Abstract
Copper and vitamin C are micronutrients needed for the living organism’s functions. Vitamin C has a great effect on the immune system of fish. The present study aimed to evaluate the effects of dietary copper nanoparticles (Cu-NPs) and vitamin C (VC) supplementations on rainbow trout (Oncorhynchus mykiss) juveniles. So, 216 rainbow trout juveniles were randomly assigned to six groups with trial diets supplemented with Cu-NPs and VC including 0/0 (T1, control diet), 0/250 (T2), 0/500 (T3), 2/250 (T4), 2/500 (T5), and 2/0 (T6) mg Cu-NPs/VC per kg diet. After the feeding trial for 60 days, the fish were challenged with Yersinia ruckeri, and the survival rate was calculated for 15 days. Based on the data analysis, weight gain (WG), specific growth rate (SGR), protein efficiency ratio (PER), lysozyme, alternative complement activity (ACH50), hematocrit (Hct), hemoglobin (Hb), and mean corpuscular volume (MCV) were significantly (p < 0.05) increased in the fish fed on T4 and T5 diets compared with the control group. Catalase (CAT), superoxide dismutase (SOD), and glutathione peroxidase (GPX) were significantly (p < 0.05) decreased in the fish fed with diets contain Cu-NPs and VC (T4 and T5). The expressions of TNF-α, IL-1ß, IL-10, SOD, CAT, and GPX genes were significantly (p < 0.05) decreased in the fish fed on T3, T4, and T5 diets versus the control. In addition, the dietary Cu-NPs and VC supplementations significantly enhanced resistance against pathogens and led to the control of infection in rainbow trout. In conclusion, Cu-NPs and VC administered as feed additives at 2/250–500 mg/kg elevated the growth performance, antioxidant capacity, and health of rainbow trout.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data availability
The datasets generated during and/or analyzed during the current study are available from the corresponding author on reasonable request.
Code availability
Not applicable.
References
Abdelazim AM, Saadeldin IM, Swelum AA, Afifi M, Alkaladi A (2018) Oxidative stress in the muscles of the fish nile tilapia caused by zinc oxide nanoparticles and its modulation by vitamins C and E. Oxid Med Cell Longev 12–19. https://doi.org/10.1155/2018/6926712
Adel A, Khara H (2016) The effects of different dietary vitamin C and iron levels on the growth, hematological and immunological parameters of rainbow trout Oncorhynchus mykiss fingerlings. Iranian J Fish Sci 15:886–897
Afifi M, Saddick S, Abu Zinada OA (2013) Toxicity of silver nanoparticles on the brain of Oreochromis niloticus and Tilapia zillii. Saudi J Biol Sci 26:742–749. https://doi.org/10.1016/j.sjbs.2016.06.008
Afshari A, Sourinejad I, Gharaei A, Johari SA, Ghasemi Z (2021). The effects of diet supplementation with inorganic and nanoparticulate iron and copper on growth performance, blood biochemical parameters, antioxidant response and immune function of snow trout Schizothorax zarudnyi (Nikolskii, 1897). Aquacult 539:736638, https://doi.org/10.1016/j.aquaculture.2021.736638
Aghamirkarimi S, Mashinchian Moradi A, Sharifpour I, Jamili S, Ghavam Mostafavi P (2017) Sublethal effects of copper nanoparticles on the histology of gill, liver and kidney of the Caspian roach, Rutilus rutilus caspicus. Global J Environ Sci Manage 3:323–332. https://doi.org/10.22034/gjesm.2017.03.03.009
Ai QH, Mai KS, Tan BP et al (2006) Effects of dietary vitamin C on survival, growth, and immunity of large yellow croaker, Pseudosciaena crocea. Aquacul 261:327–336. https://doi.org/10.1016/j.aquaculture.2006.07.027
Akbıyık T, Sönmezoğlu İ, Güçlü K, Tor İ, Apak R (2012) Protection of ascorbic acid from copper (II)-catalyzed oxidative degradation in the presence of fruit acids: citric, oxalic, tartaric, malic, malonic, and fumaric acids. Int J Food Prop 15:398–411
Al-Armoudi MM, El-Nakkadi AMN, El-Nounan BM (1992) Evaluation of optimum dietary requirement of vitamin C for the growth of Oreochromis spilurus fingerlings in water from the Red Sea. Aquacul 105:165–173. https://doi.org/10.1016/0044-8486(92)90128-8
Astete CE, Dolliver D, Whaley M, Khachatryan L, Sabliov CM (2011) Antioxidant poly(lactic-co-glycolic) acid nanoparticles made with α-tocopherol–ascorbic acid surfactant. ACS Nano 5:9313–9325. https://doi.org/10.1021/nn102845t
Babior BM (1997) Superoxide: a two-edged sword. Braz J Med Biol Res 30:141–155. https://doi.org/10.1590/S0100-879X1997000200001
Behera T, Swain P, Rangacharulu PV, Samanta M (2013) Nano-Fe as feed additive improves the hematological and immunological parameters of fish, Labeo rohita H. Appl Nanosci 4:687–694. https://doi.org/10.1007/s13204-013-0251-8
Biller JD, Takahashi LS (2018) Oxidative stress and fish immune system: phagocytosis and leukocyte respiratory burst activity. An Acad Bras Cienc 90:3403–3414. https://doi.org/10.1590/0001-3765201820170730
Birben E, Sahiner UM, Sackesen C, Erzurum S, Kalayci O (2012) Oxidative stress and antioxidant defense. World Allergy Organization J. 9–19
Chahardeh Baladehi E, Hedayati SAA, Kolangimiandare H, Bagheri T (2017) The hematological improvement of rainbow trout (Oncorhynchus mykiss) during dietary supplementation with vitamin C after exposure to zinc nano-particles. Iranian J Fish Sci 16:162–169
Chen R, Lochmann R, Goodwin A (2003) Alternative complement activity and resistance to heat stress in golden shiners (Notemigonus crysoleucas) are increased by dietary vitamin C levels in excess of requirements for prevention of deficiency signs. J Nutr 133:2281–2286. https://doi.org/10.1093/jn/133.7.2281
Chen YJ, Yuan RM, Liu YJ et al (2015) Dietary vitamin C requirement and its effects on tissue antioxidant capacity of juvenile largemouth bass, Micropterus salmoides. Aquacul 435:431–436. https://doi.org/10.1016/j.aquaculture.2014.10.013
Clauss TM, Dove AD, Arnold JE (2008) Hematologic disorders of fish. Vet Clin North Am Exot Anim Pract 11:445–462. https://doi.org/10.1016/j.cvex.2008.03.007
Combs GF (2008) The vitamins, fundamental aspects in nutrition and health, 3rdedn. Elsevier Academic Press, Burlington. https://doi.org/10.1080/07315724.2000.10718917
Davis DA, Lawrence AL, Gatlin DM III (1993) Evaluation of the dietary zinc requirement of Penaeus vannamei and effects of phytic acid on zinc and phosphorus bioavailability. J World Aquac Soc 24:40–47. https://doi.org/10.1111/j.1749-7345.1993.tb00148.x
Dawood MAO, Eweedah NM, Moustafa EM et al (2020) Copper nanoparticles mitigate the growth, immunity, and oxidation resistance in common carp (Cyprinus carpio). Biol Trace Elem Res 198:283–292. https://doi.org/10.1007/s12011-020-02068-0
Dawood MAO, Koshio S (2016) Vitamin C supplementation to optimize growth, health and stress resistance in aquatic animals. Rev Aquacult 10:334–350. https://doi.org/10.1111/raq.12163
Dawood MAO, Koshio S, Ishikawa M, Yokoyama S (2016) Immune responses and stress resistance in red sea bream, Pagrus major, after oral administration of heat-killed Lactobacillus plantarum and vitamin C, Fish & Shellfish Immunology, 54:266-275, https://doi.org/10.1016/j.fsi.2016.04.017
Dekani L, Johari SA, Salarijoo H (2018) Comparative toxicity of organic, inorganic and nanoparticulate zinc following dietary exposure to common carp (Cyprinus carpio). Sci Total Environ 656:1191–1198. https://doi.org/10.1016/j.scitotenv.2018.11.474
Di Bella LM, Alampi R, Biundo F, Toscano G, Felice MR (2017) Copper chelation and interleukin-6 proinflammatory cytokine effects on expression of different proteins involved in iron metabolism in HepG2 cell line. BMC Biochem 18:1–11. https://doi.org/10.1186/s12858-017-0076-2
El Basuini MF, El-Hais AM, Dawood MA et al (2016) Effect of different levels of dietary copper nanoparticles and copper sulfate on growth performance, blood biochemical profiles, antioxidant status and immune response of red sea bream (Pagrus major). Aquacul 455:32–40. https://doi.org/10.1016/j.aquaculture.2016.01.007
Ellis AE (1990) Lysozyme assays. Tech. Fish Immunol 1:101–103.
Eo J, Lee K (2008) Effect of dietary ascorbic acid on growth and nonspecific immune responses of tiger puffer, Takifugu rubripes. Fish Shellfish Immun 25:611–616. https://doi.org/10.1016/j.fsi.2008.08.009
Faggio C, Fedele G, Arfuso F, Panzera M, Fazio F (2014) Haematological and biochemical response of Mugil cephalus after acclimation to captivity. Cah Biol Mar 55:31–36.
Fang KM, Cheng FC, Huang YL et al (2013) Trace element, antioxidant activity, and lipid peroxidation levels in brain cortex of gerbils after cerebral ischemic injury. Biol Trace Elem Res 152:66–74. https://doi.org/10.1007/s12011-012-9596-1
Faramarzi M (2012) Effect of dietary vitamin C on growth and feeding parameters, carcass composition and survival rate of Common Carp (Cyprinus carpio). Glob Vet 8:507–510
Fracalossi DM, Allen ME, Yuyama LK, Oftedal OT (2001) Ascorbic acid biosynthesis in amazonian fishes. Aquacul 192:321–332. https://doi.org/10.1016/S0044-8486(00)00455-5
Gatlin DM, Wilson RP (1986) Dietary copper requirement of fingerling channel catfish. Aquacul 54:277–285. https://doi.org/10.1016/0044-8486(86)90272-3
Gharaei A, Ghafari M, Keyvanshokooh S, Akrami R (2010) Changes in metabolic enzyme, cortisol and glucose of Beluga (Huso huso) exposed to dietary methylmercury. Fish Physiol Biochem 37:485–493. https://doi.org/10.1007/s10695-010-9450-3
Gharaei A, Ghaffari M, Keyvanshokooh S, Akrami R (2011) Changes in metabolic enzymes, cortisol and glucose concentrations of Beluga (Huso huso) exposed to dietary methylmercury. Fish Physiol Biochem 37:485–493. https://doi.org/10.1007/s10695-010-9450-3
Gharaei A, Khajeh M, khosravanizadeh A, Mirdar Harijani J, Fadaei R, (2020a) Fluctuation of biochemical, immunological and antioxidant biomarkers in blood of beluga (Huso huso) under effect of dietary ZnO and Chitosan-ZnO NPs. Fish Physiol Biochem 46:547–561. https://doi.org/10.1007/s10695-019-00726-2
Gharaei A, Shafiei M, Mirdar Harijani J, Hassanein P, Arshadi A (2020b) Immune responses and haematological parameters changes of rainbow trout (Oncorhynchus mykiss) under effects of dietary administration of sumac (Rhus coriaria). J Agr Sci Tech 22:173–186. https://doi.org/10.1016/j.fsi.2017.08.022
Gonzales-Eguia A, Fu C, Lu F, Lien T (2009) Effects of nanocopper on copper availability and nutrients digestibility, growth performance and serum traits of piglets. Livest Sci 126:122–129. https://doi.org/10.1016/j.livsci.2009.06.009
Grosso G, Bei R, Mistretta A et al (2013) Effects of vitamin C on health: a review of evidence. Front Biosci Landmark 18:1017–1029. https://doi.org/10.2741/4160
Harsij M, Gholipour Kanani H, Adineh H (2020) Effects of antioxidant supplementation (nano‑selenium, vitamin C and E) on growth performance, blood biochemistry, immune status and body composition of rainbow trout (Oncorhynchus mykiss) under sub-lethal ammonia exposure. Aquacult 521. https://doi.org/10.1016/j.aquaculture.2020.734942
Haver JE, Hardy RW (2002) Fish nutrition 3 edition. Academic Press, 260–308.
Hoseini SM, Hedayati A, Mirghaed AT, Ghelichpour M (2016) Toxic effects of copper sulfate and copper nanoparticles on minerals, enzymes, thyroid hormones and protein fractions of plasma and histopathology in common carp Cyprinus carpio. Exp Toxicol Pathol 68:493–503. https://doi.org/10.1016/j.aquatox.2012.02.032
Hoseini SM, Mirghaed AT, Iri Y, Ghelichpour M (2018) Effects of dietary cineole administration on growth performance, hematological and biochemical parameters of rainbow trout (Oncorhynchus mykiss). Aquacult 495:766–772. https://doi.org/10.1016/j.aquaculture.2018.06.073
Hoseini SM, Yousefi M, Taheri Mirghaed A et al (2020) Effects of rearing density and dietary tryptophan supplementation on intestinal immune and antioxidant responses in rainbow trout (Oncorhynchus mykiss). Aquacul 528:735537. https://doi.org/10.1016/j.aquaculture.2020.735537
Hu Y, Huang Y, Wen H (2013) Effect of vitamin C on growth, immunity and anti-ammonia-nitrate stress ability in juvenile black carp (Mylopharyngodon piceusasiaticus). Shuichan Xuebao 37:565–573 (In Chinese, with English abstract)
Izquierdo MS, Ghrab W, Roo J et al (2016) Organic, inorganic and nanoparticles of Se, Zn and Mn in early weaning diets for gilthead seabream, Sparus aurata; Linnaeus, 1758. Aquac Res 48:2852–2867. https://doi.org/10.1111/are.13119
Jafarinejad R, Gharaei A, Mirdar Harijani J (2020) Dietary ginger improve growth performance, blood parameters, antioxidant capacity and gene expression in Cyprinus carpio. Iranian J Fish Sci 19:1237–1252. https://doi.org/10.22092/ijfs.2018.119876
Jang IS, Ko YH, Moon YS, Sohn SH (2014) Effects of vitamin C or E on the pro-inflammatory cytokines, heat shock protein 70 and antioxidant status in broiler chicks under summer conditions. Asian-australas. J Anim Sci 27749. https://doi.org/10.5713/ajas.2013.13852
Jankowski J, Otowski K, Kozłowski K et al (2020) Effect of different levels of copper nanoparticles and copper sulfate on morphometric indices, antioxidant status and mineral digestibility in the small intestine of turkeys. Ann Anim Sci. https://doi.org/10.2478/aoas-2020-0013
Kaya H, Aydın F, Gürkan M et al (2016) A comparative toxicity study between small and large size zinc oxide nanoparticles in tilapia (Oreochromis niloticus): organ pathologies, osmoregulatory responses and immunological parameters. Chemosphere 144:571–582. https://doi.org/10.1016/j.chemosphere.2015.09.024
Kim JH, Kang JC (2015) Influence of dietary ascorbic acid on the immune responses of juvenile Korean rock fish Sebastes schlegelii. J Aquat Anim Health 27:178–184. https://doi.org/10.1080/08997659.2015.1050128
Leal E, Zarza C, Tafalla C (2017) Effect of vitamin C on innate immune responses of rainbow trout (Oncorhynchus mykiss) leukocytes. Fish Shellfish Immunol 67:179–188. https://doi.org/10.1016/j.fsi.2017.06.021
Lee MH, Shiau SY (2002) Dietary copper requirement of juvenile grass shrimp, Penaeus monodon, and effects on non-specific immune responses. Fish Shellfish Immun 13:259–270. https://doi.org/10.1006/fsim.2001.0401
Li ZH, Velisek J, Zlabek V et al (2010) Hepatic antioxidant status and hematological parameters in rainbow trout, Oncorhynchus mykiss, after chronic exposure to carbamazepine. Chem Biol Interact 183:98–104. https://doi.org/10.1016/j.cbi.2009.09.009
Liang XP, Li Y, Hou YM, Qiu H, Zhou QC (2017) Effect of dietary vitamin C on the growth performance, antioxidant ability and innate immunity of juvenile yellow catfish (Pelteobagrus fulvidraco Richardson). Aquacal Res 48:149–160. https://doi.org/10.1111/are.12869
Lin MF, Shiau SY (2005) Dietary L-ascorbic acid affects growth, nonspecific immune responses and disease resistance in juvenile grouper, Epinephelus malabaricus. Aquacul 244:215–221. https://doi.org/10.1016/j.aquaculture.2004.10.026
Lin YH, Shie YY, Shiau SY (2008) Dietary copper requirements of juvenile grouper, Epinephelus malabaricus. Aquacul 274:161–165. https://doi.org/10.1016/j.aquaculture.2010.10.004Get
Liu Y, Chi L, Feng L et al (2011) Effects of graded levels of dietary vitamin C on the growth, digestive capacity and intestinal microflora of juvenile Jian carp (Cyprinus carpio). Aquac Res 42:534–548. https://doi.org/10.1111/j.1365-2109.2010.02649.x
Lorentzen M, Maage A, Julshamn K (1998) Supplementing copper to a fish meal based diet fed to Atlantic salmon parr affects liver copper and selenium concentrations. Aquac Nutr 4:67–77. https://doi.org/10.1046/j.1365-2095.1998.00046.x
Lykouras D, Sampsonas F, Kaparianos A, Karkoulias K, Spiropoulos K (2008) Role and pharmacogenomics of TNF-alpha in asthma. Mini-Rev Med Chem 8:934–942. https://doi.org/10.2174/138955708785132828
Mocellin S, Verdi D, Pooley KA, Nitti D (2015) Genetic variation and gastric cancer risk: a field synopsis and meta-analysis. Gut 64:1209–1219. https://doi.org/10.1136/gutjnl-2015-309168
Mohammadi M, Imania A, Farhangi M, Gharaei A, Hafeziehd M (2020) Replacement of fishmeal with processed canola meal in diets for juvenile Nile tilapia (Oreochromis niloticus): growth performance, mucosal innate immunity, hepatic oxidative status, liver and intestine histology. Aquacult 518:734–824. https://doi.org/10.1016/j.aquaculture.2019.734824
Mohseni M, Pourkazemi M, Baim SC (2014) Effects of dietary inorganic copper on growth performance and immune response of juvenile beluga, Huso huso. Aquacul Nutr 20:547–556. https://doi.org/10.1111/anu.12107
Muralisankar T, Bhavan PS, Radhakrishnan S et al (2014) Dietary supplementation of zinc nanoparticles and its influence on biology, physiology and immune responses of the freshwater prawn, Macrobrachium rosenbergii. Biol Trace Elem Res 160:56–66. https://doi.org/10.1007/s12011-014-0026-4
Nootash S, Sheikhzadeh N, Baradaran B et al (2013) Green tea (Camellia sinensis) administration induces expression of immune relevant genes and biochemical parameters in rainbow trout (Oncorhynchus mykiss). Fish Shellfish Immunol 35:1916–1923. https://doi.org/10.1016/j.fsi.2013.09.030
Nordberg GF, Fowler BA, Nordberg M (2015) Toxicology of metals: overview, definitions, concepts, and trends. In: Handbook on the toxicology of metals. Elsevier. https://doi.org/10.1016/C2011-0-07884-5
Opal SM, DePalo VA (2000) Anti-inflammatory cytokines. Chest 117:1162–1172. https://doi.org/10.1378/chest.117.4.1162
Opal SM, Wherry JC, Grint P (1998) Interleukin-10: potential benefits and possible risks in clinical infectious diseases. Clin Infect Dis 271:497–507. https://doi.org/10.1086/515032
Osredkar J, Sustar N (2011) Copper and zinc, biological role and significance of copper/zinc imbalance. Clin Toxicol 3:2161–495. https://doi.org/10.4172/2161-0495.S3-001
Ostaszewska T, Śliwiński J, Kamaszewski M, Sysa P, Chojnacki M (2018) Cytotoxicity of silver and copper nanoparticles on rainbow trout (Oncorhynchus mykiss) hepatocytes. Environ Sci Pollut Res 25:908–915. https://doi.org/10.1007/s11356-017-0494-0
Othman A, Andreescu D, Karunaratne DP, Babu SV, Andreescu S (2017) Functional paper-based platform for rapid capture and detection of CeO2 nanoparticles. ACS Appl Mater 9:12893–12905. https://doi.org/10.1021/acsami.7b02823
Pekiner B, Nebioglu S (1994) Effect of vitamin C on copper and iron status in men and guinea pigs. J Nutr Sci Vitaminol 40:401–410. https://doi.org/10.3177/jnsv.40.401
Pimpimol T, Phoonsamran K, Chitmanat C (2012) Effect of dietary vitamin C supplementation on the blood parameters of Mekong giant cat fish (Pangasianodongigas). Int J Agric Biol 14:256–260. https://doi.org/10.1016/S0044-8486(01)00793-1
Pirarat N, Pinpimai K, Endo M et al (2011) Modulation of intestinal morphology and immunity in Nile tilapia (Oreochromis niloticus) by Lactobacillus rhamnosus. Res Vet Sci 91:92–97. https://doi.org/10.1016/j.rvsc.2011.02.014
Qinghui A, Mai K, Zhang C et al (2004) Effects of dietary vitamin C on growth and immune response of Japanese sea bass, Lateo labrax japonicas. Aquacul 242:489–500. https://doi.org/10.1016/j.aquaculture.2004.08.016
Ramya E, Rao MV, Rao DN (2019) Nonlinear optical properties of Ag-enriched ZnO nanostructures. J Nonlinear Opt Phys Mater 281950027. https://doi.org/10.1142/S0218863519500279
Rather MA, Sharma R, Aklakur M et al (2011) Nanotechnology: a novel tool for aquaculture and fisheries development. A Prospective Mini-Review Fish Aquacul J 16:1–5. https://doi.org/10.4172/2150-3508.1000016
Rathore SS, Murthy HS, Nasren S, Mamun MAA, Rakesh K (2019) The role of vitamin c as growth promoter and its effect on intestinal histology in monosexnile tilapia, Oreochromis niloticus. J Exp Zool India 22:639–644
Ringoe E, Olsen RE, Mayhew TM, Myklebust R (2003) Electron microscopy of the intestinal microflora of fish. Aquacult 227:395–415. https://doi.org/10.1016/j.aquaculture.2003.05.001
Roosta Z, Hajimoradloo A, Ghorbani R, Hoseinifar SH (2014) The effects of dietary vitamin C on mucosal immune responses and growth performance in Caspian roach (Rutilus rutilus caspicus) fry. Fish Physiol Biochem 40:1601–1607. https://doi.org/10.1007/s10695-014-9951-6
Sabatini SE, Juarez AB, Eppis MR et al (2009) Oxidative stress and antioxidant defences in two green microalgae exposed to copper. Ecotoxicol Environ Saf 72:1200–1206. https://doi.org/10.1016/j.ecoenv.2009.01.003
Saffari S, Keyvanshokooh S, Zakeri M, Johari SA, Pasha-Zanoosi H (2016) Effects of different dietary selenium sources (sodium selenite, selenomethionine and nanoselenium) on growth performance, muscle composition, blood enzymes and antioxidant status of common carp (Cyprinus carpio). Aquac Nutr 23:611–617. https://doi.org/10.1111/anu.12428
Shafiei-Jahani P, Hurrell BPD et al (2020) R3 stimulation of adipose resident ILC2s ameliorates type 2 diabetes mellitus. Nat Commun 111-15. https://doi.org/10.1038/s41467-020-18601-7
Shao X, Liua W, Xu W et al (2010) Effects of dietary copper sources and levels on performance, copper status, plasma antioxidant activities and relative copper bioavailability in Carassius auratus gibelio. Aquacul 308:60–65. https://doi.org/10.1016/j.aquaculture.2010.07.021
Shaw BJ, Al-Bairuty G, Handy RD (2012) Effects of waterborne copper nanoparticles and copper sulphate on rainbow trout (Oncorhynchus mykiss): physiology and accumulation. Aquat Toxicol 116:90–101. https://doi.org/10.1016/j.aquatox.2012.02.032
Sheikh Asadi M, Gharaei A, Mirdar Harijani J, Arshadi A (2018) A comparison between dietary effects of Cuminum cyminum essential oil and Cuminum cyminum essential oil, loaded with iron nanoparticles, on growth performance, immunity and antioxidant indicators of white leg shrimp (Litopenaeus vannamei). Aquac Nutr 24:1466–1473. https://doi.org/10.1111/anu.12683
Shiau SY, Ning YC (2003) Estimation of dietary copper requirements of juvenile tilapia, Oreochromis niloticus and O. aureus. Anim Sci J 77:287–292. https://doi.org/10.1017/S1357729800059026
Skadberg ESS (2015) Inflammatory effects in zebrafish (Danio rerio) exposed to gold nanoparticles. Master’s Thesis in Toxicology.University of Oslo
Srivastava PK, Pandey AK (2015) Role of immunostimulants in immune responses of fish and shellfish. Biochem Cell Archiv 15:47–73
Suska F, Esposito M, Gretzer C et al (2003) IL-1α, IL-1β and TNF-α secretion during in vivo/ex vivo cellular interactions with titanium and copper. Biomaterials 24:461–468. https://doi.org/10.1016/S0142-9612(02)00359-9
Tang Q, Feng L, Jiang W D et al (2013) Effects of dietary copper on growth, digestive, and brush border enzyme activities and antioxidant defense of hepatopancreas and intestine for young grass carp (Ctenopharyngodon idella). Biol Trace Elem Res 155:370–380. https://doi.org/10.1007/s12011-013-9785-6
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 149:440–447. https://doi.org/10.1016/j.cbpc.2008.10.105
Valko M, Leibfritz D, Moncol J et al (2007) Free radicals and antioxidants in normal physiological functions and human disease. Int J Biochem Cell Biol 39:44–84. https://doi.org/10.1016/j.biocel.2006.07.001
Wahli T, Verlhac V, Girling P, Gabaudan J, Aebischer C (2003) Influence of dietary vitamin C on the wound healing process in rainbow trout (Oncorhynchus mykiss). Aquacul 225:371–386. https://doi.org/10.1016/S0044-8486(03)00302-8
Wang T, Long X, Cheng Y et al (2015) A comparison effect of copper nanoparticles versus copper sulphate on juvenile Epinephelus coioides: growth parameters, digestive enzymes, body composition, and histology as biomarkers. Int J Genomics 7:1–10. https://doi.org/10.1155/2015/783021
Wang W, Mai K, Zhang W et al (2009) Effects of dietary copper on survival, growth and immune response of juvenile abalone, Haliotis discus hannaiIno. Aquacul 297:122–127. https://doi.org/10.1016/j.aquaculture.2009.09.006
Watanabe T, Kiron V, Satoh S (1997) Trace Minerals in Fish Nutrition Aquacul 151:185–207. https://doi.org/10.1016/S0044-8486(96)01503-7
Watts DL (1989) The nutritional relationships of copper. J Orthomol Med 4:99–108
Xia J, Zhao HZ, Lu GH (2013) Effects of selected metal oxide nanoparticles on multiple biomarkers in Carassius auratus. Biomed Environ Sci 26:742–749. https://doi.org/10.3967/0895-3988.2013.09.005
Xie Z, Niu C, Zhang Z, Bao L (2006) Dietary ascorbic acid may be necessary for enhancing the immune response in Siberian sturgeon (Acipense rbaerii), a species capable of ascorbic acid biosynthesis. Comp Biochem Physiol A 145:152–157. https://doi.org/10.1016/j.cbpa.2006.05.015
Yano T (1992) Assays of hemolytic complement activity. Tech. Fish Immunol 131–141
Yilmaz S, Ergün S, Yıgıt M (2018) Effects of dietary FARMARIN® XP supplement on immunological responses and disease resistance of rainbow trout (Oncorhynchus mykiss). Aquacult 496:211–220. https://doi.org/10.1016/j.aquaculture.2018.07.024
Yousefi P, Yavari V, Zakeri M, Salati A, Keyvanshokooh S (2013) Effect of dietary supplementation of vitamin C on growth performance feed utilization and carcass composition of Barbus sharpeyi fingerlings. J Persian Gul (marine Science) 4:23–31
Yun SH, Moon YS, Sohn SH, Jang IS (2012) Effects of cyclic heat stress or vitamin C supplementation during cyclic heat stress on HSP70, inflammatory cytokines, and the antioxidant defense system in Sprague Dawley rats. Exp Anim 61:543–553. https://doi.org/10.1538/expanim.61.543
Zaboli K, Aliarabi H, Bahari AA, Abbasalipourkabir R (2013) Role of dietary nano–zinc oxide on growth performance and blood levels of mineral: a study on in Iranian Angora (Markhoz) goat kids. The International Advisory Board 2:19–26
Zhang J, Liu YJ, Tian LX et al (2013) Effects of dietary astaxanthin on growth, antioxidant capacity and gene expression in Pacific white shrimp Litopenaeus vannamei. Aquacul Nut 19:917–927. https://doi.org/10.1111/anu.12037
Zhou Q, Wang L, Wang H, Xie F, Wang T (2012) Effect of dietary vitamin C on the growth performance and innate immunity of juvenile cobia (Rachycentron canadum). Fish Shellfish Immunol 32:969–975. https://doi.org/10.1016/j.fsi.2012.01.024
Acknowledgements
We thank Dr. Khosravanizadeh for his time and energy and all staff of Hamoon International Wetland Research Institute for the financial support and cooperation.
Funding
The research project was funded by the University of Zabol (Grant cod: IR-UOZ-GR-7925).
Author information
Authors and Affiliations
Contributions
DNM: MSc student; these data are coming from his thesis; GA: Associate professor in the Department of Fisheries and the main supervisor for the student. He provided all the scientific suggestions and grants; MHJ: He is the second supervisor and provided scientific suggestions; DA: She was the advisor for the work and provided scientific comments; RA: He was the advisor for the scientific group.
Corresponding author
Ethics declarations
Ethics approval
All procedures were carried out in accordance with the Animal Care and Use Committee guidelines at the Faculty of Sciences of the University of Zabol.
Consent to participate
The authors agree to collaborate and publish this article.
Consent for publication
We will transfer the copyright of the article to editorial office for publishing.
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
Delavari, N.M., Gharaei, A., Mirdar, H.J. et al. Modulatory effect of dietary copper nanoparticles and vitamin C supplementations on growth performance, hematological and immune parameters, oxidative status, histology, and disease resistance against Yersinia ruckeri in rainbow trout (Oncorhynchus mykiss). Fish Physiol Biochem 48, 33–51 (2022). https://doi.org/10.1007/s10695-021-01036-2
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10695-021-01036-2