Skip to main content
SpringerLink
Log in

Evaluation of dietary fermented tuna by-product meal as partial replacement for unprocessed tuna by-product meal in fishmeal-based diets for juvenile olive flounder Paralichthys olivaceus

  • Published:
Fish Physiology and Biochemistry Aims and scope Submit manuscript

Abstract

This study examined the effects of feeding fermented tuna by-product (FTBP) on the growth, non-specific immune response, liver and intestinal morphology, and disease resistance of olive flounder Paralichthys olivaceus. Olive flounders (n = 20; 2 g) were randomly assigned into four dietary groups in triplicates. Fish were fed four test diets (50% crude protein; 10% crude lipid) for 10 weeks in which unprocessed tuna by-product (TBP) meal was replaced (on a protein basis) with 0% (FTBP0 as the control diet), 15% (FTBP15), 30% (FTBP30), and 60% (FTBP60) of FTBP protein. Results showed that growth performance, blood parameters, and proximate composition were not influenced by FTBP inclusion. Non-specific immune parameters such as superoxide dismutase activity in the FTBP30 and FTBP60 groups were significantly higher than in the FTBP15 and the control groups, whereas lysozyme and myeloperoxidase activities were not different. Liver histopathology revealed normal architecture in groups fed FTBP0 and FTBP15 diets although mild alterations were noted in the FTBP30- and FTBP60-fed groups. Intestinal villi height and muscular thickness were not significantly altered with FTBP inclusion. Moreover, higher cumulative survival rate was observed in the FTBP60-fed group than fish fed with the other diets following the 13-day challenge with E. tarda. Together, these results demonstrate that fermented tuna by-product meal could be included at 60% in olive flounder diets.

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
Fig. 3

Similar content being viewed by others

Data availability

Data are available from the corresponding author upon reasonable request and with permission of the funding agency.

Code availability

Not applicable.

References

  • Adams SM, Brown AM, Goede RW (1993) A quantitative health assessment index for rapid evaluation of fish condition in the field. Trans Am Fish Soc 122:63–73. https://doi.org/10.1577/1548-8659(1993)122%3c0063:AQHAIF%3e2.3.CO;2

    Article  Google Scholar 

  • AOAC (Association of Official Analytical Chemists) (2005) Official methods of analysis, 18th edn. Gaithersburg, MD, Association of Official Analytical Chemists

    Google Scholar 

  • Ashida T, Okimasu E (2005) Immunostimulatory effects of fermented vegetable product on the non-specific immunity of Japanese flounder Paralicthys olivaceus. Fish Sci 71:257–262. https://doi.org/10.1111/j.1444-2906.2005.00958.x

  • Batista S, Ramos MA, Cunha S, Barros R, Cristóvão B, Rema P, Pires MA, Valente LMP, Ozório ROA (2015) Immune responses and gut morphology of Senegalese sole (Solea senegalensis, kaup 1858) fed monospecies and multispecies probiotics. Aquac Nutr 21:625–634. org/https://doi.org/10.1111/anu.12191

  • Bae J, Hamidoghli A, Won S, Choi W, Lim SG, Kim KW, Lee BJ, Hun SW, Bai SC (2020) Evaluation of seven different functional feed additives in a low fish meal diet for olive flounder, Paralichthys olivaceus. Aquaculture 525:735333. https://doi.org/10.1016/j.aquaculture.2020.735333

  • Choi W, Hamidoghli A, Rivero CJ, Bae J, Kim K-W, Lee B-J, Hur S-W, Han H, Choi YH, Bai SC (2022) Animal and plant proteins as alternative feed ingredients in diets for sub-adult olive flounder Paralichthys olivaceus at farm conditions. Aquac Res 00:1–11. https://doi.org/10.1111/are.15789

    Article  CAS  Google Scholar 

  • Garling DL, Wilson RP (1976) Optimum dietary protein to energy ratio for channel catfish fingerling, Ictalurus punctatus. J Nutr 106:1368–1375. https://doi.org/10.1093/jn/106.9.1368

    Article  CAS  Google Scholar 

  • Güllü K, Acar U, Tezel R, Yozukmaz A (2014) Replacement of fish meal with fish processing by-product silage in diets for the rainbow trout, Oncorhynchus mykiss. Pakistan J Zool 46:1697–1703

    Google Scholar 

  • Halver JE, Hardy RW (2002) Fish Nutrition. In: Sargent JR, Tocher DR, Bell G (eds) The Lipids, 3rd edn. Academic Press, California, pp 182–246

    Google Scholar 

  • Hamidoghli A, Won S, Lee S, Lee S, Farris NW, Bai SC (2020) Nutrition and feeding of olive flounder Paralichthys olivaceus: A review. Rev Fish Sci Aquac 28:340–357. https://doi.org/10.1080/23308249.2020.1740166

    Article  Google Scholar 

  • Han Z, Zhou Y, Zhang X, Yan J, Xiao J, Luo Y, Zheng H, Zhong H (2020) Ghrelin modulates the immune response and increases resistance to Aeromonas hydrophila infection in hybrid tilapia. Fish Shellfish Immunol 98:100–108. https://doi.org/10.1016/j.fsi.2020.01.006

    Article  CAS  Google Scholar 

  • Hultmark D, Steiner H, Rasmuson T, Boman HG (1980) Insect immunity. Purification and properties of three inducible bactericidal proteins from hemolymph of immunized pupae of Hyalophora cecropia. Eur J Biochem 106:7–16. https://doi.org/10.1111/j.1432-1033.1980.tb05991.x

    Article  CAS  Google Scholar 

  • Jeon GH, Kim HS, Myung SH, Cho SH (2014) The effect of the dietary substitution of fishmeal with tuna by-product meal on growth, body composition, plasma chemistry, and amino acid profiles of juvenile Korean rockfish (Sebastes schlegeli). Aquac Nutr 20:753–761. https://doi.org/10.1111/anu.12153

    Article  CAS  Google Scholar 

  • Jung HY, Cho JY, Han KR, Jung HY, Kim IS, Lee G, Kim JK (2017) Biodegradation of the mixture of wild rice (Zizania latifolia) powder and tuna processing waste for use as an additive in fish feed. Korean Fisheries and Aquaculture Society (KOFSAS) Fisheries Conference, Busan, Republic of Korea. Book of Abstracts no. PA-48

  • Kader MA, Koshio S, Ishikawa M, Yokoyama S, Bulbul M, Honda Y, Mamauag RE, Laining A (2011) Growth, nutrient utilization, oxidative condition, and element composition of juvenile red sea bream Pagrus major fed with fermented soybean meal and scallop by-product blend as fishmeal replacement. Fish Sci 77:119–128. https://doi.org/10.1007/s12562-010-0312-9

  • Kader MA, Koshio S, Ishikawa M, Yokoyama S, Bulbul M, Nguyen BT, Gao J, Laining A (2012) Can fermented soybean meal and squid by-product blend be used as fishmeal replacements for Japanese flounder (Paralichthys olivaceus)? Aquac Res 43:1427–1438. https://doi.org/10.1111/j.1365-2109.2011.02945.x

  • Kibenge FSB, Godoy MG, Fast M, Workenhe S, Kibenge MJT (2012) Countermeasures against viral diseases of farmed fish. Antivir Res 95:257–281. https://doi.org/10.1016/j.antiviral.2012.06.003

    Article  CAS  Google Scholar 

  • Kim SS, Galaz GB, Pham MA, Jang JW, Oh DH, Yeo IK, Lee KJ (2009) Effects of dietary supplementation of a meju, fermented soybean meal, and Aspergillus oryzae for juvenile parrot fish (Oplegnathus fasciatus). Asian-Aust J Anim Sci 22:849–856. https://doi.org/10.5713/ajas.2009.80648

    Article  CAS  Google Scholar 

  • Kim SS, Pham MA, Kim KW, Son MH, Lee KJ (2010) Effects of microbial fermentation of soybean on growth performances, phosphorus availability, and antioxidant activity in diets for juvenile olive flounder (Paralichthys olivaceus). Food Sci Biotechnol 19:1605–1610. https://doi.org/10.1007/s10068-010-0227-3

    Article  CAS  Google Scholar 

  • Kim HS, Jung WG, Myung SH, Cho SH, Kim DS (2014a) Substitution effects of fishmeal with tuna byproduct meal in the diet on growth, body composition, plasma chemistry and amino acid profiles of juvenile olive flounder (Paralichthys olivaceus). Aquaculture 431:92–98. https://doi.org/10.1016/j.aquaculture.2014.03.025

    Article  CAS  Google Scholar 

  • Kim HS, Jung WG, Myung SH, Cho SH, Kim DS (2014b) Substitution effects of fishmeal with tuna by-product meal in the diet on growth, body composition, plasma chemistry and amino acid profiles of juvenile olive flounder (Paralichthys olivaceus). Aquaculture 431:92–98

    Article  CAS  Google Scholar 

  • Kim KD, Jang JW, Kim KW, Lee BJ, Hur SW, Han HS (2018) Tuna by-product meal as a dietary protein source replacing fishmeal in juvenile Korean rockfish Sebastes schlegeli. Fish Aquatic Sci 21:29. https://doi.org/10.1186/s41240-018-0107-y

    Article  CAS  Google Scholar 

  • Martínez-Llorens S, Baeza-Ariño R, Nogales-Mérida S, Jover-Cerdá M, Tomás-Vidal A (2012) Carob seed germ meal as a partial substitute in gilthead sea bream (Sparus aurata) diets: Amino acid retention, digestibility, gut and liver histology. Aquaculture 338–341:124–133. https://doi.org/10.1016/j.aquaculture.2012.01.029

    Article  CAS  Google Scholar 

  • Moniruzzaman M, Bae JH, Won SH, Cho SJ, Chang KH, Bai SC (2018) Evaluation of solid-state fermented protein concentrates as a fish meal replacer in the diets of juvenile rainbow trout, Oncorhynchus mykiss. Aquacult Nutr 24:1198–1212. https://doi.org/10.1111/anu.12658

    Article  CAS  Google Scholar 

  • Moniruzzaman M, Damusaru JH, Won SH, Cho SJ, Chang KH, Bai SC (2020) Effects of partial replacement of dietary fish meal by bioprocessed plant protein concentrates on growth performance, hematology, nutrient digestibility and digestive enzyme activities in juvenile Pacific white shrimp, Litopenaeus vannamei. J Sci Food Agric 100:1285–1293. https://doi.org/10.1002/jsfa.10141

    Article  CAS  Google Scholar 

  • Oncul FO, Aya FA, Hamidoghli A, Won S, Lee G, Han KR, Bai SC (2019) Effects of the dietary fermented tuna by-product meal on growth, blood parameters, nonspecific immune response, and disease resistance in juvenile olive flounder, Paralichthys olivaceus. J World Aquac Soc 50:65–77. https://doi.org/10.1111/jwas.12535

    Article  CAS  Google Scholar 

  • Pham HD, Siddik MAB, Ngo MV, Le HM, Rahman MA (2021) Effects of tuna hydrolysate supplementation on growth performance, nutrient utilization and physiological response of snubnose pompano (Trachinotus blochii) fed high poultry by-product meal diets. Aquaculture Reports 21:100875

    Article  Google Scholar 

  • Quade MJ, Roth JA (1997) A rapid, direct assay to measure degranulation of bovine neutrophil primary granules. Vet Immunol Immunopathol 58:239–248. https://doi.org/10.1016/s0165-2427(97)00048-2

    Article  CAS  Google Scholar 

  • Sakai M (1999) Current research status of fish immunostimulants. Aquaculture 172:63–92. https://doi.org/10.1016/S0044-8486(98)00436-0

    Article  CAS  Google Scholar 

  • Seong M, Lee S, Lee S, Song Y, Bae J, Chang K, Bai SC (2018) The effects of different levels of dietary fermented plant-based protein concentrate on growth, hematology, and non-specific immune responses in juvenile olive flounder, Paralicthys olivaceus. Aquaculture 483:196–202. https://doi.org/10.1016/j.aquaculture.2017.10.023

    Article  CAS  Google Scholar 

  • Siddik MAB, Howieson J, Ilham I, Fotedar R (2018a) Growth, biochemical response and liver health of barramundi, Lates calcarifer fed fermented and nonfermented tuna hydrolysate as fishmeal protein replacement ingredients. PeerJ 6:e4870. https://doi.org/10.7717/peerj.4870

    Article  CAS  Google Scholar 

  • Siddik MAB, Howieson J, Patridge GJ, Fotedar R, Gholipourkanani H (2018b) Dietary tuna hydrolysate modulates growth performance, immune response, intestinal morphology and resistance to Streptococcus iniae in juvenile barramundi. Lates Calcarifer Sci Rep 8:15942. https://doi.org/10.1038/s41598-018-34182-4

    Article  CAS  Google Scholar 

  • Siddik MAB, Howieson J, Fotedar R (2019) Beneficial effects of tuna hydrolysate in poultry by-product meal diets on growth, immune response, intestinal health and disease resistance to Vibrio harvei in barramundi, Lates calcarifer. Fish Shellfish Immunol 89:61–70. https://doi.org/10.1016/j.fsi.2019.03.042

    Article  CAS  Google Scholar 

  • Sogbesan A, Ugwumba A (2008) Nutritional evaluation of termite (Macrotermes subhyalinus) meal as animal protein supplements in the diets of Heterobranchus longifilis (Valenciennes, 1840) fingerlings. Turk J Fish Aquat Sci 8:149–157

    Google Scholar 

  • Uyan O, Koshio S, Teshima S, Ishikawa M, Thu M, Alam MS, Michael FR (2006) Growth and phosphorus loading by partially replacing fishmeal with tuna muscle by-product powder in the diet of juvenile Japanese flounder, Paralichthys olivaceus. Aquaculture 257:437–445. https://doi.org/10.1016/j.aquaculture.2006.02.060

    Article  CAS  Google Scholar 

  • Won S, Lee S, Hong J, Park JK, Kim S, Bai SC (2017) Evaluation of dietary natural mineral materials as an antibiotic replacer on growth performance, non-specific immune response and disease resistance in rainbow trout, Oncorhynchus mykiss. Aquac Res 48:4735–4747. https://doi.org/10.1111/are.13295

  • Zeitler MH, Kirchgessner M, Schwarz FJ (1984) Effects of different protein and energy supplies on carcass composition of carp (Cyprinus carpio L). Aquaculture 36:37–48. https://doi.org/10.1016/0044-8486(84)90052-8

    Article  Google Scholar 

Download references

Acknowledgements

The assistance of Feeds and Foods Nutrition Research Center (FFNRC) staff is gratefully appreciated. MM would like to acknowledge the National Research Foundation of Korea (NRF) for providing the postdoctoral research fellowship under the Brain Pool Program (Grant No. 2019H1D3A1A01101555) funded by the Ministry of Science, ICT, and Future Planning.

Funding

This study was supported by the National Research Foundation of Korea through the Framework of International Cooperation Program (NRF-2016K2A9A1A09913758). The study was done as part of the Postdoctoral Research Fellowship of F. A. A.

Author information

Authors and Affiliations

  1. Feeds and Foods Nutrition Research Center, Pukyong National University, Busan, 48574, Republic of Korea

    Frolan A. Aya, Seonghun Won, Ali Hamidoghli & Sungchul C. Bai

  2. Aquaculture Department, Southeast Asian Fisheries Development Center (SEAFDEC/AQD), Binangonan Freshwater Station, 1940, Binangonan, Rizal, Philippines

    Frolan A. Aya

  3. Department of Animal Biotechnology, Jeju International Animal Research Center (JIA), Sustainable Agriculture Research Institute (SARI), Jeju National University, Jeju, 63243, Republic of Korea

    Mohammad Moniruzzaman & Taesun Min

  4. Aquaculture Department, Southeast Asian Fisheries Development Center (SEAFDEC/AQD), Tigbauan Main Station, 5023, Tigbauan, Iloilo, Philippines

    Gregoria S. Pagador

  5. CJ Feed & Care, Twin Tower East, 170, Eulji-Ro, Jung-Gu, Seoul, 04548, Republic of Korea

    Seonghun Won

  6. FAO World Fisheries University Pilot Program, Busan, 48574, Republic of Korea

    Sungchul C. Bai

Authors
  1. Frolan A. Aya
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Mohammad Moniruzzaman
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Gregoria S. Pagador
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Seonghun Won
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Ali Hamidoghli
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Taesun Min
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Sungchul C. Bai
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

FAA and SCB designed the study; FAA, SW, and AH collected and analyzed data, and interpreted results; GSP performed the histological examination of liver and intestine; FAA wrote the manuscript; FAA, MM, TM, and SCB reviewed the manuscript. All authors read and approved the final manuscript.

Corresponding author

Correspondence to Sungchul C. Bai.

Ethics declarations

Ethics approval

Handling of fish specimens were conducted in accordance with the approved protocols of the Animal Care and Use Committee of Pukyong National University.

Consent to participate

All authors consent the participation.

Consent for publication

All authors consent the publication.

Conflict of interest

The authors declare no competing interests.

Additional information

Publisher's note

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

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Aya, F.A., Moniruzzaman, M., Pagador, G.S. et al. Evaluation of dietary fermented tuna by-product meal as partial replacement for unprocessed tuna by-product meal in fishmeal-based diets for juvenile olive flounder Paralichthys olivaceus. Fish Physiol Biochem 48, 1507–1519 (2022). https://doi.org/10.1007/s10695-022-01141-w

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10695-022-01141-w

Keywords

Search

Navigation