fish meal by soybean protein in diets for grouper Epinephelus coincides juveniles. Journal of Fisheries of China, 28(2): 175–181.
Mai, K., Wan, J., Ai, Q., Xu, W., Liufu, Z., Zhang, L., Zhang, C., and Li, H., 2006. Dietary methionine requirement of large yellow croaker, Pseudosciaena crocea R. Aquaculture, 253(1–4): 564–572.
Mambrini, M., Roem, A. J., Cravèdi, J. P., Lallès, J. P., and Kaushik, S. J., 1999. Effects of replacing fish meal with soy protein concentrate and of DL-methionine supplementation in high-energy, extruded diets on the growth and nutrient utilization of rainbow trout, Oncorhynchus mykiss. Journal of Animal Science, 77(11): 2990–2999.
Matsunari, H., Iwashita, Y., Suzuki, N., Saito, T., Akimoto, A., Okamatsu, K., Sugita, T., and Yamamoto, T., 2010. Influence of fermented soybean meal-based diet on the biliary bile status and intestinal morphology in rainbow trout Oncorhynchus mykiss. Aquaculture international, 58(2): 243–252.
Meunpol, O., Ruangpan, L., and Vallisut, S., 2009. Replacement of soybean meal protein in fish meal diet in organic marine shrimp feed. Asian Journal of Food and Agro-Industry, (Suppl): 175–181.
Nuangsaeng, B. and Boonyartapalin, M., 2001. Protein requirement of juvenile soft-shelled turtle Trionyx sinensis, Wiegmann. Aquaculture research, 32(S1): 106–111.
Pereira, O., Rosa, E., Pires, M. A., and Fontaínhas-Fernandes, A., 2002. Brassica by-products in diets of rainbow trout (Oncorhynchus mykiss) and their effects on performance, body composition, thyroid status and liver histology. Animal Feed Science and Technology, 101(1): 171–182.
Peres, H., Lim, C., and Klesius, P. H., 2003. Nutritional value of heat-treated soybean meal for channel catfish (Ictalurus punctatus). Aquaculture, 225(1–4): 67–82.
Qian, G. Y., 1995. Study on protein requirement of turtle and its digest-utilize. Journal of Zhejiang Agriculture University, 21(5): 547–550 (in Chinse with English abstract).
Refstie, S., Storebakken, T., and Roem, A. J., 1998. Feed consumption and conversion in Atlantic salmon (Salmo salar) fed diets with fish meal, extracted soybean meal or soybean meal with reduced content of oligosaccharides, trypsin inhibitors, lectins and soya antigens. Aquaculture, 162(3–4): 301–312.
Refstie, S., Sahlström, S., Bráthen, E., Baeverfjord, G., and Krogedal, P., 2005. Lactic acid fermentation eliminates indigestible carbohydrates and antinutritional factors in soybean meal for Atlantic salmon (Salmo salar). Aquaculture, 246(1–4): 331–345.
Refstie, S., Storebakken, T., Baeverfjord, G., and Roem, A. J., 2001. Long-term protein and lipid growth of Atlantic salmon (Salmo salar) fed diets with partial replacement of fish meal by soy protein products at medium or high lipid level. Aquaculture, 193(1–2): 91–106.
Reitman, S. and Frankel, S., 1957. A colorimetric method for determination of serum oxaloacetic and glutamic pyruvic transaminase. American Journal of Clinical Pathology, 28: 56–63.
Ren, Z. L., Zen, H., Guo, Q., Lu, J. J., Tian, J. S., Sun, X. J., Li, W. T., and Xie, X. T., 1997. Study on diets for soft-shelled turtle. Feed Industry, 18(5): 21–24 (in Chinese).
Riche, M., Trottier, N. L., Ku, P. K., and Garling, D. L., 2001. Apparent digestibility of crude protein and apparent availability of individual amino acids in tilapia (Oreochromis niloticus) fed phytase pretreated soybean meal diets. Fish Physiology and Biochemistry, 25(3): 181–194.
Song, Y. S., Frias, J., Martinez-Villaluenga, C., Vidal-Valverda, C., and Gonzalez de Mejia, E., 2008. Immunoreactivity reduction of soybean meal by fermentation, effect on amino acid composition and antigenicity of commercial soy products. Food Chemistry, 108(2): 571–581.
Song, Y. S., Pérez, V. G., Pettigrew, J. E., Martinez-Villaluenga, C., and Gonzalez de Mejia, E., 2010. Fermentation of soybean meal and its inclusion in diets for newly weaned pigs reduced diarrhea and measures of immunoreactivity in the plasma. Animal Feed Science and Technology, 159(1): 41–49.
Stellmach, B., 1992. Production. In: Bestimmungs methoden Enzyme. Qian, J. Y. ed., Chinese Light Industry Press, Bejing, China, 122–123 (in Chinese).
Tibaldi, E., Hakim, Y., Uni, Z., Tulli, F., de Defrancesco, M., Luzzana, U., and Harpaz, S., 2006. Effects of the partial substitution of dietary fish meal by differently processed soybean meals on growth performance, nutrient digestibility and activity of intestinal brush border enzymes in the European sea bass (Dicentrarchus labrax). Aquaculture, 261(1): 182–193.
Wang, L., Li, G. Y., Mao, Y. X., and Zhang, H. Y., 1994. Study of effect of immune medicine by oral on the prevention and cure of disease in culture Penaeus chinensis. Oceanology Limnology Sinica, 25: 486–491 (in Chinese with English abstract).
Worthington, V., 1993. Worthington Enzyme Manual: Enzymes and Related Biochemicals. Worthington Biochemical Corporation, New Jersey, USA, 399pp.
Yamamoto, T., Iwashita, Y., Matsunari, H., Sugita, T., Furuita, H., Akimoto, A., Okamatsu, K., and Suzuki, N., 2010. Influence of fermentation conditions for soybean meal in a non-fish meal diet on the growth performance and physiological condition of rainbow trout Oncorhynchus mykiss. Aquaculture, 309(1–4): 173–180.
Yin, J., Tezuka, Y., Subehan, S. L., Shi, L., Ueda, J. Y., Matsushige, K., and Kadota, S., 2005. A combination of soft-shell turtle powder and essential oil of a unicellular chorophyte prevents bone loss and decreased bone strength in ovariectomized rats. Biological and Pharmaceutical Bulletin, 28: 275–279.
Zhou, F., Song, W. X., Shao, Q. J., Peng, X., Xiao, J. X., Hua, Y., Owari, B. N., Zhang, T. Z., and Ng, W. K., 2011. Partial replacement of fish meal by fermented soybean meal in diets for black sea bream, Acanthopagrus schlegelii, juveniles. Journal of the World Aquaculture Society, 42(2): 184–197.
Zhou, X. Q., Yang, F., Zhou, A. G., Cai, J. Y., Yan, B. J., and Gou, L., 2001. The lysine requirement of juvenile soft shell turtle. Journal of Fisheries of China, 25(5): 454–458 (in Chinse with English abstract).
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Zou, Y., Ai, Q., Mai, K. et al. Effects of brown fish meal replacement with fermented soybean meal on growth performance, feed efficiency and enzyme activities of Chinese soft-shelled turtle, Pelodiscus sinensis . J. Ocean Univ. China 11, 227–235 (2012). https://doi.org/10.1007/s11802-012-1896-8
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11802-012-1896-8