Use of the Brazil nut in the juvenile silver catfish diet and its effect on zootechnical performance and body composition

Iuri Moraes Neyrão1
Paulo Rodinei Soares Lopes2
1Universidade Federal do Rio Grande do Sul, Faculdade de Agronomia. Porto Alegre, Brasil.
2Universidade Federal do Pampa. Dom Pedrito, Brasil.
DOI

ABSTRACT

This work aimed to evaluate the effect of dietary Brazil nut (Bertholletia excelsa), on zootechnical performance of juveniles silver catfish (Rhamdia quelen). Fifty juveniles silver catfish (14.75 ± 1.42 g) were assigned to 5 treatments in a completely randomized design. The experimental treatments were different inclusion percentages of Brazil nut in the diet (T0, T3, T6, T9, T12) for 45 days. The variables final weight gain, average daily gain, protein efficiency rate, body protein deposition, body fat deposition, carcass yield and survival were evaluated. The data were submitted to analysis of variance, and the means compared by the Tukey test at 5 % significance. A lower final weight gain and a decrease in average daily gains were observed in the animals of the T3 group compared to T0. Protein efficiency rate, body protein and fat deposition, carcass yield and survival were not affected by the treatments evaluated. The inclusion of 3 % Brazil nut in the juveniles silver catfish diet, decreased the final weight gain and affected the average daily gain of the fish evaluated, without affecting the rest of the zootechnical variables studied.

Key words: fish feeding, aquaculture, inclusion, nutrition, Bertholletia excelsa, animal performance, carcass composition, Rhamdia quelen

Uso de la nuez de Brasil en la dieta del bagre plateado juvenil y su efecto sobre el rendimiento zootécnico y la composición corporal

RESUMEN

Este trabajo tuvo como objetivo evaluar el efecto de la nuez de Brasil (Bertholletia excelsa) en la dieta, sobre el rendimiento zootécnico de juveniles de bagre plateado (Rhamdia quelen). Se asignaron cincuenta juveniles de bagre plateado (14,75 ± 1,42 g) a 5 tratamientos en un diseño completamente al azar. Los tratamientos experimentales fueron diferentes porcentajes de inclusión de nuez de Brasil en la dieta (T0, T3, T6, T9, T12) durante 45 días. Se evaluaron las variables ganancia de peso final, ganancia diaria promedio, tasa de eficiencia proteica, deposición de proteína corporal, deposición de grasa corporal, rendimiento de canal y supervivencia. Los datos se sometieron a análisis de varianza y las medias se compararon mediante la prueba de Tukey al 5 % de significancia. Se observó una menor ganancia de peso final y una disminución en las ganancias diarias promedio en los animales del grupo T3 en comparación con T0. La tasa de eficiencia proteica, la deposición de grasas y proteínas corporales, el rendimiento de la canal y la supervivencia no se vieron afectados por los tratamientos evaluados. La inclusión de nuez de Brasil al 3 % en la dieta de juveniles de bagre plateado, disminuyó la ganancia de peso final y afectó la ganancia diaria promedio de los peces evaluados, sin afectar el resto de las variables zootécnicas estudiadas.

Palabras clave: alimentación de peces, acuicultura, inclusión, nutrición, Bertholletia excelsa, desempeño animal, composición de la canal, Rhamdia quelen

INTRODUCTION

The silver catfish is one of the 11 species that make up the genus Rhamdia. Fortynine synonyms of silver catfish (Rhamdia quelen), have been reported (Silfvergrip 1996, Scaranto et al. 2018, Koerber and Reis 2020). It is a benthic animal that analyzes the substrate and feeds on crustaceans, vegetable remains, fish, as well as terrestrial and aquatic insects (Oyakawa et al. 2006, Gomiero et al. 2007, Olaya-Nieto et al. 2010, Barreto et al. 2020). According to Parra (2008), Tessaro (2012), Decarli et al. (2016) and Gomes et al. (2019), this fish has good acceptance in the consumer market, good productivity in tanks and has a high potential for commercialization, making it a great option for promoting fish farming. Due to the great commercial importance of this teleost, known as South American catfish, further studies related to its biological characteristics are still needed.

In fish farming, as in any animal breeding, food represents a high percentage of operating costs (40 to 60 %), and protein ingredients are responsible for most of this cost (Cheng et al. 2003, Borghesi et al. 2007, El-Sayed 2019). The search for alternative food sources for feed for aquaculture species is a worldwide trend, especially foods of plant origin, which are already used in the diet of fish (Alceste and Jory 2000, Yue and Zhou 2008, Yousif et al. 2019). Thus, Brandão (2009) and Brandão et al. (2018), ratifies this use in diets, as they are rich in vitamins and compounds with antioxidant capacities. However, factors such as seasonality, non-uniform distribution, absence of established production systems for most of these species, high harvest market price and the lack of knowledge about the nutritional efficiency of these ingredients, result in the low use of these products as ingredients in the formulation of diets (Guimarães and Storti Filho 2004, Rodrigues 2014).

Plant species that can provide alternative ingredients are available in large quantities and are endemic in certain regions, which facilitates obtaining them. The use of plant species with high biological value protein has been an alternative to partially replace animal protein sources (de Souza et al. 2004, dos Santos et al. 2009). The Brazil nut Bertholletia excelsa is originally from Latin America, being found in some states of the Amazon Basin and in Peru, Colombia, Bolivia, Venezuela and Ecuador (Müller et al. 1995, Damaceno 2017). The almond of the Brazil nut, contains polyunsaturated fatty acids, a lipid fraction of good quality and high food value, which present in the following proportions: 37.42 % oleic and 37.75 % linoleic, totaling 75.17 % of total fatty acids. It also contains 24.83 % of saturated acids such as palmitic, stearic and arachidonic, with 13.15 %; 10.36 % and 1.32 %, respectively (de Souza and de Menezes 2004, da Silva et al. 2010, Cardoso et al. 2017).

Therefore, the present study aimed to evaluate the effect of the use of Brazil nut at different levels of inclusion in the diet of juvenile silver catfish, on the zootechnical performance and body composition of the animals.

MATERIALS AND METHODS

Study location and experimental design

The experiment was carried out at the Laboratory of Pisciculture and Aquaculture (LAPA) at the Federal University of Pampa, Dom Pedrito Campus, RS, Brazil (30°59'37.4"S; 54°40'02.8"W ). The experiment was conducted for 45 days (May to June 2014).

Fifty juvenile Rhamdia quelen (initial weight 14.75 ± 1.42 g) (Figure 1), from Piscicultura Bela Vista, Restinga Seca, RS, Brazil (29°42'05.9"S; 53°31'36.8"W), were assigned to completely randomized design, with 5 treatments (T0, T3, T6, T9, T12) and 2 repetitions. The fish were raised in a closed water recirculation system, using 10 experimental units containing 5 animals each.

juvenile Rhamdia quelen
Figure 1. Juvenile silver catfish Rhamdia quelen used in the study.

The experimental units were arranged on a mobile galvanized iron bench, arranged on two floors with 8 units per bench, equipped with an individual water inlet and outlet system. The water circulation in the experimental units was maintained at a volume of 1.87 liters per minute, for 24 hours a day. The system had a capacity of 948.8 liters, with 500 liters of water in the fiber box and 448.8 liters in a total of 8 experimental units of 56.1 liters each, which are supplied through a submerged pump installed in the biofilter, forming thus, the closed circulation system.

The water quality was monitored daily through the following parameters and instruments: temperature and dissolved oxygen (MO-900 meter, Instrutherm®), pH (Mpa-210A meter, MS Tecnopon®), electrical conductivity (HMCDB-150 meter, Highmed), salinity (RHB0-90, AKSO), ammonia, nitrite and alkalinity (colorimetric kit, Alfakit®).

Experimental diets and feeding management

The experimental diet was prepared in LAPA; the dry ingredients were weighed and homogenized to 1 mm. For drying, the ration was placed in an oven with forced air circulation for 48 hours (55 ºC), and then it was packed in plastic pots and conditioned in a refrigerator at a temperature of 4 ºC. The treatments were T0, T3, T6, T9 and T12 with inclusion of 0 %, 3 %, 6 %, 9 % and 12 % of Brazil nut respectively. Brazil nut used can be seen in Figure 2.

Bertholletia Seed grounded
Figure 2. Brazil nut Bertholletia excelsa grounded, used in the study.

Feeding was given twice a day (9 am and 4 pm), in the proportion of 5 % of the total biomass. The diets were isoproteic and had 3300 Kcal-1 of calculated Digestible Energy. The composition of the experimental feed was described by Coldebella and Radünz Neto (2002). The diets were analyzed at the Laboratory of Bromatology and Animal Nutrition (UNIPAMPA), according to the methodology described by AOAC (1995). The diets are described in Table 1.

Table 1. Proximate and bromatological composition of diets containing different levels of inclusion of Brazil nut (Bertholletia excelsa), in dry matter.
Treatment T0 T3 T6 T9 T12
Soybean meal 24.01 25.5 23.33 22.25 22.38
Wheat bran 7 7.5 10.02 10.39 8.89
Corn in Grain 19.21 15 11.62 10.19 9.98
Canola oil 13.03 12.25 12.28 11.42 10
Brazil nut 0 3 6 9 12
Meat Flour 35 35 35 35 35
Premix2 0.75 0.75 0.75 0.75 0.75
Salt1 1 1 1 1 1
Bromatological Composition (%) (*)
DM 96.40 97.02 97.54 97.51 97.79
CP 40.61 40.67 40.33 40.47 40.78
EE 10.22 11.81 12.02 12.54 13.05
A 7.81 7.83 7.67 7.94 7.95
CF 2.69 2.36 2.97 2.85 2.68
1According to Luchini (1990); 2Vitamin premix composition (per kg): Calcium 210 g, Phosphorus 52 g, Methionine 29.40 g, Vitamin A 140,000 IU, Vitamin D 30,000 IU, Vitamin E, 250 IU, Vitamin K3 30 mg, Vitamin B1 38 mg, Vitamin B2 100 mg, Vitamin B6 52 mg, Vitamin B12 200 mcg, Pantothenic acid 260 mg, Niacin 700 mg, Folic acid 16 mg, Choline 3,030 mg, Sodium 40.50 g, Manganese 1,870 mg, Zinc 1,750 mg, Iron 1,125 mg, Copper 200 mg, Iodine 18.75 mg, Selenium 7.50 mg, Phytase 1.500 mg, Salinomycin 1.650 mg, BHT 150 mg, Chlorohydroxyquinoline 750 mg; (*)DM = dry matter; CP = crude protein; EE = ether extract; A = ash; CF = crude fiber. Analyzed - Laboratory of Bromatology and Animal Nutrition - UNIPAMPA.

Variables studied

To assess the zootechnical performance, the parameters; Final Weight Gain (WG), Average Daily Gain (ADG), Protein Efficiency Rate (PER), Body Protein Deposition (BPD), Body Fat Deposition (BFD), Carcass Yield (CY) and Survival (S), were calculated according to Silva et al. (2018) and Bomfim et al. (2020), using initial and final body weight of fish, food consumed, analysis of body composition and diets, as follows:

  • WG = final weight - initial weight.
  • ADG =
    (final weight - initial weight) / trial period
  • PER =
    weight gain / protein ingested
  • BPD =
    (final weight × final carcass crude protein)-(initial weight × initial carcass crude protein) / 100
  • BFD =
    (final weight × final carcass fat) - (initial weight × initial carcass fat) / 100
  • CY = total weight - viscera and gills.
  • S =
    fish survivors / number of fish in each treatment
    ×100

At the beginning and the end trial, 10 animals per treatment were euthanized for initial and final carcass composition determination. These were carried out using the methodology described by Melo et al. (2002) and Hilbig et al. (2017).

Statistical analysis

The averages were submitted to analysis of variance and F test (significance level of 5 %). The means were compared using the Tukey test. The statistical package used was SAS (2001).

RESULTS AND DISCUSSION

During the experimental period, the water quality parameters were: 5.68 ± 0.11 mg L-1 (dissolved oxygen), 23.91 ± 0.25 °C (temperature), 7.45 ± 0.13 (pH), 4.16 ± 2.23 mS/Cma 25 °C (conductivity), 5.37 ± 2.06 ‰ (salinity), 55 ± 5.77 mg L-1 CaCO3 (alkalinity), 0.075 ± 0.05 mg L-1 (total ammonia), 0.04 ± 0.01 mg L-1 (nitrite). The results obtained are in accordance with Boyd et al. (1997) and Lopes et al. (2009) for the development of fish and by Piedras et al. (2004, 2005) for the species R. quelen. The results of the zootechnical performance evaluation are described in Table 2.

Table 2. Zootechnical parameters of juvenile silver catfish (Rhamdia quelen) fed a diet containing different levels of inclusion of Brazil nut (Bertholletia excelsa), at 45 experimental days.
Treatment T0 T3 T6 T9 T12 P
WG (g) 11.68 ± 6.61a 4.15 ± 2.22b 8.66 ± 5.13ab 6.49 ± 3.20ab 7.6 ± 4.30ab 0.0455
ADG (g.day-1) 0.95 ± 0.28a 0.67 ± 0.11b 0.82 ± 0.22ab 0.75 ± 0.16ab 0.8 ± 0.20ab 0.0487
PER (g) 0.28 ± 0.18 0.10 ± 0.07 0.21 ± 0.17 0.16 ± 0.10 0.18 ± 0.17 0.0955
BPD (g) 8.18 ± 4.96 3.29 ± 1.98 6.20 ± 4.59 4.59 ± 2.77 5.30 ± 4.42 0.0981
BFD (g) 2.16 ± 1.22 0.39 ± 0.39 1.44 ± 1.05 1.12 ± 0.65 1.28 ± 1.03 0,0975
CY (g) 82.13 ± 29.94 81.42 ± 14.63 82.46 ± 35.39 82.29 ± 19.05 86.54 ± 40 0.9955
S (%) 100 100 100 100 100  
Different letters in the lines show a significant difference by the Tukey test (P>0.05). WG = final weight gain; ADG = average daily gain; PER = protein efficiency rate; BPD = body protein deposition; BFD = body fat deposition; CY = carcass yield; S = percentage of survivors.

The final weight gain of the fish in T3 group was lower compared to T0 (P= 0.0455). There was no difference among T0 and the rest treatments. This variation between treatments could be caused by the appearance of antinutritional factors due to the dietary adjustment of soybean meal in the formulation of the T3 diet (being the item of greatest value in the proximate composition of T3 diet). Studies carried out by Stech et al. (2010) demonstrated the presence of antinutritional factors (tannins) in soybean meal, which can affect protease inhibition and consequently generates less weight gain. Less weight gain has been observed in Oreochromis niloticus fed with a diet containing 66 and 100 % of mango flour as a carbohydrate (de Lima et al. 2011). Likewise, Guimarães et al. (2009) observed a significant reduction in WG and feed intake in O. niloticus, when using mesquite pod bran partially replacing corn in the diet, particularly as the bran levels increased. In contrast, satisfactory results have been reported with the use of cottonseed meal for O. niloticus fingerlings, canola and cottonseed meal for Leporinus macrocephalus and fingerlings, canola and sunflower meal for juveniles O. niloticus (Furuya et al. 2000, Galdioli et al. 2001, de Souza and Hayashi 2003).

Average daily gain (ADG) was affected by treatments (P=0.0487). Greater gain in T0 was observed compared to T3 (Table 3), but not among T0 and the other treatments. Similar results were reported by Lui et al. (2012), who evaluated organic wheat to replace organic corn, in the juvenile O. niloticus diets. Opposite results were found by Jesus et al. (2011), in O. niloticus fed with diets supplemented with 20 % of Prosopis juliflora bran and Manihot esculenta leaf. In this experiment, the fish presented satisfactory results, without compromising ADG. Likewise, Azevedo et al. (2013) showed positive results in juvenile O. niloticus, fed with diets containing palm oil cake. It was observed better zootechnical performance, without altering body characteristics, energy retention and plasma cholesterol level.

Table 3. Bromatological composition of the carcass of juvenile silver catfish (Rhamdia quelen) containing different levels of inclusion of Brazil nut (Bertholletia excelsa), in dry matter.
  Begin T0 T3 T6 T9 T12
DM 97.55 97.79 97.34 97.41 97.11 96.83
CP 61.46 65.21 63.59 64.61 63.99 64.46
EE 13.70 15.67 13.45 15.26 15 14.89
A 11.35 9.81 11.73 10.34 10.13 10.65
CF 2.84 2.1 2.57 3.00 2.81 2.81
DM = dry matter; CP = crude protein; EE = ether extract; A = ash; CF = crude fiber. Analyzed - Laboratory of Bromatology and Animal Nutrition - UNIPAMPA.

Protein efficiency rate (PER) was unaffected by the evaluated treatments (P = 0.0955). Previous studies have reported that the body protein percentage does not differ between fish (Ictalurus furcatus) fed with protein sources of animal or vegetable origin (Webster et al. 1995). Similar results were observed in fingerlings Prochilodus lineatus V. and Oreochromis niloticus L. during the sexual reversion period, in trials that compared meat meal and soybean meal (Galdioli et al. 2000, de Souza et al. 2004). Similar to this study, no differences were observed in Leporinus macrocephalus fed with different levels of canola meal in replacement of soybean meal (Soares et al. 2000). On the other hand, studies carried out by Hevrøy et al. (2005) indicated that the protein efficiency rate of juvenile Salmo salar was affected by the consumption of 18 to 24 % fish hydrolyzed protein.

No significant differences were observed in BDP (P = 0.0981) between the treatments tested. Different results were shown by Pradhan et al. (2018) in indian major Carps, in which an increase of the fillet protein content was observed with increased feeding levels of feed plant-ingredient-based. Protein deposition determines growth. It is a highly complex and integrated process, which involves various interactions between the mechanisms involved, such as amino acid metabolism, amino acid flux between organs, protein turnover, and skeletal muscle growth (Silva 2013). The yield and performance of R. quelen have been reported to be unaffected by dietary lipids of different sources (canola oil, cod liver oil and swine fat; Melo et al. 2002). Previous studies carried out by El-Sayed and Teshima (1992) and later confirmed by El-Sayed (2019), indicate that protein deposition in O. niloticus, is not affected by the source of dietary lipids (soy oil, cod liver oil).

The BFD values did not show significant differences between the evaluated treatments (P = 0.0975). Similar results were found by Baoshan et al. (2019), using wheat germ oil in the juvenile hybrid grouper feed. The contents of crude lipid of whole fish were not affected by diet. Opposite results were reported by Pradhan et al. (2018) in Catla catla and Labeo rohita, in which an increase of the fillet lipid content was observed with increased feeding levels of feed plant-ingredient-based. Studies conducted by Bomfim et al. (2005) in Prochilodus affins, concluding that fish fed diets containing a higher energy level showed greater body fat gain than those fed with diets containing lower energy levels.

There was no significant difference in carcass performance among the treatments tested (P = 0.9955). Similar results were found by Pradhan et al. (2018), during carcass traits evaluation of indian major Carps fed plant-ingredient-based feed. Likewise, Li et al. (2017), did not observe differences in the carcass yield of the Pond-raised Hybrid Catfish, fed with vegetable protein sources. The inclusion of mango residue bran (0, 5, 10 and 15 %) in the juveniles O. niloticus diet, produced carcass yield values close to those obtained in this experiment (de Lima et al. 2011). Lower CY values (60.93 %) were found by Lanna et al. (2004) in the evaluation of sugarcane bagasse in the diet of O. niloticus.

Survival rates of all experimental groups were 100 %, and not affected by Brazil nut. Similar results have been observed in L. macrocephalus subjected to diets with different levels of triticale (Nagae et al. 2001). The same result was reported in groups of Ctenopharyngodon idella fed different levels of inclusion of cassava bran in replacement of corn (Lacerda et al. 2005). Responses lower than the values obtained in this study were reported in O. niloticus (88 %) fed with wheat (Signor et al. 2007).

Nogueira and Rodrigues (2007) reported that factors such as the imbalance of the carrying capacity and the concentration of animals in small volumes of water, has negative effect on the survival rate. Likewise, these authors indicate that up to a 10 % mortality rate is acceptable in production systems.

The bromatological composition of juveniles silver catfish included in the experiment, are described in Table 3. The chemical composition values are within the values quoted for the species (Contreras-Guzmán et al. 1994). Protein and lipid values of 68.2 % and 13.77 % respectively, have been reported in juveniles of silver catfish fed with different sources of lipids (Melo et al. 2002). Likewise, in other study evaluating the effect of feeding on the chemical composition of the R. quelen carcass, it reported similar values of 68.58 - 73.23 % CP, 1.80 - 13.54 % EE and 7.70 - 8.72 A (Melo et al. 2003). The A values ranged from 9.81 to 11.73 %, greater than those observed by Rocha et al. (2007), for R. quelen fingerlings (6.90 and 9.39 %). The values reported in this research are higher than those observed by Maia et al. (1999), in a study that evaluated the chemical composition of Prochilodus cearensis, in different months of the year (17.8 - 19.6 % protein, 2.5 - 5.2 % lipids, 1.1 - 1.7 % ash). Similarly, our results are higher than those observed in the Prochilodus genus, reported by Oliveira (1999), who showed crude protein and lipid contents between 18.0 - 20.5 % y 0.5 - 4 % respectively, for P. scrofa, P. cearensis and P. nigricans.

The results of the zootechnical performance evaluation obtained in T6, T9 and T12 groups indicate that the Brazil nut could be included in the juvenile R. quelen diet, without affecting growth performance. However, the values shown by the T3 group require careful evaluation.

CONCLUSION

The inclusion of 3 % Brazil nut (Bertholletia excelsa) in the juveniles silver catfish (Rhamdia quelen) diet, decreased the final weight gain and affected the average daily gain of the fish evaluated, without affecting the rest of the zootechnical variables studied. Further research is required to determine the adequate level of the Brazil nut in the R. quelen diet that allows to achieve an optimal zootechnical performance, as well as, to evaluate the effect of this ingredient on the antioxidant and immune response of this species.

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