Functional assessment of citral dietary supplementation on growth performance, intestinal parameters, and specific activity of the digestive enzymes of Sardinella brasiliensis reared in recirculating aquaculture system
DOI:
https://doi.org/10.20950/1678-2305/bip.2024.50.e857Keywords:
Brazilian sardine, Feed supplementation, Marine fish farming, SustainabilityAbstract
This study evaluated the effects of dietary supplementation with citral on growth performance and intestinal parameters, and specific activity of the digestive enzymes of Sardinella brasiliensis. 240 juvenile S. brasiliensis were randomly distributed in a recirculating aquaculture system (RAS) composed of 12 circular tanks of 150 L (n = 20 per tank). A diet without citral addition (control) and three diets containing different levels of citral inclusion (0.5, 1.0 and 2.0 mL kg*feed–1) were used in the fish feeding management during 20 days. The indexes of zootechnical performance, survival, weight gain, specific growth rate, feed conversion and condition factor of the fish were verified, as well as digestive enzymes and histological analysis. A significant positive relationship was found between citral supplementation and fish survival. In the specific activity of digestive enzymes, dietary citral supplementation at 2.0 mL* kg feed–1 increased lipase and amylase activity. Citral supplementation positively influenced the number of villi and intestinal crypt depth. Furthermore, the inclusion of citral at 0.5 mL kg*feed–1 increased the intestine diameter of the fish. The results of the experiment suggest that the addition of citral as an additive in the diet of S. brasiliensis improved the survival of fish.
References
Almeida, A. P. G., Zardo, E. L., Toni, C., Behr, E. R., Picolli da Silva, L., Vieira, J. P., & Baldisserotto, B. (2018). Composition of gastrointestinal content, protease and lipase activities in summer and winter of four freshwater Siluriforms (Teleostei: Actinopterygii) with two different feeding habits. Zoologia, 35, 1-8. https://doi.org/10.3897/zoologia.35.e13286
Angelo, M., Lisboa, M. K., Magnotti, C., Pilotto, M. R., Mattos, J. J., & Cerqueira, V. R. (2021). Temperature influence on the initial development of Sardinella brasiliensis larvae. Aquaculture Research, 52(12), 6497 6503. https://doi.org/10.1111/are.15517
Bakkali, F., Averbeck, S., Averbeck, D., & Idaomar, M. (2008). Biological effects of essential oils — a review. Food and Chemical Toxicology, 46(2), 446-475. https://doi.org/10.1016/j.fct.2007.09.106
Baloi, M. F., de Carvalho, C. V., Sterzelecki, F. C., Passini, G., & Cerqueira, V. R. (2016). Effects of feeding frequency on growth, feed efficiency and body composition of juveniles Brazilian sardine, Sardinella brasiliensis (Steindacher 1879). Aquaculture Research, 47(2), 554-560. https://doi.org/10.1111/are.12514
Baloi, M. F., Magnotti, C. F., Carneiro Sterzelecki, F., Vieira Rodrigues, R., & Ronzani Cerqueira, V. (2017a). Acute toxicity of ammonia in juvenile Brazilian sardine Sardinella brasiliensis. Boletim do Instituto de Pesca, 43(1), 135-139. https://doi.org/10.20950/1678-2305.2017v43n1p135
Baloi, M. F., Sterzelecki, F. C., Sugai, J. K., Passini, G., Carvalho, C. V. A., & Cerqueira, V. R. (2017b). Growth performance, body composition and metabolic response to feeding rates in juvenile Brazilian sardine Sardinella brasiliensis. Aquaculture Nutrition, 23(6), 1458-1466. https://doi.org/10.1111/anu.12521
Benfold, D. (1955). Amylase β and α. In S. P. Colowick & N. O. Kaplan (Eds.), Method in Enzymology (pp. 149-154). Academic Press.
Berk, Z. (2016). History, production, trade, and utilization. In Z. Berk (Ed.), Citrus Fruit Processing (pp. 1-8). Academic Press. https://doi.org/10.1016/B978-0-12-803133-9.00001-1
Brum, A., Pereira, S. A., Owatari, M. S., Chagas, E. C., Chaves, F. C. M., Mouriño, J. L. P., & Martins, M. L. (2017). Effect of dietary essential oils of clove basil and ginger on Nile tilapia (Oreochromis niloticus) following challenge with Streptococcus agalactiae. Aquaculture, 468(1), 235–243. https://doi.org/10.1016/j.aquaculture.2016.10.020
Cerqueira, V. R., Sterzelecki, F. C., Baloi, M. F., Magnotti, C., Cipriano, F. S., & Manzoni, G. C. (2020). Cultivo da sardinha verdadeira. In B. Baldisserotto (Ed.), Espécies nativas para piscicultura no Brasil (pp. 57-72). Santa Maria: Editora da UFSM.
Chat, O. A., Bhat, P. A., Nazir, N., & Dar, A. A. (2019). Selfassembled systems based on surfactants and polymers as stabilizers for citral in beverages. In Value-Added Ingredients and Enrichments of Beverages (pp. 487-521). Academic Press. https://doi.org/10.1016/B978-0-12-816687-1.00015-1
Cottrell, R. S., Metian, M., Froehlich, H. E., Blanchard, J. L., Sand Jacobsen, N., McIntyre, P. B., Nash, K. L., Williams, D. R., Bouwman, L., Gephart, J. A., Kuempel, C. D., Moran, D. D., Troell, M., & Halpern, B. S. (2021). Time to rethink trophic levels in aquaculture policy. Reviews in Aquaculture, 13(3), 1583-1593. https://doi.org/10.1111/raq.12535
Gawlicka, A., Parent, B., Horn, M. H., Ross, N., Opstad, I., & Torrissen, O. J. (2000). Activity of digestive enzymes in yolksac larvae of Atlantic halibut (Hippoglossus hippoglossus): indication of readiness for first feeding. Aquaculture, 184(3-4), 303-314. https://doi.org/10.1016/S0044-8486(99)00322-1
Hidalgo, M. C., Urea, E., & Sanz, A. (1999). Comparative study of digestive enzymes in fish with different nutritional habits. Proteolytic and amylase activities. Aquaculture, 170(3-4), 267-283. https://doi.org/10.1016/S0044-8486(98)00413-X
Jensen, L. B., Provan, F., Larssen, E., Bron, J. E., & Obach, A. (2015). Reducing sea lice (Lepeophtheirus salmonis) infestation of farmed Atlantic salmon (Salmo salar L.) through functional feeds. Aquaculture Nutrition, 21(6), 983-993. https://doi.org/10.1111/anu.12222
Jesus, G. F. A., Owatari, M. S., Pereira, S. A., Silva, B. C., Syracuse, N. M., Lopes, G. R., Addam, K., Cardoso, L., Mouriño, J. L. P., & Martins, M. L. (2021). Effects of sodium butyrate and Lippia origanoides essential oil blend on growth, intestinal microbiota, histology, and haemato-immunological response of Nile tilapia. Fish & Shellfish Immunology, 117, 62-69. https://doi.org/10.1016/j.fsi.2021.07.008
Le Roux, A. B., Granger, L. A., Wakamatsu, N., Kearney, M. T., & Gaschen, L. (2016). Ex vivo correlation of ultrasonographic small intestinal wall layering with histology in dogs. Veterinary Radiology & Ultrasound, 57(5), 534-545. https://doi.org/10.1111/vru.12392
Lieke, T., Meinelt, T., Hoseinifar, S. H., Pan, B., Straus, D. L., & Steinberg, C. E. (2020). Sustainable aquaculture requires environmental‐friendly treatment strategies for fish diseases. Reviews in Aquaculture, 12(2), 943-965. https://doi.org/10.1111/raq.12365
Maarse, H. (1991). Volatile compounds in foods and beverages. Routledge. https://doi.org/10.1201/9780203734285
Magnotti, C., Sterzelecki, F., Cipriano, F., Pedrotti, F., Rocha, V., Freitas, G. L., & Cerqueira, V. (2020). Spontaneous spawning of Brazilian sardine in captivity. Boletim do Instituto de Pesca, 46(1), e539. https://doi.org/10.20950/1678-2305.2020.46.1.539
Michelotti, B. T., Mori, N. C., Magnotti, C. C. F., Heinzmann, B. M., Almeida, A. P. G., Cerqueira, V. R., & Baldisserotto, B. (2020). Citral as food additive for common snook zootechnical parameters and digestive enzymes. Ciência Rural, 50(4), e20190577. https://doi.org/10.1590/0103-8478cr20190577
Michelotti, B. T., Passini, G., Carvalho, C., Salbego, J., Cossettin, N., Rodrigues, R. V., Baldisserotto, B., & Cerqueira, V. R. (2018). Growth and metabolic parameters of common snook juveniles raised in freshwater with different water hardness. Aquaculture, 482, 31-35. https://doi.org/10.1016/j.aquaculture.2017.08.029
Mitsch, P., Zitterl-Eglseer, K., Köhler, B., Gabler, C., Losa, R., & Zimpernik, I. (2004). The effect of two different blends of essential oil components on the proliferation of Clostridium perfringens in the intestines of broiler chickens. Poultry Science, 83(4), 669-675. https://doi.org/10.1093/ps/83.4.669
Mori, N. C., Michelotti, B. T., da Silva Pês, T., Bressan, C. A., Sutili, F., Kreutz, L. C., Garlet, Q., Baldisserotto, B., Pavanato, M. A., Cerqueira, V. R., Costa, S. T., & Cerqueira, V. R. (2019). Citral as a dietary additive for Centropomus undecimalis juveniles: Redox, immune innate profiles, liver enzymes and histopathology. Aquaculture, 501, 14-21. https://doi.org/10.1016/j.aquaculture.2018.11.003
Owatari, M. S., Magnotti, C., Vargas, J. H., de Carvalho, C. V. A., Sterzelecki, F. C., & Cerqueira, V. R. (2023). Influence of salinity on growth and survival of juvenile Sardinella brasiliensis. Boletim do Instituto de Pesca, 49. https://doi.org/10.20950/1678-2305/bip.2023.49.e808
Owatari, M. S., Sterzelecki, F. C., da Silva, C. S., Magnotti, C., Mouriño, J. L. P., & Cerqueira, V. R. (2020). Amyloodiniosis in farmed Sardinella brasiliensis (Steindachner, 1879): Case report of successful therapeutic control with copper sulfate. Parasitology International, 76, 102091. https://doi.org/10.1016/j.parint.2020.102091
Park, J. T., & Johnson, M. J. (1949). A submicrodetermination of glucose. Journal of Biological Chemistry, 181(1), 149-151.
Perin, S., & Vaz-dos-Santos, A. M. (2014). Morphometry and relative growth of the Brazilian sardine, Sardinella brasiliensis (Steindachner, 1879) in the southeastern Brazilian bight. Arquivos de Zoologia, 45, 63-72. https://doi.org/10.11606/issn.2176-7793.v45iespp63-72
Rampelotto, C., de Lima, J., Pinheiro, C. G., Salbego, J., da Silva, L. P., & Emanuelli, T. (2018). Supplementation with microencapsulated lemongrass essential oil improves protein deposition and carcass yield in silver catfish (Rhamdia quelen). Acta Scientiarum– Animal Sciences, 40, 1-8. https://www.scielo.br/j/asas/a/FKY5qGyks9p6RGBWyrFXSrM/?format=pdf&lang=en. Accessed on 7 Dec. 2024
Saddiq, A. A., & Khayyat, S. A. (2010). Chemical and antimicrobial studies of monoterpene: Citral. Pesticide Biochemistry and Physiology, 98(1), 89-93. https://doi.org/10.1016/j.pestbp.2010.05.004
Santos, A. C., Bianchini, A. E., Bandeira Junior, G., Garlet, Q. I., Brasil, M. T. B., Heinzmann, B. M., Baldisserotto, B., Caron, B. O., Cunha, M. A. (2022). Essential oil of Aloysia citriodora Paláu and citral: sedative and anesthetic efficacy and safety in Rhamdia quelen and Ctenopharyngodonidella. Veterinary Anaesthesia and Analgesia, 49(1), 104-112. https://doi.org/10.1016/j.vaa.2021.10.004
Schroeder, R., Correia, A. T., Medeiros, S. D., Pessatti, M. L., & Schwingel, R. (2022). Spatiotemporal variability of the catch composition and discards estimates of the different methods of onboard preservation for the Brazilian sardine fishery in the southwest Atlantic Ocean. Thalassas: An International Journal of Marine Sciences, 38, 573-597. https://doi.org/10.1007/s41208-022-00398-5
Secretaria de Aquicultura e Pesca (SAP) (2021). Balanço 2020. Ministério da Agricultura, Pecuária e Abastecimento.
Silva, E. C., Sterzelecki, F. C., Alves Musialak, L., Sugai, J. K., Castro, J. D. J. P., Pedrotti, F. S., Magnotti, C., Cipriano, F. S., & Cerqueira, V. R. (2020). Effect of feeding frequency on growth performance, blood metabolites, proximate composition and digestive enzymes of Lebranche mullet (Mugil liza) juveniles. Aquaculture Research, 51(3), 1162- 1169. https://doi.org/10.1111/are.14466
Souza, C. D., Baldissera, M. D., Baldisserotto, B., Heinzmann, B. M., Martos-Sitcha, J. A., Mancera, J. M. (2019). Essential oils as stress-reducing agents for fish aquaculture: a review. Frontiers in Physiology, 10, 785. https://doi.org/10.3389/fphys.2019.00785
Souza, E. M., Souza, R. C., Melo, J. F. B., Costa, M. M., Souza, S. A., Souza, A. M., Copatti, C. E. (2020a). Cymbopogon flexuosus essential oil as an additive improves growth, biochemical and physiological responses and survival against Aeromonas hydrophila infection in Nile tilapia. Anais da Academia Brasileira de Ciências, 92(Suppl. 1), e20190140. https://doi.org/10.1590/0001-3765202020190140
Souza, R. C., Baldisserotto, B., Melo, J. F. B., Costa, M. M., Souza, E. M., Copatti, C. E. (2020b). Dietary Aloysia triphylla essential oil on growth performance and biochemical and haematological variables in Nile tilapia. Aquaculture, 519, 734913. https://doi.org/10.1016/j.aquaculture.2019.734913
Sterzelecki, F. C., dos Santos Cipriano, F., Vasconcelos, V. R., Sugai, J. K., Mattos, J. J., Derner, R. B., Magnotti, C. F., Lopes, R. G., & Cerqueira, V. R. (2021a). Minimum rotifer density for best growth, survival and nutritional status of Brazilian sardine larvae, Sardinella brasiliensis. Aquaculture, 534, 736264. https://doi.org/10.1016/j.aquaculture.2020.736264
Sterzelecki, F. C., Sugai, J. K., Baloi, M., Passini, G., de Carvalho, C. V. A., Fracalossi, D. M., & Cerqueira, V. R. (2017). Effect of dietary carbohydrate to lipid ratios on growth, digestive enzyme and blood metabolites of juvenile Brazilian sardines, Sardinella brasiliensis (Steindachner, 1879). Aquaculture Research, 48(9), 5111-5121. https://doi.org/10.1111/are.13330
Sterzelecki, F. C., Sugai, J. K., Baloi, M., Passini, G., de Carvalho, C. V. A., Fracalossi, D. M., & Cerqueira, V. R. (2018). Effects of increasing protein level on the performance, enzyme activity and body composition of the Brazilian sardine, Sardinella brasiliensis (Steindachner, 1879). Aquaculture Nutrition, 24(1), 366-374. https://doi.org/10.1111/anu.12567
Sterzelecki, F. C., Sugai, J. K., Mattos, J. J., Derner, R. B., Pedrotti, F. S., Magnotti, C. F., Lopes, R. G., & Cerqueira, V. R. (2021b). Live diet for first feeding of Brazilian sardine, Sardinella brasiliensis (Steindachner, 1879), larvae in captivity. Aquaculture Research, 52(11), 5558-5565. https://doi.org/10.1111/are.15431
Sugita, H., Kawasaki, J., & Deguchi, Y. (1997). Production of amylase by the intestinal microflora in cultured freshwater fish. Letters in Applied Microbiology, 24(2), 105-108. https://doi.org/10.1046/j.1472-765X.1997.00360.x
Sutili, F. J., Kreutz, L. C., Flores, F. C., da Silva, C. D. B., Kirsten, K. S., Voloski, A. P. D. S., & Baldisserotto, B. (2019). Effect of dietary supplementation with citral-loaded nanostructured systems on innate immune responses and gut microbiota of silver catfish (Rhamdia quelen). Journal of Functional Foods, 60, 103454. https://doi.org/10.1016/j.jff.2019.103454
Zago, D. C., Santos, A. C., Lanes, C. F. C., Almeida, D. V, Koakoski, G., de Abreu, M. S., & Baldisserotto, B (2018). Aloysia triphylla in the zebrafish food: effectson physiology, behavior, and growth performance. Fish Physiology and Biochemistry, 44(2), 465-474. https://doi.org/10.1007/s10695-017-0446-0
Zeppenfeld, C. C., Hernández, D. R., Santinón, J. J., Heinzmann, B. M., Cunha, M. A., Schmidt, D., & Baldisserotto, B. (2016). Essential oil of Aloysia triphylla as feed additive promotes growth of silver catfish (Rhamdia quelen). Aquaculture Nutrition, 22(4), 933-940. https://doi.org/10.1111/anu.12311
Zeppenfeld, C. C., Saccol, E. M. H., Pês, T. S., Salbego, J., Koakoski, G., dos Santos, A. C., & Baldisserotto, B. (2017). Aloysia triphylla essential oil as food additive for Rhamdia quelen– Stress and antioxidant parameters. Aquaculture Nutrition, 23(6), 1362-1367. https://doi.org/10.1111/anu.12511
Zheng, S., Jing, G., Wang, X., Ouyang, Q., Jia, L., & Tao, N. (2015). Citral exerts its antifungal activity against Penicillium digitatum by affecting the mitochondrial morphology and function. Food Chemistry, 178, 76-81. https://doi.org/10.1016/j.foodchem.2015.01.077
Downloads
Published
Issue
Section
License
Copyright (c) 2024 Bruna Tomazetti Michelotti, Marco Shizuo Owatari, Caio Magnotti, Ana Carolina Kohlrausch Klinger, Ulyssses da Silva Palma, Marina Cesconeto dos Santos, Sharine Nunes Descovi, Vinícius Ronzani Cerqueira , Sílvio Teixeira da Costa, Letícia Bogoni Bianchin, Bernardo Baldisserotto
This work is licensed under a Creative Commons Attribution 4.0 International License.
