Abstract
This study was designed to determine the effect of fishmeal (FM) replacement with soybean meal (SBM) in the diet of tilapia (Oreochromis niloticus). Growth, digestive enzyme activity, antioxidation, and gut histomorphology were assessed in the fish fed with five different formulated diets that increasingly replaced FM. The SBM0 contained 100% FM, followed by 25% (SBM25), 50% (SBM50), 75% (SBM75), and 100% (SBM100). Juvenile tilapia having weight and length of 6.6 ± 0.1 g and 5.4 ± 0.2 cm, respectively, were randomly divided into five treatment groups. Each group had 40 individual fish and fed to visual satiation for 90 days. Body weight gain and specific growth rate in fish fed with 25–75% SBM increased significantly (P < 0.01) compared with those in fish fed with SBM100. Fish having the same weight fed with diets SBM50, SBM75, and SBM100 showed a significantly (P < 0.01) longer intestine compared with those fed with SBM0 and SBM25. Villus height of the stomach and intestine was significantly (P < 0.01) greater in the fish fed with the diets SBM0, SBM25, and SBM50 compared with SBM75 and SBM100. Muscular thickness was inversely related with the increasing villus height. Protease activity increased significantly (P < 0.01) in the stomach, anterior intestine, and posterior intestine of fish fed with SBM0 compared with SBM100. In the stomach and anterior and posterior segments of the intestine, significantly (P < 0.01) higher lipase activity was observed in fish fed with the diets SBM0 and SBM25 compared with diet SBM100. In the stomach, anterior intestine, and posterior intestine, amylase activity was also significantly (P < 0.01) greater in SBM0 compared with SBM100. The antioxidant enzymes including superoxide dismutase and catalase of the liver were significantly (P < 0.01) higher in fish fed SBM100 compared with SBM0. These results suggest that the replacement of FM up to 75% with SBM could be possible considering the growth performances, gut health, and activities of digestive enzymes and antioxidant enzymes in O. niloticus.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Albro PW, Hall RD, Corbett JT, Schroeder J (1985) Activation of non-specific lipase (EC 3.1. 1) by bile salts. Biochim Biophys Acta 835(3):477–490. https://doi.org/10.1016/00052760(85)90117-1
AOAC (Association of Official Analytical Chemists) (2019) Official methods of analysis of Association of Official Analytical Chemists, 21st edn, Washington, D.C.
Bakke-McKellep AM, Frøystad MK, Lilleeng E, Dapra F, Refstie S, Krogdahl Å, Landsverk T (2007) Response to soy: T-cell-like reactivity in the intestine of Atlantic salmon, Salmo salar L. J Fish Dis 30:13–25. https://doi.org/10.1111/j.1365-2761.2007.00769.x
Barrows FT, Stone DA, Hardy RW (2007) The effects of extrusion conditions on the nutritional value of soybean meal for rainbow trout (Oncorhynchus mykiss). Aquaculture 265:244252. https://doi.org/10.1016/j.aquaculture.2007.01.017
Cabral EM, Fernandes TJR, Campos SD, Castro-Cunha M, Oliveira MBPP, Cunha LM, Valente LMP (2013) Replacement of fishmeal by plant protein sources up to 75% induces good growth performance without affecting flesh quality in on-growing Senegalese sole. Aquaculture 380-383:130–138. https://doi.org/10.1016/j.aquaculture.2012.12.006
Deng H, Gerencser AA, Jasper H (2015) Signal integration by Ca(2+) regulates intestinal stemcell activity. Nature 528:212–217. https://doi.org/10.1038/nature16170
El-Sayed AF, Nmartinez I, Moyano FJ (2000) Assessment of the effect of plant inhibitors on digestive proteases of Nile tilapia using in vitro assays. Aquac Int 8(5):403–415
García-Ortega A, Kissinger KR, Trushenski JT (2016) Evaluation of fishmeal and fish oil replacement by soybean protein and algal meal from Schizochytrium limacinum in diets for giant grouper Epinephelus lanceolatus. Aquaculture 452:1–8. https://doi.org/10.1016/j.aquaculture.2015.10.020
Gatlin DM, Barrows FT, Brown P, Dabrowski K, Gaylord TG, Hardy RW, Herman EM, Hu G, Krogdahl Å, Nelson R, Overturf K, Rust M, Sealey W, Skonberg D, Souza EJ, Stone D, Wilson R, Wurtele E (2007) Expanding the utilization of sustainable plant products in aquafeeds: a review. Aquac Res 38(6):551–579. https://doi.org/10.1111/j.13652109.2007.01704.x
Grisdale-Helland B, Helland SJ, Gatlin DM (2008) The effects of dietary supplementation with mannanoligosaccharide, fructooligosaccharide or galactooligo-saccharide on the growth and feed utilization of Atlantic salmon (Salmo salar). Aquaculture 283(1):163–167. https://doi.org/10.1016/j/aquaculture.2008.07.012
Hernández MD, Martínez FJ, Jover M, García BG (2007) Effects of partial replacement of fishmeal by soybean meal in sharpsnout seabream (Diplodus puntazzo) diet. Aquaculture 263:159–167. https://doi.org/10.1016/j.aquaculture.2006.07.040
Iwashita Y, Suzuki N, Matsunari H, Sugita T, Yamamoto T (2009) Influence of soya saponin, soya lectin, and cholyltaurine supplemented to a casein-based semipurified diet on intestinal morphology and biliary bile status in fingerling rainbow trout Oncorhynchus mykiss. Fish Sci 75(5):1307–1315. https://doi.org/10.1007/s12562-009-0158-1
Jahan H, Pervin MA, Akter R, Hossain Z (2019) Effects of soybean meal on new muscle generation and growth of silver barb, Barbonymus gonionotus. Int J Agric Environ Biores 4(3):102–110
Knudsen D, Urán P, Arnous A, Koppe W, Frøkiær H (2007) Saponin-containing subfractions of soybean molasses induce enteritis in the distal intestine of Atlantic salmon. J Agric Food Chem 55(6):2261–2267. https://doi.org/10.1021/jf0626967
Krogdahl Å, Bakke-McKellep AM, Baeverfjord G (2003) Effects of graded levels of standard soybean meal on intestinal structure, mucosal enzyme activities, and pancreatic response in Atlantic salmon (Salmo salar L.). Aquac Nutr 9:361–371. https://doi.org/10.1046/j.1365-2095.2003.00264.x
Kumar V, Wang H-P, Lalgudi RS, Mcgraw B, Cain R, Rosentrater KA (2019) Processed soybean meal as an alternative protein source for yellow perch (Perca flavescens) feed. Aquac Nutr 25:917–931. https://doi.org/10.1111/anu.12911
Lazzari R, Neto JR, Pedron FA, Loro VL, Pretto A, Gioda CR (2010) Protein sources and digestive enzyme activities in jundiá (Rhamdia quelen). Sci Agric 67(3):259–266. https://doi.org/10.1590/S0103-90162010000300002
Lin S, Luo L (2011) Effects of different levels of soybean meal inclusion in replacement for fishmeal on growth, digestive enzymes and transaminase activities in practical diets for juvenile tilapia, Oreochromis niloticus × O. aureus. Anim Feed Sci Technol 168:80–87. https://doi.org/10.1016/j.anifeedsci.2011.03.012
Mohebbi A, Nematollahi A, Dorcheh AE, Asad FG (2012) Influence of dietary garlic (Allium sativum) on the antioxidative status of rainbow trout (Oncorhynchus mykiss). Aquac Res 43:1184–1193. https://doi.org/10.1111/j.1365-2109.2011.02922.x
Monteiro MLG, Mársico ET, Lázaro CA, Anna Carolina Vilhena AC, Canto CS, Lima BRCC, Cruz AG, Conte-Júnior CA (2015) Effect of transglutaminase on quality characteristics of a value-added product tilapia wastes. J Food Sci Technol 52(5):2598–2609. https://doi.org/10.1007/s13197-014-1327-5
Mourente GE, Díaz-Salvago J, Bell G, Tocher DR (2002) Increased activities of hepatic antioxidant defence enzymes in juvenile gilthead sea bream (Sparus aurata L.) fed dietary oxidized oil: attenuation by dietary vitamin E. Aquaculture 214:343–361. https://doi.org/10.1016/S0044-8486(02)00064-9
Murashita K, Fukada H, Takahashi N, Hosomi N, Matsunari H, Furuita H, Oku H, Yamamoto T (2015) Effect of feed ingredients on digestive enzyme secretion in fish. Bull Fish Res Agen 40:69–74
Pavasovic A, Anderson AJ, Mather PB, Richardson NA (2007) Influence of dietary protein on digestive enzyme activity, growth and tail muscle composition in red claw crayfish, Cherax quadricarinatus (von Martens). Aquac Res 38:644–652. https://doi.org/10.1111/j.1365-2109.2007.01708.x
Qasem W, Azad M, Hossain Z, Azad E, Jorgensen S, San Juan SC, Cai C, Khafipour E, Beta T, Roberts LJ, Friel JK (2017) Assessment of complementary feeding of Canadian infants: effects on microbiome and oxidative stress, a randomized controlled trial. BMC Pediatr 17:54–12. https://doi.org/10.1186/s12887-017-0805-0
Radhakrishnan S, Bhavan P, Seenivasan C, Shanthi R, Muralisankar T (2014) Replacement of fish meal with Spirulina platensis, Chorella vulgaris and Azolla pinnata on nonenzymatic and enzymatic antioxidant activities of Macrobrachium rosenbergii. J Basic Appl Zool 67:25–33. https://doi.org/10.1016/j.jobaz.2013.12.003
Rašković BS, Stanković MB, Marković ZZ, Poleksić VD (2011) Histological methods in the assessment of different feed effects on liver and intestine of fish. J Agric Sci 56(1):87–100. https://doi.org/10.2298/JAS1101087R
Refstie S, Landsverk T, Bakke-McKellep AM, Ringø E, Sundby A, Shearer KD, Krogdahl Å (2006) Digestive capacity, intestinal morphology, and microflora of 1 year and 2 year old Atlantic cod (Gadus morhua) fed standard or bioprocessed soybean meal. Aquaculture 261(1):269–284. https://doi.org/10.1016/j.aquaculture.2006.07.011
Romarheim OH, Skrede A, Penn M, Mydland LT, Krogdahl Å, Storebakken T (2008) Lipid digestibility, bile drainage and development of morphological intestinal changes in rainbow trout (Oncorhynchus mykiss) fed diets containing defatted soybean meal. Aquaculture 274:329–338. https://doi.org/10.1016/j.aquaculture.2007.11.035
Swain MR, Kar S, Padmaja G, Ray RC (2006) Partial characterization and optimization of extracellular α-amylase from Bacillus subtilis isolated from cow dung microflora. Pol J Microbiol 55:289–296
Thakur M, Hurburg CR (2007) Quality of US soybean meal compared to the quality of soybean meals from other origins. J Am Oil Chem Soc 84(9):835–843
Tibaldi E, Hakim Y, Uni Z, Tulli F, de Francesco M, Luzzana U, 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. https://doi.org/10.1016/j.aquaculture.2006.06.026
Walter HE (1984) Proteinases: methods with haemoglobin, casein and azocoll as substrates. In: Bergmeyer HU (ed) Methods of enzymatic analysis. Verlag Chemie, Weinheim, pp 270–277
Wang Y, Guo JL, Li K, Bureau DP (2006) Effects of dietary protein and energy levels on growth, feed utilization and body composition of cuneate drum (Nibea miichthioides). Aquaculture 252:421–428. https://doi.org/10.1016/j.aquaculture.2005.06.051
Wang J, Tao Q, Wang Z, Mai K, Xu W, Zhang Y, Ai Q (2017a) Effects of fishmeal replacement by soybean meal with supplementation of functional compound additives on intestinal morphology and microbiome of Japanese seabass (Lateolabrax japonicus). Aquac Res 48:2186–2197. https://doi.org/10.1111/are.13055
Wang YR, Wang L, Zhang CX, Song K (2017b) Effects of substituting fishmeal with soybean meal on growth performance and intestinal morphology in orange-spotted grouper (Epinephelus coioides). Aquac Rep 5:52–57. https://doi.org/10.1016/j.aqrep.2016.12.005
Ward D, Bengtson DA, Lee CM, Gomez-Chiarri M (2016) Incorporation of soybean products in summer flounder (Paralichthys dentatus) feeds: effects on growth and survival to bacterial challenge. Aquaculture 452:395–401. https://doi.org/10.1016/j.aquaculture.2015.11.012
Yan B, Wang Z (2010) Growth, salinity tolerance and microsatellite analysis of the F2 reciprocal hybrids of Oreochromis niloticus × Sarotherodon galilaeus at different salinities. Aquac Res 41:336–344
Zhang C, Rahimnejad S, Wang YR, Lu K, Song K, Wang L, Mai K (2018) Substituting fishmeal with soybean meal in diets for Japanese seabass (Lateolabrax japonicus): effects on growth, digestive enzymes activity, gut histology, and expression of gut inflammatory and transporter genes. Aquaculture 483:173–182. https://doi.org/10.1016/j.aquaculture.2017.10.029
Zhao ZX, Song CY, Xie J, Ge XP, Liu B, Xia SL, Zhu SH (2016) Effects of fishmeal replacement by soybean peptide on growth performance, digestive enzyme activities, and immune responses of yellow catfish Pelteobagrus fulvidraco. Fish Sci 82(4):665–673. https://doi.org/10.1007/s12562-016-0996-6
Zhou F, Song W, Shao Q, Peng X, Xiao J, Hua Y, Owari BN, Zhang T, Ng WK (2011) Partial replacement of fish meal by fermented soybean meal in diets for black sea bream, Acanthopagrus schlegelii, juveniles. J World Aquacult Soc 42(2):184–197. https://doi.org/10.1111/j.1749-7345.2011.00455.x
Acknowledgements
We would like to sincerely thank Dr. Mohammad Nasif Sarowar, a post-doc fellow of Dalhousie University, Halifax, Canada, for the critical revision of the manuscript.
Funding
This research was funded from the special grants by the Ministry of Science and Technology, Government of the People’s Republic of Bangladesh, Dhaka, Bangladesh.
Author information
Authors and Affiliations
Corresponding author
Additional information
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Pervin, M.A., Jahan, H., Akter, R. et al. Appraisal of different levels of soybean meal in diets on growth, digestive enzyme activity, antioxidation, and gut histology of tilapia (Oreochromis niloticus). Fish Physiol Biochem 46, 1397–1407 (2020). https://doi.org/10.1007/s10695-020-00798-5
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10695-020-00798-5