Abstract
In a feeding experiment, cottonseed meal (CSM) was used to replace fishmeal (FM) in the diet of snubnose pompano, Trachinotus blochii, supplemented with lysine and methionine to assess the growth, nutritive profile, hematological, histological, and stress biomarker response. Experimental fishes were randomly stocked in five treatments each with triplicates. Five isonitrogenous and isolipidic diets with graded level of CSM (0, 8.7, 17.4, 26.0, and 34.7%) as replacement for FM protein (0, 25, 50, 75, and 100%) were formulated and fed to respective treatments. Comparison between various parameters among the treatments was made using orthogonal polynomial contrasts to indicate the statistical significance. Higher alkaline phosphatase, acid phosphatase, lactate dehydrogenase, malate dehydrogenase, aspartate, and alanine aminotransferase activities were observed in 0CSM group and followed by 100CSM group as higher inclusion level of CSM with higher free gossypol content did not affect the metabolic enzyme activities. The maximum muscular free gossypol accretion of 1.28 mg kg−1 (on wet basis) was recorded in 100CSM group which was very well below the critical limit set by FDA. As a conclusion, fishmeal can be completely replaced using cottonseed meal in the diet of pompano without adverse effect on growth, metabolism, and general health.
This is a preview of subscription content, access via your institution.





Data availability
The data made available upon reasonable request.
Code availability
Not applicable.
References
Agbo NW, Madalla N, Jauncey K (2015) Mixtures of oilseed meals as dietary protein sources in diets of juvenile Nile tilapia (Oreochromis niloticus L.). J Sci Technol Ghana 35:11–24
Ahmed M, Liang H, Kasiya HC, Ji K, Ge X, Ren M, Liu B, Zhu X, Sun A (2019) Complete replacement of fish meal by plant protein ingredients with dietary essential amino acids supplementation for juvenile blunt snout bream (Megalobrama amblycephala). Aquac Nutr 25:205–214. https://doi.org/10.1111/anu.12844
Ahmed I, Reshi QM, Fazio F (2020) The influence of the endogenous and exogenous factors on hematological parameters in different fish species: a review. Aquac Int 10:1–31. https://doi.org/10.1007/s10499-019-00501-3
Anderson AD, Alam MS, Watanabe WO, Carroll PM, Wedegaertner TC, Dowd MK (2016) Full replacement of menhaden fish meal protein by low-gossypol cottonseed flour protein in the diet of juvenile black sea bass Centropristis striata. Aquaculture 464:618–628. https://doi.org/10.1016/j.aquaculture.2016.08.006
AOAC (1995) Official methods of analysis of AOAC International, vol 1, 16th edn. Association of Official Analytical Chemists, Arlington, pp 1230
Bachis E (2017) Fishmeal and fish oil: a summary of global trends. 57th IFFO Annual Conference. https://docplayer.net/88460673-Fishmeal-and-fish-oil-a-summary-of-of-global-trendsdr-enrico-bachis-57-th-iffo-annual-conference-washington.html
Blaxhall PC, Daisley KW (1973) Routine haematological methods for use with fish blood. J Fish Biol 5:771–781. https://doi.org/10.1111/j.1095-8649.1973.tb04510.x
Braga AP, Maciel MV, Guerra DG, Maia IS, Oloris SC, Soto-Blanco B (2012) Extruded-expelled cottonseed meal decreases lymphocyte counts in male sheep. Rev Med Vet 163:147–152
Broderick GA, Kerkman TM, Sullivan HM, Dowd MK, Funk PA (2013) Effect of replacing soybean meal protein with protein from upland cottonseed, Pima cottonseed, or extruded Pima cottonseed on production of lactating dairy cows. J Dairy Sci 96:2374–2386. https://doi.org/10.3168/jds.2012-5723
Bu X, Chen A, Lian X, Chen F, Zhang Y, Muhammad I, Ge X, Yang Y (2017) An evaluation of replacing fish meal with cottonseed meal in the diet of juvenile Ussuri catfish Pseudobagrusus suriensis: growth, antioxidant capacity, nonspecific immunity and resistance to Aeromonas hydrophila. Aquaculture 479:829–837. https://doi.org/10.1016/j.aquaculture.2017.07.032
Cai W, Liu H, Han D, Zhu X, Jin J, Yang Y, Xie S (2022) Complete replacement of fishmeal with plant protein ingredients in Gibel carp (Carassius auratus gibelio) diets by supplementation with essential amino acids without negative impact on growth performance and muscle growth-related biomarkers. Front Mar Sci. https://doi.org/10.3389/fmars.2021.759086
Choi W, Hamidoghli A, Bae J, Won S, Choi YH, Kim KW, Lee BJ, Hur SW, Han H, Bai SC (2020) On-farm evaluation of dietary animal and plant proteins to replace fishmeal in sub-adult olive flounder Paralichthys Olivaceus. Fish Aquat Sci 23:22. https://doi.org/10.1186/s41240-020-00169-4
Covaci A, Voorspoels S, Thomsen C, van Bavel B, Neels H (2006) Evaluation of total lipids using enzymatic methods for the normalization of persistent organic pollutant levels in serum. Sci Total Environ 366:361–366. https://doi.org/10.1016/j.scitotenv.2006.03.006
Deguara S, Jauncey K, Agius C (2003) Enzyme activities and pH variations in the digestive tract of gilthead sea bream. J Fish Biol 62:1033–1043. https://doi.org/10.1046/j.1095-8649.2003.00094.x
Doumas BT, Watson W, Biggs HG (1971) Albumin standards and the measurement of serum albumin with bromcresol green. Clin Chim Acta 31:87–96. https://doi.org/10.1016/S0009-8981(96)06447-9
Drapeau G (1976) Protease from Staphylococcus aureus. Methods Enzymol 45:465–479. https://doi.org/10.1016/S0076-6879(76)45041-3
Ebeneezar S, Vijayagopal P, Srivastava PP, Gupta S, Varghese T, Prabu DL, Chandrasekar S, Varghese E, Sayooj P, Tejpal CS, Wilson L (2019) Dietary lysine requirement of juvenile Silver pompano, Trachinotus blochii (Lacepede, 1801). Aquaculture 511:734234. https://doi.org/10.1016/j.aquaculture.2019.734234
Ebeneezar S, Vijayagopal P, Srivastava PP, Gupta S, Varghese T, Prabu DL, Chandrasekar S, Varghese E, Tejpal CS, Anikuttan KK, Sayooj P (2020) Optimum dietary methionine requirement of juvenile silver pompano, Trachinotus blochii (Lacepede, 1801). Anim Feed Sci Technol 268:114592. https://doi.org/10.1016/j.anifeedsci.2020.114592
Egerton S, Wan A, Murphy K, Collins F, Ahern G, Sugrue I, Busca K, Egan F, Muller N, Whooley J, McGinnity P (2020) Replacing fishmeal with plant protein in Atlantic salmon (Salmo salar) diets by supplementation with fish protein hydrolysate. Sci Rep 10:1–16
FAO (2020) The State of World Fisheries and Aquaculture 2020, Sustainability in action. Rome, Italy. https://doi.org/10.4060/ca9229en
FDA (2021) Code of Federal Regulations Title 21, Modified cottonseed products intended for human consumption section 172.894, MD, USA. https://www.accessdata.fda.gov/scripts/cdrh/cfdocs/cfcfr/CFRSearch.cfm?fr=172.894. Accessed 11 May 2021
Fossati P, Prencipe L (1982) Serum triglycerides determined colorimetrically with an enzyme that produces hydrogen peroxide. Clin Chem 28:2077–2080
Friedewald WT, Levy RI, Fredrickson DS (1972) Estimation of the concentration of low-density lipoprotein cholesterol in plasma, without use of the preparative centrifuge. Clin Chem 18:499–500
Gadelha IC, Fonseca NB, Oloris SC, Melo MM, Soto-Blanco B (2014) Gossypol toxicity from cottonseed products. Sci World J:231635.https://doi.org/10.1155/2014/231635
Gajardo K, Jaramillo-Torres A, Kortner TM, Merrifield DL, Tinsley J, Bakke AM, Krogdahl Å (2017) Alternative protein sources in the diet modulate microbiota and functionality in the distal intestine of Atlantic salmon (Salmo salar). Appl Environ Microbiol 83:e02615-e2616
Garen A, Levinthal C (1960) A fine structure genetic and chemical study of the enzyme alkaline phosphatase of E. coli. I. Purification and Characterization of Alkaline Phosphatase. Biochim Biophys Acta 38:470–483. https://doi.org/10.1016/0006-3002(60)91282-8
Hardy RW, Brezas A (2022) Diet formulation and manufacture. In: Hardy RW, Kaushik SJ (eds) Fish Nutrition, 4th edn. Academic Press, New York, pp 643–708. https://doi.org/10.1016/B978-0-12-819587-1.00002-1
Hassaan MS, El-Sayed AMI, Soltan MA, Iraqi MM, Goda AM, Davies SJ, El-Haroun ER, Ramadan HA (2019) Partial dietary fish meal replacement with cotton seed meal and supplementation with exogenous protease alters growth, feed performance, hematological indices and associated gene expression markers (GH, IGF-I) for Nile tilapia, Oreochromis niloticus. Aquaculture 503:282–292. https://doi.org/10.1016/j.aquaculture.2019.01.009
Hossain MA, Yoshimatsu T (2014) Dietary calcium requirement in fishes. Aquac Nutr 20:1–11. https://doi.org/10.1111/anu.12135
Humason GL (1979) Animal Tissue Techniques, 4th edn. W.H. Freeman and Company, San Francisco
Kalidas C, Sakthivel M, Tamilmani G, Ramesh Kumar P, Nazar AKA, Jayakumar R, Balamurugan V, Ramkumar B, Jothi PR, Gopakumar G (2012) Survival and growth of juvenile silver pompano Trachinotus blochii (Lacepède, 1801) at different salinities in tropical conditions. Indian J Fish 59:95–98
Kalidas C, Rameshkumar P, Prabu DL, Tamilmani G, Anbarasu M, Rajendran P, Thiagu R (2020) Optimizing stocking density for grow-out culture of silver pompano, Trachinotus blochii (lacépède, 1801) in marine floating cages. J Appl Aquac:1-11.https://doi.org/10.1080/10454438.2020.1829245
Karishma R, Sahithya UL, Suneetha P, Naik VCB, Krishna MSR (2016) Determination of total gossypol and free gossypol content in different varieties of Bt and Non Bt cotton seed extracts by high-performance liquid chromatography (HPLC). Res J Biotech 11:70–74
Katsivela E, Kleppe F, Lang S, Wagner F (1995) Ustilago maydis lipase I. Hydrolysis and ester-synthesis activities of crude enzyme preparation. Enzyme Microb Technol 17:739–745. https://doi.org/10.1016/0141-0229(94)00127-D
Krogdahl A, Kortner TM, Hardy RW (2022) Antinutrients and adventitious toxins. In: Hardy RW, Kaushik SJ (eds) Fish Nutrition, 4th edn. Academic Press, New York, pp 775–821
Larsen HN, Snieszko SF (1961) Comparison of various methods of determination of haemoglobin in trout blood. Prog Fish Cult 23:8–17. https://doi.org/10.1577/1548-8659(1961)23[8:COVMOD]2.0.CO;2
Lee KJ, Rinchard J, Dabrowski K, Babiak I, Ottobre JS, Christensen JE (2006) Long-term effects of dietary cottonseed meal on growth and reproductive performance of rainbow trout: three-year study. Anim Feed Sci Technol 126:93–106. https://doi.org/10.1016/j.anifeedsci.2005.06.007
Li MH, Robinson EH (2006) Use of cottonseed meal in aquatic animal diets: a review. N Am J Aquac 68:14–22. https://doi.org/10.1577/A05-028.1
Liang H, Mi H, Ji K, Ge X, Re M, Xie J (2018) Effects of dietary calcium levels on growth performance, blood biochemistry and whole body composition in juvenile bighead carp (Aristichthys nobilis). Turk J Fish Aquat Sci 18:623–631. https://doi.org/10.4194/1303-2712-v18_4_14
Liu XY, Wang Y, Wand JH (2009) Effects of replacing fish meal with soybean meal, rapeseed meal or cottonseed meal on feeding, growth and feed utilization of sutchi catfish (Pangasius sutchi). J Fish China 33:479–487
Liu H, Yan Q, Han D, Jin J, Zhu X, Yang Y, Xie S (2016) Effect of dietary cottonseed meal on growth performance, physiological response, and gossypol accumulation in pre-adult grass carp, Ctenopharyngodon idellus. Chin J Oceanol Limnol 34:992–1003. https://doi.org/10.1007/s00343-016-4115-4
Liu H, Dong X, Tan B, Du T, Zhang S, Yang Y, Chi S, Yang Q, Liu H (2020) Effects of fish meal replacement by low-gossypol cottonseed meal on growth performance, digestive enzyme activity, intestine histology and inflammatory gene expression of silver sillago (Sillago sihama Forsskál) (1775). Aquac Nutr 26:1724–1735. https://doi.org/10.1111/anu.13123
Luo L, Xue M, Wu X, Cai X, Cao H, Liang Y (2006) Partial or total replacement of fish meal by solvent-extracted cottonseed meal in diets for juvenile rainbow trout (Oncorhynchus mykiss). Aquac Nutr 12:418–424. https://doi.org/10.1111/j.1365-2095.2006.00443.x
Mbahinzireki GB, Dabrowski K, Lee KJ, El-Saidy D, Wisner ER (2001) Growth, feed utilization and body composition of tilapia (Oreochromis sp.) fed cotton seed meal-based diets in a recirculating system. Aquac Nutr 7:189–200. https://doi.org/10.1046/j.1365-2095.2001.00172.x
Meiattini F, Prencipe L, Bardelli F, Giannini G, Tarli P (1978) The 4-Hydroxybenzoate/4-aminophenazone chromogenic system used in the enzymic determination of serum cholesterol. Clin Chem 24:2161–2165
Naylor RL, Hardy RW, Buschmann AH, Bush SR, Cao L, Klinger DH, Little DC, Lubchenco J, Shumway SE, Troell M (2021) A 20-year retrospective review of global aquaculture. Nature 591:551–563
Ochoa S (1955) Malic dehydrogenase and malic enzyme. In: Caloric SP, Kaplan N (eds) Methods of Enzymology, vol I. Academic Press, New York, pp 735–745
Prabu DL, Sahu NP, Pal AK, Dasgupta S, Narendra A (2016) Immunomodulation and interferon gamma gene expression in sutchi cat fish, Pangasianodon hypophthalmus: effect of dietary fucoidan rich seaweed extract (FRSE) on pre and post challenge period. Aquac Res 47:199–218. https://doi.org/10.1111/are.12482
Prabu DL, Ebeneezar S, Chandrasekar S, Sayooj P, Vijayagopal P (2017) Indigenous Re-circulatory Aquaculture System (i-RAS) developed for fish nutrition research. Mar Fish Inf Serv Tech Ext Ser 234:20–21
Prabu DL, Ebeneezar S, Chandrasekar S, Tejpal CS, Kavitha M, Sayooj P, Vijayagopal P (2020) Influence of graded level of dietary protein with equated level of limiting amino acids on growth, feed utilization, body indices and nutritive profile of snubnose pompano, Trachinotus blochii (Lacepede, 1801) reared in low saline water. Anim Feed Sci Technol 269:114685. https://doi.org/10.1016/j.anifeedsci.2020.114685
Prabu DL, Ebeneezar S, Chandrasekar S, Kavitha M, Vijayagopal P (2021) Antioxidant defence system based oxidative stress mitigation through dietary jamun tree leaf in experimentally infected snubnose pompano, Trachinotus blochii. Fish Physiol Biochem 47:617–637. https://doi.org/10.1007/s10695-021-00935-8
Reinhold JG (1953) Manual determination of serum total protein, albumin and globulin fractions by Biuret method. In: Reiner M (ed) Standard Method of Clinical Chemistry. Academic Press, New York, p 88
Rick W, Stegbauer HP (1974) Amylase measurement of reducing groups. In: Bergmeyer HV (ed) Methods of Enzymatic Analysis, vol 2, 2nd edn. Academic Press, New York, pp 885– 889
Rinchard J, Lee KJ, Czesny S, Ciereszko A (2003) Effect of feeding cottonseed meal-containing diets to broodstock rainbow trout and their impact on the growth of their progenies. Aquaculture 227:77–88. https://doi.org/10.1016/S0044-8486(03)00496-4
Sarker PK, Kapuscinski AR, McKuin B, Fitzgerald DS, Nash HM, Greenwood C (2020) Microalgae-blend tilapia feed eliminates fishmeal and fish oil, improves growth, and is cost viable. Sci Rep 10:1–14
Shen J, Liu H, Tan B, Dong X, Yang Q, Chi S, Zhang S (2020) Effects of replacement of fishmeal with cottonseed protein concentrate on the growth, intestinal microflora, haematological and antioxidant indices of juvenile golden pompano (Trachinotus ovatus). Aquac Nutr 26:1119–1130. https://doi.org/10.1111/anu.13069
Smith AJ (1997) Postcolumn amino acid analysis. In: Smith BJ (ed) Methods in Molecular Biology, vol 64. Protein Sequencing Protocols. Humana Press, Totowa, pp 139-146
Summerfelt RC, Penne CR (2007) Nutrient retention by fish in a multispecies recirculating aquaculture facility. Int J Recirculating Aquac 8:43–64. https://doi.org/10.21061/ijra.v8i1.1417
Sun H, Tang JW, Yao XH, Wu YF, Wang X, Liu Y, Lou B (2015) Partial substitution of fish meal with fermented cottonseed meal in juvenile black sea bream (Acanthopagrus schlegelii) diets. Aquaculture 446:30–36. https://doi.org/10.1016/j.aquaculture.2015.04.020
Terova G, Gini E, Gasco L, Moroni F, Antonini M, Rimoldi S (2021) Effects of full replacement of dietary fishmeal with insect meal from Tenebrio molitor on rainbow trout gut and skin microbiota. J Anim Sci Biotechnol 12:1–14
Tok NC, Jain KK, Prabu DL, Sahu NP, Sukham M, Pal AK, Siddiah GM, Kumar P (2017) Metabolic and digestive enzyme activity of Pangasianodon hypophthalmus (Sauvage, 1878) fingerlings in response to alternate feeding of different protein levels in the diet. Aquac Res 48:2895–2911. https://doi.org/10.1111/are.13122
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. N Am J Aquac 81:13–39
Wang X, Howell CP, Chen F, Yin J, Jiang Y (2009) Gossypol-A polyphenolic compound from cotton plant. Adv Food Nutr Res 58:215–263. https://doi.org/10.1016/S1043-4526(09)58006-0
Wang XF, Li XQ, Leng XJ, Shan LL, Zhao JX, Wang YT (2014) Effects of dietary cottonseed meal level on the growth, hematological indices, liver and gonad histology of juvenile common carp (Cyprinus carpio). Aquaculture 428:79–87. https://doi.org/10.1016/j.aquaculture.2014.02.040
Wootton IDP (1964) Microanalysis in Medical Biochemistry, 4th edn. Grune & Stratton, New York
Wroblewski F, La Due JS (1955) Lactic dehydrogenase activity in blood. Proc Soc Exp Biol Med 90:210–213
Xu WN, Li JY, Li XF, Huang GQ, Liu WB (2013) Alterations of liver histology and blood biochemistry in blunt snout bream Megalobrama amblycephala fed high-fat diets. Fish Sci 79:661–671. https://doi.org/10.1007/s12562-013-0635-4
Yan QG, Zhu XM, Yang YX, Han D, Jin JY, Xie SW, Li ZJ (2014) Effect of replacement of fish meal with cottonseed meal on growth, hematological physiology, and body composition of grass carp. Acta Hydrobiol Sin 38:362–369
Yang H, Bian Y, Huang L, Lan Q, Ma L, Li X, Leng X (2022) Effects of replacing fish meal with fermented soybean meal on the growth performance, intestinal microbiota, morphology and disease resistance of largemouth bass (Micropterus salmoides). Aquac Rep 22:100954
Yue YR, Zhou QC (2008) Effect of replacing soybean meal with cottonseed meal on growth, feed utilization, and hematological indexes for juvenile hybrid tilapia, Oreochromis niloticus × O. aureus. Aquaculture 284:185–189. https://doi.org/10.1016/j.aquaculture.2008.07.030
Zhang C, Mai K, Ai Q, Zhang W, Duan Q, Tan B, Ma H, Xu W, Liufu Z, Wang X (2006) Dietary phosphorus requirement of juvenile Japanese seabass, Lateolabrax japonicus. Aquaculture 255:201–209. https://doi.org/10.1016/j.aquaculture.2005.11.040
Zhang C, Rahimnejad S, Wang Y-R, Lu K, Song K, Wang L, Mai K (2018) Substituting fish meal with soybean meal in diets for Japanese seabass (Lateolabrax japonicus): effects on growth, digestive enzymes activity, gut histology, and expression of gut inflammatory and transporter genes. Aquaculture 483:173–182
Zhang J, Zhong L, Peng M, Chu W, Liu Z, Dai Z, Hu Y (2019) Replacement of fish meal with soy protein concentrate in diet of juvenile rice field eel Monopterus albus. Aquac Rep 15:100235
Zheng Q, Wen X, Han C, Li H, Xie X (2012) Effect of replacing soybean meal with cottonseed meal on growth, hematology, antioxidant enzymes activity and expression for juvenile grass carp, Ctenopharyngodon idellus. Fish Physiol Biochem 38:1059–1069
Zhou QL, Habte-Tsion HM, Ge X, Liu B, Xie J, Ren M, Miao L, Pan L (2017) Growth performance and TOR pathway gene expression of juvenile blunt snout bream, Megalobrama amblycephala, fed with diets replacing fish meal with cottonseed meal. Aquac Res 48:3693–3704
Acknowledgements
The authors are thankful to Dr. A. Gopalakrishnan, Director, ICAR-CMFRI, Kochi for his constant support to carry out the research work. The authors are also thankful to Scientist-in-Charge of Tuticorin Regional Station of ICAR-CMFRI for facilitating the research work. The authors are also thankful to the Chairperson, Department of Biosciences, Mangalore University, Mangalore for the valuable guidance and suggestion during the entire period of research work. The authors are indebted to Mr. Kalimuthu and Mr. K. Anandan and for their untiring support in the wet laboratory throughout the research work.
Funding
The study was financially supported by the Indian Council of Agricultural Research for the research project “Marine food fish, ornamental fish and lobster nutritional research for mariculture with the grant number: CMFRI/MBT/NTN/24” to the effective implementation.
Author information
Authors and Affiliations
Contributions
Dhanasekaran Linga Prabu: conceptualization; investigation; methodology; and writing-original draft. Pananghat Vijayagopal: funding acquisition; supervision; and writing-review & editing. Sanal Ebeneezar: validation; visualization; and writing-review & editing. Chellappa Kalidas: methodology and visualization. Palsamy Rameshkumar: formal analysis; data curation; and validation. Eldho Varghese: data curation and statistical analysis. Bose Ramar Muniswaran: formal analysis and software.
Corresponding author
Ethics declarations
Consent to participate/ethical statement
The use of juveniles of snubnose pompano for this experiment was carried out according to the guidelines of animal ethical procedures of ICAR-Central Marine Fisheries Research Institute (ICAR-CMFRI), Kochi, by carefully considering the welfare of the fishes.
Consent for publication
All authors agreed with the content, and all gave explicit consent to submit this manuscript in Fish Physiology and Biochemistry.
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
About this article
Cite this article
Prabu, D.L., Vijayagopal, P., Ebeneezar, S. et al. Enzymological, histological, and serum biomarker responses of snubnose pompano on complete replacement of fishmeal using cottonseed meal supplemented with lysine and methionine in the diet. Fish Physiol Biochem 48, 785–804 (2022). https://doi.org/10.1007/s10695-022-01081-5
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10695-022-01081-5
Keywords
- Unconventional feed ingredient
- Trachinotus blochii
- Fishmeal replacement
- Free gossypol accretion
- Lysine deficiency
- Sustainable resource