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INTRODUCTION
Snooks are euryhaline fish of the Centropomidae family that inhabit tropical and subtropical zones along the Pacific and Atlantic coasts (Álvarez-Lajonchère et al. 2013). They are demersal fish with carnivorous habits that feed on mollusks, crustaceans, and fish (Macal-López et al. 2013). The Pacific white snook, Centropomus viridis, is found from the Gulf of California to southern Ecuador (Fischer et al. 1995). It has high economic value in the Mexican market due to the quality of its meat, and it is considered to have excellent potential for cultivation, since it can grow and reproduce in captivity and has high growth rates (Labastida-Che et al. 2013, Ibarra-Castro et al. 2017); however, to successfully carry out the cultivation of this species, it is necessary to determine its nutritional requirements to develop specific diets. In aquaculture, nutrition has been shown to be a limiting factor for the development of healthy and efficient aquaculture systems (Zhang et al. 2020). In this sense, the proteins and lipids in a diet are some of the main nutrients teleost fish need to carry out numerous physiological processes (NRC 2011, Dai et al. 2018, Teles et al. 2020). Protein is essential for fish growth, tissue maintenance, and the production of many key components, such as hormones, enzymes, and antibodies (Wang et al. 2019, Yan et al. 2020); protein deficiency affects growth and immune function and increases fish susceptibility to infectious diseases (Cho et al. 2021, Steinberg 2022), and excess protein in the diet increases feed cost and excretion of nitrogenous residues, which contaminates the culture medium (Wu and Gatlin 2014, Khan et al. 2019, Liu et al. 2021). Lipids and their main constituents, essential fatty acids, are the main source of metabolic energy for fish development; they are required for the structure, maintenance, and function of cell membranes, and for the transport and metabolism of fat-soluble vitamins and carotenoids, among other functions (Sargent et al. 2002, Tocher 2003). Both lipid deficiency and excess can compromise the immune response of fish (Steinberg 2022); in addition, a diet high in lipids can decrease appetite, which affects growth (Dai et al. 2018), cause fatty liver, promote fat accumulation in muscle tissue, and impair fish fillet quality (Han et al. 2014, González-Félix et al. 2015). Therefore, it is essential to develop diets with adequate levels of both nutrients for optimal fish development and growth, and to determine the optimal ratio of protein to lipid levels in the feed so that proteins are used only for growth and lipids act as the main energy source (Grisdale-Helland et al. 2008, Li et al. 2017, Ma et al. 2020); with this, we can reduce feed cost and increase the protein utilization efficiency, improve feed efficiency, and decrease the excretion of ammonia and the environmental impact of aquaculture (Jiang et al. 2016, Grapiuna-de Carvalho et al. 2017).
The protein-sparing effect of lipids has been reported in several species, such as Melanogrammus aeglefinus (Tibbetts et al. 2005), Gadus morhua (Grisdale-Helland et al. 2008), Nibea japonica (Chai et al. 2013), Diplodus vulgaris (Bulut et al. 2014), Nibea diacanthus (Li et al. 2017), Epinephelus akaara (Wang et al. 2017), Acanthopagrus schlegelii (Wang et al. 2019), Larimichthys polyactis (Ma et al. 2020), and Centropomus undecimalis (Arenas et al. 2021b); however, in other species, such as Diplodus sargus (Ozorio et al. 2006), Umbrina cirrosa (Kokou et al. 2019), Pomadasys commersonnii (Hecht et al. 2003), and Ocyurus chrysurus (Arenas et al. 2021a), this effect has not been observed. To the best of our knowledge, there are no studies on the dietary protein and lipid requirements of C. viridis juveniles; therefore, the objective of this study was to determine the effect of different levels of protein and lipids in the diet on the productive parameters of juveniles of the white snook, C. viridis.
MATERIALS AND METHODS
Experimental diets
Eight diets were formulated with 4 protein levels (40%, 46%, 52%, and 58%) and 2 lipid levels (10% and 13%). Table 1 shows the ingredients and chemical composition (AOAC 2000) of each diet. Diets were identified as D40/10, D40/13, D46/10, D46/13, D52/10, D52/13, D58/10, D58/13. The ingredients were weighed according to the formulations with an analytical balance with a capacity of 2,000 g (Ohaus CS2000, China). Macronutrients were dry blended for 15 minutes using a CRT Global blender (model MIX-B30GA). Subsequently, micronutrients were added and mixed, and the fish oil and soybean lecithin were added. Finally, water was added (approximately 400 mL per kilogram of diet). The obtained mixture was placed in a 1-HP mill (Torrey, M-22RI; Monterey, CA) to obtain granules with a 5-mm diameter; these were dried in an oven at 60 °C for 12 hours and then refrigerated at 4 °C until their use. The diets were prepared and analyzed at the Universidad Juárez Autónoma de Tabasco, Mexico.
Table 1 Formulation and proximate composition of the experimental diets.
| Diet | 40/10 | 40/13 | 46/10 | 46/13 | 52/10 | 52/13 | 58/10 | 58/13 |
| Ingredients (%) | ||||||||
| Fish meal1 | 42.72 | 42.72 | 49.15 | 49.15 | 55.60 | 55.60 | 62.00 | 62.00 |
| Krill meal1 | 2.58 | 2.58 | 2.99 | 2.99 | 3.35 | 3.35 | 3.70 | 3.70 |
| Poultry meal1 | 8.70 | 8.70 | 10.00 | 10.00 | 11.30 | 11.30 | 12.60 | 12.60 |
| Pork meal1 | 9.38 | 9.38 | 10.75 | 10.75 | 12.20 | 12.20 | 13.60 | 13.60 |
| Fish oil1 | 2.74 | 6.11 | 1.82 | 5.19 | 0.90 | 4.27 | 0.00 | 3.37 |
| Starch2 | 29.15 | 25.78 | 20.56 | 17.19 | 11.92 | 8.55 | 3.47 | 0.10 |
| Alginate3 | 2.50 | 2.50 | 2.50 | 2.50 | 2.50 | 2.50 | 2.50 | 2.50 |
| Minerals premix4 | 0.23 | 0.23 | 0.23 | 0.23 | 0.23 | 0.23 | 0.23 | 0.23 |
| Vitamin premix4 | 0.60 | 0.60 | 0.60 | 0.60 | 0.60 | 0.60 | 0.60 | 0.60 |
| Soy bean lecithin5 | 1.00 | 1.00 | 1.00 | 1.00 | 1.00 | 1.00 | 1.00 | 1.00 |
| Vitamin C3 | 0.10 | 0.10 | 0.10 | 0.10 | 0.10 | 0.10 | 0.10 | 0.10 |
| Choline6 | 0.20 | 0.20 | 0.20 | 0.20 | 0.20 | 0.20 | 0.20 | 0.20 |
| Antioxidant3 | 0.10 | 0.10 | 0.10 | 0.10 | 0.10 | 0.10 | 0.10 | 0.10 |
| Proximate composition (% dry matter) | ||||||||
| Humidity | 7.71 | 8.29 | 8.07 | 8.68 | 8.10 | 8.55 | 7.08 | 7.48 |
| Protein | 40.60 | 40.77 | 46.20 | 45.91 | 52.19 | 51.81 | 58.45 | 57.94 |
| Lipids | 9.64 | 12.63 | 9.76 | 12.84 | 9.70 | 12.75 | 9.66 | 12.82 |
| Ash | 13.57 | 12.53 | 15.19 | 15.75 | 17.96 | 17.08 | 19.71 | 19.66 |
| Protein/energy (kJ·g-1) | 20.69 | 20.29 | 23.49 | 22.39 | 26.53 | 25.27 | 29.78 | 28.26 |
1PROTMAGRO, Guadalajara, Jalisco, Mexico.
2IMSA Corn Industrializer, Guadalajara, Jalisco, Mexico.
3Droguería Cosmopólita, Mexico City, Mexico.
4ROVIMIX R C-EC (Roche) 35% active agent. Vitamin premix composition in grams, milligrams or international units (IU) per kilogram of diet: vitamin A, 10,000,000 IU; vitamin D3, 2,000,000 IU; vitamin E, 100,000 IU; vitamin K3, 4.00 g; thiamine B1, 8.00 g; riboflavin B2, 8.70 g; pyridoxine B6, 7.30 g; vitamin B12, 20.00 mg; niacin, 50.00 g; pantothenic acid, 22.20 g; inositol, 0.15 mg; nicotinic acid, 0.16 mg; folic acid, 4.00 g; biotin, 500.00 mg; vitamin C, 10.00 g; choline 0.30 mg, excipient q.s., 2.00 g; manganese, 10.00 g; magnesium, 4.50 g; zinc, 1.60 g; iron, 0.20 g; copper, 0.20 g; iodine, 0.50 g; selenium, 40.00 mg; cobalt, 60.00 mg. Excipient q.s., 1.50 g.
5Pronat Ultra, Mérida, Yucatán, Mexico.
6Sigma-Aldrich Chemical, Toluca, Mexico State, Mexico.
Origin of fish
White snook juveniles were provided by the pilot production plant of marine fish juveniles of the Centro de Investigación en Alimentación y Desarrollo, Mazatlán Unit, Mexico, according to the protocol developed by Ibarra-Castro et al. (2017).
Experimental design, feeding, and experimental conditions
A completely randomized factorial experimental design (4 × 2) was carried out, with 3 replicates per treatment. The bioassay was carried out in 24 circular fiberglass tanks with 600-L capacity that were equipped with individual air distributors and a continuous flow of filtered seawater. Each tank was stocked with 20 organisms with an average weight of 14.80 ± 0.80 g; organisms were fed by hand to apparent satiety with the experimental diets, until the food was no longer consumed and remained at the bottom of the tank (Correia-Pinto and Pinto-Nunes 2021), 3 times a day (8:00 AM, 12:00 PM, and 4:00 PM) for 6 weeks. Culture water temperature was kept at 28.50 ± 0.07 °C, salinity at 35.0 ± 1.0, and dissolved oxygen at 5.8 ± 0.3 mg·L-1. During the entire experimental period, the photoperiod was 12 hours light/12 hours dark.
Calculated variables
At the end of the experiment, the fish from all the tanks, previously anesthetized with clove essence (0.2 mL·L-1), were weighed and measured to determine the gained weight (GW), growth rate (GR), specific growth rate (SGR), condition factor (CF), feed intake (FI), feed conversion ratio (FCR), feeding efficiency rate (FER), protein efficiency rate (PER), and survival rate (S); in addition, 3 fish from each tank were randomly selected to determine the hepatosomatic index (HI) and the peritoneal fat index (PFI) using the following formulas:
where FW is the average final weight and IW is the average initial weight;
Hematological indices
At the end of the experiment, 9 fish per treatment (3 fish per tank) were randomly taken for blood collection. The organisms remained without food for 24 hours before sampling, and later, they were anesthetized with clove oil (0.2 mL·L-1). The determination of the indices was carried out according to del Rio-Zaragoza et al. (2011). Blood was extracted from each fish with a 1.0-mL insulin syringe by puncturing the caudal vein; ~200.0 μL of blood were placed in an Eppendorf tube with ethylenediaminetretaacetic acid dipotassium (EDTA-K2) to evaluate the concentration of hemoglobin (HB) and hematocrit (HCT). Another 200.0-μL sample was placed in another Eppendorf tube without anticoagulant; this was centrifuged to separate the serum and determine the content of total protein (TP), glucose (GL), and triglycerides (TG). Hematological parameters were determined using commercial kits from Biosystems and Randox Laboratories.
Statistical analyses
Data in percentage form were transformed to arcsine. Normality (Bartlett’s test) and homoscedasticity (Levene’s test) were determined for all results, which were subjected to a 2-way analysis of variance (ANOVA) (P < 0.05). To determine significant differences between treatments, Tukey’s multiple comparison rank tests (P < 0.05) were applied (Zar 1996). Statistical analyses were carried out using the Statgraphics Centurion XVI v.16.204 program (Statpoint Technologies).
RESULTS
Growth and survival
Table 2 shows the growth and survival results of juvenile white snook fed with the different diets. FW, GW, GR, and SGR were not affected by dietary protein or lipid level (P > 0.05). The survival of juvenile white snook at the end of the experimentation period was 100% for all treatments, with the exception of D46/10 (96.6%), with no significant differences between the different treatments (P > 0.05).
Table 2 Growth and survival of juvenile Centropomus viridis fed the experimental diets. IW, initial average weight; FW, final average weight; GW, gained weight; GR, growth rate; SGR, specific growth rate; S, survival.
| Diet | IW (g) | FW (g) | GW (g) | GR (%) | SGR (%) | S (%) |
| 40/10 | 14.70 ± 0.14 | 58.86 ± 1.70 | 44.05 ± 1.93 | 299.24 ± 14.76 | 2.47 ± 0.05 | 100 |
| 40/13 | 14.71 ± 0.40 | 71.16 ± 7.75 | 56.45 ± 7.48 | 383.25 ± 43.85 | 2.80 ± 0.16 | 100 |
| 46/10 | 15.10 ± 0.22 | 66.13 ± 4.06 | 50.94 ± 4.28 | 336.14 ± 33.23 | 2.62 ± 0.13 | 96.66 ± 5.70 |
| 46/13 | 14.80 ± 0.80 | 62.90 ± 6.59 | 47.93 ± 7.19 | 327.07 ± 62.86 | 2.57 ± 0.28 | 100 |
| 52/10 | 15.20 ± 0.31 | 74.76 ± 7.43 | 59.55 ± 7.26 | 392.16 ± 45.80 | 2.83 ± 0.15 | 100 |
| 52/13 | 14.83 ± 0.39 | 67.89 ± 6.90 | 53.04 ± 7.08 | 358.74 ± 54.51 | 2.70 ± 0.20 | 100 |
| 58/10 | 14.90 ± 0.60 | 66.79 ± 5.47 | 51.90 ± 5.48 | 349.65 ± 33.22 | 2.67 ± 0.13 | 100 |
| 58/13 | 15.10 ± 0.60 | 68.60 ± 10.38 | 54.43 ± 10.30 | 360.62 ± 73.64 | 2.68 ± 0.28 | 100 |
| Means of main effect | ||||||
| Protein % | ||||||
| 40 | 14.70 | 65.01 | 50.25 | 341.24 | 2.64 | 100 |
| 46 | 14.90 | 64.51 | 49.44 | 331.60 | 2.60 | 98.33 |
| 52 | 15.00 | 71.32 | 56.29 | 375.45 | 2.77 | 100 |
| 58 | 15.00 | 67.69 | 53.16 | 355.13 | 2.67 | 100 |
| Lipid % | ||||||
| 10 | 14.90 | 66.63 | 51.61 | 344.30 | 2.65 | 99.16 |
| 13 | 14.80 | 67.63 | 52.96 | 357.42 | 2.69 | 100 |
| Two-way ANOVA (P value) | ||||||
| Protein | 0.6191 | P = 0.3150 | P = 0.3209 | P = 0.4514 | P = 0.4770 | P = 0.4180 |
| Lipid | 0.5828 | P = 0.7217 | P = 0.6322 | P = 0.5168 | P = 0.6157 | P = 0.3320 |
| Interaction | 0.6019 | P = 0.1184 | P = 0.1263 | P = 0.2206 | P = 0.2201 | P = 0.4180 |
The results are the mean (mean ± SD) of 3 replicates (n = 3). ANOVA: analysis of variance.
Feed efficiency and biometric indices
The results of the feed efficiency and morphometric parameters evaluated are shown in Table 3. According to the 2-way ANOVA, FI, FCR, FER, and PER were affected by the protein content in the diet, and the lipid level did not affect these parameters. The highest FI was obtained with the fish fed with 58% protein, and it was significantly different (P < 0.05) from the FI obtained with fish fed with other protein levels; the lowest FCR was obtained with the fish fed with 52% protein and was significantly different (P < 0.05) from the FCR obtained with the juveniles fed with the rest of the protein levels. We obtained 100% FER with fish fed 52% protein, and this rate was significantly higher (P < 0.05) than the FER we obtained with the other protein levels; the lowest PER value was obtained with the fish fed with 58% protein, and this value was significantly different (P < 0.05) from that obtained with the juveniles fed with 40% protein. HI decreased significantly (P < 0.05) when the protein content in the diet increased, regardless of lipid level; meanwhile, PFI increased significantly (P < 0.05) when lipid levels in the diet increased. The protein level did not affect the PFI. Regarding the CF, no significant differences were found between the different protein and lipid levels in the diet (P > 0.05).
Table 3 Feed efficiency and biometric indices of juvenile white snook, Centropomus viridis, fed the experimental diets. FI, food intake; FCR, food conversion ratio; FER, food efficiency rate; PER, protein efficiency rate; HI, hepatosomatic index; PFI, peritoneal fat index; CF, condition factor.
| Diet | FI (g) | FCR | FER (%) | PER | HI (%) | PFI (%) | CF |
| 40/10 | 55.69 ± 2.70 | 1.25 ± 0.04 | 79.12 ± 2.60 | 1.09 ± 0.05 | 1.49 ± 0.17 | 5.51 ± 1.03 | 0.88 ± 0.05 |
| 40/13 | 57.3 ± 3.70 | 1.01 ± 0.06 | 98.22 ± 6.50 | 1.40 ± 0.18 | 1.74 ± 0.28 | 6.41 ± 1.03 | 0.87 ± 0.03 |
| 46/10 | 56.77 ± 1.70 | 1.11 ± 0.10 | 89.79 ± 8.00 | 1.10 ± 0.09 | 1.49 ± 0.24 | 5.43 ± 0.78 | 0.83 ± 0.02 |
| 46/13 | 59.00 ± 6.40 | 1.23 ± 0.10 | 81.0 ± 6.60 | 1.03 ± 0.15 | 1.56 ± 0.18 | 6.47 ± 1.50 | 0.83 ± 0.03 |
| 52/10 | 54.13 ± 3.30 | 0.90 ± 0.06 | 109.84 ± 8.70 | 1.14 ± 0.14 | 1.50 ± 0.18 | 5.28 ± 0.86 | 0.89 ± 0.01 |
| 52/13 | 57.74 ± 7.40 | 1.08 ± 0.03 | 91.84 ± 2.60 | 1.01 ± 0.13 | 1.35 ± 0.18 | 6.27 ± 1.0 | 0.84 ± 0.02 |
| 58/10 | 65.53 ± 2.00 | 1.26 ± 0.10 | 79.11 ± 6.40 | 0.89 ± 0.09 | 1.30 ± 0.16 | 5.63 ± 1.01 | 0.86 ± 0.01 |
| 58/13 | 64.05 ± 9.20 | 1.18 ± 0.11 | 84.85 ± 8.50 | 0.93 ± 0.18 | 1.07 ± 0.17 | 5.77 ± 1.10 | 0.83 ± 0.02 |
| Means of main effect | |||||||
| Protein % | |||||||
| 40 | 56.50X | 1.13Y | 88.67X | 1.25Y | 1.62Z | 5.96 | 0.88 |
| 46 | 57.92X | 1.17Y | 85.39X | 1.06XY | 1.52YZ | 5.95 | 0.83 |
| 52 | 55.93X | 0.99X | 100Y | 1.07XY | 1.43Y | 5.78 | 0.86 |
| 58 | 64.79Y | 1.22Y | 81.98X | 0.91X | 1.19X | 5.70 | 0.84 |
| Lipid % | |||||||
| 10 | 58.03 | 1.13 | 89.46 | 1.05 | 1.45 | 5.46A | 0.86 |
| 13 | 59.54 | 1.13 | 88.97 | 1.09 | 1.43 | 6.25B | 0.84 |
| Two-way ANOVA (P value) | |||||||
| Protein | 0.0214 | 0.0015 | 0.0010 | 0.0053 | 0.0000 | 0.8481 | 0.1194 |
| Lipid | 0.4654 | 0.8487 | 0.8595 | 0.4609 | 0.6923 | 0.0031 | 0.1110 |
| Interaction | 0.8596 | 0.0020 | 0.0010 | 0.0604 | 0.0034 | 0.5498 | 0.7050 |
The results are the mean (mean ± SD) of 3 replicates (n = 3). Values in the same column with different letters are significantly different (P < 0.05). (Dietary protein = X, Y, Z; dietary lipid = A, B). ANOVA: analysis of variance.
Hematological parameters
The results of the hematological parameters evaluated are shown in Table 4. According to the results of the 2-way ANOVA, the level of protein or lipids in the diet did not influence the HB content in juveniles fed with the different treatments (P > 0.05); the HCT value was affected by the protein level regardless of the lipid level in the diet. Juveniles fed the 40% protein diets had the highest percentage of HCT, and this was significantly different (P < 0.05) from the HCT obtained with juveniles fed the 46% and 58% protein diets. Only the protein level affected the percentage of TP in the plasma of C. viridis juveniles; juveniles fed diets with 40% protein had a higher percentage of TP than juveniles fed with diets with 46% and 58% protein (P > 0.05). The content of plasma GL and TG increased significantly (P < 0.05) when the percentage of lipids in the diet increased. The content of protein in the diet also affected both parameters; the value of the GL was higher in the juveniles fed with the diets with 52% protein, and the value of the TG was significantly lower (P < 0.05) in the juveniles fed with the diets with 58% protein.
Table 4 Hematological parameters of juvenile white snook, Centropomus viridis, fed the experimental diets. HB, hemoglobin; HCT, hematocrit; TP, total protein; GL, glucose; TG, triglycerides.
| Diet | HB (g·dL-1) | HCT (%) | TP (g·dL-1) | GL (mg·dL-1) | TG (mg·dL-1) |
| 40/10 | 18.10 ± 8.30 | 54.00 ± 4.90 | 7.24 ± 0.53 | 96.90 ± 2.90 | 371.56 ± 120.06 |
| 40/13 | 22.22 ± 4.40 | 56.10 ± 10.40 | 6.83 ± 0.67 | 103.70 ± 5.60 | 447.31 ± 95.10 |
| 46/10 | 18.23 ± 7.10 | 47.60 ± 6.80 | 5.76 ± 1.52 | 97.60 ± 3.80 | 292.56 ± 142.00 |
| 46/13 | 18.19 ± 7.00 | 46.20 ± 4.40 | 6.90 ± 0.49 | 100.20 ± 4.70 | 511.10 ± 61.14 |
| 52/10 | 23.37 ± 3.70 | 55.10 ± 6.30 | 7.02 ± 0.42 | 103.60 ± 3.80 | 242.12 ± 99.01 |
| 52/13 | 20.19 ± 9.20 | 46.60 ± 7.70 | 6.67 ± 0.23 | 105.90 ± 7.20 | 407.40 ± 26.91 |
| 58/10 | 24.29 ± 7.30 | 46.90 ± 7.10 | 6.30 ± 0.53 | 99.30 ± 4.50 | 161.41 ± 122.79 |
| 58/13 | 19.04 ± 7.80 | 44.00 ± 2.60 | 5.93 ± 0.67 | 100.30 ± 5.70 | 231.62 ± 100.25 |
| Means of main effect | |||||
| Protein % | |||||
| 40 | 20.16 | 55.06Y | 7.04Z | 100.29X | 409.43Y |
| 46 | 18.21 | 46.88X | 6.33XY | 98.88X | 401.83Y |
| 52 | 21.78 | 50.90XY | 6.85YZ | 104.77Y | 324.76Y |
| 58 | 21.66 | 45.43X | 6.12X | 99.75X | 196.52X |
| Lipid % | |||||
| 10 | 21.00 | 50.89 | 6.58 | 99.60A | 284.46A |
| 13 | 19.91 | 48.25 | 6.58 | 102.25B | 381.80B |
| Two-way ANOVA (P-Value) | |||||
| Protein | 0.4004 | 0.0003 | 0.0008 | 0.0030 | 0.0000 |
| Lipid | 0.5171 | 0.1045 | 1.0000 | 0.0258 | 0.0020 |
| Interaction | 0.2255 | 0.1508 | 0.0040 | 0.1437 | 0.0062 |
The results are the mean (mean ± SD) of 3 replicates (n = 3). Values in the same column with different letters are significantly different (P < 0.05). (Dietary protein = X, Y, Z; dietary lipid = A, B). ANOVA: analysis of variance.
DISCUSSION
To be able to formulate balanced feeds and farm fish successfully, it is essential to determine the minimum requirements of nutrients, such as protein and lipids, with which fish can achieve maximum growth and good health (NRC 2011). In the present study, we evaluated the effect of 4 protein levels (40%, 46%, 52%, and 58%) and 2 lipid levels (10% and 13%) on the growth of C. viridis juveniles. The results indicated that the protein and lipid levels evaluated did not affect the growth of juveniles of this species. Considering that C. viridis is a carnivorous fish (Macal-López et al. 2013), we expected growth to be higher in fish fed diets with high levels of protein (52%-58%), as has been reported for other snook species, such as Centropomus parallelus (de Souza et al. 2011, Correia-Pinto and Pinto-Nunes 2021), C. undecimalis (Concha-Frías et al. 2018), and Lates calcarifer (Glencross 2006), and other carnivorous marine fish (NRC 2011, Bowyer et al. 2013, Teles et al. 2020, Steinberg 2022); however, the results obtained in this study are similar to those obtained for C. undecimalis by Gracia-López et al. (2003) and Arenas et al. (2021b), who reported good growth using diets with around 40% protein and 12% lipids. Likewise, to obtain optimal growth in other species of carnivorous fish, such as Thymallus thymallus (Rahimnejad et al. 2021), Acanthopagrus berda (Rahim et al. 2016), Acanthopagrus schlegelli (Wang et al. 2019), and Cynoscion othonopterus (Pérez-Velázquez et al. 2015), it has been suggested to feed them diets that contain 37%-40% protein and 9%-12% lipids. The present study did not verify the protein-sparing effect of dietary protein through lipids in the diet since no significant differences were obtained in the growth of C. viridis juveniles fed with the different treatments. The optimal protein/energy ratio in the diet allows the fish to utilize the highest amount of protein, just for growth (Ma et al. 2020). For most species of marine fish, the optimum ratio is between 20.00 and 32.00 mg·kJ-1 (NRC 2011); the results of the protein/energy ratio in the diets of this study are within the recommended range. In relation to the FCR and FER obtained in the present study, it was observed that only the protein level had significant effects; the best FCR and FER were obtained with juveniles fed diets with 52% protein and both lipid levels. For C. undecimalis juveniles fed diets with 35%-50% protein and 5%-15% lipids, Catacutan and Coloso (1995) reported that the best FCR was obtained with a diet with 50% protein and 5% lipids; for this same species, Gracia-Lopez et al. (2003) reported that the best FCRs were obtained with diets with 40% and 53% protein. Regarding the PER, several authors have reported that it decreases when the level of protein in the diet increases, regardless of the lipid level (Catacutan and Coloso 1995, Ozorio et al. 2006, Bulut et al. 2014, Zhang et al. 2017, Wang et al. 2019, Arenas et al. 2021a), as was observed in this study. The PER reflects the efficiency of utilization and the quality of dietary protein (NRC 2011, Wang et al. 2021). In this study, the highest PER value was obtained with diets containing 40% protein, which could indicate that this protein level is adequate for protein synthesis by C. viridis juveniles and, possibly, for the inclusion of higher percentages of protein as an energy source, as has been observed in other species of marine fish, such as Pomadasys commersonnli (Hecht et al. 2003), Melanogrammus aeglefinus (Tibbets et al. 2005), Epinephelus coioides (Yan et al. 2020), T. thymallus (Rahimnejad et al. 2021), and Sillago sihama (Liu et al. 2021). Somatic indices such as HI, PFI, and CF are used to evaluate the response of fish to different nutritional conditions (Liu et al. 2021). This work showed that the HI decreased when the level of protein in the diet increased and that the level of lipids did not affect it; other authors have reported this negative correlation between HI and protein level for some species of marine fish (Tibbetts et al. 2005, Grisdale-Helland et al. 2008, Chai et al. 2013, Jiang et al. 2016, Li et al. 2017, Kokou et al. 2019). On the other hand, the PFI was not affected by the percentage of protein in the diet, but was affected by the lipid content; the highest PFI was observed with the highest level of lipids, which could suggest that fat deposition was significantly greater in the peritoneal cavity when the amount of lipids in the diet increased (NRC 2011, Wang et al. 2017, Correia-Pinto and Pinto-Nunes 2021).
Haematological parameters can provide information on nutritional status, digestive function, and routine metabolism of fish, and they act as non-specific biomarkers (Satheeshkumar et al. 2011, Ahmed et al. 2020). Malnutrition, even in the initial stages, can cause detectable alterations in the blood tissue of fish, mainly in the TP and GL parameters, which tend to be significantly lower or higher in response to nutritional conditions (Yoo et al. 2022). TP content could reflect protein absorption and metabolism in fish (Wang et al. 2019, 2021); the highest concentrations of TP in this study were obtained with diets with 40% protein, which could indicate that this level is adequate for C. viridis juveniles to carry out the digestion and absorption of proteins in the blood, and that higher levels of protein in the diet could have been improperly digested and not used by these organisms, as observed in E. coioides (Yan et al. 2020), Thamnaconus septentrionali (Xu et al. 2021), and other species. Conversely, for other fish species, such as N. diacanthus (Li et al. 2017) and A. schlegelii (Wang et al. 2019), significantly higher TP values have been reported in fish fed with high levels of protein, indicating that these species require high levels of protein in the diet. In the present study, GL was significantly elevated in fish fed the highest lipid level. Rahimnejad et al. (2021) indicated that the increase in GL concentration in the serum of fish fed a high-fat diet could be associated with impaired GL homeostasis. The increase in GL concentration at higher lipid levels in this study agrees with that reported for T. thymallus (Rahimnejad et al. 2021), Takifugu obscurus females, and Takifugu rubripes males (Yoo et al. 2022). TG concentrations in the blood could be used as indicators to assess endogenous lipid transport (Ahmed et al. 2020). In the present work, the level of TG in the blood was higher in fish fed with the highest level of dietary lipids and lower in fish fed with the highest percentage of dietary protein, which may indicate that the transport of lipids was more active in the diets with the highest level of dietary lipids. Several authors have reported that the level of TG in the blood is inversely correlated with the protein content of food and positively correlated with the lipid content (Cho et al. 2015, Li et al. 2017, Wang et al. 2017, Xu et al. 2021, Yoo et al. 2022). To the best of our knowledge, there are no published reports on values of hematological parameters of C. viridis with which we can compare our results. Values of HB of 55%, HCT of 44%, GL of 64.2 mg·dL-1, and TP of 4.7 mg·dL-1 have been reported for L. calcarifer (Satheeshkumar et al. 2011); these values are similar to those obtained in the present study and are higher than those reported for fish species with sedentary behavior. Filho et al. (1992) observed that active fish species, such as bass, have higher concentrations of HB and HCT in response to the high metabolic rates of these species.
According to the results obtained in the present study, it is concluded that, under the conditions of the present study, C. viridis juveniles can be fed with diets containing 40% protein, 10% lipids, and a protein/energy ratio of 20.69 mg·kJ-1 to obtain adequate growth and feed efficiency without affecting their survival and their biometric and hematological indices. Future research is recommended to assess whether dietary protein requirements in juveniles of this species are below 40% and evaluate other dietary lipid levels to determine if there is a protein-sparing effect of dietary lipids.
