Abstract
In the current experiment the effects of brown seaweeds (Sargassum aquifolium, SA) on blood biochemical, antioxidant, innate immune, and mRNA gene expression responses of Tilapia (Oreochromis niloticus) under high stocking rate were examined. The fish were allocated into equal six experimental groups: low stocking density (LSD) (the fish reared at 10 g L−1 and fed an un-supplemented diet), High stocking density (HSD) (the fish reared at 20 g L−1 and fed an un-supplemented diet), HSD + SA50, HSD + SA100, HSD + SA150, and HSD + SA200 (the fish reared at 20 g L−1 and fed Sargassum-supplemented diet at level 50, 100, 150, 200 g kg−1, respectively). After 56 days of the feeding trial, the fish at the HSD treatment revealed remarkedly reduced growth and feed efficiency compared to those at the LSD treatment, but the HSD + SA50 and HSD + SA100 fish groups showed a marked enhancement in performance and efficiency of consumed diets comparable to the LSD treatment. Under overcrowded stress, the fish fed diets enriched with Sargassum significantly diminished ammonia releasing levels within the entire environment. Serum total protein, albumin, liver enzymes, and lipase levels had significantly improved in HSD + SA150 and HSD + SA200 fish groups compared to those in the HSD treatment. Superoxide dismutase, catalase, and glutathione peroxidase exhibited high values at HSD + SA200- and LSD-treated groups than the HSD-treated group. However, HSD suppressed all plasma antioxidant activity. The high stocking rate remarkedly recorded higher plasma malondialdehyde levels, and Sargassum treatments significantly alleviated such increases. The HSD and HSD + SA50 fish groups significantly reduced plasma lysozyme, complement C3, IgA, and IgM levels and revealed higher intestinal aerobic and anaerobic bacterial counts than those at the LSD treatment; however, enriched tilapia diets with a high level of Sargassum diminished these negative effects. The HSD fish group significantly upregulated the expression of tumor necrosis factor-alpha (TNF-a), and downregulated interleukin 10 (IL10), catalase (CAT), and glutathione (GST) genes. Sargassum dietary administration, specifically at 50 g kg−1 level notably alleviated the adverse effects of high stocking rate on the cytokines. In conclusion, enriched tilapia diets with Sargassum treatment at levels ranging from 50 up to 100 g kg−1 alleviated overcrowded stress, oxidative stress, and immunosuppression caused by high stocking rate in Tilapia (O. niloticus).
Similar content being viewed by others
Data availability
The authors confirm that the data supporting the findings of this study are available upon reasonable request from the corresponding author.
References
Abdel-Tawwab M, Hagras AE, Elbaghdady HAM, Monier MN (2014) Dissolved oxygen level and stocking density effects on growth, feed utilization, physiology, and innate immunity of Nile Tilapia, Oreochromis niloticus. J Appl Aquacult 26:340–355
Abdelghany MF, El-Sawy HB, Abd El-hameed SA, Khames MK, Abdel-Latif HM, Naiel MA (2020) Effects of dietary Nannochloropsis oculata on growth performance, serum biochemical parameters, immune responses, and resistance against Aeromonas veronii challenge in Nile tilapia (Oreochromis niloticus). Fish Shellfish Immunol 107:277–288
Abdelhamid FM, Elshopakey GE, Aziza AE (2020) Ameliorative effects of dietary Chlorella vulgaris and β-glucan against diazinon-induced toxicity in Nile tilapia (Oreochromis niloticus). Fish Shellfish Immunol 96:213–222
Abd El-hameed SA, Negm SS, Ismael NE, Naiel MA, Soliman MM, Shukry M, Abdel-Latif HM (2021) Effects of activated charcoal on growth, immunity, oxidative stress markers, and physiological responses of Nile tilapia exposed to sub-lethal imidacloprid toxicity. Animals 11:1357
Abo-Al-Ela HG, El-Nahas AF, Mahmoud S, Ibrahim EM (2017) The extent to which immunity, apoptosis and detoxification gene expression interact with 17 alpha-methyl-testosterone. Fish Shellfish Immunol 60:289–298
Adeshina I, Jenyo-Oni A, Emikpe B (2016) Use of Eugenia cayrophyllata oil as anaesthetic in farm raised african catfish Clarias gariepinus juveniles. Egypt. J Exp Biol(Zool) 12:71–76
Aebi H (1984) Catalase in-Vitro. Meth Enzymol 105:121–126
Al-Harbi AH, Truax R, Thune RL (2000) Production and characterization of monoclonal antibodies against tilapia Oreochromis niloticus immunoglobulin. Aquaculture 188:219–227
Andrade T, Afonso A, Pérez-Jiménez A, Oliva-Teles A, de las Heras V, Mancera JM, Serradeiro R, Costas B (2015) Evaluation of different stocking densities in a Senegalese sole (Solea senegalensis) farm: implications for growth, humoral immune parameters and oxidative status. Aquaculture. 438:6–11
Araújo M, Rema P, Sousa-Pinto I, Cunha LM, Peixoto MJ, Pires MA, Seixas F, Brotas V, Beltrán C, Valente LM (2016) Dietary inclusion of IMTA-cultivated Gracilaria vermiculophylla in rainbow trout (Oncorhynchus mykiss) diets: effects on growth, intestinal morphology, tissue pigmentation, and immunological response. J Appl Phycol 28:679–689
Ardiansyah D, Hartinah I (2018) Wahidah improvement of the nutritive quality of Sargassum powder through Aspergillus niger, Saccharomyces cerevisiae, and Lactobacillus spp. fermentations. AACL Bioflux 11:753–764
Barbalace MC, Malaguti M, Giusti L, Lucacchini A, Hrelia S, Angeloni C (2019) Anti-inflammatory activities of marine algae in neurodegenerative diseases. Int J Molec Sci 20:3061
Beutler E (1963) Improved method for the determination of blood glutathione. J Lab Clim Med 61:882–888
Boyd CE, Tucker CS (2012) Pond aquaculture water quality management. Kluwer, Dordrecht
Caxico Vieira CAS, Vieira JS, Bastos MS, Zancanela V, Barbosa LT, Gasparino E, Del Vesco AP (2018) Expression of genes related to antioxidant activity in Nile tilapia kept under salinity stress and fed diets containing different levels of vitamin C. J Toxicol Environ Health A 81:20–30
Chew YL, Lim YY, Omar M, Khoo KS (2008) Antioxidant activity of three edible seaweeds from two areas in South East Asia. LWT-Food Sci Technol 41:1067–1072
Chotigeat W, Tongsupa S, Supamataya K, Phongdara A (2004) Effect of fucoidan on disease resistance of black tiger shrimp. Aquaculture 233:23–30
Coeurdacier J-L, Dutto G, Gasset E, Blancheton J-P (2011) Is total serum protein a good indicator for welfare in reared sea bass (Dicentrarchus labrax)? Aquat Living Resour 24:121–127
Dai Y-L, Jiang Y-F, Nie Y-H, Lu Y-A, Kang M-C, Jeon Y-J (2020) Hepato-protective effect of fucoidan extracted from acid-processed Sargassum fusiformis in ethanol-treated Chang liver cells and in a zebrafish model. J Appl Phycol 32:4289–4298
Datta S (2012) Management of water quality in intensive aquaculture. Respiration 6:602
Draper HH, Hadley M (1990) [43] Malondialdehyde determination as index of lipid Peroxidation. Meth Enzymol 186:421–431
Ellis AE (1990) Lysozyme Assays. Techniq Fish Immunol 1:101–103
Farag MR, Alagawany M, Taha HS, Ismail TA, Khalil SR, Abou-Zeid SM (2021) Immune response and susceptibility of Nile tilapia fish to Aeromonas hydrophila infection following the exposure to Bifenthrin and/or supplementation with Petroselinum crispum essential oil. Ecotoxicol Environ Saf 216:112205
Farhadi D, Hosseini SM, Dezfuli BT (2016) Effect of house type on growth performance, litter quality and incidence of foot lesions in broiler chickens reared in varying stocking density. J BioSci Biotech 69:78–75
Fazelan Z, Vatnikov YA, Kulikov EV, Plushikov VG, Yousefi M (2020) Effects of dietary ginger (Zingiber officinale) administration on growth performance and stress, immunological, and antioxidant responses of common carp (Cyprinus carpio) reared under high stocking density. Aquaculture 518:734833
Flórez-Fernández N, López-García M, González-Muñoz MJ, Vilariño JML, Domínguez H (2017) Ultrasound-assisted extraction of fucoidan from Sargassummuticum. J Appl Phycol 29:1553–1561
Folin O, Wu H (1919) A system of blood analysis. J Biol Chem 38:81–110
Ganesan P, Kumar CS, Bhaskar N (2008) Antioxidant properties of methanol extract and its solvent fractions obtained from selected Indian red seaweeds. Bioresour Technol 99:2717–2723
Ghelichpour M, Mirghaed AT, Hoseini SM, Jimenez AP (2020) Plasma antioxidant and hepatic enzymes activity, thyroid hormones alterations and health status of liver tissue in common carp (Cyprinus carpio) exposed to lufenuron. Aquaculture. 516:734634
Giri SS, Sen SS, Chi C, Kim HJ, Yun S, Park SC, Sukumaran V (2015) Effect of guava leaves on the growth performance and cytokine gene expression of Labeo rohita and its susceptibility to Aeromonas hydrophila infection. Fish Shellfish Immunol 46:217–224
Giriwono PE, Iskandriati D, Tan CP, Andarwulan N (2019) Sargassum seaweed as a source of anti-inflammatory substances and the potential insight of the tropical species: a review. Mar Drugs 17:590
Gomez-Zavaglia A, Prieto Lage MA, Jimenez-Lopez C, Mejuto JC, Simal-Gandara J (2019) The potential of seaweeds as a source of functional ingredients of prebiotic and antioxidant value. Antioxidants 8:406
Granfors K (1979) Measurement of immunoglobulin M (IgM), IgG, and IgA antibodies against Yersinia enterocolitica by enzyme-linked immunosorbent assay: persistence of serum antibodies during disease. J Clin Microbiol 9:336–341
Hafezieh M, Azhdari D, Ajdehakosh Poori A, Hosseini S (2017) The effect of brown seaweed (Sargassum ilicifolium) powder on western white leg shrimp. Iranian J Fish Sci 16:1098–1107
Hamblin C, Barnett I, Hedger R (1986) A new enzyme-linked immunosorbent assay (ELISA) for the detection of antibodies against foot-and-mouth disease virus I. Development and method of ELISA. J Immunol Meth 93:115–121
Harikrishnan R, Balasundaram C, Heo M (2010) Supplementation diet containing probiotics, herbal and azadirachtin on hematological and biochemical changes in Cirrhina mrigala against Aphanomyces invadans. Fisheries Aquacult J 4:1–11
Hastuti S, Subandiyono S (2020) Aminotransferase, hematological indices and growth of tilapia (Oreochomis niloticus) reared in various stocking densities in aquaponic systems. Aquacult Aquar Conservat Legislat 13:813–824
Hidayati JR, Yudiati E, Pringgenies D, Arifin Z, OktaviyantI DT (2019) Antioxidant activities, total phenolic compound and pigment contents of tropical Sargassum sp. extract, macerated in different solvents polarity. Jurnal Kelautan Tropis 22:73–80
Hoseini SM, Yousefi M, Hoseinifar SH, Van Doan H (2019) Effects of dietary arginine supplementation on growth, biochemical, and immunological responses of common carp (Cyprinus carpio L.), stressed by stocking density. Aquaculture 503:452–459
Hoseinifar SH, Zou HK, Van Doan H, Harikrishnan R, Yousefi M, Paknejad H, Ahmadifar E (2019) Can dietary jujube (Ziziphus jujuba Mill.) fruit extract alter cutaneous mucosal immunity, immune related genes expression in skin and growth performance of common carp (Cyprinus carpio)? Fish Shellfish Immunol 94:705–710
Hu S, Wang J, Wang J, Yang H, Yan X, Su L (2019) Fucoidan from Acaudina molpadioides improves insulin resistance by altering gut microbiota dysfunction. J Funct Foods 57:59–67
Huynh T-G, Yeh S-T, Lin Y-C, Shyu J-F, Chen L-L, Chen J-C (2011) White shrimp Litopenaeus vannamei immersed in seawater containing Sargassum hemiphyllum var. chinense powder and its extract showed increased immunity and resistance against Vibrio alginolyticus and white spot syndrome virus. Fish Shellfish Immunol 31:286–293
Immanuel G, Sivagnanavelmurugan M, Marudhupandi T, Radhakrishnan S, Palavesam A (2012) The effect of fucoidan from brown seaweed Sargassum wightii on WSSV resistance and immune activity in shrimp Penaeus monodon (Fab). Fish Shellfish Immunol 32:551–564
Jahromi ST, Pourmozaffar S, Jahanbakhshi A, Rameshi H, Gozari M, Khodadadi M, Sohrabipour J, Behzadi S, Bazrkar N, Nahavandi R (2021) Effect of different levels of dietary Sargassum cristaefolium on growth performance, hematological parameters, histological structure of hepatopancreas and intestinal microbiota of Litopenaeus vannamei. Aquaculture. 533:736130
John PJ (2007) Alteration of certain blood parameters of freshwater teleost Mystus vittatus after chronic exposure to Metasystox and Sevin. Fish Physiol Biochem 33:15–20
Kajita Y, Sakai M, Atsuta S, Kobayashi M (1990) The immunomodulatory effects of levamisole on rainbow trout, Oncorhynchus Mykiss. Fish Pathol 25:93–98
Kamunde C, Sappal R, Melegy TM (2019) Brown seaweed (AquaArom) supplementation increases food intake and improves growth, antioxidant status and resistance to temperature stress in Atlantic salmon, Salmo salar. PloS One 14:e0219792
Kanimozhi S, Krishnaveni M, Deivasigmani B, Rajasekar T, Priyadarshni P (2013) Immunomostimulation effects of Sargassum whitti on Mugil cephalus against Pseudomonas fluorescens. Int J Curr Microbiol App Sci 2:93–103
Karlsson A, Eliason EJ, Mydland LT, Farrell AP, Kiessling A (2006) Postprandial changes in plasma free amino acid levels obtained simultaneously from the hepatic portal vein and the dorsal aorta in rainbow trout (Oncorhynchus mykiss). J Exp Biol 209:4885–4894
Kuo I-P, Lee P-T, Nan F-H (2020) Rheum officinale extract promotes the innate immunity of orange-spotted grouper (Epinephelus coioides) and exerts strong bactericidal activity against six aquatic pathogens. Fish Shellfish Immunol 102:117–124
Levine RL, Garland D, Oliver CN, Amici A, Climent I, Lenz A-G, Ahn B-W, Shaltiel S, Stadtman ER (1990) Determination of carbonyl content in oxidatively modified proteins. Meth Enzymol 186:464–478
Lobo G, Pereira LF, Gonçalves JF, Peixoto MJ, Ozório RO (2018) Effect of dietary seaweed supplementation on growth performance, antioxidant and immune responses in European seabass (Dicentrarchus labrax) subjected to rearing temperature and salinity oscillations. Int Aquat Res 10:321–331
Lopez-Santamarina A, Miranda JM, Mondragon AdC, Lamas A, Cardelle-Cobas A, Franco CM, Cepeda A (2020) Potential use of marine seaweeds as prebiotics: a review. Molecules 25:1004
Mahmoud H, Reda F, Alagawany M, Farag M (2021) Ameliorating deleterious effects of high stocking density on Oreochromis niloticus using natural and biological feed additives. Aquaculture 531:735900
Makori AJ, Abuom PO, Kapiyo R, Anyona DN, Dida GO (2017) Effects of water physico-chemical parameters on tilapia (Oreochromis niloticus) growth in earthen ponds in Teso North Sub-County, Busia County. Fisheries Aquat Sci 20:1–10
Ming C, Rui W, Liping L, Huang T, Weiyi H, Jian L, Chao L, Aiying L, Honglin L, Wanwen L (2013) Sequence and evolution differences of Oreochromis niloticus CXC contribute to the diversification of cellular immune responses in tilapias with treatment of Streptococcus iniae. J Animal Vet Adv 12:303–311
Mirghaed AT, Hoseini SM, Ghelichpour M (2018) Effects of dietary 1, 8-cineole supplementation on physiological, immunological and antioxidant responses to crowding stress in rainbow trout (Oncorhynchus mykiss). Fish Shellfish Immunol 81:182–188
Montero D, Izquierdo M, Tort L, Robaina L, Vergara J (1999) High stocking density produces crowding stress altering some physiological and biochemical parameters in gilthead seabream, Sparus aurata, juveniles. Fish Physiol Biochem 20:53–60
Naiel MA, Nasr A, Ahmed M (2012) Influence of organic selenium and stocking density on performance of Nile tilapia (Oreochromis nilotictus). Zagazig. J Agric Res 39:1–13
Naiel MAE, Ismael NE, Abd El-hameed SAA, Amer MS (2020) The antioxidative and immunity roles of chitosan nanoparticle and vitamin C-supplemented diets against imidacloprid toxicity on Oreochromis niloticus. Aquaculture. 523:735219
Naiel MAE, Ismael NE, Negm SS, Ayyat MS, Al-Sagheer AA (2020) Rosemary leaf powder–supplemented diet enhances performance, antioxidant properties, immune status, and resistance against bacterial diseases in Nile Tilapia (Oreochromis niloticus). Aquaculture. 526:735370
Naiel MAE, Khames MK, Abdel-Razek N, Gharib AA, El-Tarabily KA (2021) The dietary administration of miswak leaf powder promotes performance, antioxidant, immune activity, and resistance against infectious diseases on Nile tilapia (Oreochromis niloticus). Aquacult Rep 20:100707
Naiel MAE, Farag MR, Gewida AG, Elnakeeb MA, Amer MS, Alagawany M (2021b) Using lactic acid bacteria as an immunostimulants in cultured shrimp with special reference to Lactobacillus spp. Aquacult Int 29:219–231
Nazarudin MF, Yusoff F, Idrus ES, Aliyu-Paiko M (2020) Brown seaweed Sargassum polycystum as dietary supplement exhibits prebiotic potentials in Asian sea bass Lates calcarifer fingerlings. Aquacult Rep 18:100488
Nishikimi M, Rao NA, Yagi K (1972) The occurrence of superoxide anion in the reaction of reduced phenazine methosulfate and molecular oxygen. Biochem Biophys Res Commun 46:849–854
Pang J-c, Gao F-y, Lu M-x, Ye X, Zhu H-p, Ke X-l (2013) Major histocompatibility complex class IIA and IIB genes of Nile tilapia Oreochromis niloticus: genomic structure, molecular polymorphism and expression patterns. Fish Shellfish Immunol 34:486–496
Peixoto MJ, Ferraz R, Magnoni LJ, Pereira R, Gonçalves JF, Calduch-Giner J, Pérez-Sánchez J, Ozório RO (2019) Protective effects of seaweed supplemented diet on antioxidant and immune responses in European seabass (Dicentrarchus labrax) subjected to bacterial infection. Sci Rep 9:1–12
Peixoto MJ, Salas-Leitón E, Pereira LF, Queiroz A, Magalhães F, Pereira R, Abreu H, Reis PA, Gonçalves JFM, de Almeida Ozório RO (2016) Role of dietary seaweed supplementation on growth performance, digestive capacity and immune and stress responsiveness in European seabass (Dicentrarchus labrax). Aquacult Rep 3:189–197
Peng Y, Xie E, Zheng K, Fredimoses M, Yang X, Zhou X, Wang Y, Yang B, Lin X, Liu J (2013) Nutritional and chemical composition and antiviral activity of cultivated seaweed Sargassum naozhouense Tseng et Lu. Mar Drugs 11:20–32
Portz DE, Woodley CM, Cech JJ (2006) Stress-associated impacts of short-term holding on fishes. Rev Fish Biol Fisheries 16:125–170
Pratiwy FM, Kohbara J, AB S, (2018) Effectiveness of Sargassum meal as feed additive on growth performance of nile tilapia, Oreochromis niloticus. Aquacult Sci 66:25–31
Qiang J, He J, Yang H, Xu P, Habte-Tsion HM, Ma X, Zhu Z (2016) The changes in cortisol and expression of immune genes of GIFT tilapia Oreochromis niloticus (L.) at different rearing densities under Streptococcus iniae infection. Aquacult Int 24:1365–1378
Qu Y, Cao Z, Wang W, Wang N, Li X, Pan J (2019) Monthly variations of fucoidan content and its composition in the farmed brown alga Saccharinasculpera (Laminariales, Phaeophyceae). J Appl Phycol 31:2623–2628
Razali NM, Wah YB (2011) Power comparisons of Shapiro-Wilk, Kolmogorov-Smirnov, Lilliefors and Anderson-Darling tests. J Stat Mod Analys 2:21–33
Ridha MT (2006) Comparative study of growth performance of three strains of Nile tilapia, Oreochromis niloticus, L. at two stocking densities. Aquacult Res 37:172–179
Rosa GP, Tavares WR, Sousa P, Seca AM, Pinto DC (2020) Seaweed secondary metabolites with beneficial health effects: an overview of successes in in-vivo studies and clinical trials. Mar Drugs 18:8
Rushdi MI, Abdel-Rahman IA, Saber H, Attia EZ, Abdelraheem WM, Madkour HA, Hassan HM, Elmaidomy AH, Abdelmohsen UR (2020) Pharmacological and natural products diversity of the brown algae genus Sargassum. RSC Adv 10:24951–24972
Sadhu N, Sharma SK, Joseph S, Dube P, Philipose K (2014) Chronic stress due to high stocking density in open sea cage farming induces variation in biochemical and immunological functions in Asian seabass (Lates calcarifer, Bloch). Fish Physiol Biochem 40:1105–1113
Salama HM, Marraiki N (2010) Antimicrobial activity and phytochemical analyses of Polygonum aviculare L. (Polygonaceae), naturally growing in Egypt. Saudi J Biol Sci 17:57–63
Salas-Leiton E, Anguis V, Martín-Antonio B, Crespo D, Planas JV, Infante C, Cañavate JP, Manchado M (2010) Effects of stocking density and feed ration on growth and gene expression in the Senegalese sole (Solea senegalensis): potential effects on the immune response. Fish Shellfish Immunol 28:296–302
Salvayre R, Negre A, Radom J, Douste-Blazy L (1986) Fluorometric assay for pancreatic lipase. Clin Chem 32:1532–1536
Schleder DD, Peruch LGB, Poli MA, Ferreira TH, Silva CP, Andreatta ER, Hayash L, Vieira F (2018) Effect of brown seaweeds on Pacific white shrimp growth performance, gut morphology, digestive enzymes activity and resistance to white spot virus. Aquaculture 495:359–365
Segner H, Sundh H, Buchmann K, Douxfils J, Sundell KS, Mathieu C, Ruane N, Jutfelt F, Toften H, Vaughan L (2012) Health of farmed fish: its relation to fish welfare and its utility as welfare indicator. Fish Physiol Biochem 38:85–105
Standen B, Rodiles A, Peggs D, Davies S, Santos G, Merrifield D (2015) Modulation of the intestinal microbiota and morphology of tilapia, Oreochromis niloticus, following the application of a multi-species probiotic. Appl Microbiol Biotechnol 99:8403–8417
Tng YY, Wee NL, Ip YK, Chew SF (2008) Postprandial nitrogen metabolism and excretion in juvenile marble goby, Oxyeleotris marmorata (Bleeker, 1852). Aquaculture 284:260–267
Traifalgar RF, Kira H, Thanh Tung H, Raafat Michael F, Laining A, Yokoyama S, IShikawa M, Koshio S, Serrano AE, Corre V (2010) Influence of dietary fucoidan supplementation on growth and immunological response of juvenile Marsupenaeus japonicus. J World Aquacult Soc 41:235–244
Undeland I (2016) Oxidative stability of seafood. In: Hu M, Jacobsen C (eds) Oxidative stability and shelf life of foods containing oils and fats. Elsevier, Amsterdam, pp 391–460
Uribe C, Folch H, Enríquez R, Moran G (2011) Innate and adaptive immunity in teleost fish: a review. Vet Med 56:486–503
Valente LM, Araújo M, Batista S, Peixoto MJ, Sousa-Pinto I, Brotas V, Cunha LM, Rema P (2016) Carotenoid deposition, flesh quality and immunological response of Nile tilapia fed increasing levels of IMTA-cultivated Ulva spp. J Appl Phycol 28:691–701
Vazirzadeh A, Jalali S, Farhadi A (2019) Antibacterial activity of Oliveria decumbens against Streptococcus iniae in Nile tilapia (Oreochromis niloticus) and its effects on serum and mucosal immunity and antioxidant status. Fish Shellfush Immunol 94:407–416
Wan AH, Davies SJ, Soler-Vila A, Fitzgerald R, Johnson MP (2019) Macroalgae as a sustainable aquafeed ingredient. Rev Aquacult 11:458–492
Wang C-Y, Chen Y-C (2016) Extraction and characterization of fucoidan from six brown macroalgae. J Mar Sci Technol 24:319–328
Wang Y, XU GCN (2019) Effect of stocking density on growth, serum biochemical parameters, digestive enzymes activity and antioxidant status of largemouth bass, Micropterus salmoides. Pakistan J Zool 51:1509–1517
Wen Z-S, Xiang X-W, Jin H-X, Guo X-Y, Liu L-J, Huang Y-N, OuYang X-K, Qu Y-L (2016) Composition and anti-inflammatory effect of polysaccharides from Sargassum horneri in RAW264. 7 macrophages. Int J Biol Macromol 88:403–413
Wilkinson J, Baron D, Moss D, Walker P (1972) Standardization of clinical enzyme assays: a reference method for aspartate and alanine transaminases. J Clin Pathol 25:940
Wu Q, Liu L, Miron A, Klímová B, Wan D, Kuča K (2016) The antioxidant, immunomodulatory, and anti-inflammatory activities of Spirulina: an overview. Arch Toxicol 90:1817–1840
Wu S, Duan C, Kong L, Tu X, Wang L, Guo Z, Ye J (2021) Interleukin-10 (IL-10) participates in host defense against bacterial pathogens and promotes IgM antibody production in Nile tilapia (Oreochromis niloticus). Aquaculture. 531:735829
Yangthong M, Hutadilok-Towatana N, Thawonsuwan J, Phromkunthong W (2016) An aqueous extract from Sargassum sp. enhances the immune response and resistance against Streptococcus iniae in the Asian sea bass (Lates calcarifer Bloch). J Appl Phycol 28:3587–3598
Yarahmadi P, Miandare HK, Fayaz S, Caipang CMA (2016) Increased stocking density causes changes in expression of selected stress- and immune-related genes, humoral innate immune parameters and stress responses of rainbow trout (Oncorhynchus mykiss). Fish Shellfish Immunol 48:43–53
Yeganeh S, Adel M (2019) Effects of dietary algae (Sargassum ilicifolium) as immunomodulator and growth promoter of juvenile great sturgeon (Huso huso Linnaeus, 1758). J Appl Phycol 31:2093–2102
Yende SR, Harle UN, Chaugule BB (2014) Therapeutic potential and health benefits of Sargassum species. Pharmacogn Rev 8:1
Yuan JS, Reed A, Chen F, Stewart CN (2006) Statistical analysis of real-time PCR data. BMC Bioinformat 7:1–12
Zeraatpisheh F, Firouzbakhsh F, Khalili KJ (2018) Effects of the macroalga Sargassum angustifolium hot water extract on hematological parameters and immune responses in rainbow trout (Oncohrynchus mykiss) infected with Yersinia rukeri. J Appl Phycol 30:2029–2037
Zeynali M, Nafisi Bahabadi M, Morshedi V, Ghasemi A, Torfi Mozanzadeh M (2020) Replacement of dietary fishmeal with Sargassum ilicifolium meal on growth, innate immunity and immune gene mRNA transcript abundance in Lates calcarifer juveniles. Aquacult Nutr 26:1657–1668
Zhang R-L, Luo W-D, Bi T-N, Zhou S-K (2012) Evaluation of antioxidant and immunity-enhancing activities of Sargassum pallidum aqueous extract in gastric cancer rats. Molecules 17:8419–8429
Zou J, Secombes CJ (2016) The Function of Fish Cytokines. Biology 5:23
Acknowledgements
The authors are grateful to Dr Sarah H Rashedy, National Institute of Oceanography and Fisheries, Egypt, for collecting, isolating, identifying, and preparing the macroalga Sargassum aquifolium applied in the current study.
Author information
Authors and Affiliations
Corresponding authors
Ethics declarations
Ethical approval
The in vivo trial used fish that were subjected to the general protocol standards for the Care and Use of Laboratory Animals and were approved by Zagazig University’s Institutional Animal Care and Use Committee.
Competing interests
The authors declare no competing interests.
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
Negm, S.S., Ismael, N.E.M., Ahmed, A.I. et al. The efficiency of dietary Sargassum aquifolium on the performance, innate immune responses, antioxidant activity, and intestinal microbiota of Nile Tilapia (Oreochromis niloticus) raised at high stocking density. J Appl Phycol 33, 4067–4082 (2021). https://doi.org/10.1007/s10811-021-02572-3
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10811-021-02572-3