Effects of Single and Combined Supplementation of Dietary Probiotic with Bovine Lactoferrin and Xylooligosaccharide on Hemato-Immunological and Digestive Enzymes of Silvery-Black Porgy (Sparidentex hasta) Fingerlings

Aachary A.A., Prapulla S.G. (2011). Xylooligosaccharides (XOS) as an emerging prebiotic: microbial synthesis, utilization, structural characterization, bioactive properties, and applications. Comp. Rev. Food Sci. Food Saf., 10: 1–16.10.1111/j.1541-4337.2010.00135.xSearch in Google Scholar

Abdel-Tawwab M., Khattab Y.A., Ahmad M.H., Shalaby A.M. (2006). Compensatory growth, feed utilization, whole-body composition, and hematological changes in starved juvenile Nile tilapia, Oreochromis niloticus (L.). J. Appl. Aquacult., 18: 17–36.10.1300/J028v18n03_02Search in Google Scholar

Abdel-Tawwab M., Abdel-Rahman A.M., Ismael N.E.M. (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: 185–189.10.1016/j.aquaculture.2008.03.055Search in Google Scholar

Ahmadifar E., Sheikhzadeh N., Roshanaei K., Dargahi N., Faggio C. (2019). Can dietary ginger (Zingiber officinale) alter biochemical and immunological parameters and gene expression related to growth, immunity and antioxidant system in zebrafish (Danio rerio)? Aquaculture, 507: 341–348.10.1016/j.aquaculture.2019.04.049Search in Google Scholar

Akhter N., Wu B., Memon A.M., Mohsin M. (2015). Probiotics and prebiotics associated with aquaculture. A review. Fish Shellfish Immunol., 45: 733–741.10.1016/j.fsi.2015.05.038Search in Google Scholar

Alejo A., Tafalla C. (2011). Chemokines in teleost fish species. Develop. Comparativ. Immunol., 35: 1215–1222.10.1016/j.dci.2011.03.011Search in Google Scholar

Andrews S.R., Sahu N.P., Pal A.K., Kumar S. (2009). Hematological modulation and growth of Labeo rohita fingerlings: effect of dietary mannanoligosaccharide, yeast extract, protein hydrolysate and chlorella. Aquacult. Res., 41: 61–69.10.1111/j.1365-2109.2009.02304.xSearch in Google Scholar

Ashouri G., Yavari V., Bahmani M., Yazdani M.A., Kazemi R., Morshedi V., Fatollahi M. (2013). The effect of short-term starvation on some physiological and morphological parameters in juvenile Siberian sturgeon, Acipenser baerii (Actinopterygii: Acipenseriformes: Acipenseridae). Acta Ichthyol. Piscator., 43: 144–149.10.3750/AIP2013.43.2.07Search in Google Scholar

Association of Official Analytical Chemists (1995). Official Methods of Analysis of AOAC International, 18th ed., AOAC International, Arlington, USA.Search in Google Scholar

Azimirad M., Meshkini S., Ahmadifard N., Hoseinifar S.H. (2016). The effects of feeding with synbiotic (Pediococcus acidilactici and fructooligosaccharide) enriched adult artemia on skin mucus immune responses, stress resistance, intestinal microbiota and performance of angel-fish (Pterophyllum scalare). Fish Shellfish Immunol., 54: 516–522.10.1016/j.fsi.2016.05.001Search in Google Scholar

Azodi M., Ebrahimi E., Motaghi E., Morshedi V. (2015). Metabolic responses to short starvation and re-feeding in rainbow trout (Oncorhynchus mykiss). Ichthyolog. Res., 62: 177–183.10.1007/s10228-014-0421-zSearch in Google Scholar

Basurco B., Lovatelli A., Garcıa B. (2011). Current status of Sparidae aquaculture. In: Sparidae: Biology and aquaculture of gilthead sea bream and other species, Pavlidis M., Mylonas C. (eds). Oxford, UK, Wiley-Blackwell Scientific Publications, pp. 1–50.10.1002/9781444392210.ch1Search in Google Scholar

Blaxhall P.C., Daisley K.W. (1973). Routine hematological methods for use fish with blood. J. Fish Biol., 5: 771–781.10.1111/j.1095-8649.1973.tb04510.xSearch in Google Scholar

Bradford M.M. (1976). A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytic. Biochem., 72: 248–254.10.1006/abio.1976.9999Search in Google Scholar

Carnevali O., Vivo L., Sulpizio R., Gioacchini G., Olivotto I., Silvi S., Cresci A. (2006). Growth improvement by probiotic in European sea bass juveniles (Dicentrarchus labrax L.), with particular attention to IGF-1, myostatin and cortisol gene expression. Aquaculture, 258: 430–438.10.1016/j.aquaculture.2006.04.025Search in Google Scholar

Cerezuela R., Cuesta A., Meseguer J. (2008). Effects of inulin on gilthead seabream (Sparus aurata) innate immune parameters. Aquaculture, 24: 663–668.10.1016/j.fsi.2007.10.002Search in Google Scholar

Chang C.I., Liu W.Y. (2002). An evaluation of two probiotic bacterial strains, Enterococcus faecium SF68 and Bacillus toyoi, for reducing edwardsiellosis in cultured European eel, Anguilla anguilla L. J. Fish Dis., 25: 311–315.10.1046/j.1365-2761.2002.00365.xSearch in Google Scholar

Chitsaz H., Akrami R., Arab Arkadeh M. (2016). Effect of dietary synbiotics on growth, immune response and body composition of Caspian roach (Rutilus rutilus). Iran. J. Fish. Sci., 15: 170–182.Search in Google Scholar

Chong A.S.C., Hashim R., Lee C.Y., Ali B.A. (2002). Partial characterization and activities of proteases form the digestive tract of discus fish (Symphysodon aequifasciata). Aquaculture, 203: 321–333.10.1016/S0044-8486(01)00630-5Search in Google Scholar

Dawood M.A.O., Koshio S., Ishikawa M., Yokoyama S. (2015). Interaction effects of dietary supplementation of heat-killed Lactobacillus plantarum and β-glucan on growth performance, digestibility and immune response of juvenile red sea bream, Pagrus major. Fish Shellfish Immunol., 45: 33–42.10.1016/j.fsi.2015.01.033Search in Google Scholar

Dawood M.A.O., Koshio S., Esteban M.A. (2018). Beneficial roles of feed additives as immunostimulants in aquaculture: a review. Rev. Aquacult., 10: 950–974.10.1111/raq.12209Search in Google Scholar

Dimitroglou A., Merrifield D.L., Spring P., Sweetman J., Moate R., Davies S.J. (2010). Effects of mannan oligosaccharide (MOS) supplementation on growth performance, feed utilization, intestinal histology and gut microbiota of gilthead sea bream (Sparus aurata). Aquaculture, 300: 182–188.10.1016/j.aquaculture.2010.01.015Search in Google Scholar

Ellis A.E. (1990). Serum antiproteases in fish and lysozyme assays. In: Techniques in fish immunology, Stolen J.S., Fletcher T.C., Anderson D.P., Roberson B.S., Van Muiswinkel W.B. (eds). Fair Haven NJ, SOS Publications, pp. 95–103.Search in Google Scholar

Eslamloo K., Falahatkar B., Yokoyama S. (2012). Effects of dietary bovine lactoferrin on growth, physiological performance, iron metabolism and non-specific immune responses of Siberian sturgeon Acipenser baeri. Fish Shellfish Immunol., 32: 976–985.10.1016/j.fsi.2012.02.007Search in Google Scholar

Esteban M.A., Rodriguez A., Cuesta A., Meseguer J. (2005). Effects of lactoferrin on non-specific immune responses of gilthead seabream Sparus aurata. Fish Shellfish Immunol., 18: 109–124.10.1016/j.fsi.2004.06.003Search in Google Scholar

Faggio C., Fazio F., Marafioti S., Arfuso F., Piccione G. (2015). Oral administration of Gum Arabic: effects on haematological parameters and oxidative stress markers in Mugil cephalus. Iran. J. Fish. Sci., 14: 60–72.Search in Google Scholar

Falahatkar B., Eslamloo K., Yokoyama S. (2014). Suppression of stress responses in Siberian sturgeon, Acipenser baeri, juveniles by the dietary administration of bovine lactoferrin. J. World Aquacult. Soc., 45: 699–708.10.1111/jwas.12153Search in Google Scholar

Garcia - Carreño F.L., Haard N.F. (1993). Characterization of proteinase classes in langostilla (Pleuroncodes planipes) and crayfish (Pacifastacus astacus) extracts. J. Food Biochem., 17: 97–113.10.1111/j.1745-4514.1993.tb00864.xSearch in Google Scholar

Geraylou Z., Souffreau C., Rurangwa E., D’Hondt S., Callewaert L., Courtin C.M., Delcour J.A., Buyse J., Ollevier F. (2012). Effects of arabinoxylan-oligosaccharides (AXOS) on juvenile Siberian sturgeon (Acipenser baerii) performance, immune responses and gastrointestinal microbial community. Fish Shellfish Immunol., 33: 718–724.10.1016/j.fsi.2012.06.010Search in Google Scholar

Giansanti F., Panella G., Leboffe L., Antonini G. (2016). Lactoferrin from milk: nutraceutical and pharmacological properties. Pharmaceuticals, 9: 61.10.3390/ph9040061Search in Google Scholar

Grisdale-Helland B.G., Helland S.J., Gatlin D.M. (2008). The effect of dietary supplementation with mannanoligosacchare, fructooligosaccharide or galactooligosaccharide on the growth Atlantic salmon (Salmo salar). Aquaculture, 283: 163–167.10.1016/j.aquaculture.2008.07.012Search in Google Scholar

Guan Y., Zhou H., Wang Z. (2011). Effects of xylooligosaccharide on growth performance, activities of digestive enzymes, and intestinal microflora of juvenile Pelodiscus sinensis. Front. Agric. China, 5: 612–617.10.1007/s11703-011-1129-8Search in Google Scholar

Guzmán-Villanueva L.T., Tovar-Ramírez D., Gisbert E., Cordero H., Guardiola F.A., Cuesta A., Meseguer J., Ascencio-Valle F., Esteban M.A. (2014). Dietary administration of beta-1,3/1,6-glucan and probiotic strain Shewanella putrefaciens, single or combined, on gilthead seabream growth, immune responses and gene expression. Fish Shellfish Immunol., 39: 34–41.10.1016/j.fsi.2014.04.024Search in Google Scholar

Hoseinifar S.H., Mirvaghefi A., Mojazi Amiri B., Khoshbavar Rostami H., Merrifield D.L. (2011). The effects of oligofructose on growth performance, survival and autochthonous intestinal microbiota of beluga (Huso huso) juveniles. Aquacult. Nutr., 17: 498–504.10.1111/j.1365-2095.2010.00828.xSearch in Google Scholar

Hoseinifar S.H., Sharifian M., Vesaghi M.J., Khalili M., Esteban M.A. (2014). The effects of dietary xylooligosaccharide on mucosal parameters, intestinal microbiota and morphology and growth performance of Caspian white fish (Rutilus frisiikutum) fry. Fish Shellfish Immunol., 39: 231–236.10.1016/j.fsi.2014.05.009Search in Google Scholar

Hoseinifar S.H., Yousefi S., Capillo G., Paknejad H., Khalili M., Tabarraei A., Van Doan H., Spanò N., Faggio C. (2018). Mucosal immune parameters, immune and antioxidant defense related genes expression and growth performance of zebrafish (Danio rerio) fed on Gracilaria gracilis powder. Fish Shellfish Immunol., 83: 232–237.10.1016/j.fsi.2018.09.046Search in Google Scholar

Iijima N., Tanaka S., Ota Y. (1998). Purification and characterization of bile salt activated lipase from the hepatopancreas of red sea bream, Pagrus major. Fish Physiol. Biochem., 18: 59–69.Search in Google Scholar

Irianto A., Austin B. (2002). Use of probiotics to control furunculosis in rainbow trout, Oncorhynchus mykiss (Walbaum). J. Fish Dis., 25: 333–342.10.1046/j.1365-2761.2002.00375.xSearch in Google Scholar

Kakuta I. (1996). Effect of orally administrated bovine lactoferrin on growth and blood properties of goldfish. Suisanzoshoku, 44: 419–426.Search in Google Scholar

Kawakami H., Hiratsuka M., Dosako S. (1988). Effects of iron-saturated lactoferrin on iron absorption. Agric. Biol. Chem., 52: 903–908.10.1080/00021369.1988.10868784Search in Google Scholar

Khademi F., Sajadi M.M., Sourinejad I., Daryai R., Kondor A.T. (2013). Effects of dietary Protexin supplementation on growth performance and survival of sobaity (Sparidentex hasta) (in Persian). J. Aquacult., 3: 65–78.Search in Google Scholar

Kumari J., Swain T., Sahoo P.K. (2003). Dietary bovine lactoferrin induces changes in immunity level and disease resistance in Asian catfish Clarias batrachus. Vet. Immunol. Immunopathol., 94: 1–9.10.1016/S0165-2427(03)00065-5Search in Google Scholar

Lee W., Ahn J.Y., Oh S.M., Kim N., Kang E.A., Kim K.-N., Kim J.B., Jeong Y.-J., Jeon A. (2016). Prebiotic effect of Ecklonia cava on the growth and mortality of olive flounder infected with pathogenic bacteria. Fish Shellfish Immunol., 51: 313–320.10.1016/j.fsi.2016.02.030Search in Google Scholar

Liu W., Ran C., Liu Z., Gao Q., Xu S., Ringø E., Myklebust R., Gu Z., Zhou Z. (2016). Effects of dietary Lactobacillus plantarum and AHL lactonase on the control of Aeromonas hydrophila infection in tilapia. Microbiol. Open, 5: 687–699.10.1002/mbo3.362Search in Google Scholar

Livak K.J., Schmittgen T.D. (2001). Analysis of relative gene expression data using real-time quantitative PCR and the 2− ΔΔCT method. Methods, 25: 402–408.10.1006/meth.2001.1262Search in Google Scholar

Lonnerdal B. (2009). Nutritional roles of lactoferrin. Curr. Opin. Clin. Nutr., 12: 293–297.10.1097/MCO.0b013e328328d13eSearch in Google Scholar

Lygren B., Sveier H., Hjeltnes B., Waagbø R. (1999). Examination of the immunomodula-tory properties and the effect on disease resistance of dietary bovine lactoferrin and vitamin C fed to Atlantic salmon (Salmo salar) for a short-term period. Fish Shellfish Immunol., 9: 95–107.10.1006/fsim.1998.0179Search in Google Scholar

Mohammadian T., Alishahi M., Tabandeh M.R., Ghorbanpoor M., Gharibi D. (2017). Effect of Lactobacillus plantarum and Lactobacillus delbrueckii subsp. bulgaricus on growth performance, gut microbial flora and digestive enzymes activities in Tor grypus (Karaman, 1971). Iran. J. Fish. Sci., 16: 296–317.Search in Google Scholar

Mohapatra S., Chakrabory T., Prusty A.K., Das P., Paniprasad K., Mohanta K.N. (2012). Use of different microbial probiotics in the diet of rohu, Labeo rohita fingerlings: effects on growth, nutrient digestibility and retention, digestive enzyme activities and intestinal microflora. Aquacult. Nutr., 18: 1–11.10.1111/j.1365-2095.2011.00866.xSearch in Google Scholar

Moradian A.M., Dorafshan S., Paykan Heyrati F., Ebrahimi E. (2018). Effects of dietary bovine lactoferrin on growth, haemato-biochemical parameters, immune functions and tolerance to air exposure stress in the African cichlid Sciaenochromis fryeri. Aquacult. Nutr., 24: 392–399.10.1111/anu.12570Search in Google Scholar

Morshedi V., Agh N., Marammazi J., Noori F., Mohammadian T. (2015). Effects of dietary lactoferrin on growth performance, feed utilization, hematological and non-specific immune responses in sobaity (Sparidentex hasta) fingerling (in Persian). J. Anim. Environ., 2: 189–198.Search in Google Scholar

Morshedi V., Agh N., Marammazi J., Noori F., Mohammadian T. (2016 a). Effects of different levels of dietary lactoferrin on digestive enzymes, body composition and intestine bacterial flora of sobaity (Sparidentex hasta) fingerling (in Persian). Vet. J., 113: 65–74.Search in Google Scholar

Morshedi V., Agh N., Marammazi J., Noori F., Mohammadian T. (2016 b). Evaluation of digestive enzymes activities, carcass biochemical composition and gut bacterial flora in sobaity (Sparidentex hasta) fingerlings in response to different dietary xylooligosaccharide levels (in Persian). Anim. Physiol. Dev., 8: 37–47.Search in Google Scholar

Morshedi V., Agh N., Marammazi J., Noori F., Mohammadian T. (2016 c). Effects of dietary xylooligosaccharide on growth and feed utilization, hematological and non-especific immune parameters of sobaity (Sparidentex hasta) fingerlings (in Persian). J. Marine Biol., 26: 69–82.Search in Google Scholar

Mozanzadeh M.T., Marammazi J.G., Yaghoubi M., Agh N., Pagheh E., Gisbert E. (2017). Macronutrient requirements of silvery-black porgy (Sparidentex hasta): A comparison with other farmed sparid species. Fishes, 2: 5.10.3390/fishes2010005Search in Google Scholar

Mussatto S.I., Mancilha I.M. (2007). Non-digestible oligosaccharides: a review. Carbohyd. Polym., 68: 587–597.10.1016/j.carbpol.2006.12.011Search in Google Scholar

Nekoubin H., Sudagar M. (2012). Assessment of the effects of synbiotic (Biomin Imbo) via supplementation with artificial diet (with different protein levels) on growth performance and survival rate in grass carp (Ctenopharyngodon idella). World J. Zool., 7: 236–240.Search in Google Scholar

Nguyen D.N., Li Y., Sangild P.T., Bering S.B., Chatterton D.E.W. (2014). Effects of bovine lactoferrin on the immature porcine intestine. Brit. J. Nutr., 111: 321–331.10.1017/S0007114513002456Search in Google Scholar

Pagheh E., Marammazi J.G., Agh N., Nouri F., Sepahdari A., Gisbert E., Mozanzadeh M.T. (2018). Growth performance, hemato-immunological responses and digestive enzymes activities in silvery-black porgy (Sparidentex hasta) fed dietary bovine lactoferrin. Prob. Antimicrob. Prot., 10: 399–407.10.1007/s12602-017-9340-4Search in Google Scholar

Rahimnejad S., Agh N., Kalbassi M.R., Khosravi S. (2012). Effect of dietary bovine lactoferrin on growth, haematology and non-specific immune response in rainbow trout (Oncorhynchus mykiss). Aquacult. Res., 43: 1451–1459.10.1111/j.1365-2109.2011.02947.xSearch in Google Scholar

Ray A.K., Ghosh K., Ringø E. (2012). Enzyme-producing bacteria isolated from fish gut: a review. Aquacult. Nutr., 18: 465–492.10.1111/j.1365-2095.2012.00943.xSearch in Google Scholar

Ren T., Koshio S., Ishikawa M., Yokoyama S., Micheal F.R., Uyan O., Tung T.H. (2007). Influence of dietary vitamin C and bovine lactoferrin on blood chemistry and non-specific immune responses of Japanese eel, Anguilla japonica. Aquaculture, 267: 31–37.10.1016/j.aquaculture.2007.03.033Search in Google Scholar

Ringo E., Faggio C., Chitmanat C., Doan H., Mai N.T., Jaturasitha S., Hoseinifar S.H. (2018). Effects of corncob derived xylooligosaccharide on innate immune response, disease resistance, and growth performance in Nile tilapia (Oreochromis niloticus) fingerlings. Aqua-culture, 495: 786–793.10.1016/j.aquaculture.2018.06.068Search in Google Scholar

Rodriguez-Estrada U., Satoh S., Haga Y., Fushimi H., Sweetman J. (2009). Effects of single and combined supplementation of Enterococcus faecalis, mannanoligosaccharide and polyhydrobutyric acid on growth performance and immune response of rainbow trout Oncorhynchus mykiss. Suisanzoshoku, 57: 609–617.Search in Google Scholar

Sado R.Y., Bicudo A.J.D.A., Cyrno J.E.P. (2008). Feeding dietary mannanoligosaccharide to juvenile Nile tilapia (Oreochromis niloticus), has no effect on hematological parameters and showed decreased feed consumption. J. World Aquacult. Soc., 39: 821–826.10.1111/j.1749-7345.2008.00219.xSearch in Google Scholar

Siwicki A.K., Anderson D.P., Rumsey G.L. (1994). Dietary intake of immunostimulants by rainbow trout affects non-specific immunity and protection against furunculosis. Vet. Immunol. Immunopathol., 41: 125–139.10.1016/0165-2427(94)90062-0Search in Google Scholar

Son V.M., Chang C.C., Wu M.C., Guu Y.K., Chiu CH., Cheng W. (2009). Dietary administration of the probiotic, Lactobacillus plantarum, enhanced the growth, innate immune responses, and disease resistance of the grouper Epinephelus coioides. Fish Shellfish Immunol., 26: 691–698.10.1016/j.fsi.2009.02.018Search in Google Scholar

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. Aqua-culture, 426: 14–20.10.1016/j.aquaculture.2014.01.013Search in Google Scholar

Tort L., Gómez E., Montero D., Sunyer J.O. (1996). Serum haemolytic and agglutinating activity as indicators of fish immunocompetence: their suitability in stress and dietary studies. Aqua-cult. Int., 4: 31–41.10.1007/BF00175219Search in Google Scholar

Vallejos-Vidal E., Reyes-López F., Teles M., MacKenzie S. (2016). The response of fish to immunostimulant diets. Fish Shellfish Immunol., 56: 34–69.10.1016/j.fsi.2016.06.028Search in Google Scholar

Van Doan H., Doolgindachbaporn S., Suksri A. (2014). Effects of low molecular weight agar and Lactobacillus plantarumon growth performance, immunity, and disease resistance of basafish (Pangasius bocourti, Sauvage 1880). Fish Shellfish Immunol., 41: 340–345.10.1016/j.fsi.2014.09.015Search in Google Scholar

Van Doan H., Hoseinifar S.H., Tapingkae W., Tongsiri S., Khamtavee P. (2016). Combined administration of low molecular weight sodium alginate boosted immunomodulatory, disease resistance and growth enhancing effects of Lactobacillus plantarum in Nile tilapia (Oreochromis niloticus). Fish Shellfish Immunol., 58: 678–685.10.1016/j.fsi.2016.10.013Search in Google Scholar

Wang W., Sun J., Liu C., Xue Z. (2017). Application of immunostimulants in aquaculture: current knowledge and future perspectives. Aquacult. Res., 48: 1–23.10.1111/are.13161Search in Google Scholar

Welker T.L., Lim C., Yildirim-Aksoy M., Klesius P.H. (2007). Growth, immune function, and disease and stress resistance of juvenile Nile tilapia (Oreochromis niloticus) fed graded levels of bovine lactoferrin. Aquaculture. 262: 156–162.10.1016/j.aquaculture.2006.09.036Search in Google Scholar

Welker T.L., Lim C., Yildirim-Aksoy M., Klesius P.H. (2010). Dietary bovine lactoferrin increases resistance of juvenile channel catfish, Ictalurus punctatus, to enteric septicemia. J. World Aquacult. Soc., 41: 28–39.10.1111/j.1749-7345.2009.00330.xSearch in Google Scholar

Worthington C. (1991).Worthington Enzyme Manual: Enzymes and Related Biochemicals. Free-hold, New Jersey, USA.Search in Google Scholar

Xu B., Wang Y., Li J., Lin Q. (2009). Effect of prebiotic xylooligosaccharides on growth performances and digestive enzyme activities of allogynogenetic crucian carp (Carassius auratus gibelio). Fish Physiol. Biochem., 35: 351–357.10.1007/s10695-008-9248-8Search in Google Scholar

Yokoyama S., Koshio S., Takakura N., Oshida K., Ishikawa M., Gallardo Cigarroa F.J., Teshima S. (2005). Dietary bovine lactoferrin enhances tolerance to high temperature stress in Japanese flounder Paralichthys olivaceus. Aquaculture, 249: 367–373.10.1016/j.aquaculture.2005.03.024Search in Google Scholar

Yokoyama S., Koshio S., Takakura N., Oshida K., Ishikawa M., Gallardo Cigarroa F.J., Catacutan M.R., Teshima S. (2006). Effect of dietary bovine lactoferrin on growth response, tolerance to air exposure and low salinity stress conditions in orange spotted grouper Epinephelus coioides. Aquaculture, 255: 507–513.10.1016/j.aquaculture.2005.12.001Search in Google Scholar