DIETARY MANNAN-OLIGOSACCHARIDE INCREASES REACTIVE OXIGEN SPECIES PRODUCTION BUT DECREASES SERUM LYSOZYME IN HIGH LEVELS OF INCLUSION FOR NILE TILAPIA
DOI:
https://doi.org/10.20950/1678-2305.2020.46.3.551Keywords:
hematology, immunology, mannan-oligosaccharide;, Oreochromis niloticus ;, productive parameters.Abstract
In the present experiment, the effects of mannan-oligosaccharide (MOS) on health and growth of Nile tilapia juveniles were investigated. In addition to the control treatment (without MOS),three levels of MOS were included in Nile tilapia diets (1, 8, and 15 g kgâˆ"™1), and hematology, reactive oxygen species (ROS) production, lysozyme and productive parameters were analyzed. Fish blood was sampled at day zero (basal sample) and after 60 days of trial, and the productive parameters were evaluated at the end of the experiment. MOS feeding decreased the feed consumption (p = 0.0299) in fish fed with 1 and 8 g kg-1, but without any alteration in weight gain (WG) and feed conversion ratio (FCR). No changes were observed in the hematology due to MOS feeding after 60 days. However, the prebiotic caused changes in the innate immunity of fish, giving rise to ROS production in fish fed with 1 g kg-1 (p<0.0001) and decreasing the serum lysozyme activity of fish fed with 15 g kg-1 (p<0.0001). In conclusion, the authors recommend the inclusion of 1 g kg-1 for Nile tilapia juveniles feeding due to the positive effect in innate immune system.
References
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Akrami, R.; Chitsaz, H.; Hezarjaribi, A.; Ziaei, R. 2012. Effect of dietary mannan-oligosaccharide (MOS) on growth performance and immune response of Gibel carp juveniles (Carassius auratus gibelio). Journal of Veterinary Advances, 2(3): 507-513.
Anderson, D.; Siwicki, A. 1995. Basic hematology and serology for fish health programs. In: Shariff, M.; Arthur, J.R.; Subasinghe, R.P. (Eds.). Diseases in Asian Aquaculture II. Manila: Fish Health Section, Asian Fisheries Society. p. 185-102.
Andrews, S.R.; Sahu, N.P.; Pal, A.K.; Kumar, S. 2009. Haematological modulation and growth of Labeo rohita fingerlings: effect of dietary mannan-oligosaccharide, yeast extract, protein hydrolysate and chlorella. Aquaculture Research, 41(1): 61-69. http://dx.doi.org/10.1111/j.1365-2109.2009.02304.x.
Babior, B. 1984. The respiratory burst of phagocytes. The Journal of Clinical Investigation, 73(3): 599-601. http://dx.doi.org/10.1172/JCI111249.
Biller-Takahashi, J.; Takahashi, L.; Saita, M.; Gimbo, R.; Urbinati, E. 2013. Leukocytes respiratory burst activity as indicator of innate immunity of pacu Piaractus mesopotamicus. Brazilian Journal of Biology = Revista Brasileira de Biologia, 73(2): 425-429. http://dx.doi.org/10.1590/S1519-69842013000200026.
Bland, E.J.; Keshavarz, T.; Bucke, C. 2004. The influence of small oligosaccharides on the immune system. Carbohydrate Research, 339(10): 1673-1678. http://dx.doi.org/10.1016/j.carres.2004.05.009.
Collier, H.B. 1944. Standardization of blood haemoglobin determinations. Canadian Medical Association Journal, 50(6): 550-552.
Ellis, A. 1999. Immunity to bacteria in fish. Fish & Shellfish Immunology, 9(4): 291-308. http://dx.doi.org/10.1006/fsim.1998.0192.
FAO - Food and Agriculture Organization of the United Nations. 2016. The State of World Fisheries and Aquaculture: Contributing to food security and nutrition for all. Rome: FAO. 200p.
FAO - Food and Agriculture Organization of the United Nations. 2020. The State of World Fisheries and Aquaculture: Sustainability in action. Rome: FAO. 244p.
Goldenfarb, P.B.; Bowyer, F.P.; Hall, E.; Brosious, E. 1971. Reproducibility in the hematology laboratory: the microhematocrit determination. American Journal of Clinical Pathology, 56(1): 35-39. http://dx.doi.org/ 10.1093/ajcp/56.1.35.
Gómez, G.D.; Balcázar, J.L. 2008. A review on the interactions between gut microbiota and innate immunity of fish. FEMS Immunology and Medical Microbiology, 52(2): 145-154. http://dx.doi.org/10.1111/j.1574-695X.2007.00343.x.
Grisdale-Helland, B.; Helland, S.J.; Gatlin 3rd, D.M. 2008. The effects of dietary supplementation with mannan-oligosaccharide, fructooligosaccharide or galactooligosaccharide on the growth and feed utilization of Atlantic salmon (Salmo salar). Aquaculture (Amsterdam, Netherlands), 283(1-4): 163-167. http://dx.doi.org/10.1016/ j.aquaculture.2008.07.012.
Guzmán, D.M.M.; González, M.T. 2012. Evaluation of somatic indexes, hematology and liver histopathology of the fish Labrisomus philippii from San Jorge Bay, northern Chile, as associated with environmental stress. Revista de Biología Marina y Oceanografía, 47(1): 99-107. http://dx.doi.org/10.4067/S0718-19572012000100009.
Hoidal, J.R. 2001. Reactive oxygen species and cell signaling. American Journal of Respiratory Cell and Molecular Biology, 25(6): 661-663. http://dx.doi.org/10.1165/ajrcmb.25.6.f213.
Hrubec, T.; Smith, S. 2000. Hematology of fish. In: Schalm, O.W.; Jain, N.C.; Carroll, E.J. Schalm’s veterinary hematology. Philadelphia: Lippincott Williams and Wilkins. p. 1120-1125.
Hrubec, T.C.; Smith, S.A.; Robertson, J.L. 2001. Ageâ€Ârelated changes in hematology and plasma chemistry values of hybrid striped bass (Morone chrysops í"” Morone saxatilis). Veterinary Clinical Pathology, 30(1): 8-15. http://dx.doi.org/10.1111/j.1939-165X.2001.tb00249.x.
IBGE - Instituto Brasileiro de Geografia e Estatística. 2018. Pesquisa da Pecuária Municipal í PPM. Rio de Janeiro: IBGE. Available from: <https://www.ibge.gov.br/estatisticas/economicas/agricultura-e-pecuaria/9107-producao-da-pecuaria-municipal.html?=&t=downloads>. Accessed: Feb. 4, 2020.
Ibrahim, N.; El Naggar, G. 2010. Water quality, fish production and economics of Nile Tilapia, Oreochromis niloticus, and African Catfish, Clarias gariepinus, monoculture and polycultures. Journal of the World Aquaculture Society, 41(4): 574-582. http://dx.doi.org/10.1111/j.1749-7345.2010.00397.x.
Iwama, G.K.; Pickering, A.; Sumpter, J.; Schreck, C. (2011). Fish stress and health in aquaculture. Cambridge: Cambridge University Press. v. 62, 278p.
Levy-Pereira, N.; Yasui, G.S.; Cardozo, M.V.; Dias Neto, J.; Vaz Farias, T.H.; Sakabe, R.; Pádua, S.B.; Pilarski, F. 2018. Immunostimulation and increase of intestinal lactic acid bacteria with dietary mannan-oligosaccharide in Nile tilapia juveniles. Brazilian Journal of Animal Science, 47: 1-7. http://dx.doi.org/10.1590/rbz4720170006.
Magnadóttir, B. 2006. Innate immunity of fish (overview). Fish & Shellfish Immunology, 20(2): 137-151. http://dx.doi.org/10.1016/j.fsi.2004.09.006.
Mansour, M.R.; Akrami, R.; Ghobadi, S.H.; Denji, K.A.; Ezatrahimi, N.; Gharaei, A. 2012. Effect of dietary mannan-oligosaccharide (MOS) on growth performance, survival, body composition, and some hematological parameters in giant sturgeon juvenile (Huso huso Linnaeus, 1754). Fish Physiology and Biochemistry, 38: 829-835. http://dx.doi.org/10.1007/s10695-011-9570-4.
Mauel, M.; Soto, E.; Moralis, J.; Hawke, J. 2007. A piscirickettsiosis-like syndrome in cultured Nile tilapia in Latin America with Francisella spp. as the pathogenic agent. Journal of Aquatic Animal Health, 19(1): 27-34. http://dx.doi.org/10.1577/H06-025.1.
Mian, G.F.; Godoy, D.T.; Leal, C.A.G.; Yuhara, T.Y.; Costa, G.M.; Figueiredo, H.C.P. 2009. Aspects of the natural history and virulence of S. agalactiae infection in Nile tilapia. Veterinary Microbiology, 136(1-2): 180-183. http://dx.doi.org/10.1016/j.vetmic.2008.10.016.
Nakao, M.; Tsujikura, M.; Ichiki, S.; Vo, T.K.; Somamoto, T. 2011. The complement system in teleost fish: Progress of post-homolog-hunting researches. Developmental and Comparative Immunology, 35(12): 1296-1308. http://dx.doi.org/10.1016/j.dci.2011.03.003.
NRC - National Research Council. 1977. Nutrient requirements of warmwater fishes and shellfishes. Washington: National Academy. 80p. https://doi.org/10.17226/20664.
Olsen, R.; Myklebust, R.; Kryvi, H.; Mayhew, T.; Ringí¸, E. 2001. Damaging effect of dietary inulin on intestinal enterocytes in Arctic charr (Salvelinus alpinus L.). Aquaculture Research, 32(11): 931-934. http://dx.doi.org/10.1046/j.1365-2109.2001.00626.x.
Pohlenz, C.; Gatlin, D.M. 2014. Interrelationships between fish nutrition and health. Aquaculture, 431: 111-117. http://dx.doi.org/10.1016/j.aquaculture.2014.02.008.
Quinn, M.T.; Gauss, K.A. 2004. Structure and regulation of the neutrophil respiratory burst oxidase: comparison with nonphagocyte oxidases. Journal of Leukocyte Biology, 76(4): 760-781. https://doi.org/10.1189/jlb.0404216.
Radman, R.; Bland Elliot, J.; Sangworachat, N.; Bucke, C.; Keshavarz, T. 2006. Effects of oligosaccharides and polysaccharides on the generation of reactive oxygen species in different biological systems. Biotechnology and Applied Biochemistry, 44(3): 129-133. http://dx.doi.org/10.1042/BA20050217.
Sado, R.Y.; Bicudo, A.J.D.A.; Cyrino, J.E.P. 2008. Feeding dietary mannan-oligosaccharides to juvenile Nile tilapis, Oreochromis niloticus, has no effect on hematological parameters and showed decreased feed consumption. Journal of the World Aquaculture Society, 39(6): 821-826. http://dx.doi.org/10.1111/j.1749-7345.2008.00219.x.
Saurabh, S.; Sahoo, P. 2008. Lysozyme: an important defence molecule of fish innate immune system. Aquaculture Research, 39(3): 223-239. http://dx.doi.org/10.1111/j.1365-2109.2007.01883.x.
Selim, K.M.; Reda, R.M. 2015. Beta-glucans and mannan-oligosaccharides enhance growth and immunity in Nile Tilapia. North American Journal of Aquaculture, 77(1): 22-30. http://dx.doi.org/10.1080/15222055.2014.951812.
Soares, M.P.; Oliveira, F.C.; Cardoso, I.L.; Urbinati, E.C.; Campos, C.M.; Hisano, H. 2018. Glucan-MOSï"ºÅ¡ improved growth and innate immunity in pacu stressed and experimentally infected with Aeromonas hydrophila. Fish & Shellfish Immunology, 73: 133-140. http://dx.doi.org/10.1016/j.fsi.2017.11.046.
Song, S.K.; Beck, B.R.; Kim, D.; Park, J.; Kim, J.; Kim, H.D.; Ringí¸, E. 2014. Prebiotics as immunostimulants in aquaculture: A review. Fish & Shellfish Immunology, 40(1): 40-48. http://dx.doi.org/10.1016/j.fsi.2014.06.016.
Staykov, Y.; Spring, P.; Denev, S.; Sweetman, J. 2007. Effect of a mannan-oligosaccharide on the growth performance and immune status of rainbow trout (Oncorhynchus mykiss). Aquaculture International, 15: 153-161. http://dx.doi.org/10.1007/s10499-007-9096-z.
Talpur, A.D.; Munir, M.B.; Mary, A.; Hashim, R. 2014. Dietary probiotics and prebiotics improved food acceptability, growth performance, haematology and immunological parameters and disease resistance against Aeromonas hydrophila in snakehead (Channa striata) fingerlings. Aquaculture, 426-427: 14-20. http://dx.doi.org/10.1016/j.aquaculture.2014.01.013.
Tavares-Dias, M.; de Moraes, F.R. 2003. Características hematológicas da Tilapia rendalli Boulenger, 1896 (Osteichthyes: Cichlidae) capturada em†Pesque-Pague†de Franca, São Paulo. Brasil. Bioscience Journal, 19(1): 107-114. Available from: <http://www.seer.ufu.br/index.php/biosciencejournal/article/view/6443>. Accessed: Feb. 4, 2020.
Torrecillas, S.; Makol, A.; Caballero, M.J.; Montero, D.; Gines, R.; Sweetman, J.; Izquierdo, M. 2011. Improved feed utilization, intestinal mucus production and immune parameters in sea bass (Dicentrarchus labrax) fed mannan-oligosaccharides (MOS). Aquaculture Nutrition, 17(2): 223-233. http://dx.doi.org/10.1111/j.1365-2095.2009.00730.x.
Torrecillas, S.; Makol, A.; Caballero, M.J.; Montero, D.; Robaina, L.; Real, F.; Sweetman, J.; Tort, L.; Izquierdo, M.S. 2007. Immune stimulation and improved infection resistance in European sea bass (Dicentrarchus labrax) fed mannan-oligosaccharides. Fish & Shellfish Immunology, 23(5): 969-981. http://dx.doi.org/10.1016/j.fsi.2007.03.007.
Torrecillas, S.; Montero, D.; Izquierdo, M. 2014. Improved health and growth of fish fed mannan-oligosaccharides: Potential mode of action. Fish & Shellfish Immunology, 36(2): 525-544. http://dx.doi.org/10.1016/j.fsi.2013.12.029.
Wintrobe, M.M. 1934. Variations in the size and hemoglobin content of erythrocytes in the blood of various vertebrates. Folia Haematologie, 51: 32-49.
Akrami, R.; Chitsaz, H.; Hezarjaribi, A.; Ziaei, R. 2012. Effect of dietary mannan-oligosaccharide (MOS) on growth performance and immune response of Gibel carp juveniles (Carassius auratus gibelio). Journal of Veterinary Advances, 2(3): 507-513.
Anderson, D.; Siwicki, A. 1995. Basic hematology and serology for fish health programs. In: Shariff, M.; Arthur, J.R.; Subasinghe, R.P. (Eds.). Diseases in Asian Aquaculture II. Manila: Fish Health Section, Asian Fisheries Society. p. 185-102.
Andrews, S.R.; Sahu, N.P.; Pal, A.K.; Kumar, S. 2009. Haematological modulation and growth of Labeo rohita fingerlings: effect of dietary mannan-oligosaccharide, yeast extract, protein hydrolysate and chlorella. Aquaculture Research, 41(1): 61-69. http://dx.doi.org/10.1111/j.1365-2109.2009.02304.x.
Babior, B. 1984. The respiratory burst of phagocytes. The Journal of Clinical Investigation, 73(3): 599-601. http://dx.doi.org/10.1172/JCI111249.
Biller-Takahashi, J.; Takahashi, L.; Saita, M.; Gimbo, R.; Urbinati, E. 2013. Leukocytes respiratory burst activity as indicator of innate immunity of pacu Piaractus mesopotamicus. Brazilian Journal of Biology = Revista Brasileira de Biologia, 73(2): 425-429. http://dx.doi.org/10.1590/S1519-69842013000200026.
Bland, E.J.; Keshavarz, T.; Bucke, C. 2004. The influence of small oligosaccharides on the immune system. Carbohydrate Research, 339(10): 1673-1678. http://dx.doi.org/10.1016/j.carres.2004.05.009.
Collier, H.B. 1944. Standardization of blood haemoglobin determinations. Canadian Medical Association Journal, 50(6): 550-552.
Ellis, A. 1999. Immunity to bacteria in fish. Fish & Shellfish Immunology, 9(4): 291-308. http://dx.doi.org/10.1006/fsim.1998.0192.
FAO - Food and Agriculture Organization of the United Nations. 2016. The State of World Fisheries and Aquaculture: Contributing to food security and nutrition for all. Rome: FAO. 200p.
FAO - Food and Agriculture Organization of the United Nations. 2020. The State of World Fisheries and Aquaculture: Sustainability in action. Rome: FAO. 244p.
Goldenfarb, P.B.; Bowyer, F.P.; Hall, E.; Brosious, E. 1971. Reproducibility in the hematology laboratory: the microhematocrit determination. American Journal of Clinical Pathology, 56(1): 35-39. http://dx.doi.org/ 10.1093/ajcp/56.1.35.
Gómez, G.D.; Balcázar, J.L. 2008. A review on the interactions between gut microbiota and innate immunity of fish. FEMS Immunology and Medical Microbiology, 52(2): 145-154. http://dx.doi.org/10.1111/j.1574-695X.2007.00343.x.
Grisdale-Helland, B.; Helland, S.J.; Gatlin 3rd, D.M. 2008. The effects of dietary supplementation with mannan-oligosaccharide, fructooligosaccharide or galactooligosaccharide on the growth and feed utilization of Atlantic salmon (Salmo salar). Aquaculture (Amsterdam, Netherlands), 283(1-4): 163-167. http://dx.doi.org/10.1016/ j.aquaculture.2008.07.012.
Guzmán, D.M.M.; González, M.T. 2012. Evaluation of somatic indexes, hematology and liver histopathology of the fish Labrisomus philippii from San Jorge Bay, northern Chile, as associated with environmental stress. Revista de Biología Marina y Oceanografía, 47(1): 99-107. http://dx.doi.org/10.4067/S0718-19572012000100009.
Hoidal, J.R. 2001. Reactive oxygen species and cell signaling. American Journal of Respiratory Cell and Molecular Biology, 25(6): 661-663. http://dx.doi.org/10.1165/ajrcmb.25.6.f213.
Hrubec, T.; Smith, S. 2000. Hematology of fish. In: Schalm, O.W.; Jain, N.C.; Carroll, E.J. Schalm’s veterinary hematology. Philadelphia: Lippincott Williams and Wilkins. p. 1120-1125.
Hrubec, T.C.; Smith, S.A.; Robertson, J.L. 2001. Ageâ€Ârelated changes in hematology and plasma chemistry values of hybrid striped bass (Morone chrysops í"” Morone saxatilis). Veterinary Clinical Pathology, 30(1): 8-15. http://dx.doi.org/10.1111/j.1939-165X.2001.tb00249.x.
IBGE - Instituto Brasileiro de Geografia e Estatística. 2018. Pesquisa da Pecuária Municipal í PPM. Rio de Janeiro: IBGE. Available from: <https://www.ibge.gov.br/estatisticas/economicas/agricultura-e-pecuaria/9107-producao-da-pecuaria-municipal.html?=&t=downloads>. Accessed: Feb. 4, 2020.
Ibrahim, N.; El Naggar, G. 2010. Water quality, fish production and economics of Nile Tilapia, Oreochromis niloticus, and African Catfish, Clarias gariepinus, monoculture and polycultures. Journal of the World Aquaculture Society, 41(4): 574-582. http://dx.doi.org/10.1111/j.1749-7345.2010.00397.x.
Iwama, G.K.; Pickering, A.; Sumpter, J.; Schreck, C. (2011). Fish stress and health in aquaculture. Cambridge: Cambridge University Press. v. 62, 278p.
Levy-Pereira, N.; Yasui, G.S.; Cardozo, M.V.; Dias Neto, J.; Vaz Farias, T.H.; Sakabe, R.; Pádua, S.B.; Pilarski, F. 2018. Immunostimulation and increase of intestinal lactic acid bacteria with dietary mannan-oligosaccharide in Nile tilapia juveniles. Brazilian Journal of Animal Science, 47: 1-7. http://dx.doi.org/10.1590/rbz4720170006.
Magnadóttir, B. 2006. Innate immunity of fish (overview). Fish & Shellfish Immunology, 20(2): 137-151. http://dx.doi.org/10.1016/j.fsi.2004.09.006.
Mansour, M.R.; Akrami, R.; Ghobadi, S.H.; Denji, K.A.; Ezatrahimi, N.; Gharaei, A. 2012. Effect of dietary mannan-oligosaccharide (MOS) on growth performance, survival, body composition, and some hematological parameters in giant sturgeon juvenile (Huso huso Linnaeus, 1754). Fish Physiology and Biochemistry, 38: 829-835. http://dx.doi.org/10.1007/s10695-011-9570-4.
Mauel, M.; Soto, E.; Moralis, J.; Hawke, J. 2007. A piscirickettsiosis-like syndrome in cultured Nile tilapia in Latin America with Francisella spp. as the pathogenic agent. Journal of Aquatic Animal Health, 19(1): 27-34. http://dx.doi.org/10.1577/H06-025.1.
Mian, G.F.; Godoy, D.T.; Leal, C.A.G.; Yuhara, T.Y.; Costa, G.M.; Figueiredo, H.C.P. 2009. Aspects of the natural history and virulence of S. agalactiae infection in Nile tilapia. Veterinary Microbiology, 136(1-2): 180-183. http://dx.doi.org/10.1016/j.vetmic.2008.10.016.
Nakao, M.; Tsujikura, M.; Ichiki, S.; Vo, T.K.; Somamoto, T. 2011. The complement system in teleost fish: Progress of post-homolog-hunting researches. Developmental and Comparative Immunology, 35(12): 1296-1308. http://dx.doi.org/10.1016/j.dci.2011.03.003.
NRC - National Research Council. 1977. Nutrient requirements of warmwater fishes and shellfishes. Washington: National Academy. 80p. https://doi.org/10.17226/20664.
Olsen, R.; Myklebust, R.; Kryvi, H.; Mayhew, T.; Ringí¸, E. 2001. Damaging effect of dietary inulin on intestinal enterocytes in Arctic charr (Salvelinus alpinus L.). Aquaculture Research, 32(11): 931-934. http://dx.doi.org/10.1046/j.1365-2109.2001.00626.x.
Pohlenz, C.; Gatlin, D.M. 2014. Interrelationships between fish nutrition and health. Aquaculture, 431: 111-117. http://dx.doi.org/10.1016/j.aquaculture.2014.02.008.
Quinn, M.T.; Gauss, K.A. 2004. Structure and regulation of the neutrophil respiratory burst oxidase: comparison with nonphagocyte oxidases. Journal of Leukocyte Biology, 76(4): 760-781. https://doi.org/10.1189/jlb.0404216.
Radman, R.; Bland Elliot, J.; Sangworachat, N.; Bucke, C.; Keshavarz, T. 2006. Effects of oligosaccharides and polysaccharides on the generation of reactive oxygen species in different biological systems. Biotechnology and Applied Biochemistry, 44(3): 129-133. http://dx.doi.org/10.1042/BA20050217.
Sado, R.Y.; Bicudo, A.J.D.A.; Cyrino, J.E.P. 2008. Feeding dietary mannan-oligosaccharides to juvenile Nile tilapis, Oreochromis niloticus, has no effect on hematological parameters and showed decreased feed consumption. Journal of the World Aquaculture Society, 39(6): 821-826. http://dx.doi.org/10.1111/j.1749-7345.2008.00219.x.
Saurabh, S.; Sahoo, P. 2008. Lysozyme: an important defence molecule of fish innate immune system. Aquaculture Research, 39(3): 223-239. http://dx.doi.org/10.1111/j.1365-2109.2007.01883.x.
Selim, K.M.; Reda, R.M. 2015. Beta-glucans and mannan-oligosaccharides enhance growth and immunity in Nile Tilapia. North American Journal of Aquaculture, 77(1): 22-30. http://dx.doi.org/10.1080/15222055.2014.951812.
Soares, M.P.; Oliveira, F.C.; Cardoso, I.L.; Urbinati, E.C.; Campos, C.M.; Hisano, H. 2018. Glucan-MOSï"ºÅ¡ improved growth and innate immunity in pacu stressed and experimentally infected with Aeromonas hydrophila. Fish & Shellfish Immunology, 73: 133-140. http://dx.doi.org/10.1016/j.fsi.2017.11.046.
Song, S.K.; Beck, B.R.; Kim, D.; Park, J.; Kim, J.; Kim, H.D.; Ringí¸, E. 2014. Prebiotics as immunostimulants in aquaculture: A review. Fish & Shellfish Immunology, 40(1): 40-48. http://dx.doi.org/10.1016/j.fsi.2014.06.016.
Staykov, Y.; Spring, P.; Denev, S.; Sweetman, J. 2007. Effect of a mannan-oligosaccharide on the growth performance and immune status of rainbow trout (Oncorhynchus mykiss). Aquaculture International, 15: 153-161. http://dx.doi.org/10.1007/s10499-007-9096-z.
Talpur, A.D.; Munir, M.B.; Mary, A.; Hashim, R. 2014. Dietary probiotics and prebiotics improved food acceptability, growth performance, haematology and immunological parameters and disease resistance against Aeromonas hydrophila in snakehead (Channa striata) fingerlings. Aquaculture, 426-427: 14-20. http://dx.doi.org/10.1016/j.aquaculture.2014.01.013.
Tavares-Dias, M.; de Moraes, F.R. 2003. Características hematológicas da Tilapia rendalli Boulenger, 1896 (Osteichthyes: Cichlidae) capturada em†Pesque-Pague†de Franca, São Paulo. Brasil. Bioscience Journal, 19(1): 107-114. Available from: <http://www.seer.ufu.br/index.php/biosciencejournal/article/view/6443>. Accessed: Feb. 4, 2020.
Torrecillas, S.; Makol, A.; Caballero, M.J.; Montero, D.; Gines, R.; Sweetman, J.; Izquierdo, M. 2011. Improved feed utilization, intestinal mucus production and immune parameters in sea bass (Dicentrarchus labrax) fed mannan-oligosaccharides (MOS). Aquaculture Nutrition, 17(2): 223-233. http://dx.doi.org/10.1111/j.1365-2095.2009.00730.x.
Torrecillas, S.; Makol, A.; Caballero, M.J.; Montero, D.; Robaina, L.; Real, F.; Sweetman, J.; Tort, L.; Izquierdo, M.S. 2007. Immune stimulation and improved infection resistance in European sea bass (Dicentrarchus labrax) fed mannan-oligosaccharides. Fish & Shellfish Immunology, 23(5): 969-981. http://dx.doi.org/10.1016/j.fsi.2007.03.007.
Torrecillas, S.; Montero, D.; Izquierdo, M. 2014. Improved health and growth of fish fed mannan-oligosaccharides: Potential mode of action. Fish & Shellfish Immunology, 36(2): 525-544. http://dx.doi.org/10.1016/j.fsi.2013.12.029.
Wintrobe, M.M. 1934. Variations in the size and hemoglobin content of erythrocytes in the blood of various vertebrates. Folia Haematologie, 51: 32-49.
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2020-12-14
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