SciELO - Scientific Electronic Library Online

vol.44 número4Evaluación de la primera madurez sexual del huachinango del Pacífico (Lutjanus peru) nacido en cautiverioCaracterísticas físicas y químicas de biofloc liofilizado producido en cultivos de camarón blanco con diferente inclusión de harina de pescado en la dieta índice de autoresíndice de materiabúsqueda de artículos
Home Pagelista alfabética de revistas  

Servicios Personalizados




Links relacionados

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


Latin american journal of aquatic research

versión On-line ISSN 0718-560X

Lat. Am. J. Aquat. Res. vol.44 no.4 Valparaíso set. 2016 

Research Article


Addition of sodium nitrite and biofilm in a Litopenaeus vannamei biofloc culture system

Adición de nitrito de sodio y biofilm a un sistema de cultivo biofloc de Litopenaeus vannamei


Gabriele Lara1, Plínio S. Furtado1, Bárbara Hostins1, Luís Poersch1 & Wilson Wasielesky Jr.1

1 Institute of Oceanography, Post-graduation in Aquaculture Federal University of Rio Grande (PPGAq-FURG), Rio Grande, RS, Brazil
Corresponding author: Wilson Wasielesky Jr. (
Corresponding editor: Alvaro Bicudo

ABSTRACT. This study evaluates the effects of the previous addition of sodium nitrite (NaNO2) and biofilm in a Litopenaeus vannamei biofloc culture. Five treatments were tested in 180 L - tanks: NaNO2 (-20) addition of NaNO2 for 20 days before stocking and without artificial substrates; NaNO2+B (-20) addition of NaNO2 for 20 days before stocking, with 150% additional artificial substrates; NaNO2 (Stocking) addition of NaNO2 at stocking and no artificial substrates; NaNO2 +B (Stocking) addition of NaNO2 at stocking, with 150% additional artificial substrates and; Control, without NaNO2 addition and without artificial substrates. The study was carried out in two phases: shrimps (0.21 ± 0.08 g) were stocked at a density of 400 ind m-2/1,100 ind m-3, for 30 days (nursery). After this period, the animals were restocked at a lower density (120 ind m-2/400 ind m-3) for 18 more days (grow-out). The turbidity and seattleable solids were higher in treatments without artificial substrates, independently of the addition of NaNO2. The ammonia and nitrite were lower in control, and the nitrate concentrations were higher in treatments with addition of NaNO2 without biofilm. At the end of the nursery, the survival was lower in treatment NaNO2 (-20), and at the end of grow-out the final biomasses were higher in treatments with addition of NaNO2 at the stocking day. In conclusion, the use of a dose of NaNO2 at the stocking day could increase the nitrite-oxidizing bacteria, and the biofilm may contribute to the reduction in suspended particles in water, enhancing shrimp production in biofloc technology system.

Keywords: Litopenaeus vannamei, shrimp, biofloc, nitrogen, artificial substrates.

RESUMEN. Se evaluó los efectos de la adición previa de nitrito de sodio (NaNO2) y biofilm al cultivo de Litopenaeus vannamei en sistema biofloc. Se analizaron cinco tratamientos en estanques de 180 L: NaNO2 (-20) adición de NaNO2 durante 20 días antes de la siembra y sin sustratos artificiales; NaNO2+B (-20) adición de NaNO2 durante 20 días antes de la siembra y con 150% de adición de sustratos artificiales; NaNO2 (Stocking) adición de NaNO2 en la siembra y sin sustratos artificiales; NaNO2 +B (Stocking) adición de NaNO2 en la siembra y con 150% de adición de sustratos artificiales; Control sin adición de NaNO2 y sin substratos artificiales. La densidad de siembra utilizada inicialmente fue de 400 ind m-2/ 1.100 ind m-3 durante 30 días (pre-cría). Después de este periodo, los camarones fueron sembrados a 120 ind m-2/400 ind m-3 por más de 18 días (engorde). La turbidez y los sólidos sedimentables fueron más elevados en los tratamientos sin sustratos artificiales, independientemente de la adición del NaNO2. Las concentraciones de amonio y nitrito fueron inferiores en el control, y las concentraciones de nitrato fueron mayores con la adición de NaNO2 y sin sustratos artificiales. Después del periodo de pre-cría, la supervivencia fue menor en el tratamiento NaNO2 (-20), y al final del período de engorde las biomasas fueron más altas en los tratamientos con adición de NaNO2 en la siembra. En conclusión, la utilización de una dosis de NaNO2 en la siembra puede aumentar las bacterias nitrito-oxidantes, y el biofilm puede contribuir a la reducción de partículas suspendidas en el agua, mejorando la producción de camarones en sistema biofloc.

Palabras clave: Litopenaeus vannamei, camarón, biofloc, nitrógeno, substratos artificiales.



In conventional aquaculture systems, one of the most used management techniques to kept good water quality for cultured animals is the exchange of large volumes of water (Hopkins et al., 1993). Due to the negative environmental impact that the emission of these effluents cause, it is necessary to find alternatives to avoid or reduce this release to water bodies. Rearing in biofloc culture systems has proved to be an effective alternative for the reduction of aquaculture effluent emission. This occurs due to the possibility of reusing water for several cycles, using the microbial community to maintain good water quality and as additional food for the reared animals (Wasielesky et al., 2006; Silva et al., 2013; Krummenauer et al., 2014).

The removal of inorganic nitrogen dissolved in water made by the microbial community can occur via two types of systems: suspended or attached. When suspended, microorganisms move freely in the water, providing direct contact between bacterial cells and the water mass. When attached, microorganisms grow on a layer adhered to a solid surface, which can be artificial or natural depending on the rearing system that is used (Fitch et al., 1998; Nogueira et al., 1998). In the biofloc culture systems, both the microbial community that is formed suspended in the water (bioflocs) and the biofilm (formed on the artificial substrates) can contribute to the metabolism of the nitrogen compounds generated within the culture (Schveitzer et al., 2013; Viau et al., 2013).

However, if there is no balance between the rates of formation and removal of ammonia and nitrite within the system, an accumulation of these compounds may occur, causing production losses. Particularly, high nitrite concentrations seem to be one of the general problems in biofloc culture facilities. The toxic effects of this compound to shrimp are related to a number of different species, causing effects in metabolism, oxygen and food consumption and, immune function (Liao et al., 2012; Campos et al., 2013, 2014; Jiang et al., 2014). In biofloc culture systems, high concentrations of nitrite were reported in many studies (Cohen et al., 2005; Vinatea et al., 2010), and until now, few effective techniques to deal with this problem were found.

Therefore, the use of artificial substrates to increase the surface area for attachment of bacteria was one of the alternatives to minimize ammonia and nitrite spikes in culture (Audelo-Naranjo et al., 2011; Zhang et al., 2016). Moreover, the prior development of the bacterial community through the addition of compounds that may serve as microbial growth stimulators before initiating culture can be another alternative. Based on the view that the population of microorganisms is already mature or stable when the animals are stocked, perhaps the spikes in toxic nitrogen compounds could be avoided (Sesuk et al., 2009). Otoshi et al. (2011) showed a higher efficiency of the nitrification process with the addition of sodium nitrite in L. vannamei biofloc culture. However, these authors do not describe any procedure for the application of this compound in the rearing. Considering the described factors, the aim of this study was to evaluate the effects of the addition of sodium nitrite (NaNO2) and artificial substrates on water quality and growth of Litopenaeus vannamei in a biofloc culture system.


Experimental design

The study was performed at the Marine Station of Aquaculture, Federal University of Rio Grande (FURG), Southern Brazil. The experimental culture system was installed inside a greenhouse, in tanks with 180 L of useful volume (with a lateral surface area of 1.0 m2). Filtered marine seawater (sand filter), chlorinated at 10 ppm and dechlorinated with ascorbic acid (1 ppm) was used to fill the tanks. The study was divided in two phases: initially, juvenile Litopenaeus vannamei (mean weight of 0.21 ± 0.08 g) were stocked at a density of 400 ind m-2, value equivalent to 1.100 ind m-3 (n = 198). This period lasted 30 days and was designated as nursery phase. After this period, the animals were removed from the tanks, counted and restocked in the same tanks at a lower density (120 ind m-2 equivalent to 400 ind m-3; n = 72), for more 18 days (grow-out phase). The culture water (bioflocs) was fully recycled from nursery to the grow-out phase.

The experiment contained four treatments (three replicates each): NaNO2 (-20 days) addition of NaNO2 for 20 days before stocking and without artificial substrates; NaNO2+B (-20 days) addition of NaNO2 for 20 days before stocking, with 150% additional artificial substrates; NaNO2 (Stocking) addition of NaNO2 at stocking and no artificial substrates; NaNO2 +B (Stocking) addition of NaNO2 at stocking, with 150% additional artificial substrates and; Control, without NaNO2 addition and without artificial substrates. The additions of sodium nitrite (NaNO2) were done to stimulate the growth of nitrifying bacteria to a dosage of 2 mg L-1. The proposed value was based on the study of Otoshi et al. (2011), who reported a reduction in the nitrite peak by adding this compound during certain periods of the rearing. In this way, in treatments with previous addition of NaNO2, it was established that the application would occur every two days during the 20 days before stocking, after analysis of nitrite concentrations. Thus, when necessary, the compound was added on a regular basis in order to maintain a nitrite concentration in water of about 2 mg L-1. In other treatments (except in control) the NaNO2 was added only at stocking day, at a concentration of 2 mg L-1.

The formation of bioflocs followed the methodologies proposed by Avnimelech (1999) and Ebeling et al. (2006). Liquid molasses and rice bran were used as carbon sources in order to maintain a C:N ratio of approximately 15-20:1. The shrimp were fed with a commercial diet (Guabi® 38% crude protein and 8% lipids) provided twice a day. The feeding rates were adjusted according to the methodology proposed by Jory et al. (2001). Initially, the shrimps were fed with a feeding rate of 30% of total biomass in each tank and, this rate decreased to 4.5% of biomass until the end of the study.

For the attachment of biofilm, "Needlona™" artificial substrates composed by non-floating nets (mesh size of 1.0 mm) were used. The percentage of substrates added to each tank was calculated according to the lateral area of the tanks, given that the substrates were fixed in the upper part of the tanks and remained submerged during the entire experimental period. The tanks were aerated with air stones placed on the bottom of each experimental tank.

In order to maintain the alkalinity levels in acceptable range to shrimp growth and both to the nitrifying community development, adjustments were made according to Furtado et al. (2011), which recommended alkalinities above 100 mg CaCO3 L-1, using hydrated lime.

Physical and chemical variables of the water

During the 48 days of rearing, the concentrations of dissolved oxygen and the water temperature were monitored, twice a day, using a digital oximeter (YSI™, Model 55). The pH was analyzed once a day, during the morning, using a counter meter (Mettler Toledo, model FE20). The salinity was determinated weekly, using an optical refractometer (Atago). Water sampling to monitor changes in total ammonia (UNESCO, 1983) and water nitrite (Bendschneider & Robinson, 1952) were done daily. The nitrate and phosphate concentrations were analyzed weekly and also followed the methodology proposed by Strickland & Parsons (1972). Alkalinity analyzes were also performed weekly, according to the American Public Health Association (1989) and adjustments with calcium hydroxide were done following the methodology described by Furtado et al. (2011).

The settleable solids (mL L-1) were measured twice a week with Imhoff cones, following the methodology adapted by Avnimelech (2007). For the analysis of total suspended solids (mg L-1), samples of 20 mL of each tank were collected weekly for filtering. The analysis method was adapted from Strickland & Parsons (1972), which consisted of filtering the samples with 0.45 um mesh size membrane filters and subsequent oven drying. Turbidity (NTU) was also analyzed weekly with a digital turbidity meter (Hach, Model 2100P).

Shrimp growth

An initial biometry (n = 100) was performed to estimate the mean weight of the shrimp to be stocked. Throughout the experiment, weekly biometrics (n = 20) were performed to evaluate weight gain (g) and also to adjust the amount of feed provided to the shrimps. Survival was evaluated at the end of the two rearing phases by counting the animals of each experimental unit. The apparent feed conversion rate was calculated by the ratio between the total feed supplied to the shrimp and the difference between the final and initial biomass in each treatment. The final biomass (g) was calculated multiplying the number of survivors shrimp in each tank by its respective final weight in grow-out.

Statistical analysis

Temperature, dissolved oxygen, pH, salinity, alkalinity and performance of shrimp data were analyzed by one-way ANOVA (P < 0.05). The results of ammonia, nitrite, nitrate, turbidity, settleable solids and total suspended solids were analyzed by two-way ANOVA (P < 0.05) in order to determine if there were significant differences among treatments in different experimental days. All tests were performed after confirmation of homogeneity of variances (Levene's test) and data normality (Kolmogorov-Smirnov test). The Tukey test was applied to detect significant differences among means of treatments (Sokal & Rohlf, 1969).


The main results of the physical and chemical water parameters during the 48 days of study are presented in Table 1. The results (global mean ± standard deviation) observed for dissolved oxygen (6.46 ± 0.43), temperature (26.26 ± 1.85), pH (8.04 ± 0.11), salinity (29.76 ± 2.85) and alkalinity (147.87 ± 25.89) did not differ significantly among treatments (P > 0.05). The results of turbidity were higher in treatments where artificial substrates were not used; similarly the settleable solids in these treatments were higher (P < 0.05). The total suspended solids were lower in treatments with substrates, when compared to the treatments with addition of NaNO2 (P < 0.05).


Table 1. Means ± standard deviation of turbidity, settleable solids (SS), total suspended
solids (TSS), total ammonia nitrogen (TAN), nitrite-nitrogen (N-NO2), and nitrate-nitrogen
(N-NO3) over the 48 experimental days. Different letters in the same line correspond to
significant differences among treatments by Tukey test (P < 0.05).


The mean concentrations of ammonia (N-AT) were significantly lower in treatment with addition of NaNO2 at stocking day and without artificial substrate and in control treatments (P < 0.05). Nitrite concentrations (N-NO2) were significantly higher (P < 0.05) in treatments with use of artificial substrates, and lower in the control. Nitrate (N-NO2) concentrations were lower in these same treatments (P < 0.05). Additionally, some differences can be observed between the treatments in which substrates were used. These treatments presented compartmentalization with respect to the nitrogen cycle. In the treatments with biofilm, the nitrite peak occurred from the 42nd experimental day and from this moment the nitrite started decreasing followed by an increase in nitrate. Meanwhile, in the treatments in which only sodium nitrite was added, the concentrations of nitrite and nitrate increase almost simultaneously. Figures 1, 2 and 3 represent the changes throughout time for nitrogen compounds.


Figure 1. Mean variations of total ammonia nitrogen (TAN) during the study
in different treatments.


Figure 2. Mean nitrite concentrations during the study in different treatments.


Figure 3. Mean nitrate concentrations during the study in different treatments.


The performance of the shrimp is presented in Table 2. At the end of the nursery phase, the mean weight of shrimp did not show significant differences among treatments (P > 0.05). The survivals were significantly lower in the treatment where NaNO2 was added 20 days before stocking and without using biofilm, compared to the other treatments (P < 0.05). At the end of the grow-out period, the mean weight was significantly higher (P < 0.05) in treatments with addition of sodium nitrite in the stocking, when compared to treatments with previous addition of sodium nitrite. The control treatment was equal to the other treatments, representing an intermediate value (P > 0.05). The survival was lower in the control and did not show significant differences among the other treatments (P > 0.05). The FCR values (means between nursery and grow-out phases) were significant different (P < 0.05) only between treatments with previous addition of NaNO2 without biofilm and addition of NaNO2 at stocking with biofilm, presenting the higher and the lower values, respectively. The other treatments presented intermediate values and did not differ statistically among them (P > 0.05). The production obtained (g) at the end of the study was significantly higher in treatments with addition of sodium nitrite at stocking day (P < 0.05) and did not present significant differences among the other treatments (P > 0.05).


Table 2. Growth parameters (mean ± SD) of shrimp observed in the two phases of the study
(nursery and grow-out). Different letters in the same line correspond to significant differences
among treatments by Tukey test (P < 0.05). Wi: initial weight (g); Wf final weight (g); S(%):
survival; FCR: mean feed conversion rate of nursery + grow-out phases.



The mean temperature, dissolved oxygen concentrations and pH were maintained within the optimum range for growth and survival of L. vannamei (Ponce-Palafox et al, 1997; Van Wyk & Scarpa, 1999). The mean values obtained for ammonia, nitrite and nitrate remained within the range considered as safe for the performance and survival of the shrimp (Lin & Chen, 2001, 2003; Furtado et al., 2015).

Some studies report the improving in water quality when artificial substrates are used, mainly in the removal of ammonia in intensive shrimp cultures (Huang et al., 2013; Zhang et al., 2016). In contrast, in the present study, it can be observed that the artificial substrates could increase the concentrations of this compound in the rearing environment. The same was related in the study of Ferreira et al. (2016), which observed higher ammonia concentrations in treatments with use of artificial substrates. In addition, it can be observed that the previous addition of sodium nitrite did not contribute to the reduction of this compound in biofloc culture.

Studies dealing with artificial substrates demonstrate higher nitrite peaks when artificial substrates are used in shrimp culture (Bratvold & Browdy, 2001). This authors relates this phenomenon with higher nitrification rates coupled with an unbalance in development of nitrifying community, when the rates of ammonia oxidation exceeds the nitrite oxidation, leading to generation of toxic nitrite concentrations in cultures. Although toxic levels of nitrite were not reached in this study, a similar phenomenon seems to be occurred, where significantly higher concentrations of nitrite were observed in treatments using artificial substrates. The mean concentrations of this compound were lower in the control treatment, indicating that the addition of NaNO2 also did not influence in reducing the nitrite peaks in the system. These results are contrary to the obtained by Otoshi et al. (2011), who observed lower fluctuations in the nitrite levels throughout the rearing of L. vannamei in bioflocs systems with addition of NaNO2 at the same concentrations that were added in this study.

The higher nitrate levels were detected in treatments with only addition of NaNO2, although it was not observed a significant reduction of this compound compared to the control, could be evidence that this management practice may accelerate the growth of nitrite oxidizing bacteria. This result is in accordance with the observed by Otoshi et al. (2011), which evidenced that growth of nitrite-oxidizing bacteria was increased by the addition of sodium nitrite in shrimp biofloc culture. However, longer and more detailed studies are needed to identify these bacteria and the factors which influence its growth rates. Studies with use of artificial substrates are contradictory in regard to the metabolism of nitrogen compounds. In recent studies, Huang et al. (2013), Ferreira et al. (2015) and Zhang et al. (2016) observed an apparently more efficient process in NO2 oxidation using biofilm. Nevertheless, Audelo-Naranjo et al. (2011) did not observed significant differences in nitrogen compounds concentrations with and without biofilm in rearing system, demonstrating that the effects of biofilm in water quality could be variable according to each culture system.

The reduced values in turbidity and settleable solids in treatments with use of artificial substrates are in accordance with the studies of Ferreira et al. (2016) and Zhang et al. (2016). These authors reported a few reasons why this can occur in tanks as lower turbulence in water, resulting in increased floc size, and, absorption or adhesion of the suspended solids by the artificial substrates cloths. The formation of bioflocs occurred more rapidly in the treatments with previous addition of NaNO2, showing that possibly this compound is a stimulator of the microbial community and, therefore, of the development of the bioflocs. Studies conducted by Ray et al. (2010, 2011) and Gaona et al. (2012) demonstrate that the maintenance of low concentrations of total suspended solids can contribute to the development of nitrifying bacteria, likely as a result of competition for substrate with heterotrophic bacteria. Furthermore, these same authors highlight that the management of the solids is also fundamental for the growth of shrimp. The results of total suspended solids obtained in this work are above those recommended by these authors in order to obtain the best results of zootechnical performance in the biofloc system.

In nursery phase, the lower survival observed in treatment with previous addition of sodium nitrite and without artificial substrates could be a result of the elevated concentrations of total suspended solids in water that could cause the clogging of gills, which may retard shrimp growth and affect survival (Ray et al., 2010). Many studies highlight the importance of the natural productivity provided by the biofilm as a supplementary food item to shrimp, enhancing the body weight, final biomass and FCR obtained (Audelo-Naranjo et al., 2011; Huang et al., 2013). In the present study, the use of artificial substrates did not enhance the shrimp growth in neither of the two phases, however could be contributed to high survival in treatment with previous addition of NaNO2 and biofilm, reducing the negative effect of the excess of total suspended solids. A similar positive effect occurred in the study performed by Viau et al. (2013), which observed no significant differences in mean body weight of pink shrimp (Farfantepenaeus brasiliensis), but an increase in survival when biofilm was provided to the culture tanks.

With respect to the addition of the nitrogen compounds to the culture, there are not many studies reporting those effects on growth performance of the reared animals. A study conducted by Sesuk et al. (2009), with previous acclimation (78 days) of a type of surface for bacterial adhesion and addition of ammonium chloride (NH4Cl) proved to be efficient in improving growth results for tilapia in the biofloc technology system. The authors relate that acclimated biofilters with this compound are effective in maintaining acceptable ammonium and nitrite concentrations in water and thus, higher tilapia growth was obtained. Otoshi et al. (2011) reported better results in water quality using sodium nitrite, but did not presented results of shrimp growth in order to compare with the results obtained in this study. The treatments with addition of NaNO2 at the stocking day presented globally better growth results, probably due to the slower growth of the bacterial biomass. The higher final biomasses obtained for these two treatments comparing with others could corroborate this observation.

Analyzing the results obtained for water quality and growth performance of shrimp, the addition of NaNO2 at the stocking day could enhance the growth of nitrite oxidizing bacteria besides improving the growth of shrimp. The use of artificial substrates coupled with the addition of NaNO2, may contribute in reduce the turbidity and settleable solids in rearing system, reducing the risk of losses in growth and survival caused by the excess of suspended particles. More studies are necessary in order to determine the secure dosages of this compound and the time for maturation of microbial community, in order to develop a protocol for the application of NaNO2 in shrimp biofloc culture without losses in production.


The authors are grateful for the financial support provided by the National Council for Scientific and Technological Development (CNPq), Ministry of Fishery and Aquaculture (MPA), and Coordination for the Improvement of Higher Level Personnel (CAPES). We especially thank Centro Oeste Rações S.A. (GUABI) for donating the experimental diets. W. Wasielesky and L. H. Poersch are Research Fellows of CNPq.



American Public Health Association (APHA). 1989. Standard methods for the examination of water and wastewater. Washington, 1193 pp.         [ Links ]

Audelo-Naranjo, J.M., L.R. Martinez-Cordova, D. Voltolina & S. Gomez-Jimenez. 2011. Water quality, production parameters and nutritional condition of Litopenaeus vannamei (Boone, 1931) grown intensively in zero water exchange mesocosms with artificial substrates. Aquacult. Res., 42: 1371-1377.         [ Links ]

Avnimelech, Y. 1999. Carbon/nitrogen ratio as a control element in aquaculture systems. Aquaculture, 176: 227-235.         [ Links ]

Avnimelech, Y. 2007. Feeding with microbial flocs by tilapia in minimal discharge bio-flocs technology ponds. Aquaculture, 264: 140-147.         [ Links ]

Bendschneider, K. & R.J. Robinson. 1952. A new spectrophotometric method for the determination of nitrite in sea water. J. Mar. Res., 11: 87-96.         [ Links ]

Bratvold, D. & C.L. Browdy. 2001. Effects of sand sediment and vertical surfaces (AquaMats) on production, water quality, and microbial ecology in an intensive Litopenaeus vannamei culture system. Aquaculture, 195: 81-94.         [ Links ]

Campos, B.R, P.S. Furtado, F. D'Incao, W. Wasielesky & L.H. Poersch. 2013. Compostos nitrogenados sobre o consumo alimentar de camaräo rosa Farfantepenaeus brasiliensis. Ciencia Rural, 43(12): 2202-2207.         [ Links ]

Campos, B.R, P.S. Furtado, F. D'Incao, L.H. Poersch & W. Wasielesky. 2014. The effect of ammonia, nitrite and nitrate on the oxygen consumption of juvenile pink shrimp Farfantepenaeus brasiliensis (Latreille, 1817) (Crustacea: Decapoda). J. Appl. Aquacult., 26(1): 94-101.         [ Links ]

Cohen, J., T. Samocha, J. Fox, R. Gand & A. Lawrence. 2005. Characterization of water quality factors during intensive raceway production of juvenile Litopenaeus vannamei using limited discharge and biosecure management tools. Aquacult. Eng., 32: 425-442.         [ Links ]

Ebeling, J.M., M.B. Timmons & J.J. Bisogni. 2006. Engineering analysis of the stoichiometry of photoau-totrophic, autotrophic and heterotrophic removal of ammonia-nitrogen in aquaculture systems. Aquaculture, 257: 346-358.         [ Links ]

Ferreira, L.M., G. Lara, W. Wasielesky & P.C. Abreu. 2016. Biofilm versus biofloc: are artificial substrates for biofilm production necessary in the BFT system? Aquacult. Int., 24(4): 921-930.         [ Links ]

Fitch, M.W., N. Pearson, G. Richards & J.G. Burken. 1998. Biological fixed-film systems. Water Environ. Res., 70: 495-518.         [ Links ]

Furtado, P., L.H. Poersch & W. Wasielesky. 2011. Effect of calcium hydroxide, carbonate and sodium bicarbonate on water quality and zootechnical performance of shrimp Litopenaeus vannamei reared in bio-flocs technology (BFT) systems. Aquaculture, 321: 130-135.         [ Links ]

Furtado, P., B.R. Campos, F.P. Serra, M. Klosterhoff, L.A. Romano & W. Wasielesky. 2015. Effects of nitrate toxicity in the Pacific white shrimp, Litopenaeus vannamei, reared with biofloc technology (BFT). Aquacult. Int., 23: 315-327.         [ Links ]

Gaona, C.A.P., L.H. Poersch, D. Krummenauer, G.K. Foes & W. Wasielesky. 2012. The effect of solids removal on water quality, growth and survival of Litopenaeus vannamei in a biofloc technology culture system. Int. J. Recirc. Aquacult., 12: 54-73.         [ Links ]

Hopkins, J.S., R.D. Hamilton, P.A. Sandifer, C.L. Browdy & A.D. Stokes. 1993. Effects of water exchange rate on production, water quality, effluent characteristics and nitrogen budgets of intensive shrimp ponds. J. World Aquacult. Soc., 24: 304-320.         [ Links ]

Huang, Z., R. Wan, X. Song & E. Hallerman. 2013. Assessment of AquaMats for removing ammonia in intensive commercial Pacific white shrimp Litopenaeus vannamei aquaculture systems. Aquacult. Int., 21(6): 1333-1342.         [ Links ]

Jiang, Q., A. Dilixiati, W. Zhang, W. Li, Q. Wang, Y. Zhao, J. Yang & Z. Li. 2014. Effect of nitrite exposure on metabolic response in the freshwater prawn Macrobrachium nipponense. Cent. Eur. J. Biol., 9(1): 86-91.         [ Links ]

Jory, E.J., T.R. Cabrera, D.M. Dugger, D. Fegan, P.G. Lee, A. Lawrence, C.L. Jackson, R.P. McIntosh & J. Castañeda. 2001. A global review of shrimp feed management: status and perspectives. Proceedings of the Special Session on Sustainable Shrimp Culture, Aquaculture 2001. Baton Rouge, pp. 118-143.         [ Links ]

Krummenauer, D., T. Samocha, L.H. Poersch, G. Lara & W. Wasielesky. 2014. The reuse of water on the culture of Pacific white shrimp, Litopenaeus vannamei, in BFT system. J. World Aquacult. Soc., 45(1): 3-14.         [ Links ]

Liao, S., Q. Li, A. Wang, J. Xian, X. Chen, N. Gou, S. Zhang, L. Wang & X. Xu. 2012. Effect of nitrite on immunity of the white shrimp Litopenaeus vannamei at low temperature and low salinity. Ecotoxicology, 21: 1603-1608.         [ Links ]

Lin, Y.-C. & J.-C. Chen. 2001. Acute toxicity of ammonia on Litopenaeus vannamei (Boone) juveniles at different salinity levels. J. Exp. Mar. Biol. Ecol., 259: 109-119.         [ Links ]

Lin, Y.-C. & J.-C. Chen. 2003. Acute toxicity of nitrite on Litopenaeus vannamei (Boone) juveniles at different salinity levels. Aquaculture, 224: 193-201.         [ Links ]

Nogueira, R., V. Lazarova, J. Manem & L.F. Melo. 1998. Influence of dissolved oxygen on the nitrification kinetics in a circulating bed biofilm reactor. Bioprocess Eng., 19: 441-449.         [ Links ]

Otoshi, C.A., N. Rodriguez & S.M. Moss. 2011. Establishing nitrifying bacteria in super-intensive biofloc shrimp production. Glob. Aquacult. Advocate, 14(4): 24-26.         [ Links ]

Ponce-Palafox, J., C.A. Martinez-Palacios & L.G. Ross. 1997. The effect of salinity and temperature on the growth and survival rates of juvenile white shrimp, Penaeus vannamei, Boone, 1931. Aquaculture, 157: 107-115.         [ Links ]

Ray, A.J., K.S. Dillon & J.M. Lotz. 2011. Water quality dynamics and shrimp (Litopenaeus vannamei) production in intensive, mesohaline culture systems with two levels of biofloc management. Aquacult. Eng., 45: 127-136.         [ Links ]

Ray, A.J., K.S. Lewis, C.L. Browdy & J.W. Leffler. 2010. Suspended solids removal to improve shrimp (Litopenaeus vannamei) production and an evaluation of a plant-based feed in minimal-exchange, superintensive culture systems. Aquaculture, 299: 89-98.         [ Links ]

Schveitzer, R., R. Arantes, M.F. Baloi, P.F.S. Costôdio, L. Vinatea, W.Q. Seiffert & E.R. Andreatta. 2013. Use of artificial substrates in the culture of Litopenaeus vannamei (Biofloc System) at different stocking densities: effect on microbial activity, water quality and production rates. Aquacult. Eng., 54: 93-103.         [ Links ]

Sesuk, T., S. Powtongsook & K. Nootong. 2009. Inorganic nitrogen control in a novel zero-water exchanged aquaculture system integrated with airlift-submerged fibrous nitrifying biofilters. Bioresour. Technol., 100(6): 2088-2094.         [ Links ]

Silva, K.R., W. Wasielesky & P.C. Abreu. 2013. Nitrogen and phosphorus dynamics in the biofloc production of the pacific white shrimp, Litopenaeus vannamei. J. World Aquacult. Soc., 44(1): 30-41.         [ Links ]

Sokal, R.R. & F.J. Rohlf. 1969. Biometry. Principles and practices of statistics in biological research. W.H. Freeman, New York, 776 pp.         [ Links ]

Strickland, J.D.H. & T.R. Parsons. 1972. A practical handbook of seawater analysis. Fishery Research Board, Ottawa, 310 pp.         [ Links ]

United Nations Educational, Scientific and Cultural Organization (UNESCO). 1983. Chemical methods for use in marine environmental monitoring. Manual and Guides 12, Intergovernamental Oceanographic Commissiony, Paris, 53 pp.         [ Links ]

Van Wyk, P. & J. Scarpa. 1999. Water quality and management. In: P. Van Wyk, M. Davis-Hodkins, R. Laramore, K.L. Main, J. Mountain & J. Scar (eds.). Farming marine shrimp in recirculating freshwater systems. Florida Department of Agriculture and Consumer Services, Tallahassee, pp. 141-162.         [ Links ]

Viau, V.E., D.M. Souza, E.M. Rodríguez, W. Wasielesky, P.C. Abreu & E.L.C. Ballester. 2013. Biofilm feeding by postlarvae of the pink shrimp Farfantepenaeus brasiliensis (Decapoda, Penaidae). Aquacult. Res., 44: 783-794.         [ Links ]

Vinatea, L., A.O. Gálvez, C.L. Browdy, A. Stokes, J. Venero, J. Haveman, B.L. Lewis, A. Lawson, A. Schuler & J.W. Leffler. 2010. Photosynthesis, water respiration and growth performance of Litopenaeus vannamei in a super-intensive raceway culture with zero water exchange: interaction of water quality variables. Aquacult. Eng., 42: 17-24.         [ Links ]

Wasielesky, W., H.I. Atwood, A. Stokes & C.L. Browdy. 2006. Effect of natural production in a zero exchange suspended microbial floc based super-intensive culture system for white shrimp Litopenaeus vannamei. Aquaculture, 258: 396-403.         [ Links ]

Zhang, J., L. Chen, H. Dong, Y. Duan, Z. Li, G. Wen & J. Xie. 2016. Artificial substrates in zero-water-exchange culture system regulate the rearing performance of Pacific white shrimp Litopenaeus vannamei (Boone, 1931) under the winter indoor condition. Aquacult. Res., 47(1): 91-100.         [ Links ]


Received: 17 October 2015; Accepted: 4 July 2016

Creative Commons License Todo el contenido de esta revista, excepto dónde está identificado, está bajo una Licencia Creative Commons