INTRODUCTION
Carbohydrates should be incorporated into fish diets at appropriate levels to improve energy availability (MAAS et al., 2020), reflecting better fish development in aquaculture systems. However, fish fed with practical diets demonstrated a difference in the use of carbohydrates according to their eating habits (SOUZA et al., 2023), and carbohydrates are more readily accepted as food items by herbivorous and omnivorous fish (FELIX E SILVA et al., 2022). In general, corn meal (CM) has been used in diets for omnivorous fish as a source of energy and carbohydrates (FELIX E SILVA et al., 2020). This carbohydrate source has been considered an option to reduce the costs of manufacturing aquafeeds since it can reduce the amount of protein ingredients, the most expensive items in these diets (HEMRE et al., 2002). However, corn is a valued ingredient in the world market because it is used in the diets of several livestock species (ZHANG et al., 2021). Thus, using fruits in fish diets could be a cheaper alternative as a source of carbohydrate and energy (FELIX E SILVA et al., 2020, 2022) and can replace at least part of the amount of CM required for aquafeed formulation.
Due to its good sensory characteristics and nutritional value, the mango (Mangifera indica) is one of the world’s most cultivated tropical fruits (GOMEZ-CATURLA et al., 2022). However, the perishable nature of mango and the high losses of this fruit during the post-harvest phase affect its economic value (FELIX E SILVA et al., 2022). The post-harvest losses of this fruit can vary between 15 and 30% of its total production (PRASAD et al., 2022), constituting waste that is commonly discarded in the environment without prior treatment or being deposited in landfills or incinerated, impacting the environment (GARCÍA-MAHECHA et al., 2023). As mango is an essential source of carbohydrates, proteins, vitamins, and minerals (PATIÑO-RODRÍGUEZ et al., 2020; GOMEZ-CATURLA et al., 2022), its use in fish diets in the form of mango meal (MM) could provide an economically cheaper and potentially usable energy source in aquaculture (EYIWUNMI et al., 2021). Previous studies have already verified the potential of MM as an ingredient in the fish diet (MELO et al., 2012; SOUZA et al., 2013; DE SOUZA et al., 2018; KHIEOKHAJONKHET, 2020; FELIX E SILVA et al., 2022; CRUZ NETO et al., 2024). Furthermore, its use as a food additive would also help manage the waste produced and the fruits discarded in the environment and minimize pollution.
Conversely, mango can also have anti-nutritional effects due to its peel’s high concentration of phenols and tannins (FELIX E SILVA et al., 2022). The type and concentrations of phenolic compounds depend on the mango’s variety, place of cultivation, and maturity stage (LEBAKA et al., 2021). Therefore, it is crucial to consider that although MM has essential nutritional properties for fish growth and health, it can also contain toxic compounds that can cause harmful effects on animal development.
The piava (Megaleporinus obtusidens Valenciennes, 1837), also known as the piapara or true piau, is a species of the Anostomidae family, native to South America, which has an omnivorous feeding habit and is of great interest to fish farming of interest for human consumption (COPATTI et al., 2022a). Due to its eating habits, using fruits and their by-products, such as MM, could be a pivotal alternative in its diet. Previous studies have already shown that mango and its by-products can be used as alternative ingredients to CM in foods for omnivorous fish, such as tambaqui (Colossoma macropomum) (DE SOUZA et al., 2018), Nile tilapia (Oreochromis niloticus) (EYIWUNMI et al., 2021), and red hybrid tilapia (Oreochromis niloticus × O. mossambicus) (KHIEOKHAJONKHET, 2020). However, to our knowledge, no study has evaluated MM as an alternative to CM in diets for piavas.
Therefore, this study evaluated the possibility of totally or partially replacing CM with MM in diets for piava. So, we performed analysis in terms of zootechnical performance, plasma glucose, and intestinal enzymes.
MATERIALS AND METHODS
Local, animals, and experimental conditions
The experiment was conducted at the Aquaculture Laboratory of Universidade Federal do Vale do São Francisco (UNIVASF), Petrolina-PE, Brazil. Companhia de Desenvolvimento do Vale do São Francisco e Parnaíba in the same county supplied piava juveniles. After two weeks of adjustment, 160 fish (36.5 ± 1.8 g) were distributed in a completely randomized design (four treatments and four replications) in 500 L fiberglass tanks (n = 10 fish per tank) in a recirculation aquaculture system with constant aeration, flow rate of 60 L h-1, and physical and biological filters. The fish were fed twice daily (8:00 a.m. and 4:00 p.m.) with a commercial diet (32% crude protein; 3,600 kcal digestible energy, Supra, São Leopoldo, Brazil) until apparent satiety.
Water quality parameters remained stable during the adjustment and experiment periods. The temperature (27.11 ± 0.70 ºC), dissolved oxygen (7.11 ± 0.27 mg O2 ºL-1) (oximeter; Hanna® HI 9146, Barueri, Brazil), and pH (6.80 ± 0.29) (pH meter; Hanna® HI 98130, Barueri, Brazil) were monitored daily. The alkalinity (50.00 ± 0.00 mg CaCO3 ºL-1) and non-ionized ammonia (0.13 ± 0.02 mg NH3 ºL-1) were monitored by colorimetric analysis with the aid of a commercial kit (Alcon Ltda, Camburiú, Brazil) twice a week. The tanks were cleaned daily by siphon for waste removal and subsequent replacement with new water, representing an average renewal rate of 5% per day.
Mango meal production
Mangos (Tommy variety) not used for human consumption were purchased from a local market (Central de Comercialização e Distribuição de Frutas). Fruits that presented mechanical injuries, cuts, lack of firm texture, and reduced size were considered discarded for market and human consumption. The mangos were rinsed thoroughly in tap water to remove contaminants, followed by distilled water, 10 mL NaClO L-1, and 200 mg Cl L-1. Subsequently, the seed was removed, and the pulp and skin of the mango were cut into pieces of about 3 cm2 with a kitchen knife. Mango pieces were air dried in an oven at 55 ºC for 24 h and then ground into a fine powder using a grinder on a 1 mm sieve. The obtained meal, called MM (with peel and pulp), was stored at -20 ºC until use (according to DE SOUZA et al., 2018).
Experimental diets
Experimental diets were prepared to meet the minimum nutritional requirement for the species, above 30% of crude protein and 3,800 kcal kg-1 of gross energy (DE ALMEIDA et al., 2023). The levels of substitution of CM by MM in the diets were 0 (control), 33, 66, and 100% (Table 1). The replacement levels were based on DE SOUZA et al. (2018). These treatments represent equidistantly low (33%), intermediate (66%), and total (100%) levels of replacement of CM by MM. In addition, the CM was chosen to be replaced by MM because both are alternatives to supply energy sources and carbohydrates in the fish diet (FELIX E SILVA et al., 2020, 2022).
The diets were manufactured by grinding (hammer mill of 0.8 mm mesh), weighing and homogenizing (about 30 min), and adding water at a temperature of 50 ºC (12%). The mixture was extruded using a 1.0 mm die plate (90 ºC; 2 s) and then dehydrated in a forced-air circulation oven (55 ºC for 48 h). The pellets were stored under refrigeration (-20 ºC).
The fish were fed twice daily (8:00 a.m. and 4:00 p.m.) in the proportion of 5% of the total biomass of each experimental unit. This food management was defined based on the life phase of fish, and in a prior study with this same species, the ideal food frequency was evaluated (COPATTI et al., 2008). Every 15 days, all fish were weighed to adjust the food supply. The experiment lasted 45 days.
Chemical composition of the diets
Before preparing the experimental diets, the chemical compositions of CM, MM, and soybean meal were determined in triplicate according to AOAC (2016) (Table 2). Experimental diets were also analyzed in triplicate, according to AOAC (2016). The ether extract was determined under high pressure and temperature in an extractor (Luca-202, Lucadema, São José do Rio Preto, Brazil). The ash content was determined by combusting dry samples in a muffle furnace (TE-1100-1P, Tecnal, Piracicaba, Brazil) at 550 ºC for 4 h. The crude protein content was estimated by multiplying the nitrogen content obtained using the Kjeldahl method by 6.25 (Quimis®, Diadema, Brazil). Gross energy content was measured by combustion in a Parr bomb calorimeter (Parr 1261).
The total phenol and total tannins were analyzed only for MM. The total phenol content was analyzed as described in detail by FELIX E SILVA et al. (2020) with a spectrophotometer reading at 756 nm. The gallic acid calibration curve expressed the total phenol content as mg gallic acid equivalents (GAE) g-1. The calibration curve was obtained at 50 to 1,000 mg L-1 (R2 = 0.997). Total tannins were determined by the casein precipitation method described in detail by MONTEIRO et al. (2020). The number of total tannins corresponded to differences in absorbance of the samples precipitated with casein and those obtained by analysis of total phenols. The total tannin amounts were expressed in g kg-1 of dry material.
Microbiological analysis of mango meal
In the determination of total coliforms, the most probable number (MPN g-1) technique was used, where 1 mL aliquots were inoculated into tubes containing 9 mL of lauryl sulfate tryptase (LST) broth at 35 ºC for 48 h. The standard plate counting method was used to determine the total mold count, determining the number of colony-forming units (CFU) g-1 through surface plating. Plates were incubated at 25 ºC for seven days. The presence of Salmonella sp. was evaluated by setting the sample in lactated broth at 35 ºC for 24 h. Specific broths (Rappaport-Vassiliadis and selenite-cystine) were used for selective enrichment, and culture aliquots of the lactated broth were inoculated. The solution remained incubated at 35 ºC for 24 h. The Bacillus cereus count (CFU g-1) was enumerated by spreading on mannitol-egg yolk-polymyxin agar (MYP agar). The solution was incubated at 30 ºC for 2 h. Plates were cultured for an additional 22 h.
Microbiological analyses were adapted from the method of SILVA et al. (2010). Such analyses must comply with the parameters of Normative Instruction number 60 (BRASIL, 2019), which establishes that in farinaceous products, the count of B. cereus must be less than 5 × 103 CFU g-1, that of mold must be less than 5 × 102 CFU g-1, and total coliforms and Salmonella sp. must be absent in 25 g of product. All analyses were conducted in triplicate.
Productive performance variables
The fish were fasted for 24 h before the growth performance analysis and sample collection. The estimated production variables were:
- Survival (%) = (final fish number/initial fish number) × 100;
- Final weight (FW, g) = weight at the end of the trial period
- Weight gain (WG, g) = final body weight (g) - initial body weight (g);
- Specific growth rate (SGR, % per day) = 100 × (ln final weight (g) - ln initial weight (g))/time (days);
- Feed intake (FI, g fish-1) = total of consumed feed (g)/number of fish per tank;
- Feed conversion ratio (FCR) = feed intake (g)/weight gain (g).
Blood and intestine samples
On day 45, two fish per tank were randomly sampled for blood and intestine collection. The fish were sedated in water with benzocaine hydrochloride (50 mg L-1), and blood (1 mL) was collected from the caudal vasculature using heparinized sterile syringes. The blood was centrifuged at 3,000 g at 4 ºC (10 min), and the plasma was stored at -20 ºC for plasma glucose determinations. After blood collection, the fish were euthanized with benzocaine hydrochloride overdose (250 mg L-1) for intestine collection. The intestine was stored at -80 ºC.
Analysis of plasma glucose and intestinal enzymes
Plasma glucose (mg dL-1) was determined by a colorimetric enzymatic method using a commercial kit (Bioclin®, Belo Horizonte, Brazil), with readings performed in a spectrophotometer at 505 nm.
For analysis of intestinal enzymes (U mg protein-1), 100 mg of the whole intestinal tract was homogenized in buffer (10 mM phosphate, 20 mM Tris [pH 7.0]) using a mechanical homogenizer (Marconi MA039, Piracicaba, SP, Brazil) before centrifugation at 3,000 g for 3 min (4 ºC). The supernatant was centrifuged at 6,000 g for 8 min (4 ºC). Intestinal nonspecific alkaline protease and amylase activity was determined using kits (Labtest®, Lagoa Santa, Brazil). According to GAWLICKA et al. (2000), the intestinal lipase activity was determined.
Statistical analyses
Data are expressed as the mean ± standard error of the mean (SEM). Data were submitted to Shapiro-Wilk and Levene tests for normality and homoscedasticity. Subsequently, the data were submitted to a one-way analysis of variance (ANOVA), followed by Tukey’s test. Additionally, the results were submitted to orthogonal polynomial contrasts to determine whether there were significant linear or quadratic responses, and the best model was based on the P-value and R2-value (if the p-values were equivalents). All values were used to determine the regression effects. Differences were considered significant at P < 0.05.
RESULTS
Microbiological analysis of mango meal
The values reported in MM for molds and B. cereus were < 10 and < 100 CFU g-1, respectively (n = 3 samples). Total coliforms and Salmonella sp. were absent in MM (n = 3 samples).
Growth performance
There was no mortality, and the fish were healthy during the experiment. Fish fed with diets with 100% of the CM replaced by MM showed values significantly lower for final weight, weight gain, and feed intake and significantly higher for FCR than fish belonging to other treatments (P < 0.05). The SGR was significantly lower in the treatment with 100% MM inclusion than in the other treatments (P < 0.05) (Table 3).
The quadratic regression showed that piavas fed diets with 100% of the CM replaced by MM had lower final weight (y = 61.009 + 0.151x - 0.00319x2), weight gain (y = 24.531 + 0.156x - 0.00327x2), SGR (y = 1.138 + 0.00739x - 0.000147x2), and feed intake (y = 44.755 + 0.401x - 0.00575x2) and higher FCR (y = 1.899 - 0.0158x + 0.000357x2) than those receiving the other treatments (P < 0.05) (Table 3). According to the second-order regression analysis, the optimal level of MM inclusion in the diet estimated based on weight gain (Figure 1A) and FCR (Figure 1B) was 23.68 and 19.75%, respectively (P < 0.05).
Plasmatic glucose and intestinal enzymes
Fish that received diets with 100% of the CM replaced with MM had significantly higher plasma glucose values than those with 0 and 33% of the CM replaced with MM (P < 0.05). Linear regression analysis showed that as there was an increase in the inclusion levels of MM in the fish diet, there was a proportional increase in glycemia (y = 77.599 + 0.399x) (P < 0.05) (Table 4).
The activity of the intestinal enzymes alkaline protease and lipase was significantly higher in the control group than in the other treatments (P < 0.05). Intestinal amylase activity was significantly lower in fish fed with the diet with 100% of the CM replaced by MM than in those fed with 0 and 33% of MM inclusion (P < 0.05). The gradual increase in MM levels replacing CM in the diet reduced the activity of the intestinal enzymes amylase (y = 11.201 - 0.0601x) and lipase (y = 14.551 - 0.101x) according to linear regression and that of alkaline protease (y = 99.405 - 1.933x + 0.0121x2) according to quadratic regression (P < 0.05) (Table 4).
DISCUSSION
The results of the microbiological analysis demonstrated that MM meets the requirements of the Brazilian Ministry of Health (BRASIL, 2019) and can be used in the preparation of experimental diets for piavas. In addition, no mortality of piavas was registered in the treatments evaluated in this study.
The effects of carbohydrate sources on fish growth can be positive or negative, depending on their level of inclusion in the aquafeeds (FELIX E SILVA et al., 2022). The results of the present study demonstrated that fish growth performance can be maintained when replacing up to 66% of CM with MM. Furthermore, according to the quadratic regression for FCR and weight gain, it is possible to replace up to 19.75 and 23.68% of CM with MM, respectively, without harming the animals’ growth. Thus, under the conditions of this experiment, a 19.75 to 23.68% increment of MM with a consequent reduction in the amount of CM in diets for piavas could be safely adopted. However, replacement above this level could be disadvantageous for the zootechnical performance, as evidenced in the present study in fish fed with a diet with total replacement of CM by MM. In this study, we reported several essential findings about growth performance within 45 days of the experiment. However, a duration of 60 days can be even more advantageous for future experiments.
Unlike in our study, replacing 100% of CM with MM did not impair the zootechnical performance of Nile tilapia (MELO et al., 2012) and tambaqui (DE SOUZA et al., 2018). Conversely, SOUZA et al. (2013) and KHIEOKHAJONKHET (2020) recommended that for Nile tilapia and red hybrid tilapia diets, levels of replacement of CM by MM are between 25 and 33%. These divergent results can be explained by the difference between the species, as well as by the aquafeeds containing MM, which can affect fish nutrition by factors such as inclusion levels, types and amounts of fiber and secondary metabolites, and anti-nutritional elements (FELIX E SILVA et al., 2022; SOUZA et al., 2023).
In the current study, there was a change in the crude protein content of the ingredients, where CM and MM contained 9.90 and 4.31% crude protein, respectively. Therefore, diets with less CM and more MM had less crude protein, negatively impacting fish growth. Protein is the primary macronutrient for building tissue such as muscle, and diets with more protein can improve muscle deposition (KONNERT et al., 2022), positively affecting animal growth.
Another effect related to the protein content in the diet is the activity of digestive enzymes, which are reduced as dietary protein content is reduced (DE SOUZA, 2021). Lower activity of the intestinal enzymes investigated in this study (alkaline protease, amylase, and lipase) was recorded in the treatment with the highest MM level and, therefore, less dietary crude protein. Reducing intestinal amylase and lipase activity indicated a deficiency in the digestion and absorption of carbohydrates and lipids, with a negative impact on the use of energy sources (COPATTI et al., 2022b), while the intestinal alkaline protease activity indicated that the fish is using less protein for tissue construction (MORANTE et al., 2021). The higher proteolytic potential of piava contributed to the absorption of nutrients from diets with high amounts of proteins of plant origin, which require more complex digestion than proteins of animal origin (DE ALMEIDA et al., 2006).
The lower growth registered in fish fed a diet in which MM replaced 100% of the CM may also be related to the different sources of carbohydrates present in these ingredients. CM contains complex carbohydrates such as starch, representing about 70% of the total content (DEMIATE et al., 1997). Mangos comprise simple carbohydrates; about 17% can be glucose, while another 11% can be converted to this same carbohydrate from sucrose and fructose (BERNARDES-SILVA et al., 2003).
Glucose is the primary source of energy for animals. When found at homeostatic plasma levels, it is fundamental for the homeostasis of cellular metabolism and energy production (TEIXEIRA et al., 2018). However, if the fish are hyperglycemic, food intake tends to be reduced (WALKER et al., 2020). This behavior was observed in the present study for fish that received a diet with 100% of the CM replaced by MM. The lowest zootechnical performance in these fish was associated with the lowest feed intake, influenced by increased plasma glucose levels. Additionally, omnivorous and herbivorous fish increase gut size on higher carbohydrate diets to improve glucose absorption (HEMRE, 2002). It is presumed that using energy to build intestinal tissue reduced the energy available for building other tissue (e.g., muscle tissue), as evidenced by our study’s lower growth found in fish-fed diets with the highest MM level.
Another factor that may have impaired the growth of fish receiving the treatment with 100% MM was the presence of anti-nutritional factors. The current study showed a progressive increase in total phenols and total tannins with a rise in MM inclusion in the diets. The contents of polyphenols and tannins are influenced by the part of the fruit that was used in the preparation of the MM (DE SOUZA et al., 2018), and most compounds are present in mango peel (AJILA et al., 2010). Our study used pulp and peel to prepare the MM.
These compounds (total phenols and total tannins) reduced food consumption in fish, as they negatively affect food palatability and nutrient digestibility, in addition to being capable of triggering toxicity in animals (KOKOU & FOUNTOULAKI, 2018). Thus, the low consumption and the reduction in growth observed in the animals that received the diets with the highest levels of MM probably occurred due to higher levels of polyphenols and tannins in these diets. In addition, in the present study, the harmful effect of polyphenols and tannins may also have contributed to the decrease in the activity of digestible enzymes in fish that received diets with 100% of the CM replaced by MM.
Polyphenol compounds, especially tannins, contain hydroxyphenyl groups that, when present in the fish diet, promote changes in metabolism and, in more severe cases, cause health problems (SREERAMA et al., 2010). In the current study, although the fish fed a diet with 100% of the CM replaced by MM had a reduction in growth, there were no more severe problems, as they all survived, and there was no visualization of any sign of distress. This damage to growth performance should also have been influenced by the fact that tannins can bind to digestive enzymes, proteins, and other polymers (carbohydrates and pectins) to form stable complexes, reducing nutrient absorption (MANDAL & GHOSH, 2010). Conversely, for zebrafish (Danio rerio), dietary phenolic compounds from mango peel extract (50-200 mg kg diet-1) have been shown to have a protective effect against oxidative stress (LIZÁRRAGA-VELÁZQUEZ et al., 2019), indicating that even compounds known for their anti-nutritional products can have positive impacts on fish health. However, our study did not evaluate antioxidant activity, a relevant suggestion for future studies. Therefore, MM is a potential food to compose the nutritional matrix of aquafeeds to replace CM if it is used at levels that do not harm the growth and metabolism of the fish.
CONCLUSION
Based on the weight gain and feed conversion ratio quadratic regression, an ideal replacement level of CM by MM in piava diets would be 19.75-23.68%. At this level of inclusion, glycemia is similar to the control group. In addition, a substitution level above 33% affected the activity of the intestinal enzymes by the presence of polyphenols and tannins in the MM. Furthermore, using MM as an alternative ingredient in fish diets will add value to the non-commercialized by-products of this fruit and reduce the amount of waste discarded in the environment, minimizing pollution and health risks.
ACKNOWLEDGMENTS
This study was supported by research funds from the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior, Brazil (CAPES, Finance Code 001) for research grants provided for Marchão, R.S., da Silva, R.C., and Costa, T.S. and from the Fundação de Amparo à Ciência e Tecnologia do Estado de Pernambuco, Brazil (FACEPE) for research grants provided for Pereira, G.A. and Rocha, A.S. Copatti, C.E. is grateful to Conselho Nacional de Desenvolvimento Científico e Tecnológico, Brazil (CNPq) for the research fellowships (PQ 304329/2021-5).
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Marchão, Rafael Silva
Universidade Federal do Vale do São Francisco (UNIVASF)
Copatti, Carlos Eduardo
Universidade Federal da Bahia (UFBA)
Rocha, Aline da Silva
Universidade Federal da Bahia (UFBA)
Costa, Thaisa Sales
Universidade Federal do Vale do São Francisco (UNIVASF)
Silva, Rafael Carvalho da
Universidade Federal do Vale do São Francisco (UNIVASF)
Pereira, Gilmar Amaro
Universidade Federal do Vale do São Francisco (UNIVASF)
Rocha, David Ramos da
Universidade Federal do Vale do São Francisco (UNIVASF)
Melo, José Fernando Bibiano
Universidade Federal do Vale do São Francisco (UNIVASF)
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Abstract
Mango (Mangifera indica) production is expanding in many countries, and its discarded residues have the potential to be used in the manufacture of fish diets. This study evaluated replacing part of the corn meal (CM) with mango meal (MM) in diets for piava (Megaleporinus obtusidens) in terms of zootechnical performance, plasma glucose, and intestinal enzymes. Piavas (n = 160) were distributed in a completely randomized design (four treatments and four replications) and were fed for 45 days with diets containing different levels of MM inclusion (0, 33, 66, and 100%). There was no microbiological contamination (mold, total coliforms, Bacillus cereus, and Salmonellasp.) in MM. The MM diet had higher total phenols and total tannins (P < 0.05). Diets with 100% of the CM replaced by MM reduced the growth performance and increased the feed conversion ratio (FCR) and plasma glucose levels in piava (P < 0.05). According to the second-order regression analysis, the optimal level of MM inclusion in the diet estimated based on weight gain and FCR was 23.68 and 19.75%, respectively (P < 0.05). The gradual increase in MM levels replacing CM in the diet reduced the activity of the intestinal enzymes amylase, lipase, and alkaline protease (P < 0.05). In conclusion, we recommended replacing 19.75-23.68% of CM with MM, which can be used in piava diets.
