Use of Phytochemicals as Feed Supplements in Aquaculture: A Review on Their Effects on Growth, Immune Response, and Antioxidant Status of Finfish

Year 2021, Volume: 2 Issue: 1, 32 - 43, 29.06.2021

Yiğit Taştan Mohamed Omar Abdalla Salem

Abstract

Aquaculture production is increasing day by day to meet the protein need of the global population. Various feed additives are used in aquaculture to enhance growth, stimulate immunity, prevent diseases, and strengthen the antioxidant status of fish. Phytochemicals attract attention among these feed additives. As phytochemicals are natural products, they are considered to be safe for fish, humans, and the environment. In this paper, we reviewed recent studies that utilize phytochemicals as feed additives in cultured fish species. In agreement with the available literature, we inferred that phytochemicals could be used in aquaculture. However, as some studies reported undesirable effects on growth, we believe that phytochemicals are more effective in immunostimulation and enhancing antioxidant status rather than growth-promoting. Possible reasons for growth retardation were emphasized. Although available evidence suggests that phytochemicals display beneficial effects, we discussed the possible use of phytochemical combinations to obtain even more desirable results. To conclude, we think that phytochemicals can exert synergistic effects, and this approach should be investigated in future studies.

Keywords

Aquaculture, Feed additive, Fish, Growth, Immunostimulation, Phytochemical

References

• Abd El-Hakim, Y. M., El-Houseiny, W., Abd Elhakeem, E. M., Ebraheim, L. L., Moustafa, A. A., & Mohamed, A. A. R. (2020). Melamine and curcumin enriched diets modulate the haemato-immune response, growth performance, oxidative stress, disease resistance, and cytokine production in Oreochromis niloticus. Aquatic Toxicology, 220, 105406.‏ https://doi.org/10.1016/j.aquatox.2020.105406
• Adeshina, I., Abdel-Tawwab, M., Tijjani, Z. A, Tiamiyu, L. O., & Jahanbakhshi, A. (2021). Dietary Tridax procumbens leaves extract stimulated growth, antioxidants, immunity, and resistance of Nile tilapia, Oreochromis niloticus, to monogenean parasitic infection. Aquaculture, 532, 736047. https://doi.org/10.1016/j.aquaculture.2020.736047
• Ahmadifar, E., Dawood M. A. O., Moghadam, M. S., Sheikhzadeh, N., Hoseinifar, S. H., & Musthafa, M. S. (2019). Modulation of immune parameters and antioxidant defense in zebrafish (Danio rerio) using dietary apple cider vinegar. Aquaculture, 513, 734412. https://doi.org/10.1016/j.aquaculture.2019.734412
• Almabrok, A. A., Amhamed, I. D., Mohamed, G. A., Bilen, S., & Altief, T. A. S. (2018). Effect of Tilia tomentosa methanolic extract on growth performance, digestive enzyme activity, immune system and haematological indices of common carp (Cyprinus carpio). Marine Science and Technology Bulletin, 7(1), 12-20. https://doi.org/10.33714/masteb.421047
• Arslan, G., Sönmez, A. Y., & Yanık, T. (2018). Effects of grape Vitis vinifera seed oil supplementation on growth, survival, fatty acid profiles, antioxidant contents and blood parameters in rainbow trout Oncorhynchus mykiss. Aquaculture Research, 49(6), 2256–2266. https://doi.org/10.1111/are.13686
• Awad, E., Austin, D., & Lyndon, A. R. (2013). Effect of black cumin seed oil (Nigella sativa) and nettle extract (Quercetin) on enhancement of immunity in rainbow trout, Oncorhynchus mykiss (Walbaum). Aquaculture, 388–391, 193–197. https://doi.org/10.1016/j.aquaculture.2013.01.008
• Bhattacharjee, P., Borah, A., & Das, S. (2020). Quercetin-induced amelioration of deltamethrin stress in freshwater teleost, Channa punctata: Multiple biomarker analysis. Comparative Biochemistry and Physiology Part C: Toxicology & Pharmacology, 227, 108626.‏ https://doi.org/10.1016/j.cbpc.2019.108626
• Bilen, S., Kızak, V., & Gezen, A. M. (2013). Floating fish farm unit (3FU). Is it an appropriate method for salmonid production?. Marine Science and Technology Bulletin, 2(1), 9-13.
• Bilen, S., Karga, M., Çelik Altunoğlu, Y., Ulu, F., & Biswas, G. (2020). Immune responses and growth performance of the aqueous methanolic extract of Malva sylvestris in Oncorhynchus mykiss. Marine Science and Technology Bulletin, 9(2), 159-167. https://doi.org/10.33714/masteb.746951
• Biller-Takahashi, J. D., & Urbinati, E. C. (2014). Fish immunology. The modification and manipulation of the innate immune system: Brazilian studies. Anais da Academia Brasileira de Ciências, 86(3), 1484-1506. https://doi.org/10.1590/0001-3765201420130159
• Bulfon, C., Bongiorno, T., Messina, M., Volpatti, D., Tibaldi, E., & Tulli, F. (2017). Effects of Panax ginseng extract in practical diets for rainbow trout (Oncorhynchus mykiss) on growth performance, immune response and resistance to Yersinia ruckeri. Aquaculture Research, 48(5), 2369-2379. https://doi.org/10.1111/are.13072
• Cao, J., Chen, J., Xie, L., Wang, J., Feng, C., & Song, J. (2015). Protective properties of sesamin against fluoride-induced oxidative stress and apoptosis in kidney of carp (Cyprinus carpio) via JNK signaling pathway. Aquatic Toxicology, 167, 180–190. https://doi.org/10.1016/j.aquatox.2015.08.004.
• Cavalcante, R. B., Telli, G. S., Tachibana, L., de Carla Dias, D., Oshiro, E., Natori, M. M., da Silva, W. F., & Ranzani-Paiva, M. J. (2020). Probiotics, prebiotics and synbiotics for nile tilapia: Growth performance and protection against Aeromonas hydrophila infection. Aquaculture Reports, 17, 100343. https://doi.org/10.1016/j.aqrep.2020.100343
• Cengiz, F. (2001). Hayvanlarda zorlanım (stres) oluşturan etkenler. Journal of Research in Veterinary Medicine, 20, 147-153.
• Chakraborty, S. B., & Hancz, C. (2011). Application of phytochemicals as immunostimulant, antipathogenic and antistress agents in finfish culture. Reviews in Aquaculture, 3(3), 103–119. https://doi.org/10.1111/j.1753-5131.2011.01048.x
• Chakraborty, S. B., Horn, P., & Hancz, C. (2014). Application of phytochemicals as growth‐promoters and endocrine modulators in fish culture. Reviews in Aquaculture, 6(1), 1-19. https://doi.org/10.1111/raq.12021
• Chen, W., Ai, Q., Mai, K., Xu, W., Liufu, Z., Zhang, W., & Cai, Y. (2011). Effects of dietary soybean saponins on feed intake, growth performance, digestibility and intestinal structure in juvenile japanese flounder (Paralichthys olivaceus). Aquaculture, 318(1-2), 95-100.‏ https://doi.org/10.1016/j.aquaculture.2011.04.050
• Chen, D., Wang, W., & Ru, S. (2015). Effect of dietary genistein on growth performance, digestive enzyme activity, and body composition of nile tilapia Oreochromis niloticus. Chinese Journal of Oceanology and Limnology, 33(1), 77-83.‏ https://doi.org/10.1007/s00343-015-4037-6
• Choudhari, A. S., Mandave, P. C., Deshpande, M., Ranjekar, P., & Prakash, O. (2020). Phytochemicals in cancer treatment: From preclinical studies to clinical practice. Frontiers in Pharmacology, 10, 1614. https://doi.org/10.3389/fphar.2019.01614
• Citarasu, T. (2010). Herbal biomedicines: A new opportunity for aquaculture industry. Aquaculture International, 18, 403–414. https://doi.org/10.1007/s10499-009-9253-7
• Dawood, M. A., Metwally, A. E. S., El-Sharawy, M. E., Ghozlan, A. M., Abdel-Latif, H. M., Van Doan, H., & Ali, M. A. (2020). The influences of ferulic acid on the growth performance, haemato-immunological responses, and immune-related genes of Nile tilapia (Oreochromis niloticus) exposed to heat stress. Aquaculture, 525, 735320. https://doi.org/10.1016/j.aquaculture.2020.735320
• de Oliveira, S. T. L., Soares, R. A. N., de Negreiros Sousa, S. M., Fernandes, A. W. C., Gouveia, G. V., & da Costa, M. M. (2020) Natural products as functional food ingredients for nile tilapia challenged with Aeromonas hydrophila. Aquaculture International, 28, 913-926. https://doi.org/10.1007/s10499-019-00503-1
• Eberhardt, M. V., Lee, C. Y., & Liu, R. H. (2000). Antioxidant activity of fresh apples. Nature, 405, 903–904. https://doi.org/10.1038/35016151
• Elbesthi, R. T. A., Yürüten Özdemir, K., Taştan, Y., Bilen, S., & Sönmez, A. Y. (2020). Effects of ribwort plantain (Plantago lanceolata) extract on blood parameters, immune response, antioxidant enzyme activities, and growth performance in rainbow trout (Oncorhynchus mykiss). Fish Physiology and Biochemistry, 46, 1295-1307. https://doi.org/10.1007/s10695-020-00790-z
• Erguig, M., Yahyaoui, A., Fekhaoui, M., & Dakki, M. (2015). The use of garlic in aquaculture. European Journal of Biotechnology and Bioscience, 8(3), 28-33.
• Ferguson, R. M. W., Merrifield, D. L., Harper, G. M., Rawling, M. D., Mustafa, S., Picchietti, S., Balcazar, J. L., & Davies, S. J. (2010). The effect of Pediococcus acidilactici on the gut microbiota and immune status of on-growing red tilapia (Oreochromis niloticus). Journal of Applied Microbiology, 109(3), 851-862. https://doi.org/10.1111/j.1365-2672.2010.04713.x
• Francis, G., Makkar, H. P., & Becker, K. (2002). Dietary supplementation with a quillaja saponin mixture improves growth performance and metabolic efficiency in common carp (Cyprinus carpio L.). Aquaculture, 203(3-4), 311-320.‏ https://doi.org/10.1016/S0044-8486(01)00628-7
• Ganeva, V. O., Korytář, T., Pecková, H., McGurk, C., Mullins, J., Yanes-Roca, C., Gela, D., Lepič, P., Policar, T., & Holzer, A. S. (2020). Natural feed additives modulate immunity and mitigate infection with Sphaerospora molnari (Myxozoa: Cnidaria) in common carp: A pilot study. Pathogens, 9(12), 1013. https://doi.org/10.3390/pathogens9121013
• Giri, S. S., Sukumaran, V., & Park, S. C. (2019). Effects of bioactive substance from turmeric on growth, skin mucosal immunity and antioxidant factors in common carp, Cyprinus carpio. Fish & Shellfish Immunology, 92, 612-620.‏ https://doi.org/10.1016/j.fsi.2019.06.053
• Glencross, B., Evans, D., Rutherford, N., Hawkins, W., McCafferty, P., Dods, K., Jones, B., Harris, D., Morton, L., & Sweetingham, M. (2006). The influence of the dietary inclusion of the alkaloid gramine, on rainbow trout (Oncorhynchus mykiss) growth, feed utilisation and gastrointestinal histology. Aquaculture, 253(1-4), 512-522. https://doi.org/10.1016/j.aquaculture.2005.07.009
• Hu, H., Liu, J., Li, Y., Zhang, Y., Mai, K., Ai, Q., Shao, M., & Yang, P. (2014). Effects of dietary daidzein on growth performance, activities of digestive enzymes, anti-oxidative ability and intestinal morphology in juvenile turbot (Scophthalmus maximus L.). Journal of Fisheries of China, 38(9), 1503-1513.‏
• Jia, E., Yan, Y., Zhou, M., Li, X., Jiang, G., Liu, W., & Zhang, D. (2019). Combined effects of dietary quercetin and resveratrol on growth performance, antioxidant capability and innate immunity of blunt snout bream (Megalobrama amblycephala). Animal Feed Science and Technology, 256, 114268. https://doi.org/10.1016/j.anifeedsci.2019.114268
• Jia, R., Li, Y., Cao, L., Du, J., Zheng, T., Qian, H., Gu, Z., Jeney, G., Xu, P., & Yin, G. (2019). Antioxidative, anti-inflammatory and hepatoprotective effects of resveratrol on oxidative stress-induced liver damage in tilapia (Oreochromis niloticus). Comparative Biochemistry and Physiology Part C: Toxicology & Pharmacology, 215, 56-66.‏ https://doi.org/10.1016/j.cbpc.2018.10.002
• Karga, M., Kenanoğlu, O. N., & Bilen, S. (2020). Investigation of antibacterial activity of two different medicinal plants extracts against fish pathogens. Journal of Agricultural Production, 1(1), 5-7. https://doi.org/10.29329/agripro.2020.341.2
• Kasumyan, A. O., & Døving, K. B. (2003). Taste preferences in fishes. Fish and Fisheries, 4(4), 289–347. https://doi.org/10.1046/j.1467-2979.2003.00121.x
• Kim, S. S., Rahimnejad, S., Kim, K. W., Lee, B. J., & Lee, K. J. (2013). Effects of dietary supplementation of spirulina and quercetin on growth, innate immune responses, disease resistance against Edwardsiella tarda, and dietary antioxidant capacity in the juvenile olive flounder Paralichthys olivaceus. Fisheries and Aquatic Sciences, 16(1), 7-14.‏ https://doi.org/10.5657/FAS.2013.0007
• Koh, C. B., Romano, N., Zahrah, A. S., & Ng, W. K. (2016). Effects of a dietary organic acids 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. Aquaculture Research, 47(2), 357-369. https://doi.org/10.1111/are.12492
• Kumari, J., & Sahoo, K. P. (2006). Dietary levamisole modulates the immune response and disease resistance of asian catfish Clarias batrachus (Linnaeus). Aquaculture Research, 37, 500-509. https://doi.org/10.1111/j.1365-2109.2006.01456.x
• Lall, S. P., & Tibbetts, S. M. (2009). Nutrition, feeding, and behavior of fish. Veterinary Clinics of North America: Exotic Animal Practice, 12(2), 361–372. https://doi.org/10.1016/j.cvex.2009.01.005
• Leitzmann, C. (2016). characteristics and health benefits of phytochemicals. Complementary Medicine Research, 23(2), 69–74. https://doi.org/10.1159/000444063
• Lillehoj, H., Liu, Y., Calsamiglia, S., Fernandez-Miyakawa, M. E., Chi, F., Cravens, R. L., Oh, S., & Gay, C. G. (2018). Phytochemicals as antibiotic alternatives to promote growth and enhance host health. Veterinary Research, 49(1), 1-18. https://doi.org/10.1186/s13567-018-0562-6
• Liu, R. H. (2003). Health benefits of fruit and vegetables are from additive and synergistic combinations of phytochemicals. The American Journal of Clinical Nutrition, 78(3), 517–520. https://doi.org/10.1093/ajcn/78.3.517s
• Mahfouz, M. E. (2015). Ameliorative effect of curcumin on aflatoxin B1-induced changes in liver gene expression of Oreochromis niloticus. Molecular Biology, 49(2), 275-286.‏ https://doi.org/10.1134/S0026893315020089
• Mahmoud, H. K., Al-Sagheer, A. A., Reda, F. M., Mahgoub, S. A., & Ayyat, M. S. (2017). Dietary curcumin supplement influence on growth, immunity, antioxidant status, and resistance to Aeromonas hydrophila in Oreochromis niloticus. Aquaculture, 475, 16-23.‏ https://doi.org/10.1016/j.aquaculture.2017.03.043
• Makled, S. O., Hamdan, A. M., & El-Sayed, A. F. M. (2020). Growth promotion and immune stimulation in nile tilapia, Oreochromis niloticus, fingerlings following dietary administration of a novel marine probiotic, Psychrobacter maritimus S. Probiotics and Antimicrobial Proteins, 12(2), 365-374. https://doi.org/10.1007/s12602-019-09575-0
• Mani, J. S., Johnson, J. B., Steel, J. C., Broszczak, D. A., Neilsen, P. M., Walsh, K. B., & Naiker, M. (2020). Natural product-derived phytochemicals as potential agents against coronaviruses: A review. Virus Research, 284, 197989. https://doi.org/10.1016/j.virusres.2020.197989
• Manju, M., Akbarsha, M. A., & Oommen, O. V. (2012). In vivo protective effect of dietary curcumin in fish Anabas testudineus (Bloch). Fish Physiology and Biochemistry, 38(2), 309-318.‏ https://doi.org/10.1007/s10695-011-9508-x
• Ming, J., Ye, J., Zhang, Y., Xu, Q., Yang, X., Shao, X., Qiang, Y., & Xu, P. (2020). Optimal dietary curcumin improved growth performance, and modulated innate immunity, antioxidant capacity and related genes expression of NF-κB and Nrf2 signaling pathways in grass carp (Ctenopharyngodon idella) after infection with Aeromonas hydrophila. Fish & Shellfish Immunology, 97, 540-553.‏ https://doi.org/10.1016/j.fsi.2019.12.074
• Mohamed, G. A., Amhamed, I. D., Almabrok, A. A., Barka, A. B. A., Bilen, S., & Elbeshti, R. T. (2018). Effect of celery (Apium graveolens) extract on the growth, haematology, immune response and digestive enzyme activity of common carp (Cyprinus carpio). Marine Science and Technology Bulletin, 7(2), 51-59. https://doi.org/10.33714/masteb.457721
• Nazeri, S., Farhangi, M., & Modarres, S. (2017). The effect of different dietary inclusion levels of rutin (a flavonoid) on some liver enzyme activities and oxidative stress indices in rainbow trout, Oncorhynchus mykiss (Walbaum) exposed to oxytetracycline. Aquaculture Research, 48(8), 4356-4362.‏ https://doi.org/10.1111/are.13257
• Omnes, M. H., Le Goasduff, J., Le Delliou, H., Le Bayon, N., Quazuguel, P., & Robin, J. H. (2017). Effects of dietary tannin on growth, feed utilization and digestibility, and carcass composition in juvenile european seabass (Dicentrarchus labrax L.). Aquaculture Reports, 6, 21-27.‏ https://doi.org/10.1016/j.aqrep.2017.01.004
• Oomah, B. (1999). Health benefits of phytochemicals from selected canadian crops. Trends in Food Science & Technology, 10(6-7), 193–198. https://doi.org/10.1016/s0924-2244(99)00055-2
• Ou, W., Hu, H., Yang, P., Dai, J., Ai, Q., Zhang, W., Zhang, Y., & Mai, K. (2019). Dietary daidzein improved intestinal health of juvenile turbot in terms of intestinal mucosal barrier function and intestinal microbiota. Fish & Shellfish Immunology, 94, 132-141. ‏https://doi.org/10.1016/j.fsi.2019.08.059
• Özçelik, H., Taştan, Y., Terzi, E., & Sönmez, A. Y. (2020). Use of onion (Allium cepa) and garlic (Allium sativum) wastes for the prevention of fungal disease (Saprolegnia parasitica) on eggs of rainbow trout (Oncorhynchus mykiss). Journal of Fish Diseases, 43(10), 1325-1330. https://doi.org/10.1111/jfd.13229
• Peng, K., Wang, G., Wang, Y., Chen, B., Sun, Y., Mo, W., Li, G., & Huang, Y. (2020). Condensed tannins enhanced antioxidant capacity and hypoxic stress survivability but not growth performance and fatty acid profile of juvenile japanese seabass (Lateolabrax japonicus). Animal Feed Science and Technology, 269, 114671.‏ https://doi.org/10.1016/j.anifeedsci.2020.114671
• Pês, T. S., Saccol, E. M. H., Ourique, G. M., Londero, É. P., Gressler, L. T., Finamor, I. A., Rotili, D. A., Golombieski, J. I., Glanzner, W. G., Llesuy, S. F., Gonçalves, P. B. D., Neto, J. R., Baldisserotto, B., & Pavanato, M. A. (2016). Effect of diets enriched with rutin on blood parameters, oxidative biomarkers and pituitary hormone expression in silver catfish (Rhamdia quelen). Fish Physiology and Biochemistry, 42(1), 321-333.‏ https://doi.org/10.1007/s10695-015-0140-z
• Pês, T. S., Saccol, E. M., Londero, É. P., Bressan, C. A., Ourique, G. M., Rizzetti, T. M., Prestes, O. D., Zanella, R., Baldisserotto, B., & Pavanato, M. A. (2018). Protective effect of quercetin against oxidative stress induced by oxytetracycline in muscle of silver catfish. Aquaculture, 484, 120-125.‏ https://doi.org/10.1016/j.aquaculture.2017.10.043
• Pickering, A. D. (1993). Growth and stress in fish production. In G. A. E. Gall & H. Chen (Eds.), Genetics in Aquaculture (pp. 51-63). Elsevier. https://doi.org/10.1016/b978-0-444-81527-9.50010-5
• Safari, R., Hoseinifar, S. H., Imanpour, M. R., Mazandarani, M., Sanchouli, H., & Paolucci, M. (2020). Effects of dietary polyphenols on mucosal and humoral immune responses, antioxidant defense and growth gene expression in beluga sturgeon (Huso huso). Aquaculture, 528, 735494.‏ https://doi.org/10.1016/j.aquaculture.2020.735494
• Salem, M. O. A., Salem, T. A., Yürüten Özdemir, K., Sönmez, A. Y., Bilen, S., & Güney, K. (2021). Antioxidant enzyme activities and immune responses in rainbow trout (Onchorhynchus mykiss) juveniles fed diets supplemented with dandelion (Taraxacum officinalis) and lichen (Usnea barbata) extracts. Fish Physiology and Biochemistry. https://doi.org/10.1007/s10695-021-00962-5
• Sangari, M., Sotoudeh, E., Bagheri, D., Morammazi, S., & Mozanzadeh, M. T. (2021). Growth, body composition, and hematology of yellowfin seabream (Acanthopagrus latus) given feeds supplemented with organic acid salts (sodium acetate and sodium propionate). Aquaculture International, 29, 261-273. https://doi.org/10.1007/s10499-020-00625-x
• Schiller Vestergren, A., Wagner, L., Pickova, J., Rosenlund, G., Kamal‐Eldin, A., & Trattner, S. (2012). Sesamin modulates gene expression without corresponding effects on fatty acids in Atlantic salmon (Salmo salar L.). Lipids, 47(9), 897-911. https://doi.org/10.1007/s11745-012-3697-7
• Serrano, E., Storebakken, T., Borquez, A., Penn, M., Shearer, K. D., Dantagnan, P., & Mydland, L. T. (2011). Histology and growth performance in rainbow trout (Oncorhynchus mykiss) in response to increasing dietary concentration of sparteine, a common alkaloid in lupins. Aquaculture Nutrition, 18(3), 313-320.‏ https://doi.org/10.1111/j.1365-2095.2011.00899.x
• Shin, H. S., Yoo, J. H., Min, T. S., Lee, K. Y., & Choi, C. Y. (2010a). The effects of quercetin on physiological characteristics and oxidative stress resistance in olive flounder, Paralichthys olivaceus. Asian-Australasian Journal of Animal Sciences, 23(5), 588-597.‏ https://doi.org/10.5713/ajas.2010.90624
• Shin, H. S., Yoo, J. H., Min, T. S., Lee, J., & Choi, C. Y. (2010b). Effect of quercetin on the activity and mRNA expression of antioxidant enzymes and physiological responses in olive flounder (Paralichthys olivaceus) exposed to cadmium. Asian-Australasian Journal of Animal Sciences, 23(6), 742-749. https://doi.org/10.5713/ajas.2010.10006
• Sönmez, A. Y. (2017). Evaluating two different additive levels of fully autolyzed yeast, Saccharomyces cerevisiae, on rainbow trout (Oncorhynchus mykiss) growth performance, liver histology and fatty acid composition. Turkish Journal of Fisheries and Aquatic Sciences, 17(2), 379-385. https://doi.org/10.4194/1303-2712-v17_2_17
• Sönmez, A. Y., Bilen, S., Alak, G., Hisar, O., Yanık, T., & Biswas, G. (2015). Growth performance and antioxidant enzyme activities in rainbow trout (Oncorhynchus mykiss) juveniles fed diets supplemented with sage, mint and thyme oils. Fish Physiology and Biochemistry, 41(1), 165-175. https://doi.org/10.1007/s10695-014-0014-9
• Sönmez, A. Y., Bilen, S., Albayrak, M., Yılmaz, S., Biswas, G., Hisar, O., & Yanık, T. (2015). Effects of dietary supplementation of herbal oils containing 1, 8-cineole, carvacrol or pulegone on growth performance, survival, fatty acid composition, and liver and kidney histology of rainbow trout (Oncorhynchus mykiss) fingerlings. Turkish Journal of Fisheries and Aquatic Sciences, 15, 813-819. https://doi.org/10.4194/1303-2712-v15_4_04
• Sutili, F. J., Gatlin, D. M., Heinzmann, B. M., & Baldisserotto, B. (2017). Plant essential oils as fish diet additives: benefits on fish health and stability in feed. Reviews in Aquaculture, 10(3), 716–726. https://doi.org/10.1111/raq.12197
• Syahidah, A., Saad, C., Daud, H., & Abdelhadi, Y. (2015). Status and potential of herbal applications in aquaculture: A review. Iranian Journal of Fisheries Sciences, 14(1), 27-44. https://doi.org/10.22092/IJFS.2018.114421
• Tan, C., Zhou, H., Wang, X., Mai, K., & He, G. (2019). Resveratrol attenuates oxidative stress and inflammatory response in turbot fed with soybean meal based diet. Fish & Shellfish Immunology, 91, 130-135. ‏ https://doi.org/10.1016/j.fsi.2019.05.030
• Terzi, E., Kucukkosker, B., Bilen, S., Kenanoglu, O. N., Corum, O., Özbek, M., & Parug, S. S. (2021). A novel herbal immunostimulant for rainbow trout (Oncorhynchus mykiss) against Yersinia ruckeri. Fish & Shellfish Immunology, 110, 55-66. https://doi.org/10.1016/j.fsi.2020.12.019
• Tort, L. (2011). Stress and immune modulation in fish. Developmental & Comparative Immunology, 35(12), 1366-1375. https://doi.org/10.1016/j.dci.2011.07.002
• Villa-Cruz, V., Davila, J., Viana, M., & Vazquez-Duhalt, R. (2009). Effect of broccoli (Brassica oleracea) and its phytochemical sulforaphane in balanced diets on the detoxification enzymes levels of tilapia (Oreochromis niloticus) exposed to a carcinogenic and mutagenic pollutant. Chemosphere, 74(9), 1145-1151. https://doi.org/10.1016/j.chemosphere.2008.11.082
• Xu, Z., Li, X., Yang, H., Liang, G., Gao, B., & Leng, X. (2019). Dietary quercetin improved the growth, antioxidation, and flesh quality of grass carp (Ctenopharyngodon idella). Journal of the World Aquaculture Society, 50(6), 1182-1195.‏ https://doi.org/10.1111/jwas.12663
• Ye, Q., Feng, Y., Wang, Z., Zhou, A., Xie, S., Zhang, Y., Xiang, Q., Song, E., & Zou, J. (2019). Effects of dietary Gelsemium elegans alkaloids on growth performance, immune responses and disease resistance of Megalobrama amblycephala. Fish & Shellfish Immunology, 91, 29-39.‏ https://doi.org/10.1016/j.fsi.2019.05.026
• Yilmaz, E., Ergün, S., & Yilmaz, S. (2015). Influence of carvacrol on the growth performance, hematological, non-specific immune and serum biochemistry parameters in rainbow trout (Oncorhynchus mykiss). Food and Nutrition Sciences, 6(5), 523-531. https://doi.org/10.4236/fns.2015.65054
• Yilmaz, S. (2019). Effects of dietary caffeic acid supplement on antioxidant, immunological and liver gene expression responses, and resistance of Nile tilapia, Oreochromis niloticus to Aeromonas veronii. Fish & Shellfish Immunology, 86, 384-392. https://doi.org/10.1016/j.fsi.2018.11.068
• Yılmaz, S., & Ergün, S. (2018). Trans-cinnamic acid application for rainbow trout (Oncorhynchus mykiss): I. Effects on haematological, serum biochemical, non-specific immune and head kidney gene expression responses. Fish & Shellfish Immunology, 78, 140-157. https://doi.org/10.1016/j.fsi.2018.04.034
• Yonar, M. E., Yonar, S. M., İspir, Ü., & Ural, M. Ş. (2019). Effects of curcumin on haematological values, immunity, antioxidant status and resistance of rainbow trout (Oncorhynchus mykiss) against Aeromonas salmonicida subsp. achromogenes. Fish & Shellfish Immunology, 89, 83-90.‏ https://doi.org/10.1016/j.fsi.2019.03.038
• Yu, L., Wu, F., Liu, W., Tian, J., Lu, X., & Wen, H. (2017). Semisynthetic ferulic acid derivative: an efficient feed additive for Genetically Improved Farmed Tilapia (Oreochromis niloticus). Aquaculture Research, 48(9), 5017-5028.‏ https://doi.org/10.1111/are.13319
• Zhai, S. W., & Liu, S. L. (2013). Effects of dietary Quercetin on growth performance, serum lipids level and body composition of tilapia (Oreochromis niloticus). Italian Journal of Animal Science, 12(4), e85. https://doi.org/10.4081/ijas.2013.e85
• Zhang, L., Virgous, C., & Si, H. (2019). Synergistic anti-inflammatory effects and mechanisms of combined phytochemicals. The Journal of Nutritional Biochemistry, 69, 19-30. https://doi.org/10.1016/j.jnutbio.2019.03.009
• Zheng, Y., Hu, G., Wu, W., Zhao, Z., Meng, S., Fan, L., Song, C., Qiu, L., & Chen, J. (2019). Transcriptome analysis of juvenile genetically improved farmed tilapia (Oreochromis niloticus) livers by dietary resveratrol supplementation. Comparative Biochemistry and Physiology Part C: Toxicology & Pharmacology, 223, 1-8. https://doi.org/10.1016/j.cbpc.2019.04.011 ‏