1. bookVolume 20 (2020): Issue 3 (July 2020)
Journal Details
First Published
25 Nov 2011
Publication timeframe
4 times per year
Open Access

Replacement of Fish Meal by Solid State Fermented Lupin (Lupinus albus) Meal with Latobacillus plantarum 299v: Effect on Growth and Immune Status of Juvenile Atlantic Salmon (Salmo salar)

Published Online: 01 Aug 2020
Volume & Issue: Volume 20 (2020) - Issue 3 (July 2020)
Page range: 991 - 1009
Received: 28 Sep 2019
Accepted: 08 Jan 2020
Journal Details
First Published
25 Nov 2011
Publication timeframe
4 times per year

The aim of this study was to assess quality of SSF (Solid State Fermented) lupin with Lactobacillus plantarum 299v, and its effects (on growth, feed utilization, digestibility and immunity) of juvenile Atlantic salmon (S. salar), when used as fish meal replacer. Five experimental diets were formulated to provide 40% crude protein and 21% dietary lipid (dry matter basis) with the raw or fermented lupin meal-based protein source replacing fish meal at 15% and 30%. Triplicate groups of fish (averaging 3.53 ± 0.05 g) were fed with experimental diets for 8 weeks. Fermentation process modified nutrient profile of lupin meal and enriched it with lactic, citric and acetic acids. Fish in the FL15% group showed a higher (P < 0.05) final body weight, weight gain, FCR, SGR, and PER compared to those of C group. Apparent digestibility coefficient (ADC) of protein and Nitrogen-free extract showed a significantly higher values in FL15% experimental group, compared to those shown in C group. Fish in the FL15% group showed a higher (P<0.05) lysozyme activity and leucocyte respiratory burst compared to that shown by fish samples in the C experimental group; phagocytic activity did not record differences among experimental groups. In conclusion, replacement of fish meal by raw or fermented lupin meal did not compromise growth, apparent digestibility coefficients and immune status of juvenile Atlantic salmon and even improve fish performance when supplemented at 15%.


Abu-Elala N.M., & Ragaa N.M. (2015). Eubiotic effect of a dietary acidifier (potassium diformate) in the health status of cultured Oreochromis niloticus. J. Adv. Res, 6: 621–629.Search in Google Scholar

Acar U., Kesbic O.S., Yilmaz S., & Karabayir A. (2018). Growth performance, hematological and serum biochemical profiles in rainbow trout (Oncorhynchus mykiss) fed varying levels of lupin (Lupinus albus) meal. Aquac. Res, 49: 2579–2586.Search in Google Scholar

Al-Thobaiti A., Al-Ghanim K., Suliman E.M., &Mahboob S. (2017). Impact of replacing fish meal by a mixture of different plant protein sources on the growth performance of Nile tilapia (Oreochromis niloticus L.) diets. Braz. J. Biol., 78(3): online. http://dx.doi.org/10.1590/1519-6984.17223010.1590/1519-6984.17223029069165Search in Google Scholar

AOAC (1995). Official Methods of Analysis of the Association of Analytical Chemist. 16th Edition. AOAC: Washington, DC. 1018 pp.Search in Google Scholar

Baruah K., Sahu N.P., Pal A.K., Jain K.K., Debnath D., Mukherjee S.C. (2007). Dietary microbial phytase and citric acid synergistically enhances nutrient digestibility and growth performance of Labeo rohita (Hamilton) juveniles at sub-optimal protein level. Aquac. Res., 38(2): 109 – 120.Search in Google Scholar

Bonaldo A., Parma L., Mandrioli L., Sirri R., Fontanillas R., Badiani A., Gatta P.P. (2011). Increasing dietary plant proteins affect growth performance and ammonia excretion but not digestibility and gut histology in turbot (Psetta maxima) juveniles. Aquaculture, 318(1-2): 101 – 108.Search in Google Scholar

Bransden M.P., Carter C.G., & Nowak B.F. (2001). Effect of dietary protein source on growth, immune function, blood chemistry and disease resistance of Atlantic salmon (Salmo salar L.) parr. Anim. Sci., 73(1): 105 – 113.Search in Google Scholar

Castillo S., Rosales M., Pohlenz C., Gatlin III, D.M. (2014). Effects of organic acids on growth performance and digestive enzyme activities of juvenile red drum Sciaenops ocellatus. Aquaculture, 433: 6 – 12.Search in Google Scholar

Chi C-H., & Cho S-J. (2016). Improvement of bioactivity of soybean meal by solid-state fermentation with Bacillus amyloliquefaciens versus Lactobacillus spp. and Saccharomyces cerevisiae. LWT-Food Sci. Tech., 68: 619 – 625.Search in Google Scholar

Cizeikiene D., Juodeikiene G., & Damasius J. (2018). Use of wheat straw biomass in production of L-lactic acid applying biocatalysts and combined lactic acid bacteria strains belonging to the genus Lactobacillus. Biocatal. Agri. Biotechnol., 15: 185 – 191.Search in Google Scholar

Cunha S.C., Ferreira I.M.P.L.V.O., Fernandes J.O., Faria M.A., Beatriz M., Oliveira P.P., & Ferreira M. A. (2001). Determination of lactic, acetic, succinic, and citric acids in table olives by HPLC/UV. J. Liq. Chromatogr. R. T., 24(7): 1029 – 1038.Search in Google Scholar

Dai C., Ma H., He R., Huang L., Zhu S., Ding Q., & Luo L. (2017). Improvement of nutritional value and bioactivity of soybean meal by solid-state fermentation with Bacillus subtilis. LWT, 86: 1 – 7.Search in Google Scholar

Fu W., & Mathews A.P. (1999). Lactic acid production from lactose by Lactobacillus plantarum: kinetic model and effects of pH, substrate and oxygen. Biochem. Eng. J., 3(3): 163 – 170.Search in Google Scholar

Fuentes-Quesada J., Viana M.T., Rombenso A.N., Guerrero-Rentería Y., Nomura-Solís M., Gómez-Calle V., Lazo J.P., Mata-Sotres J.A. (2018). Enteritis induction by soybean meal in Toaba macdonaldi diets: Effects on growth performance, digestive capacity, immune response and distal intestine integrity. Aquaculture, 495: 78 – 89.Search in Google Scholar

Furukawa A. & Tsukahara H. (1996). On the acid digestion method for the determination of chromic oxide as an index substance in the study of digestibility of fish feed. Bulleting of. Jpn. Soc. Sci. Fish., 32(3): 502–506.Search in Google Scholar

Gatlin III D.M., Barrows F.T., Brown P., Dabrowsky K., Gaylord T.G., Hardy R.W., …Wurtele, E. (2007). Expanding the utilization of sustainable plant products in aquafeeds: a review. Aquac. Res., 38(6): 551-579.Search in Google Scholar

Gao X., Zhang M., Li X., Han Y., Wu F., & Liu Y. (2018). The effects of feeding Lactobacillus pentosus on growth, immunity, and disease resistance in Haliotis discus hannai Ino. Fish Shellfish Immun., 78: 42 – 51.Search in Google Scholar

Giri S.S., Sukumaran V., & Oviya M. (2013). Potential probiotic Lactobacillus plantarum VSG3 improves the growth, immunity, and disease resistance of tropical freshwater fish, Labeo rohita). Fish Shellfish Immunol., 34(2): 660 – 666.Search in Google Scholar

Gislason G., Olsen R.E., Hinge E. (1996). Comparative effects of dietary Na+ - lactate on Artic char, Salvelinus alpinus L., and Atlantic salmon, Salmo salar L. Aquac. Res., 27(6): 429 – 435.Search in Google Scholar

Glencross D.B., Boujard T., & Kaushik S.J. (2003). Influence of oligosaccharides on the digestibility of lupin meals when fed to rainbow trout, Oncorhynchus mykiss. Aquaculture, 219(1-4):703-713.Search in Google Scholar

Hang Y.D., Luh B.S., & Woodams E.E. (1987). Microbial production of Citric Acid by Solid State Fermentation of Kiwifruit Peel. J. Food Sci., 52(1): 226 – 227.Search in Google Scholar

Hansen A-C., Roselund G., Karlsen O., Olsvik P.A., & Hemre G-I. (2006). The inclusion of plant protein in cod diets, its effects on macronutrient digestibility, gut and liver histology and heat shock protein transcription. Aquac. Res., 37(8): 773 – 784Search in Google Scholar

He W., Rahimnejad S., Wang L., Song K., Lu K., & Zhang C. (2017). Effects of organic acid and essential oils blend on growth, gut microbiota, immune response and disease resistance of Pacific white shrimp (Litopenaeus vannamei) against Vibrio parahaemolyticus. Fish Shellfish Immun., 70: 164 – 173.Search in Google Scholar

Ho V.T.T., Fleet G.H., & Zhao J. (2018). Unravelling the contribution of lactic acid bacteria and acetic acid bacteria to coca fermentation using inoculating organisms. Intl. J. Food Microbiol., 279: 43 – 56.Search in Google Scholar

Johansen, R., Needham, J.R., Colquhoun, D.J., Poppe, T.T. & Smith, J. (2006) Guidelines for health and welfare monitoring of fish use in research. Laboratory Animals, 40(4), 323-340.10.1258/00236770677847645117018205Search in Google Scholar

Katya K., Park G., Bharadwaj A.S., Browdy C., Vazquez-Anon M., & Bai S.C. (2018). Organic acids blend as dietary antibiotic replacer in marine fish olive flounder, Paralichthys olivaceus. Aquac. Res., 49(8): 2861 – 2868.Search in Google Scholar

Khajepour F., & Hosseini S.A. (2012). Citric acid improves growth performance and phosphorous digestibility in Beluga (Huso huso) fed diets where soybean meal partly replaced fish meal. Anim. Feed Sci. Tech., 171(1): 68 – 73.Search in Google Scholar

Koh C-B., Romano N., Zahrah A.S., & Ng W-K (2016). Effects of dietary organic acid blend and oxytetracycline on the growth, nutrient utilization and total cultivable gut microbiota of the red hybrid tilapia, Oreochromis sp., and resistance to Streptococcus agalactiae. Aquac. Res., 47(2): 357 – 369.Search in Google Scholar

Li C., Zhang G.F., Mao X., Wang J.Y., Duan C.Y., Wang Z.J. & Liu L.B. (2016). Growth and acid production of Lactobacillus delbrueckii spp. Bulgaricus ATCC 11842 in the fermentation of algal carcass. J. Dairy Sci., 99(6): 4243 – 4250.Search in Google Scholar

Liong M.T., & Shah N.P. (2005). Production of organic acids from fermentation of mannitol, fructooligosaccharide and inulin by a cholesterol removing Lactobacillus acidophilus strain. J. Applied Microbiol., 99(4): 783 – 793.Search in Google Scholar

Liu W., Yang Y., Zhang J., Gatlin D.M., Ringo E., Zhou Z. (2014). Effects of dietary microencapsulated sodium butyrate on growth, intestinal mucosal morphology, immune response, and adhesive bacteria in juvenile common carp (Cyprinus carpio) pre-fed with or without oxidized oil. Brit. J. Nutr., 112: 15 – 29.Search in Google Scholar

Luckstadt C. (2008). The use of acidifiers in fish nutrition. CAB Reviews: Perspectives in Agri. Vet. Sci., Nutr. and Nat. Res., 3(44): 1 – 8.Search in Google Scholar

Mladenovic D., Pejin J., Kocic-Tanackov S., Radovanovic Z., Djukic-Vukovic A., Mojovic L. (2018). Lactic acid production on molasses enriched potato stillage by Lactobacillus paracasei immobilized on fish agro-industrial waste supports. Ind. Crop. Prod., 124: 142 – 148.Search in Google Scholar

Moniruzzaman M., Bae J.H., Won S.H., Cho S.J., Chang K.H., & Bai S.C. (2017). Evaluation of solid-state fermented protein concentrates as a fish meal replacer in the diets of juvenile rainbow trout Oncorhynchus mykiss. Aquac. Nutr., 24(4): 1198 – 1212.Search in Google Scholar

Ng W-K., & Koh C.B. (2016). The utilization and mode of action of organic acids in the feeds of cultured aquatic animals. Rev. Aquacult., 9(4): 342 – 368.Search in Google Scholar

Ng W-K., Koh C-B., Teoh C-T., Romano N. (2015). Farm-raised shrimp, Penaeus monodon, fed commercial feeds with added organic acids showed enhanced nutrient utilization, immune response and resistance to Vibrio harveyi challenge. Aquaculture, 449(1): 69 – 77.Search in Google Scholar

Oude-Elferink S.J.W.H., Krooneman J., Gottschal J.C., Spoelstra S.F., Faber F., Driehuis F. (2001). Aerobic conversion of Lactic Acid to Acetic Acid and 1,2-Propaneidol by Lactobacillus buchneri. Appl. Environ. Microb., 67(1): 125 – 132.Search in Google Scholar

Panigrahi A., Kiron V., Kobayashi T., Puangkaew J., Satoh S., & Sugita H. (2004). Immune responses in rainbow trout Oncorhynchus mykiss induced by a potential probiotic bacteria Lactobacillus rhamnosus JCM 1136. Vet. Immunol. Immunop., 102(4): 379 – 388.Search in Google Scholar

Pandey A. (2003). Solid-state fermentation. Biochem. Eng. J., 13(2-3): 81 – 84.Search in Google Scholar

Pandey A., & Satoh S. (2008). Effects of organic acids on growth and phosphorous utilization in rainbow trout Oncorhynchus mykiss. Fish. Sci., 74(4): 867 – 874.Search in Google Scholar

Parry R.M., Chandan R.C., & Shahani K.M. (1965). A rapid and sensitive assay of muramidase. P. Soc. Exp. Biol., 119(2): 301 – 306.Search in Google Scholar

Pranoto Y., Anggrahini S., & Efendi Z. (2013). Effect of natural and Lactobacillus plantarum fermentation on in-vitro protein and starch digestibilities of sorghum flour. Food Biosci., 2: 46 – 52.Search in Google Scholar

Rahimnejad S., Lu K., Wang L., Song K., Mai K., Davis D.A., Zhang C. (2019). Replacement of fish meal with Bacillus pumillus SE5 and Pseudpzyma aphidis ZR1 fermented soybean meal in diets for Japanese seabass (Lateolabrax japonicus). Fish & Shellfish Immunol., 84: 987 – 997.Search in Google Scholar

Ray M., (2001). Effect of fermentation on the nutritive value of sesame seed meal in the diets for rohu, Labeo rohita (Hamilton), fingerlings. Aquac. Nutr., 5(4): 229 – 236.Search in Google Scholar

Ringo E. (1991). Effects of dietary lactate and propionate on growth and ingesta in Arctic charr, Salvelinus alpinus (L.). Aquac., 96(3-4): 321 – 333.Search in Google Scholar

Ringo E., Olsen R.E., & Castell J.D. (1994). Effect of dietary lactate on growth and chemical composition of Artic Charr Salvelinus alpinus. J. World Aquacult. Soc., 25(3): 483 – 486.Search in Google Scholar

Romano N., Koh C-B., & Ng W-K. (2015). Dietary microencapsulated organic acids blend enhances growth, phosphorous utilization, immune response, hepatopancreatic integrity and resistance against Vibrio harveyi in white shrimp, Litopenaeus vannamei. Aquaculture, 435: 228 - 236.Search in Google Scholar

Saez P., Borquez A., Dantagnan P., & Hernández A. (2015) Effects of de-hulling, steam-cooking and microwave-irradiation in digestive value of white lupin (Lupinus albus) seed meal for rainbow trout (Oncorhynchus mykiss) and Atlantic salmon (Salmo salar). Arch. Anim. Nutri., 69 (2): 143 – 157.10.1080/1745039X.2015.100961325708530Search in Google Scholar

Sakai M., Kobayashi M., & Kawauchi H. (1996). In vitro activation of fish phagocytosis cells by GH, prolactina and somatolactin. J. Endocrinol., 151(1): 113 – 118.Search in Google Scholar

Salini M.J., & Adams L.R. (2014). Growth performance, nutrient utilization and digestibility by Atlantic salmon (Salmo salar) fed Tasmanian grown white (Lupinus albus) and narrow-leafed (L. angustifolius) lupins. Aquaculture., 426-427: 296 – 303.Search in Google Scholar

Sarker M.S.A., Satoh S., Kamata K., Haga Y., & Yamamoto Y. (2011). Partial replacement of fish meal with plant protein sources using organic acids to practical diets for juvenile yellowtail, Seriola quinqueradiata. Aquacult. Nutr., 18(1): 81 – 89.Search in Google Scholar

Shiu Y-L., Hsieh S-L., Guei W-C., Tsai Y-T., Chiu C-H., & Liu C-H. (2013). Using Bacillus substilis E20-fermented soybean meal as replacement for fish meal in the diet of orange-spotted grouper (Epinephelus coioides, Hamilton). Aquacult. Res., 46(6): 1403 – 1416.Search in Google Scholar

Smith D.M., Tabrett S.J., Glencross B.D., Irvin S.J., Barclay M.C. (2007). Digestibility of lupin kernel meals in feeds for the black tiger shrimp, Penaeus monodon. Aquaculture, 264(1-4). 353 – 362.10.1016/j.aquaculture.2006.12.002Search in Google Scholar

Smit G., Smit B.A., & Engels W.J. (2005). Flavor formation by lactic acid bacteria and biochemical flavor profiling of cheese products. FEMS of Microbiol. Rev., 29(3): 591 – 610.Search in Google Scholar

Sharawy Z., Goda A. M. A. S., & Hassaan M. S. (2016). Partial or total replacement of fish meal by solid state fermented soybean meal with Saccharomyces cerevisiae in diets for Indian prawn shrimp, Fenneropenaeus indicus, postlarvae. Anim. Feed Sci. Tech., 212: 90 – 99.Search in Google Scholar

Soccol C.R., Scopel-Ferreira da Costa E., Junior-Letti J.A., Karp S.G., Woiciechowski A.L., Porto de Souza-Vandenberghe L. (2017). Recent developments and innovations in solid state fermentation. Biotech. Res. Innov., 1(1): 52 – 71.Search in Google Scholar

Srisukchayakul P., Charalampopoulos D., Karatzas K. (2018). Study on the effect of citric acid adaptation toward the subsequent survival of Lactobacillus plantarum NCIMB 8826 in low pH fruit juices during refrigerated storage. Food Res. Intl., 111: 198 – 204.Search in Google Scholar

Su, X., Li X., Leng X., Tan C., Liu B., Chai X., Guo T. (2014). The improvement of growth, digestive enzyme activity and disease resistance of white shrimp by the dietary citric acid. Aquacult. Intl., 22(6): 1823 – 1835.Search in Google Scholar

Sugiura S.H., Roy P.K., Ferraris R.P. (2006). Dietary acidification enhances phosphorous digestibility but decreases H+ / K+ - ATPase expression in rainbow trout. J. Exp. Biol., 209: 3719 – 3728.Search in Google Scholar

Sun H., Tang J-W., Yao X-H., Wu Y-F., Wang X., Liu Y., & Lou B. (2015). Partial substitution of fish meal with fermented cottonseed meal in juvenile black sea bream (Acanthopagrus schlegelii) diets. Aquacult., 446: 30 – 36.Search in Google Scholar

Tabrett S., Blyth D., Bourne N., & Glencross B. (2012). Digestibility of Lupinus albus lupin meals in barramundi (Lates calcarifer). Aquacult., 364-365: 1 – 5.Search in Google Scholar

Tacon A.G.J., & Metian M. (2015). Feed matters: satisfying the feed demand of aquaculture. Reviews in Fish. Sci. Aquacult., 23: 1 – 10.Search in Google Scholar

Vandenberghe L.P.S., Karp S.G., de Oliveira P.Z., de Carvalho J.C., Rodrigues C., & Soccol C.R. (2018). Chapter 18-Solid-State fermentation for the production of organic acids. In: Current Developments in Biotechnology and Bioengineering. Current advances in Solid-State Fermentation (Pandey, A., Larroche, C., & Soccol C.R. eds), pp 415 – 434. Elsevier. Langford Lane, Kidlington, UK.Search in Google Scholar

Van-Doan H., Doolgindachbaporn S., & Suksri A. (2014). Effects of low molecular weight agar and Lactobacillus plantarum on growth performance, immunity, and disease resistance of basa fish (Pangasius bocourti, Sauvage 1880). Fish & Shellfish Immun., 41(2): 340 – 345.Search in Google Scholar

Vielma J., & Lall S.P. (2006). Dietary formic acid enhanced apparent digestibility of minerals in rainbow trout, Oncorhynchus mykiss (Walbaum). Aquacult. Nutr., 3(4): 265 – 268.Search in Google Scholar

Vo B.V., Bui D.P., Nguyen H.Q., & Fotedar R. (2015). Optimized fermented lupin (Lupinus angustifolius) inclusion in juvenile barramundi (Lates calcarifer) diets. Aquaculture, 444: 62 – 69.Search in Google Scholar

Wang J.-h., Guo H., Zhang T-r., Wang H., Liu B-n., & Xiao S. (2016a). Growth performance and digestion improvement of juvenile sea cucumber Apostichopus japonicus fed by solid-state fermentation diet. Aquacult. Nutr., 23(6): 1312 – 1318.10.1111/anu.12506Search in Google Scholar

Wang L., Zhou H., He R., Xu W., Mai K., & He G. (2016b). Effect of soybean meal fermentation by Lactobacillus plantarum P8 on growth, immune responses, and intestinal morphology in juvenile turbot (Scophthalmus maximus L.). Aquaculture, 464: 87 – 94.10.1016/j.aquaculture.2016.06.026Search in Google Scholar

Xia Y., Lu M., Chen G., Cao J., Gao F., Wang M., Yi M. (2018). Effects of dietary Lactobacillus rhamnosus JMC1136 and Lactococcus lactis subs. Lactis JCM5805 on the growth, intestinal microbioita, morphology, immune response and disease resistance of juvenile Nile tilapia, Oreochromis niloticus. Fish & Shellfish Immun., 76: 368 – 379.Search in Google Scholar

Yin G., Jeney G., Racz T., Pao X., & Jeney Z. (2006). Effect of two Chinese herbs (Astragalus radix and Scutellaria radix) on non-specific immune response of tilapia, Oreochromis niloticus. Aquaculture, 253(1-4): 39 – 47.Search in Google Scholar

Yu L., Zhai Q., Zhu J., Zhang C., Li, T. ... Chen W. (2017). Dietary Lactobacillus plantarum supplementation enhances growth performance and alleviates aluminum toxicity in tilapia. Ecotox. Environ. Safe., 143: 307 – 314.Search in Google Scholar

Zhang C., Rahimnejad S., Wang Y., Lu K., Song K., Wang L., & Mai K. (2018). Substituting fish meal 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.Search in Google Scholar

Zhang T.S., Shi Y., Zhang S.L., Shang W., Gao X.Q., & Wang H.K. (2014). Whole soybean as probiotic lactic acid bacteria carrier food in solid-state fermentation. Food Control, 41. 1 – 6.10.1016/j.foodcont.2013.12.026Search in Google Scholar

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