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Effects of dietary plant protein sources intake on growth, digestive enzyme activity, edible tissue nutritional status and intestinal health of the omnivorous Redclaw crayfish, Cherax quadricarinatus

Published online by Cambridge University Press:  04 January 2023

Zongzheng Jiang ,
Dunwei Qian ,
Zhenye Liang ,
Yongyi Jia ,
Chang Xu Open the ORCID record for Chang Xu [Opens in a new window]  and
Erchao Li Open the ORCID record for Erchao Li [Opens in a new window]
Zongzheng Jiang
Affiliation:
Key Laboratory of Tropical Hydrobiology and Biotechnology of Hainan Province, Hainan Aquaculture Breeding Engineering Research Center, College of Marine Sciences, Hainan University, Haikou, Hainan 570228, People’s Republic of China
Dunwei Qian
Affiliation:
Key Laboratory of Tropical Hydrobiology and Biotechnology of Hainan Province, Hainan Aquaculture Breeding Engineering Research Center, College of Marine Sciences, Hainan University, Haikou, Hainan 570228, People’s Republic of China
Zhenye Liang
Affiliation:
Key Laboratory of Tropical Hydrobiology and Biotechnology of Hainan Province, Hainan Aquaculture Breeding Engineering Research Center, College of Marine Sciences, Hainan University, Haikou, Hainan 570228, People’s Republic of China
Yongyi Jia
Affiliation:
Agriculture Ministry Key Laboratory of Healthy Freshwater Aquaculture, Key Laboratory of Fish Health and Nutrition of Zhejiang Province, Key Laboratory of Freshwater Aquaculture Genetics and Breeding of Zhejiang Province, Zhejiang Institute of Freshwater Fisheries, Huzhou, People’s Republic of China
Chang Xu*
Affiliation:
Key Laboratory of Tropical Hydrobiology and Biotechnology of Hainan Province, Hainan Aquaculture Breeding Engineering Research Center, College of Marine Sciences, Hainan University, Haikou, Hainan 570228, People’s Republic of China
Erchao Li
Affiliation:
Key Laboratory of Tropical Hydrobiology and Biotechnology of Hainan Province, Hainan Aquaculture Breeding Engineering Research Center, College of Marine Sciences, Hainan University, Haikou, Hainan 570228, People’s Republic of China
*
*Corresponding author: Dr Chang Xu, email cxu@hainanu.edu.cn
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Abstract

For the omnivorous Cherax quadricarinatus crayfish, plant raw materials can be good alternatives to dietary fish meal (FM). A 56-d feeding trial was conducted in C. quadricarinatus (11·70 (se 0·13) g). Diet with 100 % FM as the protein source was the control. Seven experimental diets were formulated by replacing 75 or 100 % of FM with soyabean meal (SM75, SM100) or cottonseed meal (CM75 and CM100), and a mixture of SM and CM (protein content is 1:1) replacing 50, 75 or 100 % of FM (SC50, SC75 and SC100). Crayfish fed the CM100 and SC100 showed significantly lower weight gain (WG), specific growth rate, trypsin and pepsin activities compared with the control diet. Crayfish in CM100 group showed significantly higher GPx, alanine aminotransferase, aspartate aminotransferase activities and malondialdehyde content than the control. SM100 and CM100 diets can cause slight separation of the peritrophic membrane from the intestinal folds. The pepsin activity of crayfish in SC50 was significantly higher than those in other experimental diets. The highest WG and muscle arginine content were also found in crayfish fed SC50. The relative abundance of Proteobacteria, Unclassified Enterobacteriaceae and Candidatus Bacilloplasma was significantly higher, but Actinobacteriota was significantly lower in SM100, CM100 and SC100 than in control. Microbiota functional prediction indicated that the relative abundance of ‘cell motility’ pathway in crayfish fed CM100 was significantly decreased compared with the control. In conclusion, only half of the FM can be effectively substituted with a mixture of SM and CM (protein content is 1:1) for C. quadricarinatus.

Keywords

Cherax quadricarinatusPlant protein sourcesWeight gainDigestive abilityIntestinal health
Type
Research Article
Information
British Journal of Nutrition , Volume 130 , Issue 6 , 28 September 2023 , pp. 978 - 995
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Copyright
© The Author(s), 2023. Published by Cambridge University Press on behalf of The Nutrition Society

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References

Wang, JX, Zhang, HT, Yang, QH, et al. (2020) Effects of replacing soybean meal with cottonseed meal on growth, feed utilization and non-specific immune enzyme activities for juvenile white shrimp, Litopenaeus vannamei . Aquacult Rep 16, 100255.Google Scholar
Zhang, JS, Yin, WJ & Gao, N (2021) Effect of feed protein level on growth and feed conversion ratio of Oncorhynchus masou masou juvenile fish. J Aquacult 42, 13–17.Google Scholar
FAO (2020) The State of World Fisheries and Aquaculture 2020. Sustainability in Action. Rome: FAO. pp. 44.Google Scholar
Cao, L, Naylor, R, Henriksson, P, et al. (2015) China’s aquaculture and the world’s wild fisheries. Science 347, 133–135.Google ScholarPubMed
Hardy, RW (2006) Fish meal prices drive changes in fish feed formulations. Aquacult Magazine 32, 29–31.Google Scholar
Francis, G, Makkar, HPS & Becker, K (2001) Antinutritional factors present in plant-derived alternate fish feed ingredients and their effects in fish. Aquaculture 199, 197–227.CrossRefGoogle Scholar
Brinker, A & Reiter, R (2011) Fish meal replacement by plant protein substitution and guar gum addition in trout feed, Part I: effects on feed utilization and fish quality. Aquaculture 310, 350–360.CrossRefGoogle Scholar
Dayal, JS, Jannathulla, R, Ambasankar, K, et al. (2020) Aspergillus niger fermented plant protein mix as a potential substitute for fishmeal in the diet of Penaeus vannamei (Boone, 1931). Aquacult Nutr 26, 853–865.Google Scholar
Suárez, JA, Gaxiola, G, Mendoza, R, et al. (2009) Substitution of fish meal with plant protein sources and energy budget for white shrimp Litopenaeus vannamei (Boone, 1931). Aquaculture 289, 118–123.Google Scholar
Yang, QH, Tan, BP, Zhou, XQ, et al. (2014) Replacement of fish meal with plant protein mixture in diets for pacific white shrimp (Litopenaeus vannamei). Chin J Animal Nutr 26, 1486–1495.Google Scholar
Yue, YR, Liu, YJ, Tian, LX, et al. (2012) Effects of replacing fish meal with soybean meal and peanut meal on growth, feed utilization and haemolymph indexes for juvenile white shrimp Litopenaeus vannamei, Boone. Aquac Res 43, 1687–1696.CrossRefGoogle Scholar
Tan, Q, Song, D, Chen, X, et al. (2018) Replacing fish meal with vegetable protein sources in feed for juvenile red swamp crayfish, Procambarus clarkii: effects of amino acids supplementation on growth and feed utilization. Aquacult Nutr 24, 858–864.Google Scholar
Bulbul, M, Kader, MA, Asaduzzaman, M, et al. (2016) Can canola meal and soybean meal be used as major dietary protein sources for kuruma shrimp, Marsupenaeus japonicus? Aquaculture 452, 194–199.Google Scholar
Hu, YJ, Hu, Y, Wu, TQ, et al. (2019) Effects of high dietary levels of cottonseed meal and rapeseed meal on growth performance, muscle texture, and expression of muscle-related genes in grass carp. North Am J Aquacult 81, 235–241.Google Scholar
Jiang, HB, Chen, LQ, Qin, JG, et al. (2013) Partial or complete substitution of fish meal with soybean meal and cottonseed meal in Chinese mitten crab Eriocheir sinensis diets. Aquacult Int 21, 617–628.CrossRefGoogle Scholar
Luo, Z, Li, XD, Wang, WM, et al. (2011) Partial replacement of fish meal by a mixture of soybean meal and rapeseed meal in practical diets for juvenile Chinese mitten crab Eriocheir sinensis: effects on growth performance and in vivo digestibility: partial replacement of FM by a mixture of SBM and RM. Aquacult Res 42, 1615–1622.CrossRefGoogle Scholar
Edgerton, BF (2005) Freshwater crayfish production for poverty alleviation. World Aquaculture 36, 48, 50, 52–55, 62–64.Google Scholar
Saoud, IP, Ghanawi, J, Thompson, KR, et al. (2013) A review of the culture and diseases of redclaw crayfish Cherax quadricarinatus (Von Martens 1868). J World Aquacult Soc 44, 1–29.Google Scholar
Yin, Y, Yan, WH, Zheng, Y, et al. (2018) Research progress and industrial development prospect in Jiangsu province for Cherax quadricarinatus . J Aquacult 39, 9–13.Google Scholar
Campaña-Torres, A, Martínez Córdova, LR, Villarreal Colmenares, H, et al. (2006) Apparent dry matter and protein digestibility of vegetal and animal ingredients and diets for pre-adult Australian redclaw crayfish Cherax quadricarinatus (von Martens 1858). Hidrobiológica 16, 103–106.Google Scholar
Campaña-Torres, A, Martínez Córdova, LR, Villarreal Colmenares, H, et al. (2008) Carbohydrate and lipid digestibility of animal and vegetal ingredients and diets for the pre-adult redclaw crayfish, Cherax quadricarinatus (von Martens): carbohydrate and lipid digestibility for redclaw. Aquacult Res 39, 1115–1121.CrossRefGoogle Scholar
Figueiredo, MSRB & Anderson, AJ (2003) Ontogenetic changes in digestive proteases and carbohydrases from the Australian freshwater crayfish, redclaw Cherax quadricarinatus (Crustacea, Decapoda, Parastacidae): changes in digestive enzymes. Aquacult Res 34, 1235–1239.Google Scholar
Figueiredo, MSRB, Kricker, JA & Anderson, AJ (2001) Digestive enzyme activities in the alimentary tract of redclaw crayfish, Cherax quadricarinatus (decapoda: parastacidae). J Crustacean Biol 21, 334–344.Google Scholar
Pavasovic, A, Richardson, NA, Mather, PB, et al. (2006) Influence of insoluble dietary cellulose on digestive enzyme activity, feed digestibility and survival in the red claw crayfish, Cherax quadricarinatus (von Martens). Aquacult Res 37, 25–32.Google Scholar
Xue, XM, Anderson, AJ, Richardson, NA, et al. (1999) Characterisation of cellulase activity in the digestive system of the redclaw crayfish (Cherax quadricarinatus). Aquaculture 180, 373–386.Google Scholar
Parma, L, Candela, M, Soverini, M, et al. (2016) Next-generation sequencing characterization of the gut bacterial community of gilthead sea bream (Sparus aurata, L.) fed low fishmeal based diets with increasing soybean meal levels. Anim Feed Sci Technol 222, 204–216.CrossRefGoogle Scholar
Wu, SG, Ren, Y, Peng, C, et al. (2015) Metatranscriptomic discovery of plant biomass-degrading capacity from grass carp intestinal microbiomes. FEMS Microbiology Ecology 91, fiv107.CrossRefGoogle ScholarPubMed
Zhao, HX (2015) Study on the Diversity and Function of Intestinal Bacterial Flora from Different Wild Animals (Ma Thesis). Jilin Agricultural University. https://kns.cnki.net/KCMS/detail/detail.aspx?dbname=CMFD201601&filename=1015963696.nh. Google Scholar
Zhu, H (2018) Comparative Analysis of Gut Microbiota in Five Herbivores (PhD Thesis). Sichuan Agriculture University.Google Scholar
Qian, DW, Yang, XL, Xu, C, et al. (2021) Growth and health status of the red claw crayfish, Cherax quadricarinatus, fed diets with four typical plant protein sources as a replacement for fish meal. Aquacult Nutr 27, 795–806.CrossRefGoogle Scholar
AOAC (2005) Official methods of analysis of the Association of Analytical Chemists International (18th ed.), Gaithersburg, Maryland, USA 45, 75–76.Google Scholar
Chen, GF, Feng, L, Kuang, SY, et al. (2012) Effect of dietary arginine on growth, intestinal enzyme activities and gene expression in muscle, hepatopancreas and intestine of juvenile Jian carp (Cyprinus carpio var. Jian). Br J Nutr 108, 195–207.Google ScholarPubMed
Cheng, ZY, Ai, QH, Mai, KS, et al. (2010) Effects of dietary canola meal on growth performance, digestion and metabolism of Japanese seabass, Lateolabrax japonicus . Aquaculture 305, 102–108.CrossRefGoogle Scholar
Benzie, IFF & Strain, JJ (1996) The Ferric Reducing Ability of Plasma (FRAP) as a measure of ‘Antioxidant Power’: the FRAP assay. Anal Biochem 239, 70–76.CrossRefGoogle ScholarPubMed
Buege, JA & Aust, SD (1978) [30] Microsomal lipid peroxidation. Methods Enzymol 302–310.Google Scholar
Nebot, C, Moutet, M, Huet, P, et al. (1993) Spectrophotometric assay of superoxide dismutase activity based on the activated autoxidation of a tetracyclic catechol. Anal Biochem 214, 442–451.CrossRefGoogle ScholarPubMed
Reiners, JJJ, Kodari, E, Cappel, RE, et al. (1991) Assessment of the antioxidant/prooxidant status of murine skin following topical treatment with 12-O-tetradecanoylphorbol-13-acetate and throughout the ontogeny of skin cancer. Part II: quantitation of glutathione and glutathione disulfide. Carcinog 12, 2345–2352.CrossRefGoogle ScholarPubMed
Bradford, MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72, 248–254.CrossRefGoogle ScholarPubMed
Wang, Q, Garrity, GM, Tiedje, JM, et al. (2007) Naïve Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microbiol 73, 5261–5267.CrossRefGoogle ScholarPubMed
Hammer, Ø, Harper, DAT & Ryan, PD (2001) PAST: paleontological statistics software package for education and data analysis. Palaeontol Electronica 4, 9.Google Scholar
Segata, N, Izard, J, Waldron, L, et al. (2011) Metagenomic biomarker discovery and explanation. Genome Biol 12, 1–18.CrossRefGoogle ScholarPubMed
Langille, MGI, Zaneveld, J, Caporaso, JG, et al. (2013) Predictive functional profiling of microbial communities using 16S rRNA marker gene sequences. Nat Biotechnol 31, 814–821.Google ScholarPubMed
Alvarez, JS, Hernández-Llamas, A, Galindo, J, et al. (2007) Substitution of fishmeal with soybean meal in practical diets for juvenile white shrimp Litopenaeus schmitti (Pérez-Farfante & Kensley 1997). Aquacult Res 38, 689–695.Google Scholar
Kader, MA & Koshio, S (2012) Effect of composite mixture of seafood by-products and soybean proteins in replacement of fishmeal on the performance of red sea bream, Pagrus major . Aquaculture 368, 95–102.CrossRefGoogle Scholar
Sun, H, Tang, JW, Yao, XH, et al. (2016) Effects of replacement of fish meal with fermented cottonseed meal on growth performance, body composition and haemolymph indexes of Pacific white shrimp, Litopenaeus vannamei Boone, 1931. Aquacult Res 47, 2623–2632.CrossRefGoogle Scholar
Huang, YJ, Zhang, NN, Fan, WJ, et al. (2018) Soybean and cottonseed meals are good candidates for fishmeal replacement in the diet of juvenile Macrobrachium nipponense. Aquacult Int 26, 309–324.CrossRefGoogle Scholar
Li, Y, Ai, QH, Mai, KS, et al. (2012) Effects of the partial substitution of dietary fish meal by two types of soybean meals on the growth performance of juvenile Japanese seabass, Lateolabrax japonicus (Cuvier 1828): fish meal substitution on seabass growth. Aquacult Res 43, 458–466.CrossRefGoogle Scholar
Muzinic, LA, Thompson, KR, Morris, A, et al. (2004) Partial and total replacement of fish meal with soybean meal and brewer’s grains with yeast in practical diets for Australian red claw crayfish Cherax quadricarinatus . Aquaculture 230, 359–376.Google Scholar
Liu, XH, Ye, JD, Wang, K, et al. (2012) Partial replacement of fish meal with peanut meal in practical diets for the Pacific white shrimp, Litopenaeus vannamei: utilization of peanut meal in shrimp. Aquacult Res 43, 745–755.CrossRefGoogle Scholar
Thompson, KR, Muzinic, LA, Engler, LS, et al. (2005) Evaluation of practical diets containing different protein levels, with or without fish meal, for juvenile Australian red claw crayfish (Cherax quadricarinatus). Aquaculture 244, 241–249.CrossRefGoogle Scholar
Kalhoro, H, Zhou, J, Hua, Y, et al. (2018) Soy protein concentrate as a substitute for fish meal in diets for juvenile Acanthopagrus schlegelii: effects on growth, phosphorus discharge and digestive enzyme activity. Aquacult Res 49, 1896–1906.Google Scholar
Wang, XX, Yuan, Y, Li, CC, et al. (2020) Partial substitution of fish meal with soy protein concentrate in commercial diets for juvenile swimming crab, Portunus trituberculatus . Anim Feed Sci Technol 259, 114290.Google Scholar
Fuentes-Quesada, JP, Viana, MT, Rombenso, AN, et al. (2018) Enteritis induction by soybean meal in Totoaba macdonaldi diets: effects on growth performance, digestive capacity, immune response and distal intestine integrity. Aquaculture 495, 78–89.CrossRefGoogle Scholar
Krogdahl, Å, Penn, M, Thorsen, J, et al. (2010) Important antinutrients in plant feedstuffs for aquaculture: an update on recent findings regarding responses in salmonids. Aquacult Res 41, 333–344.CrossRefGoogle Scholar
Yaghoubi, M, Mozanzadeh, MT, Marammazi, JG, et al. (2016) Dietary replacement of fish meal by soy products (soybean meal and isolated soy protein) in silvery-black porgy juveniles (Sparidentex hasta). Aquaculture 464, 50–59.Google Scholar
Falcón-Hidalgo, B, Forrellat-Barrios, A, Farnés, OC, et al. (2011) Digestive enzymes of two freshwater fishes (Limia vittata and Gambusia punctata) with different dietary preferences at three developmental stages. Comp Biochem Physiol B: Biochem Mol Biol 158, 136–141.CrossRefGoogle ScholarPubMed
Furné, M, Hidalgo, MC, López, A, et al. (2005) Digestive enzyme activities in Adriatic sturgeon Acipenser naccarii and rainbow trout Oncorhynchus mykiss. A comparative study. Aquaculture 250, 391–398.CrossRefGoogle Scholar
Turan, A & Mahmood, A (2007) The profile of antioxidant systems and lipid peroxidation across the crypt-villus axis in rat intestine. Digestive Dis Sci 52, 1840–1844.CrossRefGoogle ScholarPubMed
Ray, GW, Liang, DZ, Yang, QH, et al. (2020) Effects of replacing fishmeal with dietary soybean protein concentrate (SPC) on growth, serum biochemical indices, and antioxidative functions for juvenile shrimp Litopenaeus vannamei . Aquaculture 516, 734630.Google Scholar
Yun, H, Shahkar, E, Hamidoghli, A, et al. (2017) Evaluation of dietary soybean meal as fish meal replacer for juvenile whiteleg shrimp, Litopenaeus vannamei reared in biofloc system. Int Aquat Res 9, 11–24.CrossRefGoogle Scholar
Xie, SW, Liu, YJ, Zeng, SL, et al. (2016) Partial replacement of fish-meal by soy protein concentrate and soybean meal based protein blend for juvenile Pacific white shrimp, Litopenaeus vannamei . Aquaculture 464, 296–302.CrossRefGoogle Scholar
Takahashi, K & Cohen, HJ (1986) Selenium-dependent glutathione peroxidase protein and activity: immunological investigations on cellular and plasma enzymes. Blood 68, 640–645.CrossRefGoogle ScholarPubMed
Iwama, GK (1998) Stress in fish. Ann NY Acad Sci 851, 304–310.Google Scholar
Meng, ZN, Chen, YC, Guan, XT, et al. (2010) Effect of Chinese herb compounds on activities of transaminase in-serum and antioxidase in erythrocyte of Cyprinus carpio L. J Northeast Agricult Univ 41, 75–80.Google Scholar
McGuckin, MA, Lindén, SK, Sutton, P, et al. (2011) Mucin dynamics and enteric pathogens. Nat Rev Microbiol 9, 265–278.CrossRefGoogle ScholarPubMed
Faggio, C, Torre, A, Pelle, E, et al. (2011) Cell volume regulation following hypotonic shock in hepatocytes isolated from Sparus aurata . Comp Biochem Physiol A: Mol Integr Physiol 158, 143–149.CrossRefGoogle ScholarPubMed
Dinglasan, RR, Devenport, M, Florens, L, et al. (2009) The Anopheles gambiae adult midgut peritrophic matrix proteome. Insect Biochem Mol Biol 39, 125–134.CrossRefGoogle ScholarPubMed
Wang, AR, Ran, C, Ringø, E, et al. (2018) Progress in fish gastrointestinal microbiota research. Rev Aquacult 10, 626–640.Google Scholar
Catalán, N, Villasante, A, Wacyk, J, et al. (2018) Fermented soybean meal increases lactic acid bacteria in gut microbiota of Atlantic Salmon (Salmo salar). Probiotics & antimicro. Probiotics Antimicrob Proteins 10, 566–576.CrossRefGoogle Scholar
Qiao, F, Liu, YK, Sun, YH, et al. (2017) Influence of different dietary carbohydrate sources on the growth and intestinal microbiota of Litopenaeus vannamei at low salinity. Aquacult Nutr 23, 444–452.CrossRefGoogle Scholar
Das, S, Ward, LR & Burke, C (2008) Prospects of using marine actinobacteria as probiotics in aquaculture. Appl Microbiol Biotechnol 81, 419–429.Google ScholarPubMed
Chen, JK, Shen, CR, Yeh, CH, et al. (2011) N-acetyl glucosamine obtained from chitin by chitin degrading factors in Chitinbacter tainanesis . Int J Mol Sci 12, 1187–1195.Google ScholarPubMed
Hou, DW, Huang, ZJ, Zeng, SZ, et al. (2018) Intestinal bacterial signatures of white feces syndrome in shrimp. Appl Microbiol Biotechnol 102, 3701–3709.Google ScholarPubMed
Shin, NR, Whon, TW & Bae, JW (2015) Proteobacteria: microbial signature of dysbiosis in gut microbiota. Trends Biotechnol 33, 496–503.Google ScholarPubMed
Yagoub, SO (2009) Isolation of Enterobacteriaceae and Pseudomonas spp. from raw fish sold in fish market in Khartoum state. Afr J Bacteriol Res 1, 085–088.Google Scholar
Sivakami, R, Premkishore, G & Chandran, MR (1996) Occurrence and distribution of potentially pathogenic Enterobacteriaceae in carps and pond water in Tamil Nadu, India. Aquacult Res 27, 375–378.CrossRefGoogle Scholar
Puppel, K, Kalińska, A, Kot, M, et al. (2020) The effect of Staphylococcus spp., Streptococcus spp. and Enterobacteriaceae on the development of whey protein levels and oxidative stress markers in cows with diagnosed mastitis. Animals 10, 1591.Google ScholarPubMed
Garg, RP, Yindeeyoungyeon, W, Gilis, A, et al. (2000) Evidence that Ralstonia eutropha (Alcaligenes eutrophus) contains a functional homologue of the Ralstonia solanacearum Phc cell density sensing system. Mol Microbiol 38, 359–367.CrossRefGoogle ScholarPubMed
Yamada, T, Kawasaki, T, Nagata, S, et al. (2007) New bacteriophages that infect the phytopathogen Ralstonia solanacearum . Microbiol 153, 2630–2639.CrossRefGoogle ScholarPubMed
Toledo, M, Gutiérrez, MC, Siles, JA, et al. (2017) Chemometric analysis and NIR spectroscopy to evaluate odorous impact during the composting of different raw materials. J Cleaner Prod 167,154–162.CrossRefGoogle Scholar
López-González, JA, Suárez-Estrella, F, Vargas-García, MC, et al. (2015) Dynamics of bacterial microbiota during lignocellulosic waste composting: studies upon its structure, functionality and biodiversity. Bioresour Technol 175, 406–416.Google ScholarPubMed