Effect of dietary tannins on productive parameters and diesel toxicity in juvenile Nile tilapia (Oreochromis niloticus)

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Julio César Cruz-Valdez
Oscar Daniel García Pérez
Rodrigo Gallardo-Morales
Jorge Ramsy Kawas-Garza
Denisse Garza-Hernández
Alicia Guadalupe Marroquín-Cardona

Abstract

Nile tilapia is a highly nutritious source of protein, and its production through aquaculture practices leads to a lower carbon footprint when compared to the production of terrestrial species. However, environmental contamination poses a significant risk in aquaculture, necessitating strategies to mitigate its impacts on fish. This study evaluated the effects of experimental diets supplemented with tannins on performance parameters of Oreochromis niloticus over a 60-day feeding trial. At the end of the experiment, their potential hepatoprotective role was assessed in fish exposed to diesel-induced toxicity. The fish were fed a control diet (T1) or a diet supplemented with either 2 % (T2) or 4 % tannins (T3). Fourteen fish per tank were allocated across three tanks per treatment. After 60 days, seven fish from each treatment group were exposed to an acute diesel exposure to either an acute dose of diesel (50 µg/g) or fish oil (control). Performance parameters were then compared, and liver samples were obtained and used to determine alkaline phosphatase (ALP), carboxylesterase (CaE), and glutathione S-transferase (GST) enzymatic activity. Diesel exposure led to increased ALP activity, decreased CaE, and GST activities. However, no significant alterations in enzyme activities were observed in fish maintained under dietary treatments T2 and T3 following diesel exposure compared to the control group. Moreover, performance parameters remained unaffected by the inclusion of tannins in diets. These findings suggest that dietary tannins may provide a protective effect against diesel-induced physiological disturbances.

Keywords:
diesel toxicity, enzyme activity, Dietary tannins, Nile tilapia nutrition, Aquatic toxicology, Growth performance in fish, Oxidative stress in fish

Article Details

References

Olusola SE, Emikpe BO, Olaifa FE. The potentials of medicinal plant extracts as bio-antimicrobials in aquaculture. International Journal of Medicinal and Aromatic Plants. 2013;3(3):404–412.

Meijide FJ, da Cuna RH, Prieto JP, Dorelle LS, Babay PA, Lo Nostro FL. Effects of waterborne exposure to the antidepressant fluoxetine on swimming, shoaling, and anxiety behaviours of the mosquitofish Gambusia holbrooki. Ecotoxicology and Environmental Safety. 2018;163:646–655. doi: 10.1016/j.ecoenv.2018.07.085. DOI: https://doi.org/10.1016/j.ecoenv.2018.07.085

Zhu S, Zhang Z, Zagar D. Mercury transport and fate models in aquatic systems: a review and synthesis. Science of the Total Environment. 2018;639:538–549. doi: 10.1016/j.scitotenv.2018.04.397. DOI: https://doi.org/10.1016/j.scitotenv.2018.04.397

Bastardo A, Ravelo C, Castro N, Calheiros J, Romalde JL. Effectiveness of bivalent vaccines against Aeromonas hydrophila and Lactococcus garvieae infections in rainbow trout Oncorhynchus mykiss (Walbaum). Fish Shellfish Immunology. 2012;32(5):756–761. doi: 10.1016/j.fsi.2012.01.028. DOI: https://doi.org/10.1016/j.fsi.2012.01.028

Nogueira L, Madeira-Sanchez AL, da Silva DGH, Cid-Ferrizi V, Benedito-Moreira A, Alves de Almeida E. Biochemical biomarkers in Nile tilapia (Oreochromis niloticus) after short-term exposure to diesel oil, pure biodiesel and biodiesel blends. Chemosphere. 2011;85:97–105. doi: 10.1016/j.chemosphere.2011.05.037. DOI: https://doi.org/10.1016/j.chemosphere.2011.05.037

Mohammadi M, Mirza-Alizadeh A, Mollakhalili-Meybodi N. Off-Flavors in fish: a review of potential development mechanisms, identification and prevention methods. Journal of Human Environment and Health Promotion. 2021;7(3):120–128. doi: 10.52547/jhehp.7.3.120. DOI: https://doi.org/10.52547/jhehp.7.3.120

Shukla G. A review on liver enzymes as a useful biomarker to evaluate the effects of pesticides on freshwater fish. World Journal of Biology Pharmacy and Health Sciences. 2024;19:171–176. DOI: https://doi.org/10.30574/wjbphs.2024.19.1.0405

Wheelock CE, Miller JL, Miller MJ, Phillips BM, Huntley SA, Gee SJ, Tjeerdema RS, Hammock BD. Use of carboxylesterase activity to remove pyrethroid‐associated toxicity to Ceriodaphnia dubia and Hyalella azteca in toxicity identification evaluations. Environmental Toxicology and Chemistry. 2006;25(4):973–984. DOI: https://doi.org/10.1897/05-334R.1

Aguilera-González C, Cruz J, Mendoza-Alfaro R. Physiological response of alligator gar juveniles (Atractosteus spatula) exposed to sub-lethal doses of pollutants. Fish Physiology and Biochemistry. 2015;41:1015–1027. doi: 10.1007/s10695-015-0066-5. DOI: https://doi.org/10.1007/s10695-015-0066-5

Abdel-Latif HM, Abdel-Daim MM, Shukry M, Nowosad J, Kucharczyk D. Benefits and applications of Moringa oleifera as a plant protein source in Aquafeed: a review. Aquaculture. 2022;547:737369. doi: 10.1016/j.aquaculture.2021.737369. DOI: https://doi.org/10.1016/j.aquaculture.2021.737369

Prusty AK, Sahu NP, Pal AK, Reddy AK, Kumar S. Effect of dietary tannin on growth and haemato-immunological parameters of Labeo rohita (Hamilton) fingerling. Animal Feed Science and Technology. 2007;136:96–108. doi: 10.1016/j.anifeedsci.2006.08.023. DOI: https://doi.org/10.1016/j.anifeedsci.2006.08.023

Muniyandi K, George E, Sathyanarayanan S, George BP, Abrahamse H, Thamburaj S, Thangaraj P. Phenolics, tannins, flavonoids, and anthocyanins contents influenced antioxidant and anticancer activities of Rubus fruits from Western Ghats, India. Food Science and Human Wellness. 2019;8(1):73–81. doi: 10.1016/j.fshw.2019.03.005. DOI: https://doi.org/10.1016/j.fshw.2019.03.005

Adejoro FA, Hassen A, Akanmu AM. Effect of lipid-encapsulated acacia tannin extract on feed intake, nutrient digestibility, and methane emission in sheep. Animals. 2019;9(11):863. doi: 10.3390/ani9110863. DOI: https://doi.org/10.3390/ani9110863

Nogueira L, Humberto da Silva DGH, Kikuchi-Oliveira TY, Correa da Rosa JM, Arantes-Felicio A, Alves de Almeida E. Biochemical responses in armored catfish (Pterygoplichthys anisitsi) after short-term exposure to diesel oil, pure biodiesel and biodiesel blends. Chemosphere. 2013;93:311–319. doi: 10.1016/j.chemosphere.2013.04.083. DOI: https://doi.org/10.1016/j.chemosphere.2013.04.083

Bradford MM. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry. 1976;72(1–2):248–254. doi: 10.1016/0003-2697(76)90527-3. DOI: https://doi.org/10.1016/0003-2697(76)90527-3

Mazorra M, Rubio J, Blasco J. Acid and alkaline phosphatase activities in the clam Scrobicularia plana: kinetic characteristics and effects of heavy metals. Comparative Biochemistry and Physiology Part B: Biochemical and Molecular Biology. 2002;131:241–249. doi: 10.1016/S1096-4959(01)00502-4. DOI: https://doi.org/10.1016/S1096-4959(01)00502-4

Wilce MC, Parker MW. Structure and function of glutathione S-transferases. Biochimica et Biophysica Acta (BBA) –Protein Structure and Molecular Enzymology. 1994;1205 (1):1–18. doi: 10.1016/0167-4838(94)90086-8. DOI: https://doi.org/10.1016/0167-4838(94)90086-8

Brodeur JC, Suarez RP, Natale GS, Ronco AE, Zaccagnini ME. Reduced body condition and enzymatic alterations in frogs inhabiting intensive crop production areas. Ecotoxicology and Environmental Safety. 2011;74:1370–1380. doi: 10.1016/j. ecoenv.2011.04.024. DOI: https://doi.org/10.1016/j.ecoenv.2011.04.024

Buyukcapar HM, Atalay Aİ, Kamalak A. Growth performance of Nile tilapia (Oreochromis niloticus) fed with diets containing different levels of hydrolysable and condensed Tannin. Journal of Agricultural Science and Technology. 2011;13:1045–1051.

Peng K, Wang G, Zhao H, Wang Y, Mo W, Wu H, Huang Y. Effect of high level of carbohydrate and supplementation of condensed tannins on growth performance, serum metabolites, antioxidant and immune response, and hepatic glycometabolism gene expression of Lateolabrax japonicus. Aquaculture Reports. 2020b, Rep 18: 100515. doi: 10.1016/j.aqrep.2020.100515. DOI: https://doi.org/10.1016/j.aqrep.2020.100515

Yancheva V, Stoyanova S, Velcheva I, Georgieva E. Fish as indicators for environmental monitoring and health risk assessment regarding aquatic contamination with pesticides. International Journal of Zoology and Animal Biology. 2020;3:1–4. doi: 10.23880/izab-16000210. DOI: https://doi.org/10.23880/IZAB-16000210

Huang TL, Obih PO, Jaiswal R, Hartley WR, Thiyagarajah A. Evaluation of liver and brain esterases in the spotted gar fish (Lepisosteus oculatus) as biomarkers of effect in the lower Mississippi River basin. Bulletin of Environmental Contamination and Toxicology. 1997;58:688–695. doi: 10.1007/s001289900388. DOI: https://doi.org/10.1007/s001289900388

Simonato JD, Guedes CLB, Martinez CBR. Biochemical, physiological, and histological changes in the neotropical fish Prochilodus lineatus exposed to diesel oil. Ecotoxicology and Environmental Safety. 2008;69:112–120. doi: 10.1016/j.ecoenv.2007.01.012. DOI: https://doi.org/10.1016/j.ecoenv.2007.01.012

Zhang JF, Wang XR, Guo HY, Wu JC, Xue YQ. Effects of water-soluble fractions of diesel oil on the antioxidant defenses of the goldfish, Carassius auratus. Ecotoxicology Environmental Safety. 2004;58:110–116. doi: 10.1016/j.ecoenv.2003.08.025. DOI: https://doi.org/10.1016/j.ecoenv.2003.08.025

Van der Oost R, Beyer J, Vermeulen NPE. Fish bioaccumulation and biomarkers in environmental risk assessment: a review. Environmental Toxicology and Pharmacology. 2003;13:57–149. DOI: https://doi.org/10.1016/S1382-6689(02)00126-6

Zhang JF, Shen H, Xu TL, Wang XR, Li WM, Gu YF. Effects of long-term exposure to low-level diesel oil on the antioxidant defense system of fish. Bulletin of Environmental Contamination and Toxicology. 2003;71:234–239. doi: 10.1007/s00128-003-0155-5. DOI: https://doi.org/10.1007/s00128-003-0155-5

Kopecka-Pilarczyk J, Correia AD. Biochemical response in gilthead seabream (Sparus aurata) to in vivo exposure to a mix of selected PAHs. Ecotoxicology Environmental Safety. 2009;72:1296–1302. doi: 10.1016/j.ecoenv.2008.12.003. DOI: https://doi.org/10.1016/j.ecoenv.2008.12.003

Almeida EA, Bainy ACD, Loureiro APM, Martinez GR, Miyamoto S, Onuki J, Barbosa LF, Garcia CCM, Prado FM, Ronsein GE, Sigolo CA, Brochini CB, Martins AMG, Medeiros MHG, Mascio P. Oxidative stress in Perna perna and other bivalves as indicators of environmental stress in the Brazilian marine environment: antioxidants, lipid peroxidation, and DNA damage. Comparative Biochemistry and Physiology Part A: Molecular and Integrative Physiology. 2007;146:588–600. doi: 10.1016/j.cbpa.2006.02.040. DOI: https://doi.org/10.1016/j.cbpa.2006.02.040

Aich A, Goswami AR, Roy US, Mukhopadhyay SK. Ecotoxicological assessment of tannery effluent using guppy fish (Poecilia reticulata) as an experimental model: a biomarker study. Journal of Toxicology and Environmental Health Part A. 2015;78(4): 278–286. doi: 10.1080/15287394.2014.960045. DOI: https://doi.org/10.1080/15287394.2014.960045

Al-Attar AM. The influence of dietary grapeseed oil on DMBA-induced liver enzymes disturbance in the frog, Rana ridibunda. Pakistan Journal of Nutrition. 2004;3(5):304–309. doi: 10.3923/pjn.2004.304.309. DOI: https://doi.org/10.3923/pjn.2004.304.309

Firat O, Cogun HY, Yuzereroglu TA, Go ̈k G, Kargin F, Kotemen Y. A comparative study on the effects of a pesticide (cypermethrin) and two metals (copper, lead) to (sic.) serum biochemistry of Nile tilapia, Oreochromis niloticus. Fish Physiology and Biochemistry. 2011;37(3):657–666. doi: 10.1007/s10695-011-9466-3. DOI: https://doi.org/10.1007/s10695-011-9466-3

Huang Q, Liu X, Zhao G, Hu T, Wang Y. Potential and challenges of tannins as an alternative to in-feed antibiotics for farm animal production. Animal Nutrition and Feed Technology. 2018;4(2):137–150. doi: 10.1016/j.aninu.2017.09.004. DOI: https://doi.org/10.1016/j.aninu.2017.09.004

Peng K, Wang G, Wang Y, Chen B, Sun Y, Mo W, Li G, Huang Y. 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. 2020a;269:114671. doi: 10.1016/j.anifeedsci.2020.114671. DOI: https://doi.org/10.1016/j.anifeedsci.2020.114671

Hajra A, Mazumder A, Verma A, Ganguly DP, Mohanty BP, Sharma AP. Antinutritional factors in plant-origin fish feed ingredients: the problems and probable remedies. In: UC Goswami, editor. Advances in Fish Research. Delhi, India: Narendra Publishing House; 2013 pp.193–202.

Code of Federal Regulations. Select Committee on GRAS Substances opinion: tannic acid (hydrolyzable gallotannins). 1977. Title 21(3): 21CFR184. 1097. FDA. https://www.accessdata.fda.gov/scripts/cdrh/cfdocs/cfCFR/CFRSearch.cfm?fr=184.1097.

Jeronimo E, Pinheiro C, Lamy E, Dentinho MT, Sales-Baptista E, Lopes O, Capela e Silva F. Chapter: 5. Tannins in ruminant nutrition: impact on animal performance and quality of edible products. In: CA Combs, editor. Tannins: Biochemistry, Food Sources and Nutritional Properties. Biochemistry Research Trends, Series. New York, US: Nova Science Publishers; 2016.

Caprarulo V, Giromini C, Rossi L. Review: chestnut and quebracho tannins in pig nutrition, the effects on performance and intestinal health. Animal. 2021;15(1):100064. doi: 10.1016/j.animal.2020.100064. DOI: https://doi.org/10.1016/j.animal.2020.100064

Chen B, Qiu J, Wang Y, Huang W, Zhao H, Zhu X, Peng K. Condensed tannins increased intestinal permeability of Chinese seabass (Lateolabrax maculatus) based on microbiome-metabolomics analysis. Aquaculture. 2022;560:738615. doi: 10.1016/j.aquaculture.2022.738615. DOI: https://doi.org/10.1016/j.aquaculture.2022.738615

Redondo EA, Redondo LM, Bruzzone OA, Diaz-Carrasco JM, Cabral C, Garces VM, Liñeiro MM, Fernandez-Miyakawa ME. Effects of a blend of chestnut and quebracho tannins on gut health and performance of broiler chickens. PLoS ONE. 2022;17(1):e0254679. doi: 10.1371/journal.pone.0254679. DOI: https://doi.org/10.1371/journal.pone.0254679

Paolini V, Bergeaud JP, Grisez C, Prevot F, Dorchies P, Hoste H. Effects of condensed tannins on goats experimentally infected with Haemonchus contortus. Veterinary Parasitology. 2003;113(3-4):253–261. doi: 10.1016/S0304-4017(03)00064-5. DOI: https://doi.org/10.1016/S0304-4017(03)00064-5