Biochemical and immune response in red tilapia (Oreochromis mossambicus × O. niloticus) with dietary chitosan supplementation

• Yuniel Méndez-Martínez Facultad de Ciencias Pecuarias, Universidad Técnica Estatal de Quevedo (UTEQ), Quevedo, Los Ríos, Ecuador https://orcid.org/0000-0002-5365-5794
• Ginger K. Pacheco-Morales Facultad de Ciencias Pecuarias, Universidad Técnica Estatal de Quevedo (UTEQ), Quevedo, Los Ríos, Ecuador https://orcid.org/0000-0003-0212-9441
• Karla A. Del Barco-Ibarra Facultad de Ciencias Pecuarias, Universidad Técnica Estatal de Quevedo (UTEQ), Quevedo, Los Ríos, Ecuador https://orcid.org/0000-0001-9389-1604
• Yenny G. Torres-Navarrete Facultad de Ciencias Pecuarias, Universidad Técnica Estatal de Quevedo (UTEQ), Quevedo, Los Ríos, Ecuador https://orcid.org/0000-0003-3056-8708
• Martha P. Hernández-Vergara División de Estudios de Posgrado e Investigación, Instituto Tecnológico de Boca del Río, Boca del Río, Veracruz, México https://orcid.org/0000-0002-1589-1913

Keywords: glucose, immunostimulant, leukocytes, protein, superoxide dismutase, triglycerides

Abstract

The use of biostimulants in fish diets is a promising strategy to reduce the use of antibiotics, enhance the biochemical and immune response, which contributes to improving productive yields and reducing economic losses. The biochemical and immune response was evaluated in juvenile red tilapia (Oreochromis mossambicus × ​​O. niloticus), with different levels: 0 (control), 1, 2, 3, 4 and 5% chitosan in diet. 270 animals (7.53 ± 0.50 g of initial weight), distributed in a completely randomized design of 6 treatments with 3 replicates and 45 tilapia.treatment^-1, were sown in 18 tanks with 90 L of water in a closed system. The juveniles were fed for 55 days with the experimental diets and at the end of the bioassay the tissue and blood plasma samples were taken. Differences were found (p<0.05) in the variables evaluated responses, where the content of lipids, triglycerides, cholesterol, carbohydrates and glucose showed higher levels (p<0.05) at lower chitosan concentrations. However, for protein content, a better response (p<0.05) was found at higher levels of chitosan in the diet. Regarding dry matter and ash, no differences were found (p˃0.05). While superoxide dismutase and leukocytes were found in higher concentration (p<0.05) when supplemented with chitosan by 3 and 4%. It was concluded that the juvenile biochemical and immune response of red tilapia was favored with dietary chitosan supplementation.

References

Abdel-Ghany, H. M. and M. E. S. Salem. 2019. Effects of dietary chitosan supplementation on farmed fish; a review. Rev. Aquacult. 12(1): 438-452. https://doi.org/10.1111/raq.12326
Alishahi, A. and M. Aïder. 2012. Applications of chitosan in the seafood industry and aquaculture: a review. Food Bioproc Tech. 5(3): 817-830. https://doi.org/10.1007/s11947-011-0664-x
Al‐Sagheer, A., H. Mahmoud, F. Reda, S. Mahgoub and M. Ayyat. 2018. Supplementation of diets for Oreochromis niloticus with essential oil extracts from lemongrass (Cymbopogon citratus) and geranium (Pelargonium graveolens) and effects on growth, intestinal microbiota, antioxidant and immune activities. Aquacult. Nutr. 24: 1006-1014. https://doi.org/10.1111/anu.12637
Association of Official Analytical Chemists International (AOAC). 2019. Official Methods of Analysis of AOAC International, 21st Edition. Gaithersburg, Maryland, USA. https://www.aoac.org/official-methods-of-analysis-21st-edition-2019/
Azaza, M. S., K. Wassim, F. Mensi, A. Abdelmouleh, B. Brini and M. M. Kraϊem. 2009. Evaluation of faba beans (Vicia faba L. var. minuta) as a replacement for soybean meal in practical diets of juvenile Nile tilapia Oreochromis niloticus. Aquaculture. 287: 174-179. doi:10.1016/j.aquaculture.2008.10,007
Azizoglu, A. and I. Cengizler. 1996. An investigation on determination of some hematologic parameters in healthy Oreochromis niloticus (L.). Turk. J. Vet. Anim. Sci. 20: 425-431.
Biller, J. D. and L. S. Takahashi. 2018. Oxidative stress and fish immune system: phagocytosis and leukocyte respiratory burst activity. An. Acad. Bras. Ciênc. 90 (4): 3403-3914. https://doi: 10.1590/0001-3765201820170730.
Brum, A., S. A. Pereira, M. S. Owatari, E. C. Chagas, F. C. M. Chaves, J. L. P. Mouriño and M. L. Martins. 2017. Effect of dietary essential oils of clove basil and ginger on Nile tilapia (Oreochromis niloticus) following challenge with Streptococcus agalactiae. Aquaculture 468: 235-243. https://doi.org/10.1016/j.aquaculture.2016.10,020
Esteban, M. A., A. Cuesta, J. Ortuno and J. Meseguer. 2001. Immunomodulatory effects of dietary intake of chitin on gilthead seabream (Sparus aurata L.) innate immune system. Fish Shellfish Immunol. 11: 303-315. https://doi.org/10.1006/fsim.2000,0315
Fadl, S.E., G. A. El-Gammal, W.S. Abdo, M. Barakat, O. A. Sakr, E. Nassef, D. M. Gad and H. S. El-Sheshtawy, 2020. Evaluation of dietary chitosan effects on growth performance, immunity, body composition and histopathology of Nile tilapia (Oreochromis niloticus) as well as the resistance to Streptococcus agalactiae infection. Aquac. Res. 51: 1120-1132. https://doi.org/10.1111/are.14458
FAO. 2020. FishStatJa tool for fishery statistics analysis, Release 2.0,0. Universal software for fishery statistical time series. Global capture and aquaculture production: Quantities 1950-2018; Aquaculture values 1984-2018. Food and Agriculture Organization (FAO) Fisheries Department, Fishery Information, Data and Statistics Unit. Rome. http://www.fao.org/fishery/
Goddard, S. 1996. Feeding and diet. p.23-33. In: Chapman and Hall (Eds). Feed Management in Intensive Aquaculture. New York. USA. https://doi.org/10.1007/978-1-4613-1173-7_2
Hanington, P. C., J. Tam, B. A. Katzenback, S. J. Hitchen, D. R. Barreda and M. Belosevic. 2009. Development of macrophages of cyprinid fish. Dev. Comp. Immunol. 33: 411-429. https://doi.org/10.1016/j.dci.2008.11.004
Heo, G. J., J. H. Kim, B. G. Jeon and K. Y. R. J. Park. 2001. Effects of FST-chitosan mixture on cultured rockfish (Sebastes schlegelii) and olive flounder (Paralichthys olivaceus). Korean J. Vet. Public. Heal. 25(3): 141-149.
Hrubec, T. and S. Smith. 2010. Hematology of Fishes. p. 994-1003. In: Weiss, D. J., Wardrop, K. J. and O. W. Schalm´s (Eds). Veterinary Hematology, 6ta Edition. Wiley-Blackwell. Lowa, USA. https://www.worldcat.org/title/schalms-veterinary-hematology/oclc/338288636
Jim, F., P. Garamumhango and C. Musara. 2017. Comparative analysis of nutritional value of Oreochromis niloticus (Linnaeus), Nile Tilapia, Meat from three different ecosystems. J. Food Qual. https: //doi.org/10.1155/2017/6714347
Kim, K. W. and R. L. Thomas. 2007. Antioxidative activity of chitosans with varying molecular weights. Food Chem. 101: 308-313. https: //doi.org/10.1016/j.foodchem.2006.01.038
Kumari, J. and P. K. Sahoo. 2006. Dietary levamisole modulates the immune response and disease resistance of Asian catfish Clarias batrachus (Linnaeus). Aquac Res. 37(5): 500-509. https://doi.org/10.1111/j.1365-2109.2006.01456.x
Lara-Flores, M., M. A. Olvera-Novoa, B. E. Guzmán-Méndez and W. López-Madrid. 2003. Use of the bacteria Streptococcus faecium and Lactobacillus acidophilus, and the yeast Saccharomyces cerevisiae as growth promoters in Nile tilapia (Oreochromis niloticus). Aquaculture 216(4): 193-201. https://doi.org/10.1016/S0044-8486(02)00277-6
Li, S., C. Sang, J. Zhang, N. Chen, Z. Li, P. Jin and X. Huang. 2018. Effects of acute hyperglycemia stress on plasma glucose, glycogen content, and expressions of glycogen synthase and phosphorylase in hybrid grouper (Epinephelus fuscoguttatus ♀ × E. lanceolatus ♂). Fish Physiol. Biochem. 44: 1185–1196. https://doi.org/10.1007/s10695-018-0508-y
Mahmoud, H. K., A. A. Al-Sagheer, F. M. Reda, S. A. Mahgoub and M. S. Ayyat. 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
Malachy, N. O. A, K. P. Pramod, K. Kumar and P. Nalini. 2017. Assessment of mutagenic, hematological and oxidative stress biomarkers in liver of Nile tilapia, Oreochromis niloticus (Linnaeus, 1758) in response to sublethal verapamil exposure. Drug Chem. Toxicol. 40(3): 286-294. https://doi.org/10.1080/01480545.2016.1219914
Mastan, S. A. 2015. Use of immunostimulants in aquaculture disease management. Int. J. Fish. Aquat. Stud. 2(4): 277-280. https://www.fisheriesjournal.com/archives/2015/vol2issue4/PartF/2-4-59.pdf
McCord, J. M. and I. Fridovich. 1969. Superoxide dismutase: an enzymic function for erythrocuprein (hemocuprein). J. Biol. Chem. 244:6049-6055. https://doi.org/10.1016/S0021-9258(18)63504-5
Mehana, E. E., H. A. Rahmani and M. S. Aly. 2015. Immunostimulants and Fish Culture: An Overview. Annu. Res. Rev. Biol. 5(6): 477-489. https://doi.org/10.9734/ARRB/2015/9558
Méndez-Martínez, Y., Y. G. Torres-Navarrete, Y. Pérez-Tamames, M. Romás-Viltres, y E. Cortés-Jacinto (2021). Effect of duckweed meal dietary inclusion on growth performance and survival of African catfish fingerlings. Rev. Fac. Agron. (LUZ) 38(1): 84-104. https://doi.org/10.47280/RevFacAgron(LUZ)
Méndez-Martínez, Y., Y. Pérez, D.M. Verdecia, E. Cortés-Jacinto, O.F. Cevallos- Falquez, y O. Romero. 2019. Effect of the inclusion of Azolla filiculoides meal on the growth and survival of red tilapia small fish (Oreochromis mossambicus x O. niloticus). Cuba. J. Agric. Sci. 53: (2): 289-299. http://scielo.sld.cu/pdf/cjas/v53n3/2079-3480-cjas-53-03-289.pdf
Miao, Z., L. Guo, Y. Liu, W. Zhao and J. Zhang. 2020. Effects of dietary supplementation of chitosan on carcass composition and meat quality in growing Huoyan geese. Poult. Sci. J. 99(6): 3079-3085. https://doi.org/10.1016/j.psj.2020,03.025
Nakanishi, T., Y. Shibasaki, Y. Matsuura. 2015. T Cells in Fish. Biology. 4: 640-663. https://doi.org/10.3390/biology4040640
Ngo, D.-H. and S.-K. Kim. 2014. Antioxidant effects of chitin, chitosan, and their derivatives. Adv. Food Nutr. Res. 73: 15-31. https://doi.org/10.1016/B978-0-12-800268-1.00002-0.
Pérez, R., B. Romeu, M. Lastre, Y. Morales, O. Cabrera, L. Reyes, E. González, S. Sifontes, y O. Pérez. 2014. Inmunopotenciadores para la acuicultura TT-Immunepotentiators for the Aquaculture. Vaccimonitor. 23(1): 24–31. http://scielo.sld.cu/pdf/vac/v23n1/vac05114.pdf
Press, C. M. and O. Evensen. 1999. The morphology of the immune system in teleost fishes. Fish Shellfish Immunol. 9: 309-318. https://doi.org/10.1006/fsim.1998.0181
Sakai, M., H. Kamiya, S. Ishii, S. Atsuta and M. Kobayashi. 1992. The immunostimulating effects on chitin in rainbow trout Oncorhynchus mykiss. Dis. Asian Aquacult. 1: 413-417.
Schettler G. and E. NusselE. 1975. Colorimetric determination of Triglycerides and cholesterol. Arb. Med. Soz. Med. Prav. Med. 10: 25.
Trinder, P. 1969. Determination of blood glucose using an oxidaseperoxidase system with a non-carcinogenic chromogen. J. Clin. Path. 22(2): 158-161. DOI: 10.1136/jcp.22.2.158
Soberanes-Yepiz, M. L., Y. Méndez-Martínez, M. U. García-Guerrero, F. Ascencio, J. Violante-González, S. García-Ibañez, y E. Cortés-Jacinto. 2018. Superoxide dismutase activityin tissues of juvenile cauque river prawn (Macrobrachium americanum Bate, 1868) fed with different levels of protein and lipid. Lat. Am. J. Aquat. Res. 46(3):543–55. http://doi.org/10.3856/vol46-issue3-fulltext-7
Szwejser, E.,B. M. L. K. Verburg-van, M. Maciuszek, and M. Chadzinska. 2017. Estrogen-dependent seasonal adaptations in the immune response of fish. Horm. Behav. 88: 15-24. https://doi.org/10.1016/j.yhbeh.2016.10,007
Udo, I. U., U. Etukudo and U. I. U. Anwana. 2018. Effects of chitosan and chitosan nanoparticles on water quality, growth performance, survival rate and meat quality of the African catfish, Clarias gariepinus. Nanoscience. 1(1): 12-25. https://doi.org/10.31058/j.nano.2018.11002
Zaki, M. A., M. El-S. Salem, M. M. Gaber and A. M. Nour. 2015. Effect of chitosan supplemented diet on survival, growth, feed utilization, body composition and histology of seabass (Dicentrarchus labrax). World Journal of Engineering and Technology. 3: 38-47. https://doi.org/10.4236/wjet.2015.34C005
Zapata, A. G., A. Chibá and A. Varas. 1996. Cells and tissues of the immune system of fish. p. 61-62. In: Iwama, G., and T. Nakanishi (Eds). The fish immune system: organism, pathogen and environment. Academic Press, Ltd., London. https://agris.fao.org/agris-search/search.do?recordID=US9731677
Zhang, P, J. Iwasaki-Arai, H. Iwasaki, M. L. Fenyus, T. Dayaram, and B. M. Owens. 2004. Enhancement of hematopoietic stem cell repopulating capacity and self-renewal in the absence of the transcription factor C/EBP alpha. Immunity. 21(6): 853-863. https://doi.org/10.1016/j.immuni.2004.11.006.