Apparent digestibility coefficients for amino acids of feed ingredients in tambaqui (Colossoma macropomum) diets

Thiago Matias Torres do Nascimento Hellen Buzollo Lidiane Cristina Gonçalves de Sandre Ligia Maria Neira Eduardo Gianini Abimorad Dalton José Carneiro About the authors

ABSTRACT

This study evaluated the apparent digestibility coefficients (ADC) of essential (EAA) and non-essential (NEAA) amino acids of 13 ingredients for tambaqui (Colossoma macropomum) diets. Proteic and energetic ingredients were analyzed separately. The trial with energetic and proteic ingredients were arranged in a randomized block design, with four replicates: energetic ingredients (corn, wheat bran, broken rice, and sorghum) with four treatments, whereas proteic ingredients (corn gluten meal, soybean meal, poultry byproduct meal, salmon meal, fish meal [tilapia processing residue], wheat gluten meal, feather meal, cottonseed meal, and alcohol yeast [spray dried]) with nine treatments. Each block was considered as one round of fecal collection. A total of 420 tambaqui juveniles (mean initial weight: 70±8.58 g) were used. Among energetic ingredients, corn (94.6%) and wheat bran (91.9%) had the highest ADCEAA, followed by broken rice (75.7%), and sorghum (72.8%). On average, ADCEAA and ADCNEAA values of proteic ingredients were 79.5-98.5%, except for alcohol yeast (ADCEAA: 68.4 and ADCNEAA: 76.7%). Tryptophan was the first limiting amino acid in most ingredients tested and had the lowest chemical scores (0.06-0.51), except for wheat bran, corn gluten meal, and soybean meal, in which lysine was the first limiting amino acid. Soybean meal had the highest digestible essential amino acid index (EAAI: 1.02) and the most balanced amino acid profile, whereas wheat gluten meal had the lowest EAAI (0.48). Overall, tambaqui was very efficient to digest proteic and energetic ingredients.

Keywords:
amino acids; chemical score; digestibility; feed ingredients; fish; nutrition

Introduction

Tambaqui (Colossoma macropomum) is one of the most widely produced freshwater species in South America (Araújo-Lima and Gomes, 2005Araújo-Lima, C. A. R. M. and Gomes, L. C. 2005. Tambaqui (Colossoma macropomum). p.175-202. In: Espécies nativas para piscicultura no Brasil. Baldisserotto, B. and Gomes, L. C., eds. UFSM, Santa Maria.) and the most produced native species in continental aquaculture, with great growth in 2016 with 136.99 thousand tons (IBGE, 2016IBGE - Instituto Brasileiro de Geografia e Estatística. 2016. Produção da pecuária municipal 2016. Available at: <https://www.ibge.gov.br/media/com_materialdeapoio/arquivos/ea77821e06cad1457f9b35c1abe2137f.pdf>. Accessed on: Jan. 28, 2018.
https://www.ibge.gov.br/media/com_materi...
). Interest in the species has risen due to its adaptability to intensive production systems and artificial feeding, fast growth, omnivorous feeding habit, high feed efficiency, and excellent taste and desirable texture (Araújo-Lima and Gomes, 2005Araújo-Lima, C. A. R. M. and Gomes, L. C. 2005. Tambaqui (Colossoma macropomum). p.175-202. In: Espécies nativas para piscicultura no Brasil. Baldisserotto, B. and Gomes, L. C., eds. UFSM, Santa Maria.).

The use of balanced and highly digestible diets is crucial for sustainable fish production. Digestibility coefficients provide an indication of the amount of the nutrient that is absorbed; the higher the digestibility of the nutrient, the better it will be utilized by fish, resulting in higher production performance and reducing excretion of nutrients in the production environment (Oliveira Filho and Fracalossi, 2006Oliveira Filho, P. R. C. and Fracalossi, D. M. 2006. Coeficientes de digestibilidade aparente de ingredientes para juvenis de jundiá. Revista Brasileira de Zootecnia 35:1581-1587. https://doi.org/10.1590/S1516-35982006000600002
https://doi.org/10.1590/S1516-3598200600...
).

A previous study (Buzollo et al., 2018Buzollo, H.; Nascimento, T. M. T.; Sandre, L. C. G.; Neira, L. M.; Jomori, R. K. and Carneiro, D. J. 2018. Apparent digestibility coefficients of feedstuff used in tambaqui diets. Boletim do Instituto de Pesca 44:e316.) highlighted the importance of studies on nutrient digestibility of conventional feed ingredients used by the aquafeed industry to maximize production and reduce operating costs and levels of nitrogen, phosphorus, and organic matter released into effluents of fisheries. However, no study has evaluated the digestibility of amino acids in ingredients used in commercial tambaqui diets. Thus, limited information is available for the formulation of balanced diets for commercial tambaqui production.

We aimed to determine the apparent digestibility coefficients of amino acids of 13 ingredients, which were divided into energetic (corn, wheat bran, broken rice, and sorghum) and proteic (corn gluten meal, soybean meal, poultry byproduct meal, salmon meal, fish meal [tilapia processing residue], wheat gluten meal, feather meal, cottonseed meal, and alcohol yeast [spray dried]) ingredients. The chemical score of each amino acid was calculated, and the amino acid profile of each ingredient compared to that of tambaqui white muscle to determine the limiting digestible amino acids of each ingredient.

Material and Methods

The experimental trial was conducted in Jaboticabal, SP, Brazil (21°15'07.5" S, 48°19'46.0" W), in accordance with the ethical principles for animal experimentation adopted by the Brazilian College of Animal Experimentation (COBEA) and was approved by the Ethics Committee on Animal Use (case no. 016114/11).

In total, 420 tambaqui juveniles (mean initial weight: 70±8.58 g) were used in the study. The animals were kept in 28 tanks (430 L) provided with continuous aeration and water from a flowing artesian well (renewal rate: ∼10 times per day). The physicochemical parameters of the water were within the acceptable range for the species (Aride et al., 2004Aride, P. H. R.; Roubach, R. and Val, A. L. 2004. Water pH in central Amazon and its importance for tambaqui (Colossoma macropomum) culture. World Aquaculture 35:24-27.; Araújo Lima and Gomes, 2005Araújo-Lima, C. A. R. M. and Gomes, L. C. 2005. Tambaqui (Colossoma macropomum). p.175-202. In: Espécies nativas para piscicultura no Brasil. Baldisserotto, B. and Gomes, L. C., eds. UFSM, Santa Maria.): mean±SD, pH: 7.85±0.17; temperature: 29.72±0.34 °C; dissolved oxygen: 5.71±0.34 mg/L; electrical conductivity: 150.75±17.62 µS/cm; alkalinity: 88.67±0.82 µg/L; ammonia: 189.17±59.29 µg/L; nitrate: 419.96±100.28 µg/L; nitrite: 28.68±39.09 µg/L; and total phosphorus: 200.89±61.00 µg/L.

To determine the ADC of each ingredient, a reference diet was prepared to contain 237 g/kg of crude protein and 16.32 MJ/kg of gross energy (Table 1). The 13 test ingredients used in the experimental diets were obtained from four Brazilian industries: Guabi® (sorghum, corn gluten meal, poultry byproduct meal, wheat gluten meal, feather meal, cottonseed meal, and alcohol yeast [spray dried]), Coplana® (corn, wheat bran and soybean meal), Agromix® (broken rice), and Grupo Ambar Amaral® (fish meal [tilapia processing residue]), with exception of salmon meal that was imported from Chile, and were divided into two groups: energetic = corn, wheat bran, broken rice, and sorghum; and proteic = corn gluten meal, soybean meal, poultry byproduct meal, salmon meal, fish meal (tilapia processing residue), wheat gluten meal, feather meal, cottonseed meal, and alcohol yeast (spray dried). With these ingredients (Table 2), 13 test diets were formulated to contain 695 g/kg of the reference diet, 300 g/kg of the test ingredient (100 g/kg for wheat gluten meal due to the cohesive and viscoelastic properties of gluten that may provide result in a rubbery, dry pellet (Day at al., 2006Day, L.; Augustin, M. A.; Batey, I. L. and Wrigley, C. W. 2006. Wheat-gluten uses and industry needs. Trends in Food Science & Technology 17:82-90. https://doi.org/10.1016/j.tifs.2005.10.003
https://doi.org/10.1016/j.tifs.2005.10.0...
), and 5 g/kg of chromium-III oxide (Cr2O3) used as the inert digestibility marker. For the preparation of diets, the ingredients were ground, manually mixed, moistened, and extruded using an Exteec extruder (Ex Micro model). Pellets were dried in an oven with forced-air ventilation at 55 °C for 24 h.

Table 1
Composition and proximate analysis of reference diet (values on a dry matter basis, g/kg)
Table 2
Composition of ingredients used in experimental diets offered to juvenile tambaqui (values on dry matter basis, g/kg)

The digestibility coefficients of amino acids from the test ingredients were determined with the use of an inert marker (chromium-III oxide), according to Nose (1966)Nose, T. 1966. Recent advances in the study of fish digestion in Japan. In: Proceedings of the Symposium on Finfish Nutrition and Fish Feed Technology. EIFAC/FAO, Belgrade. 15p.. For fecal collection, 14 glass fiber collectors (80-L each) provided with continuous aeration and water circulation were constructed according to the modified Guelph system described by Abimorad and Carneiro (2004)Abimorad, E. G. and Carneiro, D. J. 2004. Métodos de coleta de fezes e determinação dos coeficientes de digestibilidade da fração protéica e da energia de alimentos para o pacu, Piaractus mesopotamicus (Holmberg, 1887). Revista Brasileira de Zootecnia 33:1101-1109. https://doi.org/10.1590/S1516-35982004000500001
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. Fecal collection from the four replicates of the 14 treatments (13 test diets and a reference diet) was divided into two periods. First period – distribution of replicates 1 and 2 in 28 feeding tanks. The adaptation to the diets was carried out for seven days. On day 8, feces were collected from replicate 1 (first 14 feeding tanks), and on day 9, from replicate 2 (another 14 feeding tanks). Second period – redistribution of the diets of replicates 3 and 4 in 28 feed tanks. The adaptation to the diets was carried out for seven days. On day 8, feces were collected from replicate 3 (first 14 feeding tanks), and on day 9, from replicate 4 (another 14 feeding tanks). In both periods, the fish from each replicate were fed to apparent satiation and transferred after the last feeding of the day (18.00 h) to the conical tanks and, therefore, the collections were performed during the night. Feces were collected into Falcon conical tubes (kept on ice to reduce feces degradation), every 3 h, for ease of animal management, according to previous project, until 6.00 h of the next day. All feces collected from each replicate were lyophilized using a Thermo Electron Corporation Fisher®, freeze-dried, and analyzed.

Chromium-III oxide concentrations in diets and feces were determined by nitric-perchloric digestion according to the method described by Furukawa and Tsukahara (1966)Furukawa, A. and Tsukahara, H. 1966. On the acid digestion for the determination of chromic oxide as index substance in the study digestibility of fish feed. Bulletin of the Japanese Society of Fisheries 32:502-506.. The amino acids were analyzed using liquid chromatography in cationic exchange resin columns and post-column derivation with ninhydrin and an autoanalyzer. For the amino acid count, the samples were hydrolyzed with HCl 6 N for 22 h at 110 °C according to the method described by Moore and Stein (1963)Moore, S. and Stein, W. H. 1963. Chromatographic determination of amino acids by use of automatic recording equipament. Methods in Enzymology 6:819-831. https://doi.org/10.1016/0076-6879(63)06257-1
https://doi.org/10.1016/0076-6879(63)062...
. Tryptophan was determined after the enzymatic hydrolysis with Pronase at 40 °C for 24 h, followed by a colorimetric reaction with 4-(dimethylamino)benzaldehyde in sulfuric acid 21.2 N and read at 590 nm. The tryptophan content was calculated according to Spies (1967)Spies, J. R. 1967. Determination of tryptophan in proteins. Analytical Chemistry 39:1412-1416. https://doi.org/10.1021/ac60256a004
https://doi.org/10.1021/ac60256a004...
.

The apparent digestibility coefficient (ADC) for a test ingredients was calculated from the amount of marker and amino acid in the reference diet, test diet, and feces according to the equation of Nose (1966)Nose, T. 1966. Recent advances in the study of fish digestion in Japan. In: Proceedings of the Symposium on Finfish Nutrition and Fish Feed Technology. EIFAC/FAO, Belgrade. 15p.:

ADC = [ 1 ( % marker in diet % marker in feces × % aa in feces % aa in diet ) ] × 100

The ADC for an amino acid in a test ingredient was calculated according to the following equation of Forster (1999)Forster, I. 1999. A note on the method of calculating digestibility coefficients of nutrients provided by single ingredients to feeds of aquatic animals. Aquaculture Nutrition 5:143-145. https://doi.org/10.1046/j.1365-2095.1999.00082.x
https://doi.org/10.1046/j.1365-2095.1999...
:

ADC ingredient = [ ( a + b ) × ADC test diet ( a ) × ADC reference diet ] b

in which a = AA contribution of the reference diet to the AA content of the test diet (% AA in reference diet × 0.695), and b = AA contribution of test ingredient to AA content of test diet (% AA in test ingredient).

Amino acid limitations in test ingredients were estimated by calculating the chemical score index (CSI) for each amino acid according to the following equation of Sgarbieri (1987)Sgarbieri, V. C. 1987. Alimentação e nutrição: fator de saúde e desenvolvimento. 2.ed. UNICAMP, Campinas. 387p.:

CSI = [ % EAA in ingredient protein % corresponding EAA in muscle protein ] × 100

The essential amino acid index (EAAI) of the test ingredients were calculated according to the following equation of Oser (1959)Oser, B. L. 1959. An integrated essential amino acid index for predicting the biological value of proteins. p.281-291. In: Protein and amino acid nutrition. Albanese, A. A., ed. Academic Press, New York.:

EAAI = 100 a a p × 100 b b p × 100 c c p × 100 j j p n

in which a, b, c…j are the % digestible EAA of test ingredient protein; ap, bp, cp…jp are the % EAA in tambaqui muscle; and n = number of amino acids considered.

The two methods compare the amount of digestible AA in the ingredients with the amino acid profile of fish white muscle (Hepher, 1988Hepher B. 1988. Nutrition of pond fishes. Cambridge University Press, New York. https://doi.org/10.1017/CBO9780511735455
https://doi.org/10.1017/CBO9780511735455...
). For these calculations, nine fish (mean weight: 42.0±5.76 g) from the same population were killed by ice-slurry immersion and, white muscle samples were taken for amino acid analysis.

The essential amino acid (EAA) with the lowest chemical score index was considered the first limiting amino acid of the ingredient. The EAAI was calculated from the geometric mean of all EAA scores. Protein quality is high in ingredients with higher EAAI values.

Proteic and energetic ingredients were analyzed separately. The trial with energetic and proteic ingredients were arranged in a randomized block design, with four replicates; energetic ingredients with four treatments (ingredients) and four replicates, whereas proteic ingredients with nine treatments (ingredients) and four replicates. Each block was considered as one round of fecal collection. The ADC values were subjected to ANOVA using the PROC GLM procedure of SAS (Statistical Analysis System, version 9.2). When significant differences were detected, treatment means were compared using Tukey's test at 5% significance level.

Results

No fish mortality was observed during the experimental period. No effect of the fecal collection period (round) was observed; therefore, the ADC data of all test diets were analyzed together. Of the 13 proteic and energetic ingredients tested, only six had digestibility coefficients <70% for some amino acids, and significant differences in the ADC of amino acids were observed across ingredients (P<0.05).

High ADC values (>70%) were observed for most amino acids (Table 3), and only the ADC of arginine, phenylalanine, threonine, serine, and tyrosine for sorghum and threonine, serine, and tyrosine for broken rice were <70%. Additionally, corn (95%) and wheat bran (92%) had the highest ADC values, whereas broken rice (78.7%) and sorghum (74.6%) had the lowest ADC values.

Table 3
Apparent digestibility coefficients (ADC) for essential (EAA) and non-essential (NEAA) amino acids of energetic ingredients offered to tambaqui (%)

Mean ADCEAA and ADCNEAA values of most proteic ingredients were high (>70%; Table 4). Only wheat gluten meal, feather meal, cottonseed meal, and alcohol yeast had ADC <70% for a few amino acids. Amino acid digestibility varied across proteic ingredients, but some EAA had low ADC common to a few ingredients: arginine (wheat gluten meal, feather meal, and alcohol yeast), isoleucine (alcohol yeast), lysine (wheat gluten meal and cottonseed meal), threonine (wheat gluten meal, cottonseed meal, and alcohol yeast), and valine (alcohol yeast).

Table 4
Apparent digestibility coefficients (ADC) for essential (EAA) and non-essential (NEAA) amino acids of proteic ingredients offered to tambaqui (%)

The non-essential amino acids (NEAA) glycine and serine also had low ADC values for wheat gluten meal and alcohol yeast. Conversely, alanine had the highest ADCNEAA values (>90%) in all proteic ingredients, whereas the other NEAA had a wide variation in ADC values. Additionally, corn gluten meal and soybean meal had the highest ADCEAA (96.9 and 96.6%, respectively) and overall ADCAA (corn gluten meal: 97.6%, soybean meal: 96.6%) values.

The crude and digestible amino acid compositions of proteic and energetic test ingredients were used to calculate the chemical scores and EAAI of ingredients relative to tambaqui white muscle protein (Table 5).

Table 5
Chemical score and essential amino acid index (EAAI) of ingredients relative to juvenile tambaqui white muscle protein

Tryptophan was the first limiting amino acid in ten ingredients (CSI: 0.06-0.51) and lysine was the second limiting amino acid in eight ingredients (CSI: 0.25-0.75).

Soybean meal had the highest EAAI (1.02) and was the most complete ingredient relative to the amino acid profile of juvenile tambaqui white muscle. Conversely, wheat gluten meal had the lowest EAAI (0.48).

Discussion

Corn and wheat bran had the highest ADCEAA and ADCNEAA among energetic ingredients, in addition to the highest mean EAAI. In fish, corn digestibility depends on the digestibility capacity of each species (Halver and Hardy, 2002Halver, J. E. and Hardy, R. W. 2002. Nutrient flow and retention. p.755-770. In: Fish nutrition. 3rd ed. Halver, J. E. and Hardy, R. W., eds. Academic Press, London.). Buzollo et al. (2018)Buzollo, H.; Nascimento, T. M. T.; Sandre, L. C. G.; Neira, L. M.; Jomori, R. K. and Carneiro, D. J. 2018. Apparent digestibility coefficients of feedstuff used in tambaqui diets. Boletim do Instituto de Pesca 44:e316. evaluated the digestibility of crude protein, ether extract, and energy of some ingredients used in tambaqui diets and reported that corn had the highest ADCprotein (94.5%) of all ingredients tested. Guimarães et al. (2014)Guimarães, I. G.; Miranda, E. C. and Araújo, J. G. 2014. Coefficients of total tract apparent digestibility of some feedstuffs for Tambaqui (Colossoma macropomum). Animal Feed Science and Technology 188:150-155. https://doi.org/10.1016/j.anifeedsci.2013.11.007
https://doi.org/10.1016/j.anifeedsci.201...
, for tambaqui, and Abimorad et al. (2008)Abimorad, E. G.; Squassoni, G. H. and Carneiro, D. J. 2008. Apparent digestibility of protein, energy, and amino acids in some selected feed ingredients for pacu Piaractus mesopotamicus. Aquaculture Nutrition 14:374-380. https://doi.org/10.1111/j.1365-2095.2007.00544.x
https://doi.org/10.1111/j.1365-2095.2007...
, for pacu (Piaractus mesopotamicus) juveniles, also found high ADCprotein of corn (87.5 and 85.8%, respectively). Even though protein digestibility of corn by tambaqui and pacu is high, the comparison of amino acid profiles of ingredients and white muscle shows that corn protein quality was lower for tambaqui (EAAI: 0.84) than for pacu (EAAI: 1.03; Abimorad et al., 2008Abimorad, E. G.; Squassoni, G. H. and Carneiro, D. J. 2008. Apparent digestibility of protein, energy, and amino acids in some selected feed ingredients for pacu Piaractus mesopotamicus. Aquaculture Nutrition 14:374-380. https://doi.org/10.1111/j.1365-2095.2007.00544.x
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).

Other studies also reported lower protein and amino acid digestibility in wheat bran than in corn: Furuya et al. (2001)Furuya, W. M.; Pezzato, L. E.; Pezzato, A. C.; Barros, M. M. and Miranda, E. C. 2001. Coeficientes de digestibilidade e valores de aminoácidos digestíveis de alguns ingredientes para a tilápia do Nilo (Oreochromis niloticus). Revista Brasileira de Zootecnia 30:1143-1149. https://doi.org/10.1590/S1516-35982001000500002
https://doi.org/10.1590/S1516-3598200100...
for Nile tilapia (Oreochromis niloticus), Abimorad et al. (2008)Abimorad, E. G.; Squassoni, G. H. and Carneiro, D. J. 2008. Apparent digestibility of protein, energy, and amino acids in some selected feed ingredients for pacu Piaractus mesopotamicus. Aquaculture Nutrition 14:374-380. https://doi.org/10.1111/j.1365-2095.2007.00544.x
https://doi.org/10.1111/j.1365-2095.2007...
for pacu, and Wilson et al. (1981)Wilson, R. P.; Robinson, E. H. and Poe, W. E. 1981. Apparent and true availability of amino acids from common feed ingredients for channel catfish. Journal of Nutrition 111:923-929. https://doi.org/10.1093/jn/111.5.923
https://doi.org/10.1093/jn/111.5.923...
for channel catfish (Ictalurus punctatus). According to Furuya et al. (2001)Furuya, W. M.; Pezzato, L. E.; Pezzato, A. C.; Barros, M. M. and Miranda, E. C. 2001. Coeficientes de digestibilidade e valores de aminoácidos digestíveis de alguns ingredientes para a tilápia do Nilo (Oreochromis niloticus). Revista Brasileira de Zootecnia 30:1143-1149. https://doi.org/10.1590/S1516-35982001000500002
https://doi.org/10.1590/S1516-3598200100...
, this reduced digestibility may be due to the shorter transit time of wheat bran in the gastrointestinal tract and its high content of crude fiber and non-starch polysaccharides. In fact, some of these polysaccharides, including pentosans and beta-glucans in triticale, may act as digestibility reducers, increasing intestinal viscosity and impairing enzymatic action (Furlan et al., 1997Furlan, A. C.; Fraiha, M.; Murakami, A. E.; Martins, E. N.; Scapinello, C. and Moreira, I. 1997. Utilização de complexo multienzimático em dietas de frangos de corte contendo triticale. 1. Ensaio de digestibilidade. Revista Brasileira de Zootecnia 26:759-764.). Nevertheless, based on the high ADC values observed for tambaqui in this study, the digestibility of wheat bran and corn was not affected by crude fiber or polysaccharide content.

In this study, ADC of amino acids of broken rice were on average 16 and 13% lower than those of corn and wheat bran, respectively. These results are in agreement with our previous study (Buzollo et al., 2018Buzollo, H.; Nascimento, T. M. T.; Sandre, L. C. G.; Neira, L. M.; Jomori, R. K. and Carneiro, D. J. 2018. Apparent digestibility coefficients of feedstuff used in tambaqui diets. Boletim do Instituto de Pesca 44:e316.), in which we observed low values of ADCprotein (71.21%) of broken rice for tambaqui. These low values may be related to the high levels of trypsin inhibitors in broken rice (Butolo, 2002Butolo, J. E. 2002. Qualidade de ingredientes na alimentação animal. 1.ed. Colégio Brasileiro de Nutrição Animal, Campinas, SP.). A similar ADCprotein of broken rice (81%) was reported by Abimorad and Carneiro (2004)Abimorad, E. G. and Carneiro, D. J. 2004. Métodos de coleta de fezes e determinação dos coeficientes de digestibilidade da fração protéica e da energia de alimentos para o pacu, Piaractus mesopotamicus (Holmberg, 1887). Revista Brasileira de Zootecnia 33:1101-1109. https://doi.org/10.1590/S1516-35982004000500001
https://doi.org/10.1590/S1516-3598200400...
for pacu. However, even lower ADCprotein values were reported for other carnivorous species: 43% for Pseudoplatystoma corruscans (Gonçalves and Carneiro, 2003Gonçalves, E. G. and Carneiro, D. J. 2003. Coeficientes de digestibilidade aparente da proteina e energia de alguns ingredientes utilizados em dietas para o pintado (Pseudoplatystoma coruscans). Revista Brasileira de Zootecnia 32:779-786. https://doi.org/10.1590/S1516-35982003000400001
https://doi.org/10.1590/S1516-3598200300...
) and 71% for hybrid striped bass (Morone saxatilis × M. chrysops) (Sullivan and Reigh, 1995Sullivan, J. A. and Reigh, R. C. 1995. Apparent digestibility of selected feedstuffs in diets for hybrid striped bass (Morone saxatilis x Morone chrysops). Aquaculture 138:313-322. https://doi.org/10.1016/0044-8486(95)01071-8
https://doi.org/10.1016/0044-8486(95)010...
). In fact, the enzymatic profile of carnivorous species does not support the use of starchy foods such as broken rice (Lundstedt et al., 2004Lundstedt, L. M.; Melo, J. F. B. and Moraes, G. 2004. Digestive enzymes and metabolic profile of Pseudoplatystoma corruscans (Teleostei: Siluriformes) in response to diet composition. Comparative Biochemistry and Physiology Part B: Biochemistry and Molecular Biology 137:331-339. https://doi.org/10.1016/j.cbpc.2003.12.003
https://doi.org/10.1016/j.cbpc.2003.12.0...
). Nevertheless, higher ADCprotein values of broken rice than the ADCprotein of corn found in this study for tambaqui were reported for Rhamdia quelen (86%; Oliveira Filho and Fracalossi, 2006Oliveira Filho, P. R. C. and Fracalossi, D. M. 2006. Coeficientes de digestibilidade aparente de ingredientes para juvenis de jundiá. Revista Brasileira de Zootecnia 35:1581-1587. https://doi.org/10.1590/S1516-35982006000600002
https://doi.org/10.1590/S1516-3598200600...
) and Nile tilapia (96%; Gonçalves et al., 2007Gonçalves, G. S.; Pezzato, L. E.; Padilha, P. M. and Barros, M. M. 2007. Disponibilidade aparente do fósforo em alimentos vegetais e suplementação da enzima fitase para tilápia-do-nilo. Revista Brasileira de Zootecnia 36:1473-1480. https://doi.org/10.1590/S1516-35982007000700003
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), but these values may reflect methodological differences in fecal collection across studies.

Sorghum is the preferred substitute for corn due to its higher crude protein content and lower concentration of ether extract, lysine, and methionine in its composition (Antunes et al., 2007Antunes, R. C.; Rodriguez, N. M.; Gonçalves, L. C.; Rodrigues, J. A. S.; Borges, I.; Borges, A. L. C. C. and Saliba, E. O. S. 2007. Composição bromatológica e parâmetros físicos de grãos de sorgo com diferentes texturas do endosperma. Arquivo Brasileiro de Medicina Veterinária e Zootecnia 59:1351-1354. https://doi.org/10.1590/S0102-09352007000500042
https://doi.org/10.1590/S0102-0935200700...
). In the current study, sorghum had larger quantities of phenylalanine, isoleucine, leucine, lysine, threonine, tryptophan, and valine than corn. Nevertheless, the ADC and EAAI of sorghum were low, indicating that for tambaqui, protein quality was significantly lower in sorghum than in the other energetic ingredients tested. Similar results were reported by Buzollo et al. (2018)Buzollo, H.; Nascimento, T. M. T.; Sandre, L. C. G.; Neira, L. M.; Jomori, R. K. and Carneiro, D. J. 2018. Apparent digestibility coefficients of feedstuff used in tambaqui diets. Boletim do Instituto de Pesca 44:e316. for tambaqui and Pezzato et al. (2002)Pezzato, L. E.; Miranda, E. C.; Barros, M. M.; Pinto, L. G. Q.; Furuya, W. M. and Pezzato, A. C. 2002. Digestibilidade aparente de ingredientes para a tilápia do Nilo (Oreochromis niloticus). Revista Brasileira de Zootecnia 31:1595-1604. https://doi.org/10.1590/S1516-35982002000700001
https://doi.org/10.1590/S1516-3598200200...
, who found lower ADCprotein in sorghum than in corn for Nile tilapia. The low nutrient digestibility of sorghum may be due to tannins, which are an antinutritional factor found in many sorghum varieties (Rostagno, 1986Rostagno, H. S. 1986. Utilização do sorgo nas rações de aves e suínos. Informe Agropecuário 12:18-27.).

In general, protein digestibility of energetic ingredients by tambaqui was high. Considering the large contribution of energetic ingredients in commercial diets, we conclude that they contribute significantly to meet the amino acid requirements of the species.

Corn gluten meal and soybean meal had the highest ADC of all proteic ingredients tested. High ADCprotein values of corn gluten meal have also been reported for tambaqui 98.09% (Buzollo et al., 2018Buzollo, H.; Nascimento, T. M. T.; Sandre, L. C. G.; Neira, L. M.; Jomori, R. K. and Carneiro, D. J. 2018. Apparent digestibility coefficients of feedstuff used in tambaqui diets. Boletim do Instituto de Pesca 44:e316.) and other omnivorous and carnivorous species: 96% for Nile tilapia (Pezzato et al., 2002Pezzato, L. E.; Miranda, E. C.; Barros, M. M.; Pinto, L. G. Q.; Furuya, W. M. and Pezzato, A. C. 2002. Digestibilidade aparente de ingredientes para a tilápia do Nilo (Oreochromis niloticus). Revista Brasileira de Zootecnia 31:1595-1604. https://doi.org/10.1590/S1516-35982002000700001
https://doi.org/10.1590/S1516-3598200200...
), 93.6% for largemouth bass (Micropterus salmoides; Portz and Cyrino, 2004Portz, L. and Cyrino, J. E. P. 2004. Digestibility of nutrients and amino acids of different protein sources in practical diets by largemouth bass, Micropterus salmoides (Lacepéde, 1802). Aquaculture Research 35:312-320. https://doi.org/10.1111/j.1365-2109.2004.00984.x
https://doi.org/10.1111/j.1365-2109.2004...
), 92.3% for haddock (Melanogrammus aeglefinus; Tibbetts et al., 2004Tibbetts, S. M.; Lall, S. P. and Milley, J. E. 2004. Apparent digestibility of common feed ingredients by juvenile haddock, Melanogrammus aeglefinus L. Aquaculture Research 35:643-651. https://doi.org/10.1111/j.1365-2109.2004.01060.x
https://doi.org/10.1111/j.1365-2109.2004...
), 94.4% for cobia (Rachycentron canadum; Zhou et al., 2004Zhou, Q. C.; Tan, B. P.; Mai, K. S. and Liu, Y. J. 2004. Apparent digestibility of selected feed ingredients for juvenile cobia Rachycentron canadum. Aquaculture 241:441-451. https://doi.org/10.1016/j.aquaculture.2004.08.044
https://doi.org/10.1016/j.aquaculture.20...
), 95% for catfish (Oliveira Filho and Fracalossi, 2006Oliveira Filho, P. R. C. and Fracalossi, D. M. 2006. Coeficientes de digestibilidade aparente de ingredientes para juvenis de jundiá. Revista Brasileira de Zootecnia 35:1581-1587. https://doi.org/10.1590/S1516-35982006000600002
https://doi.org/10.1590/S1516-3598200600...
), and 95.6% for pacu (Abimorad et al., 2008Abimorad, E. G.; Squassoni, G. H. and Carneiro, D. J. 2008. Apparent digestibility of protein, energy, and amino acids in some selected feed ingredients for pacu Piaractus mesopotamicus. Aquaculture Nutrition 14:374-380. https://doi.org/10.1111/j.1365-2095.2007.00544.x
https://doi.org/10.1111/j.1365-2095.2007...
). In our study, corn gluten meal showed an imbalance in essential amino acid composition (EAAI: 0.82). The CSI for some amino acids such as leucine (2.21) and lysine (0.20) differed from this profile, and a similar imbalance in the same amino acids detected by CSI was also reported for pacu in a study by our research group (Abimorad et al., 2008Abimorad, E. G.; Squassoni, G. H. and Carneiro, D. J. 2008. Apparent digestibility of protein, energy, and amino acids in some selected feed ingredients for pacu Piaractus mesopotamicus. Aquaculture Nutrition 14:374-380. https://doi.org/10.1111/j.1365-2095.2007.00544.x
https://doi.org/10.1111/j.1365-2095.2007...
). Thus, chemical scoring of AA in our study showed that, despite its high digestibility, availability of some amino acids in corn gluten meal is limited, which may hinder its use as the primary protein source in animal diets, further increasing its inclusion cost.

Soybean meal was the best protein source for tambaqui. This ingredient had the highest EAAI (1.02) and a balanced amino acid profile with chemical scores ranging from 0.60 for lysine to 1.46 for arginine. Similar to corn gluten meal, lysine had the lowest CSI (0.60) in soybean meal. Similar results have also been reported for other species, including channel catfish (Lim et al., 1998Lim, C.; Klesius, P. H. and Higgs, D. A. 1998. Substitution of canola meal for soybean meal in diets for channel catfish Ictalurus punctatus. Journal of the World Aquaculture Society 29:161-168. https://doi.org/10.1111/j.1749-7345.1998.tb00975.x
https://doi.org/10.1111/j.1749-7345.1998...
), Nile tilapia (Furuya et al., 2001Furuya, W. M.; Pezzato, L. E.; Pezzato, A. C.; Barros, M. M. and Miranda, E. C. 2001. Coeficientes de digestibilidade e valores de aminoácidos digestíveis de alguns ingredientes para a tilápia do Nilo (Oreochromis niloticus). Revista Brasileira de Zootecnia 30:1143-1149. https://doi.org/10.1590/S1516-35982001000500002
https://doi.org/10.1590/S1516-3598200100...
; Köprücü and Özdemir, 2005Köprücü, K. and Özdemir, Y. 2005. Apparent digestibility of selected feed ingredients for Nile tilapia (Oreochromis niloticus). Aquaculture 250:308-316. https://doi.org/10.1016/j.aquaculture.2004.12.003
https://doi.org/10.1016/j.aquaculture.20...
), rainbow trout (Oncorhynchus mykiss; Cheng et al., 2003Cheng, Z. J.; Hardy, R. W. and Usry, J. L. 2003. Plant protein ingredients with lysine supplementation reduce dietary protein level in rainbow trout (Oncorhynchus mykiss) diets, and reduce ammonia nitrogen and soluble phosphorus excretion. Aquaculture 218:553-565. https://doi.org/10.1016/S0044-8486(02)00502-1
https://doi.org/10.1016/S0044-8486(02)00...
), largemouth bass (Portz and Cyrino, 2004Portz, L. and Cyrino, J. E. P. 2004. Digestibility of nutrients and amino acids of different protein sources in practical diets by largemouth bass, Micropterus salmoides (Lacepéde, 1802). Aquaculture Research 35:312-320. https://doi.org/10.1111/j.1365-2109.2004.00984.x
https://doi.org/10.1111/j.1365-2109.2004...
), Murray cod (Maccullochella peelii peelii), Australian shortfin eel (Anguilla australis; De Silva et al., 2000De Silva, S. S.; Gunasekara, R. M. and Gooley, G. 2000. Digestibility and amino acid availability of three protein-rich ingredient-incorporated diets by Murray cod Maccullochella peelii peelii (Mitchell) and Australian shortfin eel Anguilla australis Richardson. Aquaculture Research 31:195-205. https://doi.org/10.1046/j.1365-2109.2000.00432.x
https://doi.org/10.1046/j.1365-2109.2000...
), and pacu (Abimorad et al., 2008Abimorad, E. G.; Squassoni, G. H. and Carneiro, D. J. 2008. Apparent digestibility of protein, energy, and amino acids in some selected feed ingredients for pacu Piaractus mesopotamicus. Aquaculture Nutrition 14:374-380. https://doi.org/10.1111/j.1365-2095.2007.00544.x
https://doi.org/10.1111/j.1365-2095.2007...
). Other studies observed reduced growth when using soybean meal as the primary protein source in carnivorous fish diets, which was mainly attributed to antinutritional factors and methionine deficiency (Anderson et al., 1993Anderson, S. J.; Lall, S. P.; Anderson, D. M. and McNiven, M. A. 1993. Quantitative dietary lysine requirement of Atlantic salmon (Salmo salar) fingerlings. Canadian Journal of Fisheries and Aquatic Sciences 50:316-322. https://doi.org/10.1139/f93-037
https://doi.org/10.1139/f93-037...
; Baeverfjord and Krogdahl, 1996Baeverfjord, G. and Krogdahl, Å. 1996. Development and regression of soybean meal induced enteritis in Atlantic salmon, Salmo salar L., distal intestine: a comparison with the intestines of fasted fish. Journal of Fish Diseases 19:375-387. https://doi.org/10.1046/j.1365-2761.1996.d01-92.x
https://doi.org/10.1046/j.1365-2761.1996...
; Degani, 1987Degani, G. 1987. Effect of replacement of fish and chicken meals by soybean meal in a purified diet on growth and body composition of juvenile European eel Anguilla anguilla. Indian Journal of Fisheries 34:213-217.; García-Gallego et al., 1998García-Gallego, M.; Akharbach, H. and De La Higuera, M. 1998. Use of protein sources alternatives to fish meal in diets with amino acids supplementation for the European ell (Anguilla anguilla). Animal Science 66:285-292. https://doi.org/10.1017/S1357729800009073
https://doi.org/10.1017/S135772980000907...
). Nevertheless, soybean meal is a potential substitute for protein sources such as fish meal and poultry byproduct meal in tambaqui diets.

Mean ADC values of poultry byproduct meal were significantly higher than those of fish meal. Conversely, Abimorad and Carneiro (2004)Abimorad, E. G. and Carneiro, D. J. 2004. Métodos de coleta de fezes e determinação dos coeficientes de digestibilidade da fração protéica e da energia de alimentos para o pacu, Piaractus mesopotamicus (Holmberg, 1887). Revista Brasileira de Zootecnia 33:1101-1109. https://doi.org/10.1590/S1516-35982004000500001
https://doi.org/10.1590/S1516-3598200400...
found no significant difference in ADC between the two ingredients for pacu. Chemical scores of EAA of poultry byproduct meal were high and showed little variation (0.75-1.58), except for tryptophan (0.31), which was limiting for tambaqui. Moreover, poultry byproduct meal had the third highest EAAI (0.93) of all ingredients tested. However, ADC of byproduct meals such as poultry byproduct meal may vary according to the composition and percentage of ingredients used in their production (Thompson et al., 2008Thompson, K. R.; Rawles, S. D.; Metts, L. S.; Smith, R. G.; Wimsatt, A.; Gannam A. L.; Twibell, R. G.; Johnson, R. B.; Brady, Y. J. and Webster, C. D. 2008. Digestibility of dry matter, protein, lipid, and organic matter of two fish meals, two poultry by-product meals, soybean meal, and distiller's dried grains with solubles in practical diets for sunshine bass, Morone chrysops × M. saxatilis. Journal of the World Aquaculture Society 39:352-363. https://doi.org/10.1111/j.1749-7345.2008.00174.x
https://doi.org/10.1111/j.1749-7345.2008...
).

In this study, the two fish meal sources tested, one made from tilapia filleting byproducts and produced in Brazil and one of Chilean origin made from salmon byproducts, had high ADCAA for all amino acids. However, tilapia processing residue and salmon meal had only satisfactory amino acid profiles, with EAAI values of 0.96 and 0.80, respectively. In addition, the mean ADC for total amino acids was 5.0% higher in the poultry byproduct meal than in the processed tilapia residue. Crude protein and ash content indicate that poultry byproduct meal was a superior protein source for tambaqui over the processed tilapia residue: even though crude protein content was similar (poultry byproduct meal: 65.8%, processed tilapia residue: 60.2%), mineral matter content was higher in the processed tilapia residue (25.2%) than in the poultry byproduct meal (16.3%), indicating that a larger amount of bone was used in the processed tilapia residue production, resulting in an inferior ingredient.

Wheat gluten meal is an excellent protein source, but despite its high ADC values (mean: 84.5%), it had the lowest EAAI (0.48) as a result of the large variation in CSI and the low CSI of lysine (0.12) and tryptophan (0.06). Few studies have evaluated the digestibility of wheat gluten meal in fish (Buzollo et al., 2018Buzollo, H.; Nascimento, T. M. T.; Sandre, L. C. G.; Neira, L. M.; Jomori, R. K. and Carneiro, D. J. 2018. Apparent digestibility coefficients of feedstuff used in tambaqui diets. Boletim do Instituto de Pesca 44:e316.; Allan et al., 2000Allan, G. L.; Parkinson, S.; Booth, M. A.; Stone, D. A. J.; Rowland, S. J.; Frances, J. and Warner-Smith, R. 2000. Replacement of fish meal in diets for Australian silver perch, Bidyanus bidyanus: I. Digestibility of alternative ingredients. Aquaculture 186:293-310. https://doi.org/10.1016/S0044-8486(99)00380-4
https://doi.org/10.1016/S0044-8486(99)00...
; Robaina et al., 1999Robaina, L.; Corraze, G.; Aguirre, P.; Blanc, D.; Melcion, J. P. and Kaushik, S. 1999. Digestibility, postprandial ammonia excretion and selected plasma metabolites in European sea bass (Dicentrarchus labrax) fed pelleted or extruded diets with or without wheat gluten. Aquaculture 179:45-56. https://doi.org/10.1016/S0044-8486(99)00151-9
https://doi.org/10.1016/S0044-8486(99)00...
; Storebakken et al., 2000Storebakken, T.; Shearer, K. D.; Baeverfjord, G.; Nielsen, B. G.; Åsgård, T.; Scott, T. and De Laporte, A. 2000. Digestibility of macronutrients, energy and amino acids, absorption of elements and absence of intestinal enteritis in Atlantic salmon, Salmo salar, fed diets with wheat gluten. Aquaculture 184:115-132. https://doi.org/10.1016/S0044-8486(99)00316-6
https://doi.org/10.1016/S0044-8486(99)00...
; Sugiura et al., 1998Sugiura, S. H.; Dong, F. M.; Rathbone, C. K. and Hardy, R. W. 1998. Apparent protein digestibility and mineral availabilities in various feed ingredients for salmonid feeds. Aquaculture 159:177-202. https://doi.org/10.1016/S0044-8486(97)00177-4
https://doi.org/10.1016/S0044-8486(97)00...
). Allan et al. (2000)Allan, G. L.; Parkinson, S.; Booth, M. A.; Stone, D. A. J.; Rowland, S. J.; Frances, J. and Warner-Smith, R. 2000. Replacement of fish meal in diets for Australian silver perch, Bidyanus bidyanus: I. Digestibility of alternative ingredients. Aquaculture 186:293-310. https://doi.org/10.1016/S0044-8486(99)00380-4
https://doi.org/10.1016/S0044-8486(99)00...
also reported high ADCAA of wheat gluten meal (100%) for Australian silver perch (Bydianus bydianus). However, none of the studies evaluated the CSI and EAAI of wheat gluten meal, and thus failed to determine the actual protein quality of wheat gluten meal for the species evaluated.

Similar to wheat gluten meal, feather meal and cottonseed meal also had high ADC, but an unbalanced amino acid profile, resulting in low chemical scores for tryptophan (feather meal: 0.06, cottonseed meal: 0.18) and low EAAI values (feather meal: 0.66, cottonseed meal: 0.61). Pezzato et al. (2002)Pezzato, L. E.; Miranda, E. C.; Barros, M. M.; Pinto, L. G. Q.; Furuya, W. M. and Pezzato, A. C. 2002. Digestibilidade aparente de ingredientes para a tilápia do Nilo (Oreochromis niloticus). Revista Brasileira de Zootecnia 31:1595-1604. https://doi.org/10.1590/S1516-35982002000700001
https://doi.org/10.1590/S1516-3598200200...
compared the mean ADCprotein of proteic ingredients for Nile tilapia and reported that feather meal had the lowest ADC (29.1%), which was lower than the value observed for tambaqui. Feather meal hydrolysis was not as efficient at the time of that study, which may explain the low ADC found by Pezzato et al. (2002)Pezzato, L. E.; Miranda, E. C.; Barros, M. M.; Pinto, L. G. Q.; Furuya, W. M. and Pezzato, A. C. 2002. Digestibilidade aparente de ingredientes para a tilápia do Nilo (Oreochromis niloticus). Revista Brasileira de Zootecnia 31:1595-1604. https://doi.org/10.1590/S1516-35982002000700001
https://doi.org/10.1590/S1516-3598200200...
. Cottonseed meal had no harmful effects on tambaqui juveniles, despite the presence of gossypol, an antinutritional factor in cottonseed meal that can reduce its digestibility and affect biochemical processes by inhibiting enzyme activity (Beaudoin, 1985Beaudoin, A. R. 1985. The embriotoxicity of gossypol. Teratology 32:251-257. https://doi.org/10.1002/tera.1420320213
https://doi.org/10.1002/tera.1420320213...
).

Mean ADCAA values of alcohol yeast for tambaqui were low in this study. In our previous study (Buzollo et al., 2018Buzollo, H.; Nascimento, T. M. T.; Sandre, L. C. G.; Neira, L. M.; Jomori, R. K. and Carneiro, D. J. 2018. Apparent digestibility coefficients of feedstuff used in tambaqui diets. Boletim do Instituto de Pesca 44:e316.), we also observed that alcohol yeast was not classified as a good source of protein and energy for juvenile tambaqui. Similar results were reported by Storebakken et al. (1998)Storebakken, T.; Kvien, I. S.; Shearer, K. D.; Grisdale-Helland, B.; Helland, S. J. and Berge, G. M. 1998. The apparent digestibility of diets containing fish meal, soybean meal or bacterial meal fed to Atlantic salmon (Salmo solar): evaluation of different faecal collection methods. Aquaculture 169:195-210. https://doi.org/10.1016/S0044-8486(98)00379-2
https://doi.org/10.1016/S0044-8486(98)00...
for Atlantic salmon (Salmo solar), and the authors attributed the low digestibility of the alcohol yeast to the low digestibility of certain amino acids in its composition. In fact, essential amino acids of alcohol yeast such as arginine, threonine, and valine had low digestibility (<54%) by tambaqui juveniles. This low digestibility may be explained by the high inclusion level of alcohol yeast in test diets (300 g/kg), which has been generally lower in fish diets (Koch et al., 2015Koch, J. F. A.; Pezzato, L. E.; Barros, M. M.; Koberstain, T. C. D. R.; Teixeira, C. P.; Fernandes Junior, A. C. and Nakagome, F. K. 2015. Levedura íntegra e autolisada como pronutriente em dietas de tilápia do nilo durante a fase de masculinização. Veterinária e Zootecnia 22:254-267.; Meurer et al., 2000Meurer, F.; Hayashi, C.; Soares, C. M. and Boscolo, W. R. 2000. Utilização de levedura spray dried na alimentação de alevinos de tilápia do Nilo (Oreochromis niloticus L.). Acta Scientiarum 22:479-484.; Sheikhzadeh et al., 2012Sheikhzadeh, N.; Heidarieh, M.; Pashaki, A. K.; Nofouzi, K.; Farshbafi, M. A. and Akbari, M. 2012. Hilyses®, fermented Saccharomyces cerevisiae, enhances the growth performance and skin non-specific immune parameters in rainbow trout (Oncorhynchus mykiss). Fish & Shellfish Immunology 32:1083-1087. https://doi.org/10.1016/j.fsi.2012.03.003
https://doi.org/10.1016/j.fsi.2012.03.00...
). Moreover, the amino acid balance of alcohol yeast was suitable for the species, with little variation in chemical score and EAAI values (0.70).

This is the first study to combine apparent digestibility coefficients and chemical scores to evaluate a large number of ingredients used in fish diets for tambaqui. Our findings may improve least-cost diet formulations and enable effective substitution of ingredients that meet the limiting amino acid requirements of the species. Moreover, our findings may provide the basis for future studies on the digestible amino acid requirements for tambaqui.

Conclusions

Amino acids of proteic and energetic ingredients are well utilized by juvenile tambaqui. Corn and wheat bran have the highest mean ADC for total amino acids among energetic ingredients (95 and 92%, respectively), whereas corn gluten meal and soybean meal have the highest ADC for total amino acids among proteic ingredients (97.6 and 96.6, respectively).

Acknowledgments

We thank the Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP) for financial support (process 2012/09126-4) and for the scholarship granted (2011/12964-9).

References

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Publication Dates

  • Publication in this collection
    01 June 2020
  • Date of issue
    2020

History

  • Received
    24 Feb 2019
  • Accepted
    11 Feb 2020
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