Effects of Dietary Vitamin C on the Growth Performance, Biochemical Parameters, and Antioxidant Activity of Coho Salmon <i>Oncorhynchus kisutch</i> (Walbaum, 1792) Postsmolts

Xu, Cong-mei; Yu, Hai-rui; Li, Ling-yao; Li, Min; Qiu, Xiang-yi; Fan, Xiao-qian; Fan, Yan-lin; Shan, Ling-ling

doi:https://doi.org/10.1155/2022/6866578

Aquaculture Nutrition

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Abstract Introduction Materials and Methods Results Discussion Conclusion Data Availability Ethical Approval Conflicts of Interest Acknowledgments References Copyright Related Articles

Research Article | Open Access

Volume 2022 | Article ID 6866578 | https://doi.org/10.1155/2022/6866578

Effects of Dietary Vitamin C on the Growth Performance, Biochemical Parameters, and Antioxidant Activity of Coho Salmon Oncorhynchus kisutch (Walbaum, 1792) Postsmolts

Cong-mei Xu,¹Hai-rui Yu,¹Ling-yao Li,^1,2Min Li,^1,2Xiang-yi Qiu,¹Xiao-qian Fan,¹Yan-lin Fan,¹and Ling-ling Shan²

Academic Editor: M Xue

Received15 Apr 2022

Revised19 Sept 2022

Accepted01 Dec 2022

Published26 Dec 2022

Abstract

Vitamin C (VC) plays an essential role in fish physiological function and normal growth. However, its effects and requirement of coho salmon Oncorhynchus kisutch (Walbaum, 1792) are still unknown. Based on the influences on growth, serum biochemical parameters, and antioxidative ability, an assessment of dietary VC requirement for coho salmon postsmolts ( g) was conducted with a ten-week feeding trial. Seven isonitrogenous (45.66% protein) and isolipidic (10.76% lipid) diets were formulated to include graded VC concentrations of 1.8, 10.9, 50.8, 100.5, 197.3, 293.8, and 586.7 mg/kg, respectively. Results showed that VC markedly improved the growth performance indexes and liver VC concentration, enhanced the hepatic and serum antioxidant activities, and increased the contents of serum alkaline phosphatase (AKP) activity, low-density lipoprotein cholesterol (LDL-C), high-density lipoprotein cholesterol (HDL-C), and total cholesterol (TC) whereas decreased the serum aspartate aminotransferase (AST), alanine aminotransferase (ALT) activities, and triglyceride (TG) level. Polynomial analysis showed that the optimal VC levels in the diet of coho salmon postsmolts were 188.10, 190.68, 224.68, 132.83, 156.57, 170.12, 171.00, 185.50, 142.77, and 93.08 mg/kg on the basis of specific growth rate (SGR), feed conversion ratio (FCR), liver VC concentration, catalase (CAT), hepatic superoxide dismutase (SOD) activities, malondialdehyde (MDA) content, and serum total antioxidative capacity (T-AOC), AKP, AST, and ALT activities, respectively. The dietary VC requirement was in the range of 93.08–224.68 mg/kg for optimum growth performance, serum enzyme activities, and antioxidant capacity of coho salmon postsmolts.

1. Introduction

Fish require vitamins to survive because they act as enzyme cofactors [1], through which vitamins help organisms maintain optimal health and normal metabolic functions [2, 3]. As a water-soluble vitamin, vitamin C (VC) plays a crucial role in maintaining normal fish growth and physiological function [4–9]. Examples of physiological effects of VC proved in fish are related to reproduction [6, 10, 11], normal growth [12, 13], cartilage and bone formation [14], the iron metabolism and hematology [15, 16], lipid metabolism [17, 18], stress [19–21], immune response [22–24], and interactions with other micronutrients [25, 26]. VC had also been proved to reduce the oxidative stress of fish, thus benefiting the fish health [20, 27–29]. Compared to feeding with VC-deficient diet, yellow catfish, Pelteobagrus fulvidraco (Richardson, 1846), feeding with adequate dietary VC showed higher catalase (CAT), superoxide dismutase (SOD), and glutathione peroxidase (GPx) activities [30]. VC was also found to have an active influence on antioxidant ability of black carp, Mylopharyngodon piceus (Richardson, 1846) [31], and Siberian sturgeon, Acipenser baerii (Brandt, 1869) [32]. Thus, VC supplementation is required for fishes [1].

VC or L-ascorbic acid cannot be synthesized by teleost fishes, because of the mutation of the L-gulonolactone oxidase gene that encodes the enzyme charging for catalyzing the final procedure of VC de novo synthesis [33, 34]. Therefore, farmed fish need to gain VC through the diets for optimum growth and other physiological function maintenance. Inappropriate supplementation of VC would lead to lower enzyme activities, thus resulting in poor growth performance, low survival rate, and being susceptible to diseases of fish [1, 8, 30, 35]. Dietary VC deficiency would also lead to some nonspecific signs, such as changes of serum triglycerides and cholesterol levels [1, 36]. The dietary VC requirement had been investigated in many farmed fish species, and the optimal dietary VC levels are varied among fish species [1], which can be affected by the growth rates, age, size, various environmental factors, and nutrient interrelationships of the fish [1, 7, 24]. Consequently, it is crucial to analyze dietary VC requirement for a certain fish species.

In order to meet the increased needs for fish as food source, the aquaculture industry has dramatically expanded in recent years compared with other sectors of food production [37]. Coho salmon, Oncorhynchus kisutch (Walbaum, 1792), is a Pacific salmon (genus Oncorhynchus) species well known for its high protein and high unsaturated fatty acids (HUFAs) contents, especially omega-3 HUFAs which had a series of health benefits for human being [38–40]. Over the past few years, coho salmon is increasingly farmed in China. As large-scale farming expands, studies on the nutrition of coho salmon have been relatively backwards, and little is known about its dietary VC requirements for this fish. In this study, we investigated the efficacy of graded dietary VC on growth, serum biochemical parameters, and antioxidant activities of coho salmon postsmolts.

2. Materials and Methods

2.1. Diet Preparation

In Table 1, we present the formulation and approximate composition of diets. Seven isonitrogenous (45.66% protein) and isolipidic (10.76% lipid) diets were formulated. Ascorbic acid-2-phosphate (NHU Co. Ltd., Shaoxing, China) was added to the seven diets as a VC source because of its high heat resistance compared with the unprotected VC [41]. The corresponding levels of dietary VC were determined by high performance liquid chromatography (HPLC; LC-20AD, Shimadzu, Japan) to contain 1.8, 10.9, 50.8, 100.5, 197.3, 293.8, and 586.7 mg/kg, respectively (Table 1).

Vitamin mixtures and mineral mixtures were premixed with α-cellulose in advance. The dry ingredients, except vitamin and mineral mixtures, were sieved through a 60-mesh sieve and then weighed and mixed accurately in a Hobart-type mixer until homogenous; after that, vitamin and mineral mixtures were added and continued to mix. Finally, fish oil as well as distilled water (30%) was added in order; after that, the mixture was pelleted (diameters 3 mm) by using a laboratory pelleting mill. In order to ensure the quality of the diets, they were air-dried until moisture levels are less than 10% and sieved, after which they were sealed in airtight bags and stored at -20°C until used.

2.2. Fish and Experimental Procedures

The postsmolts were acclimated in the culture system with two weeks, during which they were fed with basal diets (with no VC supplementation). After the acclimation, 210 fish (initial body weight: g) were assigned randomly to 21 cages (water volume 1,000 l) in a pond. Fish were fed three times daily for 10 weeks, 4 weeks with 5% of body weight per day and the next 6 weeks with 3%. Food residues, if any, should be sucked out and collected, and then, the dry weight is determined by drying at 105°C. During the experimental period, fish were gently moved out and bulk weighed biweekly and were fasted at that very day. A high-pressure water gun was used to brush and rinse cages at the same time. The water flow rate was in the range of 1.8-2.2 l/min; the water pH and temperature were and °C, respectively; dissolved oxygen was ranged between 7.5 and 8.0 mg O₂/l; the ammonia nitrogen was mg/l; and the alkalinity was between 90-130 mg/l. Postsmolts were reared under natural lighting and in freshwater.

2.3. Sample Collection

Fish were counted and weighed in bulk from each cage after a 24-hour fast at the end of the feeding period, following which seven fish from each cage were sampled for analysis. For determining morphological indexes, containing hepatosomatic index (HSI), intestosomatic index (ISI), and condition factor (CF), three were selected from each cage. Following the measurement of the body length, another four were chose to gain serum samples by taking blood from the caudal vein. The blood samples stood for 2 hours at room temperature and then were centrifuged for 3500 g for 10 minutes; after that, the supernatant was collected and then stored at -80°C until it was analyzed for biochemical parameters and antioxidant activity. The 4 fish were dissected quickly after exsanguination, and the liver and muscle were removed and stored at -80°C. The liver samples were used to analyze hepatic VC concentration and antioxidant capacity, and muscle samples were for the assessments of muscle proximate composition.

2.4. Data Collection

2.4.1. Growth Performance

The parameters of growth performance and body indices were calculated with the following formula:

2.4.2. Proximate Composition Analysis

The moisture was assessed according to drying at 105°C, the ash was determined through incineration at 550°C, the crude lipid was extracted with petroleum ether and determined by the Soxhlet apparatus, and crude protein was determined by the Kjeldahl apparatus (nitrogen ×6.25) [42].

2.4.3. Serum and Hepatic Biochemical Analysis

The liver samples were homogenized in 0.1 M Tris-HCl buffer () at 4°C; after that, the homogenate was gathered and then stored at -80°C until analyzed. The hepatic malondialdehyde (MDA) content; SOD and CAT activities; the serum aspartate aminotransferase (AST), alanine aminotransferase (ALT), alkaline phosphatase (AKP), and total antioxidative capacity (T-AOC) activities; high-density lipoprotein cholesterol (HDL-C), low-density lipoprotein cholesterol (LDL-C), triglyceride (TG), and total cholesterol (TC) contents were determined using the reagent kits (Nanjing Jiancheng Bioengineering Institute, Nanjing, China).

2.4.4. VC Content Assay

The VC concentration of the experimental diets was analyzed by HPLC with a C18 column (5 μm, mm). The protocols were referred to a national standard method (GB/T238882-2009). In brief, the phosphate-buffered saline (PBS) solution was prepared to contain 0.054 g/ml KH₂PO₄; the mobile phase was prepared by dissolving the KH₂PO₄, tetrabutyl ammonium hydrogen sulfate, and methanol with a certain proportion; and then, the solution was filtered and degassed. The diet samples (about 3 g) were extracted in PBS, then degassed, centrifuged, and filtered. The tris-(cyclohexyl-ammonium)-ascorbic acid-2-phosphate (Merck, Germany) dissolving in PBS was used as standard sample. Hepatic VC content was analyzed using the reagent kit (Nanjing Jiancheng Bioengineering Institute, Jiangsu, China) [43].

2.4.5. Statistical Analyses

The data are showed with (SE). The response of the dependent variable to the VC level was described by orthogonal polynomial contrasts [44]. The means of each group were determined by Duncan’s test, and were considered to have significant difference. Linear and cubic regression analyses were used to analyze optimal dietary VC levels of coho salmon.

3. Results

3.1. Growth Performance

Graded dietary VC concentrations did not have significant influence on the coho salmon postsmolts survival () (Table 2). The SGR was increased and FCR decreased in fish when fed diets with graded VC concentrations (linear, quadratic, and cubic; ). HSI, VSI, and CF showed no significant effect with different VC levels (). According to the polynomial regression analysis of SGR and FCR, the VC requirements for coho salmon postsmolts were predicted to be 188.10 and 190.68 mg/kg, respectively (Figures 1(a) and 1(b)).

(a)

(b)

3.2. Muscle Proximate Composition and Liver VC Concentration

Dietary VC levels did not have significant effects on the muscle proximate composition including moisture, crude protein, crude lipid, and ash of coho salmon postsmolts () (Table 3). The crude protein content varied among 19.56 to 20.12%. The crude lipid content varied among 3.78 to 3.94%. The ash was ranged between 2.50 and 2.76%. The moisture was in the range of 71.59 to 73.54%. With the rising of VC concentrations in the diets, the hepatic VC concentration showed linear and cubic increases () (Table 3). The optimal dietary VC requirement based on liver VC concentration was 224.68 mg/kg (Figure 2).

3.3. Biochemical Parameters and Enzymes Activities of Serum

The TG level declined, and the LDL-C and HDL-C levels rose in linear, quadratic, and cubic manners when fish fed diets with increasing VC concentrations (). TC level was showed with linear and cubic rising trends (linear and cubic, ) and the AKP activity with linear, quadratic, and cubic rising trends () when fish fed diets with graded VC concentrations. With the VC concentrations increased, the AST activity was showed with linear, quadratic, and cubic reducing trends () and ALT activity with linear and quadratic reducing trends () (Table 4). The VC requirements for coho salmon postsmolts were 185.50, 142.77, and 93.08 mg/kg based on serum AKP, AST, and ALT activities, respectively (Figures 3(a)–3(c)).

(a)

(b)

(c)

3.4. Activities of Serum and Hepatic Antioxidant Enzymes

The hepatic CAT, SOD activities, and serum T-AOC activity were risen, and the hepatic MDA contents declined in linear, quadratic, and cubic manners when fish fed diets with graded VC concentrations () (Table 5). The VC requirements for coho salmon postsmolts were 71.46 and 176.19 mg/kg according to hepatic SOD, CAT activities (Figures 4(a) and 4(b)), MDA content (Figure 4(c)), and serum T-AOC activity (Figure 4(d)), respectively.

(a)

(b)

(c)

(d)

4. Discussion

It has been well known that dietary VC can enhance survival rates, growth, immune, and stress resistance [1, 7, 8, 30, 45]. Deficiency in VC supplementation caused retarded growth, poor survival rate, or abnormal pigmentation in many studied fishes [4, 24, 46, 47]. In the study, the adequate VC level of the diet could obviously improve the growth performance of coho salmon postsmolts. It was suggested that the improvement of growth might result from the rising of feed efficiency to the diet [7, 8]. VC might have effects on nutrient utilization, because of its importance in the process of protein metabolism and stimulating protein synthesis [48]. Dietary VC requirement was also needed for Atlantic salmon, Salmo salar (Linnaeus, 1758) alevins, in which the SGR was significantly improved with VC supplementation [9]. However, in rainbow trout, Oncorhynchus mykiss (Walbaum, 1792), the growth was not obviously changed when fed with diets with graded VC levels [49]. Impacts of VC supplementation on fish can be influenced by fish species, size, developmental stage, and variation in experimental conditions as well as cultivation environment [1].

This study showed that no other VC deficiency signs mentioned above were observed throughout the experiment except a reduction in weight gain. This was similar with that in yellow croaker Pseudosciaena amblyceps (Richardson, 1846) [50], Atlantic salmon [51], and seabream Sparus aurata (Linnaeus, 1758) [52]. Lack of phenotype might be caused by the fish size in the experiment, which was larger than that of Japanese seabass Lateolabrax japonicus (Cuvier, 1828) [12], common carp Cyprinus carpio (Linnaeus, 1758) [53], and hybrid tilapia Oreochromis niloticus × Oreochromis aureus [54]. According to a study about the effects of size or age on VC supplement deficiency in fish, the size of fish was positively related to the onset of fish deficiency symptoms [55].

TG and TC are suggested to be important in the process of lipid metabolism. High TG levels can result in liver dysfunction, nephritic syndrome, and glycogen storage disease [56, 57]. In this study, VC supplementation obviously decreased the TG level of serum, suggesting that dietary VC levels did affect the coho salmon health. Blood TC including HDL-C as well as LDL-C levels had been documented to decrease [58–61], increase [36, 62, 63], or be independent [23, 30, 64] with dietary VC supplementation in fishes. VC had synergistic effects on cholesterol synthesis and catabolism; this might be the reason that VC had variable influences on serum cholesterol contents [65]. In the study, TC, LDL-C, and HDL-C contents showed dramatic increase with VC supplementation, which were similar with those in rainbow trout [36]. It was suggested that dietary VC levels increased the cholesterol synthesis and inhibited the degradation and clearance of serum LDL-C [36].

Radicals like reactive oxygen species (ROS) were considered to be harmful to some vital cellular components, for example, DNA, proteins, carbohydrates, and lipids [35, 66]. The increasing of free radical production in cells would lead to oxidative stress and further result in cell and tissue damages [67, 68]. MDA, produced by lipid peroxidation, is toxic for cells, whose structure and function would be damaged. As a consequence, MDA is suggested to be an indicator of oxidative cell damage [69]. The antioxidative enzymes like CAT and SOD could eliminate excess ROS, thus decreased the damages caused by lipid peroxidation [70, 71]. In the present study, fish supplied with appropriate dietary VC exhibited higher contents of serum T-AOC and hepatic CAT, SOD, and lower levels of hepatic MDA. This was in agreement with that in the studies of thornfish Bovichtus variegatus (Richardson, 1846) [72], juvenile cobia [24], juvenile black carp Mylopharyngodon piceus (Richardson, 1846) [32], and Nile tilapia fingerlings [8]. In addition, the AKP can act as a hydrolytic enzyme which could promote the recognition and phagocytosis capacity of organism, thus increased the nonspecific immunity of organism [73]. Serum AKP levels in cobia, Rachycentron canadum (Linnaeus, 1766), and Tilapia, Oreochromis niloticus, (Linnaeus, 1758) were significantly increased with VC supplementation [24, 74]. Another previous study showed that the serum AKP level was increased with VC supplementation in Wuchang bream, Megalobrama amblycephala (Yih, 1955), when suffered with stress from pH [46]. This study also reported that the serum AKP activity was increased with adequate VC supplementation of coho salmon. All these are considered to be attributed to the powerful antioxidative activity of VC. Acting as an electron donor, VC is an antioxidant that scavenges free radicals, thus inhibiting radical injuries to cellular components [75, 76].

ALT and AST generally exist in the body [77]. These enzymes also play key roles in evaluating the healthy status of the liver and some other organs [78]. Their higher activities in serum may suggest organ dysfunction or tissue injury [79]. AST and ALT are important in hepatic function that contributes to the mutual transformation of amino acid, carbohydrates, and lipid. Their contents are high in tissue and low in serum when fish is in health status [35]. The rising of AST and ALT activities in serum might primarily be caused by hepatic AST and ALT enzymes leaking to the extracellular space and ultimately to the plasma [80], indicating the hepatotoxic effect of VC deficiency. In this report, the ALT and AST levels exhibited obvious declines following treatment with adequate VC supplementation, suggesting the efficacy of this nutrient to protect liver cells from damages. This is in agreement with that in juvenile Chinese sucker Myxocyprinus asiaticus (Bleeker, 1865) and juvenile striped catfish Pangasianodon hypophthalmus (Sauvage, 1878), in which the optimal dietary VC is helpful to maintain the proper function of liver [35, 81].

5. Conclusion

In conclusion, adequate VC supplementation is essential to improve the growth performance and liver VC content; decreased serum TG level and AST and ALT activities; increased serum TC, HDL-C, and LDL-C contents; and enhanced antioxidant capacity of coho salmon postsmolts. The optimal VC level was in the range of 93.08–224.68 mg/kg for optimum growth performance, serum enzyme activities, and antioxidative ability of coho salmon postsmolts.

Data Availability

All the data in the article are available from the corresponding author upon reasonable request.

Ethical Approval

The study was conducted in accordance with the recommendations in the Guide for the Use of Experimental Animals of the Weifang University.

Conflicts of Interest

The authors declare that they have no conflicts of interest.

Acknowledgments

This study was supported by the Shandong Provincial Key Research and Development Programs (Major Scientific and Technological Innovation Project of Shandong Province, MSTIP), Grant/Award Numbers: 2018CXGC0102 and 2019JZZY020710; the Scientific and Technologic Development Program of Weifang, Grant/Award Number: 2019ZJ1046; and the Shandong Provincial Natural Science Foundation, Grant/Award Number: ZR2020MC174.

References

National Research Council, Nutrient Requirements of Fish and Shrimp, National Academy Press, Washington, DC, 2011.
View at: Publisher Site
L. Gasco, F. Gai, G. Maricchiolo et al., “Supplementation of vitamins, minerals, enzymes and antioxidants in fish feeds,” in Feeds for the Aquaculture Sector: Current Situation and Alternative Sources, pp. 63–103, Springer International Publishing, Cham, 2018.
View at: Publisher Site | Google Scholar
A. Gouda, S. A. Amer, S. Gabr, and S. A. Tolba, “Effect of dietary supplemental ascorbic acid and folic acid on the growth performance, redox status, and immune status of broiler chickens under heat stress,” Tropical Animal Health and Production, vol. 52, no. 6, pp. 2987–2996, 2020.
View at: Publisher Site | Google Scholar
C. Lim and R. T. Lovell, “Pathology of the vitamin C deficiency syndrome in channel catfish (Ictalurus punctatus),” Journal of Nutrition, vol. 108, no. 7, pp. 1137–1146, 1978.
View at: Publisher Site | Google Scholar
T. Ren, S. Koshio, M. Ishikawa et al., “Influence of dietary vitamin C and bovine lactoferrin on blood chemistry and non-specific immune responses of Japanese eel, Anguilla japonica,” Aquaculture, vol. 267, no. 1-4, pp. 31–37, 2007.
View at: Publisher Site | Google Scholar
E. Shahkar, H. Yun, D. J. Kim, S. K. Kim, B. I. Lee, and S. C. Bai, “Effects of dietary vitamin C levels on tissue ascorbic acid concentration, hematology, non-specific immune response and gonad histology in broodstock Japanese eel, Anguilla japonica,” Aquaculture, vol. 438, pp. 115–121, 2015.
View at: Publisher Site | Google Scholar
M. A. O. Dawood and S. Koshio, “Vitamin C supplementation to optimize growth, health and stress resistance in aquatic animals,” Reviews in Aquaculture, vol. 10, no. 2, pp. 334–350, 2018.
View at: Publisher Site | Google Scholar
R. E. Ibrahim, S. A. Ahmed, S. A. Amer et al., “Influence of vitamin C feed supplementation on the growth, antioxidant activity, immune status, tissue histomorphology, and disease resistance in Nile tilapia , Oreochromis niloticus,” Aquaculture Reports, vol. 18, article 100545, 2020.
View at: Publisher Site | Google Scholar
K. Sandnes, O. Torrissen, and R. Waagbø, “The minimum dietary requirement of vitamin C in Atlantic salmon (Salmo salar) fry using Ca ascorbate-2-monophosphate as dietary source,” Fish Physiology and Biochemistry, vol. 10, no. 4, pp. 315–319, 1992.
View at: Publisher Site | Google Scholar
M. J. Darias, D. Mazurais, G. Koumoundouros, C. L. Cahu, and J. L. Zambonino-Infante, “Overview of vitamin D and C requirements in fish and their influence on the skeletal system,” Aquaculture, vol. 315, no. 1-2, pp. 49–60, 2011.
View at: Publisher Site | Google Scholar
N. L. A. F. Sarmento, E. F. F. Martins, D. C. Costa et al., “Reproductive efficiency and egg and larvae quality of Nile tilapia fed different levels of vitamin C,” Aquaculture, vol. 482, pp. 96–102, 2018.
View at: Publisher Site | Google Scholar
Q. H. Ai, K. S. Mai, C. X. Zhang et al., “Effects of dietary vitamin C on growth and immune response of Japanese seabass, Lateolabrax japonicus,” Aquaculture, vol. 242, no. 1-4, pp. 489–500, 2004.
View at: Publisher Site | Google Scholar
Y. J. Chen, R. M. Yuan, Y. J. Liu, H. J. Yang, G. Y. Liang, and L. X. Tian, “Dietary vitamin C requirement and its effects on tissue antioxidant capacity of juvenile largemouth bass, Micropterus salmoides,” Aquaculture, vol. 435, pp. 431–436, 2015.
View at: Publisher Site | Google Scholar
V. B. Kraus, J. L. Huebner, T. Stabler et al., “Ascorbic acid increases the severity of spontaneous knee osteoarthritis in a guinea pig model,” Arthritis and Rheumatism, vol. 50, no. 6, pp. 1822–1831, 2004.
View at: Publisher Site | Google Scholar
K. Sandnes, T. Hansen, J. E. A. Killie, and R. WaagbØ, “Ascorbate-2-sulfate as a dietary vitamin C source for Atlantic salmon (Salmo salar): 2. effects of dietary levels and immunization on the metabolism of trace elements,” Fish Physiology and Biochemistry, vol. 8, no. 6, pp. 429–436, 1990.
View at: Publisher Site | Google Scholar
S. J. Padayatty and M. Levine, “New insights into the physiology and pharmacology of vitamin C,” Canadian Medical Association Journal, vol. 164, no. 3, pp. 353–355, 2001.
View at: Google Scholar
T. M. John, J. C. Gorge, J. W. Hilton, and S. J. Slinger, “Influence of dietary ascorbic acid on plasma lipid levels in the rainbow trout,” International Journal for Vitamin and Nutrition Research, vol. 49, no. 4, pp. 400–405, 1979.
View at: Google Scholar
R. Waagbø, T. Thorsen, and K. Sandnes, “Role of dietary ascorbic acid in vitellogenesis in rainbow trout (Salmo gairdneri),” Aquaculture, vol. 80, no. 3-4, pp. 301–314, 1989.
View at: Publisher Site | Google Scholar
R. Chakrabarti, M. K. Singh, J. G. Sharma, and P. Mittal, “Dietary supplementation of vitamin C: an effective measure for protection against UV-B irradiation using fish as a model organism,” Photochemical & Photobiological Sciences, vol. 18, no. 1, pp. 224–231, 2019.
View at: Publisher Site | Google Scholar
C. A. S. Caxico Vieira, J. S. Vieira, M. S. Bastos et al., “Expression of genes related to antioxidant activity in Nile tilapia kept under salinity stress and fed diets containing different levels of vitamin C,” Journal of Toxicology and Environmental Health, Part A, vol. 81, pp. 20–30, 2018.
View at: Publisher Site | Google Scholar
J. Yan, X. Liang, Y. Zhang, Y. Li, X. Cao, and J. Gao, “Cloning of three heat shock protein genes (HSP70, HSP90 α and HSP90 β) and their expressions in response to thermal stress in loach (Misgurnus anguillicaudatus) fed with different levels of vitamin C,” Fish & Shellfish Immunology, vol. 66, pp. 103–111, 2017.
View at: Publisher Site | Google Scholar
M. M. Barros, D. R. Falcon, R. O. Orsi et al., “Non-specific immune parameters and physiological response of Nile tilapia fed β-glucan and vitamin C for different periods and submitted to stress and bacterial challenge,” Fish & Shellfish Immunology, vol. 39, no. 2, pp. 188–195, 2014.
View at: Publisher Site | Google Scholar
M. A. O. Dawood, S. Koshio, M. El-Sabagh et al., “Changes in the growth, humoral and mucosal immune responses following β-glucan and vitamin C administration in red sea bream, Pagrus major,” Aquaculture, vol. 470, pp. 214–222, 2017.
View at: Publisher Site | Google Scholar
Q. Zhou, L. Wang, H. Wang, F. Xie, and T. Wang, “Effect of dietary vitamin C on the growth performance and innate immunity of juvenile cobia (Rachycentron canadum),” Fish & Shellfish Immunology, vol. 32, no. 6, pp. 969–975, 2012.
View at: Publisher Site | Google Scholar
H. P. Liu, B. Wen, Z. Z. Chen et al., “Effects of dietary vitamin C and vitamin E on the growth, antioxidant defence and digestive enzyme activities of juvenile discus fish (Symphysodon haraldi),” Aquaculture Nutrition, vol. 25, no. 1, pp. 176–183, 2019.
View at: Publisher Site | Google Scholar
Y. N. Min, Z. Y. Niu, T. T. Sun et al., “Vitamin E and vitamin C supplementation improves antioxidant status and immune function in oxidative-stressed breeder roosters by up-regulating expression of GSH-Px gene,” Poultry Science, vol. 97, no. 4, pp. 1238–1244, 2018.
View at: Publisher Site | Google Scholar
D. R. Tocher, G. Mourente, A. Van der Eecken et al., “Comparative study of antioxidant defence mechanisms in marine fish fed variable levels of oxidised oil and vitamin E,” Aquaculture International, vol. 11, no. 1-2, pp. 195–216, 2003.
View at: Publisher Site | Google Scholar
J. Gao, S. Koshio, M. Ishikawa, S. Yokoyama, R. E. P. Mamauag, and Y. Han, “Effects of dietary oxidized fish oil with vitamin E supplementation on growth performance and reduction of lipid peroxidation in tissues and blood of red sea bream Pagrus major,” Aquaculture, vol. 356-357, pp. 73–79, 2012.
View at: Publisher Site | Google Scholar
J. Gao, S. Koshio, M. Ishikawa, S. Yokoyama, R. E. P. Mamauag, and B. T. Nguyen, “Effect of dietary oxidized fish oil and vitamin C supplementation on growth performance and reduction of oxidative stress in red sea bream Pagrus major,” Aquaculture Nutrition, vol. 19, no. 1, pp. 35–44, 2013.
View at: Publisher Site | Google Scholar
X. P. Liang, Y. Li, Y. M. Hou, H. Qiu, and Q. C. Zhou, “Effect of dietary vitamin C on the growth performance, antioxidant ability and innate immunity of juvenile yellow catfish (Pelteobagrus fulvidraco Richardson),” Aquaculture Research, vol. 48, no. 1, pp. 149–160, 2017.
View at: Publisher Site | Google Scholar
Y. Hu, Y. Huang, H. Wen et al., “Effect of vitamin C on growth,immunity and anti-ammonia-nitrite stress ability in juvenile black carp (Mylopharyngodon piceus),” Journal of Fisheries of China, vol. 37, no. 4, pp. 565–573, 2013.
View at: Publisher Site | Google Scholar
Z. Xie, C. Niu, Z. Zhang, and L. Bao, “Dietary ascorbic acid may be necessary for enhancing the immune response in Siberian sturgeon (Acipenser baerii), a species capable of ascorbic acid biosynthesis,” Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology, vol. 145, no. 2, pp. 152–157, 2006.
View at: Publisher Site | Google Scholar
M. Nishikimi and K. Yagi, “Molecular basis for the deficiency in humans of gulonolactone oxidase, a key enzyme for ascorbic acid biosynthesis,” American Journal of Clinical Nutrition, vol. 54, no. 6, pp. 1203S–1208S, 1991.
View at: Publisher Site | Google Scholar
G. Drouin, J. R. Godin, and B. Pagé, “The genetics of vitamin C loss in vertebrates,” Current Genomics, vol. 12, no. 5, pp. 371–378, 2011.
View at: Publisher Site | Google Scholar
F. Huang, F. Wu, S. Zhang et al., “Dietary vitamin C requirement of juvenile Chinese sucker (Myxocyprinus asiaticus),” Aquaculture Research, vol. 48, no. 1, pp. 37–46, 2011.
View at: Publisher Site | Google Scholar
J. M. Deng, X. D. Zhang, J. W. Zhang et al., “Effects of dietary ascorbic acid levels on cholesterol metabolism in rainbow trout (Oncorhynchus mykiss),” Aquaculture Nutrition, vol. 25, no. 6, pp. 1345–1353, 2019.
View at: Publisher Site | Google Scholar
FAO (Agriculture Organization of the United Nations), “The State of World Fisheries and Aquaculture 2018-Meeting the Sustainable Development Goals. Licence. Rome. CC BY-NC-SA 3.0 IGO,” http://www.fao.org/fishery/statistics/globalaquacultureproduction/query/en.
View at: Google Scholar
D. Swanson, R. Block, and S. A. Mousa, “Omega-3 fatty acids EPA and DHA: health benefits throughout life,” Advances in Nutrition, vol. 3, no. 1, pp. 1–7, 2012.
View at: Publisher Site | Google Scholar
Q. L. Ma, B. Teter, O. J. Ubeda et al., “Omega-3 fatty acid docosahexaenoic acid increases SorLA/LR11, a sorting protein with reduced expression in sporadic Alzheimer’s disease (AD): relevance to AD prevention,” Journal of Neuroscience, vol. 27, no. 52, pp. 14299–14307, 2007.
View at: Publisher Site | Google Scholar
I. J. Tinsley, H. M. Krueger, and J. B. Saddler, “Fatty acid content of coho salmon,Oncorhynchus kisutch— a statistical approach to changes produced by diet,” Journal of the Fisheries Board of Canada, vol. 30, no. 11, pp. 1661–1666, 1973.
View at: Publisher Site | Google Scholar
K. Dabrowski, “Primitive actimoterigian fishes can synthesize ascorbic acid,” Experientia, vol. 50, no. 8, pp. 745–748, 1994.
View at: Publisher Site | Google Scholar
AOAC, Association of Official Analytical Chemists, Van Nostrand’s Encyclopedia of Chemistry, G. D. Considine, Ed., AOAC, Association of Official Analytical Chemists, Arlington, USA, 2005.
View at: Publisher Site
K. Dabrowski and S. Hinterleitner, “Applications of a simultaneous assay of ascorbic acid, dehydroascorbic acid and ascorbic sulphate in biological materials,” Analyst, vol. 114, no. 1, pp. 83–87, 1989.
View at: Publisher Site | Google Scholar
R. Yossa and M. Verdegem, “Misuse of multiple comparison tests and underuse of contrast procedures in aquaculture publications,” Aquaculture, vol. 437, pp. 344–350, 2015.
View at: Publisher Site | Google Scholar
F. C. J. Gerald and J. P. McClung, The Vitamins: Fundamental Aspects in Nutrition and Health, American Academic Press, US, 5th edition, 2016.
J. J. Wan, X. P. Ge, B. Liu et al., “Effect of dietary vitamin C on non-specific immunity and mRNA expression of three heat shock proteins (HSPs) in juvenile Megalobrama amblycephala under pH stress,” Aquaculture, vol. 434, pp. 325–333, 2014.
View at: Publisher Site | Google Scholar
C. H. Cheng, H. Y. Liang, Z. X. Guo, A. L. Wang, and C. X. Ye, “Effect of dietary vitamin C on the growth performance, antioxidant ability and innate immunity of juvenile yellow catfish (Pelteobagrus fulvidraco Richardson),” Israeli Journal of Aquaculture-Bamidgeh, vol. 48, no. 1, pp. 149–160, 2017.
View at: Publisher Site | Google Scholar
G. C. Chatterjee, “Effects of ascorbic acid deficiency in animals,” in The Vitamins, W. H. Sebrell Jr. and R. S. Harris, Eds., vol. 1, pp. 407–456, Academic Press, New York, 1967.
View at: Google Scholar
K. Dabrowski, K. Matusiewicz, M. Matusiewicz, P. P. Hoppe, and J. Ebeling, “Bioavailability of vitamin C from two ascorbyl monophosphate esters in rainbow trout, Oncorhynchus mykiss (Walbaum),” Aquaculture Nutrition, vol. 2, no. 1, pp. 3–10, 1996.
View at: Publisher Site | Google Scholar
Q. H. Ai, K. M. Mai, B. P. Tan et al., “Effects of dietary vitamin C on survival, growth, and immunity of large yellow croaker, Pseudosciaena crocea,” Aquaculture, vol. 261, no. 1, pp. 327–336, 2006.
View at: Publisher Site | Google Scholar
I. Thompson, A. White, T. C. Fletcher, D. F. Houlihan, and C. J. Secombes, “The effect of stress on the immune response of Atlantic salmon (Salmo salar L.) fed diets containing different amounts of vitamin C,” Aquaculture, vol. 114, no. 1-2, pp. 1–18, 1993.
View at: Publisher Site | Google Scholar
M. M. F. Henrique, E. F. Gomes, M. F. Gouillou-Coustans, A. Oliva-Teles, and S. J. Davies, “Influence of supplementation of practical diets with vitamin C on growth and response to hypoxic stress of seabream, Sparus aurata,” Aquaculture, vol. 161, no. 1-4, pp. 415–426, 1998.
View at: Publisher Site | Google Scholar
M. F. Gouillou-Coustans, P. Bergot, and S. J. Kaushik, “Dietary ascorbic acid needs of common carp (Cyprinus carpio) larvae,” Aquaculture, vol. 161, no. 1-4, pp. 453–461, 1998.
View at: Publisher Site | Google Scholar
S. Y. Shiau and Y. P. Yu, “Dietary supplementation of chitin and chitosan depresses growth in tilapia, Oreochromis niloticus × O. aureus,” Aquaculture, vol. 179, no. 1-4, pp. 439–446, 1999.
View at: Publisher Site | Google Scholar
K. R. Dabrowski, “Ontogenetical aspects of nutritional requirements in fish,” Comparative Biochemistry and Physiology Part A: Physiology, vol. 85, no. 4, pp. 639–655, 1986.
View at: Publisher Site | Google Scholar
M. Osman, S. Fayed, G. Mahmoud, and R. Romeilah, “Protective effects of chitosan, ascorbic acid and Gymnema sylvestre against hypercholesterolemia in male rats,” Australian Journal of Basic and Applied Sciences, vol. 4, p. 89, 2009.
View at: Publisher Site | Google Scholar
R. Coz-Rakovac, I. Strunjak-Perovic, M. Hacmanjek, N. T. Popovic, Z. Lipej, and B. Sostaric, “Blood chemistry and histological properties of wild and cultured sea bass (Dicentrarchus labrax) in the North Adriatic Sea,” Veterinary Research Communications, vol. 29, no. 8, pp. 677–687, 2005.
View at: Publisher Site | Google Scholar
H. A. Taalab, E. Y. Mohammady, T. M. M. Hassan, M. M. Abdella, and M. S. Hassaan, “β-Carotene of Arthrospira platensis versus vitamin C and vitamin E as a feed supplement: effects on growth, haemato-biochemical, immune-oxidative stress and related gene expression of Nile tilapia fingerlings,” Aquaculture Research, vol. 53, no. 13, pp. 4832–4846, 2022.
View at: Publisher Site | Google Scholar
Y. Ishibashi, K. Kato, S. Ikeda, O. Murata, T. Nasu, and H. Kumai, “Effect of dietary ascorbic acid supplementation on gonadal maturation in Japanese parrot fish,” Suisanzoshoku, vol. 42, pp. 279–285, 1994.
View at: Google Scholar
T. Ren, S. Koshio, O. Uyan et al., “Effects of dietary vitamin C on blood chemistry and nonspecific immune response of juvenile red sea bream, Pagrus major,” Journal of the World Aquaculture Society, vol. 39, no. 6, pp. 797–803, 2008.
View at: Publisher Site | Google Scholar
M. S. Hossain, S. Koshio, M. Ishikawa et al., “Influence of dietary inosine and vitamin C supplementation on growth, blood chemistry, oxidative stress, innate and adaptive immune responses of red sea bream, Pagrus major juvenile,” Fish & Shellfish Immunology, vol. 82, pp. 92–100, 2018.
View at: Publisher Site | Google Scholar
C. E. Trenzado, A. E. Morales, and M. de la Higuera, “Physiological changes in rainbow trout held under crowded conditions and fed diets with different levels of vitamins E and C and highly unsaturated fatty acids (HUFA),” Aquaculture, vol. 277, no. 3-4, pp. 293–302, 2008.
View at: Publisher Site | Google Scholar
Z. H. Kashani, M. R. Imanpoor, A. Shabani, and S. Gorgin, “Effect of dietary vitamin C and highly unsaturated fatty acids on some biochemical blood parameters in goldfish (Carassius auratus gibelio),” World Journal of Fish and Marine Sciences, vol. 4, pp. 454–457, 2012.
View at: Publisher Site | Google Scholar
M. F. El Basuini, A. M. El-Hais, M. A. O. Dawood et al., “Effects of dietary copper nanoparticles and vitamin C supplementations on growth performance, immune response and stress resistance of red sea bream, Pagrus major,” Aquaculture Nutrition, vol. 23, no. 6, pp. 1329–1340, 2017.
View at: Publisher Site | Google Scholar
H. Hemilä, “Vitamin C and plasma cholesterol,” Critical Reviews in Food Science and Nutrition, vol. 32, no. 1, pp. 33–57, 1992.
View at: Publisher Site | Google Scholar
T. Finkel and N. J. Holbrook, “Oxidants, oxidative stress and the biology of ageing,” Nature, vol. 408, no. 6809, pp. 239–247, 2000.
View at: Publisher Site | Google Scholar
R. Kohen and A. Nyska, “Invited review: oxidation of biological systems: oxidative stress phenomena, antioxidants, redox reactions, and methods for their quantification,” Toxicologic Pathology, vol. 30, no. 6, pp. 620–650, 2002.
View at: Publisher Site | Google Scholar
R. Castro and C. Tafalla, “2 - Overview of fish immunity,” in Mucosal Health in Aquaculture, B. H. Beck and E. Peatman, Eds., pp. 3–54, Academic Press, USA, 2015.
View at: Publisher Site | Google Scholar
H. Esterbauer, “Cytotoxicity and genotoxicity of lipid-oxidation products,” The American Journal of Clinical Nutrition, vol. 57, no. 5, pp. 779S–786S, 1993.
View at: Publisher Site | Google Scholar
B. A. Freeman and J. D. Crapo, “Biology of disease: free radicals and tissue injury,” Laboratory Investigation, vol. 47, no. 5, pp. 412–426, 1982.
View at: Google Scholar
H. Sies, “Oxidative stress: oxidants and antioxidants,” Experimental Physiology, vol. 82, no. 2, pp. 291–295, 1997.
View at: Publisher Site | Google Scholar
L. T. Chien and D. F. Hwang, “Effects of thermal stress and vitamin C on lipid peroxidation and fatty acid composition in the liver of thornfish Terapon jarbua,” Comparative Biochemistry and Physiology Part B: Biochemistry and Molecular Biology, vol. 128, no. 1, pp. 91–97, 2001.
View at: Publisher Site | Google Scholar
Z. Liu, P. Yu, M. Cai et al., “Effects of microplastics on the innate immunity and intestinal microflora of juvenile Eriocheir sinensis,” Science of the Total Environment, vol. 685, pp. 836–846, 2019.
View at: Publisher Site | Google Scholar
F. Huang, M. Jiang, H. Wen et al., “Dietary vitamin C requirement of genetically improved farmed tilapia, Oreochromis Niloticus,” Aquaculture Research, vol. 47, no. 3, pp. 689–697, 2016.
View at: Publisher Site | Google Scholar
R. S. Verma, A. Mhta, and N. Srivastava, “In vivo chlorpyrifos induced oxidative stress: attenuation by antioxidant vitamins,” Pesticide Biochemistry and Physiology, vol. 88, no. 2, pp. 191–196, 2007.
View at: Publisher Site | Google Scholar
F. E. Pehlivan, “Vitamin C: an antioxidant agent,” in Vitamin C. Chapter 2, pp. 23–35, 2017.
View at: Publisher Site | Google Scholar
A. Hadi, A. Shokr, and S. Alwan, “Effects of aluminum on the biochemical parameters of fresh water fish Tilapia zillii,” Journal of Applied Polymer Science, vol. 3, pp. 33–41, 2009.
View at: Google Scholar
S. R. Verma, S. Rani, and R. C. Dalela, “Isolated and combined effects of pesticides on serum transaminases in Mystus vittatus (African catfish),” Toxicology Letters, vol. 8, no. 1-2, pp. 67–71, 1981.
View at: Publisher Site | Google Scholar
R. Wells, R. McIntyre, A. Morgan, and P. Davie, “Physiological stress responses in big gamefish after capture: observations on plasma chemistry and blood factors,” Comparative Biochemistry and Physiology Part A: Physiology, vol. 84, no. 3, pp. 565–571, 1986.
View at: Publisher Site | Google Scholar
C. Navarro, P. Montilla, A. Martin, J. Jimenez, and P. Utrilla, “Free radical scavenger and antihepatotoxic activity ofRosmarinus tomentosus,” Planta Medica, vol. 59, no. 4, pp. 312–314, 1993.
View at: Publisher Site | Google Scholar
N. Daniel, A. P. Muralidhar, P. P. Srivastava et al., “Dietary ascorbic acid requirement for growth of striped catfish, Pangasianodon hypophthalmus (Sauvage, 1878) juveniles,” Aquaculture Nutrition, vol. 24, no. 1, pp. 616–624, 2018.
View at: Publisher Site | Google Scholar

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