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Efficacy of using sunflower meal as an ingredient, and partial fishmeal‐replacer, in practical feed formulated for stinging catfish (Heteropneustes fossilis)

Efficacy of using sunflower meal as an ingredient, and partial fishmeal‐replacer, in practical... INTRODUCTIONThe stinging catfish, Heteropneustes fossilis (Bloch, 1974), belonging to the family Heteropneustidae, is a commercially vital freshwater fish species (Ali et al., 2016; Rahman et al., 2019), and commonly known as ‘shing’ or ‘singhi’ in Bangladesh and India (Khan et al., 2003; Samad et al., 2017). This species is widely available in many countries throughout the South and Southeast Asia (Talwar & Jhingran, 1991). It has gained consumer preferences and become one of the popular aquaculture species due to delicious taste and nutritional value (Chakraborty & Nur, 2012; Kohinoor et al., 2012; Nushy et al., 2020). The fish has often been regarded as a highly nutritious food fish species and is recommended as a healthy diet for recuperating patients (Nushy et al., 2020). Saha and Ratha (2007) reported that this fish can sustain prolonged periods to high levels of ammonia and low oxygen conditions and resides in low depth lentic as well as lotic waterbodies with weak water flow such as agricultural fields, swamps, and wetlands, which makes it a potential aquaculture candidate. Although the species has recently gained popularity as a commercially important fish species among fish farmers, one of its biggest challenges is its heavy reliance on commercial feed, which is expensive (Nushy et al., 2020).With the intensification of aquaculture, the demand for commercial feed has increased largely. In intensive or semi‐intensive grow‐out farming, commercial feeds are the main source of the dietary protein requirements of fish, which accounts for 60%–70% of total production costs (Khan et al., 2018). Protein is considered one of the costliest elements in fish feeds and an important factor influencing the growth performance of fish and the cost of feeds (Luo et al., 2004). In aquafeed, fish meal (FM) has been widely used as the primary source of protein due to its higher content of digestible protein with balanced amino acids (AA), including a high presence of taurine, selenium, and unsaturated fatty acids, as well as its high palatability (NRC, 2011; Luthada‐Raswiswi et al. 2021; Tacon & Metian, 2008, 2015). However, there is a big concern regarding the sustainability of using FM and fish oil from the ocean as wild marine forage fish cannot meet growing demand and will thus limit aquaculture growth (Checkley et al., 2017; Pauly & Zeller, 2016). Due to limited supply and high demand, FM has currently become the most expensive ingredient that affects the price of aquafeeds, especially for feeding carnivorous fish that requires high level of FM in the diets (Han et al., 2018). Therefore, it is crucial to find a cost‐effective and sustainable alternative protein source for FM in the diets of commercial fish species.Various plant‐based ingredients have been commonly considered as an excellent source of alternative protein for partial or complete substitution of FM in aquafeeds due to several factors, including their lower cost and more sustainability (El‐Sayed, 1999; Hardy, 2010; Liti et al., 2006; Olivera‐Castillo et al., 2011; Richie & William, 2011). A plant‐based ingredient is not only used as potential protein sources but also for nutritional‐functional requirements such as binding. The use of plant‐based proteins can substitute up to 50% of the FM in a carnivorous fish diet without causing any adverse effects on growth (Hardy, 2010). Oilseed meals are commonly known as plant‐derived protein supplements that are produced after extracting oil from oilseeds including soybeans, cottonseed, canola, peanuts, and sunflower seeds (Bernard, 2016). Among the world's most widely used oilseeds, sunflower meal (SFM) is a byproduct of the oil extraction process from sunflower seeds that has a high protein value (Saleh et al., 2021), palatability, and a low level of anti‐nutritional factors, making it an ingredient suitable for use in aquaculture diet formulations (Shchekoldina & Aider, 2014). It was found to have a high content of sulphur AA (Olvera‐Novoa et al., 2002) but a poor content of lysine (Tacon et al., 1984). According to Sanz et al. (1994), a high level of digestible protein is derived from SFM though the level of digestible energy is low because of their high fibre content.Several previous studies were found to use SFM up to 25% as a partial replacement for FM without adverse effects on the growth performance of mozambique tilapia (Oreochromis mossambicus), redbreast tilapia (Tilapia rendali), and nile tilapia (Oreochromis niloticus L.) under laboratory conditions, as reported by Jackson et al. (1982), Olvera‐Novoa et al. (2002), and Ogello et al. (2017), respectively. Partially substituting FM with SFM in the feed of trout (Oncorhynchus mykiss) significantly improved growth performance (Rab, 1993). In addition, Rahmdel et al. (2018) reported that SFM could be used in the diet of common carp (Cyprinus carpio) fingerlings to replace up to 75% of FM without any adverse effects on growth performance, body composition, haematological and biochemical parameters.Despite the availability of SFM around the world and their lower cost as an alternative potential protein source for partially replacing FM, sufficient research has not been conducted on the diet of stinging catfish. Therefore, considering the availability and nutritional aspects of SFM, this study was aimed at assessing the effects of partial replacement of FM with SFM in the practical diet on the growth performance, body composition, and haematology of stinging catfish, H. fossilis.MATERIALS AND METHODSExperimental designsThe experiment was carried out in the wet laboratory of the Department of Aquaculture, Bangabandhu Sheikh Mujibur Rahman Agricultural University, Gazipur, Bangladesh. The rearing trial was conducted for a period of 8 weeks. The experiment was conducted in a completely randomized design (CRD). A total of 15 glass aquaria of 150‐L water capacity were used for the feeding trial of the H. fossilis fingerling. All the glass aquaria were divided into five groups (one control group and four treatment groups) including three replications for each treatment where FM protein was replaced by SFM protein at a rate of 0% (T0), 10% (T10), 20% (T20), 30% (T30), and 40% (T40) levels, respectively. Each tank was stocked with 40 fish. The experimental site was facilitated with good water supply, easy access, continuous electricity, adequate inlet and outlet systems, aeration system, and other necessary facilities.Collection and rearing of experimental fishThe fingerlings of H. fossilis were collected from a commercial fish hatchery. Live and healthy fingerlings were collected and brought to the wet Laboratory, Department of Aquaculture, BSMRAU, in polythene bags with oxygen. After arriving, fish were kept in circular tanks with adequate aeration. Fish were acclimatized in a 300‐L circular tank for 1 week and fed with commercial feed containing 30% protein, 8.3% lipid, 13% ash, and 11% moisture. Then, fish were given a salt treatment with 1% salt solution before releasing into the experimental aquaria. Forty fish (initial average body weight of 2.42 ± 0.01 g) were distributed per aquarium in such a way that the biomass of all 15 aquaria became similar. The fish were fed two times a day, one in the morning and one in the evening to apparent satiation (until fish stopped feeding). The excreta of fish were cleaned by the siphoning method. Approximately 30% of the water in each aquarium was replenished every 3 days. Each aquarium was continuously aerated with an air stone that was connected to a central air compressor. A natural photoperiod (approximately 10:14 light/dark) was maintained during the experimental period.Experimental diet preparationFive iso‐nitrogenous (35% protein) diets T0, T10, T20, T30, and T40 were prepared by replacing FM protein with SFM protein at a rate of 0%, 10%, 20%, 30%, and 40%, respectively. The control diet (T0) was prepared without using SFM protein. Feed ingredients were purchased from the local feed market, and their proximate composition was analyzed (Table 1). The quality of feed ingredients was considered during purchasing. Ingredients were ground using a laboratory grinder (Panasonic AC MX‐AC400). All the ingredients were mixed properly with adequate water to prepare dough and were pelleted with a laboratory‐type pellet machine to obtain pellets of 2 mm diameter and then sun dried for 2 days. After preparing the experimental diet, the proximate composition of experimental diets were analyzed at a fish nutrition laboratory under the Department of Aquaculture, Faculty of Fisheries, Bangabandhu Sheikh Mujibur Rahman Agricultural University (Table 2). The calculated gross energy was similar in all treatments and ranged between 13.75 and 14.45 kJ/g. Finally, diets were preserved in a refrigerator (−4°C) until used.1TABLEProximate composition of different feed ingredients of H. fossilis feedIngredientsMoisture (%)Protein (%)Lipid (%)Ash (%)Fibre (%)Fish meal8.261.46.38.20.12Sunflower meal6.428.311.213.422Soybean meal8.343.66.69.25.8Rice bran10.212.313.214.18.25Mustard oil cake8.634.310.49.412.21Wheat flour8.412.13.32.30.562TABLEFormulation and proximate composition (g/100g dry matter) of experimental dietsExperimental diet (%)T0T10T20T30T40Ingredient (% dry matter basis)Fish meal26.2323.6120.9818.3615.74Sunflower meal0.005.7111.4317.1422.86Soybean meal25.5826.7427.2129.3030.00Mustard oil cake12.5012.5013.1311.2512.50Rice bran25.0020.8316.6713.338.33Wheat flour7.697.697.697.697.69Vitamin1‐premix1.001.001.001.001.00Mineral2‐premix1.001.001.001.001.00Soybean oil1.001.001.001.001.00Total100100100100100Nutrients (% dry matter basis)Protein35.10 ± 0.0335.07 ± 0.0334.98 ± 0.0534.97 ± 0.0635.11 ± 0.03Lipid6.2 ± 0.045.87 ± 0.016.39 ± 0.035.71 ± 0.085.59 ± 0.05Ash10.6 ± 0.0910.2 ± 0.0210.1 ± 0.019.60 ± 0.029.56 ± 0.02Moisture15 ± 0.0314.66 ± 0.0513.9 ± 0.0814.25 ± 0.0614.7 ± 0.171Vitamin premix (mg/kg): Hiamin‐HCl, 60; riboflavin, 200; pyridoxine‐HCl, 40; vitamin B, 0.09; 12 nicotinic acid, 800; Ca pantothenate, 280; inositol, 4000; biotin, 6; folic acid, 15; PABA, 400; choline chloride, 8000; ascorbic acid, 2000; alpha‐tocopherol, 400; menadione, 40; beta‐carotene, 12; vitamin D, 0.05. (Hossain & Furuichi, 2000a, 2000b).2Mineral premix (mg/kg): KCl, 3840; MgSO4·5H2O, 4080; NaH2 PO4·2H2O, 34,260; Fe‐citrate, 1200; AlCl3·6H2O, 45; ZnSO4·7H2O, 132; MnSO4·5H2O, 877; CuCl, 7.9; KI, 1.9; CoCl4·6H2O, 0.7. (Hossain & Furuichi, 2000a, 2000b).Monitoring water quality parametersWater quality parameters were measured every day at 9.00 AM during the study period. Water temperature (°C) was recorded using a Celsius thermometer (digi‐thermo WT‐2) from each aquarium. pH (hydrogen ion concentration) was measured using a digital pH meter (Hach Co., Colorado, USA). A digital dissolved oxygen (DO) meter (Lutron DO‐5509) was used to determine the dissolved oxygen content of water. Ammonia (mg/L) was determined by an ammonia measuring kit (Hanna Instrument Test Kit).Fish sampling and growth performanceAt the end of the experimental period, all the fish were picked up from the aquaria by scope net. Then, all the fish were counted and weighted individually by a digital electric balance (model‐EK600i) to determine the weight gain. During sampling, fish were handled very carefully. Growth performance was determined, and feed utilization was calculated according to Akter et al. (2021) and Chakraborty et al. (2021) as follows:Weight gain (g) = W2 − W1;Weight gain rate (%) = 100 (W2 − W1) / W1;Specific growth rate (SGR; %/day) = 100 [Ln W2 (g) − Ln W1 (g)]/T, where W1 is the initial fish weight, W2 is the final fish weight, and T is the rearing period (56 days);Feed intake = the total of the consumed feed (g) to fish during the rearing period;Feed conversion ratio (FCR) = dry consumed feed (g)/weight gain (g);Protein efficiency ratio (PER) = weight gain (g)/protein intake (g);Fish survival (%) = 100 (final number of fish/initial number of fish).Proximate composition analysisProximate compositions of feed ingredients, experimental diets, and fish carcasses were determined according to standard procedures given by AOAC (1997). Five fish from each tank were used to analyze the whole‐body proximate composition at the end of feeding trial. Briefly, crude protein content was determined by the Kjeldahl systematic method following acid digestion with an auto‐Kjeldahl System (UDK 152, VELP), crude lipid content was measured by ether extraction using a solvent extractor (SER 148, VELP), crude ash was detected following combusting at 550°C, and moisture content was measured by drying the samples in an oven at 105°C for 24 h. Crude fibre was detected by a fibre analyzer (FIWE 6, VELP) following the Weende method.Haematological analysisAt the end of 8‐week feeding trial, 10 fish from each treatment were randomly taken for blood collection. Blood samples were collected from the caudal vein with a 1‐mL tuberculin syringe. The needle was soaked into a 2% heparin solution as an anticoagulant during blood collection. Blood was then transferred into the tube containing ethylene diamine tetra acetic acid (EDTA) (BD Microtainer®, UK) and preserved at 4°C for haematological analyses (Neepa et al., 2022). A digital haematology analyzer (DH36, Dymind Biotechnology) was used to determine haematological parameters such as haemoglobin (Hb, g/dL), packed cell volume (PCV), white blood cells (WBC), and red blood cells (RBC). Mean corpuscular volume (MCV), mean corpuscular haemoglobin (MCH), and mean corpuscular haemoglobin concentration (MCHC) were calculated using the following formula: MCHC (%) = Hb/Hct × 100; MCV (fL) = PCV/RBC × 10; MCH (pg) = Hb/RBC × 10 (Kole et al., 2022; Mrong et al., 2021).Statistical analysisPrior to statistical analysis, all data were tested for normality and homogeneity using the Shapiro–Wilk test and Levene's test, respectively. The data were analyzed statistically by one‐way analysis of variance using statistical software Statistix 10 (2013), and significance was indicated by least significant difference option of the package. The significance level was determined at p < 0.05.RESULTSWater quality parametersDifferent physio‐chemical parameters of fish culture were recorded throughout the experimental period, which are presented in Table 3. The water temperature (°C), dissolved oxygen (mg/L), hydrogen ion concentration (pH), and ammonia‐nitrogen (mg/L) ranged from 26.19 to 27.35°C (26.77 ± 0.16; mean ± SD), 6.12 to 6.95 mg/L (6.55 ± 0.10; mean ± SD), 6.21 to 7.34 (6.75 ± 0.13; mean ± SD), and 0.35 to 0.55 mg/L (0.43 ± 0.02; mean ± SD), respectively. However, there was no significant (p > 0.05) variation in water quality parameters among the tanks in the same sampling day.3TABLERanges of water quality parameters recorded from different treatments during the experimental periodTreatmentWater temperature (°C)pHDO (mg/L)Total ammonia (mg/L)T026.18–27.276.21–6.686.23–6.950.35–0.45T1026.21–27.226.23–6.866.76–6.850.37–0.44T2026.51–27.246.25–6.866.71–6.950.35–0.46T3026.22–27.356.85–7.326.12–6.350.35–0.55T4026.42–27.156.92–7.346.18–6.440.44–0.54Growth and feed utilization performance of H. fossilisThe effects of five experimental diets containing different levels of SFM on the growth and feed utilization of H. fossilis were investigated during the experiment (Table 4). Statistical analysis showed that all growth and feed utilization parameters of fish were significantly different among the treatments (p ˂ 0.05). Significantly, the best growth performance (weight gain 6.25 ± 0.11g, % weight gain 163.32 ± 4.84, SGR 1.61 ± 0.03%/day) was observed in the control treatment (T0), but there was no significant difference among T0, T10, and T20 treatments where FM protein was replaced by SFM protein at 0%, 10%, and 20% levels, respectively. However, there is a negative impact of higher level of replacement of FM with SFM on growth performance. The lowest weight gain (1.93 ± 0.10 g), % weight gain (83.24 ± 4.23 g), and SGR (1.01 ± 0.04%/day) were observed in T40 treatment where SFM protein replaced 40% of FM protein in diet. In regression analysis, cubic model (Y = −0.000015X3 + 0.000321X2 – 0.003857X + 1.608286, R2 = 0.972, Ymax = X value of 14.3%) was found to be the most suitable model between SGR and replacement level of FM with SFM, and the optimum replacement level of FM with SFM was determined to be 14.3% for stinging catfish diet (Figure 1). The mean values of FCR were observed as 1.53 ± 0.01, 1.54 ± 0.02, 1.56 ± 0.02, 1.73 ± 0.04, and 1.93 ± 0.15 in treatments T0, T10, T20, T30, and T40, respectively. The highest PER (2.11 ± 0.05) was found in treatment T0, but there was no significant difference between T0, T10, and T20 treatments (2.11 ± 0.05%, 2.07 ± 0.01% and 2.03 ± 0.11%, respectively). The lowest (1.34 ± 0.09%) PER value was found in treatment T40, where 40% of the FM protein was replaced by SFM protein in the diet. The survival rate of H. fossilis was not affected by the replacement of FM with SFM in the experimental diet. In the case of growth and feed utilization parameters, there was no significant difference among T0, T10, and T20 treatments.4TABLEGrowth and feed utilization performance by H. fossilis feed different experimental diets for 8 weeksTreatmentParameterT0T10T20T30T40Initial weight (g)2.41 ± 0.012.43 ± 0.012.41 ± 0.012.42 ± 0.042.41 ± 0.01Final weight (g)6.25 ± 0.116.17 ± 0.065.93 ± 0.165.25 ± 0.214.34 ± 0.11Weight gain (g)3.84 ± 0.11a3.74 ± 0.07a3.52 ± 0.16a2.83 ± 0.20b1.93 ± 0.10cWeight gain rate (%)163.32 ± 4.84a158.63 ± 3.34a154.48 ± 6.48a128.56 ± 8.25b83.24 ± 4.23cSGR (%/day)1.61 ± 0.03a1.58 ± 0.02a1.55 ± 0.04a1.37 ± 0.06b1.01 ± 0.04cFCR1.53 ± 0.01b1.54 ± 0.02b1.56 ± 0.02b1.73 ± 0.04a1.93 ± 0.15aPER2.11 ± 0.05a2.07 ± 0.01a2.03 ± 0.11ab1.89 ± 0.16b1.34 ± 0.09cSurvivability (%)100100100100100Note: Data in the same row with different superscript letters are significantly different (p < 0.05).Abbreviations: FCR, feed conversion ratio; PER, protein efficiency ratio; SGR, specific growth rate.1FIGUREPolynomial regression analysis between specific growth rate (SGR) (%/day) and replacement level of fish meal (FM) with sunflower meal (SFM) in the diet of H. fossilis (Y = − 0.000015X3 + 0.000321X2 – 0.003857X+ 1.608286, R2 = 0.972, Ymax = X value of 14.3%).Proximate composition of whole‐body carcassesCarcass composition (moisture, crude protein, total lipids, and ash) is a conventional index for estimating a carcass's quality, which can also be affected by the quality of diet. Crude protein (%), moisture (%), lipid (%), and ash (%) content of stinging catfish in various treatments are compiled in Table 5. A significant difference in proximate composition in the whole body carcass among the treatments (p < 0.05) was observed at the end of the feeding trial. The result showed that the maximum value of protein (15.75 ± 0.06%), lipid (5.80 ± 0.06%), and ash (2.74 ± 0.02%) contents were found in T0 treatment. Carcass protein, lipid, and ash contents gradually decreased with the increasing level of SFM; however, a drastic decline was observed in T30 and T40 treatments at 30% and 40% level of replacement, respectively. On the other hand, moisture content increased when the inclusion level of SFM increased in different diets.5TABLEProximate carcass composition (% on fresh weight basis) of H. fossilis fed different level of sunflower meal (SFM)‐incorporated diets for 8 weeksTreatmentParameterT0T10T20T30T40Crude protein15.75 ± 0.06a15.73 ± 0.05a15.66 ± 0.04ab15.55 ± 0.03bc15.52 ± 0.06cMoisture74.22 ± 0.06b74.28 ± 0.02b74.45 ± 0.03a74.49 ± 0.05a74.54 ± 0.03aLipid5.72 ± 0.03a5.80 ± 0.06a5.49 ± 0.09b4.19 ± 0.04d4.48 ± 0.12cAsh2.74 ± 0.02a2.69 ± 0.03ab2.65 ± 0.03b2.41 ± 0.02c2.31 ± 0.03dNote: Data in the same row with different superscript letters are significantly different (p < 0.05).Haematological parameters in H. fossilisThe haematological parameters of H. fossilis are presented in Table 6. The highest haemoglobin value was found in T0 (11.62 ± 0.04 g/dL) treatment and the lowest was in T40 (10.44 ± 0.10 g/dL) treatment. The RBC count was significantly different (p < 0.05) among the treatments, but up to 20% level of replacement, the RBC count was similar, and there was no significant difference among T0 (3.37 × 1015/mL), T10 (3.35 × 1015/mL), and T20 (3.36 × 1015/mL) treatments. However, the RBC count decreased both in T30 (3.06 × 1015/mL) and T40 (2.3 × 1015/mL) treatments. In T0, T10, and T20 treatments, there was no significant difference in Hg and RBC contents, whereas these contents decreased significantly with the higher level of inclusion of SFM.6TABLEHematological parameters of H. fossilis fed in different treatmentsTreatmentsBlood parametersT0T10T20T30T40Hg (g/dL)11.62 ± 0.04a11.61 ± 0.04a11.59 ± 0.05a11.01 ± 0.19b10.44 ± 0.10cRBC (× 1015/mL)3.37 ± 0.10a3.35 ± 0.10a3.36 ± 0.07a3.06 ± 0.04b2.3 ± 0.16cWBC (×1012/mL)9.14 ± 0.11d9.11 ± 0.12d9.33 ± 0.04c9.71 ± 0.04b10.07 ± 0.03aPCV (%)30.62 ± 0.04a30.61 ± 0.04a30.32 ± 0.04ab29.84 ± 0.07b28.54 ± 0.49cMCV (fL)91.02 ± 2.66b91.36 ± 2.92b90.39 ± 1.94b97.53 ± 0.95b124.75 ± 6.7aMCH (pg)12.71 ± 0.12a12.73 ± 0.19a12.43 ± 0.10a11.34 ± 0.20b10.36 ± 0.11cMCHC (%)37.96 ± 0.08ab37.92 ± 0.10ab38.22 ± 0.14a36.91 ± 0.57bc36.57 ± 0.67cNote: Data in the same row with different superscript letters are significantly different (p < 0.05).Abbreviations: MCH, mean corpuscular haemoglobin; MCHC, mean corpuscular haemoglobin concentration; MCV, mean corpuscular volume; PCV, packed cell volume; RBC, red blood cells; WBC, white blood cells.The highest WBC count was found in T40 (10.07 ± 0.03 × 1012/mL) treatment and the lowest in T10 (9.11 ± 0.04 × 1012/mL) treatment. From T10 treatment, the number of WBC increased gradually up to T40 treatment. The results of the present study revealed that the level of inclusion of SFM has affected the WBC count. Most of the blood parameters were insignificant up to 20% level of replacement, but PCV, MCH, and MCHC decreased and MCV increased significantly at a higher level of inclusion of SFM.DISCUSSIONThis study was designed to find out the effect of replacement of FM by SFM on growth performance, body composition, and haematological profile of H. fossilis and also to find out the optimum replacement level of FM by SFM. The water quality parameters that are the prerequisite for good fish production (Rahman et al., 2017) were within the optimum range for stinging catfish culture during the experiment (Ahmmed et al., 2017; Rahman et al., 2014; Saha et al., 2022).The growth and feed utilization parameters of H. fossilis showed no adverse impact in response to the replacement of FM with SFM up to 20% level. However, a negative response was observed at a further level of replacement of FM with SFM. Olvera‐Novoa et al. (2002) conducted an experiment on the possibility of replacing animal protein sources in tilapia diets with SFM and also found no significant effect up to 20% replacement in the body weight of redbreast tilapia T. rendalli fingerlings, while the higher replacing levels significantly decreased the body weight. Akintayo et al. (2008) recorded the effect of toasted sunflower seed meal on weight gain in the diets of African catfish (Clarias gariepinus) and found that SFM protein could replace up to 40% of FM protein. This type of processing can remove the anti‐nutritional factors from SFM and increase the replacement level. The significant factor that affected the result is perhaps the presence of some endogenous anti‐nutritional factors in SFM (Francis et al., 2001; Tacon et al., 1984). In several previous studies, it is reported that SFM contains 0.45% tannin, 0.18% oxalate, 0.16% phytate (Falaye et al., 2016), 2.85% saponin (Verma et al., 2016), 1.56%–2.70% chlorogenic acid, and 0.38%–0.48% quinic acid (Alagawany et al., 2015; Senkoylu & Dale, 1999). These anti‐nutritional factors suppress feed intake, affect metabolism, and reduce growth and feed utilization in fish (Akande et al., 2010; Francis et al., 2001; Jithender et al., 2019). The reduced growth in stinging catfish in the present study even after maintaining the best rearing condition for equal growth of all fishes is probably due to increasing anti‐nutritional factors in experimental diet with the increasing inclusion level of SFM. Moreover, among the essential AAs (arginine 2.48%, histidine 0.80%, isoleucine 1.20%, leucine 2.07%, lysine 1.01%, methionine 0.67%, phenylalanine 1.42%, threonine 1.21%, and valine 1.52%) of SFM well described earlier in other studies by several researchers, it was reported that SFM contains low levels of lysine and methionine (Alagawany et al., 2015; Batterham et al., 1978; Villamide & San Juan, 1998). The limiting AAs perhaps negatively affected the growth performance of fish. This was further confirmed by the reduced protein utilization efficiency and higher FCR of the experimental diet in the present study at a high inclusion level of SFM. Some plant protein sources such as SFM contain phosphorus phytate (77% of the total phosphorus), which binds phosphorus, reduces palatability, and interferes with the bioavailability of divalent trace elements (El‐Gendy et al., 2016; Senkoylu & Dale, 1999). In our experiment, these could also be the reasons behind the higher FCR and lower PER values when the SFM level was increased in the experimental diet. However, unlike the present findings, Rahmdel et al. (2018) found that FM in the diet could be replaced by SFM up to 75% without sacrificing the growth of common carp C. carpio. On the other hand, Dayal et al. (2011) recommended that SFM could be incorporated up to 5% level in the diet of tiger shrimp Penaeus monodon without compromising growth. This difference in the level of utilization of SFM as a replacement of FM in the diet could be due to species differences.According to Merida et al. (2010), higher SFM replacement percentages led to decreased protein, lipid, and ash retention in sea bream (Diplodus puntazzo). Olvera‐Novoa et al. (2002) also observed that increasing the percentages of SFM led to reductions in body protein in their experiment where higher protein (17.27%) content was found at a 10% replacement level and lower protein content (16.93%) was found at 50% level of replacement of FM by SFM in T. rendalli. Ahmed and Ahmad (2020) reported the highest carcass moisture and lowest lipid content in silver barb Puntius gonionotus when the experimental diet was formulated with a higher level of plant protein. The ash content of C. gariepinus was highest (3.49 ± 0.04%) when 15% SFM was used to replace FM (Jimoh, 2020). All these findings agree with the observation of the present study.The reason behind the reduction of whole body protein, lipid, and ash content at the highest SFM replacement percentages indicated a reduction in feed digestibility. High levels of indigestible carbohydrates such as dietary fibre led to intensified intestinal evacuation rates (Hardy, 2010), which caused a considerable part of dietary nutrients to be excreted before absorption. The presence of anti‐nutritional factors such as protease inhibitor and tannin in SFM, which are responsible for inhibiting protein digestibility, could explain the gradual reduction in carcass protein (Rahmdel et al., 2018). The reduction in carcass lipid at a higher replacement level might be linked with the presence of phenolic compound (chlorogenic acid) in sunflower, which has the capacity to reduce carcass lipid (Sun et al., 2017). Milić et al. (1968) also reported that chlorogenic acid present in SFM can inhibit the activity of trypsin and lipase, which are essential enzymes for metabolism of protein and lipid. The palatability of many plant materials is hampered by the presence of anti‐nutritional components and low bioavailability (Goda et al., 2007). Some plant proteins reduce palatability and interfere with the bioavailability of divalent trace elements (Francis et al., 2001). This may be the reason behind the lower ash content with higher SFM in the diet.Haematological parameters are very useful tools to determine any occurrence of infection or feed toxicity. The presence of stressors can alter blood chemistry and cause metabolic disturbance in fish (Shahi et al., 2013). According to El‐Gendy et al. (2016), haemoglobin levels in fish fed ration containing 100% SFM protein were about half as low as the control group. El‐Saidy and Gaber (2002) conducted an experiment and found the highest haemoglobin content (10.10 ± 0.12 g/dL) of O. niloticus when 15% SFM protein was used in the diet. Jimoh (2020) conducted an experiment with C. gariepinus and recorded a higher level of WBC in a higher inclusion level of sunflower seed meal. Compared to the control group, the WBC level increased proportionally with increasing substituting levels of oil seed meal (El‐Gendy et al., 2016). Rahmdel et al. (2018) conducted an experiment with common carp fingerlings and recorded haematological parameters among the fish fed the control diet and those fed differently toasted SFM up to a 100% replacement level of FM. He observed the highest RBC (3.89 ± 0.03 ×1015/L) count at lower replacement level of FM by SFM and the lowest RBC count at a higher replacement level. Merida et al. (2010) evaluated the suitability of SFM as a substitute for FM in sharp snout sea bream fingerlings and found no significant differences in the RBC content among the treatments. The progressive decrease in haemoglobin and RBC values was most likely caused by the increasing presence of anti‐nutritional factors with increasing dietary SFM level (Tacon et al., 1984). Akande et al. (2010) similarly reported that saponin, an anti‐nutritional factor found in SFM, is responsible for erythrocyte haemolysis and reduction of blood haemoglobin concentration. The increase or decrease in the WBC count in fish is a normal reaction in fish due to the presence of stressors or infection (Kori‐Siakpere et al., 2006). In the present study, the high count was associated with the excitation of the defence mechanism of fish to deal with the stressor (Parrino et al., 2018). Stress factors such as anti‐nutrient, higher fibre content, and quality of AA content could be responsible for haematological variations (Jimoh, 2020). The decrease in PCV is an indication of shrinking cell size and reduction of blood cells, which could be due to the destruction of hematopoietic tissue or inhibition of erythropoiesis (Daniel, 2018). MCV, MCH, and MCHC are called red cell indices and indicate the symptoms of blood toxicity or anaemia in animals (Demir et al., 2014). The higher MCV values indicate macrocytic anaemia, a critical condition that denotes swelling of RBC, destruction of RBC, and disturbed osmoregulation (Javed et al., 2016). Alterations in MCH and MCHC counts could be signs of disorders in hematopoietic tissues such as the liver and spleen Rahmdel et al. (2018).In conclusion, the present study revealed that replacement of FM with SFM up to 20% level gave a better result in terms of growth, feed utilization, carcass composition, and haematological parameters in stinging catfish. The inclusion level of more than 20% of SFM in the diet showed signs of impaired health status. Therefore, FM protein could be substituted with SFM protein up to 20% in the diet of H. fossilis without compromising the growth and physiological status of fish. However, based on polynomial regression analysis, the optimum level of replacement of FM protein with SFM protein was estimated to be 14.3% in the diet of H. fossilis.AUTHOR CONTRIBUTIONSAnamika Hossain:methodology; investigation; and writing – original draft. Md. Amzad Hossain: methodology; data analysis; review; and editing. Md. Golam Rasul: methodology; data analysis; review; and editing. Taslima Akter: review and editing. Md. Farid Uz Zaman: review and editing. Md. Rabiul Islam: supervision; project administration; funding acquisition; review; and editing.ACKNOWLEDGEMENTSThe authors are grateful to the Research Management Committee (RMC), BSMRAU, for funding the research and Department of Aquaculture, BSMRAU, for giving this opportunity to carry out the study.CONFLICT OF INTEREST STATEMENTThe authors declare no conflict of interest.DATA AVAILABILITY STATEMENTThe data used to support the findings of this study are included within the article.ETHICS STATEMENTThis study did not involve any endangered species. Stinging catfish (H. fossilis) is not a protected fish by Bangladeshi law. The feeding trial and subsequent handling and sampling of experimental fish were carried out as per the ethical guideline of Bangabandhu Sheikh Mujibur Rahman Agricultural University, Gazipur‐1706, Bangladesh.PEER REVIEWThe peer review history for this article is available at https://publons.com/publon/10.1002/aff2.109.REFERENCESAhmed, I. & Ahmad, I. 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Efficacy of using sunflower meal as an ingredient, and partial fishmeal‐replacer, in practical feed formulated for stinging catfish (Heteropneustes fossilis)

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Abstract

INTRODUCTIONThe stinging catfish, Heteropneustes fossilis (Bloch, 1974), belonging to the family Heteropneustidae, is a commercially vital freshwater fish species (Ali et al., 2016; Rahman et al., 2019), and commonly known as ‘shing’ or ‘singhi’ in Bangladesh and India (Khan et al., 2003; Samad et al., 2017). This species is widely available in many countries throughout the South and Southeast Asia (Talwar & Jhingran, 1991). It has gained consumer preferences and become one of the popular aquaculture species due to delicious taste and nutritional value (Chakraborty & Nur, 2012; Kohinoor et al., 2012; Nushy et al., 2020). The fish has often been regarded as a highly nutritious food fish species and is recommended as a healthy diet for recuperating patients (Nushy et al., 2020). Saha and Ratha (2007) reported that this fish can sustain prolonged periods to high levels of ammonia and low oxygen conditions and resides in low depth lentic as well as lotic waterbodies with weak water flow such as agricultural fields, swamps, and wetlands, which makes it a potential aquaculture candidate. Although the species has recently gained popularity as a commercially important fish species among fish farmers, one of its biggest challenges is its heavy reliance on commercial feed, which is expensive (Nushy et al., 2020).With the intensification of aquaculture, the demand for commercial feed has increased largely. In intensive or semi‐intensive grow‐out farming, commercial feeds are the main source of the dietary protein requirements of fish, which accounts for 60%–70% of total production costs (Khan et al., 2018). Protein is considered one of the costliest elements in fish feeds and an important factor influencing the growth performance of fish and the cost of feeds (Luo et al., 2004). In aquafeed, fish meal (FM) has been widely used as the primary source of protein due to its higher content of digestible protein with balanced amino acids (AA), including a high presence of taurine, selenium, and unsaturated fatty acids, as well as its high palatability (NRC, 2011; Luthada‐Raswiswi et al. 2021; Tacon & Metian, 2008, 2015). However, there is a big concern regarding the sustainability of using FM and fish oil from the ocean as wild marine forage fish cannot meet growing demand and will thus limit aquaculture growth (Checkley et al., 2017; Pauly & Zeller, 2016). Due to limited supply and high demand, FM has currently become the most expensive ingredient that affects the price of aquafeeds, especially for feeding carnivorous fish that requires high level of FM in the diets (Han et al., 2018). Therefore, it is crucial to find a cost‐effective and sustainable alternative protein source for FM in the diets of commercial fish species.Various plant‐based ingredients have been commonly considered as an excellent source of alternative protein for partial or complete substitution of FM in aquafeeds due to several factors, including their lower cost and more sustainability (El‐Sayed, 1999; Hardy, 2010; Liti et al., 2006; Olivera‐Castillo et al., 2011; Richie & William, 2011). A plant‐based ingredient is not only used as potential protein sources but also for nutritional‐functional requirements such as binding. The use of plant‐based proteins can substitute up to 50% of the FM in a carnivorous fish diet without causing any adverse effects on growth (Hardy, 2010). Oilseed meals are commonly known as plant‐derived protein supplements that are produced after extracting oil from oilseeds including soybeans, cottonseed, canola, peanuts, and sunflower seeds (Bernard, 2016). Among the world's most widely used oilseeds, sunflower meal (SFM) is a byproduct of the oil extraction process from sunflower seeds that has a high protein value (Saleh et al., 2021), palatability, and a low level of anti‐nutritional factors, making it an ingredient suitable for use in aquaculture diet formulations (Shchekoldina & Aider, 2014). It was found to have a high content of sulphur AA (Olvera‐Novoa et al., 2002) but a poor content of lysine (Tacon et al., 1984). According to Sanz et al. (1994), a high level of digestible protein is derived from SFM though the level of digestible energy is low because of their high fibre content.Several previous studies were found to use SFM up to 25% as a partial replacement for FM without adverse effects on the growth performance of mozambique tilapia (Oreochromis mossambicus), redbreast tilapia (Tilapia rendali), and nile tilapia (Oreochromis niloticus L.) under laboratory conditions, as reported by Jackson et al. (1982), Olvera‐Novoa et al. (2002), and Ogello et al. (2017), respectively. Partially substituting FM with SFM in the feed of trout (Oncorhynchus mykiss) significantly improved growth performance (Rab, 1993). In addition, Rahmdel et al. (2018) reported that SFM could be used in the diet of common carp (Cyprinus carpio) fingerlings to replace up to 75% of FM without any adverse effects on growth performance, body composition, haematological and biochemical parameters.Despite the availability of SFM around the world and their lower cost as an alternative potential protein source for partially replacing FM, sufficient research has not been conducted on the diet of stinging catfish. Therefore, considering the availability and nutritional aspects of SFM, this study was aimed at assessing the effects of partial replacement of FM with SFM in the practical diet on the growth performance, body composition, and haematology of stinging catfish, H. fossilis.MATERIALS AND METHODSExperimental designsThe experiment was carried out in the wet laboratory of the Department of Aquaculture, Bangabandhu Sheikh Mujibur Rahman Agricultural University, Gazipur, Bangladesh. The rearing trial was conducted for a period of 8 weeks. The experiment was conducted in a completely randomized design (CRD). A total of 15 glass aquaria of 150‐L water capacity were used for the feeding trial of the H. fossilis fingerling. All the glass aquaria were divided into five groups (one control group and four treatment groups) including three replications for each treatment where FM protein was replaced by SFM protein at a rate of 0% (T0), 10% (T10), 20% (T20), 30% (T30), and 40% (T40) levels, respectively. Each tank was stocked with 40 fish. The experimental site was facilitated with good water supply, easy access, continuous electricity, adequate inlet and outlet systems, aeration system, and other necessary facilities.Collection and rearing of experimental fishThe fingerlings of H. fossilis were collected from a commercial fish hatchery. Live and healthy fingerlings were collected and brought to the wet Laboratory, Department of Aquaculture, BSMRAU, in polythene bags with oxygen. After arriving, fish were kept in circular tanks with adequate aeration. Fish were acclimatized in a 300‐L circular tank for 1 week and fed with commercial feed containing 30% protein, 8.3% lipid, 13% ash, and 11% moisture. Then, fish were given a salt treatment with 1% salt solution before releasing into the experimental aquaria. Forty fish (initial average body weight of 2.42 ± 0.01 g) were distributed per aquarium in such a way that the biomass of all 15 aquaria became similar. The fish were fed two times a day, one in the morning and one in the evening to apparent satiation (until fish stopped feeding). The excreta of fish were cleaned by the siphoning method. Approximately 30% of the water in each aquarium was replenished every 3 days. Each aquarium was continuously aerated with an air stone that was connected to a central air compressor. A natural photoperiod (approximately 10:14 light/dark) was maintained during the experimental period.Experimental diet preparationFive iso‐nitrogenous (35% protein) diets T0, T10, T20, T30, and T40 were prepared by replacing FM protein with SFM protein at a rate of 0%, 10%, 20%, 30%, and 40%, respectively. The control diet (T0) was prepared without using SFM protein. Feed ingredients were purchased from the local feed market, and their proximate composition was analyzed (Table 1). The quality of feed ingredients was considered during purchasing. Ingredients were ground using a laboratory grinder (Panasonic AC MX‐AC400). All the ingredients were mixed properly with adequate water to prepare dough and were pelleted with a laboratory‐type pellet machine to obtain pellets of 2 mm diameter and then sun dried for 2 days. After preparing the experimental diet, the proximate composition of experimental diets were analyzed at a fish nutrition laboratory under the Department of Aquaculture, Faculty of Fisheries, Bangabandhu Sheikh Mujibur Rahman Agricultural University (Table 2). The calculated gross energy was similar in all treatments and ranged between 13.75 and 14.45 kJ/g. Finally, diets were preserved in a refrigerator (−4°C) until used.1TABLEProximate composition of different feed ingredients of H. fossilis feedIngredientsMoisture (%)Protein (%)Lipid (%)Ash (%)Fibre (%)Fish meal8.261.46.38.20.12Sunflower meal6.428.311.213.422Soybean meal8.343.66.69.25.8Rice bran10.212.313.214.18.25Mustard oil cake8.634.310.49.412.21Wheat flour8.412.13.32.30.562TABLEFormulation and proximate composition (g/100g dry matter) of experimental dietsExperimental diet (%)T0T10T20T30T40Ingredient (% dry matter basis)Fish meal26.2323.6120.9818.3615.74Sunflower meal0.005.7111.4317.1422.86Soybean meal25.5826.7427.2129.3030.00Mustard oil cake12.5012.5013.1311.2512.50Rice bran25.0020.8316.6713.338.33Wheat flour7.697.697.697.697.69Vitamin1‐premix1.001.001.001.001.00Mineral2‐premix1.001.001.001.001.00Soybean oil1.001.001.001.001.00Total100100100100100Nutrients (% dry matter basis)Protein35.10 ± 0.0335.07 ± 0.0334.98 ± 0.0534.97 ± 0.0635.11 ± 0.03Lipid6.2 ± 0.045.87 ± 0.016.39 ± 0.035.71 ± 0.085.59 ± 0.05Ash10.6 ± 0.0910.2 ± 0.0210.1 ± 0.019.60 ± 0.029.56 ± 0.02Moisture15 ± 0.0314.66 ± 0.0513.9 ± 0.0814.25 ± 0.0614.7 ± 0.171Vitamin premix (mg/kg): Hiamin‐HCl, 60; riboflavin, 200; pyridoxine‐HCl, 40; vitamin B, 0.09; 12 nicotinic acid, 800; Ca pantothenate, 280; inositol, 4000; biotin, 6; folic acid, 15; PABA, 400; choline chloride, 8000; ascorbic acid, 2000; alpha‐tocopherol, 400; menadione, 40; beta‐carotene, 12; vitamin D, 0.05. (Hossain & Furuichi, 2000a, 2000b).2Mineral premix (mg/kg): KCl, 3840; MgSO4·5H2O, 4080; NaH2 PO4·2H2O, 34,260; Fe‐citrate, 1200; AlCl3·6H2O, 45; ZnSO4·7H2O, 132; MnSO4·5H2O, 877; CuCl, 7.9; KI, 1.9; CoCl4·6H2O, 0.7. (Hossain & Furuichi, 2000a, 2000b).Monitoring water quality parametersWater quality parameters were measured every day at 9.00 AM during the study period. Water temperature (°C) was recorded using a Celsius thermometer (digi‐thermo WT‐2) from each aquarium. pH (hydrogen ion concentration) was measured using a digital pH meter (Hach Co., Colorado, USA). A digital dissolved oxygen (DO) meter (Lutron DO‐5509) was used to determine the dissolved oxygen content of water. Ammonia (mg/L) was determined by an ammonia measuring kit (Hanna Instrument Test Kit).Fish sampling and growth performanceAt the end of the experimental period, all the fish were picked up from the aquaria by scope net. Then, all the fish were counted and weighted individually by a digital electric balance (model‐EK600i) to determine the weight gain. During sampling, fish were handled very carefully. Growth performance was determined, and feed utilization was calculated according to Akter et al. (2021) and Chakraborty et al. (2021) as follows:Weight gain (g) = W2 − W1;Weight gain rate (%) = 100 (W2 − W1) / W1;Specific growth rate (SGR; %/day) = 100 [Ln W2 (g) − Ln W1 (g)]/T, where W1 is the initial fish weight, W2 is the final fish weight, and T is the rearing period (56 days);Feed intake = the total of the consumed feed (g) to fish during the rearing period;Feed conversion ratio (FCR) = dry consumed feed (g)/weight gain (g);Protein efficiency ratio (PER) = weight gain (g)/protein intake (g);Fish survival (%) = 100 (final number of fish/initial number of fish).Proximate composition analysisProximate compositions of feed ingredients, experimental diets, and fish carcasses were determined according to standard procedures given by AOAC (1997). Five fish from each tank were used to analyze the whole‐body proximate composition at the end of feeding trial. Briefly, crude protein content was determined by the Kjeldahl systematic method following acid digestion with an auto‐Kjeldahl System (UDK 152, VELP), crude lipid content was measured by ether extraction using a solvent extractor (SER 148, VELP), crude ash was detected following combusting at 550°C, and moisture content was measured by drying the samples in an oven at 105°C for 24 h. Crude fibre was detected by a fibre analyzer (FIWE 6, VELP) following the Weende method.Haematological analysisAt the end of 8‐week feeding trial, 10 fish from each treatment were randomly taken for blood collection. Blood samples were collected from the caudal vein with a 1‐mL tuberculin syringe. The needle was soaked into a 2% heparin solution as an anticoagulant during blood collection. Blood was then transferred into the tube containing ethylene diamine tetra acetic acid (EDTA) (BD Microtainer®, UK) and preserved at 4°C for haematological analyses (Neepa et al., 2022). A digital haematology analyzer (DH36, Dymind Biotechnology) was used to determine haematological parameters such as haemoglobin (Hb, g/dL), packed cell volume (PCV), white blood cells (WBC), and red blood cells (RBC). Mean corpuscular volume (MCV), mean corpuscular haemoglobin (MCH), and mean corpuscular haemoglobin concentration (MCHC) were calculated using the following formula: MCHC (%) = Hb/Hct × 100; MCV (fL) = PCV/RBC × 10; MCH (pg) = Hb/RBC × 10 (Kole et al., 2022; Mrong et al., 2021).Statistical analysisPrior to statistical analysis, all data were tested for normality and homogeneity using the Shapiro–Wilk test and Levene's test, respectively. The data were analyzed statistically by one‐way analysis of variance using statistical software Statistix 10 (2013), and significance was indicated by least significant difference option of the package. The significance level was determined at p < 0.05.RESULTSWater quality parametersDifferent physio‐chemical parameters of fish culture were recorded throughout the experimental period, which are presented in Table 3. The water temperature (°C), dissolved oxygen (mg/L), hydrogen ion concentration (pH), and ammonia‐nitrogen (mg/L) ranged from 26.19 to 27.35°C (26.77 ± 0.16; mean ± SD), 6.12 to 6.95 mg/L (6.55 ± 0.10; mean ± SD), 6.21 to 7.34 (6.75 ± 0.13; mean ± SD), and 0.35 to 0.55 mg/L (0.43 ± 0.02; mean ± SD), respectively. However, there was no significant (p > 0.05) variation in water quality parameters among the tanks in the same sampling day.3TABLERanges of water quality parameters recorded from different treatments during the experimental periodTreatmentWater temperature (°C)pHDO (mg/L)Total ammonia (mg/L)T026.18–27.276.21–6.686.23–6.950.35–0.45T1026.21–27.226.23–6.866.76–6.850.37–0.44T2026.51–27.246.25–6.866.71–6.950.35–0.46T3026.22–27.356.85–7.326.12–6.350.35–0.55T4026.42–27.156.92–7.346.18–6.440.44–0.54Growth and feed utilization performance of H. fossilisThe effects of five experimental diets containing different levels of SFM on the growth and feed utilization of H. fossilis were investigated during the experiment (Table 4). Statistical analysis showed that all growth and feed utilization parameters of fish were significantly different among the treatments (p ˂ 0.05). Significantly, the best growth performance (weight gain 6.25 ± 0.11g, % weight gain 163.32 ± 4.84, SGR 1.61 ± 0.03%/day) was observed in the control treatment (T0), but there was no significant difference among T0, T10, and T20 treatments where FM protein was replaced by SFM protein at 0%, 10%, and 20% levels, respectively. However, there is a negative impact of higher level of replacement of FM with SFM on growth performance. The lowest weight gain (1.93 ± 0.10 g), % weight gain (83.24 ± 4.23 g), and SGR (1.01 ± 0.04%/day) were observed in T40 treatment where SFM protein replaced 40% of FM protein in diet. In regression analysis, cubic model (Y = −0.000015X3 + 0.000321X2 – 0.003857X + 1.608286, R2 = 0.972, Ymax = X value of 14.3%) was found to be the most suitable model between SGR and replacement level of FM with SFM, and the optimum replacement level of FM with SFM was determined to be 14.3% for stinging catfish diet (Figure 1). The mean values of FCR were observed as 1.53 ± 0.01, 1.54 ± 0.02, 1.56 ± 0.02, 1.73 ± 0.04, and 1.93 ± 0.15 in treatments T0, T10, T20, T30, and T40, respectively. The highest PER (2.11 ± 0.05) was found in treatment T0, but there was no significant difference between T0, T10, and T20 treatments (2.11 ± 0.05%, 2.07 ± 0.01% and 2.03 ± 0.11%, respectively). The lowest (1.34 ± 0.09%) PER value was found in treatment T40, where 40% of the FM protein was replaced by SFM protein in the diet. The survival rate of H. fossilis was not affected by the replacement of FM with SFM in the experimental diet. In the case of growth and feed utilization parameters, there was no significant difference among T0, T10, and T20 treatments.4TABLEGrowth and feed utilization performance by H. fossilis feed different experimental diets for 8 weeksTreatmentParameterT0T10T20T30T40Initial weight (g)2.41 ± 0.012.43 ± 0.012.41 ± 0.012.42 ± 0.042.41 ± 0.01Final weight (g)6.25 ± 0.116.17 ± 0.065.93 ± 0.165.25 ± 0.214.34 ± 0.11Weight gain (g)3.84 ± 0.11a3.74 ± 0.07a3.52 ± 0.16a2.83 ± 0.20b1.93 ± 0.10cWeight gain rate (%)163.32 ± 4.84a158.63 ± 3.34a154.48 ± 6.48a128.56 ± 8.25b83.24 ± 4.23cSGR (%/day)1.61 ± 0.03a1.58 ± 0.02a1.55 ± 0.04a1.37 ± 0.06b1.01 ± 0.04cFCR1.53 ± 0.01b1.54 ± 0.02b1.56 ± 0.02b1.73 ± 0.04a1.93 ± 0.15aPER2.11 ± 0.05a2.07 ± 0.01a2.03 ± 0.11ab1.89 ± 0.16b1.34 ± 0.09cSurvivability (%)100100100100100Note: Data in the same row with different superscript letters are significantly different (p < 0.05).Abbreviations: FCR, feed conversion ratio; PER, protein efficiency ratio; SGR, specific growth rate.1FIGUREPolynomial regression analysis between specific growth rate (SGR) (%/day) and replacement level of fish meal (FM) with sunflower meal (SFM) in the diet of H. fossilis (Y = − 0.000015X3 + 0.000321X2 – 0.003857X+ 1.608286, R2 = 0.972, Ymax = X value of 14.3%).Proximate composition of whole‐body carcassesCarcass composition (moisture, crude protein, total lipids, and ash) is a conventional index for estimating a carcass's quality, which can also be affected by the quality of diet. Crude protein (%), moisture (%), lipid (%), and ash (%) content of stinging catfish in various treatments are compiled in Table 5. A significant difference in proximate composition in the whole body carcass among the treatments (p < 0.05) was observed at the end of the feeding trial. The result showed that the maximum value of protein (15.75 ± 0.06%), lipid (5.80 ± 0.06%), and ash (2.74 ± 0.02%) contents were found in T0 treatment. Carcass protein, lipid, and ash contents gradually decreased with the increasing level of SFM; however, a drastic decline was observed in T30 and T40 treatments at 30% and 40% level of replacement, respectively. On the other hand, moisture content increased when the inclusion level of SFM increased in different diets.5TABLEProximate carcass composition (% on fresh weight basis) of H. fossilis fed different level of sunflower meal (SFM)‐incorporated diets for 8 weeksTreatmentParameterT0T10T20T30T40Crude protein15.75 ± 0.06a15.73 ± 0.05a15.66 ± 0.04ab15.55 ± 0.03bc15.52 ± 0.06cMoisture74.22 ± 0.06b74.28 ± 0.02b74.45 ± 0.03a74.49 ± 0.05a74.54 ± 0.03aLipid5.72 ± 0.03a5.80 ± 0.06a5.49 ± 0.09b4.19 ± 0.04d4.48 ± 0.12cAsh2.74 ± 0.02a2.69 ± 0.03ab2.65 ± 0.03b2.41 ± 0.02c2.31 ± 0.03dNote: Data in the same row with different superscript letters are significantly different (p < 0.05).Haematological parameters in H. fossilisThe haematological parameters of H. fossilis are presented in Table 6. The highest haemoglobin value was found in T0 (11.62 ± 0.04 g/dL) treatment and the lowest was in T40 (10.44 ± 0.10 g/dL) treatment. The RBC count was significantly different (p < 0.05) among the treatments, but up to 20% level of replacement, the RBC count was similar, and there was no significant difference among T0 (3.37 × 1015/mL), T10 (3.35 × 1015/mL), and T20 (3.36 × 1015/mL) treatments. However, the RBC count decreased both in T30 (3.06 × 1015/mL) and T40 (2.3 × 1015/mL) treatments. In T0, T10, and T20 treatments, there was no significant difference in Hg and RBC contents, whereas these contents decreased significantly with the higher level of inclusion of SFM.6TABLEHematological parameters of H. fossilis fed in different treatmentsTreatmentsBlood parametersT0T10T20T30T40Hg (g/dL)11.62 ± 0.04a11.61 ± 0.04a11.59 ± 0.05a11.01 ± 0.19b10.44 ± 0.10cRBC (× 1015/mL)3.37 ± 0.10a3.35 ± 0.10a3.36 ± 0.07a3.06 ± 0.04b2.3 ± 0.16cWBC (×1012/mL)9.14 ± 0.11d9.11 ± 0.12d9.33 ± 0.04c9.71 ± 0.04b10.07 ± 0.03aPCV (%)30.62 ± 0.04a30.61 ± 0.04a30.32 ± 0.04ab29.84 ± 0.07b28.54 ± 0.49cMCV (fL)91.02 ± 2.66b91.36 ± 2.92b90.39 ± 1.94b97.53 ± 0.95b124.75 ± 6.7aMCH (pg)12.71 ± 0.12a12.73 ± 0.19a12.43 ± 0.10a11.34 ± 0.20b10.36 ± 0.11cMCHC (%)37.96 ± 0.08ab37.92 ± 0.10ab38.22 ± 0.14a36.91 ± 0.57bc36.57 ± 0.67cNote: Data in the same row with different superscript letters are significantly different (p < 0.05).Abbreviations: MCH, mean corpuscular haemoglobin; MCHC, mean corpuscular haemoglobin concentration; MCV, mean corpuscular volume; PCV, packed cell volume; RBC, red blood cells; WBC, white blood cells.The highest WBC count was found in T40 (10.07 ± 0.03 × 1012/mL) treatment and the lowest in T10 (9.11 ± 0.04 × 1012/mL) treatment. From T10 treatment, the number of WBC increased gradually up to T40 treatment. The results of the present study revealed that the level of inclusion of SFM has affected the WBC count. Most of the blood parameters were insignificant up to 20% level of replacement, but PCV, MCH, and MCHC decreased and MCV increased significantly at a higher level of inclusion of SFM.DISCUSSIONThis study was designed to find out the effect of replacement of FM by SFM on growth performance, body composition, and haematological profile of H. fossilis and also to find out the optimum replacement level of FM by SFM. The water quality parameters that are the prerequisite for good fish production (Rahman et al., 2017) were within the optimum range for stinging catfish culture during the experiment (Ahmmed et al., 2017; Rahman et al., 2014; Saha et al., 2022).The growth and feed utilization parameters of H. fossilis showed no adverse impact in response to the replacement of FM with SFM up to 20% level. However, a negative response was observed at a further level of replacement of FM with SFM. Olvera‐Novoa et al. (2002) conducted an experiment on the possibility of replacing animal protein sources in tilapia diets with SFM and also found no significant effect up to 20% replacement in the body weight of redbreast tilapia T. rendalli fingerlings, while the higher replacing levels significantly decreased the body weight. Akintayo et al. (2008) recorded the effect of toasted sunflower seed meal on weight gain in the diets of African catfish (Clarias gariepinus) and found that SFM protein could replace up to 40% of FM protein. This type of processing can remove the anti‐nutritional factors from SFM and increase the replacement level. The significant factor that affected the result is perhaps the presence of some endogenous anti‐nutritional factors in SFM (Francis et al., 2001; Tacon et al., 1984). In several previous studies, it is reported that SFM contains 0.45% tannin, 0.18% oxalate, 0.16% phytate (Falaye et al., 2016), 2.85% saponin (Verma et al., 2016), 1.56%–2.70% chlorogenic acid, and 0.38%–0.48% quinic acid (Alagawany et al., 2015; Senkoylu & Dale, 1999). These anti‐nutritional factors suppress feed intake, affect metabolism, and reduce growth and feed utilization in fish (Akande et al., 2010; Francis et al., 2001; Jithender et al., 2019). The reduced growth in stinging catfish in the present study even after maintaining the best rearing condition for equal growth of all fishes is probably due to increasing anti‐nutritional factors in experimental diet with the increasing inclusion level of SFM. Moreover, among the essential AAs (arginine 2.48%, histidine 0.80%, isoleucine 1.20%, leucine 2.07%, lysine 1.01%, methionine 0.67%, phenylalanine 1.42%, threonine 1.21%, and valine 1.52%) of SFM well described earlier in other studies by several researchers, it was reported that SFM contains low levels of lysine and methionine (Alagawany et al., 2015; Batterham et al., 1978; Villamide & San Juan, 1998). The limiting AAs perhaps negatively affected the growth performance of fish. This was further confirmed by the reduced protein utilization efficiency and higher FCR of the experimental diet in the present study at a high inclusion level of SFM. Some plant protein sources such as SFM contain phosphorus phytate (77% of the total phosphorus), which binds phosphorus, reduces palatability, and interferes with the bioavailability of divalent trace elements (El‐Gendy et al., 2016; Senkoylu & Dale, 1999). In our experiment, these could also be the reasons behind the higher FCR and lower PER values when the SFM level was increased in the experimental diet. However, unlike the present findings, Rahmdel et al. (2018) found that FM in the diet could be replaced by SFM up to 75% without sacrificing the growth of common carp C. carpio. On the other hand, Dayal et al. (2011) recommended that SFM could be incorporated up to 5% level in the diet of tiger shrimp Penaeus monodon without compromising growth. This difference in the level of utilization of SFM as a replacement of FM in the diet could be due to species differences.According to Merida et al. (2010), higher SFM replacement percentages led to decreased protein, lipid, and ash retention in sea bream (Diplodus puntazzo). Olvera‐Novoa et al. (2002) also observed that increasing the percentages of SFM led to reductions in body protein in their experiment where higher protein (17.27%) content was found at a 10% replacement level and lower protein content (16.93%) was found at 50% level of replacement of FM by SFM in T. rendalli. Ahmed and Ahmad (2020) reported the highest carcass moisture and lowest lipid content in silver barb Puntius gonionotus when the experimental diet was formulated with a higher level of plant protein. The ash content of C. gariepinus was highest (3.49 ± 0.04%) when 15% SFM was used to replace FM (Jimoh, 2020). All these findings agree with the observation of the present study.The reason behind the reduction of whole body protein, lipid, and ash content at the highest SFM replacement percentages indicated a reduction in feed digestibility. High levels of indigestible carbohydrates such as dietary fibre led to intensified intestinal evacuation rates (Hardy, 2010), which caused a considerable part of dietary nutrients to be excreted before absorption. The presence of anti‐nutritional factors such as protease inhibitor and tannin in SFM, which are responsible for inhibiting protein digestibility, could explain the gradual reduction in carcass protein (Rahmdel et al., 2018). The reduction in carcass lipid at a higher replacement level might be linked with the presence of phenolic compound (chlorogenic acid) in sunflower, which has the capacity to reduce carcass lipid (Sun et al., 2017). Milić et al. (1968) also reported that chlorogenic acid present in SFM can inhibit the activity of trypsin and lipase, which are essential enzymes for metabolism of protein and lipid. The palatability of many plant materials is hampered by the presence of anti‐nutritional components and low bioavailability (Goda et al., 2007). Some plant proteins reduce palatability and interfere with the bioavailability of divalent trace elements (Francis et al., 2001). This may be the reason behind the lower ash content with higher SFM in the diet.Haematological parameters are very useful tools to determine any occurrence of infection or feed toxicity. The presence of stressors can alter blood chemistry and cause metabolic disturbance in fish (Shahi et al., 2013). According to El‐Gendy et al. (2016), haemoglobin levels in fish fed ration containing 100% SFM protein were about half as low as the control group. El‐Saidy and Gaber (2002) conducted an experiment and found the highest haemoglobin content (10.10 ± 0.12 g/dL) of O. niloticus when 15% SFM protein was used in the diet. Jimoh (2020) conducted an experiment with C. gariepinus and recorded a higher level of WBC in a higher inclusion level of sunflower seed meal. Compared to the control group, the WBC level increased proportionally with increasing substituting levels of oil seed meal (El‐Gendy et al., 2016). Rahmdel et al. (2018) conducted an experiment with common carp fingerlings and recorded haematological parameters among the fish fed the control diet and those fed differently toasted SFM up to a 100% replacement level of FM. He observed the highest RBC (3.89 ± 0.03 ×1015/L) count at lower replacement level of FM by SFM and the lowest RBC count at a higher replacement level. Merida et al. (2010) evaluated the suitability of SFM as a substitute for FM in sharp snout sea bream fingerlings and found no significant differences in the RBC content among the treatments. The progressive decrease in haemoglobin and RBC values was most likely caused by the increasing presence of anti‐nutritional factors with increasing dietary SFM level (Tacon et al., 1984). Akande et al. (2010) similarly reported that saponin, an anti‐nutritional factor found in SFM, is responsible for erythrocyte haemolysis and reduction of blood haemoglobin concentration. The increase or decrease in the WBC count in fish is a normal reaction in fish due to the presence of stressors or infection (Kori‐Siakpere et al., 2006). In the present study, the high count was associated with the excitation of the defence mechanism of fish to deal with the stressor (Parrino et al., 2018). Stress factors such as anti‐nutrient, higher fibre content, and quality of AA content could be responsible for haematological variations (Jimoh, 2020). The decrease in PCV is an indication of shrinking cell size and reduction of blood cells, which could be due to the destruction of hematopoietic tissue or inhibition of erythropoiesis (Daniel, 2018). MCV, MCH, and MCHC are called red cell indices and indicate the symptoms of blood toxicity or anaemia in animals (Demir et al., 2014). The higher MCV values indicate macrocytic anaemia, a critical condition that denotes swelling of RBC, destruction of RBC, and disturbed osmoregulation (Javed et al., 2016). Alterations in MCH and MCHC counts could be signs of disorders in hematopoietic tissues such as the liver and spleen Rahmdel et al. (2018).In conclusion, the present study revealed that replacement of FM with SFM up to 20% level gave a better result in terms of growth, feed utilization, carcass composition, and haematological parameters in stinging catfish. The inclusion level of more than 20% of SFM in the diet showed signs of impaired health status. Therefore, FM protein could be substituted with SFM protein up to 20% in the diet of H. fossilis without compromising the growth and physiological status of fish. However, based on polynomial regression analysis, the optimum level of replacement of FM protein with SFM protein was estimated to be 14.3% in the diet of H. fossilis.AUTHOR CONTRIBUTIONSAnamika Hossain:methodology; investigation; and writing – original draft. Md. Amzad Hossain: methodology; data analysis; review; and editing. Md. Golam Rasul: methodology; data analysis; review; and editing. Taslima Akter: review and editing. Md. Farid Uz Zaman: review and editing. Md. Rabiul Islam: supervision; project administration; funding acquisition; review; and editing.ACKNOWLEDGEMENTSThe authors are grateful to the Research Management Committee (RMC), BSMRAU, for funding the research and Department of Aquaculture, BSMRAU, for giving this opportunity to carry out the study.CONFLICT OF INTEREST STATEMENTThe authors declare no conflict of interest.DATA AVAILABILITY STATEMENTThe data used to support the findings of this study are included within the article.ETHICS STATEMENTThis study did not involve any endangered species. Stinging catfish (H. fossilis) is not a protected fish by Bangladeshi law. The feeding trial and subsequent handling and sampling of experimental fish were carried out as per the ethical guideline of Bangabandhu Sheikh Mujibur Rahman Agricultural University, Gazipur‐1706, Bangladesh.PEER REVIEWThe peer review history for this article is available at https://publons.com/publon/10.1002/aff2.109.REFERENCESAhmed, I. & Ahmad, I. 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Journal

Aquaculture Fish and Fisheries – Wiley

Published: Jun 1, 2023

Keywords: feed utilization; fish meal; growth performance; Heteropneustes fossilis; immunity; sunflower meal

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