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Ciencias marinas

versión impresa ISSN 0185-3880

Cienc. mar vol.45 no.3 Ensenada sep. 2019  Epub 30-Jul-2021

https://doi.org/10.7773/cm.v45i3.3007 

Articles

Apparent digestibility of amino acids in feedstuffs used in diets for the Pacific white shrimp, Penaeus vannamei

Eficiencia digestiva aparente de aminoácidos en ingredientes utilizados en dietas para camarón blanco del pacífico, Penaeus vannamei

David Alonso Villarreal-Cavazos1  * 
http://orcid.org/0000-0001-5572-9710

Denis Ricque-Marie1 
http://orcid.org/0000-0003-1029-1561

Martha Nieto-López1 
http://orcid.org/0000-0002-1000-4406

Mireya Tapia-Salazar1 
http://orcid.org/0000-0002-1048-9781

Andreas Lemme2 

Julián Gamboa-Delgado1 
http://orcid.org/0000-0001-9041-1388

Lucia Elizabeth Cruz-Suárez1 
http://orcid.org/0000-0003-3808-2972

1Departamento de Ecología, Facultad de Ciencias Biológicas, Universidad Autónoma de Nuevo León, Cd. Universitaria, CP 66450, Monterrey (San Nicolás de los Garza), Nuevo León, Mexico.

2Evonik Degussa GmbH, Rodenbacher Chaussee 4, D-63457 Hanau (Wolfgang), Germany.


Abstract

Apparent digestibility coefficients (ADC) for dry matter, energy, crude protein (CP), and amino acids (AA) were evaluated for 4 feedstuffs used to feed juvenile white shrimp (Penaeus vannamei): fish meal (73.5% CP), potato protein concentrate (89.3% CP), brewer’s yeast (42.5% CP), and crustacean meal (47.2% CP). Experimental diets included 30% of the test ingredient and 69% of a commercial diet supplemented with 1% chromium oxide as inert marker. Amino acid contents in the ingredients, experimental diets, leached diets, and feces were analyzed by high-performance liquid chromatography. Nutrient loss in water was highest in the fishmeal diet (25%). The AA with the highest losses in water were lysine, methionine, and arginine (25%, 23%, and 21%, respectively). The ADC for dry matter oscillated between 79.2% and 90.6%, for CP between 78.1% and 91.8%, and for AA between 75.4% and 96.6%. In all cases the lower limit corresponded to the meal with potato protein concentrate and the upper limit to the crustacean meal. The ADC for energy fluctuated between 89.1% and 95.2%, with the lower limit for the crustacean meal and the upper limit for the meal with potato protein concentrate.

Key words:  digestibility; shrimp; Penaeus vannamei; amino acids

Resumen

Los coeficientes de digestibilidad aparente (CDA) de materia seca, energía, proteína cruda (PC) y aminoácidos (AA) fueron evaluados en 4 ingredientes utilizados para alimentar juveniles de camarón blanco (Penaeus vannamei): harina de pescado (73.5% PC), concentrado proteico de papa (89.3% PC), levadura de cerveza (42.5% PC) y harina de crustáceo (47.2% PC). Las dietas experimentales incluyeron 30% del ingrediente prueba y 69% de una dieta comercial suplementada con 1% de óxido de cromo como marcador inerte. El contenido de aminoácidos en los ingredientes, las dietas formuladas, las dietas lixiviadas y las heces fue analizado por cromatografía líquida de alta resolución. La mayor pérdida de nutrientes en el agua se presentó con la dieta de harina de pescado (25%). Los AA con mayor pérdida en el agua fueron la lisina, la metionina y la arginina (25%, 23% y 21%, respectivamente). Los CDA para la materia seca oscilaron entre el 79.2% y el 90.6%, para la PC entre el 78.1% y el 91.8%, y para los AA entre el 75.4% y el 96.6%. En todos los casos el límite inferior correspondió al concentrado proteico de papa y el superior a la harina de crustáceo. El CDA para la energía fluctuó entre el 89.1% y el 95.2%, con el límite inferior para la harina de crustáceo y el superior para el concentrado proteico de papa.

Palabras clave: eficiencia digestiva; camarón; Penaeus vannamei; aminoácidos

Introduction

Aquaculture feed production is increasingly challenged by the rising cost and limited production of fish meal, the main ingredient in feeds. In the shrimp farming industry, feed is the most expensive input in the variable costs of production when operating grow-out farms. Today a wide range of alternative feedstuffs have to be considered to reduce the amount of fish meal used in penaeid shrimp feed. These feedstuffs must be well characterized to understand their nutritional quality, which is particularly important in the formulation of efficient (highly digestible), ecologically sustainable (low-polluting), and economically competitive feeds. In particular, the apparent digestibility of nutrients in feedstuffs, namely amino acids, plays a very important role in the nutritional quality of feeds. The aim of the present study is to evaluate the apparent digestibility efficiency of dry matter, energy, proteins, and amino acids in a reference diet (commercial diet) and in 4 feedstuffs used in shrimp feed: Pilchard meal (Sardinops sagax), potato protein concentrate (Solanum tuberosum), brewer’s yeast (Saccharomyces cerevisiae), and crustacean meal (Heterocarpus reedi). Apparent digestibility coefficients were adjusted to account for nutrient losses (nutrient leaching) in seawater.

Materials and Methods

Feedstuffs were obtained from feed mills and/or their distributors. We obtained the fish meal (S. sagax) and potato protein concentrate (S. tuberosum) from Sonora (Mexico), the brewer’s yeast (S. cerevisiae) from Baja California (Mexico), and the crustacean meal (H. reedi) from Santiago (Chile). Feeds were prepared following the method described by Villarreal-Cavazos et al. (2017); test ingredients were mixed in a KitchenAid mixer (Benton Harbor, Michigan) for 10 min while adding warm water (30%), and then for 15 min after water was incorporated. A Torrey meat grinder (Monterrey, Mexico) with 1.6-mm holes was used. Manufacturing time was 40 min per kilogram of feed, and manufacturing temperatures reached 75-80 ºC. The extruded feed was dried in a ventilated oven at 100 ºC for 8 min and kept at room temperature for one night before packing. Digestibility of feedstuffs was determined following the method described by Cho and Slinger (1979). Experimental diets contained 30% of the test ingredient and 70% of the reference diet (Cruz-Suárez et al. 2009).

The digestibility trial was carried out in a closed recirculating artificial seawater system at the Mariculture Program facilities (Faculty of Biological Sciences, Autonomous University of Nuevo León). Twenty-eight identical, fiberglass aquariums with 120-L capacity and regulated flow rate of 710 mL·min-1 were used. Tanks were randomly distributed. Each diet was tested in 4 replicate tanks with 24 Peaneus vannamei juveniles (5.4 ± 0.1 g) each. Shrimp were fed ad libitum starting with 10% of total biomass in the tank. Fresh feces were collected (12 g) from each tank with a siphon, immediately after excretion, over a period of 7 d.

The bromatological composition of feedstuffs, diets, and feces was determined with the following methods: 930.15, 990.03, 942.05, and 962.09B for moisture, crude protein, ash, and fiber, respectively (AOAC International 1997). Lipids were extracted using the Soxhlet method (Tecator 1983), and the nitrogen free extract was calculated as the difference. Nutrient loss in seawater was determined according to the method reported by Tapia-Salazar et al. (2012). Chrome content was determined according to the method described by Bolin et al. (1952) and modified by Cruz-Suárez et al. (2009). Amino acid composition was determined according to Llames and Fontaine (1994) and Fontaine (2003). The apparent digestibility coefficients (ADCs) for dry matter, protein, and amino acids in the diets were calculated using the following equation: %ADCdiet = 100 - [100(Cdiet/Ndiet) × (Nfeces/ Cfeces)], where C and N are, respectively, the chromium oxide and nutrient concentrations in the diets or feces (dry weight basis). The ADCs for feedstuffs were calculated according to Bureau and Hua (2006). The ADCs for diets and feedstuffs were adjusted considering the percentage of nutrient loss in water due to leaching (Villarreal-Cavazos et al. 2014). We used the leaching values that were obtained after 1-h immersions of feeds in seawater. To account for losses in dietary dry matter, protein, and amino acids before ingestion by the animal, the ADC for each nutrient was corrected for using the equations reported by Nieto-López et al. (2011). Nutrient concentration values (feedstuffs, diets, leached diets, feces) and ADCs were subjected to a one-way analysis of variance and Duncan’s multiple range test to separate the treatment averages into normal and homogenous groups. The software used was SPSS v.22 for Windows.

Results

Crude protein content ranged from 42.5% to 89.3%. Lipids oscillated between 1.4% and 10.8% and crude fiber between 0.1% and 3.4%. The range for ash content was 5.3-18.1%. Amino acid (AA) proximate composition and AA contents varied greatly between feedstuffs (Table 1). The composition of experimental feeds showed values that were very close to the expected values, according to calculations based on the nutrient concentrations of feedstuffs in the formulated feeds (Table 2). Feeds containing crustacean meal and the fish meal showed the highest nutrient losses (20% and 24%, respectively) in seawater (Table 3). The AAs with the highest losses in seawater were lysine, methionine, and arginine (27%, 24%, and 20%, respectively) (Table 3).

Table 1 Proximate composition and amino acid contents for the different experimental feedstuffs. 

FM PPC BY CM
Proximal composition (% DM)
Crude protein 69.7 89.3 42.5 47.2
Crude fat 10.8 1.4 3.2 3.4
Crude fiber 0.0 0.2 2.2 3.4
Ash 18.1 5.3 6.3 13.3
Nitrogen-free extract 0.0 3.2 45.0 31.3
Gross energy (cal·g-1) 4,605 5,510 5,052 4,773
Amino acid profile (%)
Arginine 4.03 4.4 2.5 2.2
Histidine 1.87 2.0 1.0 0.9
Isoleucine 2.62 5.0 1.7 1.7
Leucine 4.86 9.2 2.5 2.7
Lysine 5.22 7.2 2.6 2.2
Methionine 1.80 1.9 0.6 0.8
Phenylalanine 2.63 5.7 1.6 2.1
Threonine 2.81 5.2 1.8 1.6
Valine 3.19 6.0 2.1 2.1
Sum of EAA 29.0 46.7 16.3 16.3
Alanine 4.31 4.4 2.3 2.4
Aspartic acid 6.20 10.9 3.5 3.8
Cystine 0.58 1.2 0.5 0.4
Glutamic acid 8.51 9.5 5.7 5.1
Glycine 4.67 4.5 1.9 2.5
Proline 3.07 4.6 2.0 1.9
Serine 2.67 4.8 1.8 1.6
Sum of analyzed AA 59.10 86.4 34.2 34.0

DM: dry matter; cal: calories; EAA: essential amino acids; AA: amino acids; FM: fish meal; PCC: potato protein concentrate; BY: beer yeast; CM: crustacean meal.

Table 2 Formula (g·kg-1; dry matter, DM) for experimental diet composition.  

RD FMD PPCD BYD CMD
Reference ingredient+ 1,000 700 700 700 700
Fish meal - 300 - - -
Potato protein concéntrate - 300 - -
Beer yeast - - 300 -
Crustacean meal - - - 300
Proximal composition (% DM)
Crude protein 34.6 46.5 50.3 36.2 37.7
Crude fat 10.6 10.5 7.8 8.3 8.4
Crude fiber 3.7 2.1 2.6 3.3 3.7
Ash 11.0 14.5 9.4 9.7 12.0
Nitrogen-free extract 39.9 26.9 --- 42.2 ---
Gross energy (cal·g-1) 4,750 4,162 4,949 4,811 4,728
Arginine 2.0 2.8 2.7 2.1 2.0
Histidine 0.7 1.1 1.1 0.8 0.8
Isoleucine 1.3 1.8 2.4 1.5 1.4
Leucine 2.3 3.2 4.3 2.5 2.4
Lysine 1.8 3.1 3.4 2.2 1.8
Methionine 0.7 1.1 1.0 0.7 0.7
Phenylalanine 1.6 2.0 2.7 1.6 1.7
Threonine 1.2 1.8 2.3 1.5 1.3
Valine 1.5 2.2 2.9 1.8 1.7
Sum of EAA 13.1 19.0 22.8 14.7 13.8
Alanine 1.8 2.7 2.5 2.1 1.9
Aspartic acid 2.9 4.1 5.2 3.3 3.1
Cystine 0.4 0.4 0.6 0.4 0.4
Glutamic acid 6.0 7.1 7.0 5.7 5.7
Glycine 2.0 3.0 2.7 2.0 2.1
Proline 2.2 2.6 2.8 2.1 2.1
Serine 1.4 1.8 2.3 1.7 1.4
Sum of analyzed AA 29.8 40.8 45.9 32.0 30.5

+Shrimp commercial feed.

RD: reference diet; FMD: fish meal diet; PPCD: potato protein concentrate diet; BYD: beer yeast diet; CMD: crustacean meal diet; cal: calories; EAA: essential amino acids; AA: amino acids.

Table 3 Dietary nutrient losses (percentage of initial content) in seawater. 

RD FMD PPCD BYD CMD Mean+
Dry matter 14 5 13 11 7 10
Crude protein 25 25 13 2 20 17b
Arginine 23 19 19 14 24 20c
Histidine 11 20 16 6 18 14ab
Isoleucine 13 34 16 3 20 17b
Leucine 9 20 13 4 16 12a
Lysine 25 42 23 16 29 27e
Methionine 31 22 25 17 26 24e
Phenylalanine 12 26 13 4 16 14ab
Threonine 11 38 12 4 15 16ab
Valine 9 21 16 5 20 14ab
Sum of EAA 15 10 17 8 20 14ab
Alanine 15 19 16 11 22 17b
Aspartic acid 13 25 13 5 15 14ab
Cystine 18 22 12 5 11 14ab
Glutamic acid 16 20 16 6 16 15ab
Glycine 26 32 19 11 25 23c
Proline 23 32 18 10 19 20c
Serine 14 30 12 9 18 17b
Sum of analyzed AA 17 22 16 8 19 16ab
Mean (all AA) 17 24 17 8 20 17b

+Analysis of variance for AA (P < 0.001); different letters indicate significant differences according to Duncan’s multiple range test (α = 0.05).

RD: reference diet; FMD: fish meal diet; PPCD: potato protein concentrate diet; BYD: beer yeast diet; CMD: crustacean meal diet; EAA: essential amino acids; AA: amino acids.

The ADC varied between 79% and 91% for dry matter, between 89% and 95% for energy, and between 78% and 93% for crude protein. The ADC for total AAs varied between 75% and 97% (Table 4). AAs in the crustacean meal feed proved to be highly digestible (94.6% mean digestibility). Digestibility of AAs in the brewer’s yeast meal was good (87.1%). Mean AA digestibility was lowest in the potato protein concentrate (75.2%). In general, mean digestibility of AAs in the experimental feedstuffs was more than 90%, except in the case of cystine (80.6%). The AAs with digestibility values greater than 95% were methionine, isoleucine, lysine, glycine, and proline. Cystine was the least digestible AA. Corrections for nutrient leaching tended to reduce standard ADC values for most of the experimental feedstuffs (Table 5).

Table 4 Apparent digestibility coefficients for dry matter, energy, crude protein, and amino acids of ingredients used in Pacific white shrimp (Litopenaeus vannamei) diets. 

FM PPC BY CM+
Dry matter 90 ± 3a 79 ± 1c 82 ± 2b 91 ± 2a
Energy 93 ± 1b 95 ± 1a 90 ± 4c 89 ± 1c
Crude protein 93 ± 2a 78 ± 2d 87 ± 4b 92 ± 2a
Arginine 98 ± 1a 79 ± 1d 92 ± 4c 96 ± 4b
Histidine 97 ± 1a 77 ± 1d 88 ± 5c 92 ± 4b
Isoleucine 93 ± 1a 75 ± 1d 88 ± 6c 96 ± 4b
Leucine 94 ± 1a 75 ± 1c 88 ± 6b 96 ± 5a
Lysine 96 ± 1a 80 ± 2c 92 ± 8b 96 ± 6a
Methionine 99 ± 1a 80 ± 2d 90 ± 6c 97 ± 4b
Phenylalanine 93 ± 1a 74 ± 1d 87 ± 5c 93 ± 4b
Threonine 99 ± 1a 72 ± 1d 84 ± 6c 93 ± 4.b
Valine 97 ± 1a 76 ± 1c 90 ± 6b 96 ± 3a
Sum of EAA 98 ± 1a 76 ± 1d 88 ± 6c 95 ± 4b
Alanine 97 ± 1a 76 ± 1c 89 ± 4b 97 ± 4a
Aspartic acid 97 ± 1a 73 ± 1d 87 ± 5c 94 ± 4b
Cystine 90 ± 3a 66 ± 1d 73 ± 6c 87 ± 5b
Glutamic acid 97 ± 1a 76 ± 1d 88 ± 4c 95 ± 4b
Glycine 89 ± 2b 77 ± 1c 89 ± 3c 100 ± 1a
Proline 97 ± 1a 72 ± 1d 85 ± 5c 92 ± 4b
Serine 98 ± 1a 76 ± 1c 87 ± 4b 97 ± 3a
Sum of analyzed AA 97 ± 1a 75 ± 1c 88 ± 5b 95 ± 4a

+Analysis of variance for AA (P < 0.001); different letters indicate significant differences according to Duncan’s multiple range test (a = 0.05).

FM: fish meal; PPC: potato protein concentrate; BY: beer yeast; CM: crustacean meal; EAA: essential amino acids; AA: amino acids.

Table 5 Apparent digestibility coefficients (%) adjusted for nutrient losses in seawater prior to ingestion. 

FM PPC BY CM+
Dry matter 85 ± 5b 78 ± 1d 82 ± 3c 94 ± 2a
Crude protein 86 ± 3c 77 ± 2d 91 ± 5b 97 ± 2a
Arginine 98 ± 2a 75 ± 2c 92 ± 4b 94 ± 5b
Histidine 97 ± 2a 71 ± 1c 88 ± 5b 87 ± 5b
Isoleucine 96 ± 2a 69 ± 1c 90 ± 5b 92 ± 5b
Leucine 96 ± 1a 70 ± 1d 89 ± 6c 92 ± 5b
Lysine 99 ± 1a 74 ± 3c 93 ± 1b 93 ± 1b
Methionine 97 ± 2a 75 ± 2c 96 ± 5ab 98 ± 2a
Phenylalanine 94 ± 2a 69 ± 1c 89 ± 5b 91 ± 5b
Threonine 96 ± 2a 68 ± 1d 85 ± 1c 91 ± 2b
Valine 95 ± 1a 71 ± 1d 88 ± 2c 90 ± 1b
Sum of EAA 97 ± 2a 71 ± 2c 90 ± 1b 92 ± 1b
Alanine 96 ± 2a 71 ± 2d 90 ± 2c 93 ± 1b
Aspartic acid 96 ± 2a 69 ± 1c 89 ± 2b 92 ± 2b
Cystine 87 ± 1b 64 ± 1d 81 ± 2c 95 ± 1a
Glutamic acid 96 ± 2a 72 ± 2d 90 ± 2c 94 ± 1b
Glycine 85 ± 2b 74 ± 1c 99 ± 1a 99 ± 1a
Proline 96 ± 2a 69 ± 1c 85 ± 1b 88 ± 1b
Serine 96 ± 1a 71 ± 1c 92 ± 1b 98 ± 1a
Sum of analyzed AA 96 ± 2a 71 ± 1d 90 ± 2c 93 ± 2b

+Analysis of variance for AA (P < 0.001); different letters indicate significant differences according to Duncan’s multiple range test (a = 0.05).

FM: fish meal; PPC: potato protein concentrate; BY: beer yeast; CM: crustacean meal; EAA: essential amino acids; AA: amino acids.

Discussion

The AA proximate composition and AA contents found for the different feedstuffs were similar to what has been previously reported (NRC 1983, Novus 1996, Hess et al. 2006). In addition, in terms of dry matter, energy, crude protein, and total AAs, all feedstuffs (fish meal, crustacean meal, brewer’s yeast, and potato protein concentrate) were more digestible than the reference diet. Goytortúa-Bores et al. (2006) analyzed the crustacean meal (red crab, Pleuroncodes planipes) used to feed Pacific white shrimp and found that ADC values for crude protein were lower than the value observed in the present study (82-84% vs 92.8%). This value coincides with that reported by Tibbets et al. (2006) for whole krill fed to cod (96%). Ozório et al. (2012) evaluated the increasing levels of brewer’s yeast in tilapia feed and found that apparent digestibility of crude protein decreased (82.3%, 81.3%, 78.6%, 78.1%, and 79.4%) as inclusion levels of brewer’s yeast in the diet increased (0%, 10%, 15%, 20%, and 30%, respectively). In the present study, for Pacific white shrimp, brewer’s yeast was a highly digestible feedstuff (91.8%) in terms of crude protein at an inclusion level of 30%. Terrazas-Fierro et al. (2010) reported ADC values for essential AAs in a red crab (P. planipes) meal that were much lower (82.1%) than the values found for crustacean meal in the present study (95%). In the present study, experimental diets were formulated with 30% of the test ingredient. The Commonwealth Scientific and Industrial Research Organisation (Australia) work group indicates that the higher the inclusion level of the feedstuff in the experimental diet, the higher the precision in the determination of feedstuff digestibility because differences with the reference diet become clearer and more accurate (Cruz-Suárez et al. 2008). Correction for nutrient leaching tended to increase ADC values for brewer’s yeast, whereas the rest of the feedstuffs showed the opposite effect. Tusche et al. (2011) reported low growth rates for rainbow trout when feed contained 50% of potato protein concentrate. Xie and Jokumsen (1997) reported that growth rates for rainbow trout decreased as inclusion levels of potato protein concentrate increased, which could be associated with low AA digestibility, as shown in the present study for shrimp. The present study showed that the digestive efficiency of essential AAs in the experimental fish meal was high (97%), much higher than the values reported by Yang et al. (2009) (87%), Terrazas-Fierro et al. (2010) (89%), and Carvalho et al. 2016 (84%). This differences could be associated with different factors, such as fish species, raw material (whole fish, by-products resulting from the filleting process, mixture of viscera from other species, etc.), or the elaboration process (drying by direct flame or by steam jacket). However, the previously mentioned studies do not specify on the raw material or elaboration process used.

English translation by Claudia Michel-Villalobos

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Received: May 01, 2019; Accepted: June 01, 2019

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