Abstract
We evaluated the impact of a combined vitamin E (vit E), a mixture of nucleotide (mixed-NT), Haematococcus pluvialis (H. pluvialis), arachidonic acid (AA), and yeast extract powder (YEP) supplementations on the relative mRNA expression of reproduction and antioxidant-related genes in red claw crayfish Cherax quadricarinatus using an orthogonal design (L16 45) plus control diet for 70 days feeding trial. Five factors with four levels: A, vit E 40, 160, 240, and 320 mg/kg diet; B, mixed-NT 2, 4, 6, and 8 g/kg diet; C, H. pluvialis 2, 4, 6, and 8 g/kg diet; D, AA 5, 10, 15, and 20 g/kg diet; E, YEP 2.5, 5, 10, and 15 g/kg diet were studied. The relative mRNA expression of reproduction-related genes (vitellogenin (vtg) and fatty acid-binding protein (fabp)), and antioxidant-related genes (heat shock protein 70 (hsp70), glutathione peroxidase (gpx), glutathione S-transferase (gst), mitochondrial manganese superoxide dismutase (mmnsod), and ferritin) in hemocyte, hepatopancreas, and ovary tissues were measured. There was a major depression in gene expression levels throughout the experimental diet at high vit E 320 mg/kg level with other factors. Expression of antioxidant enzyme genes significantly increased in treatments of T9, T10, T11, and T12, while significantly decreasing in treatment of T13 and other treatment groups with high vit E 320 mg/kg levels with the other factors. Gene expression of vtg and fabp demonstrated similar patterns to those of antioxidant genes. These results provide evidence that combined supplementations of vit E, mixed-NT, H. pluvialis, AA, and YEP with vit E 240 mg/kg, mixed-NT 8 g/kg, H. pluvialis 4 g/kg, AA 5 g/kg, and YEP 10 g/kg may present a novel strategy for improving reproduction performance and antioxidant activities in RC-crayfish, C. quadricarinatus by the positive impact on the molecular level of reproduction and antioxidant genes.






Similar content being viewed by others
Data availability
The data that support the findings of this study are available on request from the corresponding author. The data are not publicly available due to privacy or ethical constraints.
References
Ai C, Chen L (2001) Study of nutrition physiology of Eriochei sinensis. East China Normal University, Shanghai, China
Alam MS, Watanabe WO, Carroll PM, Rezek T (2009) Effects of dietary protein and lipid levels on growth performance and body composition of black sea bass Centropristis striata (Linnaeus 1758) during grow-out in a pilot-scale marine recirculating system. Aquac Res 40:442–449. https://doi.org/10.1111/j.1365-2109.2008.02113.x
Alexander TC, Han FX, Arslan Z, Tchounwou PB (2019) Toxicity of As in Crassostrea virginica (Gmelin, 1791) from the Northern Gulf of Mexico at the presence of Zn and its antioxidant defense mechanisms. Ecotoxicol Environ Saf 172:514–522. https://doi.org/10.1016/j.ecoenv.2019.02.009
Arcos FG, Ibarra AM, Racotta LS (2011) Vitellogenin in hemolymph predicts gonad maturity in adult female Litopenaeus (Penaeus) vannamei shrimp. Aquaculture 316:93–98. https://doi.org/10.1016/j.aquaculture.2011.02.045
Arshadi A, Yavari V, Oujifard A, Mousavi SM, Gisbert E, Mozanzadeh MT (2018) Dietary nucleotide mixture effects on reproductive and performance, ovary fatty acid profile and biochemical parameters of female Pacific shrimp Litopenaeus vannamei. Aquac Nutr 24:515–523. https://doi.org/10.1111/anu.12584
Asaikkutti A, Bhavan PS, Vimala K, Karthik M, Cheruparambath P (2016) Effect of different levels dietary vitamin C on growth performance, muscle composition, antioxidant and enzyme activity of freshwater prawn, Macrobrachium malcolmsonii. Aquac Rep 3:229–236. https://doi.org/10.1016/j.aqrep.2016.04.002
Ayiku S, Jianfei S, Tan B-p, Dong X-h, Liu H-y (2020) Effects of dietary yeast culture on shrimp growth, immune response, intestinal health and disease resistance against Vibrio harveyi. Fish Shellfish Immunol. https://doi.org/10.1016/j.fsi.2020.04.036
Blum J, Fridovich I (1985) Inactivation of glutathione peroxidase by superoxide radical. Arch Biochem Biophys 240:500–508. https://doi.org/10.1016/0003-9861(85)90056-6
Borda E, Martinez-Puig D, Cordoba X (2003) Well-balanced nucleotide supply makes sense. Feed Mix 11:24–26
Bownes M (1986) Expression of the genes coding for vitellogenin (yolk protein). Annu Rev Entomol 31:507–531
Browdy C (1992) A review of the reproductive biology of Penaeus species: perspectives on controlled shrimp maturation system for high quality nauplii production. Proceeding of the special session on shrimp farming:22–51
Burrells C, Williams P, Forno P (2001) Dietary nucleotides: a novel supplement in fish feeds: 1. Effects on resistance to disease in salmonids. Aquaculture 199:159–169. https://doi.org/10.1016/S0044-8486(01)00577-4
Casagrande D, Waib PH, Júnior AAJ (2018) Mechanisms of action and effects of the administration of Coenzyme Q10 on metabolic syndrome. J Nutr Intermed Metab 13:26–32. https://doi.org/10.1016/j.jnim.2018.08.002
Cavalli RO, Menschaert G, Lavens P, Sorgeloos P (2000) Maturation performance, offspring quality and lipidcomposition of Macrobrachium rosenbergii femalesfed increasing levels of dietary phospholipids. Aquac Int 8:41–58. https://doi.org/10.1023/A:1009220932268
Cheng Y, Li S, Wang G, Chen X, Lin Q, Xu J (2001) Changes in lipid class and fatty acid compositions in the ovaries and hepatopancreas of the mud crab Scylla serrata during the vitellogensis of the second ovarian maturation. Acta Oceanolog Sin 22:66–77
Chien Y-H, Shiau W-C (2005) The effects of dietary supplementation of algae and synthetic astaxanthin on body astaxanthin, survival, growth, and low dissolved oxygen stress resistance of kuruma prawn, Marsupenaeus japonicus Bate. J Exp Mar Biol Ecol 318:201–211. https://doi.org/10.1016/j.jembe.2004.12.016
Coman G, Arnold S, Barclay M, Smith D (2011) Effect of arachidonic acid supplementation on reproductive performance of tank-domesticated Penaeus monodon. Aquac Nutr 17:141–151. https://doi.org/10.1111/j.1365-2095.2009.00716.x
Cortés-Jacinto E, Villarreal-Colmenares H, Cruz-Suárez L, Civera-Cerecedo R, Nolasco-Soria H, Hernandez-Llamas A (2005) Effect of different dietary protein and lipid levels on growth and survival of juvenile Australian redclaw crayfish, Cherax quadricarinatus (von Martens). Aquac Nutr 11:283–291. https://doi.org/10.1111/j.1365-2095.2005.00353.x
Díaz-Jiménez L, Hernández-Vergara MP, Pérez-Rostro CI, Ortega-Clemente LA (2019) The effect of astaxanthin and β-carotene inclusion in diets for growth, reproduction and pigmentation of the peppermint shrimp Lysmata wurdemanni. Lat Am J Aquat Res 47:559–567 (10.3856)
Ding L-Y et al (2017) Cloning, tissue expression of the fatty acid-binding protein (Pt-FABP1) gene, and effects of dietary phospholipid levels on fabp and vitellogenin gene expression in the female swimming crab Portunus trituberculatus. Aquaculture 474:57–65. https://doi.org/10.1016/j.aquaculture.2017.03.029
Ding Z et al (2014) Molecular cloning, characterization and expression analysis of the fatty acid-binding protein (M n FABP), involved in dietary lipid sources response in oriental river prawn, M acrobrachium nipponense. Aquac Nutr 20:399–409. https://doi.org/10.1111/anu.12088
Du S, Hu C, Cai S, Shen Q, Zheng S (2006) Effect of different levels of dietary α-tocopherol on ovarian maturation and reproductive performance of broodstock Litopenaeus vannamei (Boone). J Shellfish Res 25:589–593. https://doi.org/10.2983/0730-8000(2006)25[589:EODLOD]2.0.CO;2
Duan Y, Zhang Y, Dong H, Zhang J (2016) Effect of desiccation on oxidative stress and antioxidant response of the black tiger shrimp Penaeus monodon. Fish Shellfish Immunol 58:10–17. https://doi.org/10.1016/j.fsi.2016.09.004
Fatima H, Ayub Z, Ali SA, Siddiqui G (2013) Biochemical composition of the hemolymph, hepatopancreas, ovary, and muscle during ovarian maturation in the penaeid shrimps Fenneropenaeus merguiensis and F. penicillatus (Crustacea: Decapoda). Turk J Zool 37:334–347
Ghanawi J, Saoud IP (2012) Molting, reproductive biology, and hatchery management of redclaw crayfish Cherax quadricarinatus (von Martens 1868). Aquaculture 358:183–195. https://doi.org/10.1016/j.aquaculture.2012.06.019
Glencross BD, Booth M, Allan GL (2007) A feed is only as good as its ingredients–a review of ingredient evaluation strategies for aquaculture feeds. Aquac Nutr 13:17–34. https://doi.org/10.1111/j.1365-2095.2007.00450.x
Guo X et al (2019) Dietary nucleotides can directly stimulate the immunity of zebrafish independent of the intestinal microbiota. Fish Shellfish Immunol 86:1064–1071. https://doi.org/10.1016/j.fsi.2018.12.058
Hayes JD, Strange RC (1995) Invited commentary potential contribution of the glutathione S-transferase supergene family to resistance to oxidative stress. Free Radic Res 22:193–207. https://doi.org/10.3109/10715769509147539
Hung SS, Cho C, Slinger SJ (1981) Effect of oxidized fish oil, DL-α-tocopheryl acetate and ethoxyquin supplementation on the vitamin E nutrition of rainbow trout (Salmo gairdneri) fed practical diets. Nutr J 111:648–657. https://doi.org/10.1093/jn/111.4.648
Izquierdo M, Fernandez-Palacios H, Tacon A (2001) Effect of broodstock nutrition on reproductive performance of fish. Aquaculture 197:25–42. https://doi.org/10.1016/S0044-8486(01)00581-6
Jacob RA (1995) The Integrated Antioxidant System Nutrition Research 15:755–766
Jin M, Xiong J, Zhou Q-C, Yuan Y, Wang X-X, Sun P (2018) Dietary yeast hydrolysate and brewer’s yeast supplementation could enhance growth performance, innate immunity capacity and ammonia nitrogen stress resistance ability of Pacific white shrimp (Litopenaeus vannamei). Fish Shellfish Immunol 82:121–129. https://doi.org/10.1016/j.fsi.2018.08.020
Johansson MW, Holmblad T, Thornqvist P-O, Cammarata M, Parrinello N, Soderhall K (1999) A cell-surface superoxide dismutase is a binding protein for peroxinectin, a cell-adhesive peroxidase in crayfish. J Cell Sci 112:917–925
Kaewsrithong J, Ohshima T, Ushio H, Nagasaka R, Maita M, Sawada M (2001) Effects of an excess dose of dietary α-tocopherol on hydroperoxide accumulation and erythrocyte osmotic fragility of sweet smelt Plecoglossus altivelis (Temminck et Schlegel). Aquac Res 32:191–198. https://doi.org/10.1046/j.1355-557x.2001.00056.x
Lan WG, Wong MK, Chen N, Sin YM (1995) Effect of combined copper, zinc, chromium and selenium by orthogonal array design on alkaline phosphatase activity in liver of the red sea bream, Chrysophrys major. Aquaculture 131:219–230. https://doi.org/10.1016/0044-8486(94)00326-J
Li M, Dong W-j, Xu J-y, Wang Y-f (2007) The effect of vitamin E in diet on spawning of red swamp crayfish Procambarus clarkii Girard. JFSC 31:65–68
Li W-W, Jin X-K, He L, Gong Y-N, Jiang H, Wang Q (2011a) Molecular cloning and tissue expression of the fatty acid-binding protein (Es-FABP9) gene in the reproduction seasons of Chinese mitten crab, Eriocheir sinensis. Mol Biol Rep 38:5169–5177. https://doi.org/10.1007/s11033-010-0666-1
Li X, Li Z, Liu J, De Silva SS (2011b) Advances in precocity research of the Chinese mitten crab Eriocheir sinensis. Aquac Int 19:251–267. https://doi.org/10.1007/s10499-010-9400-1
Li Y, Fan B, Huang Y, Wu D, Zhang M, Zhao Y (2018) Effects of dietary vitamin E on reproductive performance and antioxidant capacity of Macrobrachium nipponense female shrimp. Aquac Nutr 24:1698–1708. https://doi.org/10.1111/anu.12804
Liu X, Wang B, Li Y, Wang L, Liu J (2018) Effects of dietary botanical and synthetic astaxanthin on E/Z and R/S isomer composition, growth performance, and antioxidant capacity of white shrimp, Litopenaeus vannamei, in the nursery phase [For this article an Erratum has been published]. Invertebr Surviv J 15:131–140 (10.25431/1824-)
Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2− ΔΔCT method. Methods 25:402–408
Ma N, Long X, Liu J, Chang G, Deng D, Cheng Y, Wu X (2019) Defatted Haematococcus pluvialis meal can enhance the coloration of adult Chinese mitten crab Eriocheir sinensis. Aquaculture 510:371–379. https://doi.org/10.1016/j.aquaculture.2019.05.063
Maulana F, Arfah H, Istifarini M, Setiawati M (2017) Supplementation of astaxanthin and vitamin E in feed on the development of gonads white shrimp broodstock Litopenaeus vannamei Boone 1931. Jurnal Akuakultur Indonesia 16:124–135. https://doi.org/10.19027/jai.16.2.124-135
Meusy J, Charniaux-Cotton H (1984) Endocrine control of vitellogenesis in Malacostraca crustaceans. Adv Invertebr Reprod 3:231–242
Mourente G, Dıaz-Salvago E, Bell JG, Tocher DR (2002) Increased activities of hepatic antioxidant defence enzymes in juvenile gilthead sea bream (Sparus aurata L.) fed dietary oxidised oil: attenuation by dietary vitamin E. Aquaculture 214:343–361. https://doi.org/10.1016/S0044-8486(02)00064-9
Naessens E et al (1997) Maturation performance of Penaeus vannamei co-fed Artemia biomass preparations. Aquaculture 155:87–101. https://doi.org/10.1016/S0044-8486(97)00111-7
Niu J, Tian LX, Liu YJ, Yang HJ, Ye CX, Gao W, Mai KS (2009) Effect of dietary astaxanthin on growth, survival, and stress tolerance of postlarval shrimp, Litopenaeus vannamei. J World Aquac Soc 40:795–802. https://doi.org/10.1111/j.1749-7345.2009.00300.x
Normant M, Chrobak M, Szaniawska A (2002) Energy value and chemical composition (CHN) of the Chinese mitten crab Eriocheir sinensis (Decapoda: Grapsidae) from the Baltic Sea. Thermochim Acta 394:233–237. https://doi.org/10.1016/S0040-6031(02)00259-9
NRC (2011) Nutrient requirements of fish and shrimp. National academies press,
Orino K, Lehman L, Tsujl Y, Ayaki H, Torti SV, Torti FM (2001) Ferritin and the response to oxidative stress. Biochem J 357:241–247. https://doi.org/10.1042/bj3570241
Paibulkichakul C, Piyatiratitivorakul S, Sorgeloos P, Menasveta P (2008) Improved maturation of pond-reared, black tiger shrimp (Penaeus monodon) using fish oil and astaxanthin feed supplements. Aquaculture 282:83–89. https://doi.org/10.1016/j.aquaculture.2008.06.006
Plantivaux A et al (2004) Molecular characterization of two CuZn-superoxide dismutases in a sea anemone. Free Radical Biol Med 37:1170–1181. https://doi.org/10.1016/j.freeradbiomed.2004.06.043
Ravid T, Tietz A, Khayat M, Boehm E, Michelis R, Lubzens E (1999) Lipid accumulation in the ovaries of a marine shrimp Penaeus semisulcatus (De Haan). J Exp Biol 202:1819–1829
Raviv S, Parnes S, Segall C, Davis C, Sagi A (2006) Complete sequence of Litopenaeus vannamei (Crustacea: Decapoda) vitellogenin cDNA and its expression in endocrinologically induced sub-adult females. Gen Comp Endocrinol 145:39–50. https://doi.org/10.1016/j.ygcen.2005.06.009
Rimbach G, Moehring J, Huebbe P, Lodge JK (2010) Gene-regulatory activity of α-tocopherol. Molecules 15:1746–1761. https://doi.org/10.3390/molecules15031746
Ringø E et al (2016) Effect of dietary components on the gut microbiota of aquatic animals. A never-ending story? Aquac Nutr 22:219–282. https://doi.org/10.1111/anu.12346
Rodriguez J, Boulo V, Mialhe E, Bachere E (1995) Characterisation of shrimp haemocytes and plasma components by monoclonal antibodies. J Cell Sci 108:1043–1050
Ross PJ, Ross PJ (1988) Taguchi techniques for quality engineering: loss function, orthogonal experiments, parameter and tolerance design. vol TS156 R12. McGraw-Hill New York,
Rota C, Rimbach G, Minihane A-M, Stoecklin E, Barella L (2005) Dietary vitamin E modulates differential gene expression in the rat hippocampus: potential implications for its neuroprotective properties. Nutr Neurosci 8:21–29. https://doi.org/10.1080/10284150400027123
Roy R (1990) A Primer on Taguchi Method; Van Noshtrand Reinhold Int Co. Ltd: New York, NY, USA
Schlotz N, Sørensen JG, Martin-Creuzburg D (2012) The potential of dietary polyunsaturated fatty acids to modulate eicosanoid synthesis and reproduction in Daphnia magna: a gene expression approach. Comp Biochem Physiol A 162:449–454. https://doi.org/10.1016/j.cbpa.2012.05.004
Shehata AI, Wang T, Jibril Habib Y, Wang J, Fayed WM, Zhang Z (2020) The combined effect of vitamin E, arachidonic acid, Haemtococcus pluvialis, nucleotides and yeast extract on growth and ovarian development of crayfish (Cherax quadricarinatus) by the orthogonal array design. Aquac Nutr n/a. https://doi.org/10.1111/anu.13142
Sies H (1993) Strategies of antioxidant defense. Eur J Biochem 215:213–219. https://doi.org/10.1111/j.1432-1033.1993.tb18025.x
Spaziani E, Hinsch G, Edwards S (1993) Changes in prostaglandin E 2 and F 2α during vitellogenesis in the Florida crayfish Procambarus paeninsulanus. J Comp Physiol B 163:541–545. https://doi.org/10.1007/BF00302112
Spaziani EP, Hinsch GW, Edwards SC (1995) The effect of prostaglandin E2 and prostaglandin F2α on ovarian tissue in the Florida crayfish Procambarus paeninsulanus. Prostaglandins 50:189–200. https://doi.org/10.1016/0090-6980(95)00124-7
Storch J, Thumser AE (2000) The fatty acid transport function of fatty acid-binding proteins. Biochim Biophys Acta Mol Cell Biol Lipids 1486:28–44. https://doi.org/10.1016/S1388-1981(00)00046-9
Sumpownon C et al (2015) Variation of prostaglandin E2 concentrations in ovaries and its effects on ovarian maturation and oocyte proliferation in the giant fresh water prawn, Macrobrachium rosenbergii. Gen Comp Endocrinol 223:129–138. https://doi.org/10.1016/j.ygcen.2015.04.019
Suo Y, Li E, Li T, Jia Y, Qin JG, Gu Z, Chen L (2017) Response of gut health and microbiota to sulfide exposure in Pacific white shrimp Litopenaeus vannamei. Fish Shellfish Immunol 63:87–96. https://doi.org/10.1016/j.fsi.2017.02.008
Tahara D, Yano I (2004) Maturation-related variations in prostaglandin and fatty acid content of ovary in the kuruma prawn (Marsupenaeus japonicus). Comp Biochem Physiol A 137:631–637. https://doi.org/10.1016/j.cbpb.2003.12.005
Tizkar B et al (2016) Effects of dietary astaxanthin and β-carotene on gonadosomatic and hepatosomatic indices, gonad and liver composition in goldfish Carassius auratus (Linnaeus, 1758) broodstocks. Lat Am J Aquat Res 44:363–370. https://doi.org/10.3856/vol44-issue2-fulltext-17
Trenzado CE, Morales AE, Palma JM, de la Higuera M (2009) Blood antioxidant defenses and hematological adjustments in crowded/uncrowded rainbow trout (Oncorhynchus mykiss) fed on diets with different levels of antioxidant vitamins and HUFA. Comp Biochem Physiol C Pharmacol Toxicol Endocrinol 149:440–447. https://doi.org/10.1016/j.cbpc.2008.10.105
Tukey JW (1953) Section of mathematics and engineering: some selected quick and easy methods of statistical analysis. Trans N Y Acad Sci 16:88–97. https://doi.org/10.1111/j.2164-0947.1953.tb01326.x
Wade NM, Gabaudan J, Glencross BD (2017) A review of carotenoid utilisation and function in crustacean aquaculture. Rev Aquac 9:141–156. https://doi.org/10.1111/raq.12109
Wang K, Zhou Z, Geng Y (2007) Study on the pathology of vitamin E deficiency in common carp (Cyprinus carpio). Acta Hydrobiol Sin 31:359
Wang L-U, Chen J-C (2005) The immune response of white shrimp Litopenaeus vannamei and its susceptibility to Vibrio alginolyticus at different salinity levels. Fish Shellfish Immunol 18:269–278. https://doi.org/10.1016/j.fsi.2004.07.008
Wang L, Zuo D, Lv W, Li J, Wang Q, Zhao Y (2013) Effects of dietary soybean lecithin on gonadal development and vitellogenin mRNA expression in the female redclaw crayfish Cherax quadricarinatus (von M artens) at first maturation. Aquac Res 44:1167–1176. https://doi.org/10.1111/j.1365-2109.2012.03128.x
Williams TD (1994) Intraspecific variation in egg size and egg composition in birds: effects on offspring fitness. Biol Rev Camb Philos Soc 69:35–59. https://doi.org/10.1111/j.1469-185x.1994.tb01485.x
Wimuttisuk W, Tobwor P, Deenarn P, Danwisetkanjana K, Pinkaew D, Kirtikara K, Vichai V (2013) Insights into the prostanoid pathway in the ovary development of the penaeid shrimp Penaeus monodon. PLoS ONE 8:e76934. https://doi.org/10.1371/journal.pone.0076934
Wu X, Zhao L, Long X, Liu J, Su F, Cheng Y (2017) Effects of dietary supplementation of Haematococcus pluvialis powder on gonadal development, coloration and antioxidant capacity of adult male Chinese mitten crab (Eriocheir sinensis). Aquac Res 48:5214–5223. https://doi.org/10.1111/are.13333
Xu H et al (2017) Arachidonic acid in diets for early maturation stages enhances the final reproductive performances of Pacific white shrimp (Litopenaeus vannamei). Aquaculture 479:556–563. https://doi.org/10.1016/j.aquaculture.2017.06.037
Yan L-l, Zhang G-f, Liu Q-g (2009) Optimization of culturing the freshwater pearl mussels, Hyriopsis cumingii with filter feeding Chinese carps (bighead carp and silver carp) by orthogonal array design. Aquaculture 292:60–66. https://doi.org/10.1016/j.aquaculture.2009.03.037
Yang W, Xiang F, Liang L, Yang Z (2010) Toxicity of ammonia and its effects on oxidative stress mechanisms of juvenile crucian carp (Carassius auratus). J Freshw Ecol 25:297–302. https://doi.org/10.1080/02705060.2010.9665080
Yousefi M, Paktinat M, Mahmoudi N, Pérez-Jiménez A, Hoseini SM (2016) Serum biochemical and non-specific immune responses of rainbow trout (Oncorhynchus mykiss) to dietary nucleotide and chronic stress. Fish Physiol Biochem 42:1417–1425. https://doi.org/10.1007/s10695-016-0229-z
Zapata V, Greco LL, Medesani D, Rodrıguez E (2003) Ovarian growth in the crab Chasmagnathus granulata induced by hormones and neuroregulators throughout the year. In vivo and in vitro studies. Aquaculture 224:339–352. https://doi.org/10.1016/S0044-8486(03)00226-6
Zhang P et al (2019a) Effects of inosine 5′-monophosphate supplementation in high fishmeal and high soybean diets on growth, immune-related gene expression in gibel carp (Carassius auratus gibelio var. CAS III), and its challenge against Aeromonas hydrophila infection. Fish Shellfish Immunol 86:913–921. https://doi.org/10.1016/j.fsi.2018.12.016
Zhang R, Jiang Y, Zhou L, Chen Y, Wen C, Liu W, Zhou Y (2019b) Effects of dietary yeast extract supplementation on growth, body composition, non-specific immunity, and antioxidant status of Chinese mitten crab (Eriocheir sinensis). Fish Shellfish Immunol 86:1019–1025. https://doi.org/10.1016/j.fsi.2018.12.052
Funding
This work was supported by the Startup Fund for Dr. Ziping Zhang (No. 104–61201403610) and Special Fund for Adjusting Marine and Fisheries Structure of Fujian Province (2019MDS-YT006).
Author information
Authors and Affiliations
Contributions
Akram Ismael Shehata: conceptualization, methodology, validation, writing—original draft. Mayada Alhoshy: writing. Tao Wang: conceptualization, methodology, validation. Jianfeng Wang: helped supervise the project, provided crayfish and equipment. Ruoxuan Wang: collecting samples. Mahmoud A.O. Dawood: Mohamed A.A. Zaki: formal analysis, writing—review and editing. Yilei Wang: the original idea—review and editing. Ziping Zhang: original idea, writing—review and editing, Supervision. All authors contributed to preparing the final manuscript.
Corresponding authors
Ethics declarations
Conflict of interest
The authors declare no competing interests.
Ethics approval
All of the study design and animal experiments were conducted in accordance with the guidelines of Fujian Agriculture and Forestry University’s Animal Care and Use Committee.
Additional information
Handling Editor: Gavin Burnell
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.
Rights and permissions
About this article
Cite this article
Shehata, A.I., Alhoshy, M., Wang, T. et al. Expression of reproduction and antioxidant-related genes in crayfish Cherax quadricarinatus fed with dietary feed additives. Aquacult Int 30, 699–720 (2022). https://doi.org/10.1007/s10499-021-00816-0
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10499-021-00816-0