Chemoprotection of amazonian Mauritia flexuosa fruit pulp against ammonia and nitrite toxicity to postlarvae shrimps Litopenaeus vannamei




bioactive molecules, nitrogen compounds, functional feed, sustainable aquaculture


The chemoprotection of "buriti†Mauritia flexuosa (inclusion in diet: 0-control group; 1.25; 2.50; 5.00; and 10.00% W/W) to Litopenaeus vannamei postlarvae (PL) exposed to ammonia or nitrite was investigated. Analyzed variables include antioxidant (ACAP) and oxidative damage (TBARS) responses and levels of total carotenoids. The results indicated that there was no significant difference (p >0.05) in zootechnical variables between diets. The PL carotenoid content (R2 = 0.86), ACAP (R2 = 0.78), and TBARS (R2 = 0.91) showed a dose-dependent relationship with the inclusion levels of "buriti†(p <0.05). After 43 days, juvenile shrimps were exposed for 96 h to ammonia (0.48 mg NH3-N L-1) or nitrite (40 mg NO3 L-1). Higher scavenging activity against peroxyl radicals was observed in PL fed with 2.50 and 5.00% of "buriti†(ammonia exposure), or 5.00 and 10.00% (nitrite exposure) of "buriti†inclusion. Content of reduced glutathione was higher in shrimps exposed to ammonia and fed with 10.00% of "buritiâ€Â. Lipid peroxidation levels were lower in shrimps exposed to ammonia or nitrite and previously fed with inclusion higher than 2.50% of "buritiâ€Â. The increased scavenging activity and lower lipid peroxidation in ammonia or nitrite-exposed organisms and previously supplemented with "buriti†point to a hormetic response that increases the resilience of L. vannamei to cope with nitrogenous compounds, pointing to the use of this fruit as a chemoprotectant agent.


Agathokleous, E. 2018. Environmental hormesis, a fundamental non-monotonic biological phenomenon with implications in ecotoxicology and environmental safety. Ecotoxicology and Environmental Safety, 148: 1042-1053.

Albuquerque, M.L.S.; Guedes, I.; Alcantara, P.; Moreira, S.G.C.; Barbosa Neto, N.M.; Correa, D.S.; Zilio, S.C. 2005. Characterization of Buriti (Mauritia flexuosa L.) oil by absorption and emission spectroscopies. Journal of Brazilian Chemical Society, 16(6a): 1113-1117.

Amado, L.L.; Garcia, M.L.; Ramos, P.B.; Freitas, R.F.; Zafalon, B.; Ferreira, J.L.R.; Yunes, J.S.; Monserrat, J.M. 2009. A method to measure total antioxidant capacity against peroxyl radicals in aquatic organisms: Application to evaluate microcystins toxicity. Science of the Total Environment, 407(6): 2115-2123.

Arnold, S.J.; Sellars, M.J.; Crocos, P.J.; Coman, G.J. 2006. Intensive production of juvenile tiger shrimp Penaeus monodon: An evaluation of stocking density and artificial substrates. Aquaculture, 261(3): 890-896.

APHA - American Public Health Association. 1998. Standard methods for the examination of water and wastewater (20th ed.). Washington, DC: APHA - American Public Health Association, 1193p.

Berry, R.; López-Martí­­nez, G. 2020. A dose of experimental hormesis: When mild stress protects and improves animal performance. Comparative Biochemistry and Physiology, Part A: Molecular & Integrative Physiology, 242: 110658.
Birnie-Gauvin, K.; Costantini, D.; Cooke S.J.; Willmore, W.G. 2017. A comparative and evolutionary approach to oxidative stress in fish: A review. Fish and Fisheries, 18(5): 928-942.

Calabrese, E.J.; Agathokleous, E. 2020. Theodosius Dobzhansky’s view on biology and evolution v.2.0: "Nothing in biology makes sense except in light of evolution and evolution’s dependence on hormesis-mediated acquired resilience that optimizes biological performance and numerous diverse short. Environmental Research, 186: 109559.

Chen, J.C.; Liu, P.C.; Lei, S.C. 1990. Toxicities of ammonia and nitrite to Penaeus monodon adolescents. Aquaculture, 89(2): 127-137.

Chen, X.; Lin, H.Z.; Jiang, S.G.; Wu, K.C.; Liu, Y.J.; Tian, L.X.; Niu, J. 2013. Dietary supplementation of honeysuckle improves the growth, survival and immunity of Penaeus monodon. Fish and Shellfish Immunology, 35(1): 161-169.

Colombo, G.M.; dos Santos Simião, C.; Schmitz, M.J.; Pedrosa, V.F.; Romano, L.A.; Tesser, M.B.; Ramos,P.B.; Wasiliesky, W.; Monserrat, J.M. 2020. The role of açaí­­ (Euterpe oleracea Mart. 1824) as a chemoprotective agent in the evaluation of antioxidant defence, oxidative damage and histology of juvenile shrimp Litopenaeus vannamei (BOONE, 1931) exposed to ammonia. Aquaculture Research, 51(4): 1551-1566.

Colt, J. 2002. List of spreadsheets prepared as a complement to the book Fish Hatchery Management. In: Wedemeyer, G.A. (ed.). American Fisheries Society Publication, 751p. Available at: Accessed: Sept. 21, 2013.

Craig, S.; Helfrich, L. 2017. Understanding fish nutrition, feeds, and feeding. Virginia Cooperative Extension, 420(256): 1-6.

Da Silva, F.O.; Tramonte, V.L.C.G.; Parisenti, J.; Lima-Garcia, J.F.; Maraschin, M.; Da Silva, E.L. 2015. Litopenaeus vannamei muscle carotenoids versus astaxanthin: A comparison of antioxidant activity and in vitro protective effects against lipid peroxidation. Food Bioscience, 9: 12-19.
De Jesus Raposo, M.F.; De Morais, A.M.M.B.; De Morais, R.M.S.C. 2015. Carotenoids from marine microalgae: A valuable natural source for the prevention of chronic diseases. Marine Drugs, 13(8): 5128-5155.

Duan, Y.; Zhang, J.; Dong, H.; Wang, Y.; Liu, Q.; Li, H. 2015. Oxidative stress response of the black tiger shrimp Penaeus monodon to Vibrio parahaemolyticus challenge. Fish and Shellfish Immunology, 46(2): 354-365.

Elizondo-González, R.; Quiroz-Guzmán, E.; Escobedo-Fregoso, C.; Magallón-Serví­­n, P.; Peí­±a-Rodrí­­guez, A. 2018. Use of seaweed Ulva lactuca for water bioremediation and as feed additive for white shrimp Litopenaeus vannamei. PeerJ, 6: e4459

Esparza-Leal, H.M.; Cardozo, A.P.; Wasielesky, W. 2015. Performance of Litopenaeus vannamei postlarvae reared in indoor nursery tanks at high stocking density in clear-water versus biofloc system. Aquacultural Engineering, 68: 28-34.

Failla, M.L.; Chitchumronchokchai, C.; Ferruzzi, M.G.; Goltz, S.R.; Campbell, W.W. 2014. Unsaturated fatty acids promote bioaccessibility and basolateral secretion of carotenoids and α-tocopherol by Caco-2 cells. Food & Function, 6: 1101-1112.

Fóes, G.K.; Fróes, C.; Krummenauer, D.; Poersch, L.; Wasielesky, W. 2011. Nursery of pink shrimp Farfantepenaeus paulensis in Biofloc Technology Culture System: Survival and growth at different stocking densities. Journal of Shellfish Research, 30(2): 367-373.

Furtado, P.S.; Poersch, L.H.; Wasielesky, W. 2011. Effect of calcium hydroxide, carbonate and sodium bicarbonate on water quality and zootechnical performance of shrimp Litopenaeus vannamei reared in bio-flocs technology (BFT) systems. Aquaculture, 321(1-2): 130-135.

Gao, Y.; He, Z.; Vector, H.; Zhao, B.; Li, Z.; He, J.; Chu, Z. 2017. Effect of stocking density on growth, oxidative stress and HSP 70 of Pacific white shrimp Litopenaeus vannamei. Turkish Journal of Fisheries and Aquatic Science, 17: 877-884.

Geng, Z.; Liu, Q.; Wang, T.; Ma, S.; Shan, H. 2020. Changes in physiological parameters involved in glutamine and urea synthesis in Pacific white shrimp, Litopenaeus vannamei, fed Ampithoe sp. meal and exposed to ammonia stress. Aquaculture Research, 51(7): 2725-2734.

Han, S.; Wang, B.; Wang, M.; Liu, Q.; Zhao, W.; Wang, L. 2017. Effects of ammonia and nitrite accumulation on the survival and growth performance of white shrimp Litopenaeus vannamei. Invertebrate Survival Journal, 14(1): 221-232.

He, W.; Rahimnejad, S.; Wang, L.; Song, K.; Lu, K.; Zhang, C. 2017. Effects of organic acids and essential oils blend on growth, gut microbiota, immune response and disease resistance of Pacific white shrimp (Litopenaeus vannamei) against Vibrio parahaemolyticus. Fish and Shellfish Immunology, 70: 164-173.

Huang, M.; Xie, J.; Yu, Q.; Xu, C.; Zhou, L.; Qin, J.G.; Chen, L.; Li, E. 2020. Toxic effect of chronic nitrite exposure on growth and health in Pacific white shrimp Litopenaeus vannamei. Aquaculture, 529: 735664.

Jory, D.E.; Cabrera, T.R.; Dugger, D.M.; Fegan, D.; Lee, P.G.; Lawrence, A.L.; Jackson, C.J.; Mcintosh, R.P.; Castaí­±eda, J. 2001. A global review of shrimp feed management: status and perspectives. In: Browdy, C.L.; Jory, D.E. (eds.). The New Wave, Proceedings of the Special Session on Sustainable Shrimp Culture, Aquaculture. The World Aquaculture Society, Baton Rouge, LA, EUA, pp.104-152.

Kütter, M.T.; Romano, L.A.; Ventura-Lima, J.; Tesser, M.B.; Monserrat, J.M. 2014. Antioxidant and toxicological effects elicited by alpha-lipoic acid in aquatic organisms. Comparative Biochemistry and Physiology, Part C: Toxicology & Pharmacology, 162: 70-76.

Lee, C.; Lee, K.J. 2018. Dietary protein requirement of Pacific white shrimp Litopenaeus vannamei in three different growth stages. Fisheries and Aquatic Science, 21(30): 1-6.

León, D.C.M.; Wasiliesky Jr., W.; Monserrat, J.M. 2018. Quercetin influence in water quality and biochemical responses of shrimp Litopenaeus vannamei reared in Biofloc Technology System. Aquaculture Research, 49(11): 3569-3576.

Lin, Y.C.; Chen, J.C. 2001. Acute toxicity of ammonia on Litopenaeus vannamei Boone juveniles at different salinity levels. Journal of Experimental Marine Biology and Ecology, 259(1): 109-119.

Lin, Y.C.; Chen, J.C. 2003. Acute toxicity of nitrite on Litopenaeus vannamei (Boone) juveniles at different salinity levels. Aquaculture, 224(1-4): 193-201.

Mishra, J.K.; Samocha, T.M.; Patnaik, S.; Speed, M.; Gandy, R.L.; Ali, A.M. 2008. Performance of an intensive nursery system for the Pacific white shrimp, Litopenaeus vannamei, under limited discharge condition. Aquacultural Engineering, 38(1): 2-15.

Nga, B.T.; Lürling, M.; Peeters, E.T.H.M.; Roijackers, R.; Scheffer, M.; Nghia, T.T. 2005. Chemical and physical effects of crowding on growth and survival of Penaeus monodon Fabricius post-larvae. Aquaculture, 246(1-4): 455-465.

Niu, J.; Xie, J.J.; Guo, T.Y.; Fang, H.H.; Zhang, Y.M.; Liao, S.Y.; Tian, L.X. 2019. Comparison and evaluation of four species of macro-algaes as dietary ingredients in Litopenaeus vannamei under normal rearing and WSSV challenge conditions: Effect on growth, immune response, and intestinal microbiota. Frontiers in Physiology, 10: 1-15.

Niu, J.; Xie, S. W.; Fang, H.H.; Xie, J.J.; Guo, T.Y.; Zhang, Y.M.; Liu, Y.J. 2018. Dietary values of macroalgae Porphyra haitanensis in Litopenaeus vannamei under normal rearing and WSSV challenge conditions: Effect on growth, immune response and intestinal microbiota. Fish and Shellfish Immunology, 81: 135-149.

Oakes, K.D.; Van der Kraak, G.J. 2003. Utility of the TBARS assay in detecting oxidative stress in white sucker (Catostomus commersoni) populations exposed to pulp mill effluent. Aquatic Toxicology, 63(4): 447-463.

Pakravan, S.; Akbarzadeh, A.; Sajjadi, M.M.; Hajimoradloo, A.; Noori, F. 2017. Partial and total replacement of fish meal by marine microalga Spirulina platensis in the diet of Pacific white shrimp Litopenaeus vannamei: Growth, digestive enzyme activities, fatty acid composition and responses to ammonia and hypoxia stress. Aquaculture Research, 48(11): 5576-5586.

Ramí­­rez-Rochin, J.; Frí­­as-Espericueta, M.G.; Fierro-Saí­±udo, J.F.; Alarcón-Silvas, S.G.; Fregoso-López, M.G.; Páez-Osuna, F. 2017. Acute toxicity of nitrite on white shrimp Litopenaeus vannamei (Boone) juveniles in low-salinity water. Aquaculture Research, 48(5): 2337-2343.

Ray, A.J.; Dillon, K.S.; Lotz, J.M. 2011. Water quality dynamics and shrimp (Litopenaeus vannamei) production in intensive, mesohaline culture systems with two levels of biofloc management. Aquacultural Engineering, 45(3): 127-136.

Ray, P.D.; Huang, B.W.; Tsuji, Y. 2012. Reactive oxygen species (ROS) homeostasis and redox regulation in cellular signaling. Cellular Signaling, 24(5): 981-990.

Romano, N.; Zeng, C. 2013. Toxic effects of ammonia, nitrite, and nitrate to decapod crustaceans: A review on factors influencing their toxicity, physiological consequences, and coping mechanisms. Reviews in Fisheries Science, 21(1): 1-21.

Schmitz, M.J.; Colombo, G.M.; Simião, C.; Ortiz, C.R.; Fonseca Costa, L.D.; Nascimento da Silva, T.V.; Monserrat, J.M. 2020. Modulation of nodularin toxicity in shrimp Litopenaeus vannamei (BOONE, 1931) fed with dietary açai (Euterpe oleracea) inclusion. Fish and Shellfish Immunology, 103: 464-471.

Searle, S.R.; Casella, G.; McCulloch, C.E. 2006. Variance components. John Wiley & Sons, New Jersey. 537p.

Sedlak, J.; Lindsay, R.H. 1968. Estimation of total, protein-bound, and nonprotein sulfhydryl groups in tissue with Ellman’s reagent. Analytical Biochemistry, 25: 192-205.

Shan, H.; Geng, Z.; Ma, S.; Wang, T. 2019. Comparative study of the key enzymes and biochemical substances involved in the energy metabolism of Pacific white shrimp, Litopenaeus vannamei, with different ammonia-N tolerances. Comparative Biochemistry and Physiology, Part C: Toxicology & Pharmacology, 221: 73-81.

Shi, J.; Lei, Y.; Shen, H.; Hong, H.; Yu, X.; Zhu, B.; Luo, Y. 2019. Effect of glazing and rosemary (Rosmarinus officinalis) extract on preservation of mud shrimp (Solenocera melantho) during frozen storage. Food Chemistry, 272: 604-612.

Simião, C.; Colombo, G.M.; Schmitz, M.J.; Ramos, P.B.; Tesser, M.B.; Wasielesky Jr., W.; Monserrat, J.M. 2020. Inclusion of Amazonian Mauritia flexuosa fruit pulp as functional feed in the diet for the juvenile Pacific white shrimp Litopenaeus vannamei. Aquaculture Research, 51(4): 1731-1742.

Souza, D.M.; Kutter, M.T.; Furtado, P.S.; Romano, L.A.; Wasielesky Jr., W.; Monserrat, J.M.; Garcia, L. 2019. Growth, antioxidant system, and immunological status of shrimp in bioflocs and clear water culture systems. Pesquisa Agropecuária Brasileira, 54: e00363.

Sowmya, R.; Sachindra, N.M. 2012. Evaluation of antioxidant activity of carotenoid extract from shrimp processing by products by in vitro assays and in membrane model system. Food Chemistry, 134(1): 308-314.

Srichaiyo, N.; Tongsiri, S.; Hoseinifar, S.H.; Dawood, M.A.O.; Jaturasitha, S.; Esteban, M.Á.; Van Doan, H. 2020. The effects gotu kola (Centella asiatica) powder on growth performance, skin mucus, and serum immunity of Nile tilapia (Oreochromis niloticus) fingerlings. Aquaculture Reports, 16: 100239.

Takeungwongtrakul, S.; Benjakul, S. 2016. Astaxanthin degradation and lipid oxidation of Pacific white shrimp oil: kinetics study and stability as affected by storage conditions. International Aquatic Research, 8: 15-27.

UNESCO. 1983. Chemical methods for use in marine environmental monitoring. Intergovernmental Oceanographic Commission. Manuals and Guides 12. Paris, France: UNESCO. 53p.
Van Bennekum, A.; Werder, M.; Thuahnai, S.T.; Han, C.H.; Duong, P.; Williams, D.L.; Hauser, H. 2005. Class B scavenger receptor-mediated intestinal absorption of dietary β-carotene and cholesterol. Biochemistry, 44(11): 4517-4525.

Wang, T.; Shan, H.W.; Geng, Z.X.; Yu, P.; Ma, S. 2020. Dietary supplementation with freeze-dried Ampithoe sp. enhances the ammonia-N tolerance of Litopenaeus vannamei by reducing oxidative stress and endoplasmic reticulum stress and regulating lipid metabolism. Aquaculture Reports, 16: 100264.

Wasielesky Jr., W.; Froes, C.; Fóes, G.; Krummenauer, D.; Lara, G.; Poersch, L. 2013. Nursery of Litopenaeus vannamei reared in a biofloc system: The effect of stocking densities and compensatory growth. Journal of Shellfish Research, 32(3): 799-806. .

Xiao, J.; Liu, Q.Y.; Du, J.H.; Zu, W-L.; Li, Q-Y.; Chen, X-L.; Chen, X-H.; Liu, H.; Zhou, X-Y.; Zhao, Y-Z.; Huang, H-L. 2020. Integrated analysis of physiological, transcriptomic and metabolomic responses and tolerance mechanism of nitrite exposure in Litopenaeus vannamei. Science of the Total Environment, 711: 134416.

Xie, J.J.; Chen, X.; Guo, T.Y.; Xie, S.W.; Fang, H.H.; Liu, Z.L.; Niu, J. 2018. Dietary values of Forsythia suspensa extract in Penaeus monodon under normal rearing and Vibrio parahaemolyticus 3HP (VP3HP) challenge conditions: Effect on growth, intestinal barrier function, immune response and immune related gene expression. Fish and Shellfish Immunology, 75: 316-326.

Yang, S.-P.; Wu, Z.-H.; Jian, J.-C.; Zhang, X.-Z. 2010. Effect of marine red yeast Rhodosporidium paludigenum on growth and antioxidant competence of Litopenaeus vannamei. Aquaculture, 309(1-4): 62-65.

Yi, X.; Xu, W.; Zhou, H.; Zhang, Y.; Luo, Y.; Zhang, W.; Mai, K. 2014. Effects of dietary astaxanthin and xanthophylls on the growth and skin pigmentation of large yellow croaker Larimichthys croceus. Aquaculture, 433: 377-383.

Yin, X.L.; Li, Z.J.; Yang, K.; Lin, H.Z.; Guo, Z.X. (2014). Effect of guava leaves on growth and the non-specific immune response of Penaeus monodon. Fish and Shellfish Immunology, 40(1): 190-196.

Zhang, J.; Liu, Y.J.; Tian, L.X.; Yang, H.J.; Liang, G.Y.; Yue, Y.R.; Xu, D.H. 2013. Effects of dietary astaxanthin on growth, antioxidant capacity and gene expression in Pacific white shrimp Litopenaeus vannamei. Aquaculture Nutrition, 19(6): 917-927.

Zhang, P.; Zhang, X.; Li, J.; Huang, G. 2006. The effects of body weight, temperature, salinity, pH, light intensity and feeding condition on lethal DO levels of whiteleg shrimp, Litopenaeus vannamei (Boone, 1931). Aquaculture, 256(1-4): 579-587.






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