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Latin american journal of aquatic research

versión On-line ISSN 0718-560X

Lat. Am. J. Aquat. Res. vol.46 no.3 Valparaíso jul. 2018 

Research Article

In vitro protein digestibility of animal, vegetal and microbial feed ingredients for Macrobrachium tenellum

Cynthia Montoya-Martínez1 

Héctor Nolasco-Soria2 

Fernando Vega-Villasante1 

Olimpia Carrillo-Farnés3 

Alfonso Álvarez-González4 

Roberto Civera-Cerecedo2 

1Laboratorio de Calidad de Agua y Acuicultura Experimental, Centro de Investigaciones Costeras Universidad de Guadalajara, Jalisco, México

2Centro de Investigaciones Biológicas del Noroeste S.C., La Paz, B.C.S., México

3Facultad de Biología, Universidad de La Habana, Cuba

4Laboratorio de Acuicultura Tropical, División Académica de Ciencias Biológicas Universidad Juárez Autónoma de Tabasco, México


Due to the cost of raw materials, the need to formulate balanced feeds with highly digestible ingredients is indispensable for the aquaculture feed industry. For this reason, the protein in vitro digestibility, assessed by the pH-stat method, of ingredients with potential of using them on the balanced feed for Macrobrachium tenellum, were evaluated. The relative protein digestibility was assessed in twelve feed ingredients, including animal (pork meal, feather poultry meal, prime poultry meal, turkey meal, fish meal, shrimp meal), vegetal (coconut paste, chickpea meal, soybean meal, wheat gluten) and microbial (yeast and Spirulina meal); casein (Hammerstein grade) was used as the reference protein. The highest relative protein digestibility was found in: Spirulina meal (52.6%); following by pork meal (45.6%), and feather poultry meal (39.6%). The lowest digestibilities were found in soybean meal (15.9%), chickpea meal (12.1%), and fish meal (11.6%). The protein digestibility value should be considered for selecting potential ingredients for the formulation of balanced feeds for M. tenellum.

Keywords: Macrobrachium tenellum; prawns; nutrition; protein; enzyme activity; digestibility; aquaculture


The production of the aquaculture feed is one of the fastest growing sectors of animal feed worldwide (Rust et al., 2012). In aquaculture, feeding represents one of the highest production costs, according protein content and source, therefore the protein quality on the commercial feeds, is one of the most important nutritional parameters, as influence the prawns growth and the body composition (Chisty et al., 2009). The feed digestibility and assimilation are also very important to reduce its conversion into a source of water pollutants, with negative effects on the ecosystem (Terrazas et al., 2010a). An efficient feeding depends on the nutritional characteristics of the feed, its digestibility, and feeding strategy since they are essential elements in providing nutrients and energy needed for efficient growth of cultivated species (Carrillo-Farnés et al., 2007; Chisty et al., 2009).

The digestive capacity of the aquaculture species is sustained by the activity of digestive enzymes present in their digestive tract (Ali et al., 2009). The study of the digestive enzymes and nutrient digestibility is essential for understanding the mechanisms of digestion, and for being useful for selection of ingredients and feeds with higher nutritional value, for each species (Cruz-Suárez et al., 2002).

Since the in vivo digestibility methods are lengthy and expensive, it has been necessary to apply in vitro methods, that are fast and reliable, for assessing protein digestibility, using the digestive enzymes of the species of interest (Nolasco et al., 2006). The pH-stat in vitro method has been widely used in the evaluation of the nutritional quality of raw materials and processed feeds, because it is simple, fast, and with high reproducibility (Moyano et al., 2014). The use of pH-stat system has proved to be suitable for checking the quality of the protein sources, for marine shrimp feed formulation (Ezquerra et al., 1998; Lemos et al., 2004, 2009).

Although M. rosenbergii production has been profitable in some countries, just few studies have been performed on ingredient and feed digestibility (in vivo methods: Taechanuruk & Stickney, 1982; Ashmore et al., 1985; Ellis et al., 1987; Chin, 1988; Gomes & Peña, 1997). In general, information about native American species is limited (in vitro method: Manríquez-Santos et al., 2011).

This research contributes to the knowledge of the protein in vitro digestibility, by using the pH-stat method, of protein from animal, vegetal and microbial origin, with actual or potential for inclusion in feeds for M. tenellum.


Preparation of enzyme reagent

Twenty six pre-adults prawns (4-10 g) of M. tenellum, at intermolt stage, randomly collected from an artificial pond located at the Centro Universitario de la Costa (CUCOSTA), Universidad de Guadalajara, in Puerto Vallarta, Jalisco, Mexico, were used. The prawns were weighed (0.01 g precision, Ohaus, NJ, USA) and then were sacrificed by immersion in ice water, and subsequent freezing (-20°C).

Stomach and digestive gland of M. tenellum were dissected and weighed. One single pool of organs was homogenized, adding distilled water (1:4 w/v) in cold bath, with a homogenizer (Pro Scientific, Pro 200, Oxford CT, USA). The enzymatic extract (EE) was clarified by centrifugation (20,800 x g, 8 min, 10°C), the lipid fraction was removed and the supernatant was recovered. The EE was immediately stored at -20°C until use for protein content and enzymatic activity.

The enzymatic reactive (ER) for determining in vitro protein digestibility of feed ingredients, was prepared as follows: the enzymatic extract was homogenized (homogenizer Pro Scientific) pH was adjusted to pH 8.0, with sodium hydroxide (NaOH 1M). The ER was stored at -20°C until use. All assays were performed by triplicate.

Determination of protein and enzyme activity in enzymatic extract (EE)

The EE concentration for soluble protein was determined by the Bradford method (1976), by using bovine serum albumin (A4503, Sigma-Aldrich, St. Louis, MO, USA) as a standard.

The activity of total proteases was determined according Vega-Villasante et al. (1995) using azocasein (2% in Tris-HCl 50 mM, pH 7.5) as substrate. The specific activity of general protease was expressed in U protease/mg protein (a unit of protease is defined as the amount of the enzyme required to increase 0.01 U absorbance by min, at 440 nm).

The chymotrypsin activity was determined according Delmar et al. (1979), and trypsin activity by the modified micromethod based on Erlanger et al. (1961), using SAPNA (No. S7388, SIGMA, St. Louis, MO, USA), and BAPNA (No. B3133, SIGMA, St. Louis, MO, USA) (9.6 mM in dimethyl sulfoxide (DMSO)), as a substrate, respectively. The specific activity of trypsin and chymotrypsin was expressed as U/mg protein (a unit of trypsin and chymotripsin is defined as the amount of enzyme required to release 1 μMol of pnitroanilide/min).

The amylase activity was determined to Vega-Villasante et al. (1993), using a starch solution (1% in Tris-HCl, 50 mM pH 8.0) as substrate. The specific activity of amylase was expressed U amylase/mg protein (a unit of amylase is defined as the amount of enzyme required to release 1 μMol of maltose/min).

The lipase activity was determined according to Versaw et al. (1989), using β-naphthylcaprilate as substrate. The specific activity of lipase expressed in U lipase/mg protein (a unit of lipase is defined as the amount of the enzyme required to release 1 μMol of β-naphthol/min).

In vitro protein digestibility

The twelve ingredients used were: pork meal (meat and bones, USA); poultry meal (poultry products prime, USA); hydrolyzed feather meal (USA); turkey meal (60% turkey and 40% poultry products, USA); fish meal (sardine, Mexico); shrimp meal (Mexico), all animal meal were supplied by Proteínas Marinas y Agropecuarias, S.A. de C.V.; coconut paste hydrolyzate by Copreros Unidos por Tabasco S. de P.R. de R.L. (Mexico); chickpea meal elaborated in the Centro Interdisciplinario de Investigación para el Desarrollo Integral Regional (CIIDIR-IPN unidad Sinaloa, Mexico); soybean meal by Procesadora de Ingredientes, S.A. de C.V. (Mexico); wheat gluten by Arancia Ingredientes Especiales (Mexico); Spirulina meal by Producción y Comercialización de Microalgas y sus Derivados GENIX (Cuba); Bakers' yeast (Saccharomyces cerevisiae) by SAFMEX, S.A. de C.V./FERMEX, S.A. de C.V. (Mexico) and Hammerstein grade bovine casein (No. 101289, MP Biomedicals, Santa Ana, California, USA). The chemical composition is presented in Table 1. All the ingredients were ground, in a coffee grinder, and sieved to 250 μm.

Table 1 Proximal composition of ingredients. 

The in vitro protein digestibility was performed by the pH-stat method (Nolasco, 2008). Adding the corresponding amount of ingredient to have 6.25 mg of protein mL-1, the pH was adjusted 8.0, with sodium hydroxide (NaOH 1M). To start the digestion 10 U protease of the ER, of M. tenellum, were added, with an initial reaction volume of 5 mL, and incubated in the pH-stat (Metrohom 842 Titrando, Herisau, Switzerland) at pH 8, for 30 min at 25°C, under stirring (120 rpm). The consumption NaOH (0.02 M) required to maintain the pH at 8.0 was recorded, and the number of moles of NaOH /min was calculated, using casein as reference protein. All tests were performed in triplicate. For the controls, of each ingredient, the procedure was performed in the same way, but using denatured (heat treatment at boiling water bath, for 10 min) ER. The relative protein digestibility (RD) was expressed according to the following formula:

RD% =Consumption of NaOH/min by the hydrolysis of the problem sampleConsumption of NaOH/min by the hydrolysis of the reference protein×100

The correlation coefficient between the percentage of crude protein (CP) of the ingredients and RD was evaluated, with the purpose to determine if these data could be used to predict the digestibility of ingredients in prawn.

A test for normality Kolmogorov-Smirnov (α = 0.05) and homogeneity of variance Bartlett (α = 0.05) before the variance analysis (ANOVA) of a track, was applied. Statistically significant differences (P < 0.05) between treatment means were determined by the method of multiple comparisons of Tukey. All tests were performed using the statistical software version 11.0 SigmaPlot (Systat Software, Inc. Chicago, IL, USA).

The values of the concentration of CP ingredients were correlated with the results of RD and statistically analyzed to determine their correlation coefficient.


The enzyme activity in the enzymatic extract (EE) is shown in Table 2. The finding significant differences (P < 0.05) of RD, of ingredients used in this study is shown in Fig. 1. Spirulina meal showed the highest digestibility (52.6%), followed by the pork meal (45.6%); and the lowest digestibility was found in chickpea meal (12.1%), and fish meal (11.6%). The correlation between the CP concentration of the ingredients and the RD, was not significant, with a correlation coefficient of r2 = 0.25, with P > 0.05.

Table 2 Digestive enzyme activity (average ± SE) in M. tenellum

Enzyme U/mg protein
General proteases 1.254 ± 0.31
Trypsin 0.018 ± 0.01
Chymotrypsin 0.004 ± 0.0005
Amylases 0.634 ± 0.47
Lipases 0.746 ± 0.23

Figure 1 Relative protein digestibility (RD) of ingredients for M. tenellum. The digestibility of Casein Hammerstein type was considered as 100% (0.0068 μmol of peptide bonds hydrolyzed per min). Bars represent RD ± SE (standard error). Columns with differing letters are significantly different (P < 0.05). 


The search for new sources of available, nutritious and cheaper protein has been a constant need in the development of aquaculture feed (García-Galano et al., 2007). The digestibility of an ingredient depends not only on its protein content, as show the results of correlation between the CP concentration and RD, obtained in this study. This depends on many other factors such as the physical properties (i.e., particle size, solubility, etc.), and chemical properties (i.e., amino acid content); but also biological characteristics of the animal; the architecture of the digestive tract, and physiology will affect protein digestibility, and also environmental conditions are important (pH, temperature, salinity, ions); all these aspect should be considered for the determination of in vitro protein digestibility of ingredients or feed (Cruz-Suárez, 1996; Ezquerra et al., 1998; Carrillo-Farnés et al., 2007). However, most of the new protein ingredients have not been assessed from the digestibility point of view (Álvarez-González, 2003).

The digestibility results of the different protein sources, as potential ingredients for M. tenellum in this research, confirms that M. tenellum is omnivorous; and that the species is able to efficiently digest a variety of ingredients of microbial, animal and plant origin. Bhavan et al. (2010) in M. rosenbergii postlarvae fed enriched Artemia with Spirulina or yeast, found that both produced favorable growth, but Spirulina produced higher growing effect than yeast. This is probably due not only to the quality of its nutrients but also to its digestibility, the highest recorded in the present study.

In this context, Zhao et al. (2015) proved that shrimp feed in which fish meal was replaced by yeast extract, showed a higher apparent protein digestibility (APD) than control treatment in Penaeus vannamei, stating that approximately 45% of fish meal can be replaced by the yeast extract, in the presence of fish oil, phosphorus and calcium. For M. rosenbergii postlarvae, Prasad et al. (2013) suggest that feeds containing 0.5% S. cerevisiae yeast, are suitable to promote growth, although Seenivasan et al. (2014) reported that yeast inclusion levels at 4%, improved growth, enzyme activity, and amino acid production. Similarly, Parmar et al. (2012) demonstrated that 1% yeast inclusion in the diet improve the immune response, and control of white muscle disease. Therefore, Spirulina meal and yeast could be used as feed supplements for Macrobrachium species.

Related to the in vitro protein digestibility evaluations on different protein sources, Lemos et al. (2004) by pH-stat method and using digestive proteases of Farfantepenaeus paulensis juveniles, reported that Brazilian fish meal, meat meal and wheat meal presented the highest values of protein hydrolysis; in contrast the less digestible ingredients were soybean meal, Mexican fish meal, and blood meal; particularly, soybean meal showed high inhibitory effects (38%) on shrimp proteases. Manríquez-Santos et al. (2011) evaluated the protein in vitro digestibility of nine ingredients by the pH-stat method, using a multienzyme extract of M. carcinus, and using casein as reference protein. They found the highest values on yeast, beef blood meal, and pork meal; in contrast, the lowest digestibility values were found on soybean paste, fish meal, and fish hydrolyzate. In general, relative digestibility and protein hydrolysis values were higher (88.3-189.0% and 27.8-59.5%, respectively), than those reported in other studies (Ezquerra et al., 1998; Lemos et al., 2004; Nieto et al., 2005).

Our results are in agreement with Manríquez-Santos et al. (2011) with M. carcinus, and Lemos et al. (2004) with F. paulensis, suggesting that pork meal, and poultry meal are a good alternative to be used in the feed formulation for prawns. In this regard Cruz-Suárez et al. (2007), reported that poultry meals are a good amino acids and cholesterol source for P. vannamei; moreover, according digestibility coefficients, fish meal protein can be replaced up to 80% with poultry meal. Yu (2006) considers that 60% fish meal replacement as the maximum, in order to do not affect the growth, due to a low essential amino acids (EAA) ingestion by reducing high digestible (84%) fish meal. In the case of Macrobrachium, Yang et al. (2004) evaluated the potential use of poultry by product meal and meat and bones meal as alternative dietary protein sources, finding that both could replace up to 50% protein fish meal in diets for M. nipponense. Hossain & Islam (2007) considers that the meat and bone meal could be replacing 14% the fish meal in diet of M. rosenbergii postlarvae.

The low digestibility of soybean meal, obtained in this investigation, coincide with values reported for F. paulensis (Lemos et al., 2004) and M. carcinus (Manríquez-Santos et al., 2011). Campaña-Torres et al. (2005) reported that APD of plant origin ingredients was higher than those of animal origin; the highest digestibility was found on soybean meal, in Cherax quadricarinatus juveniles. Also, Chin (1988), evaluated APD in juveniles, adults and females of M. rosenbergii, reporting that coconut paste, wheat meal, and soybean meal were better digested than fish, and shrimp meal (by juveniles and adults); although soybean meal digestibility results do not coincide with our study, but match about the low digestibility of shrimp meal, and fish meal. Hasanuzzaman et al. (2009), in feeding trials with soybean meal, obtained a higher weight, protein efficiency ratio and feed conversion, in M. rosenbergii juveniles with diets with 80% of fish meal replacement by soybean meal. García-Ulloa et al. (2008), in M. tenellum juveniles, compared the growth of prawns fed isoproteic diets (40% CP), replacing fish meal by soybean meal (20, 40, 60, 80 and 100% (w/w) of substitution), finding no significant differences in any of the evaluated growth parameters. This could be due to that reported in present study, where no significant differences on protein digestibility between fish meal and soybean meal was found. Besides Montoya et al. (2016) when comparing the essential amino acids (EAA) profile, of different ingredients, with M. tenellum muscle, found that fish meal (CP > 60%), and soybean meal (47% CP), both only have three limiting amino acids (threonine, lysine, leucine, and methionine lysine, threonine, respectively).

The relative low digestibility of fish meal, obtained in the present study, is according with Campaña-Torres et al. (2005) who found low digestibility of fish meal by C. quadricarinatus juveniles. Lemos et al. (2004) concluded that the differences in protein digestibility of fish meals may be related to the freshness of the raw material used in its production, exhibiting higher digestibility less fresh fish meals, possibly due to hydrolysis during decomposition of the raw material. In this respect, García-Galano et al. (2007) indicate that fish meal used in aquaculture feeds, may vary its quality according fish species used as raw materials, methods of manufacture, cooking and drying temperature, used during processing; also fish meal quality affects the availability of nutrients (Terrazas-Fierro et al., 2010b). Our study is according with the results obtained by Nieto et al. (2005), who found significant differences between degree of hydrolysis (DH) (21.6 to 39.6%) of 15 different fish meals, by in vitro digestibility in pH-stat system using P. vannamei enzymes, these authors consider that the pH-stat method works better on fish meal with high level of protein and low level of ash. Therefore, the low digestibility, found for fish meal in this study may due to low quality (low protein content, <60% CP and high ash content, >18%), according to the classification used by Nieto et al. (2005). In addition, when comparing the EAA profile, according M. tenellum muscle profile (Montoya et al., 2016), the amino acid composition of sardine fish meal (used in our experiment) was adjusted to a lesser extent if compared with to tuna fish meal (with the highest protein content), also according to its amino acid content according to Terrazas et al. (2010a), who proposed that amino acid profile of the tissue of aquaculture animal, must be considered for selecting ingredient for feed formulation, for any species.

In conclusion, the best digestible ingredient for M. tenellum was the Spirulina meal, followed by pork meal, and poultry meal, with high potential be used to formulate diets for prawns, particularly to Macro-brachium species. However, future research work include in vivo digestibility test and feeding trials with diets with the best ingredients, selected by in vitro protein digestibility test, to determine the optimal inclusion level of these ingredients.


We want to thank to Proteínas Marinas y Agropecuarias, S.A. de C.V. for donating the animal meals used in this research. To Patricia Hinojosa Baltazar, for technical support in the Laboratory of Comparative Physiology and Functional Genomics CIBNOR. To Dr. Ernesto Goytortua Bores, for technical support in the Laboratory of Animal Nutrition and Food Plant at CIBNOR.


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Received: January 03, 2017; Accepted: September 03, 2017

Corresponding author: Héctor Nolasco (

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