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Fishmeal is an important protein source for fish, but the increase of prices and low availability of this resource in the market motivated studies for its partial or total replacement by other protein sources (Guzel et al. 2011 and Valenzuela and Morales 2016). In Cuba, as part of import substitution, there is a search for alternative foods that allows to use national raw materials and, thus, contribute to food sustainability and sovereignty. In this context, fishery by-product silages (FS) are considered a practical and economically viable alternative to guarantee sustainable fish production (Perea et al. 2018).
The African catfish (Clarias gariepinus) is the main freshwater species of intensive culture in Cuba. They are fed with wet food (40 - 45% of dry matter), consisting of vegetable feed and FS (Toledo and Llanes 2013). Through an international project (AID010713 - IPEPAC) of the Italian Agency for Development Cooperation (AICS, initials in Italian), this feeding methodology has been extended to Sancti Spiritus province, where the extrusion of this food is foreseen. Hence, the need to carry out new studies that allow greater efficiency in the recycling of fishing by-products and finished food.
Studies of Llanes and Parisi (2020) evaluated two extruded diets with 10% (dry basis) of FS in African catfish. These authors obtained better productive and economic indicators with the inclusion of 10% of fishmeal (FM), with respect to commercial feed (control). Considering this result, the objective of this research was to evaluate the total substitution of high percentage of fishmeal for chemical silage of fishery by-products in extruded diets for Clarias gariepinus.
Materials and Methods
The bioassay was carried out in the Laboratorio de Nutrición de la Empresa de Desarrollo de Tecnologías Acuícolas (EDTA), in Cotorro municipality, Havana province.
Animals, experimental design and treatments. Clarias gariepinus fingerlings come from the juvenile area of the Unidad de Desarrollo-Innovación El Dique, of the EDTA. They spent a week of adaptation in a 4.5 m2 cement pool, where they received the catfish fry feed (35% crude protein). At the end of this time, 270 fish were caught and selected, with an average weight of 10.4 ± 0.06 g, which were randomly distributed in three treatments with three repetitions, according to a completely randomized design. The experimental units consisted of nine 68 L cement circular tanks, where 30 fish were placed and the water flow was maintained at 0.2 L/ min for 24 h.
The treatments were catfish fingerling feed (control) and two alternative diets with chemical silage of fishing by-products: one made with 98% of sulfuric acid and the other with formic acid (table 1).
Table 1 Chemical and percentual composition of experimental diets for fingerlings of Clarias gariepinus (g/100 g of dry weight)
| Ingredients | D-I Control | D-II EPS | D-III EPF |
|---|---|---|---|
| Fishmeal | 25 | - | - |
| Silage with sulfuric acid (EPS) | - | 10 | - |
| Silage with formic acid (EPF) | - | - | 10 |
| Soybean meal | 30 | 40 | 40 |
| Wheat meal | 25 | 25 | 25 |
| Wheat bran | 15 | 20 | 20 |
| Soybean oil | 4 | 3 | 3 |
| Dicalcium phosphate | - | 1 | 1 |
| Mineral and vitamin premix | 1 | 1 | 1 |
| Total | 100 | 100 | 100 |
| Dry matter, % | 88.11 | 88.46 | 89.11 |
| Crude protein, % | 34.50 | 27.91 | 27.39 |
| Ether extract, % | 7.54 | 7.66 | 7.36 |
| Crude fiber, % | 4.55 | 4.97 | 4.81 |
| Ashes, % | 8.32 | 7.18 | 7.13 |
| Digestible energy (MJ/kg) | 12.40 | 12.11 | 11.96 |
| CP/DE (g/MJ) | 27.82 | 23.04 | 22.90 |
*Vitamin-mineral mixture (kg of diet): vitamin A, 500IU; vitamin D, 100 IU; vitamin E, 75,000 mg; vitamin K, 20,000 mg; vitamin B1, 10,000 mg; vitamin B3, 30,000 mg; vitamin B6, 20,000 mg; vitamin B12, 100 mg; vitamin D, 60,000 mg; niacin, 200,000 mg; folic acid, 500 mg; biotin, 0.235 mg; selenium, 0.2 g, iron, 80 g; manganese, 100g; zinc, 80g; copper, 15g; potassium chloride, 4g; manganese oxide, 0.6g; sodium bicarbonate, 1.5g; iodine, 1.0g; cobalt, 0.25g; EPS: fish silage with sulfuric acid; EPF: fish silage with formic acid
Silage preparation. By-products of tilapia meat were used, which were ground in a meat mill (JAVAR 32, Colombia). The resulting paste was divided into two portions: one, with the addition of 2% of sulfuric acid at 98% (w/v) and the other, with 2% of formic acid (w/v). Both were stored in two covered plastic containers for seven days.
Diet preparation. Meals (fish, soybean and wheat) and wheat bran were ground in a hammer mill, to a particle size of 250 µm. It was mixed (HOBART MC-600 mixer, Canada) for 10 min. to form a homogeneous product, and, subsequently, soybean oil, vitamin-mineral mixture and FS were added wet (10% of inclusion calculated on a dry basis and after neutralization with 2.5% of calcium carbonate), and continued mixing for 5 min. The agglomeration of diets was performed with an extruder (DGP 70, China) with a diameter of 3 mm and pellets were dried in an oven (Selecta, Spain) at 60 oC for 24 h. The control food was prepared under the same conditions as the experimental ones. The bromatological determinations were carried out according to the methods described by AOAC (2016) and digestible energy was calculated regarding the caloric coefficients referred by Toledo et al. (2015).
Experimental procedure. Values of temperature and dissolved oxygen were daily taken with a digital oximeter (HANNA, Romania), and ammonium levels were determined once a week with a water colorimetric kit (Aquamerck, Germany). Diets were offered in two rations at 6% of body weight (9:00 and 15:30 h) for 60 d. Every 15 d, rations were fit, and, at the end of the bioassay, all animals were individually weighed with the use of a digital balance (Sartorius, Germany) to calculate the following productive indicators:
Final mean weight
Feed conversion (FCN) = added feed/weight gain
Protein efficiency (PE) = weight gain/ provided protein
Survival (S) = Number of final animals/number of initial animals x 100
Statistical analysis. The assumptions of normality were verified with Shapiro and Wilk (1965) test and by homogeneity of variance, according to Levene (1960) test. One-way analysis of variance was performed using the statistical package INFOSTAT version 2012 (Di Rienzo et al. 2012). When differences were found (P <0.05), means were compared by Duncan (1955) multiple range test.
Economic analysis. It was carried out according to Toledo et al. (2015). Costs of diets were calculated from the international prices of raw materials for August, 2020 (http//www.indexmundi.com) (table 2), plus 45% of additional expenses for Cuba (transportation, maquila and administrative costs) (table 2). These values were multiplied by food conversions to find out feed costs, which accounted for 60% of total production expenses. The value of the production (US $ 3,400.00 / t) and the silage were obtained from the records of the EDTA Department of Economics.
Results and Discussion
During the experimental period, temperature and dissolved oxygen of water in the containers ranged between 25.7 and 26.9 oC, and between 5.1 and 6.0 mg/L, respectively. Ammonia level was maintained close to 0.01 mg/L through water circulation. These values are considered comfortable for the good productive performance of the species (Toledo et al. 2015).
The fast intake of both diets with FS was observed, which shows its good acceptability by the fish throughout the bioassay. On the contrary, Llanes et al. (2017) ensiled meat by-products with 1% of sulfuric acid at 98% (w/v) and included the product in an extruded ration for African catfish. As a result, they obtained the highest feed intake and the best productive indicators with commercial feed, which they attributed to the high levels of saturated fat in meat by-products and ration acidity.
It is important to note that the pH value of the silage with 98% of sulfuric acid was between 3.2 and 3.4 during storage, values higher than those obtained in meat silages, with a pH of 1.81 (Portales et al. 2015) and 2.06 (Llanes et al. 2017) during the seven days of storage. This could indicate that the concentration of scales and spines of tilapia by-products contributes to the buffering effect on the acidity of silage, which, when subsequently neutralized with calcium carbonate, further reduces the acidity for its inclusion into the extruded diets.
No differences were found in the growth indicators and feed conversion (P <0.05) between control and FS diets (table 3). These results were favorable with respect to those reported by Llanes and Parisi (2020), who managed to substitute 15% more FM, with the same experimental diets, and they were also favorable in relation to Llanes et al. (2017), who worked with meat silage in the same species. They are also superior to those reported by Guzel et al. (2011), by substituting 50% of FM by FS in rainbow trout (Oncorhynchus mykiss), and those of Bringas et al. (2018), who only succeeded in substituting 9% of soybean meal by the inclusion of 5% of fermented silage of tilapia by-products in American catfish (Ictalurus punctatus). These variations may be possible due to the different feeding habits of the species, silage material, ingredients and their inclusion levels in rations, as well as water quality.
Table 3 Productive performance of Clarias gariepinus fingerlings when replacing fishmeal by chemical silage of fishery by-products
| Indicators | D-I Control | D-II EPS | D-III EPF | ±SE | |
|---|---|---|---|---|---|
| Final weight, g | 66.63 ± 3.51 | 66.27 ± 3.08 | 70.71 ± 3.44 | - | 0.652 |
| Feed conversion | 1.18 | 1.18 | 1.15 | 0.01 | 0.316 |
| Protein efficiency | 2.34a | 3.09b | 3.18b | 0.13 | 0.001 |
| Survival, % | 100 | 100 | 96.66 | 0.78 | 0.125 |
a,b Different letters in the same row indicate differences for P < 0.05 according to Duncan (1955)
EPS: fish silage with sulfuric acid
EPF: fish silage with formic acid
It should also be considered that the African catfish is an omnivorous species with carnivorous tendencies (Toledo et al. 2015), but it has been exploited for 20 years with a diet based, fundamentally, on plant feed. Taking this condition into account, it could be predicted that, from multiple generations of descendants, there will be an adaptation of the digestive physiology, in terms of the most efficient use of this type of protein, which would allow it to be more effective with protein of animal origin.
Protein efficiency was higher (P <0.05) for diets with FS, due to the fact that, with lower levels of dietary protein, equal weight gains were achieved with respect to control. This is related to greater availability of partially hydrolyzed protein and energy, as well as the acidification offered by FSs, which improve digestibility of nutrients and the availability of minerals such as phosphorus, which means a growth of animals (Toledo and Llanes 2013 and Suárez et al. 2018). It is also evidenced, protein savings due to the oil contribution of the FSs. These provide a lower protein/energy ratio compared to control, and the productive indicators are not affected.
Bringas et al. (2018) characterized the by-products of tilapia filleting and found all the essential amino acids, and particularly adequate concentrations of lysine (7.29 g/100g of protein) and methionine (3.99 g/100g of protein), which must be quantified in formulations for fish because they are limiting in most protein ingredients (Abdo-de la Parra et al. 2017), mainly in plant feed. In addition, the cited authors reported the fatty acid profile, in which the highest concentrations were palmitic acid C16: 0 (25.56%), palmitoleic acid C16:1 (6.70%), linoleic acid C18:2n-6 (34.31%) and linolenic acid C18:3n-3 (11.51%), and the proportion of fatty acids n-6/n-3 from 2.3 to 1, very favorable values in the nutrition of African catfish.
Raa and Gilberg (1982) reported that chemical silages have high protein hydrolysis coefficients, due to the activity of digestive enzymes, specifically proteases of the fish itself, which increase low molecular weight proteins. The increase in the content of released peptides and free amino acids can generate greater chemoattractant potential, and consequently increase the nutritional stimulus in carnivorous and omnivorous fish (Valenzuela and Morales 2016).
Survival was excellent (superior to 96.66%), which indicates that the inclusion of chemical fish silage in extruded diets does not promote mortality in fingerlings, and did not affect the productive indicators during the bioassay (table 3).
It was confirmed that there were no differences between the use of sulfuric and formic acids, with respect to growth and feed efficiency indicators (table 3). Therefore, either of the two can be used in the preparation of FS for its inclusion in dry diets, as long as they are neutralized and the pH is verified before their inclusion into the ration.
According to the consulted literature, in fish feeding, the first FSs were made with mineral acids (sulfuric and hydrochloric) and good results were obtained, but silos were not protected against Aspergillus flavus fungi, a producer of aflatoxins capable of growing on the lipid surface of FSs (Raa and Gilberg 1982). Hence, to retain bacterial growth with mineral acids, the pH must range between 2 and 3, so a rigorous neutralization will be required for its incorporation into dry rations. A recent study (Perea et al. 2018) reported that organic acids are preferred, mainly formic, because although they are more expensive, the price is offset by their antifungal power and by ensuring the preservation of the product for a longer time, without causing excessive decrease pH (close to 4), important issue in the manufacture of extruded feed.
In Cuba, there are productive experiences in the preparation of FS with sulfuric acid, in which an adequate conservation is reported for 8 and 10 days of storage, without previous neutralization, for its use in the preparation of humid rations (40-50% of dry matter), which supply 20-30% of the daily diet for African catfish, with good zootechnical results (Toledo et al. 2013). This could indicate that, in humid diets, water percentage in the ration dilutes the acidity concentration, which does not occur in extruded diets, in which extrusion concentrates the ration acidity.
The economic analysis (table 4) showed that diets with FS were less expensive, because FM was not included, which has the highest price of all protein inputs (table 2). Likewise, food costs and total expenses of production were lower with FS, due to the low cost of diets and the similar food conversions with respect to commercial feed. Therefore, they provided the highest profits and savings in the production of one ton of whole fish. Llanes and Parisi (2020) had less savings with equal diets (US $ 557.65 and 367.35), because commercial feed had 10% of FM.
Table 4 Economic analysis of the production of Clarias gariepinus with the experimental diets (US $/t)
| Indicator | D-I Control | D-II EPS | D-III EPF |
|---|---|---|---|
| Ration cost | 869.78 | 440.23 | 506.06 |
| Feeding cost | 1026.34 | 519.47 | 581.97 |
| Total production expenses | 1710.56 | 865.78 | 969.95 |
| Profits | 1689.44 | 2534.22 | 2430.05 |
| Savings | - | 844.78 | 740.61 |
Production value: $ US 3,400.00 /t of whole fish
Profits= production value - total expenses
EPS: fish silage with sulfuric acid
EPF: fish silage with formic acid
Regarding FSs, the use of 98% of sulfuric acid was the most economical alternative because this input is produced in Cuba, while formic acid is imported. Thus, the cost of processing these by-products by silage techniques with 98% of sulfuric acid was US $ 0.362/kg of dry matter (DM), while it cost US $0.816/kg of DM with formic acid. These amounts may vary depending on the price of acids and fishery by-products, but the trend is for them to be lower, compared to the use of FM (US $ 1.47/kg).
It is evident that the substitution of FM for FS in the formulation of aquaculture feeds has repercussions in the reduction of feeding costs and in obtaining higher profits, which coincides with studies by Guzel et al. (2011), Perea et al. (2018) and Llanes and Parisi (2020). FM is the key protein ingredient in feeds for fish due to its high nutritional value, but its high price does not support the development of intensive fish farming for freshwater species of low commercial value. Furthermore, its production in Cuba is not justified by the limited availability of fishery by-products. Hence, an alternative is FS made with the same raw material, to which quality and digestibility of its protein are added (Valenzuela and Morales 2016).
