Penaeus vannamei nursery in a synbiotic system: Effects of different forms of artificially salinized in low-salinity water

doi:10.21203/rs.3.rs-2491805/v1

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Penaeus vannamei nursery in a synbiotic system: Effects of different forms of artificially salinized in low-salinity water

https://doi.org/10.21203/rs.3.rs-2491805/v1

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This study aimed to evaluate the effect of different forms of artificially salinized on the zootechnical performance, TCBS and Sabouraud Dextrose counts in Penaeus vannamei juveniles reared in a synbiotic system. Four treatments were established in triplicate using a completely randomized design: SD (diluted seawater); LCSM (low-cost salt mix with freshwater); CS (commercial salt); and SW (seawater) in experimental tanks of 60 L, with a density of 2,000 PL m^− 3 for 40 days. An ammonia stress test was performed at the end of the culture and TCBS and Sabouraud Dextrose counts in gut was performed at the 20th and 40th. The synbiotic system proved to be effective in the control of nitrogen compounds. The values of calcium, magnesium and total hardness remained above 30, 75 and 400 mg L^− 1, respectively in low salinity treatments. Better values of final average weight were obtained with the different forms of artificially salinized (LCSM, SD and CS), but survival was lower when compared to SW. There was no influence of different forms of artificially salinized on bacterial counts of TCBS and Sabouraud Dextrose, and on resistance to ammonia stress. Based on the results obtained, it can be concluded that it is possible to rear P. vannamei juveniles in artificially salinized water of low salinity (3 g L^− 1) in a synbiotic system.

Growth

Ionic composition

Fungi

Vibrio

Ammonia resistance.

The world aquaculture production in 2020 exceeded 122.5 million tonnes, of which 54.4 million tonnes (44.4%) came from inland waters. The third most produced group is crustaceans, with 11.2 million tons in 2020, with 39% in inland waters. Among these, the most reared species is the shrimp Penaeus vannamei, representing 51.7% of crustacean production (FAO 2022).

The production of P. vannamei is carried out mainly in coastal areas, however, in recent years it has expanded to locations far from the coast and in low salinity conditions (Roy et al. 2010a; Fierro et al. 2018). This can be related to the various economic and environmental advantages presented in these regions when compared to coastal zones, such as lower cost of land acquisition, less conflicts arising from the use of common resources, and reduced impact on not very resilient ecosystems such as mangroves (Jory 2017; Lacerda et al. 2021). This is possible because the shrimp P. vannamei supports a wide range of salinity (0.5–60 g L^− 1), although large variations and an inadequate ionic profile can affect the osmoregulation mechanism and change the nutrient absorption strategy of the species.

In addition, the shrimp culture in low salinities with an inappropriate ionic profile can lead to lower shrimp performance, such as poor survival, reduced growth and/or high feed conversion ratio (Diaz et al. 2001; Li et al. 2017; Ye et al. 2009), which can be minimized by adjusting the mineral supplementation (Ca, Mg, Na and K) so that the water in low salinity becomes similar to the proportions of ions (cations and anions) found in seawater, even with the culture of this species in waters with salinities below 0.5 g L^− 1 (Moraes et al. 2020).

When culture in low salinity uses the technologies of artificially salinized and/or ionic adjustment of the water, with similarity in the proportions of ions in relation to seawater, it favors greater osmotic comfort for the animals, avoiding energy expenditure and helping to increase shrimp growth and survival (Boyd 2002; Nehru et al. 2018). For P. vannamei, the main ratios of cations are Na:K, Mg:Ca and Ca:K, making it necessary to apply these ions in water, through the use of agricultural fertilizers or artificial sea salts.

In order to increase the growth of aquaculture activity in inland regions and minimize the high cost of transporting and/or producing saline water from saline/brackish effluents, techniques such as adding artificial sea salt or diluting the hypersaline water with freshwater, has been widely used, respectively in the USA and Thailand (Boyd and Thunjai 2003; Sowers et al. 2006, Roy et al. 2010a). However, the use of inappropriate technologies can cause a series of environmental impacts on natural ecosystems (Araneda et al. 2008). To minimize these impacts and increase the efficiency of water reuse, generating less application of new fertilizers and/or sea salt in the water, systems with minimum water exchange can be used.

Among the systems of minimum water exchange, the synbiotic stands out, consists of the use of bran after the fermentation process and/or microbial respiration with probiotic microorganisms. This process allows a more diversified growth of microbial aggregates composed of phytoplankton, zooplankton, autotrophic and heterotrophic bacteria, provides an increase in the availability of natural food, reducing the organic load and enhancing the stability of nitrogen when compared to other intensive systems, addition to having low concentrations of suspended solids (Romano et al. 2018; De Andrade et al. 2021; Oliveira et al. 2022a,b; Santos et al. 2022a,b; Pimentel et al. 2022).

The combination of the use of sybiotic systems with ion supplementation (artificially salinized) for the production of juvenile shrimp in low salinity increases could be possibility of shrimp culture far from the coast, since the population of the grow-out phase with juveniles instead of post-larvae increases the survival rate during grow-out phase and the number of production cycles during the year, in addition to providing better acclimatization and resistance to shrimp to the water quality conditions of the ponds.

In this sense, the objective of this work is to evaluate the effect of different forms of artificially salinized on zootechnical performance and water quality, bacterial counts of TCBS and Sabouraud Dextrose and the resistance to ammonia stress in the production of P. vannamei juveniles in a synbiotic system.

2.1 Experimental design and system

The study was carried out for 40 days at the Laboratório de Carcinicultura (LACAR [Shrimp Culture Lab]), of the Departamento de Pesca e Aquicultura (DEPAq [Fisheries and Aquaculture Department]) of Universidade Federal Rural de Pernambuco (UFRPE [Rural Federal University of Pernambuco)], in Brazil. Four treatments in triplicate using a completely randomized design were established: SD, diluted seawater; LCSM, low-cost salt mixture; CS, commercial salt mixture; and SW, seawater.

A matrix tank (0.8 m³ by treatment) with seawater and freshwater was chlorinated with 20 mg L^− 1 of active chlorine and dechlorinated through constant aeration. Twenty days before stocking the postlarvae, the synbiotic started being added at two-day intervals, for a total of ten addition. This synbiotic was obtained through an anaerobic (24 h) and aerobic (24 h) process, from a mixture of 20 g m^− 3 of rice bran (< 200 µm), 2 g m⁻³ of sugar, 0.5 g m^− 3 of commercial bacterial mix (Bacillus subtilis [2.2 × 10⁹ CFU g^− 1], B. licheniformis [1.8 × 10⁹ CFU g^− 1], Bacillus sp. (1.6 × 10⁹ CFU g^− 1), sodium chloride (NaCl), and magnesium hydroxide [Mg(OH)₂], from Kayros Agrícola and Ambiental, SP, Brazil), 4 g m⁻³ of sodium bicarbonate, and previously chlorinated water (20 mg L^− 1 of chlorine per 24 hours, followed by dechlorination by aeration) in the proportion of ten times the amount of rice bran.

An initial inoculum of 5% of the tank volume, with water from a shrimp nursery in a synbiotic system and artificial substrate (14 cm length × 14 cm width × 3.2 cm height made with Anomalocardia brasiliana shells) corresponding to 1% of the volume of the experimental units (60 L), were used. Throughout the culture, the procedure for the preparation of the synbiotic was the same, for four times a week with 50% of the concentrations of the inputs, apart from the probiotic, which continued at 0.5 g m⁻³. The use of the synbiotic was until settleable solids reached 5 ml L^− 1, and applications were suspended past this limit.

The experimental units (60 L) were constantly aerated (dissolved oxygen > 5.0 mg L^− 1), with temperature maintained at ~ 30°C (Hopar Sh-608 heater 100 W), a 12:12 h photoperiod, and mean luminance of 8.65 µmol photons m^− 2 (Equitherm Lux-204). No water exchange was performed during the experimental time. Dechlorinated freshwater was added four times a week to compensate for evaporation loss. Alkalinity correction with sodium bicarbonate (NaHCO₃) was also performed every 10 days after water analysis to reach values > 150 mg L^− 1.

2.2 Salinization adjustment

Prior to the salinization of the treatments, previous studies were carried out on the efficiency of increasing ions in the water by applying chemical products. The tests were performed in experimental units of 14 L, with salinity of ~ 2.5 g L^− 1, obtained by diluting seawater in freshwater under constant aeration. The increase in pH and ion concentration was analyzed after 72 hours of application of 100 g m⁻³ of potassium chloride (KCl), calcium carbonate (CaCO₃), magnesium sulfate heptahydrate (MgSO₄7H₂O), magnesium chloride hexahydrate (MgCl₂6H₂O), and Lithothamnium (Lothar, Primasea, Bahia, Brazil) (Table 1).

Table 1

Increase in percentage of ionic concentration (after 72 hours of application of 100 g m⁻³) of chemical fertilizers used in ionic adjustment.
Fertilizers		KCl	MgSO₄7H₂O	MgCl₂6H₂O	Lithothamnium	NaCl−
% target ion increment	pH^#	0.41 ± 0.04	0.40 ± 0.07	0.17 ± 0.01	0.00 ± 0.00	-
	Ca2+	-	-	-	26.70 ± 1.80	-
	K+	51.10 ± 11.38	-	-	-	-
	Mg2+	-	9.40 ± 0.51	10.52 ± 1.37	5.20 ± 2.00	-
	Na⁺	-	-	-	-	39.42 ± 0.08
	Cl⁻	-	-	-	-	60.33 ± 0.02

Data correspond to the mean of two replicates ± standard deviation. KCl: potassium chloride; CaCO₃: calcium carbonate; MgSO₄7H₂O: magnesium sulfate heptahydrate; MgCl₂6H₂O: magnesium chloride hexahydrate. ^#pH in absolute value.

In view of the results obtained from Table 1 on the increase of ions in the water from the application of mineral fertilizers, the salinization adjustments of the treatments were carried out with commercial products and a commercial salt mixture (Veromix, São Paulo, Brazil) (Table 2), taking into account the salinity of 3.0 g L^− 1 and the proportions of cations (sodium, potassium, calcium and magnesium) and anions (bicarbonate, chloride, sulfate) (Table 3). The adjustment was based on the proportion factors referring to the salinity of the seawater (Boyd and Thunjai 2003; Roy et al. 2010).

Table 2

Fertilizers used in the artificially salinized low-salinity water used in the of *P. vannamei* nursery synbiotic system.
Treatment	Inputs	Ions made available
Commercial salt mixture (CS)	Commercial salt mixture (830 g m⁻³, Veromix) and coarse salt (1,660 g m⁻³)	Sodium, magnesium, potassium, strontium, chlorides, carbonates, bicarbonates, borates, sulfates, bromides, fluorides, and trace elements
Low-cost salt mixture (LCSM)	Coarse salt (1,951 g m⁻³), potassium chloride (52.45 g m⁻³), Lithothamnium (96.67 g m⁻³), magnesium chloride (466.67 g m⁻³), magnesium sulfate (515.13 g m⁻³)	Sodium, chloride, potassium, magnesium, sulfate, and calcium

Table 3

Initial ionic profile in the artificially salinized low-salinity water and seawater used in the *P. vannamei* nursery in synbiotic system.
Variables	Treatments
Variables	LCSM	CS	SD	SW
Ca²⁺ (mg L^− 1)	37.87 ± 9.38^b	26.67 ± 0.92^b	38.40 ± 4.23^b	600.00 ± 105.83^a
Mg²⁺ (mg L^− 1)	90.07 ± 7.55^b	115.67 ± 3.50^b	77.76 ± 3.89^b	1,514.70 ± 248.21^a
K⁺ (mg L^− 1)	34.94 ± 0.98^b	22.22 ± 0.90^b	26.85 ± 1.06^b	322.67 ± 66.89^a
Na⁺ (mg L^− 1)	646.46 ± 19.58^b	679.11 ± 39.59^b	705.23 ± 19.59^b	13,323.53 ± 607.77^a
SO₄²⁻ (mg L^− 1)	230.53 ± 14.37^b	257.97 ± 29.90^b	212.17 ± 44.86^b	3,135.67 ± 212.01^a
Cl⁻ (mg L^− 1)	1,169.85 ± 35.45^b	1,228.93 ± 71.63^b	1,276.20 ± 35.45^b	20,561.00 ± 937.92^a
TA (mg CaCO₃ L^− 1)	61.67 ± 2.89^b	80.00 ± 0.01^b	63.33 ± 5.77^b	135.00 ± 5.00^a
TH (mg CaCO₃ L^− 1)	417.33 ± 20.13^b	542.67 ± 16.65^b	400.00 ± 16.00^b	7,733.33 ± 184.62^a
Salinity (g L^− 1)	3.01 ± 0.09^a	2.99 ± 0.12^b	3.12 ± 0.36^b	35.07 ± 0.54^a
Mg:Ca	2.38	4.34	2.03	2.52
Mg:K	2.58	5.20	2.90	4.69
Ca:K	1.08	1.20	1.43	1.86
Na:K	18.50	30.56	26.26	41.29
TH:TA	6.80	6.78	6.32	57.28
Error (%)	0.88	0.90	2.24	13.88

Data correspond to mean (n = 3) ± standard deviation. SD, seawater diluted; LCSM, low-cost salt mixture; CS, commercial salt mixture; and SW, seawater. TA: total alkalinity; TH: total hardness.

After analyzing the water in all treatments, ion concentrations in milliequivalent L^− 1 (mEq L^− 1) were calculated to check the cation and anion equilibrium. The calculation was performed by determining the difference between the sum of the cation mEq L^− 1 (Na⁺ = 23 mg mEq^− 1; K⁺ = 39.1 mg mEq^− 1; Ca²⁺ = 20 mg mEq^− 1; and Mg²⁺ = 12.15 mg mEq^− 1) and sum of the anion mg mEq^− 1 (HCO₃⁻ = 61 mg mEq^− 1; Cl⁻ = 35.45 mg mEq^− 1; and SO₄²⁻ = 48.03 mg mEq^− 1) (Boyd 2020). A balance error lower than 15% between cations and anions was adopted as a standard for certifying the accuracy of the analysis of these major ions (Boyd 2002). This error was calculated using the following equation:

$$Error \left(\%\right)= \frac{|\varSigma cations - \varSigma anions|}{\varSigma cations + \varSigma anions}\times 200$$

In which:

Σ cations: sum of cations
Σ anions: sum of anions.

2.3 Water Quality

Dissolved oxygen and temperature (Asko multiparameter meter, model AZ86031) were monitored twice a day (8 am and 4 pm). Salinity and pH (Asko multiparameter meter, model AZ86031) were monitored twice a week. The settleable solids (Avnimelech 2009) were monitored three times a week. Total ammonia nitrogen (TAN; APHA 2012), nitrite-nitrogen (NO₂⁻-N; Fries 1971), nitrate nitrogen (NO₃⁻-N; APHA 2012), orthophosphate (PO₄³⁻; APHA 2012), total alkalinity (TA; APHA 2012), total hardness (TH; APHA 2012), Ca²⁺ (APHA 2012), Mg²⁺ (APHA 2012), Na⁺ (APHA 2012), Cl⁻ (APHA 2012), SO₄²⁻ (APHA 2012), and K⁺ (Fries and Getrost, 1977) were monitored every 10 days. All water samples were previously filtered through a 45µm paper filter before performing the analyses.

2.4 Shrimp stocking, feeding, and monitoring

The post-larvae (PL₁₀ ~ 2.0 mg) were acquired in a commercial hatchery (Aquatec, RN, Brazil), produced in water with salinity at 20 g L^− 1. The batch was divided into two tanks with a useful volume of 800 liters (7,500 PL m^− 3), where a part of the PL was acclimated to a salinity of 3.0 g L^− 1 and the other to a salinity of 35 g L^− 1 for 10 days. At the end of the acclimatization period, the PL₂₄ (12 mg ± 1.0 mg) were randomly selected and stocked at a density of 2,000 PL m⁻³ in experimental units.

The postlarvae were fed with a commercial feed of 0.3–0.6 mm granulometry (45% crude protein and 7% lipids, Inve Aquaculture Inc) between day 1 and day 17 of the experimental time. Between day 17 and day 40 of the experimental time, the shrimps were fed with a commercial feed of 0.8–1.3 mm granulometry (45% crude protein, and 9.5% lipids, ADM Animal Nutrition Company). The feed was offered four times a day (8 am, 11 am, 2 pm and 5 pm). Initially, a 27.2% daily feeding rate was adopted, which was gradually reduced to 4.8% of body weight for 40 days. The feeding rate was adjusted daily according to the estimated shrimp feed consumption and mortality rate in each experimental unit (Van Wyk 1999), plus a mix of commercial probiotic (2 g kg feed^− 1) with colony forming units (CFU) g^− 1 containing Bacillus subtilis (8.5 × 10⁸ CFU g^− 1), B. licheniformis (8.5 × 10⁸ CFU g^− 1), B. pumilus (5.0 × 10⁸ CFU g^− 1), B. cereus var. toyoi (8.0 × 10⁸ CFU g^− 1), B. amyloliquefaciens (8.5 × 10⁸ CFU g^− 1), Lactobacillus acidophilus (3.7 × 10⁸ CFU g^− 1), L. plantarum (3.7 × 10⁸ CFU g^− 1), yeast extract, magnesium, and mannan oligosaccharide, in addition to a dispersing agent (Kayros Agrícola e Ambiental, São Paulo, Brazil), manually added to the feed using the commercial binder ®GelSim (Kayros Agrícola e Ambiental, São Paulo, Brazil).

Shrimp weight was monitored every 10 days to determine growth and adjust the amount of feed offered. At the end of the experimental period, final weight, specific growth rate (SGR), feed conversion ratio (FCR), survival, and yield were determined using the following equations:

Final weight (g) = final biomass (g)/number of individuals at the end of evaluation period

SGR (% day^− 1) = 100 × [ln final weight (g) – ln initial weight (g)]/time (days)

FCR = feed supplied/ (final biomass – initial biomass)

Survival (%) = (final number of individuals/initial number of individuals) × 100

Yield (Kg m^− 3) = final biomass (Kg)/volume of experimental unit (m³).

2.5 Presumptive total count on Thiosulphate Citrate Bile Sucrose – TCBS (Vibrio spp.) and Sabouraud dextrose agar (fungi)

Presumptive total count were performed at the Laboratório de Sanidade de Organismos Aquáticos (LASAq [Aquatic Animal Health Lab]), of the Fisheries and Aquaculture Department] of Rural Federal University of Pernambuco, Brazil for the quantification of the colony-forming units (CFUs g^− 1) of Thiosulphate Citrate Bile Sucrose – TCBS (Vibrio spp.) and Sabouraud dextrose agar (Fungi). Shrimp samples for analysis were collected at the 20th and 40th days (pools of 50 mg gut samples each experimental units) (Vandenberghe et al. 1998).

The shrimp were disinfected by immersion in 70% ethanol for 15 seconds, followed by immersion for 15 minutes in sodium hypochlorite solution (1.5%) with 0.1% tween-80 and rinse with sterile distilled water. Subsequently, the biological samples were weighed, macerated and homogenized with a solution of peptone water (2%) in the 1:10 ratio, for the 10^− 1 dilution, serially diluted from 10^− 1 to 10^− 5 and 100 µL were seeded in the plates containing the culture media TCBS and Sabouraud dextrose agar (fungal count made of yeast and filamentous fungi), with the aid of an “L” loop, and then incubated at 30°C for 24 hours (TCBS) and 36°C for 72 hours (Sabouraud dextrose agar), all in triplicate (APHA 2017). After incubation, total colonies were counted using a colony counter, and macromorphological colonial aspects for the characterization of yeast and filamentous fungi were analyzed based on Trabulsi and Alterthum (2015). The conversion to CFU g^− 1 for the shrimp samples and gut samples was performed using the following formula: CFU g^− 1 = number of colonies × dilution factor / weight (g) gut of the sample.

2.6 Ammonia nitrogen Stress tests

At the end of the culture time, shrimp were submitted to resistance test for water ammonia nitrogen concentration (NH₃-N). For the NH₃-N resistance test, at the end of the experiment, 10 shrimps were randomly collected in each experimental unit and were stocked to experimental units containing 10 L of water salinity 3.0 g L⁻¹ (LCSM, CS and SD), and 10 L of water salinity 35 g L⁻¹ (SW) with NH₃-N concentrations between 0.39 and 0.42 mg L⁻¹ (Table 4), water temperature close to 29°C, and pH close to 8.1–8.5. The NH₃-N concentration was achieved by applying a stock solution of 10 g L⁻¹ of NH₄Cl. The test was carried out for 96 h, and survival was measured every 24 h (Zhang et al. 2012).

Table 4

Total ammonia nitrogen (TAN) concentration and non-ionized ammonia (NH₃-N) produced in the experimental units from NH₄Cl solution application.
	TAN (mg L^− 1)		NH₃-N (mg L^− 1)
	SW	LCSM, CS and SD	SW	LCSM, CS and SD
Initial	2.57	4.91	0.41	0.42
24hrs	2.44	4.79	0.39	0.41
48hrs	2.56	4.88	0.41	0.42
72hrs	2.48	4.77	0.40	0.41
96hrs	2.56	4.80	0.41	0.41

Data correspond to the mean concentration of TAN and NH₃-N.

Total hemocyte count (THC)

Hemolymph (10 shrimp per treatment) was collected for the blood analysis before and after the stress tests of ammonia nitrogen concentration (NH₃-N following the protocol described by Guertler et al. 2013). For such, the hemolymph (200 µL) was collected from the hemocoel located in the ventral region of the surviving animals with the aid of a syringe (1 ml) containing anticoagulant (modified Alsever's solution [MAS: 336 mmol L^− 1 of NaCl, 115 mmol L^− 1 of glucose, 27 mmol L^− 1 of sodium citrate, and 9 mmol L^− 1 of EDTA, pH 7.2]) at a proportion of 1:2 (v:v). One aliquot of hemolymph was separated and stored in MAS and 4% formaldehyde (1:3). The total hemocyte count was performed in a Neubauer chamber in a similar manner used for white blood cells in triplicate.

2.8 Data analysis

Statistical analyses were performed using the IBM SPSS Statistic 25.0 software. Data were checked for homogeneity of variances using the Levene test (p ≤ 0,05) and for normality using the Shapiro-Wilk test (p ≤ 0,05). For normal and homogeneous data, parametric one-way ANOVA (shrimp zootechnical performance and total hemocyte count) and repeated measures ANOVA (water quality – dissolved oxygen, temperature, pH, salinity, Ca²⁺, Mg²⁺, Clˉ, K⁺, Na⁺, magnesium hardness, calcium hardness, TH, and TA) were used, followed by Tukey's mean comparison test (P ≤ 0.05). Non-parametric data were analyzed using the Friedman's test with Conover’s multiple comparison test with Holm-Bonferroni correction for TAN, N-NO₂⁻, N-NO₃⁻, settleable solids, and SO₄⁻². TCBS and Sabouraud dextrose agar counts were analyzed using the non-parametric Kruskal-Wallis test (P ≤ 0.05) followed by Dunn's post-hoc test with Holm-Bonferroni correction (P ≤ 0.05).

3.1 Ions

Ion concentration had no significant differences (P > 0.05) among low salinity treatments, but it did have (P < 0.05) when regarding seawater (SW) (Table 5). Calcium concentration showed a little decrease only in CS over the time, while in LCSM and SD they were similar between the beginning and the end. Magnesium concentrations showed a little increased in LCSM and SD over the time, while in CS a little decreased. Potassium concentration a little decreased in LCSM over the time, while in CS and SD they were similar between the beginning and the end.

Table 5

Concentrations (mg L^− 1) of ions from artificially salinized low-salinity water and seawater used in the of *P. vannamei* nursery in synbiotic system.
Variables	Treatments
Variables	LCSM	CS	SD	SW
Ca²⁺ (mg L^− 1)	39.36 ± 5.03^b	34.45 ± 6.42^b	39.78 ± 5.78^b	626.66 ± 46.18^a
Mg²⁺(mg L^− 1)	122.92 ± 20.32^b	86.44 ± 19.05^b	102.38 ± 19.91^b	1,747.80 ± 329.39^a
K⁺ (mg L^− 1)	28.33 ± 5.19^b	24.00 ± 5.86^b	25.37 ± 2.87^b	231.69 ± 71.14^a
Na⁺ (mg L^− 1)	714.37 ± 347.97^b	692.82 ± 294.57^b	767.26 ± 359.91^b	16,482.12 ± 4,052.30^a
SO₄²⁻ (mg L^− 1)	333.18 ± 91.95^b	317.34 ± 54.52^b	316.82 ± 108.13^b	3,881.13 ± 691.12^a
Cl⁻ (mg L^− 1)	1,127.30 ± 552.83^b	1,132.03 ± 455.60^b	1,207.66 ± 549.45^b	25,169.50 ± 6,371.14^a
TA (mg CaCO₃ L^− 1)	165.00 ± 11.92^b	151.00 ± 72.35^b	157.66 ± 104.80^b	200.80 ± 86.65^a
TH (mg CaCO₃ L^− 1)	613.33 ± 10.27^b	498.67 ± 90.25^b	497.33 ± 99.06^b	9,500.00 ± 568.37^a
Calcium hardness (mg CaCO₃ L^− 1)	96.00 ± 26.54^b	81.33 ± 16.13^b	97.33 ± 16.46^b	1,500.00 ± 110.23^a
Magnesium hardness (mg CaCO₃ L^− 1)	512.00 ± 80.30^b	390.67 ± 89.86^b	400.00 ± 85.92^b	8,000.00 ± 464.48^a
Mg:Ca	3.12	2.50	2.57	2.79
Mg:K	4.33	3.60	4.03	7.54
Ca:K	1.39	1.43	1.57	2.70
Na:K	25.22	28.87	30.24	71.13
TH:TA	3.72	3.30	3.15	47.31
Error (%)	0.94	0.46	0.79	13.32

Data correspond to mean ± SD. The results were analyzed by means of a repeated measures ANOVA (P ≤ 0.05) followed by the Tukey test, Friedman's test and Conover's multiple comparison test (P ≤ 0.05) for non-parametric data. SD, seawater diluted; LCSM, low-cost salt mixture; CS, commercial salt mixture; and SW, seawater. TH, total hardness; TA, total alkalinity.

3.2 Water quality

Data on water quality variables are summarized in Table 6. No significant differences among the treatments were found regarding nitrogen compounds (TAN, N-NO_2, N-NO₃). However, significant differences were found for salinity, pH, and SS. The higher values for SS were found in CS treatment (1.64 ± 0.80 ml L^− 1) and the lowest in SW treatment (0.20 ± 0.08 ml L^− 1).

Table 6

Water quality variables in the artificially salinized low-salinity water and seawater used in the of *P. vannamei* nursery in synbiotic system.
Variables	Treatments
Variables	LCSM	CS	SD	SW
Temperature (ºC)	30.50 ± 0.46^a	30.15 ± 0.33^a	30.30 ± 0.44^a	30.01 ± 0.15^a
Oxygen (mg L^− 1)	5.28 ± 0.30^a	5.35 ± 0.22^a	5.21 ± 0.29^a	4.67 ± 0.15^a
Salinity (g L^− 1)	3.00 ± 0.07^b	2.96 ± 0.15^b	2.99 ± 0.34^b	36.50 ± 0.03^a
pH	8.89 ± 0.01^a	8.86 ± 0.08^a	8.90 ± 0.08^a	8.11 ± 0.22^b
TAN (mg L^− 1)	0.18 ± 0.12^a	0.20 ± 0.31^a	0.24 ± 0.12^a	0.23 ± 0.27^a
N-Nitrite (mg L^− 1)	0.42 ± 0.90^a	0.24 ± 0.50^a	0.23 ± 0.10^a	0.42 ± 0.90^a
N-Nitrate (mg L^− 1)	2.84 ± 1.44^a	2.48 ± 1.60^a	3.00 ± 1.66^a	0.82 ± 1.24^a
Settleable solids (ml L^− 1)	1.43 ± 0.56^a	1.64 ± 0.80^a	0.49 ± 0.62^ab	0.20 ± 0.08^b

Data correspond to mean ± standard deviation. The results were analyzed by means of a repeated measures ANOVA (P ≤ 0.05) followed by the Tukey test for the parametric data, and Friedman's test and Conover's multiple comparison test (P ≤ 0.05) for non-parametric data. SD, seawater diluted; LCSM, low-cost salt mixture; CS, commercial salt mixture; and SW, seawater.

3.3 Shrimp zootechnical performance

The shrimp zootechnical performance data at the end of the 40 days of experimental culture are summarized in Table 7. Significant differences among the treatments were found in final weight, with highest value in LCSM (0.87 ± 0.24 g) and lowest in SW (0.65 ± 0.10 g), however, regarding survival, LCSM (70.00 ± 5.00%) showed lower values when compared to SW (90.55 ± 10.58%). No significant differences among the treatments were found regarding yield, FCR and SGR (Table 7).

Table 7

Zootechnical performance of *P. vannamei* juveniles from artificially salinized low-salinity water and seawater in synbiotic system.
Variables	Treatments
Variables	LCSM	CS	SD	SW
Final weight (g)	0.84 ± 0.18^a	0.84 ± 0.04^a	0.72 ± 0.03^a	0.65 ± 0.10^b
Survival (%)	70.00 ± 5.00^b	78.61 ± 3.15^ab	82.77 ± 3.93^ab	90.55 ± 10.58^a
FCR	1.04 ± 0.31^a	1.18 ± 0.01^a	1.25 ± 0.01^a	1.16 ± 0.05^a
Yield (kg m^− 3)	1.01 ± 0.42^a	1.14 ± 0.02^a	1.05 ± 0.06^a	1.09 ± 0.05^a
SGR (% day^− 1)	4.25 ± 0.36^a	4.34 ± 0.81^a	4.56 ± 0.56^a	4.52 ± 0.27^a

Data correspond to mean ± standard deviation. The results were analyzed by means of ANOVA (P ≤ 0.05) followed by the Tukey test. Mean values on the same line with different superscripts differ significantly. SD- seawater diluted; LCSM- low-cost salt mixture; CS- commercial salt mixture; and SW- seawater. FCR- feed conversion ratio; and SGR- specific growth rate.

3.4 Thiosulphate Citrate Bile Sucrose (TCBS, Vibrio spp.) and Sabouraud dextrose agar (fungi)

The Vibrio spp. samples from the shrimp gut at 20 days of culture, were highest in the SW (7.44 ± 9.73 × 10⁴ CFU g^− 1), and the lowest in CS (0.91 ± 1.89 × 10⁴ CFUg ^− 1). The counts at the end of the culture cycle ranged from 15.6 ± 15.5 × 10⁴ CFU g^− 1 (LCSM) to 0.72 ± 1.27 × 10⁴ CFU g^− 1 (SD), however there were no significant differences between treatments. The highest percentage of Vibrio spp. at the end of the culture time were found in SW (28%) and CS (39.9%) (Fig. 1).

Regarding fungi, the SW treatment presented the highest concentration levels (260.0 ± 244.0 × 10⁴ CFU g^− 1) at 20 days of culture. At the end, an increase in filamentous fungi was observed in all low salinity treatments, but they were still less representative when compared to yeasts. The final counts varied between 323.0 ± 287.0 × 10⁴ CFU g^− 1 (LCSM) and 40.2 ± 41.1 × 10⁴ CFU g^− 1 (SW), however, there were no significant differences between treatments. The highest percentage of yeast at the end of the culture time were found in SD (95.7%) and LCSM (92.8%) (Fig. 1).

3.5 Stress tests

Regarding the N-NH₃ resistance test, no significant differences were observed between treatments. After being submitted to the stress test, 100% survival was observed in all treatments, and total hemocyte counts did not differ significantly between treatments. Juveniles had hemocyte counts ranging between 5.00 ± 1.77 × 10⁶ cells mL^− 1 (LCSM) and 2.00 ± 1.17 × 10⁶ cells mL^− 1 in the SD treatment (Fig. 2).

Regarding ions, the different forms of artificially salinized used in this experiment managed to maintain appropriate levels during the nursery phase, even with the observed ecdysis processes, unlike Huong et al. (2010), who described a reduction of ions (calcium and magnesium) in the culture water during the growth of shrimp by the ecdysis process, as they have a high demand for shell formation. These minimal ions variation observed is probably related to the use of the natural substrate of A. brasiliana and rice bran as a source of organic carbon. This maintenance of calcium and magnesium ions provides greater total water hardness and, in addition to higher concentrations of total alkalinity, favor the growth of shrimp. According to Pimentel et al. (2022), there are positive correlations for the concentrations of total alkalinity and calcium regarding final average weight and specific growth rate of P. vannamei juveniles in low salinity water.

The ratio of potassium to sodium in seawater is approximately 28:1, although the shrimp P. vannamei support variations of up to 10 points without interfering with its osmoregulatory capacity (Sowers et al. 2006), especially when alkalinity is greater than or equal to 100 mg CaCO₃ L^− 1 (Pimentel et al. 2022). The Na:K ratio in the low salinity and total alkalinity treatments during the shrimp nursery remained close to the recommended and may have contributed to the activation of the Na⁺, K⁺-ATPase enzyme, allowing the maintenance of cellular metabolism homeostasis and improving the uptake of glucose and amino acids by shrimp (Roy et al. 2007; Galkanda-Arachchige et al. 2021).

Dissolved oxygen and temperature remained within the ideal values for the production of P. vannamei in intensive nursery system (Samocha 2019). The levels of dissolved oxygen in the SW treatment were lower than 5 mg L^− 1, due to the higher concentrations of salts, generating lower solubility of dissolved oxygen (Fiorucci and Filho 2005). However, these concentrations were not limiting for a good development of the shrimp and the transformation of nitrogen compounds by the bacteria in the culture system.

The pH values showed a significant difference between the low salinity treatments (LCSM, CS and SD) in relation to SW. The application of mineral fertilizers for artificially salinized, in addition to the use of sodium bicarbonate in low salinity, contributed to increase the pH of the water. According to Brito et al. (2021), low salinity sodium bicarbonate behaves differently when compared to its use in a marine water system, as it has greater power to increase the pH. Alkalinity adjustments with sodium bicarbonate (NaHCO₃) every ten days in the nursery phase maintained mean concentrations greater than 150 mg CaCO₃ L^− 1, within the recommended range for intensive systems (Samocha 2019), however, it is necessary to pay attention to the pH values.

At low salinity, nitrogen compounds are more toxic, causing large mortalities of shrimp. This problem with nitrogen concentrations can be more accentuated in intensive systems with minimal water exchange in the first days of culture, due to the high concentrations of ammonia and nitrite. In all treatments in this study, TAN and N-NO₂ levels were maintained within the ideal levels for low salinity treatments (< 0.81 mg TAN L^− 1 and < 0.45 mg N-NO₂ L^− 1) and for the seawater (< 3 mg TAN L^− 1 and < 10 mg N-NO₂ L^− 1) (Valencia-Castañeda et al. 2018; Samocha 2019).

This control of nitrogen in different forms of artificial salinization of water is related to the combination of the use of a 5% water reuse inoculum, a synbiotic system and an artificial substrate, as also observed by Pimentel et al. (2022) and Oliveira et al. (2022b), with production of P. vannamei juveniles in low salinity water. These results contribute to the installation of intensive nurseries with minimal water exchange with salinity close to 3 g L^− 1, reducing production costs with artificially salinized, since many researches and productions in artificial waters use higher or close salinity to 10 g L^− 1 (Pinto et al. 2020; Fleckenstein et al. 2022), which makes the cost per m³ of water economically onerous for the production of shrimp in artificially salinized water in some countries.

The concentrations of settleable solids were not different between the forms of artificially salinized, however they were higher than the concentrations with seawater, mainly in the LCMS and CS treatments, due to the application of minerals, similar to the data observed by Oliveira et al. (2022b), in synbiotic with low salinity water. These results are probably related to the lower solubility of these ions in water, as well as the increase in pH, which hinders the solubility of some ions, especially calcium carbonate (Boyd 2020).

Regarding the zootechnical performance of P. vannamei juveniles, observed significant differences in survival between treatments, with the lowest survival in LCSM (70%). However, this results are expressive in relation to those observed by Pinto et al. (2020), who compared only mineral fertilizers and obtained a low survival (15%) compared to artificial sea salt (81%). The application of Lithothamnium (marine algae fossils), which has some important macro and micro minerals for shrimp, probably contributed to the survival of close to 70% in the LCSM treatment, and its application may be increased in future evaluations, since artificial sea salts have a series of micro-constituents and trace elements (Atkinson and Bingman 1997), which contribute to better survival.

The final weight was significantly higher in the low salinity treatments (LSCM, CD to SD) when compared to seawater, which may be related to the higher survival rates found in the SW. However, the other variables of zootechnical performance were similar without the effect of the form of artificially salinized, demonstrating the possibility of producing juveniles in low salinity water in synbiotic system. The final weight and productivity results were similar to those observed in low salinity water (3 g L^− 1) by Pimentel et al. (2022) and Oliveira et al. (2022b); seawater (32 g L^− 1) by Brito et al. (2016).

The FCR values observed were satisfactory for intensive nurseries, in the different forms of artificially salinized. FCR values at low salinity can usually be higher, due to the energy expenditure that shrimp use for osmoregulation, needing to use diets with higher carbohydrate contents or application of mineral supplements (Roy and Davis 2010b). However, in the synbiotic system, the complementation with natural food has contributed to maintain the values in adequate ranges (Pimentel et al. 2022; Oliveira et al. 2022b).

In a system with minimal water exchange, Vibrio spp. have their development favored due to the large amount of organic matter present in the crop cycle (Ferreira et al. 2011; Yanong and Erlaher-Reid 2012). Thus, in a synbiotic system and the application of commercial probiotic on the feed, can reduce the proportion of Vibrio in shrimp, because contributes to the supply of beneficial microorganisms, and can therefore alter the host's microbiota, increasing competition with pathogens and production of enzymes and organic acids, in addition to the reduction of intestinal pH (Huynh et al. 2017; Dawood and Koshio 2020), which can be used as a preventive tool to control Vibrio (Valente and Wan 2021). The artificially salinized of water does not seem to have a direct influence on Vibrio spp. concentration in the shrimp gut when compared to seawater.

As well as bacteria, the presence of fungi (filamentous and yeasts) is observed in synbiotic systems (water and hepatopancreas) of shrimp, however with yeast dominance (de Andrade et al. 2021). These data are similar to the observed in this study, with a synbiotic system and application of probiotics on the feed, with no significant effect of salinity and the forms of artificially salinized. This dominance of yeasts in synbiotic system is important, because yeasts have a high protein value and are rich in B vitamins, with an important effect on the digestive system, helping the functioning of the gut, and playing a role in the defense of the organism against pathogens (Agboola et al. 2021), as the health of shrimp is closely linked to the gut microbiota (Holt et al. 2021).

After 96 hours of the ammonia stress test, the juveniles showed 100% survival, with reduced circulating THC in the hemolymph, indicating an effect of N-NH₃ levels on the immune response. The reduced circulating THC indicate negative effects of environmental stress or infection (Le Moullac et al., 1998; Perazollo et al. 2002), however, with the survivals obtained, we can infer that the shrimp tolerated the evaluated concentrations and the exposure time well, even though the N-NH₃ values were approximately 3 to 4 times higher than the safety limit (concentrations equivalent to 10% of the LC₅₀) for P. vannamei (post-larvae and juveniles) in low salinity (0.12 mg N-NH₃ L^− 1; ValenciaCastaneda et al. 2018) and seawater (0.16 mg N-NH₃ L^− 1; Lin and Chen 2003).

The different forms of artificially salinized were efficient for the maintenance of the main water ions. Regarding the production of P. vannamei juveniles in nurseries with a synbiotic system in artificially salinized water, they obtained similar zootechnical results and resistance to ammonia stress when compared to seawater. Regarding the presumptive count of bacteria in TCBS (Vibrio spp.) the use of the synbiotic and the commercial probiotic on the feed were efficient to keep the concentrations low in artificially salinized water and seawater.

Acknowledgements

The authors are grateful for the financial support provided by the Rural Federal University of Pernambuco, the National Council for Scientific and Technological Development (CNPq), and the Coordination for the Improvement of Higher Education Personnel (CAPES).

Ethical Approval and Consent to participate

The research undertaken complies with the current animal welfare laws in Brazil. Penaeus vannamei used in this experimental work does not need approval from the Ethics Committee for Animal Use in Brazil. All the authors agree to participate in this experiment.

Human and Animal Ethics

The authors followed international and institutional animal management guidelines for the experiments.

Consent for publication

All the authors of this article agree to the publication

Availability of supporting data

The data that support the findings of this study are available on request from the corresponding author.

Competing interests

The authors declare no competing interests.

Funding sources

This work was supported by the Rural Federal University of Pernambuco (Pró-Reitoria de Pesquisa e Pós-Graduação — PRPPG 015/2018), the National Council for Scientific and Technological Development — CNPq (PQ 308063/2019-8 and PQ309669/2021-9), and the Coordination for the Improvement of Higher Education Personnel (CAPES - process numbers 88887. 480069/2020-00, 88887.480067/2020-00, 8887.480542/2020-00 and Financing Code 001).

Credit author statement

Agatha Catharina Limeira: investigation, conceptualization, methodology, formal analysis, writing (original draft). Gênison Carneiro da Silva: investigation, data curation, methodology, formal analysis. Gisely Karla de Almeida Costa: data curation, methodology, formal analysis. Suzianny Maria Bezerra Cabral da Silva: methodology, writing (review and editing). Alfredo Oliveira Galvez: methodology, writing (review and editing). Luis Otavio Brito: supervision, methodology, resources, writing (review and editing).

Declaration of competing interest

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

Authors' information

Departamento de Pesca e Aquicultura, Universidade Federal Rural de Pernambuco, Recife, Brazil.

Agatha Catharina Limeira. E-mail: [email protected]: ORCID: https://orcid.org/

0000-0001-5168-9619

Gênison Carneiro Silva. E-mail: [email protected]: ORCID: https://orcid.org/0000-0002-5760-1726

Gisely Karla de Almeida Costa. E-mail: [email protected]: ORCID: https://orcid.org/0000-0001-8207-1643

Suzianny Maria Bezerra Cabral da Silva. E-mail: [email protected]: https://orcid.org/0000-0002-7571-3465

Alfredo Olivera Galvez. E-mail: [email protected]: http://orcid.org/0000-0001-5149-2605

Luis Otavio Brito. E-mail: [email protected]: ORCID: https://orcid.org/0000-0002-6971-3020.

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Penaeus vannamei nursery in a synbiotic system: Effects of different forms of artificially salinized in low-salinity water

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Abstract

Figures

1. Introduction

2. Material And Methods

2.1 Experimental design and system

2.2 Salinization adjustment

2.3 Water Quality

2.4 Shrimp stocking, feeding, and monitoring

2.6 Ammonia nitrogen Stress tests

2.8 Data analysis

3. Results

3.1 Ions

3.2 Water quality

3.3 Shrimp zootechnical performance

3.4 Thiosulphate Citrate Bile Sucrose (TCBS, Vibrio spp.) and Sabouraud dextrose agar (fungi)

3.5 Stress tests

4. Discussion

5. Conclusion

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