SciELO - Scientific Electronic Library Online

 
vol.46 número3Partial characterization of digestive proteases in adults of bigclaw river shrimp Macrobrachium carcinusSuperoxide dismutase activity in tissues of juvenile cauque river prawn (Macrobrachium americanum Bate, 1868) fed with different levels of protein and lipid índice de autoresíndice de materiabúsqueda de artículos
Home Pagelista alfabética de revistas  

Servicios Personalizados

Revista

Articulo

Indicadores

Links relacionados

  • En proceso de indezaciónCitado por Google
  • No hay articulos similaresSimilares en SciELO
  • En proceso de indezaciónSimilares en Google

Compartir


Latin american journal of aquatic research

versión On-line ISSN 0718-560X

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

http://dx.doi.org/10.3856/vol46-issue3-fulltext-6 

Research Article

Growth and survival of juvenile cauque river prawn Macrobrachium americanum fed with diets containing different protein levels

Juan Carlos Pérez-Rodríguez1 

Stig Yamasaki-Granados2 

Marcelo Ulises García-Guerrero3 

Marcel Martínez-Porchas4 

Yuniel Méndez-Martínez5 

José R. Latournerié-Cervera6 

Edilmar Cortés-Jacinto1 

1Programa de Acuicultura, Centro de Investigaciones Biológicas del Noroeste, La Paz, B.C.S., México

2Instituto Nacional de Pesca (INAPESCA), Centro Regional de Investigación Pesquera La Paz (CRIP-LPZ), La Paz, B.C.S., México

3Laboratorio de Acuacultura, CIIDIR-IPN Oaxaca, Santa Cruz Xoxocotlán, Oaxaca, México

4Departamento de Tecnología de Alimentos de Origen Animal Centro de Investigación en Alimentación y Desarrollo, Sonora, México

5Facultad de Ciencias Pecuarias, Universidad Técnica Estatal de Quevedo (UTEQ) Quevedo, Los Ríos, Ecuador

6Laboratorio de Acuacultura y Producción Acuática, Departamento de Biología Comparada Facultad de Ciencias, Universidad Nacional Autónoma de México, Ciudad de Mexico, Mexico

ABSTRACT

The effect of five diets with different crude protein levels (27, 33, 38, 43, and 48%) on growth and survival of Macrobrachium americanum prawns was determined. Optimum dietary protein level was also calculated. Specimens were collected in the Coyuca River, Guerrero, Mexico, and classified into seven weight groups with 0.67 g intervals amplitude. Five diets with different levels of crude protein were formulated and supplied to individuals of the seven weight groups as an experimental treatment. Weight gain percentage (WG%), specific growth rate (SGR), food intake (FI), protein intake (PI), protein efficiency ratio (PER), food conversion ratio (FCR) and survival rate (SR) were calculated weekly along the 70 days experiment. A quadratic model was fitted to weekly mean weight gain and to WG% rates data to estimate protein requirement for every week of the experiment and weight group. A mortality model was also fitted to mortality data to compare mortality trend among the different experimental diets. 33% protein level resulted in the best treatment because of the parameters calculated, cost to produce and survival trend. Weekly optimum level of protein calculus varied on a range from 39.4 to 43.3% and optimal crude protein percentage for the seven weight ranges was between 49% for smaller prawns (0.248-0.918 g) and 35.7% for the larger prawns (4.271-4.940 g). Thus, it is recommended juvenile feeding prawns with different crude protein levels while the culture time elapses to achieve the maximum weight gain.

Keywords: Macrobrachium americanum; prawn; protein-optimum; survival rate; nutrition; juvenile; aquaculture

INTRODUCTION

Macrobrachium prawns have the potential for freshwater aquaculture and large areas are suitable for its production in Mexico (García-Guerrero et al., 2013). It can be executed in simple facilities at low-cost (Valenti & New, 2000; Moraes-Valenti & Valenti, 2007). Some species are already appreciated as high cuisine products and source of high-quality protein (Gupta et al., 2007). One good example of this is Macrobrachium americanum (Bate, 1868), which is an endemic species distributed along the Pacific coast rivers from Mexico to Peru (Wicksten & Hendrickx, 2003). This species has aquaculture potential and has already demanded as cuisine product in local markets. It is likely to attain higher prices in the market if a proper stable quota of biomass is offered to national and international markets (Ponce-Palafox et al., 2002; García-Guerrero et al., 2013). However, technology for its culture is not available yet.

Supply the optimal protein in food is one of the main requirements for a good profit on cultured animals regarding survival, growth rates, and feed conversion factors (Cortés-Jacinto et al., 2003). A basic nutrient in any balanced diet is protein, one of the major nutrients required for growth and energy production as well as for all physiological processes. Dietary proteins provide the amino acids for the synthesis of muscle, connective tissue and hemolymph respiratory proteins (Harrison, 1990). However, it has been observed the reduction of growth when at low or exceeded protein in the food. If protein level in the diet is low, prawns may not have enough available protein for tissue formation, resulting in growth reduction, whereas an excess could increase energy expenditure and undesired toxicity on water due ammonia excretion (Goda, 2008; Méndez-Martínez et al., 2017).

A protein-efficient diet will reduce the production cost that is a very important aspect, considering that feeding may represent up to 60% of total production costs (Du & Niu, 2003). The optimum dietary protein levels on formulated food for prawns depend on many factors such as age, feeding strategy, protein quality, dietary energy level and protein sources (Méndez-Martínez et al., 2018). Optimum dietary protein level for crustaceans ranges between 23 and 60% depending on those factors (Teshima et al., 2006). For Macrobrachium rosenbergii, an herbivorous-omnivorous and the best-studied freshwater prawn, New (2002) suggested that a 35% of protein on food must be given for the first two months after postlarvae stocking and 30% from month three to harvest. However species-specific differences in protein requirements need to be considered in establishing recommended levels. Considering the above mentioned the study was designed to determine the optimum dietary protein of M. americanum juveniles of seven groups of size subjected to different protein content diets during a seven-week experiment.

MATERIALS AND METHODS

Prawn collection

A total of 105 M. americanum juveniles from the Coyuca River, Coyuca de Benítez, Guerrero, Mexico (17°03'36.14”N, 100°01'42.80”W; 69-132 m above sea level) were collected using a cast-net. The weight of the individuals ranged between 0.25 and 4.94 g. All specimens were acclimated to laboratory conditions and fed with a commercial shrimp pellet (Camaronina® 35% protein) for one week before the experiment (García-Guerrero & Apun-Molina, 2008). Individuals were grouped in seven weight ranges (WR) of 0.67 g length, and 15 individuals included per group (Table 2).

Experimental diets

Five diets with different levels of crude protein (CP) were formulated with Mixit-win® (Agricultural Software Consultants Inc., San Diego, CA, USA) (Table 1). Each different protein amount in the diet (27, 33, 38, 43, 48%) was considered as a treatment, and every treatment had three replicates. So, a total of 15 experimental units were used to test the effect of the five diets.

Table 1 Formulation and proximate composition of five diets (g kg−1 in dry matter) for M. americanum juveniles. 

Ingredient T (CP %)
27 33 38 43 48
Fish meal1 111 209 308 406 505
Whole wheat flour1 625 536 447 357 268
Soybean paste1 100 100 100 100 100
Fish oil1 44 35 26 17 8
Squid meal1 50 50 50 50 50
Alginic acid2 20 20 20 20 20
Soy lecithin3 10 10 10 10 10
Mineral premix in diet4 25 25 25 25 25
Vitamin premix5 3 3 3 3 3
Ascorbic acid6 1 1 1 1 1
Calcium carbonate7 10 10 10 10 10
Choline chloride8 60 60 60 60 60
Proximate composition (g kg−1 as fed-basis)
Crude protein9 268 ± 2.8 327 ± 1.0 378 ± 3.6 428 ± 0.7 477 ± 1.6
Ether extract9 48 ± 1.3 59 ± 7.1 66 ± 0.8 80 ± 0.5 75 ± 0.4
Ash9 62 ± 0.6 79 ± 0.8 97 ± 0.4 114 ± 0.2 129 ± 0.9
Fiber9 5 ± 0.5 5 ± 0.9 5 ± 1.6 5 ± 0.9 3 ± 0.4
Nitrogen free extract 9 617 ± 3.5 531 ± 4.9 455 ± 3.9 373 ± 1.5 317 ± 2.0
Humidity9 69 ± 4.5 74 ± 2.4 59 ± 1.1 60 ± 2.0 57 ± 3.3

1Promotora Industrial Acuasistemas, S.A., La Paz, B.C.S., Mexico.

2SIGMA-ALDRICH® # cat. 180947-500G.

3ODONAJI®, Distribuidora de Alimentos Naturales, S.A. de C.V., Mexico City, Mexico.

4Mineral premix in diet: KCl, 0.05; MgSO4·7H2O, 0.5; ZnSO4·7H2O, 0.09; MnCl2·4H2O, 0.0234; CuSO4·5H2O, 0.005; KCl, 0.005; CoCl2·2H2O, 0.0025; Na2HPO4; 2.37. ALDRICH-SIGMA® Co. St. Louis, USA.

5Vitamin premix diet (mg kg−1): ICN Biomedicals Inc. Ohio, U.S.A. [A (Retinyl acetate), 1.72; D3 (Colacalcipherol), 0.1; E (Cavalli, Tamtin, Lavens, Sorgeloos, Nelis, De Leenheer), 100; K (Menadione), 5; B1 (Thiamine), 60; B2 (Riboflavin), 50; B6 (Pyridoxine), 50; B12 (Cyanocobalamin), 0.2; Pantothenic acid, 75; Nicotinic acid (niacin), 40; folic acid, 10]; SIGMA-ALDRICH® (Biotin, 1; Inositol, 400).

6Vitamin C (35% active) stable Roche®.

7ACS reagent, SIGMA-ALDRICH®.

862% active agent.

9Average of three replications expressed on a dry basis (mean ± standard deviation). T: treatment. CP: crude protein.

Table 2 The seven different prawn groups of Macrobrachium americanum with a weight range of 0.67 g and the number of juveniles per group. 

Group Weight range (g) n
WR1 0.248 - 0.918 26
WR2 0.919 - 1.589 9
WR3 1.59 - 2.259 14
WR4 2.26 - 2.929 17
WR5 2.93 - 3.599 20
WR6 3.6 - 4.27 11
WR7 4.271 - 4.94 8

Proximate analyses of ingredients and diets were determined according to AOAC (2016) to corroborate the real protein level in diets. Each diet was prepared as reported by Cortés-Jacinto et al. (2003).

Experimental design

The 15 experimental units used for this experiment were 30 L containers cover with Styrofoam trays and a bottom area of 0.12 m2. In each experimental seven M. americanum juveniles were placed (average density of 58.3 juveniles per m2), one of each the seven weight ranges previously defined. Each unit was provided with PVC tubes (15 cm long×1.27 cm diameter) and three pieces of the plastic net (25×30 cm) for shelter and to minimize cannibalism over soft prawns by increasing the area (Mariappan et al., 2004; Méndez-Martínez et al., 2018).

Daily water exchange was 30% by siphoning while uneaten feed and feces were discarded. All experiments were maintained with tap freshwater under this procedure: temperature 28.6 ± 0.65°C (Correia et al., 2000), pH 8.0-8.2, dissolved oxygen concentration was always maintained in saturation using air diffusers (8.7 ± 0.3 mg L-1) (Yamasaki-Granados et al., 2013). Juveniles were fed three times per day (5:30, 12:30 and 19:30 h). The total daily ration was set at 5% of total prawn biomass and later diminished to 4% depending on consumption.

Estimation of yield parameters

The experiment lasted 70 days and all parameters were registered every week starting from the first day. Growth was measured as weight increase: weight gain percentage (WG%), specific growth rate (SGR), food intake (FI), protein intake (PI), protein efficiency ratio (PER) and food conversion ratio (FCR) (Table 3). Survival rate (SR) was estimated also. Parameters were calculated as follows:

WG% = (FBW - IBN) × 100 (1)
SR = (final number/initial number of prawns) × 100 (2)
SGR = (ln FBW - ln IBW)/t × 100 (3)
FI = (SF / number of juveniles) / t (4)
PI = (FI) (PF) / SF (5)
FCR = FI (g) / weight gain (g) (6)
PER = weight gain (g) /protein intake (g) (7)

Table 3 Crude protein (CP %) productivity parameters (mean ± SE) and their significant differences in M. americanum juveniles after 70 days of culture. Values within columns with the same superscript are not significantly different (P > 0.05). 

CP (%) SR (%) WG (%) SGR (% day−1) Food intake (g day−1 ind−1) Protein intake (mg day−1 ind−1) FCR PER
27 85.71 9.58 ± 0.99 0.07 ± 0.08a 0.12 ± 0.008a 25 ± 2.08 0.71 ± 0.20a 0.82 ± 0.05a
33 90.47 15.87 ± 1.06a 0.27 ± 0.09a 0.11 ± 0.008a 26 ± 2.42ab 1.26 ± 0.21a 0.79 ± 0.06a
38 90.47 16.09 ± 1.02a 0.27 ± 0.09a 0.12 ± 0.008a 33 ± 3.23abc 1.27 ± 0.20a 0.86 ± 0.06a
43 76.19 14.83 ± 0.99a 0.12 ± 0.08a 0.11 ± 0.008a 35 ± 2.78abc 1.20 ± 0.20a 0.78 ± 0.05a
48 90.47 14.41 ± 0.95a 0.08 ± 0.08a 0.12 ± 0.007a 44 ± 3.45ac 0.96 ± 0.19a 0.84 ± 0.05a

SR: survival rate, WG: Weight gain, SGR: specific growth rate.

In these equations, FBW is the final body weight (g), IBW is the initial body weight (g), t is the time in days, SF is the amount food (g) supplied, PF is the grams of protein in the food.

Statistical analysis

A two-way analysis of variance (ANOVA) was performed to determine the effects of crude protein (CP) level and the initial prawn weight on SGR. The nonparametric Friedman's test tested all others variables (WG%, FI, PI, FCR, and PER) measured-nonparametric Friedman's test. Significant levels were considered at P < 0.05.

A quadratic model was fitted to weekly mean weight gain to estimate protein requirement (Shearer, 2000). The quadratic model was defined as

Y= α + βx+cx2 (8)

where x is the protein level, Y is the response variable, α is the constant, β and c are the linear coefficient and the quadratic coefficient respectively, and x = -β/2c is the inflection point that represents the optimum protein level for the best growth (Shearer, 2000). The quadratic model was also fitted to WG% rates data calculated for each WR as well as the optimum requirement of CP.

A mortality model (Pauly, 1983) was fitted to mortality data to describe the decrease in many individuals and to compare the mortality trend among the different experimental diets and not only the final value. The model is defined as:

y = a × e(-b×t) (9)

where a is the y-intercept, e is the Euler number (2.71828), b is the slope (mortality rate), and t is the number of prawn remaining at the end of time "t".

RESULTS

Growth

The values calculated for all yield parameters and the significant differences among the five different protein treatments are shown (Tables 3-4). There was only a significant difference in diet 27% CP for WG%. It had the smaller value for SGR, and WG% was significantly (P < 0.05) smaller than obtained for all other diets, it was the worst treatment. 38% CP diet had the highest and best values for SR (90.48), WG% (16.09 ± 1.02), SGR (0.27 ± 0.09); and the highest and worst values for FI (0.12 ± 0.008), FCR (1.27 ± 0.20) and PER (0.86 ± 0.06). 33 CP (%) had the same values of 38% CP diet for SR, SGR, and all other variables values were very close (Table 3). Considering only these yield parameters, 33% CP diet seems to offer the best results. It has the lowest protein content, and there were no significant differences in WG% or SGR between the remaining treatments (Table 3).

Table 4 Weight range productivity parameters (mean ± SE) and their significant differences in M. americanum juveniles after 70 days of culture. Values within columns with the same superscript are not significantly different (P > 0.05). 

Weight range SR(%) WG(%) SGR
(% day−1)
Food intake
(g day−1 ind−1)
Protein intake
(mg day−1 ind−1)
FCR PER
1 92.30 14.04 ± 0.77a 0.04 ± 0.06a 0.11 ± 0.12ac 3.16 ± 3.45abcd 0.28 ± 0.15b 0.79 ± 0.04abc
2 100.00 13.30 ± 1.52a 0.12 ± 0.12a 0.08 ± 0.07a 2.00 ± 1.71abc 1.03 ± 0.30ab 0.52 ± 0.08ab
3 85.70 18.97 ± 1.08 0.27 ± 0.09a 0.10 ± 0.12ac 2.84 ± 3.67abcd 1.26 ± 0.22a 0.75 ± 0.06abc
4 76.47 14.63 ± 0.99a 0.16 ± 0.08a 0.11 ± 0.07ac 2.93 ± 1.95abcd 1.13 ± 0.20a 0.74 ± 0.05abc
5 90.00 11.89 ± 0.92a 0.21 ± 0.08a 0.12 ± 0.09abc 3.47 ± 2.59acde 1.11 ± 0.19a 0.86 ± 0.05acd
6 81.81 12.74 ± 1.37a 0.19 ± 0.11a 0.15 ± 0.11bc 4.27 ± 3.08de 1.46 ± 0.27a 1.09 ± 0.07cd
7 75.00 13.53 ± 1.46a 0.13 ± 0.12a 0.14 ± 0.06abc 3.89 ± 1.91acde 1.31 ± 0.20a 1.00 ± 0.08acd

Table 4 presents values of weight range groups. WR3 was the only one significantly different from the others in WG%, food, and protein intake, FCR and PER values. Even though there was a difference in WG%, it was not observed for SGR as we could expect. The groups formed on FCR, PER, food and protein intake seem to cause by size differences since larger individuals consumed more food than small ones and had FCR and PER values are also bigger.

The quadratic model fitted to WG% weekly-data for each experimental diet group, and its inflection point calculus showed that optimum CP is not constant and varied along the experiment on a range from 39.4% to 43.3% (Fig. 1), mean value was 42.2%.

Figure 1 M. americanum juveniles optimum CP variation in diet along with the experiment (70 days). 

WR curves fitted to WG% rates data (Fig. 2) show how protein level on a diet is related to weight gain for the different WR. Optimum CP percentage on a diet calculated had a range from 49 to 36 (Table 5). The smallest WR seems to have higher optimum CP on diet and vice versa, as expected.

Figure 2 Rate curves of WG% for each weight range (WR) of Macrobrachium americanum fed with different amounts of crude protein in their diet. The x and y values presented in the legend represent the inflection points calculated for every fitted curve. 

Table 5 Optimum dietary protein (%) calculated from models fitted to WG% rates for every weight range. 

Weight range (g) Optimum dietary protein (%)
WR1 (0.248 - 0.918) 29
WR2 (0.919 - 1.589) 49
WR3 (1.59 - 2.259) 37
WR4 (2.26 - 2.929) 38
WR5 (2.93 - 3.599) 38
WR6 (3.6 - 4.27) 40
WR7 (4.271 - 4.94) 36

Survival

By diet groups, 33%, 38% and 48% CP diets had the same highest survival rates (90%), followed by 27% CP (86%) and 43% CP (76%) (Table 3). Mortality started at different moments for each treatment. It was first observed at the third week on 48% CP group, last observed at the ninth week on 27% CP group and at sixth week for 33% CP group (Fig. 3). 27% CP group had the highest rate (-0.05) and 43% CP the lowest (-0.007). 33% CP, 38% CP, and 43% CP had similar slope values. Meanwhile, WR groups it seems small individuals had higher survival rates than the big ones. In fact, first two WR had very high values (92% and 100% respectively), and last two had the lower survival rates (81.81% and 75%) (Table 4).

Figure 3 Curves of mortality fitted to survival data for each experimental treatment of Macrobrachium americanum fed with different amounts of protein in their diet. 

DISCUSSION

Water quality was maintained as recommended for prawns (García-Guerrero et al., 2011; Langer et al., 2011; Ding et al., 2015) for all experimental units of all treatments. Diets were formulated using highly digestible ingredients (approximately 87%) similar to those used in experimental diets formulated for prawns and other decapod crustaceans (Campaña-Torres, 2001; Campaña-Torres et al., 2005; Cortés-Jacinto et al., 2009, Méndez-Martínez et al., 2017, 2018). It was observed that M. americanum juveniles were able to digest the presented diets efficiently. Therefore, differences in growth rates could be attributed to different treatments.

The highest WG (16.1%) obtained on the 70 experimental days is lower if compared to that reported for M. rosenbergii by New (2002), which may have a requirement from 35 to 40% of dietary protein depending on stage (Teshima et al., 2006). This author reported that 0.33 g juveniles stocked at a density of 6 ind m-2 in a temperate zone reached an average of 30 g in 106 days in ponds without shelter and nearly 37 g in ponds provided with shelter. These weights increase several times its initial size on a similar time, producing larger prawns than those of present experiment. However, it has to be considered that M. rosenbergii may vary in its food requirements and has well-developed culture techniques and very adapted to pelletized food. It is possible, in agreement with present results, that M. americanum has a slower growth in comparison with other Macrobrachium such as M. rosenbergii even considering this, is possible to observe that 27% CP was the only diet that results in a significant lower WG%. Because of this, 33% CP is suggested as best option since it had very similar results to 38% CP but at a lower cost. Is possible that the lack of proper culture techniques limits its growth potential at commercial scale. So, it is necessary to improve the knowledge on its growth potential by the formulation of a specific diet meeting its requirements to know if the slow growth rate is reasonable for this species or if it is due to improper diet.

The quadratic model used to estimate optimum protein requirement (Shearer, 2000) showed that if only results presented in Table 3 are considered we would underestimate the M. americanum need of CP on a diet. The calculated weekly CP optimum had an average value of 42.2 (range = 39.4-43.3), and the maximum was registered during the fifth week (Fig. 1). 33% CP diet had less protein than the average value calculated by the inflection points, and even below the minimum optimum CP(%) estimated. The optimum CP value in the last week was 41.1%. Therefore if predictions are only based on the final inflection points (week 10) to determine the optimum CP in the diet as has been done in previous studies (Cortés-Jacinto et al., 2003; Goda, 2008), there may be an underestimated optimum for early stages too. That is why size should be considered while formulating and using diets. So, it is suggested to feed prawns with CP from 39.4% to 43.3% depending on size.

WR3 had the best growth response in general for all diet treatments; it had an optimum calculated rate of 4.6 that would be reached at 37.2% of CP in diet, whereas the WR7 had the lowest estimated rate (2.9%) with 35.7% CP. WG% rates tend to be higher at small body sizes (Ra'anan et al., 1991). WR1 seems to have an optimum CP in the diet of 28.9% but, in fact, the optimum level would be >49%. Protein levels required, in the earliest stages, are supposed to be higher. Because the general trend, for most animals, is that the weight gain rate becomes slower as size increases (Lim & Persyn, 1989), so it is possible to assume that if WR2 had an optimum of 49%, then WR1 would have a CP optimum higher. Maybe the curve fitted is underestimating the optimum CP level due to the nature of the data.

Dietary trends observed in this experiment for M. americanum are better in comparison to those reported for M. rosenbergii by New (2002) (35% protein for postlarvae and 30% after three months of culture and until harvest). Du & Niu (2002) also reported the best growth rates were obtained between 20% and 30% of protein level in the diet for M. rosenbergii juveniles (0.075 ± 0.022 g). They also reported ammonia excretion rate was similar between prawns fed 20 and 30% protein level diets but increased beyond 30%, suggesting that 30% protein is near to optimum CP in the diet for the growth of M. rosenbergii. Beyond 30%, some of the ingested protein is wasted as ammonia lowering water quality, whereas prawns fed with 30% protein in their diet may require less energy for basic physiological maintenance. So it seems M. americanum is a more like carnivorous-omnivorous species compared with M. rosenbergii.

The use of a mortality model in experiments such as this has been justified before as useful for populations with discontinuous or irregular survival along a trial since survival is higher or lower depending on culture stage and age (Miller, 2003). When a species requirement is not determined, stress during culture is another factor that may turn irregular the survival, making difficult to describe it by only defining survival as a percentage. Because of this, mortality slopes varied considerably among treatments (Fig. 3). The highest occurred in 27% CP (-0.05) and is mainly associated with the lowest protein content, which may not comply with the minimum required amount, pushing the prawns into cannibalism. Cannibalism is enhanced when such prawns have low protein amounts in the diet, particularly over soft specimens (García-Guerrero & Apún-Molina, 2008; Méndez-Martínez et al., 2018). In fact, food consumption, growth, food-storing behavior are all altered under a lack of an adequate food scheme (Karplus, 2005). In fact, 48% CP diet had the smallest mortality slope, possibly due to the high amount of protein on a diet. Behavioral issues are also involved. Aggressive or dominant prawns may obtain more amount of food, so they can grow faster, while subordinate prawns may have limited food and, hence, show lower growth rates. Because M. americanum is naturally aggressive and territorial, this behavior could be one of the leading causes of cannibalism and dominance, causing low growth rates in captivity and may help to explain the relatively low survival of 27% CP group. If also, food has low quality, this lack of nutrients may cause even slower growth (Kulesh, 2009). We consider that 33% CP is a proper treatment because it showed mortality at the sixth week of the experiment and has a medium slope (Fig. 3). However, although other treatments had similar SR values, overall productivity parameters led to suggest that 33% CP was the best treatment regarding growth and survival. But more studies are required for better understanding of protein digestibility and use by prawns in addition to the proper amount in the diet. For example, it is known circadian, and molt cycles are related, particularly post-molt period generates a need of a gradual accumulation of nutrients for growth and energy production (Amer-Hamsa, 1982). Circadian rhythm in crustaceans varies along the day having an effect on digestive enzymatic activity and therefore in protein digestion (Nolasco-Soria & Vega-Villasante, 1998; Casillas-Hernández et al., 2006).

In conclusion, the optimum protein requirement for growth of M. americanum juveniles may vary ranging from 36% to 49% depending mostly on size. If the final inflection points are considered as criteria in an experiment to determine the optimum CP in the diet, this may help to determine when food with lower protein must be given, but still maintaining best results.

ACKNOWLEDGMENTS

We thank Ernesto Goytortua, Guillermo García Cortés (CIBNOR), and Ahiezer Hernández Valencia for technical support. Thanks to Guadalupe Talamantes for her hard work to complete this study, and Ingrid Mascher for editorial services. This research was supported by the Consejo Nacional de Ciencia y Tecnología of Mexico. The project was supported by CONACYT research grant 156252, 2014/ 227565, and AMEXCID CTC/06038/14. M. García-Guerrero wishes to thank IPN scholarship programs EDI and COFAA. E.C.J. is a fellow of CONACyT (sabbatical project 262236-I0010-2015-03).

REFERENCES

Amer-Hamsa, K.M.S. 1982. Observations on molting of crab Portunus pelagicus Linnaeus reared in the laboratory. J. Mar. Biol. Assoc. India, 24: 69-71. [ Links ]

Association of Official Analytical Chemists (AOAC). 2016. Official methods of analysis of AOAC International. Association of Official Analytical Chemists, Arlington, 2610 pp. [ Links ]

Campaña-Torres, A.L.R. Martínez-Córdova, H. Villarreal-Colmenares & R. Civera-Cerecedo. 2005. In vivo dry matter and protein digestibility of three plant-derived and four animal-derived feedstuffs and diets for juvenile Australian redclaw, Cherax quadricarinatus. Aquaculture, 250: 748-754. [ Links ]

Campaña-Torres, A. 2001. Digestibility of vegetal and animal ingredients and diets for juvenile and pre-adult redclaw Cherax quadricarinatus. M. Sc. Thesis, CIBNOR, S.C. La Paz, B.C.S., México, 124 pp. [ Links ]

Casillas-Hernández, R., H. Nolasco-Soria, F. Lares-Villa, T. García-Galano, O. Carrillo-Farnes & F. Vega-Villasante. 2006. Ritmo circadiano de la actividad enzimática digestiva del camarón blanco Litopenaeus vannamei y su efecto en el horario de alimentación. Rev. Latinoam. Rec. Nat., 2(2): 55-64. [ Links ]

Correia, E., S. Suwannatous & M. New. 2000. Flow-through hatchery systems and management. In: M. New & W. Valenti (eds.). 2000. Freshwater prawn culture: the farming of Macrobrachium rosenbergii. Blackwell Science, Oxford, pp. 52-68. [ Links ]

Cortés-Jacinto, E., H. Villareal-Colmenares, R. Civera-Cerecedo & L.R. Martínez-Córdova. 2003. Effect of dietary protein level on growth and survival of juvenile freshwater crayfish Cherax quadricarinatus (Decapoda Parastacidae). Aquacult. Nutr., 9: 207-213. [ Links ]

Cortés-Jacinto, E., Á. Campa-Córdova, F. Ascencio, H. Villarreal-Colmenares & R. Holguín-Peña. 2009. The effect of protein and energy levels in diet on the antioxidant activity of juvenile redclaw Cherax quadricarinatus (Von Martens, 1868). Hidrobiologica, 19(2): 77-83. [ Links ]

Ding, Z., Y. Zhang, J. Ye, Z. Du & Y. Kong. 2015. An evaluation of replacing fish meal with fermented soybean meal in the diet of Macrobrachium nipponense: Growth, nonspecific immunity, and resistance to Aeromonas hydrophila. Fish. Shellfish Immunol., 44: 295-301. [ Links ]

Du, L. & C.J. Niu. 2002. Effects of dietary protein level on bioenergetics of the giant freshwater prawn, Macrobrachium rosenbergii (De Man, 1879) (Decapoda, Natantia). Crustaceana, 75(7): 875-889. [ Links ]

Du, L. & C.J. Niu. 2003. Effects of dietary substitution of soya bean meal for fish meal on consumption, growth, and metabolism of juvenile giant freshwater prawn, Macrobrachium rosenbergii. Aquacult. Nutr., 9: 139-143. [ Links ]

García-Guerrero, M. & J. Apún-Molina. 2008. Density and shelter influence during adaptation to culture conditions of wild Macrobrachium americanum juveniles. N. Am. J. Aquacult., 70: 343-346. [ Links ]

García-Guerrero, M., J. Orduña-Rojas & E. Cortés-Jacinto. 2011. Size and temperature effects on oxygen consumption of the river prawn Macrobrachium americanum Bate over its regular temperature range. N. Am. J. Aquacult., 73: 320-326. [ Links ]

García-Guerrero, M., F. Becerril-Morales, F. Vega-Villasante & L.D. Espinosa-Chaurand. 2013. Los langostinos del género Macrobrachium con importancia económica y pesquera en América Latina: conocimiento actual, rol ecológico y conservación. Lat. Am. J. Aquat. Res., 41(4): 651-675. [ Links ]

Goda, M.A-S.A. 2008. Effect of dietary protein and lipid levels and protein-energy ratio on growth indices feed utilization and body composition of freshwater prawn, Macrobrachium rosenbergii (de Man, 1879) postlarvae. Aquacult. Res., 39: 891-901. [ Links ]

Gupta, A., H. Singh & G. Kaur. 2007. Growth and carcass composition on giant freshwater prawn, Macrobrachium rosenbergii (De Man), fed different isonitrogenous and isocaloric diets. Aquacult. Res., 38: 1355-1363. [ Links ]

Harrison, K. 1990. The role of nutrition in maturation, reproduction and embryonic development of decapod crustaceans: a review. J. Shellfish Res., 9: 1-28. [ Links ]

Karplus, I. 2005. Social control of growth in Macrobrachium rosenbergii (De Man): a review and prospects for future research. Aquacult. Res., 36: 238-254. [ Links ]

Kulesh, V.F. 2009. Effect of biotic factors on growth and survival of the oriental river prawn Macrobrachium nipponense (Kulesh). Russ. J. Ecol., 40(6): 405-414. [ Links ]

Langer, S., Y. Bakhtiyar & R. Lakhnotra. 2011. Replacement of fishmeal with locally available ingredients in diet composition of Macrobrachium dayanum. Afr. J. Agricult. Res., 6(5):1080-1084. [ Links ]

Lim, C. & A. Persyn. 1989. Practical feeding-penaeid shrimps. In: T. Lovell (ed.). Nutrition and feeding of fish. Van Nostrand Reinhold, New York, pp. 205-222. [ Links ]

Mariappan, P., P. Balamurugan & B. Balasundaram. 2004. Freshwater prawn Macrobrachium nobilii, a promising candidate for rural nutrition. Curr. Sci., 8: 13-14. [ Links ]

Méndez-Martínez, Y., S. Yamasaki-Granados, M.U. García-Guerrero, L.R. Martínez-Córdova, M.E. Rivas-Vega, F.G. Arcos-Ortega & E. Cortés-Jacinto. 2017. Effect of dietary protein content on growth rate, survival and body composition of juvenile cauque river prawn, Macrobrachium americanum (Bate, 1868). Aquacult. Res., 48: 741-751. [ Links ]

Méndez-Martínez, Y., M.U. García-Guerrero, F.G. Arcos-Ortega, L.R. Martínez-Córdova, S. Yamasaki-Granados, J.C. Pérez-Rodríguez & E. Cortés-Jacinto. 2018. Effect of different ratios of dietary protein-energy on growth, body proximal composition, digestive enzyme activity, and hepatopancreas histology in Macrobrachium americanum (Bate, 1868) prawn juveniles. Aquaculture, 485: 1-11. [ Links ]

Miller, T.J. 2003. Incorporating space into models of the Chesapeake Bay blue crab population. Bull. Mar. Sci., 72-2: 567-588. [ Links ]

Moraes-Valenti, P. & W. Valenti. 2007. Effect of intensification on grow out of the Amazon River prawn, Macrobrachium amazonicum. J. World. Aquacult. Soc., 38(4): 516-526. [ Links ]

New, M.B. 2002. Farming freshwater prawns. A manual for the culture of the giant river prawn (Macrobrachium rosenbergii). FAO Fish. Tech. Pap., 428: 215 pp. [ Links ]

Nolasco-Soria, H. & F. Vega-Villasante. 1998. Actividad enzimática digestiva, ritmos circadianos y su relación con la alimentación del camarón, In: R. Civera-Cerecedo, C.J. Pérez-Estrada, D. Ricque-Marie & L.E. Cruz-Suárez (eds.). Avances en nutrición acuícola. IV. Memorias del IV Simposium Internacional de Nutrición Acuícola. 15-18 Noviembre 2000, La Paz, B.C.S., México, pp. 149-165. [ Links ]

Pauly, D. 1983. Algunos métodos simples para la evaluación de recursos pesqueros tropicales. FAO Doc. Tec. Pesca, 234: 49 pp. [ Links ]

Ponce-Palafox, J.F., C. Arana-Magallón, H. Cabanillas-Beltrán & H. Esparza-Leal. 2002. Bases biológicas y técnicas para el cultivo de los camarones de agua dulce nativos del Pacífico americano Macrobrachium tenellum (Smith, 1871) y M. americanum (Bate, 1868). Congreso Iberoamericano Virtual de Acuicultura, 2002: 534-546 pp. [ Links ]

Ra'anan, Z., A. Sagi', Y. Wax, I. Karplus, G. Hulata & A. Kuris. 1991. Growth, size rank, and maturation of the freshwater prawn, Macrobrachium rosenbergii: analysis of marked prawns in an experimental population. Bid. Bull., 181: 379-386. [ Links ]

Shearer, K.D. 2000. Experimental design, statistical analysis, and modelling of dietary nutrient requirement studies for fish: a critical review. Aquacult. Nutr., 6: 91-102. [ Links ]

Teshima, I., S. Koshio, M. Ishikawa, S. Alam & L. Hernandez. 2006. Protein requirements of the freshwater prawn Macrobrachium rosenbergii evaluated by the factorial method. J. World Aquacult. Soc., 37(2): 145-153. [ Links ]

Valenti, W.C. & M. New. 2000. Grow out systems-monoculture. In: M.B. New & W.C. Valenti (eds.). Freshwater prawn culture: the farming of Macrobrachium rosenbergii. Blackwell Scientific, Oxford, pp. 157-176. [ Links ]

Wicksten, M.K. & M. Hendrickx. 2003. Checklist of penaeoid and caridean shrimps (Decapoda: Panaeiodea) from the eastern tropical Pacific. Proc. San Diego Soc. Nat. Hist., 9: 1-11. [ Links ]

Yamasaki-Granados, S., M. García-Guerrero, F. Vega-Villasante, F. Castellanos-León, R.O. Cavalli & E. Cortés-Jacinto. 2013. Experimental culture of the river prawn Macrobrachium americanum larvae (Bate, 1868), with emphasis on feeding and stocking density effect on survival. Lat. Am. J. Aquat. Res., 41(4): 793-800. [ Links ]

Received: June 29, 2017; Accepted: December 11, 2017

Corresponding author: Edilmar Cortés-Jacinto (ecortes04@cibnor.mx)

Creative Commons License This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License, which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.