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Cuantificacion de las bacterias intestinales, costo de operacion y desempeno de alevines de tilapia del Nilo sometido a probioticos.

Quantification of intestinal bacteria, operating cost and performance of fingerlings Nile tilapia subjected to probiotics


Probiotics are living microorganisms that are used as dietary additives; they live in the gastrointestinal tract of the host, adhering to the epithelial wall and proliferating in the intestine. Probiotics may act in the reduction and prevention of infection by pathogens by improving the intestinal bacterial flora, thus reducing the load of harmful bacteria by producing inhibitory substances, and assisting in digestion by producing digestive enzymes and further stimulating the immune system. If they will be used as dietary supplements, they should be able to survive for long periods of storage (Saad, 2006; Sahu et al., 2008; Cutting, 2011; Cruz et al., 2012; Mohapatra et al., 2013).

The tilapia culture generates jobs and income and it has been considered a strong sector in food production in Brazil and tropical places. The productions of large-scale commercial demand a high density of fish stocked, and therefore is common the emergence of diseases caused by stress during cultivation, entailing in a high mortality and economic losses to producer. The minimization of these problems has fostered several studies in last years, looking for changes of the antibiotics in animal production, especially in aquatic organisms culture (Nayak, 2010).

It is noteworthy that the use of probiotics in aquaculture deserves an important highlight on the economic evaluation, within view of the producer can get profitably environmental sustainably a quality fish. Bacillus cereus var. toyoi and B. subtilis C-3102 are products approved by the European Food Safety Authority (EFSA). These probiotics have been recently used in Nile tilapia (Albuquerque, 2011; Moura, 2011; Albuquerque et al., 2013; Mello et al., 2013; Nakandakare et al., 2013; Wild et al., 2014) and shrimp research (Silva et al., 2011; Souza et al., 2012).

The B. subtilis and B. cereus are great candidates probiotics used in aquatic organisms, because according to El-Haroun et al. (2006) this bacterial species can be lyophilized and thus are, capable to survive in high temperatures, such as; after the pelleting process, it can be stored at room temperature without any deleterious effect, and resisted to the low pH that can reach intact to the small intestine (Cutting, 2011), although further development of this technique is required.

This study aimed to quantify total bacteria and total coliforms from the intestinal microbiota and estimate the partial operating costs and productive performance of fingerlings of Nile tilapia of the Genetically Improved Farmed Tilapia (GIFT) strain, fed diets under inclusion of probiotic B. cereus var. toyoi and B. subtilis C-3102.


The experiment was performed at the Aquaculture Laboratory of West Parana State University, Unioeste/ Toledo, Parana, Brazil, from March 2010 to June 2010. Microbiological analyses were carried out in the Laboratory of Microbiology at the Catholic University of Parana, PUCPR/Toledo, over 113 days of cultivation that was divided in the sex reversion and fingerling phases.

A total of 1,200 Nile tilapia post-larvae (Oreochromis niloticus) of the GIFT strain, with an initial average weight of 24.7 [+ or -] 0.50 mg were used. Post-larvae were distributed into 24 aquaria (0.03-[m.sup.3] capacity) in a completely randomized design, comprising in 2 x 3 factorial (phase x bacteria), with four replications. Each aquarium, containing 50 post-larvae (sex reversal phase) or 30 fish (fingerlings phase) it was considered to be an experimental unit, consisting of three treatments (diet+Bacillus subtilis C-3102, diet+Bacillus cereus var. toyoi and diet without probiotic addition).

The fish were reversed sexually, adding in experimental diets the synthetic androgen 17 [alpha]-methyltestosterone, by volatilization of ethanol at a concentration of 60 mg [kg.sup.-1]. The fish were fed ad libitum six times a day and at the end of the day, all aquaria were siphoned to remove any residues.

Initially, during the sex reversal phase was considered an experimental unit an aquarium (0.03-[m.sup.3] capacity) containing 50 post-larvae and in the final period of sex reversal were removed 20% of majors and minors around the mean of the average individual weight of fish with intent to homogenize, the batch for the fingerlings phase. At the beginning of the fingerlings culture, there was a decreased of stocking density for an aquarium containing 30 fish.

A probiotic containing 500 million spores per gram, B. subtilis C-3102 (Comercio e Industria Uniquimica Ltda.) or B. cereus var. toyoi (Sumitomo Chemical do Brazil Ltda.) was used as growth promoters of fish performance. In the diets, which contains probiotic it was added 1% of the product when the ingredients was mixed (Table 1).

It were collected randomly at the end of the sexual reversion and fingerlings phase, one gram of intestines of each experimental unit, in order to quantify the total number of bacteria, total coliforms bacteria, and colonization by probiotics per gram of intestine.

The intestines removed aseptically were weighed and diluted in 1 mL of sterile distilled water per gram of intestine in a test tube, and subsequently homogenized in vortex. Decimal dilutions were performed in sterile distilled water pipes ([10.sup.-1], [10.sup.-2], [10.sup.-3] and [10.sup.-4]) from the homogenized material. The agar medium pattern count (PCA) and Mc Conkey agar (MAC) were used to quantify total bacteria and coliforms bacteria, respectively.

The agar medium selective differentiator for Bacillus was used in Petri dishes with 1 mL of dilute solutions of [10.sup.-1], [10.sup.-2], [10.sup.-3] and [10.sup.-4] for verify the presence of B. subtilis C-3102 and B. cereus var. toyoi. The duly prepared Petri dishes were incubated in a greenhouse microbiological at 28[degrees]C for 24 h. The colonies of bacteria were quantified with the aid of electronic colony counter marks Phoenix CP 600 Plus Electronic, using the official analytical methods for microbiological analysis for control of animal products and water, proposed by the Ministry of Agriculture, Livestock and Supply (Brasil, 2003).

It was used an adaptation of the mathematical model described by Silva et al. (2003) for the economic analysis of the production of tilapia fed with probiotics that considers the costs of acquiring fingerlings and feed prices and gross commercialization of fish. 1) OCP = [(FI x PR) + (NF x UPF)], 2) GR = PP x TB, 3) IC = OCP/TB; 4) = NIP = GR - OCP, wherein: OCP: operating costs partial, FI: feed intake, PR: price per kg [diet.sup.-1]; NF: initial number of fingerlings, UPF: unit price of fingerlings; GR: gross revenue, TB: total biomass; PP: purchase price of the fish, IC: incidence of cost; NIP: net income partial.

The normality of experimental errors and homogeneity of variance for each trait were previously evaluated using the Shapiro-Wilk and Levene tests, respectively. The microbiological data, it is partially operating costs and productive performance were subjected to analysis of variance (ANOVA) and Tukey's test ([alpha] = 0.05) when significant differences were detected (StatSoft, 2005).


It is observed on the Table 2 that the quantification of the total bacteria and total coliforms of intestinal microbiota of tilapia were influenced (P < 0.05) by the stages of culture. The number of colony forming units was lower in the sex reversal phase compared to the fingerlings phase.

The count (log CFU m[L.sup.-1]) of total bacteria ranged between 4.85 for the fish fed without addition of probiotic in the diet formulation and 5.54 for diet with B. cereus. The total bacteria and total coliforms of intestinal microbiota of Nile tilapia were not influenced (P > 0.05) by adding probiotics in the diets. There was not observed effect of interaction between phase and bacteria during tilapia fingerlings culture (Table 2).

It was observed the presence of Bacillus in all treatments. Whereas Bacillus are bacteria Gram positive cosmopolitan which can be isolated from various habitats as water, soil air, then, possibly the fishes which there were not fed with probiotic, it may have exposed by another transmission, such as within ingredient in the diet it contained the genus Bacillus, external manipulation or even water in which the fish were cultured.

The addition of probiotic B. cereus var. toyoi or B. subtilis C-3102 in the diet did not influence (P > 0.05) weight gain (WG), daily weight gain (DWG), specific growth rate (SGR) and apparent feed conversion (AFC) of Nile tilapia fingerlings (Table 3).

The gain in biomass was significantly higher (P < 0.05) in the fish group fed a diet containing B. subtilis than in the group lacking probiotics, however, no differences were observed when compared with fish fed with B. cereus. There were no differences of gain in biomass between fish fed with B. cereus and treatment without probiotics (Table 3).

The survival values were greater (P < 0.05) in the fish group fed, adding probiotic B. cereus var. toyoi or B. subtilis C-3102 in relation to the group fed probiotic-free (Table 3). It is noted that the fish fed B. cereus or B. subtilis resulted a higher biomass of fingerlings compared to those that not fed with probiotics (P < 0.05). The feed intake was not affected by the addition of probiotic B. cereus var. toyoi or B. subtilis C-3102 in diet for Nile tilapia fingerlings (P > 0.05).

Gross revenues of the fingerlings cultivation of Nile tilapia was highly influenced (P < 0.01) by use of probiotics in food, where the revenues from the sale of the fish ranged between 64.18 and 95.41, respectively, for the fish group lacking probiotic and fed adding B. subtilis (Table 3).

The partial operational costs arising with feed costs showed that, the price of the post-reversed fingerlings was affected significantly (P < 0.05) by treatment which in its formulation contained B. subtilis in relation to fishes did not fed with probiotics. However, the partial operational costs of fishes fed with B. cereus did not differ significantly from the group fed with B. subtilis and probiotic-free. The values in this economic parameter did not promote a return satisfactory. Probably this is due to the final biomass together with survival of the fingerlings obtained at the end of cultivation. Wild et al. (2014) evaluating the economic viability of adding probiotic in the Nile tilapia diet found that use of B. cereus showed higher return on investment that the use of B. subtilis or the combination B. cereus and B. subtilis, as part of diets for tilapias.

Body weight and length of fish at the end of fingerlings culture showed geometrical behavior that was expressed by the regression equations (y = 0.1078[x.sup.4.1817]; [R.sup.2] = 0.82; y = 0.209[x.sup.3.1023]; [R.sup.2] = 0.69 and y = 0.1018[x.sup.4.2136]; [R.sup.2] = 0.92), respectively for fish diets that did not contain probiotic B. subtilis and B. cereus (Fig. 1). The determination coefficient ([R.sup.2]) of the weight and length relation represents the proportion the correlation resulting of casual factors, ranged between 0.69 and 0.92 for the fishes that were not fed by probiotics and B. cereus. These results are important and can interfere in a productive performance, aiming to provide fishes more uniforms and get a better use at the time of marketing, because the interaction of the fishes larger about the smaller promotes a hierarchy resulting in a variation of the cultivated lots.

According to Fox et al. (1997), elevated cortisol levels may induce alterations in the production of growth hormone (GnRH), therefore, explains the difference in the weight and size between individuals of the same lot. Therefore, the dominant fishes tend to form feeding zones the incumbent subordinates to feed, therefore increasing the range of fish size.


Jatoba et al. (2008) while studying the isolation of lactic acid bacteria of the intestine of tilapia through probiotics potential, they observed values of total bacteria different to those found in the present study in which varied between 6.35 and 8.06 log CFU m[L.sup.-1].

The addition of probiotic B. cereus var. toyoi and B. subtilis C-3102 did not influence (P > 0.05) the weight gain, average daily weight gain, specific growth rate and feed conversion of Nile tilapia juvenile (Table 3). Like the present study, Marengoni et al. (2010), using B. subtilis, B. pumilus and B. lincheniformis as probiotic in diets for red tilapia fingerlings, found similar results whose probiotics did not influenced the production performance and survival. Albuquerque (2011) and Moura (2011) also found no differences in the addition of probiotics in diets on performance of Nile tilapia fingerlings of GIFT strain.

Probably the time of use of probiotics has influenced in the total bacteria count during cultivation. In addition, the probiotics used in vivo were isolated from gut of the fishes of the same population that would be subsequently subjected to a challenge, as opposed to what was done in this study. Together with this hypothesis, these values may have been different due to the inhibition mechanisms by competitive exclusion for nutrients, space or specificity relationship probiotic-host, as reported by Gomez-Gil et al. (2000).

In relation to incidence of cost it was found that, it was no significant differences between the treatments containing probiotic or not in formulation (P > 0.05). The values of incidence of cost are not in accordance with those observed by Marengoni et al. (2008) and when evaluated the different stocking densities upon performance and economic viability of juvenile Nile tilapia in western Parana, it were obtained in this parameter a variation of values between 0.67 and 2.00, resulting this, due to the higher biomass obtained at the end of cultivation.

Similarly, Olvera-Novoa et al. (2002) which studying the utilization of Candida utilis as protein source for tilapia fingerlings they obtained a minimum value of 2.24 whereas that, within this study they showed values of 1.09 and 2.64, respectively for maximum and minimum incidence of cost (Table 3).

Taking into consideration that there were no significant differences (P > 0.05) in feed consumption of fingerlings that contained B. subtilis in the formulation and, more expressive values of total biomass and gross income (P < 0.05), generating a lesser of cost incidence it is possible recommend the utilization of this probiotic for fingerlings the Nile tilapia, with particular emphasis on environmental sustainability of fish farming (Wild et al., 2014).


The inclusion of Bacillus subtilis C-3102 and Bacillus cereus var. toyoi in diets for Nile tilapia fingerlings of the GIFT strain promotes intestinal colonization and can be recommended in the cultivation of this species during sex reversal and fingerlings phases.

The inclusion of B. subtilis and B. cereus as part of diets for Nile tilapia promotes intestinal colonization and improves the survival rate without negatively influencing the feed intake of the fingerlings, total biomass, gross revenue and partial operating costs and net revenue. Therefore it recommends the use of these probiotics in growth of fingerlings Nile tilapia, GIFT strain.

DOI: 10.3856/vol43-issue2-fulltext-13


The authors thank to "Coordenacao de Aperfeicoamento de Pessoal de Nivel Superior (CAPES)" by partially grant funding for the research. The authors are also thankful to Mr. Milton Cezar de Moura (PUC/PR) and Mr. Ilson Mahl (Copacol/PR) for supporting during the research period.


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Received: 29 June 2013; Accepted: 2 March 2015

Nilton Garcia-Marengoni (1) & Daniele Menezes-Albuquerque (2)

(1) Universidade Estadual do Oeste do Parana (Unioeste) Marechal Candido Rondon, 85960-000, Parana, Brasil

(2) Universidade Federal da Grande Dourados (UFGD), Mato Grosso do Sul, Brasil

Corresponding author: Nilton Garcia-Marengoni (

Caption: Figure 1. Weight curves (g) and length (cm) of fingerlings Nile tilapia probiotic-free (a), Bacillus subtilis (b), and Bacillus cereus (c).
Table 1. The percentage of composition and chemistry of experimental
diets for Nile tilapia grown during the sex reversal and fingerlings

Ingredient                                     Bacteria

                                  Probiotic-free   Bacillus subtilis

Soybean meal                               44.91               44.25
Fish meal                                  24.50               24.65
Corn bran                                  24.13               23.07
Probiotic                                     --                1.00
Mineral and Vitamin Premix (1)              1.00                1.00
DL-methionine                               0.21                0.21
Antioxidant                                 0.02                0.02
Soybean oil                                 3.71                4.28
Dicalcium phosphate                         2.12                2.13
Limestone                                     --                0.01
Salt                                        0.30                0.30

Total                                        100                 100

Nutrient                                                         (%)

Starch                                     15.04               16.29
Calcium                                     1.55                1.44
Digestible energy (tilapia)             3,296.00            3,272.00
Crude fiber                                 3.22                2.96
total phosphorus                            1.11                1.00
Ether extract                              6.565                5.92
Total lysine                                2.35                2.39
Methionine total                            0.87                1.05
Crude protein                              37.53               37.24

Ingredient                            Bacteria

                                  Bacillus cereus

Soybean meal                                44.25
Fish meal                                   24.65
Corn bran                                   23.07
Probiotic                                    1.00
Mineral and Vitamin Premix (1)               1.00
DL-methionine                                0.21
Antioxidant                                  0.02
Soybean oil                                  4.28
Dicalcium phosphate                          2.13
Limestone                                    0.01
Salt                                         0.30

Total                                         100


Starch                                      16.29
Calcium                                      1.44
Digestible energy (tilapia)              3,272.00
Crude fiber                                  2.96
total phosphorus                             1.00
Ether extract                                5.92
Total lysine                                 2.39
Methionine total                             1.05
Crude protein                               37.24

(1)Mineral and Vitamin Premix: Composition per kg of product: iron:
10.312 mg, Mn: 6.875 mg, cooper: 1.100 mg, zinc: 16.500 mg, iodo: 137
mg, cobalt: 82.50 mg, selenium: 124.00 mg, chrome: 68.75 mg, vit. A:
1,100.000 UI; vit. [D.sub.3]: 344.000 UI; vit.: E: 27.500 mg; vit. K:
1.375 mg; vit. C: 41.250 mg; biotin: 130.50 mg; choline: 75.625 mg;
vit. [B.sub.9]: 825.00 mg; inositol: 27.500 mg; niacin: 13.750 mg;
vit. [B.sub.5]: 6.875 mg; vit. [B.sub.6]: 2.063 mg; vit. [B.sub.2]:
2.750 mg; vit. [B.sub.1]: 2.750 mg and vit. [B.sub.12]: 4.120 mg.

Table 2. Mean values and standard deviation (log CFU m[L.sup.-1]) of
total bacteria, coliforms, presence (+) or absence (-) of Bacillus in
Nile tilapia fed with different probiotics during periods of sex
reversal and fingerlings phases. F: variable test, P: critical

Parameter             Total Bacteria        Bacterial count

Phase cultivation       F = 12.59;            F = 18.83;
                        P = 0.00097           P = 0.00009

Sex reversal        4.59 [+ or -] 0.10b   3.05 [+ or -] 0.06b
Fingerlings         5.97 [+ or -] 0.39a   4.66 [+ or -] 0.36a

Bacteria                 F = 1.23;             F = 0.05;
                        P = 0.30304           P = 0.94724

Probiotic-free      4.85 [+ or -] 0.53    3.79 [+ or -] 0.48
Bacillus subtilis   5.54 [+ or -] 0.29    3.93 [+ or -] 0.31
Bacillus cereus     5.44 [+ or -] 0.28    3.84 [+ or -] 0.33

Bacteria Phase           F = 2.48;             F = 1.54;
                        P = 0.09607           P = 0.22666

Parameter           Bacillus

Phase cultivation

Sex reversal           +
Fingerlings            +


Probiotic-free         +
Bacillus subtilis      +
Bacillus cereus        +

Bacteria Phase

Table 3. Mean values and standard deviations of economic variables in
the cost of production of Nile tilapia fed different probiotics. F:
variable test, P: critical values.

Parameter                          Bacteria


WG (g) (1)                    8.53 [+ or -] 0.48
DWG (g [day.sup.-1]) (2)      0.11 [+ or -] 0.01
SGR (% [day.sup.-1])          4.58 [+ or -] 0.07
GB (g) (4)                   155.5 [+ or -] 25.85b
afc (5)                       1.63 [+ or -] 0.41
SUR (%) (6)                  76.43 [+ or -] 0.08b
TFC (kg) (7)               7 001.63 [+ or -] 909.90
PR (R$) (8)                          1.72
UPF (R$) (9) (##)                    0.08
SPF (R$) (10)                       102.00
BT (kg) (11)               5 465.04 [+ or -] 865.34b
GR (R$) (12)                 64.18 [+ or -] 10.53b
OCP (R$) (13)                91.88 [+ or -] 1.63b
NIP (R$) (14)                -27.71 [+ or -] 9.32b
IC (R$ [kg.sup.-1]) (15)      0.03 [+ or -] 0.01

Parameter                          Bacteria

                               Bacillus subtilis

WG (g) (1)                    8.99 [+ or -] 0.64
DWG (g [day.sup.-1]) (2)      0.12 [+ or -] 0.01
SGR (% [day.sup.-1])          4.85 [+ or -] 0.10
GB (g) (4)                  242.25 [+ or -] 21.27a
afc (5)                       1.02 [+ or -] 0.06
SUR (%) (6)                  94.58 [+ or -] 0.01a
TFC (kg) (7)               8 897.51 [+ or -] 690.78
PR (R$) (8)                          1.91
UPF (R$) (9) (##)                    0.08
SPF (R$) (10)                       106.50
BT (kg) (11)               8 315.33 [+ or -] 707.78a
GR (R$) (12)                 95.41 [+ or -] 2.64a
OCP (R$) (13)                96.82 [+ or -] 1.12a
NIP (R$) (14)                -1.41 [+ or -] 2.44a
IC (R$ [kg.sup.-1]) (15)      0.01 [+ or -] 0.00

Parameter                           Bacteria             (F; P) (#)

                                Bacillus cereus

WG (g) (1)                     8.46 [+ or -] 0.48       0.28; 0.75576
DWG (g [day.sup.-1]) (2)       0.11 [+ or -] 0.01       0.28; 0.75576
SGR (% [day.sup.-1])           4.59 [+ or -] 0.08       3.02; 0.07060
GB (g) (4)                  221.48 [+ or -] 13.78ab     4.70; 0.02060
afc (5)                        1.11 [+ or -] 0.05       1.87; 0.17855
SUR (%) (6)                   93.76 [+ or -] 0.02a      5.46; 0.01233
TFC (kg) (7)                8 981.59 [+ or -] 399.80    2.57; 0.10059
PR (R$) (8)                           1.85                   --
UPF (R$) (9) (##)                     0.08                   --
SPF (R$) (10)                        102.00                  --
BT (kg) (11)               7 659.96 [+ or -] 463.19ab   4.57; 0.02257
GR (R$) (12)                  90.10 [+ or -] 4.48a      5.60; 0.00869
OCP (R$) (13)                96.02 [+ or -] 0.80ab      4.63; 0.02159
NIP (R$) (14)                -5.92 [+ or -] 4.48ab      5.27; 0.01410
IC (R$ [kg.sup.-1]) (15)       0.01 [+ or -] 0.00       1.77; 0.19412

(##) The price according to weight-thousand (g) data
Atoaqui--Associacao Toledana de Aquicultura haverst-2010-2011 in Toledo,
Parana, Brazil; (1) Weight Gain (WG), (2) Daily Weight Gain (DWG),
(3) Specific Growth Rate (SGR), (4) Gain in Biomass (GB), (5)
Apparent Feed Conversion (AFC), (6) Survival Rate (SUR), (7) Total
Feed Consumption (TFC), (8) Price per kg diet-1 (PR), (9) Unit Price
of Fingerlings (UPF), (10) Selling Price of Fingerlings (SPF) (11)
Biomass Total (BT) (12) Gross Revenue (GR) (13) Operating Cost
Partial (OCP), (14) Net Income Partial (NIP) (15) Incidence of cost
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Title Annotation:Research Article
Author:Garcia-Marengoni, Nilton; Menezes-Albuquerque, Daniele
Publication:Latin American Journal of Aquatic Research
Date:May 1, 2015
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