Skip to main content
SpringerLink
Log in

Use of Corn Husk Meal in the Development of a Functional Diet for Nile tilapia (Oreochromis niloticus) Fingerlings: Effect on Growth Performance, Antioxidant Status and Intestinal Microbiota

  • Original Paper
  • Published:
Waste and Biomass Valorization Aims and scope Submit manuscript

Abstract

The effect of dietary supplementation of corn husk meal (CHM) on growth performance, liver antioxidant status and intestinal microbiota in Nile tilapia (Oreochromis niloticus) fingerlings was evaluated. Four experimental groups of fish with initial weight 0.47 ± 0.7 g in triplicate tanks were used; three of them were fed CHM incorporated diets (12.5 g/kg, DH12; 25 g/kg, DH25; and 50 g/kg, DH50), whereas a CHM-free basal diet served as control (DH0). No significant differences were observed in growth performance or feed efficiency in fish fed experimental diets (P > 0.05); however, fish fed the DH50 diet had a significant higher proportion of crude protein of whole-body composition (P < 0.05). Analysis of antioxidant enzyme activity showed significant differences (P < 0.05) with higher superoxide dismutase (SOD) activity in fish fed the DH25 diet, and lower glutathione peroxidase (GPx) activity in fish fed the DH12 diet. No significant differences were found in catalase (CAT) activity between treatments. Fusobacteria, Bacteroidetes and Proteobacteria were the most abundant phyla in all feces samples but no significant differences were found in microbial diversity among diets. Results suggest that CHM is safe for Nile tilapia consumption improving crude protein of whole-body composition and enhancing SOD activity.

Graphic Abstract

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  1. FAO. US Department of Agriculture. World grain production. http://www.fao.org/faostat/ (2019). Accessed 20 Feb 2020

  2. Li, H.Y., Xu, L., Liu, W.J., Fang, M.Q., Wang, N.: Assessment of the nutritive value of whole corn stover and its morphological fractions. Asian Austral. J. Anim. 27(2), 194 (2014). https://doi.org/10.5713/ajas.2013.13446

    Article  Google Scholar 

  3. Ruan, Z., Wang, X., Liu, Y., Liao, W.: Corn. In: Pan, Z., Zhang, R., Zicari, S. (eds.) Integrated Processing Technologies for Food and Agricultural By-Products, pp. 59–72. Academic Press, Cambridge (2019). https://doi.org/10.1016/b978-0-12-814138-0.00003-4

    Chapter  Google Scholar 

  4. Vazquez-Olivo, G., López-Martínez, L.X., Contreras-Angulo, L., Heredia, J.B.: Antioxidant capacity of lignin and phenolic compounds from corn stover. Waste Biomass Valori. 10, 95–102 (2019). https://doi.org/10.1007/s12649-017-0028-5

    Article  Google Scholar 

  5. Galeana-López, J.A., Hernández, C., Leyva-López, N., Lizárraga-Velázquez, C.E., Sánchez-Gutiérrez, E.Y., Heredia, J.B.: Corn husk extracts as an antioxidant additive in diets for Nile tilapia (Oreochromis niloticus) fingerlings: effect on growth performance, feed intake and toxicity. Biotecnia 22(2), 147–154 (2020). https://doi.org/10.18633/biotecnia.v22i2.1256

    Article  Google Scholar 

  6. Kurutas, E.B.: The importance of antioxidants which play the role in cellular response against oxidative/nitrosative stress: current state. Nutr. J. 15(1), 71 (2015). https://doi.org/10.1186/s12937-016-0186-5

    Article  Google Scholar 

  7. Fairweather-Tait, S.J., Southon, S.: Bioavailability of nutrients. In: Caballero, B. (ed.) Encyclopedia of Food Sciences and Nutrition, pp. 478–484. Oxford Academic Press, Oxford (2003). https://doi.org/10.1016/B0-12-227055-X/00096-1

    Chapter  Google Scholar 

  8. D’Archivio, M., Filesi, C., Di Benedetto, R., Gargiulo, R., Giovannini, C., Masella, R.: Polyphenols, dietary sources and bioavailability. Ann. Ist. Super Sanita 43(4), 348 (2007)

    Google Scholar 

  9. Manach, C., Scalbert, A., Morand, C., Remesy, C., Jimenez, L.: Polyphenols: food sources and bioavailability. Am. J. Clin. Nutr. 79, 727–747 (2004). https://doi.org/10.1093/ajcn/79.5.727

    Article  Google Scholar 

  10. Liu, Z., Hu, M.: Natural polyphenol disposition via coupled metabolic pathways. Expert Opin. Drug. Metab. Toxicol. 3(3), 389–406 (2007). https://doi.org/10.1517/17425255.3.3.389

    Article  Google Scholar 

  11. Burkitt, D.P., Walker, A.R.P., Painter, N.S.: Effect of dietary fibre on stools and transit-times, and its role in the causation of disease. Lancet 300(7792), 1408–1411 (1972). https://doi.org/10.1016/s0140-6736(72)92974-1

    Article  Google Scholar 

  12. Gibson, G.R., Roberfroid, M.B.: Dietary modulation of the human colonic microbiota: introducing the concept of prebiotics. J. Nutr. 125(6), 1401–1412 (1995). https://doi.org/10.1093/jn/125.6.1401

    Article  Google Scholar 

  13. Gibson, G.R.: Dietary modulation of the human gut microflora using prebiotics. British J. Nutr. 80(S2), S209–S212 (1998). https://doi.org/10.1017/S0007114500006048

    Article  Google Scholar 

  14. Manning, T.S., Gibson, G.R.: Microbial-gut interactions in health and disease. Prebiotics. Best Pract. Res. Clin. Gastroenterol. 18(2), 287–298 (2004). https://doi.org/10.1016/j.bpg.2003.10.008

    Article  Google Scholar 

  15. El-Mesallamy, A., Ahmad, M., Souleman, A., El Morsy, A., Abd El-Naby, A.: Effects of Roselle calyx (Hibiscussabdariffa L.)-supplemented diets on growth and disease (Aeromonashydrophila) resistance in Nile tilapia (Oreochromisniloticus L.). Egypt. Pharmaceut. J. 15, 78–87 (2016). https://doi.org/10.4103/1687-4315.190403

    Article  Google Scholar 

  16. Armenta-López, G.E., Sumaya-Martínez, M.T., Spanopoulos-Hernández, M., Balois-Morales, R., Sánchez-Herrera, L.M., Jiménez-Ruíz, E.I.: Inclusion of natural antioxidant compounds in fish feeds to counteract oxidative stress. Rev. Bio Cienc. (2015). https://doi.org/10.15741/revbio.03.02.01

    Article  Google Scholar 

  17. Abd El-Naby, A.S., Samir, F., Abdel Razek, N., Khattaby, A.A.: Effect of Aquaviance product as dietary supplementation to improve growth performance, feed intake, innate immunity and antioxidant activity for Nile tilapia, (Oreochromis niloticus). Abbassa Int. J. Aqua. 10(1), 114–138 (2017)

    Google Scholar 

  18. Welker, T.L., Lim, C.: Use of probiotics in diets of tilapia. J. Aquac. Res. Dev. S1, 014 (2011). https://doi.org/10.4172/2155-9546.S1-014

    Article  Google Scholar 

  19. Sinha, A.K., Kumar, V., Makkar, H.P., De Boeck, G., Becker, K.: Non-starch polysaccharides and their role in fish nutrition–a review. Food Chem. 127(4), 1409–1426 (2011). https://doi.org/10.1016/j.foodchem.2011.02.042

    Article  Google Scholar 

  20. FAO. Total Fishery Production. Fishery Statistics. Fishstat Plus. Electronic edition. http://www.fao.org/fishery/species/3217/en (2016). Accessed 20 February 2020.

  21. Montoya-Camacho, N., Marquez-Ríos, E., Castillo-Yáñez, F.J., Cárdenas López, J.L., López-Elías, J.A., Ruíz-Cruz, S., Jiménez-Ruíz, E.I., Rivas-Vega, M.E., Ocaño-Higuera, V.M.: Advances in the use of alternative protein sources for tilapia feeding. Rev. Aquacult. 11, 515–526 (2019). https://doi.org/10.1111/raq.12243

    Article  Google Scholar 

  22. Anderson, J., Jackson, A.J., Matty, A.J., Capper, B.S.: Effects of dietary carbohydrate and fiber on the tilapia (Oreochromis niloticus). Aquacult. 37, 303–414 (1984). https://doi.org/10.1016/0044-8486(84)90296-5

    Article  Google Scholar 

  23. Singleton, V.L., Orthofer, R., Lamuela-Raventós, R.M.: Analysis of total phenols and other oxidation substrates and antioxidants by means of folin-ciocalteu reagent. Method. Enzymol. 299, 152–178 (1999). https://doi.org/10.1016/S0076-6879(99)99017-1

    Article  Google Scholar 

  24. Brand-Williams, W., Cuvelier, M.E., Berset, C.: Use of a free radical method to evaluate antioxidant activity. LWT-Food Sci. Technol. 28, 25–30 (1995). https://doi.org/10.1016/S0023-6438(95)80008-5

    Article  Google Scholar 

  25. AOAC. Official methods of analysis of AOAC International. In W. Horwitz (18th Ed.), Gaithersburg: International AOAC. (2011).

  26. Ebeling, M.E.: The Dumas method for nitrogen in feeds. J. Assoc. Off. Anal. Chem 51, 766–770 (1968). https://doi.org/10.1093/jaoac/51.4.766

    Article  Google Scholar 

  27. Bradford, M.M.: A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72(1–2), 248–254 (1976). https://doi.org/10.1016/0003-2697(76)90527-3

    Article  Google Scholar 

  28. Azmat, M.A., Khan, I.A., Cheema, H.M.N., Rajwana, I.A., Khan, A.S., Khan, A.A.: Extraction of DNA suitable for PCR applications from mature leaves of Mangifera indica L. J. Zhejiang Univ. Sci. B. 13(4), 239–243 (2012). https://doi.org/10.1631/jzus.B1100194

    Article  Google Scholar 

  29. Huse, S.M., Dethlefsen, L., Huber, J.A., Welch, D.M., Relman, D.A., Sogin, M.L.: Exploring microbial diversity and taxonomy using SSU rRNA hypervariable tag sequencing. PLoS Genet. 4(11), e1000255 (2008). https://doi.org/10.1371/journal.pgen.1000255

    Article  Google Scholar 

  30. Navarro-Barrón, E., Hernández, C., Llera-Herrera, R., García-Gasca, A., Gómez-Gil, B.: Overfeeding a high-fat diet promotes sex-specific alterations on the gut microbiota of the Zebrafish (Danio rerio). Zebrafish. 16(3), 268–279 (2019). https://doi.org/10.1089/zeb.2018.1648

    Article  Google Scholar 

  31. Martin, M.: Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnet. J. 17(1), 10–12 (2011). https://doi.org/10.14806/ej.17.1.200

    Article  Google Scholar 

  32. Rognes, T., Flouri, T., Nichols, B., Quince, C., Mahé, F.: VSEARCH: a versatile open source tool for metagenomics. PeerJ. 4, e2584 (2016). https://doi.org/10.7717/peerj.2584

    Article  Google Scholar 

  33. Yoon, S.H., Ha, S.M., Kwon, S., Lim, J., Kim, Y., Seo, H., Chun, J.: Introducing EzBioCloud: a taxonomically united database of 16S rRNA gene sequences and whole-genome assemblies. Int. J. Sys. Evol. Micr. 67(5), 1613 (2017). https://doi.org/10.1099/ijsem.0.001755

    Article  Google Scholar 

  34. Yarza, P., Yilmaz, P., Pruesse, E., Glöckner, F.O., Ludwig, W., Schleifer, K.H., Rosselló-Móra, R.: Uniting the classification of cultured and uncultured bacteria and archaea using 16S rRNA gene sequences. Nat. Rev. Microbiol. 12(9), 635–645 (2014). https://doi.org/10.1038/nrmicro3330

    Article  Google Scholar 

  35. Zar, J.H.: Biostatistical analysis. Prentice-Hall, Englewood Cliffs (1984)

    Google Scholar 

  36. Naveed, M., Hejazi, V., Abbas, M., Kamboh, A.A., Khan, G.J., Shumzaid, M., WenHua, L.: Chlorogenic acid (CGA): a pharmacological review and call for further research. Biomed. Pharmacother. 97, 67–74 (2018). https://doi.org/10.1016/j.biopha.2017.10.064

    Article  Google Scholar 

  37. Yu, L.-J., Wu, F., Jiang, M., Yang, C.-G., Liu, W., Tian, J., Lu, X., Wen, H.: Ferulic acid: a natural compound as an efficient feed additive for GIFT (Oreochromis niloticus). Aquac. Nutr. 24, 27–35 (2017). https://doi.org/10.1111/anu.12529

    Article  Google Scholar 

  38. Ringø, R., Olsen, R.E., Gifstad, T.Ø., Dalmo, R.A., Amlund, H., Hemre, G.-I., Bakke, A.M.: Prebiotics in aquaculture: a review. Aquac. Nutr. 16(2), 117–136 (2010). https://doi.org/10.1111/j.1365-2095.2009.00731.x

    Article  Google Scholar 

  39. Van Doan, H., Hoseinifar, S.H., Tapingkae, W., Seel-audom, M., Jaturasitha, S., Dawood, M.A.O., Esteban, M.Á.: Boosted growth performance, mucosal and serum immunity, and disease resistance Nile tilapia (Oreochromis niloticus) fingerlings using corncob-derived xylooligosaccharide and Lactobacillus plantarum CR1T5. Probiotics Antimicrob. Proteins. (2019). https://doi.org/10.1007/s12602-019-09554-5[28]

    Article  Google Scholar 

  40. Ighodaro, O.M., Akinloye, O.A.: First line defense antioxidants-superoxide dismutase (SOD), catalase (CAT) and glutathione peroxidase (GPX): their fundamental role in the entire antioxidant defense grid. Alexandria J. Med. 54(4), 287–293 (2018). https://doi.org/10.1016/j.ajme.2017.09.001

    Article  Google Scholar 

  41. Miao, L., Clair, D.K.S.: Regulation of superoxide dismutase genes: implications in disease. Free Radical Bio. Med. 47(4), 344–356 (2009). https://doi.org/10.1016/j.freeradbiomed.2009.05.018

    Article  Google Scholar 

  42. Lopes, J.M., de Freitas Souza, C., Saccol, E.M.H., Pavanato, M.A., Antoniazzi, A., Rovani, M.T., Baldisserotto, B.: Citrus x aurantium essential oil as feed additive improved growth performance, survival, metabolic, and oxidative parameters of silver catfish (Rhamdia quelen). Aquac. Nutr. 25(2), 310–318 (2019). https://doi.org/10.1111/anu.12854

    Article  Google Scholar 

  43. Lizárraga-Velázquez, C.E., Hernández, C., González-Aguilar, G.A., Heredia, J.B.: Effect of dietary intake of phenolic compounds from mango peel extract on growth, lipid peroxidation and antioxidant enzyme activities in zebrafish (Danio rerio). Lat. Am. J. Aquat. Res. 47, 602–611 (2019). https://doi.org/10.3856/vol47-issue4-fulltext-3

    Article  Google Scholar 

  44. Vicente, I.S., Fleuri, L.F., Carvalho, P.L., Guimarães, M.G., Naliato, R.F., Müller, H.D.C., Barros, M.M.: Orange peel fragment improves antioxidant capacity and haematological profile of Nile tilapia subjected to heat/dissolved oxygen-induced stress. Aquac. Res. 50(1), 80–92 (2019). https://doi.org/10.1111/are.13870

    Article  Google Scholar 

  45. Ray, C., Bujan, N., Tarnecki, A., Davis, A.D., Browdy, C., Arias, C.R.: Analysis of the gut microbiome of Nile tilapia Oreochromisniloticus L. fed diets supplemented with Previda® and saponin. J Fish Sci 11(2), 36 (2017). https://doi.org/10.21767/1307-234X.1000116

    Article  Google Scholar 

  46. Yuji-Sado, R., Raulino-Domanski, F., de Freitas, P.F., Baioco-Sales, F.: Growth, immune status and intestinal morphology of Nile tilapia fed dietary prebiotics (mannan oligosaccharides-MOS). Lat. Am. J. Aquat. Res. 43(5), 944–952 (2015). https://doi.org/10.3856/vol43-issue5-fulltext-14

    Article  Google Scholar 

  47. de Souza, F.P., de Lima, C.S., Urrea-Rojas, A.M., Suphoronski, S.A., Facimoto, C.T., Júnior, J.D.S.B., Lopera-Barrero, N.M.: Effects of dietary supplementation with a microalga (Schizochytrium sp.) on the hemato-immunological, and intestinal histological parameters and gut microbiota of Nile tilapia in net cages. PLoS ONE 15(1), 1–19 (2020). https://doi.org/10.1371/journal.pone.0226977

    Article  Google Scholar 

  48. Janda, J.M., Abbott, S.L., McIver, C.J.: Plesiomonas shigelloides revisited. Clin. Microbiol. Rev. 29(2), 349–374 (2016). https://doi.org/10.1128/CMR.00103-15

    Article  Google Scholar 

  49. Sierralta, C., Mayta, H., León, Q.: First report of Plesiomonas shigelloides as opportunistic pathogen in tilapia Oreochromis niloticus (Linnaeus, 1758) in a fish farm in Lima, Peru. Rev. de Investig Vet. del Perú (RIVEP). 27(3), 565–572 (2016). https://doi.org/10.15381/rivep.v27i3.11996

    Article  Google Scholar 

  50. Liu, Z., Ke, X., Lu, M., Gao, F., Cao, J., Zhu, H., Wang, M.: Identification and pathological observation of a pathogenic Plesiomonas shigelloides strain isolated from cultured tilapia (Oreochromis niloticus). Acta Microbiol. Sin. 55(1), 96–106 (2015)

    Google Scholar 

  51. Yilmaz, S.: Effects of dietary blackberry syrup supplement on growth performance, antioxidant, and immunological responses, and resistance of Nile tilapia, Oreochromis niloticus to Plesiomonas shigelloides. Fish Shellfish Immun. 84, 1125–1133 (2019). https://doi.org/10.1016/j.fsi.2018.11.012

    Article  Google Scholar 

Download references

Acknowledgements

Funding was provided by Consejo Nacional de Ciencia y Tecnología (CONACyT) Grant 292474. The authors wish to acknowledge the CONACyT for the graduate scholarship 552436 Granted to José Andres Galeana Lopez. This manuscript is part of the activities of the Thematic Network 12.3: to reduce and valorize the losses and the waste of food systems Project 294768 and it is part of Cátedras-CONACYT Project #729: Applied biotechnologies for the development of functional foods for aquaculture. The authors are grateful to Karen Enciso-Ibarra, Erika Yazmin Sánchez-Gutiérrez, María del Carmen Bolan-Mejia, Nancy Vera-Rivera, Cecilia Cervantes-Briseño and Susanna Janette Gurrola for technical support.

Author information

Authors and Affiliations

  1. Centro de Investigación en Alimentación y Desarrollo A.C., Unidad Mazatlán, Av. Sábalo Cerritos S/N, Mazatlán, Sinaloa, C.P. 82112, México

    José Andrés Galeana-López, Bruno Gómez-Gil, Crisantema Hernández, Nayely Leyva-López & Cynthia E. Lizárraga-Velázquez

  2. Cátedras CONACYT- Centro de Investigación en Alimentación y Desarrollo A.C. Unidad Mazatlán, Av. Sábalo Cerritos S/N, Mazatlán, Sinaloa, C.P. 82112, México

    Nayely Leyva-López

  3. Centro de Investigaciones Biológicas del Noroeste, S.C. Planeación Ambiental y Conservación. Av, Instituto Politécnico Nacional 195, Playa Palo de Santa Rita Sur, La Paz, Baja California Sur., C.P. 23096, México

    Tania Zenteno-Savín

Authors
  1. José Andrés Galeana-López
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Bruno Gómez-Gil
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Crisantema Hernández
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Nayely Leyva-López
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Cynthia E. Lizárraga-Velázquez
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Tania Zenteno-Savín
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Crisantema Hernández.

Ethics declarations

Conflict of interest

The authors declare no conflict of interest.

Research involving human and animal rights

The authors followed all applicable international, national and/or institutional guidelines for the care and use of animals.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (PDF 218 KB)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Galeana-López, J.A., Gómez-Gil, B., Hernández, C. et al. Use of Corn Husk Meal in the Development of a Functional Diet for Nile tilapia (Oreochromis niloticus) Fingerlings: Effect on Growth Performance, Antioxidant Status and Intestinal Microbiota. Waste Biomass Valor 12, 4355–4365 (2021). https://doi.org/10.1007/s12649-020-01314-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12649-020-01314-9

Keywords

Search

Navigation