Effect of Different Total Suspended Solids Levels On A Litopenaeus Vannamei (Boone, 1931) BFT Culture System During Biofloc Formation
Effect of Different Total Suspended Solids Levels On A Litopenaeus Vannamei (Boone, 1931) BFT Culture System During Biofloc Formation
Effect of Different Total Suspended Solids Levels On A Litopenaeus Vannamei (Boone, 1931) BFT Culture System During Biofloc Formation
12949
Carlos Augusto Prata Gaona1, Marcos Souza de Almeida1, Veronica Viau2, Luis Henrique
Poersch1 & Wilson Wasielesky Jr1
1
Marine Station of Aquaculture, Institute of Oceanography, Federal University of Rio Grande, Rio Grande (RS), Brazil
2
Biology of Reproduction and Growth in Crustaceans, Department of Biodiversity and Experimental Biology, FCEyN,
University of Buenos Aires, Ciudad Universitaria, Buenos Aires, Argentina
Correspondence: C A P Gaona, Marine Station of Aquaculture, Institute of Oceanography, Federal University of Rio Grande,
C.P. 474, Rio Grande (RS), CEP 96201-900, Brazil. E-mail: carlosgaona@ig.com.br
Crab, Defoirdt, Boon & Verstraete 2008). This mix- As the density of suspended solids increases, a
ing becomes more important in impermeable culture’s success will depend on a balance between
structures where there is minimal or no water cul- waste production and the capacity of the environ-
ture renewal, providing access to the solids and ment of the cultured species to assimilate nutri-
organic matter accumulated from offered food and ents. One of the strategies for formation of biofloc
the natural productivity in the suspended aggre- is to stimulate heterotrophic bacteria growth and
gates (Ray, Lewis, Browdy & Leffler 2010; Gaona, metabolism by adding organic carbon (C) sources,
Poersch, Krummenauer, Foes & Wasielesky 2011; balancing this substrate with the total ammonia
Schveitzer, Arantes, Cost
odio, Santo, Vinatea, Seif- nitrogen (N) through the C:N ratio (Avnimelech
fert & Andreatta 2013). The natural biota main- 1999; Ebeling et al. 2006). Nitrifying bacteria
tained in suspension acts in the recycling of require an inorganic carbon substrate for nitrite
nitrogen compounds (ammonia and nitrite) and assimilation to reduce the concentrations of this
supplements the feeding of penaeid shrimp (Wasie- compound (Ebeling et al. 2006). Due to concerns
lesky, Atwood, Stokes & Browdy 2006; Arnold, about the establishment of ammonium-oxidizing
Coman, Jackson & Groves 2009; Ballester, Abreu, and nitrite-oxidizing bacteria in cultures, some
Cavalli, Emerenciano, Abreu & Wasielesky 2010; studies have focused on the analysis of suspended
Megahed 2010). solids concentrations and zootechnical perfor-
Simultaneously, there is an increase in nutrient mance using biofloc inoculum from previous crops
concentrations, which can result in rapid eutroph- (Gaona et al. 2011; Ray, Dillon & Lotz 2011;
ication in closed systems (Thakur & Lin 2003). Schveitzer et al. 2013).
Silva, Wasielesky and Abreu (2013) analysed the Apart from the nutritional benefits of bioflocs
nitrogen and phosphorus dynamics in BFT systems and their ability to maintain water quality, moni-
and found that 39% of the nitrogen input into the toring of biofloc formation must be conducted
system is in dissolved form and 7.7% of that through a specific analysis of the progression of
fraction is in inorganic form. Of the phosphorus the concentration of suspended solids and water
that remained in the system, 34.1% was in dis- quality parameters. However, none study started
solved form, with 50.7% of that portion being with different concentration of total suspended
inorganic. However, the bacterial community in solids on biofloc system without inoculum. In this
the water culture assimilates and converts inor- sense, the objective of this study was to analyse
ganic nitrogen species, improving water quality during biofloc formation, the effect of different
(Avnimelech 2009; De Schryver & Verstraete suspended solids levels on water quality and
2009; Luo, Avnimelech, Pan & Tan 2013). the growth performance of the penaeid shrimp
The capacity of an intensive biofiltration system Litopenaeus vannamei in a BFT system.
is dependent on a continuous oxygen supply (Har-
greaves 2006). Nitrifying bacteria, which maintain
Materials and methods
water quality by reducing nitrite concentrations,
depend on an environment with high dissolved
Location and period of the study
oxygen (Ebeling, Timmons & Bisogni 2006; Avn-
imelech 2009). Organic carbon is the energetic The study was conducted at the Marine Station of
substrate for many microorganisms, and its con- Aquaculture (EMA), Institute of Oceanography,
sumption contributes to the use of dissolved oxy- Federal University of Rio Grande, located at Cas-
gen, posing a risk of inadequate oxygen supply for sino Beach in Rio Grande, RS, Southern Brazil
the animals reared in the system if facilities are (32°110 S; 52°100 W). A 42-day trial was con-
inadequate (Avnimelech 2009; Mook, Chakrabarti, ducted from December 2010 to January 2011.
Aroua, Khan, Ali, Islam & Abu Hassan 2012). In
addition, the interactions between the biofloc and
Experimental design
water quality may interfere with the stability of
the system, potentially causing changes in pH, The experimental design was completely random-
alkalinity and carbon dioxide concentration (Ebel- ized, consisting of three treatments with three repli-
ing et al. 2006; Furtado, Poersch & Wasielesky cates each. Nine tanks (1.0 m3) with a useful
2011; Furtado, Gaona, Poersch & Wasielesky capacity of 0.86 m3 were installed in a greenhouse
2014). for shrimp growth via a BFT system. The aeration
system consisted of an Aero-TubeTM (a hose with value was adjusted posteriorly according to the
micropores distributed evenly across its length) to consumption observed in the trays within each
optimize oxygen transfer and aeration efficiency. interval between feedings.
Forty-centimetre lengths of this hose were cut and
installed in pairs in each experimental unit, cou-
Physical and chemical water parameters
pled to a PVC pipe (20 mm diameter) and supplied
by mechanical aeration from a 2 hp blower. Monitoring of dissolved oxygen, pH, temperature
Three treatments were defined by ranges of TSS: and salinity was performed daily. Samples were
100–300 mg L1 as low (TL), 300–600 as med- collected daily for total ammonia nitrogen (TAN)
ium (TM) and 600–1000 as high (TH). The water and nitrite (NO2–N) analysis and once a week
used in the experiment was obtained by pumping for nitrate (NO3–N), orthophosphate (PO4–P)
directly from Cassino Beach, which has a salinity and alkalinity. Total suspended solids (TSS) and
of 33 g L1. Before the beginning of the experi- settleable solids (SS) were monitored twice a
ment, the water was treated with 10 mg L1 of week. Dissolved oxygen, pH, temperature and
chlorine and neutralized with ascorbic acid 24 h salinity were measured using multiparameter
later and then fertilized with sugar cane molasses YSIâ mod. 556 (YSI Incorporated, Yellow Springs,
in a 20:1 ratio (C:N) to achieve the initial sus- OH, USA). The concentrations of ammonia (TAN)
pended solids concentrations: 100, 200 and and nitrite (NO2–N) were measured according to
500 mg L1. A first adjustment was made to the UNESCO (1983) and Bendschneider and Robinson
total suspended solids concentrations before (1952) respectively. The method used for nitrate
the start of the experiment. Further adjustments to (NO3–N) and orthophosphate (PO4–P) was Ami-
the suspended solids levels were made (third and not and Chaussepied (1983), and alkalinity was
fifth week) by suspended solids removal (6 h each measured according to APHA (1998). The TSS
removing) in all treatments, based on sedimenta- was determined through gravimetry by filtering
tion methods (clarification) used in previous studies aliquots of 20 mL of water through GF 50-A
(Ray et al. 2010, 2011; Gaona et al. 2011). Clari- glass fibre filters, according to Strickland and Par-
fiers were assembled into a conical-cylindrical glass sons (1972) and AOAC (2000). Settleable solids
fibre chamber with a diameter of 0.48 m, height of was analysed using Imhoff cone and the volume
0.50 m and useful volume of 48 L, representing of floc on the bottom of the cone was measured
5.5% of the total volume of the experimental unit. after 15 minutes of sedimentation (Avnimelech
A PVC pipe (100 mm diameter) was placed inside 2009).
this chamber to reduce the turbulence of the water
pumped from the culture tank by a submerged
Growth performance
pump with a flow of 1500 L h1.
Shrimp growth was monitored every 15 days, and
used to adjust the amount of supplied feed accord-
Biological material and feeding
ing to Jory, Cabreras, Durwood, Fegan, Lee, Lawr-
The juveniles of L. vannamei used in this study ence, Jackson, Mcintosh and Casta~ neda (2001).
were first kept for 60 days in the nursery and For that purpose, 30 shrimps were collected ran-
grow-out BFT system inside the greenhouse at the domly from each experimental unit, individually
Marine Station of Aquaculture (EMA). Each experi- weighed and returned to their respective tank.
mental unit was stocked at a density of 372 After weighing, the mean individual weight (g)
shrimp m3 (265 individuals m2) with an aver- was calculated.
age weight per shrimp of 4.54 1.19 g. Shrimp At the end of the experiment the following vari-
were fed twice a day (at 9:00 and 16:00 hours) ables were calculated:
with commercial feed (Potimar Active 38; Centro
Survival ð%Þ ¼ ðfinal shrimp number/
Oeste Racßo~es SA, Campinas, Brazil) containing
38% crude protein and 8% lipid. The food was initial shrimp numberÞ 100:
offered on feeding trays (Wasielesky, Atwood, Feed conversion ratio (FCR)
Stokes et al. 2006) at an initial rate of 10% of ¼ offered feed (g)/(final biomass (g)
shrimp biomass and was adjusted according to initial biomass (g));
consumption observed in a period of 24 h. This
Productivity ðkg m3 Þ ¼ ðfinal biomass treatments throughout the study, whereas the TM
group exhibited intermediate values (Fig. 1a).
initial biomassÞ=volume ðm Þ 3
However, after 6 weeks of the experiment, the TSS
concentrations did not present a significant differ-
Statistical analysis
ence (P > 0.05) between the TM and TL treat-
The water quality parameters and growth perfor- ments (Fig. 1a).
mances in the different treatments were submitted From de second week onward, the settleable
to a one-way analysis of variance (ANOVA), taking solids (SS) presented significant differences
into account the assumptions (Levene and Kol- (P < 0.05) among all treatments (Fig. 1b).
mogorov–Smirnov tests) necessary for its imple- The pH was significantly higher (P < 0.05) in
mentation. Tukey’s test was applied when TL compared to TH tanks from the third week
significant differences were detected (P < 0.05). onward (Fig. 1c).
The survival data were transformed (arcsine x0.5) The variations in alkalinity observed in the
before analysis (Zar 1996). study (Fig. 1d) were marked by significant differ-
ences (P < 0.05) between treatments in the last
2 weeks, when the concentrations were signifi-
Results
cantly higher (P < 0.05) in TL with respect to TH.
Ammonia and nitrate concentrations were not dif-
Water quality
ferences (P > 0.05) between treatments during the
Temperature and dissolved oxygen were main- experiment. However, the nitrite concentration
tained above 26°C and 5 mg L1, respectively, increased throughout the experiment for the TM and
throughout the experiment and did not exhibit sig- TH treatments while it remained low for the TL group
nificant differences (P > 0.05) between treatments. (Fig. 1e). Concentrations were significantly lower
Salinity increased at the end of the study; how- (P < 0.05) in the low TSS treatment (TL) relative to
ever, the mean salinity values were similar the other two groups during the final 2 weeks.
(P > 0.05) between groups. The highest orthophosphate concentration was
Means and standard deviations of the parame- recorded for the TH treatment during the last
ters monitored throughout the experiment are pre- week, being significantly different (P < 0.05) from
sented in Table 1. the TL group.
The concentrations of total suspended solids
(TSS) outside of setting ranges of the treatments
Growth performance
were recorded during the culture. Significant dif-
ferences (P < 0.05) in total suspended solids con- Shrimp kept at low (TL) and medium (TM) TSS
centrations were found between the TL and TH concentrations exhibited similar (P > 0.05) growth
Table 1 Physical and chemical parameters data for L. vannamei in a BFT system with three suspended solids levels
(low = TL, medium = TM, and high = TH), with mean values standard deviation
Treatment
TL TM TH
Different letters in the same row indicate significant difference (P < 0.05) between treatments.
(a)
(b)
(c)
(d)
Discussion
treatments, which, respectively, varied below and nitrite and nitrate prevalence at the end of the
above 500 mg L1, a value recommended by crop cycle.
Samocha et al. (2007). Suspended solids are Phosphorus concentrations remained at concen-
involved in the organic matter decomposition pro- trations that accompanying TSS levels, remaining
cesses and reflect changes in water quality (Vina- accumulated in the water culture. Barak, Cytryn,
tea, Galvez, Browdy, Stokes, Venero, Haveman, Gelfand, Krom and Van Rijn (2003) reported that
Lewis, Lawson, Shuler & Leffler 2010). Changes in the source of phosphorus in the culture is mainly
pH and alkalinity during the study correlated due to unconsumed feed and nutrients excreted by
inversely with TSS levels; a similar pattern was cultured organisms. In cultures with biofloc tech-
noted by Furtado et al. (2011) for TSS levels above nology, L. vannamei can incorporate up to 35% of
850 mg L1. The respiration in the water column the total phosphorus that enters the system,
by microorganisms present in the biofloc results in whereas the majority remains in the dissolved and
the excretion of carbon dioxide, which drives a particulate forms, with accumulation expected in a
reduction in pH (Wasielesky, Atwood, Stokes et al. BFT system (Silva et al. 2013).
2006; Vinatea et al. 2010; Ray, Seaborn et al. The shrimp’s performance was determined by
2010). Simultaneously, the dissociation of carbon- the water quality during the experiment. The
ate and bicarbonate ions reduces the alkalinity of lower total suspended solids concentration (at
the water culture (Ebeling et al. 2006). The alka- range of 100–300 mg L1) used in the study pro-
linity and pH remained above 100 mg CaCO3 L1 vided the best conditions for the shrimp, most
and 7, respectively, and within the recommended likely due to the low levels of nitrites maintained
values for L. vannamei in a BFT system (Ebeling throughout the 42-day trial. Lin and Chen (2003)
et al. 2006; Wasielesky, Atwood, Kegl, Bruce, verified a nitrite (NO2–N) safe level of
Stokes & Browdy 2006). 25.7 mg L1 for L. vannamei juveniles at a salinity
Nitrogen cycling by heterotrophic and nitrifying of 35 g L1 indicating the high tolerance of the
bacteria resulted, respectively, in similar reductions species, as the concentration indicated by these
in ammonia concentrations and increases in authors was only achieved in the sixth week for
nitrite with increasing organic matter at the the TM treatment in higher salinity. The TH treat-
higher TSS levels. Due to the addition of molasses, ment exceeded this concentration from the fifth
heterotrophic bacteria had a substrate for obtain- week, exposing the animals for longer toxicity of
ing carbon and subsequently metabolizing ammo- nitrite. At low salinity to 48 h LC50 (median lethal
nia (Avnimelech 1999; Samocha et al. 2007), concentration) studies, Schuler, Boardman, Kuhn
reducing the ammonia concentrations to levels tol- and Flick (2010) in salinity of 10 g L1 observed
erable to L. vannamei (Lin & Chen 2001). Luo et al. 154 mg L1 NO2–N, while Lin and Chen (2003)
(2013) observed that the effect of the organic sub- at 15 g L1 recorded 143 mg L1 NO2–N. How-
strate in the inhibition of nitrifying bacteria was ever, the nitrite concentration was determinant for
not toxic, but stimulated rapid heterotrophic the growth rate of the animals, and the two vari-
growth and competition for dissolved oxygen, ables may have an inverse relationship (Vinatea
space, total ammonia and micronutrients. Inhibi- et al. 2010). These interactions were reflected in
tion of nitrifying bacteria may have led to slowed the better growth and survival in treatment TL,
growth, and the reduction in alkalinity in the TH which was observed to have the lowest nitrite con-
treatment may have limited the availability of centration. In an L. vannamei culture with a TSS
inorganic carbon (Ebeling et al. 2006). In the pre- concentration of 465 mg L1, Ray, Lewis et al.
sent study, there were increased concentrations of (2010) recorded a maximum nitrite concentration
nitrite in treatments TM and TH, in which the oxi- of 5.4 mg L1, obtaining a final mean weight of
dation necessary to decrease and stack nitrate did 11.6 g and mean survival of 71% at a stocking
not occur. Nitrite concentrations in the TL treat- density of 460 shrimp m3 after 12 weeks. Gaona
ment also increased, but it was a very gentle rise. et al. (2011) observed, after 16 weeks of culture,
It was clear that the length of the experiment was that shrimp stocked at a density of 250 individuals
most likely not sufficient for the establishment of m2 reached 10.76 g with a survival of 81%,
characteristic nitrification in BFT systems. Accord- maintaining the TSS level at 500 mg L1. Schveit-
ing to Silva et al. (2013), the route of nitrification zer et al. (2013) observed 83% survival in L. van-
occurs with successive conversions of ammonia to namei reared under suspended solids conditions
kept within the range of 400–600 mg L1. Con- W. Wasielesky, and L.H. Poersch are research fel-
comitantly, there was a better conversion of feed lows of CNPq.
consumed to shrimp growth in the present study.
The best FCR was observed in the treatment with
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