1. Introduction
Over the past few decades, the aquaculture industry has played an even more crucial role in alleviating global hunger, malnutrition, and poverty [1]. Nevertheless, against the backdrop of the ongoing stagnation of world capture fisheries production, the aquaculture industry is confronted with unprecedented growth challenges in response to the considerable increase in per capita consumption of aquatic animal food resulting from rapid population growth [2]. As one of the most relied-on protein sources for aquaculture production, the disparity between the demand and supply sides of fish meal is widening, causing its price escalation, and the search for novel animal or plant protein sources has emerged as the primary research direction of the aquatic feed sector [3].
Recently, there has been pronounced interest in nascent protein sources such as terrestrial animal derivatives, bacteria, yeast, and fermenting plants, especially the latter, whose superiority in terms of price and yield has elicited extensive scholarly attention [4,5]. Soybean meal (SO) is extensively utilized in aquatic animal feed for its high protein content, balanced amino acid composition, and high digestibility [6,7]. Nevertheless, it is noteworthy that soybeans and soybean processing byproducts (SO and soybean oil) are also significant food sources for humans. With the continuous increase in the price of SO, the supply conflict between the human food sector and farmed animals is growing increasingly acute; thus, the large-scale utilization of SO as a protein source in aquatic feed is no longer feasible [8,9].
Rapeseed/canola, a byproduct of rapeseed after the oil extraction process and mainly produced in the European Union, Canada, China, and India, had a production exceeding 88 million tons in 2023, making it the second largest oilseed crop in the world [10]. The production cost of rapeseed is among the lowest of the commonly utilized plant protein sources in aquatic feed [11]. However, rapeseed meal (RM) incorporates multiple anti-nutritional constituents such as glucosinolates (GS), tannin (TA), and phytic Acid (PA), along with crude fiber (CF), which can evoke toxic responses in fish, engendering swelling and impairment to the liver and potentially culminating in mortality [12,13]. In recent years, the role of fermentation technology in resolving the predicaments of elevated anti-nutritional factor content, suboptimal nutrient utilization, and microbial contamination of animal and plant raw materials has attracted widespread scholarly attention [14]. Microbial fermentation is a procedure that utilizes beneficial microorganisms (such as Bacillus, lactic acid bacteria, yeast, etc.) to diminish the content of anti-nutritional factors in feed ingredients and augment palatability and utilization rate under opportune conditions through specific metabolic routes. The synergy between bacteria and enzymes can escalate the content of nutrients such as macromolecular proteins, amino acids, mineral elements, and small peptides with specific functionalities in feed [8]. Nonetheless, the detoxification efficacy of fermentation is not consummated, and the supplementation of elevated levels of fermented raw materials in feed leads to growth retardation and sub-optimal health status in fish [5,15]. In RM, thioglucoside and its decomposition products, such as thiocyanate and oxazolidinthione, these goitrogens will preferentially combine with iodine in the blood, resulting in insufficient iodine sources required for thyroxine synthesis and inhibiting the combination of diiodothyronine (T2) from forming thyroxine (T4), thereby causing compensatory hyperplasia and swelling of the thyroid gland and interfering with thyroid metabolism [11,16]. Therefore, we hypothesized that the supplementation of iodine in feed could augment the iodine concentration in fish to alleviate the competitive pressure exerted by glucosinolate and its decomposition products on iodine and, thereby, counteract its adverse effects. In previous studies, dietary iodine supplementation had inconsistent effects on the growth and health of farmed animals, and the main studies focused on the larval stage: dietary 2.5% Saccharina japonica meal (rich in iodine) is beneficial to the growth of juvenile black sea bream (Acanthopagrus schlegelii), and the iodine content in the fillets increases by 5 times [17]. However, the supplementation of 72 mg kg−1 KI in the RM diet exerted no significant effects on the growth performance, feed intake, nitrogen and fat retention, and feed utilization of yellow catfish (Tachysurus fulvidraco) [18]. The same results were found in gilthead seabream [19]. The iodine requirements of the majority of fish species remain, hitherto, undefined, and our supposition requires further validation on account of the extensive disparity in physiological and metabolic conditions among species.
Tilapia (Oreochromis niloticus), a typical herbivorous fish, constitutes one of the most productive farmed fish species worldwide [20]. In actual production circumstances, fish meal is commonly not incorporated into the commercial feed of tilapia, and the predominant vegetable protein source is SO, with an inclusion ratio spanning from 20 to 40% [21]. The utilization of more economical meals from plant sources to substitute for SO represents one of the efficacious measures to further curtail feed costs. The objective of this study was to explore whether iodine can efficaciously alleviate the adverse effects of anti-nutritional factors in fermented rapeseed meal (FRM) on tilapia and its influences on the growth, antioxidant status, and liver health of tilapia.
2. Materials and Methods
2.1. Animal Ethics Statement
All experimental protocols in this study were reviewed following animal care protocols approved by the Animal Welfare Committee of Yangtze River Fisheries Research Institute, Chinese Academy of Fishery Sciences (Approval Code, YFI2022JM02).
2.2. Experimental Diets
RM for the current experiment was obtained from COFCO Grain and Oil Industry Co., LTD (Guangzhou, China). The RM was processed for solid-state fermentation using the mixed bacterial solution consisting of Rhodotorula rubra, Lactococcus lactis, and Aspergillus niger, along with 2000 U/g cellulase. R. rubra, L. lactis, and A. niger were supplied by Hubei Biopesticide Engineering Research Center, and the cellulase was acquired from Nanjing Jiancheng Biology Co., LTD (Nanjing, China). Soybean meal, FRM, and cottonseed meal were included in all diets to serve as a protein source, while corn oil and soybean oil were supplied as lipid sources, and wheat flour was used as a nitrogen-free extract source. Six isonitrogenous and isolipidic diets (about 33% crude protein and 8% crude lipid) from a two-factorial design of 2 × 3 were formulated with three levels of dietary FRM (25.8% and 51.6%) and two levels of potassium iodide (0 mg/kg, 6 mg/kg and 12 mg/kg), respectively. Ingredients and proximate compositions of experimental diets are presented in Table 1, and the amino acid profiles in the diets are displayed in Table 2.
All dry ingredients are passed through a 60-mesh sieve and then thoroughly homogenized in a blender, subsequently followed by including oil and water. The F-26 double-screw pelleting machine (The South China University of Technology Science and Technology Industrial Co., LTD, Guangzhou, China) was utilized to manufacture feed pellets, and a caterpillar feed dryer (Changzhou Suzheng Drying Equipment Co., LTD, Changzhou, China) was used for air drying. Finally, the dry diets were placed in a ziplock bag and then stored at −20 °C until used.
2.3. Fish and Feeding Trial
Genetically improved farmed tilapia (GIFT) were provided by the Fisheries Research Institute of Wuhan Academy of Agricultural Sciences. The fish were acclimated to laboratory conditions for 2 weeks, and then a total of 360 fish (initial body weight: 3.50 ± 0.15 g) were randomly assigned to 18 tanks (400 L, diameter 85 cm and depth 70 cm), with 20 fish per tank. Three replication tanks were fed with each diet. Fish were hand-fed three times a day at 08:30, 12:30, and 17:00. Throughout the entire test period, the food intake was adjusted in accordance with the size of the fish body, feeding desire, water temperature, and other conditions, and it was 3–10%. Daily records were maintained regarding water temperature, feeding behaviors, and mortality. One-third of the water was replaced daily. The feeding trial lasted for 8 weeks. During the culture period, the water temperature ranged between 25 and 28 °C; the dissolved oxygen concentration exceeded 5 mg/L; the pH was within the range of 6.8–7.3, and the ammonia nitrogen concentration was beneath 0.05 mg/L.
2.4. Sample Collection
After a 56-day feeding period, the fish were fasted for 24 h and subsequently anesthetized with MS-222 (tricaine methane sulfonate, Sigma Aldrich, St. Louis, MO, USA), then weighed and counted. Blood was collected from the tail veins of six randomly chosen fish from each tank, using a 1 mL disposable sterile syringe, and after being left to stand at 4 °C for 4 h, the serum was centrifuged at 4000 rpm for 10 min and stored at −80 °C. Subsequently, the visceral mass and liver were promptly extracted on the ice, while the visceral mass and liver underwent weighing to calculate the viscerosomatic and hepatosomatic indexes, respectively. Then, a portion of the liver and midgut tissues were fixed with a 4% paraformaldehyde solution for histomorphological observation. The remaining liver tissue was stored at −40 °C until the antioxidant indices were determined. Another three fish were taken from each tank to determine the whole-body composition.
2.5. Chemical Composition and Anti-Nutritional Factors Analysis Methods
The contents of crude protein and lipids in diet and tissues were determined via Kjeldahl nitrogen determination and Soxhlet extraction [22]. An automatic amino acid detector (L-8900, Hitachi, Tokyo, Japan) was employed to detect the content of hydrolyzed amino acids in feed. The contents of tannin and phytic acid in feed were assayed using kits produced by Suzhou Comin Biotechnology Co., LTD. (Suzhou, China), numbered DN-2-Y and SAP-2-Y, respectively. The content of crude fiber was determined by the filter bag method. According to the method described by Wang [23], the content of glucosinolate in the diet was determined by the palladium chloride method.
2.6. Serum Biochemical Analysis
Serum biochemical parameters (Glucose (GLU), total cholesterol (T-CHO), triglyceride (TG), total protein (TP), total bilirubin (T-Bil), and albumin (ALB)) were assessed using an automated biochemical analyzer (BX-3010, Sysmex Corporation, Tokyo, Japan). Serum aspartate aminotransferase (AST), alanine aminotransferase (ALT), and alkaline phosphatase (ALP) were determined, respectively, by the LDH-UV method, the MDH-UV method, and the NPP-AMP method. The serum total triiodothyronine (T3) and total thyroxine (T4) were determined by the kit from Nanjing Jiancheng Bioengineering Institute (Nanjing, China).
2.7. Antioxidant Index Analysis
Antioxidant indices, namely, malondialdehyde (MDA), total superoxide dismutase (T-SOD), total antioxidant capacity (T-AOC), catalase (CAT), and total protein (TP) in the liver, were assessed through the kit (Nanjing Institute of Biological Engineering, Nanjing, China) with 10% liver homogenate (liver: normal saline (NS) = 1:9; w/v).
2.8. Histological Analysis
The procedures of histological analysis of the liver and intestine were referred to the previous procedure in our laboratory [24]. Number of cell nuclei in liver was measured using (National Institutes of Health, Bethesda, MD, USA).
2.9. Statistical Analysis
All data analyses were conducted using R packages (version 1.2.5019). Before the statistical analysis, the data were examined for homogeneity of variances. Two-way ANOVA was employed to analyze the individual effects of dietary FRM and iodine, as well as the interaction between them. When overall differences were identified, differences between means were examined by Tukey’s multiple range test. The results were presented as the mean ± standard deviation (n = 3), and p < 0.05 indicated a significant difference.
3. Results
3.1. Growth Performance
At the end of the feeding trial, there were no significant differences in SR among fish fed all diets; survival percentage varied from 96 to 99% (Table 3). FRM and iodine levels had significant effects on FBW, WG, SGR, and FI of tilapia (p < 0.05), and there were significant interactions between FRM and iodine levels on these indexes (p < 0.05). The increased level of FRM significantly reduced the WG and SGR of tilapia (p < 0.05). Around 6–12 mg/kg iodine inclusion in a high FRM level diet (51.6%) significantly increased the WG of tilapia compared with the D4 group (p < 0.05). Moreover, FRM and iodine levels significantly affected HSI and VSI of tilapia (p < 0.05), but there was no significant interaction effect (p > 0.05).
3.2. Proximate Composition
FRM levels had no significant effects on the approximate compositions of whole fish and muscle of tilapia (p > 0.05) (Table 4). Dietary iodine levels had significant effects on the crude protein content of whole fish and the crude lipid content of muscle (p < 0.05). High FRM level (51.6%) supplemented with 6–12 mg/kg iodine significantly increased the crude protein content of tilapia whole fish (p < 0.05). Dietary iodine level significantly increased the level of crude lipid in muscle under different concentrations of FRM (p < 0.05). Different levels of FRM and potassium iodide had significant interaction on the crude protein level of whole fish but had no interaction on other basic compositions of whole fish and muscle (p > 0.05).
3.3. Serum Biochemical Parameters
FRM levels had significant effects on the contents of T-Bil, TG, T3, and T4 in serum and the activities of ALP and AST in tilapia (p < 0.05) (Table 5). Dietary iodine level had significant effects on the contents of ALB, T-Bil, TG, T3, and T4 and the activities of ALP, AST, and ALT in tilapia serum (p < 0.05). Dietary 12 mg/kg iodine significantly increased the serum ALB content of tilapia compared with the D2 group (p < 0.05). The content of T-Bil and the activities of AST and ALT in the serum of tilapia were significantly decreased by adding 6–12 mg/kg iodine at high FRM level (51.6%) (p < 0.05), and the content of T3 in serum was significantly increased by 12 mg/kg iodine inclusion (p < 0.05). A two-factor analysis was conducted on the effects of the level of FRM and iodine, and the results showed that the two had significant interaction effects on the contents of T-Bil, T3, T4, T-CHO, and TG and AST activities in the serum of tilapia (p < 0.05).
3.4. Antioxidant Capacity
No significant differences were observed in contents TP between dietary FRM and iodine (p > 0.05) (Table 6). T-AOC activity was enhanced by supplementation of iodine regardless of the dietary FRM levels (p < 0.05). Supplementation of 6–12 mg/kg iodine with a high FRM diet (51.6%) significantly increased the activities of CAT and T-AOC and decreased the content of MDA in the liver of tilapia (p < 0.05). Different levels of FRM and potassium iodide exerted significant interactive effects on the activities of T-SOD, CAT, and T-AOC and the content of MDA in the liver of tilapia (p < 0.05).
3.5. Liver Histology
As illustrated in Figure 1, the liver cell structure was further ameliorated in each iodine treatment group. This was evidenced by the attenuation of hepatic nuclear migration and vacuolation, and the tilapia liver health status was conspicuously enhanced. Dietary FRM and iodine significantly affected the number of hepatocyte cell nuclei in the H&E staining of tilapia (p < 0.05) (Figure 2).
4. Discussion
The anti-nutritional factors in FRM can lead to the growth retardation of aquatic animals. To avoid these issues, this study evaluated the interaction between iodine and FRM levels on the growth and health of tilapia through a two-factorial design experiment.
In the present study, high levels of FRM (D4) conspicuously hindered the growth of tilapia, which is consistent with the previous research results in tilapia, Asian red-tailed catfish (Hemibagrus wyckioides), and Asian seabass (Lates calcarifer) [25,26,27]. This adverse effect on growth can be attributed in part to anti-nutritional factors such as phytic acid and glucosinolate. Surprisingly, at high FRM levels (51.6%), 6–12 mg/kg iodine inclusion in the diet significantly enhanced the WG and SGR of tilapia. This indicates that dietary iodine can mitigate the adverse growth effects of increasing the content of FRM in the diet. Iodine is an indispensable trace element for the organism and an essential nutrient element for thyroid hormone synthesis, which is vital for maintaining thyroid function and the normal growth and development of the body [28]. Thyroid hormones are synthesized under the facilitation of iodine, which, in turn, promotes bone development and protein synthesis and raises the basal metabolic rate [29]. This study also affirmed that an appropriate iodine intake can efficaciously facilitate the growth of tilapia. The information regarding the effects of iodine on fish growth is limited, and the main studies have focused on terrestrial animals; for instance, Ludke et al. discovered that supplementing 1 mg/kg iodine to RM diet significantly increased the WG and FI and decreased the FCR in pigs [30]. Similarly, Maroufyan et al. found that adding an appropriate amount of iodine to the feed containing RM could alleviate the adverse effects of anti-nutrient factors in RM on the growth performance and feed utilization rate of broiler chickens to a certain extent, and the improvement effect was more pronounced as dietary iodine increased [31]. Pattanaik et al. found in the experiments of goats and rams that supplementing 0.075 mg and 0.1 mg of iodine per day could effectively promote their growth rate [32]. Furthermore, the augmented content of FRM in the diet reduced the FI of tilapia. This could be thoroughly elucidated by the existence of glucosides, tannins, and phytic acids, particularly glucosides, which can generate numerous active substances such as thiocyanate, isothiocyanate, and nitrile compounds upon hydrolysis, exerting detrimental effects on the palatability of the feed and diminishing the appetite and intake of animals [33]. This is consistent with results in grass carp (Ctenopharyngodon idellus), rainbow trout, and yellow catfish; high RM in diet sacrificed feed intake [18,34,35]. Interestingly, tilapia significantly augmented their FI after dietary iodine supplementation. There are limited reports regarding the effects of iodine on food intake and appetite in fish, and further studies are requisite to draw conclusions.
Dietary FRM did not exert any significant influence on the proximate composition of the whole fish and the muscle of tilapia. A comparable result was noted in gibel carp (Carassius auratus gibelio var. CAS V), where the incorporation of fermented plant meal within the diet failed to modify the proximate composition of the fish [4]. Supplying 6–12 mg/kg KI to the diet significantly elevated the crude protein content in whole fish and the lipid content in muscle, indicating that iodine might have enhanced the utilization of protein and lipids in the diet by tilapia. Nevertheless, there is limited information regarding the impacts of iodine on protein and lipid metabolism in fish.
Serum biochemical parameters are key indicators for evaluating the nutrition, metabolism, and physiological status of fish [5]. AST and ALT are mainly found in the mitochondria and cytoplasm of liver cells. When the liver is severely damaged, these enzymes are released into the bloodstream, causing a significant increase in enzyme activity in the serum and also serving as an indicator of liver damage [36]. Tilapia serum AST and ALT activities were significantly enhanced after high levels of FRM were substituted for SO, suggesting that excess FRM in the diet might still have adverse effects on liver health. Nevertheless, the supplementation of 6–12 mg/kg iodine in diets featuring high levels of FRM (51.6%) significantly decreased the serum T-Bil content as well as the activities of AST and ALT in tilapia. On the contrary, at the dietary level of 25.8% FRM, iodine failed to significantly improve the liver health of tilapia, which may be related to the diverse adaptability of tilapia to different concentrations of FRM. Triiodothyronine (T3), an active form of thyroid hormone, is transported to various tissues and cells across the body through the bloodstream, binds to thyroid hormone receptors within cells, activates a succession of signaling pathways, and governs cell metabolism, growth, and differentiation [28]. Under normal conditions, T3 and T4 maintain a specific equilibrium relationship to uphold normal physiological functions [18]. In the present study, serum T3 levels were conspicuously elevated after dietary iodine supplementation, suggesting that tilapia could have efficiently utilized dietary iodine for the synthesis of thyroid hormones, counteracting the detrimental effects of glucosinone on thyroid function in tilapia and, thereby, facilitating its growth.
Cells generate reactive oxygen species during normal metabolism, while the cell’s antioxidant defense system is accountable for eliminating excessive oxygen free radicals from the body, maintaining a dynamic equilibrium between the two. When there is an excess of free radicals in the body, they inflict damage on normal cells and tissues [24]. Superoxide dismutase and catalase are indispensable antioxidant enzymes within the organism, whose primary function is to eradicate and disintegrate excessive free radicals within the organism [37]. MDA content can reflect the degree of lipid peroxidation or tissue damage in the body, and its level also indirectly indicates the severity of free radical attack on the body [38]. In the current study, high levels of dietary FRM significantly augmented the MDA content in the liver, suggesting a possible risk of lipid peroxidation in the liver. Nevertheless, supplementation of 6–12 mg/kg iodine in diets with a high FRM level (51.6%) significantly enhanced the activities of T-SOD, CAT, and T-AOC in the liver and reduced the content of MDA. These results suggest that appropriate iodine supplementation in the FRM diet can effectively alleviate the adverse effects of anti-nutritional factors in FRM on the antioxidant status of the liver and subsequently improve the liver health status of tilapia, which was also confirmed by liver morphology.
5. Conclusions
In conclusion, the increase in the dietary level of FRM limited the growth performance of tilapia, but dietary iodine supplementation markedly mitigated the adverse effects of anti-nutrient factors in FRM, particularly when the high level of FRM diet included 6–12 mg KI, and the growth performance of tilapia was not substandard to that of the low-FRM treatment. Significant interactions were observed between the effects of dietary FRM level and iodide on growth performance and antioxidant capacity but not between the effects of both variables on body composition. Up to 20% of SO in the tilapia diet can be substituted by FRM, provided that 6–12 mg/kg iodine is supplemented to the diet, and this substitution level has no significant adverse impact on the growth, liver health, and antioxidant capacity of tilapia.
Feeding management, data curation, and writing—original draft preparation, D.P., J.-M.Z., Y.-Y.L. and K.C.; methodology, data curation, Y.-X.L. and L.-X.D.; investigation, resources, M.-D.L. and W.-H.G.; microbial strains required for testing, Y.M.; supervision and project administration, M.J., H.W. and J.T. All authors have read and agreed to the published version of the manuscript.
This study was conducted in accordance with the Animal Experimental Ethical Inspection of Laboratory Animal Centre and approved by the Yangtze River Fisheries Research Institute, Chinese Academy of Fishery Sciences (Permit Number: YFI2022JM02).
Not applicable.
The original contributions presented in this study are included in the Materials.
The authors declare no conflicts of interest.
Footnotes
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Enlarge this image.Figure 1. Effects of different levels of fermented rapeseed meal and potassium iodide on liver tissue morphology of tilapia. Note: NC: nuclear migration; AB: cavitation; Q: nuclear dissolution.
![View Image - Figure 2. Effects of different levels of fermented rapeseed meal and potassium iodide on hepatocyte nucleus. Note: Values represent means ± SD. Different letters in the same row indicated statistically significant differences (p [less than] 0.05).](https://media.proquest.com/media/hms/THUM/4/kOZ2b?_a=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%2BgIBWYIDA1dlYooDHENJRDoyMDI1MDgwMzE1MzcxMTYzMDo0Njk0MDk%3D&_s=kkcIEFkzi4g601WnqSshz4RN%2BPM%3D "View Image - Figure 2. Effects of different levels of fermented rapeseed meal and potassium iodide on hepatocyte nucleus. Note: Values represent means ± SD. Different letters in the same row indicated statistically significant differences (p [less than] 0.05).")
Enlarge this image.Figure 2. Effects of different levels of fermented rapeseed meal and potassium iodide on hepatocyte nucleus. Note: Values represent means ± SD. Different letters in the same row indicated statistically significant differences (p [less than] 0.05).
Feed formula, nutrient composition, and anti-nutrient factor contents.
| Ingredients | D2 | D2-6 | D2-12 | D4 | D4-6 | D4-12 |
|---|---|---|---|---|---|---|
| Soybean meal | 20 | 20 | 20 | 0 | 0 | 0 |
| Fermented rapeseed meal | 25.8 | 25.8 | 25.8 | 51.6 | 51.6 | 51.6 |
| Cotton meal | 10 | 10 | 10 | 10 | 10 | 10 |
| Wheat flour | 19.85 | 19.85 | 19.85 | 19.85 | 19.85 | 19.85 |
| Corn protein meal | 5 | 5 | 5 | 5 | 5 | 5 |
| Fish meal | 3 | 3 | 3 | 3 | 3 | 3 |
| Soybean oil | 2.5 | 2.5 | 2.5 | 2.5 | 2.5 | 2.5 |
| Corn oil | 2.5 | 2.5 | 2.5 | 2.5 | 2.5 | 2.5 |
| Amargosite | 1 | 1 | 1 | 1 | 1 | 1 |
| Ca(H2PO4)2 | 2 | 2 | 2 | 2 | 2 | 2 |
| Choline chloride | 0.25 | 0.25 | 0.25 | 0.25 | 0.25 | 0.25 |
| Mineral premix 1 (without iodine) | 1 | 1 | 1 | 1 | 1 | 1 |
| Vitamin premix 2 | 1 | 1 | 1 | 1 | 1 | 1 |
| Cellulose | 6.1 | 6.1 | 6.1 | 0.3 | 0.3 | 0.3 |
| Total | 100 | 100 | 100 | 100 | 100 | 100 |
| Potassium iodide (mg/kg) | 0 | 6 | 12 | 0 | 6 | 12 |
| Proximate composition (%, by dry matter content) | ||||||
| Crude protein | 33.32 | 33.34 | 33.32 | 33.38 | 33.39 | 33.33 |
| Crude lipid | 8.28 | 8.32 | 8.12 | 8.28 | 8.12 | 8.23 |
| Ash | 7.86 | 7.85 | 7.80 | 7.94 | 7.92 | 7.95 |
| Crude fiber | 5.30 | 5.30 | 5.29 | 5.92 | 5.90 | 5.89 |
| Gross energy (KJ/g) | 19.28 | 19.07 | 19.10 | 19.38 | 19.11 | 19.15 |
| Anti-nutrient factor (%, by dry matter content) | ||||||
| Phytic Acid | 1.69 | 1.67 | 1.68 | 2.45 | 2.44 | 2.44 |
| Tannin | 0.26 | 0.25 | 0.26 | 0.34 | 0.33 | 0.34 |
| Glucosinolates (μmol/g) | 3.05 | 3.01 | 3.02 | 5.85 | 5.85 | 5.76 |
Note: 1. Each kilogram of vitamin premix contains the following: vitamin A (500,000 IU/g), 0.8 g; vitamin D3, 0.08 g; vitamin E, 20 g; vitamin K3, 18.6 g; vitamin B1, thiamine hydrochloride, 10 g; riboflavin B2, 12.5 g; pyridoxine B6, 8 g; L-ascorbic acid, 400 mg; calcium pantothenate B5, 20 g; folic acid, 3.2 g; biotin, 3 g; inositol, 406 g; niacin, 12 g. 2. Each kilogram of mineral premix contains the following: calcium lactate, 500 g; sodium dihydrogen phosphate, 100 g; ferrous sulfate, 20 g; sodium chloride, 20 g; anhydrous magnesium sulfate, 100 g; aluminum chloride, 0.6 g; zinc sulfate, 20 g; manganese sulfate, 4 g; copper sulfate, 2 g; potassium chloride, 40 g; cobalt chloride, 2 g; potassium iodate, 0.6 g; sodium selenite, 0.004 g.
Amino acid composition of diet.
| Item | D2 | D2-6 | D2-12 | D4 | D4-6 | D4-12 |
|---|---|---|---|---|---|---|
| EAA | ||||||
| Arginine | 1.71 | 1.59 | 1.53 | 1.51 | 1.49 | 1.49 |
| Histidine | 0.53 | 0.49 | 0.45 | 0.47 | 0.46 | 0.47 |
| Isoleucine | 1.26 | 1.20 | 1.15 | 1.07 | 1.14 | 1.16 |
| Leucine | 2.51 | 2.40 | 2.28 | 2.17 | 2.22 | 2.25 |
| Lysine | 1.19 | 1.11 | 1.00 | 0.94 | 0.92 | 0.97 |
| Methionine | 0.25 | 0.25 | 0.27 | 0.24 | 0.32 | 0.39 |
| Phenylalanine | 1.10 | 1.05 | 0.99 | 0.94 | 0.95 | 0.96 |
| Threonine | 0.89 | 0.85 | 0.80 | 0.78 | 0.80 | 0.82 |
| Valine | 1.15 | 1.09 | 1.04 | 1.02 | 1.07 | 1.07 |
| NEAA | ||||||
| Alanine | 1.45 | 1.40 | 1.33 | 1.31 | 1.35 | 1.35 |
| Aspartic acid | 2.17 | 1.98 | 1.97 | 1.45 | 1.46 | 1.51 |
| Cysteine | 0.37 | 0.28 | 0.28 | 0.36 | 0.34 | 0.32 |
| Glycine | 1.12 | 1.07 | 1.01 | 1.06 | 1.09 | 1.10 |
| Glutamate | 5.77 | 5.55 | 5.20 | 5.40 | 5.15 | 5.20 |
| Proline | 2.46 | 2.42 | 2.32 | 2.44 | 2.35 | 2.32 |
| Serine | 1.06 | 1.01 | 0.96 | 0.90 | 0.89 | 0.91 |
| Tyrosine | 0.88 | 0.86 | 0.84 | 0.80 | 0.82 | 0.83 |
| ΣEAA | 10.57 | 10.02 | 9.52 | 9.13 | 9.37 | 9.58 |
| ΣNEAA | 15.28 | 14.57 | 13.92 | 13.72 | 13.43 | 13.54 |
| ΣTAA | 25.85 | 24.59 | 23.44 | 22.85 | 22.80 | 23.12 |
Effects of fermented rapeseed meal and potassium iodide levels on growth performance of tilapia.
| Item | 25.8% | 51.6% | p-Value | ||||||
|---|---|---|---|---|---|---|---|---|---|
| D2 | D2-6 | D2-12 | D4 | D4-6 | D4-12 | FRM | Iodine | FRM * | |
| IBW (g) | 3.51 ± 0.01 | 3.52 ± 0.01 | 3.51 ± 0.02 | 3.52 ± 0.03 | 3.49 ± 0.05 | 3.53 ± 0.02 | 0.674 | 0.320 | 0.145 |
| FBW (g) | 32.77 ± 0.14 b | 34.71 ± 0.34 c | 34.27 ± 3.05 c | 27.90 ± 0.43 a | 33.03 ± 0.22 b | 33.49 ± 0.35 ab | <0.001 | <0.001 | <0.001 |
| SR (%) | 98.33 ± 2.89 | 98.33 ± 2.89 | 98.33 ± 2.89 | 98.33 ± 2.89 | 96.67 ± 2.89 | 98.33 ± 2.89 | 0.690 | 0.848 | 0.848 |
| WG (%) | 848.56 ± 48.56 b | 885.88 ± 6.91 b | 889.69 ± 22.63 b | 692.57 ± 82.54 a | 848.33 ± 5.83 b | 847.79 ± 13.9 b | 0.002 | 0.002 | 0.045 |
| SGR (%/d) | 6.11 ± 0.18 b | 6.14 ± 0.02 b | 6.14 ± 0.05 b | 5.73 ± 0.12 a | 6.05 ± 0.01 b | 6.07 ± 0.02 b | 0.001 | 0.007 | 0.020 |
| FI (g/fish) | 35.09 ± 1.95 b | 38.45 ± 1.01 c | 39.46 ± 0.87 c | 31.18 ± 0.73 a | 38.41 ± 0.42 c | 38.98 ± 0.36 c | 0.011 | <0.001 | 0.014 |
| FCR | 1.14 ± 0.07 | 1.23 ± 0.03 | 1.26 ± 0.02 | 1.29 ± 0.15 | 1.30 ± 0.01 | 1.30 ± 0.03 | 0.027 | 0.283 | 0.404 |
| HSI (%) | 2.48 ± 0.05 ab | 2.09 ± 0.32 a | 2.46 ± 0.18 ab | 3.15 ± 0.16 c | 2.74 ± 0.14 bc | 2.61 ± 0.30 abc | <0.001 | 0.021 | 0.095 |
| VSI (%) | 12.46 ± 0.27 bc | 11.45 ± 0.53 ab | 11.00 ± 0.54 a | 13.25 ± 0.04 c | 12.20 ± 0.60 bc | 12.19 ± 0.32 abc | 0.001 | 0.001 | 0.643 |
Note: Values represent means ± SD. Different letters in the same row indicate statistically significant differences (p < 0.05). Survival rate (SR) = 100 × final fish number/initial fish number; weight gain (WG) = 100 × (final weight–initial weight)/initial weight; feed efficiency ratio (FCR) = wet weight gain/(final weight–initial weight); feed intake (FI) = feed consumed in dry matter/number of fish; specific growth rate (SGR) = 100 × [ln(final weight) – ln (initial weight)]/duration of feeding trial; hepatosomatic index (HSI) = 100 × liver weight/bodyweight; viscerosomatic index (VSI) = 100 × viscera weight/body weight; FRM * Iodine, Interaction between dietary iodine and FRM levels.
Effects of fermented rapeseed meal and potassium iodide levels on proximate composition of tilapia.
| Item | 25.8% | 51.6% | p-Value | ||||||
|---|---|---|---|---|---|---|---|---|---|
| D2 | D2-6 | D2-12 | D4 | D4-6 | D4-12 | FRM | Iodine | FRM * | |
| Whole fish | |||||||||
| Moisture | 66.31 ± 2.66 | 64.43 ± 1.57 | 65.35 ± 3.99 | 68.26 ± 1.26 | 63.75 ± 2.05 | 65.43 ± 1.54 | 0.949 | 0.013 | 0.847 |
| Crude protein | 15.79 ± 1.23 a | 16.11 ± 0.62 ab | 17.14 ± 0.63 b | 15.26 ± 0.90 a | 17.28 ± 0.10 b | 16.89 ± 0.11 b | 0.363 | <0.001 | 0.016 |
| Crude lipid | 10.62 ± 0.32 | 10.50 ± 0.22 | 10.21 ± 0.14 | 10.55 ± 0.18 | 10.46 ± 0.41 | 10.41 ± 0.22 | 0.857 | 0.800 | 0.730 |
| Ash | 3.86 ± 0.26 | 3.58 ± 0.14 | 3.62 ± 0.14 | 3.84 ± 0.29 | 3.96 ± 0.23 | 3.80 ± 0.23 | 0.254 | 0.861 | 0.566 |
| Muscle | |||||||||
| Moisture | 67.43 ± 0.57 | 67.16 ± 2.25 | 63.71 ± 2.93 | 65.79 ± 0.68 | 68.14 ± 4.04 | 63.62 ± 1.76 | 0.949 | 0.013 | 0.847 |
| Crude protein | 25.21 ± 0.48 | 27.07 ± 0.66 | 27.54 ± 2.85 | 26.43 ± 1.08 | 27.44 ± 1.10 | 26.90 ± 0.44 | 0.642 | 0.162 | 0.521 |
| Crude lipid | 3.21 ± 0.23 a | 3.94 ± 0.11 b | 3.89 ± 0.10 b | 3.16 ± 0.27 a | 3.92 ± 0.07 b | 3.95 ± 0.02 b | 0.932 | <0.001 | 0.786 |
| Ash | 1.93 ± 0.11 | 2.22 ± 0.17 | 2.14 ± 0.15 | 2.11 ± 0.17 | 2.09 ± 0.10 | 1.99 ± 0.04 | 0.254 | 0.861 | 0.566 |
Note: Values represent means ± SD. Different letters in the same row indicated statistically significant differences (p < 0.05). FRM * Iodine, Interaction between dietary iodine and FRM levels.
Effects of fermented rapeseed meal and potassium iodide levels on serum biochemical indices of tilapia.
| Item | 25.8% | 51.6% | p-Value | ||||||
|---|---|---|---|---|---|---|---|---|---|
| D2 | D2-6 | D2-12 | D4 | D4-6 | D4-12 | FRM | Iodine | FRM * | |
| TP (g/L) | 30.39 ± 1.42 | 31.04 ± 1.24 | 31.82 ± 0.40 | 30.55 ± 0.21 | 32.57 ± 1.28 | 33.24 ± 2.13 | 0.123 | 0.056 | 0.602 |
| ALB (g/L) | 12.40 ± 0.35 a | 13.40 ± 0.46 ab | 13.47 ± 0.31 b | 12.63 ± 0.35 ab | 13.03 ± 0.45 b | 13.53 ± 0.35 b | 0.102 | 0.004 | 0.447 |
| T-CHO (mmol/L) | 4.29 ± 0.17 a | 5.32 ± 0.46 b | 5.58 ± 0.10 b | 5.31 ± 0.59 b | 5.23 ± 0.45 ab | 5.26 ± 0.29 b | 0.237 | 0.022 | 0.013 |
| T-Bil (μmol/L) | 2.34 ± 0.04 a | 2.29 ± 0.12 a | 2.58 ± 0.44 a | 4.24 ± 0.21 b | 2.52 ± 0.16 a | 2.72 ± 0.37 a | <0.001 | <0.001 | <0.001 |
| ALP (U/L) | 33.00 ± 0.75 ab | 29.73 ± 2.49 a | 29.23 ± 1.70 a | 34.47 ± 0.81 b | 32.07 ± 0.06 ab | 32.93 ± 1.85 ab | 0.004 | 0.012 | 0.460 |
| AST (U/L) | 134.30 ± 3.32 a | 126.77 ± 2.45 a | 132.43 ± 3.11 a | 205.93 ± 4.38 c | 156.87 ± 0.96 b | 154.37 ± 3.66 b | <0.001 | <0.001 | <0.001 |
| ALT (U/L) | 47.87 ± 2.46 ab | 42.37 ± 2.06 a | 42.83 ± 3.81 a | 51.37 ± 2.56 b | 45.73 ± 3.18 ab | 42.80 ± 2.17 a | 0.078 | 0.003 | 0.405 |
| TG | 4.49 ± 0.07 a | 4.35 ± 0.27 a | 4.19 ± 0.03 a | 6.44 ± 0.27 b | 4.70 ± 0.23 a | 4.32 ± 0.35 a | <0.001 | <0.001 | <0.001 |
| GLU (mmol/L) | 8.73 ± 0.31 | 7.96 ± 0.42 | 8.10 ± 0.30 | 8.34 ± 0.18 | 8.20 ± 0.59 | 7.82 ± 0.59 | 0.493 | 0.087 | 0.416 |
| T3 (ng/mL) | 0.27 ± 0.01 b | 0.31 ± 0.00 c | 0.31 ± 0.03 c | 0.21 ± 0.01 a | 0.23 ± 0.01 a | 0.27 ± 0.01 b | <0.001 | <0.001 | 0.035 |
| T4 (ng/mL) | 101.22 ± 1.19 | 110.17 ± 2.34 | 107.19 ± 5.50 | 102.52 ± 3.74 | 113.35 ± 8.95 | 105.02 ± 3.62 | <0.001 | <0.001 | 0.035 |
Note: Values represent means ± SD. Different letters in the same row indicate statistically significant differences (p < 0.05). TP, total protein; ALB, albumin; T-CHO, total cholesterol; T-Bil, total bilirubin; ALP, alkaline phosphatase; AST, aspartate aminotransferase; ALT, alanine aminotransferase; TG, triglyceride; GLU, glucose; T3, triiodothyronine; T4, total thyroxine. FRM * Iodine, Interaction between dietary iodine and FRM levels.
Effect of fermented rapeseed meal and potassium iodide levels on liver antioxidant status of tilapia.
| Item | 25.8% | 51.6% | p-Value | ||||||
|---|---|---|---|---|---|---|---|---|---|
| D2 | D2-6 | D2-12 | D4 | D4-6 | D4-12 | FRM | Iodine | FRM * | |
| T-AOC (U/mg prot) | 24.09 ± 0.87 b | 26.69 ± 0.67 c | 27.59 ± 0.03 c | 20.56 ± 0.19 a | 26.66 ± 0.97 c | 26.95 ± 0.53 c | 0.001 | <0.001 | 0.001 |
| T-SOD (U/mg prot) | 17.75 ± 1.57 ab | 17.31 ± 0.21 ab | 19.65 ± 0.80 b | 16.03 ± 0.82 a | 18.72 ± 0.66 ab | 18.83 ± 0.79 b | 0.392 | 0.003 | 0.030 |
| MDA (nmol/mg prot) | 6.29 ± 0.51 c | 5.16 ± 0.40 b | 2.91 ± 0.25 a | 10.87 ± 0.22 d | 5.13 ± 0.22 b | 4.58 ± 0.14 b | <0.001 | <0.001 | <0.001 |
| CAT (U/mg prot) | 298.78 ± 15.86 c | 294.07 ± 3.46 c | 305.10 ± 21.62 c | 186.46 ± 1.09 a | 226.17 ± 14.75 b | 226.17 ± 14.75 b | <0.001 | 0.036 | 0.043 |
| TP (g/L) | 4.31 ± 0.05 | 4.35 ± 0.19 | 4.36 ± 0.34 | 4.37 ± 0.06 | 4.72 ± 0.27 | 4.30 ± 0.10 | 0.200 | 0.173 | 0.210 |
Note: Values represent means ± SD. Different letters in the same row indicated statistically significant differences (p < 0.05). T-AOC, total antioxidant capacity; T-SOD, total superoxide dismutase; MDA, malondialdehyde; CAT, catalase; TP, total protein. FRM * Iodine, Interaction between dietary iodine and FRM levels.
References
1. Garlock, T.M.; Asche, F.; Anderson, J.L.; Eggert, H.; Anderson, T.M.; Che, B.; Chávez, C.A.; Chu, J.; Chukwuone, N.; Dey, M.M. et al. Environmental, economic, and social sustainability in aquaculture: The aquaculture performance indicators. Nat. Commun.; 2024; 20, 5274. [DOI: https://dx.doi.org/10.1038/s41467-024-49556-8] [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/38902254]
2. FAO. The State of World Fisheries and Aquaculture 2024—Blue Transformation in Action; FAO: Rome, Italy, 2024; [DOI: https://dx.doi.org/10.4060/cd0683en]
3. Chakraborty, P.; Mallik, A.; Sarang, N.; Lingam, S.S. A review on alternative plant protein sources available for future sustainable aqua feed production. Int. J. Chem. Stud.; 2019; 7, pp. 1399-1404.
4. Cao, S.; Mo, P.; Xiao, Y.B.; Chen, Y.; Shi, Y.; Hu, Y.; Tang, J.; Qu, F.; Luo, M.; Ai, X.H. et al. Dietary supplementation with fermented plant meal enhances growth, antioxidant capacity and expression of TOR signaling pathway genes in gibel carp (Carassius auratus gibelio var. CAS V). Aquac. Rep.; 2021; 19, 100559. [DOI: https://dx.doi.org/10.1016/j.aqrep.2020.100559]
5. Dossou, S.; Koshio, S.; Ishikawa, M.; Yokoyama, S.; Dawood, M.A.; El Basuini, M.F.; El-Hais, A.M.; Olivier, A. Effect of partial replacement of fish meal by fermented rapeseed meal on growth, immune response and oxidative condition of red sea bream juvenile, Pagrus major. Aquaculture; 2018; 490, pp. 228-235. [DOI: https://dx.doi.org/10.1016/j.aquaculture.2018.02.010]
6. Montoya-Camacho, N.; Marquez-Ríos, E.; Castillo-Yáñez, F.J.; Cárdenas López, J.L.; López-Elías, J.A.; Ruíz-Cruz, S.; Jiménez-Ruíz, E.I.; Rivas-Vega, M.E.; Ocaño-Higuera, V.M. Advances in the use of alternative protein sources for tilapia feeding. Rev. Aquac.; 2019; 11, pp. 515-526. [DOI: https://dx.doi.org/10.1111/raq.12243]
7. Yao, J.; Chen, P.; Ringø, E.; Zhang, G.; Huang, Z.; Hua, X. Effect of diet supplemented with rapeseed meal or hydrolysable tannins on the growth, nutrition, and intestinal microbiota in grass carp (Ctenopharyngodon idellus). Front. Nutr.; 2019; 6, 154. [DOI: https://dx.doi.org/10.3389/fnut.2019.00154]
8. Huang, H.; Liu, Y.; Zhou, H.; Lin, X.; Wang, X.; Jiang, W.; Zhang, L.; Mi, H.; Deng, J. Effects of Replacing Soybean Meal with Sunflower Meal or Fermented Sunflower Meal on the Growth Performance, Intestinal Microbiota, and Intestinal Health of Tilapia (GIFT, Oreochromis niloticus). Aquac. Nutr.; 2024; 2024, 9366952. [DOI: https://dx.doi.org/10.1155/2024/9366952]
9. Zhang, L.; Wu, H.X.; Li, W.J.; Qiao, F.; Zhang, W.B.; Du, Z.Y.; Zhang, M.L. Partial replacement of soybean meal by yellow mealworm (Tenebrio molitor) meal influences the flesh quality of Nile tilapia (Oreochromis niloticus). Anim. Nutr.; 2023; 12, pp. 108-115. [DOI: https://dx.doi.org/10.1016/j.aninu.2022.09.007]
10. USDA. World Oilseed Markets and Trade: Record Sunflower Seed Oil Trade Predicted; Foreign Agricultural Service: Washington, DC, USA, 2024.
11. Kaiser, F.; Harbach, H.; Schulz, C. Rapeseed proteins as fishmeal alternatives: A review. Rev. Aquac.; 2022; 14, pp. 1887-1911. [DOI: https://dx.doi.org/10.1111/raq.12678]
12. Danwitz, A.; Schulz, C. Effects of dietary rapeseed glucosinolates, sinapic acid and phytic acid on feed intake, growth performance and fish health in turbot (Psetta maxima L.). Aquaculture; 2020; 516, 734624. [DOI: https://dx.doi.org/10.1016/j.aquaculture.2019.734624]
13. Francis, G.; Makkar, H.P.; Becker, K. Antinutritional factors present in plant-derived alternate fish feed ingredients and their effects in fish. Aquaculture; 2001; 199, pp. 197-227. [DOI: https://dx.doi.org/10.1016/S0044-8486(01)00526-9]
14. Siddik, M.A.; Julien, B.B.; Islam, S.M.; Francis, D.S. Fermentation in aquafeed processing: Achieving sustainability in feeds for global aquaculture production. Rev. Aquac.; 2024; 16, pp. 1244-1265. [DOI: https://dx.doi.org/10.1111/raq.12894]
15. Dossou, S.; Koshio, S.; Ishikawa, M.; Yokoyama, S.; Dawood, M.A.; El Basuini, M.F.; Olivier, A.; Zaineldin, A.I. Growth performance, blood health, antioxidant status and immune response in red sea bream (Pagrus major) fed Aspergillus oryzae fermented rapeseed meal (RM-Koji). Fish Shellfish. Immunol.; 2018; 75, pp. 253-262. [DOI: https://dx.doi.org/10.1016/j.fsi.2018.01.032]
16. Mawson, R.; Heaney, R.K.; Zdunczyk, Z.; Kozlowska, H. Rapeseed meal-glucosinolates and their antinutritional effects. Part; 1994; 3, pp. 167-177.
17. Yu, C.; Liu, G.; Yu, J.; Lin, F.; Wen, X. Dietary Saccharina japonica is a natural and effective tool to fortify marine teleost black sea bream fillets with iodine: Effects on growth, flesh quality, and serum thyroid hormones. J. Appl. Phycol.; 2020; 32, pp. 3447-3456. [DOI: https://dx.doi.org/10.1007/s10811-020-02131-2]
18. Wang, C.; Jiang, L.; Qian, G.; Gao, Y. Supplying rapeseed meal to the diets with or without potassium iodide for yellow catfish (Tachysurus fulvidraco). Aquac. Int.; 2017; 25, pp. 2061-2078. [DOI: https://dx.doi.org/10.1007/s10499-017-0171-9]
19. Ribeiro, A.R.; Goncalves, A.; Colen, R.; Nunes, M.L.; Dinis, M.T.; Dias, J. Dietary macroalgae is a natural and effective tool to fortify gilthead seabream fillets with iodine: Effects on growth, sensory quality and nutritional value. Aquaculture; 2015; 437, pp. 51-59. [DOI: https://dx.doi.org/10.1016/j.aquaculture.2014.11.028]
20. El-Sayed, A.F.; Fitzsimmons, K. From Africa to the world—The journey of Nile tilapia. Rev. Aquac.; 2023; 15, pp. 6-21. [DOI: https://dx.doi.org/10.1111/raq.12738]
21. Kumar, G.; Engle, C.R. Technological advances that led to growth of shrimp, salmon, and tilapia farming. Rev. Fish. Sci. Aquac.; 2016; 24, pp. 136-152. [DOI: https://dx.doi.org/10.1080/23308249.2015.1112357]
22. AOAC. Official Methods of Analysis of AOAC International; 21st ed. AOAC International: Gaithersburg, MD, USA, 2019.
23. Wang, X.; Jin, Q.; Wang, T.; Huang, J.; Xi, Y.; Yao, L.; Wang, X. Screening of glucosinolate-degrading strains and its application in improving the quality of rapeseed meal. Ann. Microbiol.; 2012; 62, pp. 1013-1020. [DOI: https://dx.doi.org/10.1007/s13213-011-0341-3]
24. Xu, G.; Wei, H.; Peng, D.; Zhang, L.; Lu, X.; Li, Q.; Dong, L.; Tian, J.; Wen, H.; Wang, G. et al. Effects of Dietary Fish Meal Replaced by Cottonseed Protein Concentrate on Growth Performance, Antioxidant Capacity, and Liver and Intestinal Health of Juvenile Hybrid Culter. Fishes; 2024; 9, 127. [DOI: https://dx.doi.org/10.3390/fishes9040127]
25. Ngo, D.T.; Wade, N.M.; Pirozzi, I.; Glencross, B.D. Effects of canola meal on growth, feed utilisation, plasma biochemistry, histology of digestive organs and hepatic gene expression of barramundi (Asian seabass; Lates calcarifer). Aquaculture; 2016; 464, pp. 95-105. [DOI: https://dx.doi.org/10.1016/j.aquaculture.2016.06.020]
26. Wu, F.; Tian, J.; Yu, L.; Wen, H.; Jiang, M.; Lu, X. Effects of dietary rapeseed meal levels on growth performance, biochemical indices and flesh quality of juvenile genetically improved farmed tilapia. Aquac. Rep.; 2021; 20, 100679. [DOI: https://dx.doi.org/10.1016/j.aqrep.2021.100679]
27. Zhang, X.; Wang, H.; Zhang, J.; Lin, B.; Chen, L.; Wang, Q.; Li, G.; Deng, J. Assessment of rapeseed meal as fish meal alternative in diets for juvenile Asian red-tailed catfish (Hemibagrus wyckioides). Aquac. Rep.; 2020; 18, 100497. [DOI: https://dx.doi.org/10.1016/j.aqrep.2020.100497]
28. De la Vieja, A.; Santisteban, P. Role of iodide metabolism in physiology and cancer. Endocr. -Relat. Cancer; 2018; 25, pp. R225-R245. [DOI: https://dx.doi.org/10.1530/ERC-17-0515]
29. Ribeiro, A.R.A.; Ribeiro, L.; Sæle, Ø.; Dinis, M.T.; Moren, M. Iodine and selenium supplementation increased survival and changed thyroid hormone status in Senegalese sole (Solea senegalensis) larvae reared in a recirculation system. Fish Physiol. Biochem.; 2012; 38, pp. 725-734. [DOI: https://dx.doi.org/10.1007/s10695-011-9554-4]
30. Lüdke, H.; Schöne, F. Copper and iodine in pig diets with high glucosinolate rapeseed meal. I. Performance and thyroid hormone status of growing pigs fed on a diet with rapeseed meal treated with copper sulphate solution or untreated and supplements of iodine, copper or a quinoxaline derivative. Anim. Feed. Sci. Technol.; 1988; 22, pp. 33-43.
31. Maroufyan, E.; Kermanshahi, H. Effect of different levels of rapeseed meal supplemented with calcium iodate on performance, some carcass traits, and thyroid hormones of broiler chickens. Int. J. Poult. Sci.; 2006; 5, pp. 1110-1114.
32. Pattanaik, A.K.; Khan, S.A.; Mohanty, D.N.; Varshney, V.P. Nutritional performance, clinical chemistry and semen characteristics of goats fed a mustard (Brassica juncea) cake based supplement with or without iodine. Small Rumin. Res.; 2004; 54, pp. 173-182. [DOI: https://dx.doi.org/10.1016/j.smallrumres.2003.10.014]
33. Zhou, B.; Ran, H.; Zhang, Q.; Chen, H.; Han, F.; Xu, C.; Zhao, Q. Unveiling the Impact of Rapeseed Meal on Feeding Behavior and Anorexigenic Endocrine in Litopenaeus vannamei. Animals; 2024; 14, 540. [DOI: https://dx.doi.org/10.3390/ani14040540]
34. Jiang, J.; Shi, D.; Zhou, X.Q.; Feng, L.; Liu, Y.; Jiang, W.D.; Wu, P.; Tang, L.; Wang, Y.; Zhao, Y. Effects of lysine and methionine supplementation on growth, body composition and digestive function of grass carp (Ctenopharyngodon idella) fed plant protein diets using high-level canola meal. Aquac. Nutr.; 2016; 22, pp. 1126-1133. [DOI: https://dx.doi.org/10.1111/anu.12339]
35. Shafaeipour, A.; Yavari, V.; Falahatkar, B.; Maremmazi, J.G.; Gorjipour, E. Effects of canola meal on physiological and biochemical parameters in rainbow trout (Oncorhynchus mykiss). Aquac. Nutr.; 2008; 14, pp. 110-119. [DOI: https://dx.doi.org/10.1111/j.1365-2095.2007.00509.x]
36. Chen, H.; Luo, D. Application of haematology parameters for health management in fish farms. Rev. Aquac.; 2023; 15, pp. 704-737. [DOI: https://dx.doi.org/10.1111/raq.12753]
37. Kim, J.H.; Kim, S.K.; Hur, Y.B. Toxic effects of waterborne nitrite exposure on antioxidant responses, acetylcholinesterase inhibition, and immune responses in olive flounders, Paralichthys olivaceus, reared in bio-floc and seawater. Fish Shellfish. Immunol.; 2020; 97, pp. 581-586. [DOI: https://dx.doi.org/10.1016/j.fsi.2019.12.059]
38. Dawood, M.A.; Koshio, S.; El-Sabagh, M.; Billah, M.M.; Zaineldin, A.I.; Zayed, M.M.; Omar, A.A.E.D. Changes in the growth, humoral and mucosal immune responses following β-glucan and vitamin C administration in red sea bream, Pagrus major. Aquaculture; 2017; 470, pp. 214-222. [DOI: https://dx.doi.org/10.1016/j.aquaculture.2016.12.036]
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Details
1 Yangtze River Fisheries Research Institute, Chinese Academy of Fishery Sciences, Wuhan 430000, China
2 Hubei Key Laboratory of Waterlogging Disaster and Agricultural Use of Wetland, Yangtze University, Jingzhou 434000, China
3 Hubei Biopesticide Engineering Research Center, Hubei Academy of Agricultural Sciences, Wuhan 430000, China