Received: 13 May 2019 Revised: 23 June 2021 Accepted: 23 July 2021

DOI: 10.1111/jwas.12845

FUNDAMENTAL STUDIES

Effect of water salinity on the oxidative system of

juveniles of the North Atlantic white shrimp
Litopenaeus setiferus reared in biofloc technology

Manuel Valenzuela-Jiménez1,2 | Claudia Durruty-Lagunes1 |

Gerard Cuzon1 | Eduardo Pacheco1 | Miguel Arévalo1 |
Diana Aguilera-Rivera3 | Wilson Wasielesky2 |
Gabriela Rodríguez-Fuentes4 | Alvaro Barreto5 | Gabriela Gaxiola1

1
Unidad Multidisciplinaria de Docencia e

n de Sisal, Fac. de Ciencias,
Investigacio
Abstract
Universidad Nacional Auto
noma de México, This study evaluated the effect of biofloc technology (BFT) at
Sisal, Mexico
3 (lsBFT) and 35 (hsBFT) practice salinity units (psu) on the
2
PPGAqui, Estaç~ao Marinha de Aquacultura,
zootechnical performance, oxygen consumption, antioxidant
Instituto de Oceanografia, Universidade
Federal do Rio Grande (FURG), Rio Grande, activity, and oxidative damage of Litopenaeus setiferus juve-
Brazil niles reared in outdoor tanks. After 90 days, no significant dif-
3
Escuela Nacional de Estudios Superiores, ferences were observed in terms of survival (p > .05). The final
Unidad Mérida, Universidad Nacional

noma de México, Merida, Mexico
Auto
weight as well as wet weight gain, final biomass, and feeding
4
Unidad de Química-Sisal, Facultad de conversion ratio (FCR) showed higher values for shrimp reared
Química, Universidad Nacional Auto
noma de with hsBFT than those reared with lsBFT (p < .05). Compared
México, Sisal, Mexico
to that for the hsBFT treatment, high oxygen consumption
5

gicas y
Posgrado de Ciencias Biolgo

noma de
(VO2) was observed for the lsBFT treatment under fasting and
Agropecuarias, Universidad Auto
Nayarit, Tepic, Mexico postprandial conditions (p < .05). The activity of the enzymes
catalase, superoxide dismutase, and glutathione-S-transferase
Correspondence
Gabriela Gaxiola, Unidad Multidisciplinaria de from shrimp muscle did not show significant differences

n de Sisal, Fac. de
Docencia e Investigacio between the treatments (p > .05). Regarding the lipid peroxi-

noma de
Ciencias, Universidad Nacional Auto
dation (LPO) and oxidized protein (PO) in muscle samples, no
México, 97356, Sisal, Yucatan, Mexico.
Email: mggc@ciencias.unam.mx significant differences were observed in LPO, whereas the PO
was significantly higher for the lsBFT treatment (p < .05),
Funding information
UNAM DGAPA, Grant/Award Number: which was related to higher fasting and postprandial oxygen
221316-3 consumption of the juveniles (p < .05). The adaptation of

This is an open access article under the terms of the Creative Commons Attribution-NonCommercial-NoDerivs License, which
permits use and distribution in any medium, provided the original work is properly cited, the use is non-commercial and no
modifications or adaptations are made.
© 2021 The Authors. Journal of the World Aquaculture Society published by Wiley Periodicals LLC on behalf of World Aquaculture
Society.

J World Aquac Soc. 2021;1–13. wileyonlinelibrary.com/journal/jwas 1

2

VALENZUELA-JIMENEZ ET AL.

L. setiferus juveniles reared in BFT at low salinity is relatively

weak because of their low growth and excessive oxygen con-
sumption and the oxidative damage (PO) produced.

KEYWORDS
antioxidant, biofloc, immunology, Litopenaeus setiferus, shrimp
activity

1 | I N T RO DU CT I O N

Many studies have been performed to increase the production of the North Atlantic white shrimp Litopenaeus
setiferus in the southern states (Browdy, Stokes, Hopkins, & Sandifer, 1991; Chapman, Browdy, Savin, Prior, &
Wenner, 2004; Gandy, 2007; Samocha et al., 1998; Sandifer, Hopkins, Stokes, & Browdy, 1993) and the Gulf of
Mexico (Rosas et al., 2004; Valenzuela, Sánchez, Rosas, Suárez, & Arevalo, 2002). L. setiferus is a native species of
the North Atlantic; it tolerates low salinity and is sustained under some extreme environmental conditions
(Laramore, Laramore, & Scarpa, 2001).
Currently, in the Yucatán Peninsula, infrastructure for aquaculture exists, but a lack of biotechnology with regard
to L. setiferus prevents its development. Furthermore, a reduction in the natural population of this species puts it at
risk from an ecological viewpoint not only for its capture but also for its conservation. Litopenaeus setiferus shows
good survival in seawater or in low salinity in clear water systems; however, the growth rate and feeding conversion
ratio (FCR) are low (Brito, Chimal, & Rosas, 2000). Moreover, advances in biofloc technology (BFT) have proven to
be a sustainable alternative for other native shrimp species, including Farfantepenaeus duorarum and F. brasiliensis
(Emerenciano et al., 2012; Magaña-Gallegos et al., 2018). Therefore, this rearing system may present an opportunity
to develop the rearing of L. setiferus with either high or low salinity. Shrimp juveniles of L. setiferus as euryhaline spe-
cies are adapted to different salinities in the environment.
At low salinities, shrimp juveniles hyperregulate to maintain internal homeostasis, and this has an energetic
cost that is provided by respiration (Ye et al., 2009). Especially in this condition, free radicals are produced and
some cellular defense mechanisms in crustaceans depend on their controlled production (during phagocytosis and
encapsulation) (Smith, Brown, & Hauton, 2003), which results from the activation of antioxidant enzymes to pro-
tect the organism against oxidative stress and prevent or repair oxidative damage (Duan, Wen, Shen, Shen, &
Chen, 2016). Antioxidant enzyme activity and immunological aspects (such as hemocytes) are parameters that
need to be evaluated to understand the effect of rearing in captivity on the health status of shrimp (Destoumieux,
Moñoz, Bulet, & Bachere, 2000; Johansson, Keyser, Sritunyalucksana, & Söderhall, 2000; Rodríguez & Le
Moullac, 2000).
Due to environmental variations (including salinity variations), aerobic metabolism of crustaceans generates
reactive oxygen species (ROS) at concentrations that prevent microbial infection. However, ROS and their residues
can result in severe damage to cells, as measured through lipid peroxidation (LPO) and oxidized protein (PO). To
maintain a balance, ROS are eliminated by a lipid-soluble antioxidant system (LSAS), including superoxide dismutase
(SOD), catalase (CAT), and glutathione-S-transferase (GST) (Contreras-Vergara, Valenzuela-Soto, García-Orozco,
Sotelo-Mundo, & Yepiz-Plascencia, 2004; Muñoz et al., 2000; Quiu, Wang, Wang, Liu, & Wang, 2011; Song
et al., 2015; Zhou et al., 2009).
The aim of this study was to evaluate the effect of salinity on the growth, survival, oxygen consumption, stress
oxidative system, and oxidative damage of juveniles of L. setiferus reared in the BFT system.


VALENZUELA-JIMENEZ ET AL. 3

2 | MATERIALS AND METHODS

n (UMDI), Facultad de
The experiment was carried out at Unidad Multidisciplinaria de Docencia e Investigacio

noma de México, Campus Sisal, located in the coastal region NE of Yucatan
Ciencias, Universidad Nacional Auto
State (21
90 55.22N, 90
10 54.93W) in Puerto de Abrigo, S/N in Sisal, Hunucma (Yucatan, Mexico).
Litopenaeus setiferus juveniles were reared at the UMDI hatchery. After an initial acclimation phase (from
postlarvae 10 days old to 0.98 g), the shrimp were separated into two groups: low and high salinity (5 and
35 practice salinity units (psu), respectively). The water used for the experimental phase was obtained from two dif-
ferent wells. The salinity was gradually increased or decreased until the required values were obtained (5 and
35 psu), and the water was filtered with a sand filter.
At the end of the acclimation phase, the juveniles (0.1 ± 0.3 g) were distributed into six fiberglass tanks (3,000
juveniles per tank; 20 m3 in diameter; 150 shrimp m3) and acclimated for 5 days. Three replicates were established
and monitored during the experiment (90 days). For biofloc stimulation in the experimental tanks, a volume of
1,000 L biofloc inoculum was used and filled at full capacity with filtered clear water. This inoculum came from a sta-
ble outdoor mother tank where equilibrium was reached. The water quality parameters of this water were as follows:
temperature, 28.2
C; pH, 7.8; dissolved oxygen >5 mg/L; NH3 concentration, 0.42 mg/L; nitrite concentration,
1.06 mg/L; and nitrate concentration, 23.1 mg/L. During the experimental period, molasses was added in a 6:1 (C:N)
proportion when the NH3 level increased above 1 mg/L.
The temperature (T
), dissolved oxygen (DO), and pH were measured daily at 08:00, 16:00, 20:00, 24:00, and
04:00 h with a multiparameter HACH™ (model Sension6-Hq40; Loveland, Colorado) that was calibrated for each salinity
value, which was measured daily with a self-compensating refractometer (Fisherbrand™, Fisher Scientific Company;
Ottawa, Canada). During the experimental phase, sugar cane molasses was added as a source of organic carbon (6g of
Carbon/ 1g of Nitrogen) (Avnimelech, 1999, 2007, 2015; Ebeling, Timmons, & Bisogni, 2006); sediments were removed
daily when flushing the water. Every 3 days, water samples were collected for ammonia (NH4), nitrite (NO2), and nitrate
(NO3) analyses, which were performed every week with a HACH™ colorimetric test kit (model NI-SA; Loveland, Colorado)
using the manufacturer's method for measuring diluted and full seawater (Rice, Baird, Eaton, & Clescen, 2012; Intergov-
ernmental Oceanographic Commission, 1983). For both biofloc treatments, the water lost by evaporation was replaced in
tanks at 2.0% with low salinity well water. Feed was given five times per day at 3% biomass; juveniles from each tank
were weighed weekly to adjust the amount of commercial feed (35% CP, Malta Clayton; Culiacan, Sinaloa, Mexico).

2.1 | Zootechnical performance

At the end of the experiment, all juveniles from both treatments were counted and weighed to estimate the survival
rate, final weight, final biomass, and food conversion factor (FCA) (Molina, Cadena, & Orellana, 2000). After the
experiment, 15 shrimp for each treatment (five replicates) were placed in water that was 5
C colder than the temper-
ature of the culture tank to reduce their metabolism (Pascual, Sánchez, Vargas-Albores, LeMoullac, & Rosas, 2003).
Then, these juveniles were dissected to obtain a portion of muscle tissue, which was collected and stored at 80
C
for further antioxidant and oxidative damage analysis. Muscle protein was tested (Bradford, 1976) using a microplate
assay with a dye reagent concentrate (Bio-Rad, Philadelphia, PA). Bovine serum albumin was used as a standard
(EMD Biosciences, Inc., La Jolla, CA), and the absorbance was read at 595 nm.

2.2 | Oxygen consumption of shrimp

For each treatment, nine juveniles were individually placed in acrylic 400-mL respirometric chambers filled with clear
water filtered by a 5-μm cartridge. This water was at the two salinities tested in the experiment (5 and 35 psu) and
4

VALENZUELA-JIMENEZ ET AL.

was connected to a recirculation system for each salinity. The chambers were sealed, taking care to avoid creating
air bubbles inside the chambers, which were the same size and volume. For each treatment, a chamber without
shrimp was used as a control. The oxygen consumption of juveniles was measured using a precision sensing digital
optical fiber oximeter with optical O2 sensors connected through an interface to a computer using OXY 10 Software
(Pre Sens™ OXY 10 Model 10-Channel, PreSens Precision Sensing GmbH, Regensburg, Germany).
The shrimp remained inside the respirometric chambers for 48 hr, and data from the first 24 hr were used to analyze
routine metabolism (RM). After the first 24 hr, a feed ration was provided for all chambers, including the control, and oxy-
gen consumption was measured. After the shrimp used for measurements were removed from the chamber, they were
sacrificed, dried, and weighed (live weight). The O2 consumption was determined for each chamber by the input minus
output value multiplied by the flow rate (mL hr1). Values were calculated by subtracting the consumption in the control
chamber, and data were calculated and expressed in mg O2 g 1 hr1 (Rosas et al., 2001) using the following formula:
VO2 ¼ ð½ðO2 e – O2 sÞ xFÞ
where:
VO2 = Oxygen consumption in mg O2 g/hr,
O2e = Oxygen concentration in mg/L obtained at the entrance of the chamber,
O2s = Oxygen concentration in mg/L obtained at the exit of the chamber,
F = Flux in L/hr.

2.3 | Antioxidant activity

The SOD activity was quantified with a commercial kit (Sigma-Aldrich, St. Louis, MO); one unit was defined as the amount
of enzyme required to inhibit xanthine activity by 50% in 20 min, and the absorbance was measured at 450 nm. The CAT
activity (Hadwan & Abed, 2016) was measured using a microplate assay. Samples were incubated in two 96-well plates
with 100 μL of phosphate buffer (pH 7.4) or 100 μL of the same buffer with H2O2; both microplates were incubated for
3 min, and the reaction was stopped by the addition of 100 μL of ammonium molybdate. The absorbance was measured
at 450 nm, and the amounts of both enzymes are expressed as U mg protein1. The GST activity was evaluated with a
microplate method using 190 μL of Na phosphate buffer; 200 mM reduced glutathione plus 1-chloro-2,4-dinitrobenzene
was added to a final concentration of 100 mM, and the absorbance was read at 412 nm after 5 min. The activity was cal-
culated using an extinction coefficient of E = 9.6 mM/cm; all the results are expressed in nmol mg1 protein min1.

2.4 | Oxidative damage

LPO was quantified (Fox, Blow, Brown, & Watson, 1994) using the PeroxiDetect© kit (Sigma-Aldrich, St. Louis, MO)
after extraction without centrifugation, homogenization with methanol 1:1 (v/v) and centrifugation at an RCF of
10,000g for 5 min at 27
C. Then, 10 μL of extract was placed in two 96-well plates, and 160 μL of working solution
was added. The samples were incubated for 60 min, and the absorbance was measured at 595 nm. A standard curve
was prepared using serial dilutions with 129 μL of 1 M tert-butyl hydroperoxide (TBOOH) plus 871 μL of methanol
(with the results expressed in nmol peroxide mL1).
Moreover, the PO level was evaluated (Mesquita et al., 2014) by adding 100 μL of dinitrophenylhydrazine
(DNPH) plus 2 N HCl combined with 100 μL of Tris buffer pH 7.4 (blank) or 100 μL of homogenized solution, without
centrifugation, to Eppendorf© tubes, which were incubated for 10 min. Then, 50 μL of 6 M NaOH was added to the
samples and blank. All tubes were centrifuged at an RCF of 10,000g for 5 min at 27
C. Finally, 150 μL of each sample
and the blank were added to a 96-well plate, and the absorbance was read at 450 nm. The results are expressed in
nmol mg protein1.


VALENZUELA-JIMENEZ ET AL. 5

2.5 | Statistical analysis

A Student t-test was performed to detect significant differences among treatments on survival percentages previously
transformed to arsine. For final wet weight and wet weight gain, the treatments effects were evaluated using a distribu-
tion t-test based on permutations (999), due to no normality of the data was observed (Eude, Kerr, & Trumbo, 2010).
When analyzing the antioxidant activity of each enzyme, the oxidative damage indicators, and the oxygen con-
sumption of L. setiferus juveniles, the treatment effects were evaluated using a distribution-free t-test based on per-
mutations (999) (Quinn and Keough, 2002). Principal component analysis (PCA) was performed to identify the
contribution of the activity to the underlying group differences between the low and high salinity conditions. Other-
wise, centroid clustering (UPGMC: underweighted centroid clustering) was performed to visualize the grouping for
each treatment (hsBFT and lsBFT). All statistical analyses were performed with R Statistical Software (R Core
Team, 2018).

3 | RESULTS

All physicochemical parameters of the water remained within the recommended levels for the penaeid shrimp cul-
ture throughout the 90 days of the experiment, except for the nitrogen compounds (Table 1, Figure 1). For the lsBFT
treatment, NH4 high values were observed in 4 weeks, and NO2 in 6 weeks respectively. This tendency was similar
for the hsBFT treatment only for NO2 (Figure 1).
The results related to the zootechnical performance of L. setiferus juveniles indicated that the FW (2.47
± 0.88 g), wet weight gain (25.9 ± 3 mg/day), final biomass (5,244 ± 21 g), and FCA (2.22 ± 0.24) were higher for the
hsBFT group than for the lsBFT group (p < .05) (Table 2), whereas the survival rate (lsBFT: 67.0 ± 7.81%; hsBFT:
76.0 ± 6.0%) did not show significant differences between treatments (p > .05) (Table 2).

3.1 | Oxygen consumption of shrimp

Regarding the oxygen consumption of juvenile L. setiferus measured at the end of the experiment, the permutation
test showed significant differences in fasting juveniles (p < .05). Additionally, significantly higher postprandial oxygen

T A B L E 1 Physicochemical parameters recorded in water after the experiment (90 days) for L. setiferus postlarvae
reared in a BFT system with low salinity (lsBFT) or high salinity (hsBFT) (mean ± SD)

Physicochemical parameter lsBFT hsBFT

Dissolved oxygen (mg/L) 7.61 ± 1.20 5.33 ± 0.98
Temperature (
C) 27.49 ± 2.95 28.02 ± 0.58
pH 8.50 ± 1.15 8.03 ± 0.69
Salinity (psu) 5.25 ± 1.8 35.73 ± 1.01
Ammonia (mg/L) 0.11 ± 0.18 0.29 ± 0.67
VC = 1.63 VC = 2.3
Nitrite (mg/L) 1.47 ± 1.34 1.37 ± 1.85
VC = 0.91 VC = 1.35
Nitrate (mg/L) 87.34 ± 10.1 92.31 ± 9.23
VC = 0.1 VC = 0.09
Total suspended solids (TSS) 7.25 ± 3.61 6.6 ± 4.5
Turbidity 37.71 ± 16.06 34.18 ± 17.58

Abbreviation: VC, variation coefficient.

6

VALENZUELA-JIMENEZ ET AL.

F I G U R E 1 Values of NH4 (a) and NO2 (b) during the 90 days of the experiment for L. setiferus postlarvae reared
in a BFT system with low salinity (lsBFT; dashed line) or high salinity (hsBFT; solid line)

T A B L E 2 Zootechnical performance after 90 days for L. setiferus postlarvae reared in a BFT system with low
salinity (lsBFT) or high salinity (hsBFT)

Zootechnical performance lsBFT hsBFT

Initial weight (IW) (g) 0.1 ± 0.3 0.1 ± 0.3
Final weight (FW) (g) 1.83 ± 0.47b 2.47 ± 0.88a
Wet weight gain (mg/day) 15.4 ± 3b 25.9 ± 3.1a
a
Survival rate (%) 67.0 ± 7.81 76.0 ± 6.0a
Final biomass (g) 3,843 ± 29b 5,244 ± 21a
b
FCA 3.48 ± 0.25 2.22 ± 0.24a
Hepatosomatic index (HI) 0.06 ± 0.0a 0.13 ± 0.01b

Note: Different letters indicate significant differences (p < .05) (mean ± SD).

consumption was observed for juveniles previously reared in lsBFT than for those in the hsBFT group (p < .05,
Figure 2).

3.2 | Antioxidant activity and oxidative damage

In this study, enzymes with antioxidant activity (CAT, SOD, and GST) were measured for the lsBFT and hsBFT
treatments, resulting in similar values for both groups (p > .05) (Table 3). Regarding oxidative damage, a statisti-
cally significant difference in PO was detected (PERMANOVA, pseudo-F = 4.42, p < .05). The differences are
shown in Table 3 and Figure 3b (PCA, plot of PC1 vs. PC2, 65.2% of the total variance). The most important anti-
oxidant enzyme activity that explained the variability for the first component of L. setiferus juveniles was that of
GST, followed by CAT and SOD enzyme activity, whereas PO and LPO (as oxidative damage measures) explained
the variability for the second component for the same penaeid shrimp under the same rearing conditions (lsBFT
and hsBFT) (Figure 3b).


VALENZUELA-JIMENEZ ET AL. 7

F I G U R E 2 Variations in O2 consumption (mg O2 g1 hr1) for fasting (a) and postprandial (b) L. setiferus juveniles
reared in a BFT system with low salinity (lsBFT) or high salinity (hsBFT)

4 | DISCUSSION

In this study, the growth rates obtained for both treatments (15.4 ± 3.1 mg/day for lsBFT and 25.9 ± 3 mg/day for
hsBFT) were low but higher than the values reported in a previous study realized in clear water (mean value of
8

VALENZUELA-JIMENEZ ET AL.

T A B L E 3 Values obtained for antioxidant enzymes (SOD, CAT, and GST) and the oxidative damage (LOP and PO)
from muscle tissue of L. setiferus juveniles (15 shrimp per treatment, five replicates) reared in a BFT system with low
salinity (lsBFT) or high salinity (hsBFT) (mean ± SE)

Variable lsBFT hsBFT Permutation (p-value)

1
CAT (U mg prot) 0.27 ± 0.04 0.32 ± 0.07 .50
1
SOD (U mg prot) 57.7 ± 5.1 46.9 ± 5 .13
GST (nmol min mg1 prot) 0.059 ± 0.008 0.049 ± 0.009 .37
LPO (nmol peroxide mg1 tissue) 0.7 ± 0.2 0.9 ± 0.1 .32
PO (nmol mg1 tissue) 0.2 ± 0.03a 0.2 ± 0.01b .04

Note: Different letters in the superscript indicate significant differences in the permutation test.
Abbreviations: CAT, catalase; GST, glutathione-S-transferase; LPO, lipid peroxidation; PO, oxidized protein; SOD,
superoxide dismutase.

2 mg/day, Taboada et al., 1998) with other non-domesticated species, such as F. paulensis (0.62 g in 28 days, Froés,
Abe, Wasielesky Jr, Prentice, & Cavalli, 2006); (0.61 g in 45 days, Ballester et al., 2010), Litopenaeus schmitti (3 g in
120 days, Henriques, Alves, Barreto, & M.R. de Souza M.R., 2014), and F. duorarum (20 mg/ week) (Gullian,
Aramburu, Sanders, & Lope, 2010). The values for zootechnical performance recorded for L. setiferus in the hsBFT
treatment were higher than those reported by Perez-Velazquez, González-Félix, Davis, Roy, and Zhu (2013). These
authors pointed out a decrease in the growth rate of L. setiferus when it reaches 5 g, although older juveniles larger
than 5 g grew at a higher rate.
The low FCA obtained for the hsBFT treatment suggests that the feed consumption of L. setiferus juveniles was
more efficient in seawater, whereas the low weight gain for juveniles reared in freshwater (lsBFT) resulted in a
greater amount of feed being used during the experimental phase, which would result in economic losses due to
feeding. The low survival rate obtained for the lsBFT treatment was likely a consequence of the immature biofloc
inoculated in the experimental tanks, which may have had a greater toxicity due to the presence of nitrites (Alcaraz,
Espinoza, Vanegas, & Chiappa Carrara, 2007) resulting from an ionic imbalance, because shrimp tend to lose Cl1
ions and absorb NO2, to maintain the homeostasis, as both ions have the same gill receptor, resulting in functional
anemia (Soares de Moura, Walielesky, De la Paz Sera, Braga, & Poersch, 2021). Regarding the concept of a safe level
of nitrites, several studies (Frias-Espiricueta et al., 2000; Lin & Chen, 2001; Li et al., 2007; Furtado et al., 2016) have
provided further discussion on this matter to explain the lower survival and growth rates based on such toxicity if
the levels are close to the LC50. In this study, the zootechnical conditions require focusing more on nutrition
(an appropriate diet for this species) for ion balance (Frías-Espericueta, Harfush-Melendez, & Páez-Osuna, 2000) and
breeding status. Such aspects are related to the benefit of biofloc bacteria in the control of water quality, probiotic
quality, abundance and diversity of microorganisms as well as adequate conditions for breeders to maturate.
McMahon (1988) examined the regulation of ventilation and cardiac mechanisms to maintain the O2 supply of
tissues. L. setiferus juveniles change energy substrates in response to DO and salinity levels, which may be a possible
strategy to allow organisms to derive energy from protein (Rosas, Ocampo, Gaxiola, Sánchez, & Soto, 1999).
The oxygen consumption level, including the postprandial oxygen consumption, of the juveniles subjected to the
lsBFT treatment was high. Shrimp subjected to the hsBFT treatment were under better conditions from the begin-
ning of the trial until postprandial oxygen consumption. These results can explain the excess ROS, which could not
be controlled by the oxidative enzymatic system, and the production of the highest PO and LPO values (Thabet,
Ayadi, Koken, & Leignel, 2017).
Shrimp have a permanently stimulated immune condition that limits oxidative stress, which probably leads to
decreased cell damage and improved physiological performance during rearing. After PCA analyses, the GST activity
revealed a high level of detoxification in the hsBFT group, which was followed by the CAT and SOD activity, which also
decreased the cell damage reported for the hsBFT treatment. The important activity of these enzymes suggests immune
stimulation and continuous antioxidant and antimicrobial activity during stress (Bachére et al., 1995; Xu & Pan, 2013).


VALENZUELA-JIMENEZ ET AL. 9

F I G U R E 3 Principal component analysis (PCA) of the antioxidant enzyme activity (CAT, SOD, and GST) and oxidative
damage (LPO and PO) for L. setiferus postlarvae at low salinity (lsBFT) and high salinity (hsBFT). (a) Percentage of the
variance explained by each component for both treatments (lsBFT and hsBFT). (b) Principal components 1 and 2 of the
antioxidant enzyme activity and oxidative damage in muscle tissue of L. setiferus postlarvae

However, the high PO values recorded for the lsBFT group suggest increased cell damage, as reflected by mem-
brane oxidation (Kwiecien et al., 2014). Oxidative stress can directly damage proteins or modify amino acids to pro-
mote protein carbonyl formation (Fedorova, Bollineni, & Hoffmann, 2014). LPO can promote the attack of any
species capable of removing H+ from PUFAs in membranes and leads to the formation of peroxyl radicals; the pro-
cess attacks fatty acids and propagates peroxidation. The final result of this cellular damage is membrane destabiliza-
tion (Halliwell & Gutteridge, 1984).

5 | C O N CL U S I O N

The data presented here suggest that the biofloc system can stabilize and improve conditions for L. setiferus, a pen-
aeid species with a high potential for farming, under high salinity condition. During the experimental phase, oxidative
10

VALENZUELA-JIMENEZ ET AL.

stress was stimulated, which increased cell damage at low salinity due to the high oxygen consumption under fasting
and postprandial conditions. Additionally, in the lsBFT group, exposure to high levels of ammonium and nitrite cau-
sed high mortality and low growth.

ACKNOWLEDGMENTS
The authors thank the financial support of the government of Brazil through the Program of Students in Agreement
for Post-Graduation (PEC-PG) and the Coordination for the Improvement of Higher-Level Personnel (Brasil-CAPES)
Finance Code 001 and the Project DGAPA-UNAM No. 221316. We would like to thank M. in A. Miguel Arevalo, Ing
Adriana Paredes, Tech. Patricia Balan and M Sc. Gabriela Palomino for technical support.

ORCID
Wilson Wasielesky https://orcid.org/0000-0002-7267-4755
Gabriela Gaxiola https://orcid.org/0000-0001-6260-9653

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How to cite this article: Valenzuela-Jiménez, M., Durruty-Lagunes, C., Cuzon, G., Pacheco, E., Arévalo, M.,
Aguilera-Rivera, D., Wasielesky, W., Rodríguez-Fuentes, G., Barreto, A., & Gaxiola, G. (2021). Effect of water
salinity on the oxidative system of juveniles of the North Atlantic white shrimp Litopenaeus setiferus reared in
biofloc technology. Journal of the World Aquaculture Society, 1–13. https://doi.org/10.1111/jwas.12845