2015 – Volume 4, Issue 2 / (Page 21-28)

Effects of different probiotic bacteria on growth, body composition, immune response and hematological parameters of rainbow trout (Oncorhynchus mykiss) under sublethal water temperature

Irfan Selcuk Yazıcı, Olcay Hisar, Sevdan Yilmaz, Murat Yigit



The aim of this study was to evaluate the effects of probiotic bacteria Lactobacillus plantarum, Bacillus subtilis and their mix additives on growth performance, body composition, immune response and hematological parameters of rainbow trout (Oncorhynchus mykiss) under sublethal water temperature. Feeding trial was carried out for 60 days. The first group was fed with commercial feed plus fish oil. The second and third groups were given commercial feed plus Lactobacillus plantarum and Bacillus subtilis at a rate of 107 CFU g-1 fish oil, respectively. The fourth group was also fed with commercial feed plus 50% of both probiotic bacteria. After 60 days, there were no differences among the survival rates and body proximate composition of experimental groups. Results also showed that all additives (L. plantarum, B. subtilis and their mix) to diets had no significant effect on growth parameters of rainbow trout, although the fish fed the diet with L. plantarum had statistically better feed conversion ratio (FCR) compared to the other groups (p<0.05). However, the additives could improve the immunity and alter hematological parameters of the rainbow trout. In conclusion, it might be suggested that L. plantarum can be used as a beneficial dietary probiotic in rainbow trout reared under sublethal water temperature.



Probiotics, Rainbow trout, Bacillus, Lactobacillus, Growth, Immune response


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  • Abdel-Tawwab, M., Abdel-Rahman, A.M. and N.E. Ismael. 2008. Evaluation of commercial live bakers’ yeast, Saccharomyces cerevisiae as a growth and immunity promoter for fry Nile tilapia, Oreochromis niloticus (L.) challenged in situ with Aeromonas hydrophila. Aquaculture, 280(1):185-189.
  • Al-Dohail, M.A., Hashim, R. and M. Aliyu-Paiko. 2009. Effects of the probiotic, Lactobacillus acidophilus, on the growth performance, haematology parameters and immunoglobulin concentration in African Catfish (Clarias gariepinus, Burchell 1822) fingerling. Aquaculture Research, 40(14):1642-1652.
  • Andani, H.R.R., Tukmechi, A., Meshkini, S. and N. Sheikhzadeh. 2012. Antagonistic activity of two potential probiotic bacteria from fish intestines and investigation of their effects on growth performance and immune response in rainbow trout (Oncorhynchus mykiss). Journal of Applied Ichthyology, 28(5):728-734.
  • AOAC International, 2000. Association of Official Analytical Chemists. Official Methods of Analysis (17th ed.).Washington DC. 2200 pp.
  • Aras-Hisar, S., Yanik, T. and O. Hisar. 2003. Hatchery and growth performance of two trout pure breeds, Salvelinus alpinus and Salmo trutta fario, and their hybrid. The Israeli Journal of Aquaculture-Bamidgeh, 55:154-159.
  • Bagheri, T., Hedayati, S.A., Yavari, V., Alizade, M. and A. Farzanfar. 2008. Growth, survival and gut microbial load of rainbow trout (Onchorhynchus mykiss) fry given diet supplemented with probiotic during the two months of first feeding. Turkish Journal of Fisheries and Aquatic Sciences, 8:43-48.
  • Barnes, M.E., Durben, D.J., Reeves, S.G. and R. Sanders. 2006. Dietary yeast culture supplementation improves initial rearing of McConaughy strain rainbow trout. Aquaculture Nutrition, 12(5):388-394.
  • Başusta, G.A. 2005. Fish hematology and hematological techniques. In: Karatas M (ed) Research techniques in fish biology (in Turkish), 1st edn. Nobel Publications, Ankara, pp 275-300.
  • Blaxhall, P.C. and K.W. Daisley. 1973. Routine haematological methods for use with fish blood. Journal of Fish Biology, 5(6):771-781.
  • Bulut, M., Yigit, M., Ergün, S., Kesbic, O.S., Acar, Ü., Gültepe, N., Karga, M. and T.W. Campbell. 2004. Clinical chemistry of fish and amphibians. In: Thrall MA, Baker DC, Campbell TW, DeNicola D, Fettman MJ, Lassen ED, Rebar A, Weiser G (eds) Veterinary hematology and clinical chemistry, 1st ed. Lippincott Williams & Wilkins, Pennsylvania, pp 499–517.
  • Caruso, D., Lusiastuti, A.M., Slembrouck, J., Komarudin, O. and M. Legendre. 2013. Traditional pharmacopeia in small scale freshwater fish farms in west Java, Indonesia: An ethnoveterinary approach. Aquaculture, 416:334-345.
  • Cha, J.H., Rahimnejad, S., Yang, S.Y., Kim, K.W. and K.J. Lee. 2013. Evaluations of Bacillus spp. as dietary additives on growth performance, innate immunity and disease resistance of olive flounder (Paralichthys olivaceus) against Streptococcus iniae and as water additives. Aquaculture, 402:50-57.
  • Chiu, C.H., Cheng, C.H., Gua, W.R., Guu, Y.K. and W. Cheng. 2010. Dietary administration of the probiotic, Saccharomyces cerevisiae P13, enhanced the growth, innate immune responses, and disease resistance of the grouper, Epinephelus coioides. Fish & Shellfish Immunology, 29(6):1053-1059.
  • Daniels, H.V. and M.L. Gallagher. 2000. Effect of dietary protein level on growth and blood parameters in summer flounder, Paralichthys dentatus. Journal of Applied Aquaculture, 10(1):45-52.
  • De Schrijver, R. and F. Ollevier. 2000. Protein digestion in juvenile turbot (Scophthalmus maximus) and effects of dietary administration of Vibrio proteolyticus. Aquaculture, 186(1):107-116.
  • Diab, A.S., Abdel-Hadi, Y.M., Ahmed, M.H., Saber, S.F. and M.E. Aboel-Atta. 2006. Out-door study on the use of Echinacea (Echinacea purpurea), Marjoram (Origanum dictamnus) and yeast (Saccharomyces cerevisiae) as feed additives for Oreochromis niloticus. Egyptian Journal of Agricultural Research, 84(18):537-551.
  • Eslamloo, K., Akhavan, S.R. and M.A. Henry. 2013. Effects of dietary administration of Bacillus probiotics on the nonspecific immune responses of tinfoil barb, Barbonymus schwanenfeldii (Actinopterygii: Cypriniformes: Cyprinidae). Acta Ichthyologica et Piscatoria, 43(3):211-218.
  • FAO, 2013. Food and Agriculture Organization of the United Nations. Fisheries and Aquaculture Department, Information and Statistics Branch.
  • Fauconneau, B. 1984. The measurement of whole body protein synthesis in larval and juvenile carp (Cyprinus carpio). Comparative Biochemistry and Physiology Part B, 78(4):845-850.
  • Fournier, V., Gouillou-Coustans, M.F., Metailler, R., Vachot, C., Moriceau, J., Le Delliou, H. and S.J. Kaushik. 2002. Nitrogen utilisation and ureogenesis as affected by dietary nucleic acid in rainbow trout (Oncorhynchus mykiss) and turbot (Psetta maxima). Fish Physiology and Biochemistry, 26(2):177-188.
  • Giri, S.S., Sukumaran, V., Sen, S.S. and P.K. Jena. 2014. Effects of dietary supplementation of potential probiotic Bacillus subtilis VSG1 singularly or in combination with Lactobacillus plantarum VSG3 or/and Pseudomonas aeruginosa VSG2 on the growth, immunity and disease resistance of Labeo rohita. Aquaculture Nutrition, 20(2):163-171.
  • Gopalakannan, A. and V. Arul. 2010. Enhancement of the innate immune system and disease‐resistant activity in Cyprinus carpio by oral administration of β‐glucan and whole cell yeast. Aquaculture Research, 41(6):884-892.
  • Günther, J. and R. Jiménez-Montealegre. 2004. Effect of the probiotic Bacillus subtilis on the growth and food utilization of tilapia (Oreochromis niloticus) and prawn (Macrobrachium rosenbergii) under laboratory conditions. International Journal of Tropical Biology and Conservation, 1(1):937-943.
  • Haney, D.C., Hursh, D.A., Mix, M.C. and J.R. Winton. 1992. Physiological and hematological changes in chum salmon artificially infected with erythrocytic necrosis virus. Journal of Aquatic Animal Health, 4(1):48-57.
  • Harikrishnan, R., Rani, M.N. and C. Balasundaram. 2003. Hematological and biochemical parameters in common carp, Cyprinus carpio, following herbal treatment for Aeromonas hydrophila infection. Aquaculture, 221(1):41-50.
  • Heidarieh, M., Mirvaghefi, A.R., Akbari, M., Farahmand, H., Sheikhzadeh, N., Shahbazfar, A.A. and M. Behgar. 2012. Effect of dietary Ergosan on growth performance, digestive enzymes, intestinal histology, hematological parameters and body composition of rainbow trout (Oncorhynchus mykiss). Fish Physiology and Biochemistry, 38(4):1169-1174.
  • Henderson, R.J. 1996. Fatty acid metabolism in freshwater fish with particular reference to polyunsaturated fatty acids. Archives of Animal Nutrition, 49(1):5-22.
  • Hoseinifar, S.H., Mirvaghefi, A. and D.L. Merrifield. 2011. The effects of dietary inactive brewer’s yeast Saccharomyces cerevisiae var. ellipsoideus on the growth, physiological responses and gut microbiota of juvenile beluga (Huso huso). Aquaculture, 318(1):90-94.
  • Ineno, T., Tsuchida, S., Kanda, M. and S. Watabe. 2005. Thermal tolerance of a rainbow trout Oncorhynchus mykiss strain selected by high‐temperature breeding. Fisheries Science, 71(4):767-775.
  • Irianto, A. and B. Austin. 2002. Use of probiotics to control furunculosis in rainbow trout, Oncorhynchus mykiss (Walbaum). Journal of Fish Diseases, 25(6):333-342.
  • Kesarcodi-Watson, A., Kaspar, H., Lategan, M. J. and L. Gibson. 2008. Probiotics in aquaculture: the need, principles and mechanisms of action and screening processes. Aquaculture, 274(1):1-14.
  • Kobeisy, M.A. and S.Y. Hussein. 1995. Influence of dietary live yeast on growth performance and some blood constituents in Oreochromis niloticus. In Proc. 5th Science Conference Animal Nutrition, Ismailia, Egypt, (pp. 12-13).
  • Lara-Flores, M., Olvera-Novoa, M.A., Guzmán-Méndez, B.E. and W. López-Madrid. 2003. Use of the bacteria Streptococcus faecium and Lactobacillus acidophilus, and the yeast Saccharomyces cerevisiae as growth promoters in Nile tilapia (Oreochromis niloticus). Aquaculture, 216(1):193-201.
  • Li, P. and D.M. Gatlin. 2003. Evaluation of brewers yeast (Saccharomyces cerevisiae) as a feed supplement for hybrid striped bass (Morone chrysops×M. saxatilis). Aquaculture, 219(1):681-692.
  • Li, P., Burr, G.S., Goff, J., Whiteman, K.W., Davis, K.B., Vega, R. R. and D.M. Gatlin. 2005. A preliminary study on the effects of dietary supplementation of brewers yeast and nucleotides, singularly or in combination, on juvenile red drum (Sciaenops ocellatus). Aquaculture Research, 36(11):1120-1127.
  • Merrifield, D.L., Dimitroglou, A., Foey, A., Davies, S.J., Baker, R. T., Bøgwald, J. and E. Ringø. 2010. The current status and future focus of probiotic and prebiotic applications for salmonids. Aquaculture, 302(1):1-18.
  • Mayes, P.A. and K.M. Botham. 2003. Lipid transport and storage. Harper’s Illustrated Biochemistry. 26th ed. California: Lange Medical Books/McGraw-Hill.
  • Miller, M.R., Nichols, P.D. and C.G. Carter. 2007. Replacement of dietary fish oil for Atlantic salmon parr (Salmo salar L.) with a stearidonic acid containing oil has no effect on omega-3 long-chain polyunsaturated fatty acid concentrations. Comparative Biochemistry and Physiology Part B, 146(2):197-206.
  • Mohanty, S.N., Swain, S. K. and S.D. Tripathi. 1996. Rearing of catla (Catla catla) spawn on formulated diets. Journal of Aquaculture in the Tropics, 11:253-258.
  • Molony, B. 2001. Environmental requirements and tolerances of rainbow trout (Oncorhynchus mykiss) and brown trout (Salmo trutta) with special reference to Western Australia: a review. Fisheries Research Division, Report No:130.
  • Morgan, J.D. and G.K. Iwama. 1997. Measurements of stressed states in the field. In: Iwama GK, Pickering AD, Sumpter JP, Schreck CB (eds) Fish stress and health in aquaculture. Cambridge university Press, Cambridge, pp 247-270.
  • Morgan, A.L., Thompson, K.D., Auchinachie, N.A. and H. Migaud, 2008. The effect of seasonality on normal haematological and innate immune parameters of rainbow trout Oncorhynchus mykiss L. Fish & Shellfish Immunology, 25(6):791-799.
  • Nayak, S.K. 2010. Probiotics and immunity: a fish perspective. Fish & Shellfish Immunology, 29(1):2-14.
  • Nayar, S., Hegde, S., Srinivas Rao, P. and P. Sudha. 1998. Live organisms as feed in aquaculture. Infofish International, 36- 48.
  • Noh, H., Han, K.I., Won T.H. and Y.J. Choi. 1994. Effect of antibiotics, enzymes, yeast culture and probiotics on the growth performance of Israeli carp. Korean Journal of Animal Science, 36:480-486.
  • Nudo, L P. and E.S. Catap. 2011. Immunostimulatory effects of Uncaria perrottetii (A. Rich.) Merr.(Rubiaceae) vinebark aqueous extract in Balb/C mice. Journal of Ethnopharmacology, 133(2):613-620.
  • Oduleye, S.O. 1982. Growth and growth regulation in the cichlids. Aquaculture, 27(3):301-306.
  • Oliva-Teles, A. and P. Gonçalves. 2001. Partial replacement of fishmeal by brewers yeast (Saccaromyces cerevisae) in diets for sea bass (Dicentrarchus labrax) juveniles. Aquaculture, 202(3):269-278.
  • Pooramini, M., Kamali, A., Hajimoradloo, A., Alizadeh, M. and R. Ghorbani. 2009. Effect of using yeast (Saccharomyces cerevisiae) as probiotic on growth parameters, survival and carcass quality in rainbow trout Oncorhynchus mykiss fry. International Aquatic Research, 1(1):39-44.
  • Quade, M.J. and J.A. Roth. 1997. A rapid, direct assay to measure degranulation of bovine neutrophil primary granules. Veterinary Immunology and Immunopathology, 58(3):239-248.
  • Skalli, A. and J.H. Robin. 2004. Requirement of n-3 long chain polyunsaturated fatty acids for European sea bass (Dicentrarchus labrax) juveniles: growth and fatty acid composition. Aquaculture, 240(1):399-415.
  • Smith, M.A.K. 1981. Estimation of growth potential by measurement of tissue protein synthetic rates in feeding and fasting rainbow trout, Salmo gairdnerii Richardson. Journal of Fish Biology, 19(2):213-220.
  • Soivio, A., Niemistö, M. and Bäckström. 1989. Fatty acid composition of Coregonus muksun Pallas: changes during incubation, hatching, feeding and starvation. Aquaculture, 79(1):163-168.
  • Son, V.M., Chang, C.C., Wu, M.C., Guu, Y.K., Chiu, C.H. and W. Cheng. 2009. Dietary administration of the probiotic, Lactobacillus plantarum, enhanced the growth, innate immune responses, and disease resistance of the grouper Epinephelus coioides. Fish & Shellfish Immunology, 26(5):691-698.
  • Spisni, E., Tugnoli, M., Ponticelli, A., Mordenti, T. and V. Tomasi, 1998. Hepatic steatosis in artificially fed marine teleosts. Journal of Fish Diseases, 21(3):177-184.
  • Subasinghe, R.P. 2005. Epidemiological approach to aquatic animal health management: opportunities and challenges for developing countries to increase aquatic production through aquaculture. Preventive Veterinary Medicine, 67(2):117-124.
  • Stasiak, S.A. and P.C. Baumann. 1996. Neutrophil activity as a potential bioindicator for contaminant analysis. Fish & Shellfish Immunology, 6(7):537-539.
  • Swain, S.K., Rangacharyulu, P. V., Sarkar, S. and K.M. Das. 1996. Effect of a probiotic supplement on growth, nutrient utilization and carcass composition in mrigal fry. Journal of Aquaculture, 4:29-35.
  • Taoka, Y., Maeda, H., Jo, J.Y., Jeon, M.J., Bai, S.C., LEE, W.J., Yuge, K. and S. Koshio. 2006. Growth, stress tolerance and non‐specific immune response of Japanese flounder Paralichthys olivaceus to probiotics in a closed recirculating system. Fisheries Science, 72(2):310-321.
  • Todorčević, M., Kjær, M.A., Djaković, N., Vegusdal, A., Torstensen, B.E. and B. Ruyter. 2009. N-3 HUFAs affect fat deposition, susceptibility to oxidative stress, and apoptosis in Atlantic salmon visceral adipose tissue. Comparative Biochemistry and Physiology Part B, 152(2):135-143.
  • Tovar, D., Zambonino, J., Cahu, C., Gatesoupe, F. J., VázquezJuárez, R. and R. Lésel. 2002. Effect of live yeast incorporation in compound diet on digestive enzyme activity in sea bass (Dicentrarchus labrax) larvae. Aquaculture, 204(1):113-123.
  • Vendrell, D., Balcazar, J.L., de Blas, I., Ruiz-Zarzuela, I., Gironés, O. and J.L. Muzquiz. 2008. Protection of rainbow trout (Oncorhynchus mykiss) from lactococcosis by probiotic bacteria. Comparative Immunology, 31(4):337-345.
  • Verschuere, L., Rombaut, G., Sorgeloos, P. and W. Verstraete 2000. Probiotic bacteria as biological control agents in aquaculture. Microbiology and Molecular Biology Reviews, 64(4):655-671.
  • Waché, Y., Auffray, F., Gatesoupe, F.J., Zambonino, J., Gayet, V., Labbé, L. and C. Quentel. 2006. Cross effects of the strain of dietary Saccharomyces cerevisiae and rearing conditions on the onset of intestinal microbiota and digestive enzymes in rainbow trout, Onchorhynchus mykiss, fry. Aquaculture, 258(1):470-478.
  • Yılmaz, S., Ergün, S. and E.Ş. Çelik. 2014. Effect of dietary spice supplementations on welfare status of sea bass, Dicentrarchus labrax L. Proceedings of the National Academy of Sciences, India Section B:1-9.
  • Zilberg, D., Tal, A., Froyman, N., Abutbul, S., Dudai, N. and A. Golan‐Goldhirsh. 2010. Dried leaves of Rosmarinus officinalis as a treatment for streptococcosis in tilapia. Journal of Fish Diseases, 33:361-369.