Skip to main content
Log in

Use of alternative protein sources for fishmeal replacement in the diet of largemouth bass (Micropterus salmoides). Part I: effects of poultry by-product meal and soybean meal on growth, feed utilization, and health

  • Original Article
  • Published:
Amino Acids Aims and scope Submit manuscript

Abstract

Five isonitrogenous and isocaloric diets [containing 54, 30, 15, 10, and 5% fishmeal crude-protein (CP), dry matter (DM) basis] were prepared by replacing fishmeal with poultry by-product meal plus soybean meal to feed juvenile largemouth bass (LMB, with an initial mean body weight of 4.9 g) for 8 weeks. All diets contained 54% CP and 13% lipids. There were four tanks of fish per treatment group (15 fish/tank). The fish were fed twice daily with the same feed intake (g/fish) in all the dietary groups. Results indicated that the inclusion of 15% fishmeal protein in the diet is sufficient for LMB growth. However, some of the fish that were fed diets containing ≤ 15% fishmeal CP had black skin syndrome (characterized by skin darkening and retinal degeneration, as well as intestinal and liver atrophies and structural abnormalities). The concentrations of taurine, methionine, threonine and histidine in serum were reduced (P < 0.05) in fish fed the diets containing 5, 10 and 15% fishmeal CP, compared with the 30 and 54% fishmeal CP diets. Interestingly, the concentrations of tyrosine and tryptophan in serum were higher in fish fed diets with ≤ 15% fishmeal CP than those in the 54% fishmeal CP group. These results indicated that 15% fishmeal CP in the diet containing poultry by-product meal and soybean meal was sufficient for the maximum growth and feed efficiency in LMB but inadequate for their intestinal, skin, eye, and liver health. A reduction in dietary methionine and taurine content and the possible presence of antinutritional factors in the fishmeal replacements diets containing high inclusion levels of soybean meal may contribute to black skin syndrome in LMB. We recommend that the diets of juvenile LMB contain 30% fishmeal CP (DM basis).

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

Access this article

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
Fig. 4
Fig. 5

Similar content being viewed by others

Abbreviations

AA:

Amino acid

BW:

Body weight

CP:

Crude protein

DM:

Dry matter

FCR:

Feed conversion ratio

FI:

Feed intake

HSI:

Hepatosomatic index

IPFR:

Intraperitoneal fat ratio

LMB:

Largemouth bass

PER:

Protein efficiency ratio

VSI:

Viscerosomatic index

WG:

Weight gain

References

  • Akiyoshi H, Inoue A (2004) Comparative histological study of teleost livers in relation to phylogeny. Zool Sci 21:841–850

    Google Scholar 

  • Aragão C, Conceição LE, Martins D, Rønnestad I, Gomes ED, Dinis MT (2004) A balanced dietary amino acid profile improves amino acid retention in post-larval Senegalese sole (Solea senegalensis). Aquaculture 233:293–304

    Google Scholar 

  • Biswas AK, Kaku H, Ji SC, Seoka M, Takii K (2007) Use of soybean meal and phytase for partial replacement of fish meal in the diet of red sea bream, Pagrus major. Aquaculture 267:284–291

    CAS  Google Scholar 

  • Bonaldo A, Roem AJ, Fagioli P, Pecchini A, Cipollini I, Gatta PP (2008) Influence of dietary levels of soybean meal on the performance and gut histology of gilthead sea bream (Sparus aurata L.) and European sea bass (Dicentrarchus labrax L.). Aquac Res 39:970–978

    CAS  Google Scholar 

  • Bruslé J, Anadon GG (1996) The structure and function of fish liver. In: Munshi JSD and Dutta HM (ed) Fish morphology. Boston: Massachusetts. pp 77–93

  • Chen W, Ai Q, Mai K, Xu W, Liufu Z, Zhang W, Cai Y (2011) Effects of dietary soybean saponins on feed intake, growth performance, digestibility and intestinal structure in juvenile Japanese flounder (Paralichthys olivaceus). Aquaculture 318:95–100

    CAS  Google Scholar 

  • Cheng ZJ, Hardy RW, Usry JL (2003) Effects of lysine supplementation in plant protein-based diets on the performance of rainbow trout (Oncorhynchus mykiss) and apparent digestibility coefficients of nutrients. Aquaculture 215:255–265

    CAS  Google Scholar 

  • Chou R, Her B, Su M, Huang G, Wu Y, Chen H (2004) Substituting fish meal with soybean meal in diets of juvenile cobia Rachycentron canadum. Aquaculture 229:325–333

    Google Scholar 

  • Clayton TA, Lindon JC, Everett JR, Charuel C, Hanton G, Le Net JL, Provost JP, Nicholson JK (2007) Hepatotoxin-induced hypertyrosinemia and its toxicological significance. Arch Toxicol 81:201–210

    CAS  PubMed  Google Scholar 

  • Daniel N (2018) A review on replacing fish meal in aqua feeds using plant protein sources. Int J Fish Aquat Study 6:164–179

    Google Scholar 

  • Dashti H, Behbehani A, Abul H, Hussein T (1994) Amino acids in experimental liver cirrhosis: influence of scavengers. Surg Res Commun 16:65–65

    Google Scholar 

  • Du ZY, Clouet P, Huang LM, Degrace P, Zheng WH, He JG, Tian LX, Liu YJ (2008) Utilization of different dietary lipid sources at high level in herbivorous grass carp (Ctenopharyngodon idella): mechanism related to hepatic fatty acid oxidation. Aquac Nutr 14:77–92

    CAS  Google Scholar 

  • Elmada CZ, Huang W, Jin M, Liang X, Mai K, Zhou Q (2016) The effect of dietary methionine on growth, antioxidant capacity, innate immune response and disease resistance of juvenile yellow catfish (Pelteobagrus fulvidraco). Aquac Nutr 22:1163–1173

    CAS  Google Scholar 

  • Evans JJ, Pasnik DJ, Peres H, Lim C, Klesius PH (2005) No apparent differences in intestinal histology of channel catfish (Ictalurus punctatus) fed heat-treated and non-heat-treated raw soybean meal. Aquac Nutr 11:123–129

    CAS  Google Scholar 

  • Folch J, Lees M, Stanley GS (1957) A simple method for the isolation and purification of total lipids from animal tissues. J Biol Chem 226:497–509

    CAS  PubMed  Google Scholar 

  • Food and Agricultural Organization of the United Nations (FAO (2012) The State of World Fisheries and Aquaculture 2012 (SOFIA). FAO Fisheries and Aquaculture Department, Rome

    Google Scholar 

  • Francis G, Makkar HP, Becker K (2001) Antinutritional factors present in plant-derived alternate fish feed ingredients and their effects in fish. Aquaculture 199:197–227

    CAS  Google Scholar 

  • Gao Z, Wang X, Tan C, Zhou H, Mai K, He G (2019) Effect of dietary methionine levels on growth performance, amino acid metabolism and intestinal homeostasis in turbot (Scophthalmus maximus L.). Aquaculture 498:335–342  

    CAS  Google Scholar 

  • Gaylord TG, Sealey WM, Barrows FT, Myrick CA, Fornshell G (2017) Evaluation of ingredient combinations from differing origins (fishmeal, terrestrial animal and plants) and two different formulated nutrient targets on rainbow trout growth and production efficiency. Aquac Nutr 23:1319–1328

    CAS  Google Scholar 

  • Gipson IK, Anderson RA (1977) Response of the lysosomal system of the corneal epithelium to tyrosine-induced cell injury. J Histochem Cytochem 25:1351–1362

    CAS  PubMed  Google Scholar 

  • Glencross BD, Carter CG, Duijster N, Evans DR, Dods K, McCafferty P, Hawkins WE, Maas R, Sipsas S (2004) A comparison of the digestibility of a range of lupin and soybean protein products when fed to either Atlantic salmon (Salmo salar) or rainbow trout (Oncorhynchus mykiss). Aquaculture 237:333–346

    CAS  Google Scholar 

  • Goldsmith LA, Reed J (1976) Tyrosine-induced eye and skin lesions: a treatable genetic disease. JAMA 236:382–384

    CAS  PubMed  Google Scholar 

  • Goytortua-Bores E, Civera-Cerecedo R, Rocha-Meza S, Green-Yee A (2006) Partial replacement of red crab (Pleuroncodes planipes) meal for fish meal in practical diets for the white shrimp Litopenaeus vannamei. Effects on growth and in vivo digestibility. Aquaculture 256:414–422  

    CAS  Google Scholar 

  • Hardy RW (2010) Utilization of plant proteins in fish diets: effects of global demand and supplies of fishmeal. Aquac Res 41:770–776

    CAS  Google Scholar 

  • Hardy RW, Shearer KD (1985) Effect of dietary calcium phosphate and zinc supplementation on whole body zinc concentration of rainbow trout (Salmo gairdneri). Can J Fish Aquat Sci 42:181–184

    CAS  Google Scholar 

  • Hou YQ, He WL, Hu SD, Wu G (2019) Composition of polyamines and amino acids in plant-source foods for human consumption. Amino Acids 51:1153–1165

    CAS  PubMed  Google Scholar 

  • Huang D, Wu Y, Lin Y, Chen J, Karrow N, Ren X, Wang Y (2017) Dietary protein and lipid requirements for juvenile largemouth bass, Micropterus salmoides. J World Aquac Soc 48:782–790

    CAS  Google Scholar 

  • Jacques B, Anadon GG (1996) The structure and function of fish liver. In: Dutta HM (ed) Fish morphology. Taylor & Francis Group, London, pp 77–93

    Google Scholar 

  • Johnston IA (2001) Muscle development and growth, vol 18. Gulf Professional Publishing, Oxford, United Kingdom

    Google Scholar 

  • Kader MA, Koshio S, Ishikawa M, Yokoyama S, Bulbul M (2010) Supplemental effects of some crude ingredients in improving nutritive values of low fishmeal diets for red sea bream, Pagrus major. Aquaculture 308:136–144

    Google Scholar 

  • Kaushik SJ, Seiliez I (2010) Protein and amino acid nutrition and metabolism in fish: current knowledge and future needs. Aquac Res 41:322–332

    CAS  Google Scholar 

  • Kikuchi K, Furuta T, Iwata N, Onuki K, Noguchi T (2009) Effect of dietary lipid levels on the growth, feed utilization, body composition and blood characteristics of tiger puffer Takifugu rubripes. Aquaculture 298:111–117

    CAS  Google Scholar 

  • Kuang SY, Xiao WW, Feng L, Liu Y, Jiang J, Jiang WD, Hu K, Li SH, Tang L, Zhou XQ (2012) Effects of graded levels of dietary methionine hydroxy analogue on immune response and antioxidant status of immune organs in juvenile Jian carp (Cyprinus carpio var. Jian). Fish Shellfish Immunol 32:629–636

    CAS  PubMed  Google Scholar 

  • Laviano A, Cangiano C, Preziosa I, Riggio O, Conversano L, Cascino A, Ariemma S, Fanelli FR (1997) Plasma tryptophan levels and anorexia in liver cirrhosis. Int J Eating Dis 21:181–186

    CAS  Google Scholar 

  • Li P, Wu G (2020) Composition of amino acids and related nitrogenous nutrients in feedstuffs for animal diets. Amino Acids 52:523–542

    CAS  PubMed  Google Scholar 

  • Li P, Yin YL, Li D, Kim SW, Wu G (2007) Amino acids and immune function. Br J Nutr 98:237–252

    CAS  PubMed  Google Scholar 

  • Li P, Mai K, Trushenski J, Wu G (2009) New developments in fish amino acid nutrition: towards functional and environmentally oriented aquafeeds. Amino Acids 37:43–53

    PubMed  Google Scholar 

  • Li X, Rezaei R, Li P, Wu G (2011) Composition of amino acids in feed ingredients for animal diets. Amino Acids 40:1159–1168

    CAS  PubMed  Google Scholar 

  • Li S, Ding G, Wang A, Sang C, Chen N (2019) Replacement of fishmeal by chicken plasma powder in diets for largemouth bass (Micropterus salmoides): Effects on growth performance, feed utilization and health status. Aquac Nutr 25:1431–1439

    CAS  Google Scholar 

  • Li X, Zheng SX, Ma XK, Cheng KM, Wu GY (2020a) Oxidation of energy substrates in tissues of largemouth bass (Micropterus salmoides). Amino Acids 52:1017–1032

    CAS  PubMed  Google Scholar 

  • Li X, Zheng SX, Jia SC, Song F, Zhou CP, Wu GY (2020b) Effects of dietary starch and lipid levels on the protein retention and growth of largemouth bass (Micropterus salmoides). Amino Acids 52:999–1016

    CAS  PubMed  Google Scholar 

  • Li XY, Zheng SX, Ma XK, Cheng KM, Wu G (2020c) Effects of dietary protein and lipid levels on growth performance, feed utilization, and liver histology of largemouth bass (Micropterus salmoides). Amino Acids 52:1043–1061

    CAS  PubMed  Google Scholar 

  • Li XL, Zheng SX, Wu G (2020d) Nutrition and metabolism of glutamate and glutamine in fish. Amino Acids 52:671–691

    CAS  PubMed  Google Scholar 

  • Li XY, Zheng SX, Cheng KM, Ma XK, G Wu (2020e) Use of alternative protein sources for fishmeal replacement in the diet of largemouth bass (Micropterus salmoides). Part II: Effects of supplementation with methionine or taurine on growth, feed utilization, and health. Amino Acids. https://doi.org/10.1007/s00726-020-02922-4

  • Machado M, Azeredo R, Díaz-Rosales P, Afonso A, Peres H, Oliva-Teles A, Costas B (2015) Dietary tryptophan and methionine as modulators of European seabass (Dicentrarchus labrax) immune status and inflammatory response. Fish Shellfish Immunol 42:353–362

    CAS  PubMed  Google Scholar 

  • Miao S, Zhao C, Zhu J, Hu J, Dong X, Sun L (2018) Dietary soybean meal affects intestinal homoeostasis by altering the microbiota, morphology and inflammatory cytokine gene expression in northern snakehead. Sci Rep 8:1–10

    Google Scholar 

  • Naylor RL, Hardy RW, Bureau DP, Chiu A, Elliott M, Farrell AP, Forster I, Gatlin DM III, Goldburg RJ, Hua K (2009) Feeding aquaculture in an era of finite resources. Proc Natl Acad Sci USA 106:15103–15110

    CAS  PubMed  Google Scholar 

  • Ninomiya T, Yoon S, Sugano M, Nagano H, Kasuga M, Hayashi Y, Kumon Y, Seo Y, Shimizu K (1999) Improvement of molar ratio of branched-chain amino acids to tyrosine (btr) associated with liver fibrosis in chronic hepatitis C patients treated with interferon-α. Dig Dis Sci 44:1027–1033

    CAS  PubMed  Google Scholar 

  • Olsen RL, Hasan MR (2012) A limited supply of fishmeal: impact on future increases in global aquaculture production. Trends Food Sci Technol 27:120–128

    CAS  Google Scholar 

  • Rašković BS, Stanković MB, Marković ZZ, Poleksić VD (2011) Histological methods in the assessment of different feed effects on liver and intestine of fish. J Agric Sci 56:87–100

    Google Scholar 

  • Rawles SD, Green BW, McEntire ME, Gaylord TG, Barrows FT (2018) Reducing dietary protein in pond production of hybrid striped bass (Morone chrysops × M. saxatilis): effects on fish performance and water quality dynamics. Aquaculture 490:217–227

    CAS  Google Scholar 

  • Ren X, Wang Y, Chen JM, Wu YB, Huang D, Jiang DL, Li P (2018) Replacement of fishmeal with a blend of poultry byproduct meal and soybean meal in diets for largemouth bass, Micropterus salmoides. J World Aquac Soc 49:155–164

    Google Scholar 

  • Rimoldi S, Finzi G, Ceccotti C, Girardello R, Grimaldi A, Ascione C, Terova G (2016) Butyrate and taurine exert a mitigating effect on the inflamed distal intestine of European sea bass fed with a high percentage of soybean meal. Fish Aquatic Sci 19:40

    Google Scholar 

  • Rossi W Jr, Davis DA (2012) Replacement of fishmeal with poultry by-product meal in the diet of Florida pompano Trachinotus carolinus L. Aquaculture 338:160–166

    Google Scholar 

  • Saavedra M, Pousão-Ferreira P, Yúfera M, Dinis M, Conceição L (2009) A balanced amino acid diet improves Diplodus sargus larval quality and reduces nitrogen excretion. Aquac Nutr 15:517–524

    CAS  Google Scholar 

  • Sabbagh M, Schiavone R, Brizzi G, Sicuro B, Zilli L, Vilella S (2019) Poultry by-product meal as an alternative to fish meal in the juvenile gilthead seabream (Sparus aurata) diet. Aquaculture 511:734220

    Google Scholar 

  • Salerno F, Dell’Oca M, Incerti P, Uggeri F, Beretta E (1984) Alterations of plasma and brain tryptophan in hepatic encephalopathy: a study in humans and in experimental animals. In: Capocaccia L, Fischer JE, Rossi-Fanelli F (eds) Hepatic encephalopathy in chronic liver failure. Springer, New York, pp 95–106

    Google Scholar 

  • Salze G, McLean E, Battle PR, Schwarz MH, Craig SR (2010) Use of soy protein concentrate and novel ingredients in the total elimination of fish meal and fish oil in diets for juvenile cobia, Rachycentron canadum. Aquaculture 298:294–299

    CAS  Google Scholar 

  • Santos GA, Rodrigues I, Starkl V, Naehrer K, Hofstetter U, Encarnação P (2010) Mycotoxins in aquaculture: Occurrence in feeds components and impact on animal performance. In: Cruz-Suarez LE, Ricque Marie D, Tapia-Salazar M, Nieto-López MG, Villarreal-Cavazos DA, Gamboa-Delgado J (eds) Avances en Nutrición Acuicola. Universidad Autónoma de Nuevo León, Monterrey, México, pp 502–513

    Google Scholar 

  • Silva-Carrillo Y, Hernández C, Hardy RW, González-Rodríguez B, Castillo-Vargasmachuca S (2012) The effect of substituting fish meal with soybean meal on growth, feed efficiency, body composition and blood chemistry in juvenile spotted rose snapper Lutjanus guttatus (Steindachner, 1869). Aquaculture 364:180–185

    Google Scholar 

  • Tacon AGJ, Cowey CB (1985) Protein and amino acid requirements. In: Tytler P, Calow P (eds) Fish energetics. Springer, New York, pp 155–183

    Google Scholar 

  • Tacon AGJ, Metian M (2008) Global overview on the use of fish meal and fish oil in industrially compounded aquafeeds: trends and future prospects. Aquaculture 285:146–158

    CAS  Google Scholar 

  • Takeuchi T (2014) Progress on larval and juvenile nutrition to improve the quality and health of seawater fish: a review. Fish Sci 80:389–403

    CAS  Google Scholar 

  • Tidwell JH, Coyle SD, Bright LA (2019) Largemouth bass aquaculture. 5M Publishing Ltd., Sheffield, UK, pp 37–47

    Google Scholar 

  • Torrecillas S, Mompel D, Caballero MJ, Montero D, Merrifield D, Rodiles A, Robaina L, Zamorano MJ, Karalazos V, Kaushik S, Izquierdo M (2017) Effect of fishmeal and fish oil replacement by vegetable meals and oils on gut health of European sea bass (Dicentrarchus labrax). Aquaculture 468:386–398

    CAS  Google Scholar 

  • Turchini GM, Trushenski JT, Glencross BD (2019) Thoughts for the future of aquaculture nutrition: realigning perspectives to reflect contemporary issues related to judicious use of marine resources in aquafeeds. North Am J Aquac 81:13–39

    Google Scholar 

  • Venou B, Alexis M, Fountoulaki E, Haralabous J (2006) Effects of extrusion and inclusion level of soybean meal on diet digestibility, performance and nutrient utilization of gilthead sea bream (Sparus aurata). Aquaculture 261:343–356

    CAS  Google Scholar 

  • Vielma J, Mäkinen T, Ekholm P, Koskela J (2000) Influence of dietary soy and phytase levels on performance and body composition of large rainbow trout (Oncorhynchus mykiss) and algal availability of phosphorus load. Aquaculture 183:349–362

    CAS  Google Scholar 

  • Wilkins BJ, Pack M (2013) Zebrafish models of human liver development and disease. Compr Physiol 3:1213–1230

    PubMed  PubMed Central  Google Scholar 

  • Wilson RP (1994) Utilization of dietary carbohydrate by fish. Aquaculture 124:67–80

    CAS  Google Scholar 

  • Wu G (2013) Amino acids: biochemistry and nutrition. CRC Press, Boca Raton, Florida

    Google Scholar 

  • Wu G (2018) Principles of animal nutrition. CRC Press, Boca Raton, Florida

    Google Scholar 

  • Yamamoto T, Sugita T, Furuita H (2005) Essential amino acid supplementation to fish meal-based diets with low protein to energy ratios improves the protein utilization in juvenile rainbow trout Oncorhynchus mykiss. Aquaculture 246:379–391

    CAS  Google Scholar 

  • Yang YH, Wang YY, Lu Y, Li QZ (2011) Effect of replacing fish meal with soybean meal on growth, feed utilization and nitrogen and phosphorus excretion on rainbow trout (Oncorhynchus mykiss). Aquac Int 19:405–419

    CAS  Google Scholar 

  • Zhou QC, Mai KS, Tan BP, Liu YJ (2005) Partial replacement of fishmeal by soybean meal in diets for juvenile cobia (Rachycentron canadum). Aquac Nutr 11:175–182

    CAS  Google Scholar 

Download references

Acknowledgments

We thank students and research assistants in our laboratory for helpful discussions. Financial support by Guangdong Yuehai Feeds Group Co., Ltd. is gratefully appreciated.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Guoyao Wu.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

This study was approved by the Institutional Animal Care and Use Committee of Texas A&M University.

Informed consent

No informed consent is required for this study.

Additional information

Handling editor: F. Blachier.

Publisher's Note

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

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Li, X., Zheng, S., Ma, X. et al. Use of alternative protein sources for fishmeal replacement in the diet of largemouth bass (Micropterus salmoides). Part I: effects of poultry by-product meal and soybean meal on growth, feed utilization, and health. Amino Acids 53, 33–47 (2021). https://doi.org/10.1007/s00726-020-02920-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00726-020-02920-6

Keywords

Navigation