Aquaculture and Fisheries 4 (2019) 214–218

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Aquaculture and Fisheries

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aquaculture-and-fisheries

Tilapia processing waste silage (TPWS): An alternative ingredient for

Litopenaeus vannamei (Boone, 1931) diets in biofloc and clear-water systems
Joaquim da Rocha Soares Netoa, Felipe de Azevedo Silva Ribeiroa, Alex Augusto Gonçalvesb,
Maurício Gustavo Coelho Emerencianoc,∗
a
Universidade Federal Rural do Semi-Árido (UFERSA), Departamento de Ciência Animal, Setor de Aquicultura, Mossoró, 59625-900, Brazil
b
UFERSA, Departamento de Ciência Animal, Laboratório de Tecnologia e Controle de Qualidade do Pescado, Mossoró, 59625-900, Brazil
c
Universidade do Estado de Santa Catarina (UDESC), Laboratório de Aquicultura (LAQ), 88790-000, Laguna, SC, Brazil and Programa de Pós-Graduação em Zootecnia
(PPGZOO/UDESC), Chapecó, 89815-630, Brazil

A R T I C LE I N FO A B S T R A C T

Keywords: The aim of this study was to evaluate the growth performance of Litopenaeus vannamei juveniles reared under
Silage biofloc and clear-water conditions fed with different inclusion levels of tilapia processing waste silage (TPWS)
Nutrition based-diets. The experiment was performed in two individual systems: biofloc (BS) and clear-water systems
Waste (CWS). The trial used forty 40 L rectangular plastic bins (twenty per system) in a density of 63 shrimp/m2. The
BFT
juveniles were distributed in a factorial completely randomized experimental design. The treatments were based
Pacific white shrimp
on the percentage of silage inclusion (control or 0, 1.5%, 3.0%, 4.5% and 6.0% of inclusion) in BS or CWS,
totalizing ten treatments and four replicates. Survival was above 80% in all treatments and was not affected by
both systems and diet. Shrimp final weight and SGR were statistically influenced by system (P < 0.05) but not
by the diet; and presented high values in BS. The inclusion of TPWS in L. vannamei diets did not affect shrimp
performance. In addition, shrimp raised in BS demonstrated better growth performance as compared to CWS.

1. Introduction
In recent years, studies approaching the production of Pacific white
shrimp Litopenaeus vannamei in biofloc system desired great attention
(Avnimelech, 2015; Lobato, Ribeiro, Miranda-Baeza, & Emerenciano,
2019). The recent diseases outbreaks and low productivity lead the
scientists to search for alternative systems to improve efficiently the
shrimp growth and meet the market demand (Emerenciano, Ballester,
Cavalli, & Wasielesky, 2012a; Vargas-Albores et al., 2019).
Biofloc system, also called as biofloc technology (BFT), has the
advantage to allow the production of a great amount of shrimp per area
or volume with limited or no water exchange. Such technology provides
better biosecurity for the production, especially if the farm is located
close to areas with high concentration of aquaculturists using the same
water source. BFT has gained popularity because it offers a practical
solution to maintaining water quality and recycle feed nutrients si-
multaneously (Xu & Pan, 2012). Another advantage of the biofloc
system is the possibility to use alternatives low protein diets and con-
sequently, decrease the production costs (Ballester et al., 2010; Scopel
et al., 2011; Xu & Pan, 2014); mainly due to the continuous availability
of natural food source in a form of live microorganisms (Azim & Little,
2008; Decamp, Conquest, Forster, & Tacon, 2002; Ray et al., 2010).
Fishmeal is an unsustainable and one of the most expensive in-
gredient used in aquaculture diets (Naylor et al., 2009). Therefore, the
replacement or reduction of fishmeal presents a great interest for the
aquaculture industry. On the other hand, problems related to the fish-
meal replacement by alternative ingredients have been identifying in-
cluding deficiency of some essential amino acids, the presence of anti-
nutritional factors, palatability and digestibility (Forster, Dominy,
Obaldo, & Tacon, 2003; Naylor et al., 2009). Although problems exist,
many cases of success have been reported in L. vannamei diets (Amaya,
Davis, & Rouse, 2007; Bauer, Prentice-Hernandez, Tesser, Wasielesky,
& Poersch, 2012; Cruz-Suárez et al., 2007; Davis & Arnold, 2000;
Forster et al., 2003; Hernández, Olvera-Novoa, Aguilar-Vejar, González-
Rodríguez, & Parra, 2008; Samocha, Davis, Saoud, & DeBault, 2004;
Suarez et al., 2009), including fishmeal replacement by plant protein
sources (Moreno-Arias et al., 2018) also supported by relevant mineral
supplementation (Huang, Wang, Zhang, & Song, 2017).
Fish silage can be produced using fisheries and aquaculture pro-
cessing residues. Fish silage is an alternative protein source to the
fishmeal (Vidotti, Viegas, & Carneiro, 2003) and posses a simpler and
cheaper production method (Gallardo et al., 2012). Furthermore, the

∗
Corresponding author. CSIRO Agriculture and Food, Aquaculture Program, Bribie Island Research Centre, 4507, Bribie Island, QLD, Australia.
E-mail address: mauricioemerenciano@hotmail.com (M.G. Coelho Emerenciano).

https://doi.org/10.1016/j.aaf.2019.04.005
Received 23 December 2018; Received in revised form 28 April 2019; Accepted 29 April 2019
Available online 17 May 2019
2468-550X/ © 2019 Shanghai Ocean University. Published by Elsevier B.V. This is an open access article under the CC BY license
(http://creativecommons.org/licenses/BY/4.0/).
J. da Rocha Soares Neto, et al.
use of fish silage as a substitute for protein ingredients in aquafeeds
emerges as an alternative to solve environmental and sanitary problems
caused by the lack of use and/or inadequate disposition of fish residues.
Besides, it is also a way of decreasing the feeding costs, and, conse-
quently, the production costs since feeding corresponds around of 60%
of the overall expenses (Arruda, Borghesi, & Oetterer, 2007).
On this context, tilapia is a worldwide relevant species for aqua-
culture industry and has demonstrated positive results as a fish silage
incorporated into diets (Carvalho, Pires, Veloso, Silva, & Carvalho,
2006; Fernandes, Bueno, Rodrigues, Fabregat, & Sakomura, 2007) due
to its nutritional quality (Oliveira, Pimenta, Camargo, Fiorini, &
Pimenta, 2006). Thus, the aim of this study was to evaluate the inclu-
sion of tilapia processing waste silage (TPWS) in diets for L. vannamei
juveniles reared under clear-water and biofloc conditions.
2. Material and methods
2.1. Experimental design and culture conditions
The study was carried-out in the Aquaculture Sector, Department of
Animal Sciences, Universidade Federal Rural do Semi-Árido (UFERSA),
RN, Brazil. The postlarvae of Pacific white shrimp L. vannamei (PL20)
were supplied by a local commercial hatchery.
Before the experiment, PLs were stocked in a 15 m3 fiberglass cir-
cular tank (called as “macrocosm”) aiming to an acclimation and prior
biofloc formation. Water was vigorously aerated using one air diffuser
(composed by ¾” PVC pipe with several 1 mm holes) located in the
center of the macrocosm tank. In order to maintain biofloc culture
medium, shrimp were stocked at a density of 200 shrimp/m2 and
maintained until the end of the experimental period. Shrimp feeding
was carried-out at 08:00 am and 6:00 pm, with 35% crude protein
commercial feed (Aquabalance 35, Presence Animal Nutrition, Paulínia,
SP, Brazil) in two feed trays in order to monitor the food consumption.
The sugar cane molasses as a carbon source was daily added after the
feed addition in order to maintain a high C:N ratio (20:1) (Avnimelech,
1999) aiming to ensure optimal heterotrophic bacteria growth (Crab,
Kochva, Verstraete, & Avnimelech, 2009). The vertical substrates
(polyethylene 1.0 mm mesh) were placed in the center of the tank to
provide an additional area of 30% of the tank. This experiment was
performed in euryhaline conditions (∼5). Limited water exchange was
carried out not exceeding 0.5% daily by a central drain to prevent ac-
cumulation of sludge throughout the experimental period. De-
chlorinated freshwater was added to compensate evaporation losses
and sludge removal.
Two individual systems were set-up according to Emerenciano et al.
(2007): biofloc (BS) and clear-water systems (CWS). The trial was in-
itiated stocking L. vannamei juveniles (1.43 ± 0.33 g) in forty
(20 + 20) 40 L rectangular plastic bins (27 cm × 37 cm × 54 cm) in a
density of 63 shrimp/m2 (12 juveniles per bin). The juveniles were
distributed in a factorial completely randomized experimental design
(water type and % of tilapia waste silage inclusion as the main factors)
and reared during 45 days. Four replicate tanks were randomly as-
signed to each treatment. The treatments were based on the percentage
of TPWS inclusion (0 or control, 1.5%, 3.0%, 4.5% and 6.0% of inclu-
sion) in BS or CWS system, totalizing ten treatments. The formulation of
diets was described below (section 2.4).
For both treatments, the water was pumped from the macrocosm
tank to the experimental units by a submerged pump (¾ HP pumps) and
returned by gravity. Water flow in all experimental units was checked
two times per day in order to maintain uniformity between units as
much as possible (∼500%/d of water circulation between macrocosm
and bins). The experimental units were also siphoned once a week
aiming to remove faeces and any other residues.
For the CWS treatments, the same scheme described above in BS
was performed, except by the macrocosm tank (i) was not stocked with
animals, (ii) didn't receive carbon addition in order to maintain the
215
Aquaculture and Fisheries 4 (2019) 214–218
water clear. In addition, the aeration was supplied by two 4 HP blowers
connected to an emergency diesel electric generator to keep optimum
dissolved oxygen levels in both systems.
Temperature, salinity, pH (YSI-100, Yellow Springs Instruments
Inc., OH, USA) and dissolved oxygen (YSI-55, Yellow Springs
Instruments Inc., OH, USA) concentration were monitored twice daily.
Settling solids (Imhoff cones) was monitored daily (08:00am). Total
ammonia nitrogen (NH4–N) and nitrite (NO2–N) were measured once a
week (UNESCO, 1983). All shrimps were weighed to the nearest 0.1 g at
the beginning and the end of the experiment. Final body weight (g),
specific growth rate (SGR = [(ln final body weight - ln initial body
weight)/experimental time] × 100), feed conversion ratio (FCR = total
feed intake/total weight gain) and survival (final number of live
shrimp/total number of shrimp × 100) were assessed.
2.2. Fish silage production
The TPWS used in this study was produced in the Laboratory of
Seafood Technology and Quality Control (LAPESC/UFERSA) using filet
residues of Nile tilapia (Oreochromis niloticus) processing including
head, bones, skin, fins and viscera. The acid silage was produced using
the methodology described by Arruda, Borghesi, Brum, D′Arce, and
Oetterer (2006) with some modifications: 2% Formic acid (purity
≥95%, Sigma-Aldrich) and 3% Phosphoric acid (purity 85%–90%,
Sigma-Aldrich), and 1% Sorbic acid (purity ≥99.0%, Sigma-Aldrich) as
antifungal. The silage was dried in the oven at 60 °C for 24 h (to obtain
moisture below 13%), ground in a Rotor Mill (Rotating Knives and
Swing Hammer MA900, Marconi Equip. Lab. Ltda., Brazil) and homo-
genized (500-μm mesh). Before formulation of the experimental diets,
fish silage was neutralized by adding 1.6% calcium hydroxide to raise
the silage pH from 2.8 to 7.1.
2.3. Diet formulation and feeding
Five experimental diets were formulated to be isocaloric and iso-
proteic and to attend the nutritional requirements of the species
(Table 1). The TPWS inclusion ranged from zero to 6% of the diet. The
overall low level of inclusion was due to the high level of crude lipid
presented in the silage (37.4%). All diets were processed in the La-
boratory of Aquatic Animal Nutrition of the Universidade Federal do
Ceará (UFC) using the method described by Nunes, Sa, and Sabry-Neto
(2011), with some modifications (i.e., inclusion of sardine hydrolyzed
as EAA source; and reduced amount of salmon oil due to the high lipid
content of the TPWS). All diets were kept frozen at − 20 °C until use.
For both treatments, the juveniles were fed twice a day (08:00 am and
06:00 pm) using a feed tray to monitor feed consumption.
2.4. Statistical analysis
After a check for homoscedasticity and normality (Zar, 1996),
shrimp performance data were analyzed using a two-way ANOVA and
Tukey's test to compare the means with α fixed in 0.05 (Zar, 1996)
using the software R (version 3.0.2). Survival data in percentage was
transformed using the arcsine transformation in order to normalize the
data before the analysis; however, the original means and standard
deviation are presented.
3. Results
In regards to proximate analysis, the results demonstrated that
TPWS contained 83.8% dry matter, 33.7% crude protein, 37.4% crude
lipid, and 21.5% ash based on dry matter (Table 2). Water quality
parameters maintained in the recommended ranges for L. vannamei in
both systems with temperature ranging from 24 to 32 °C, pH ranging
from 6.7 to 8.7 and salinity 4 to 5. The dissolved oxygen always was
kept > 3.7 mg/L, total ammonia nitrogen < 0.52 mg/L and nitrite <
J. da Rocha Soares Neto, et al. Aquaculture and Fisheries 4 (2019) 214–218

Table 1 Table 3
Ingredients and chemical composition of diets used in the present study. Growth performance of L. vannamei fed increasing percentages of tilapia pro-
cessing waste silage (TPWS) inclusion in clear-water and biofloc systems during
Ingredients Unit Dietary tilapia silage inclusion (%)
45-d.
0 1.5 3.0 4.5 6.0 Diet (% of SGR (% day−1) Mean final Survival (%) FCR
tilapia weight (g)
Soybean meal % 40.00 40.00 40.00 40.00 40.00 silage
Wheat bran % 20.00 20.00 20.00 20.00 20.00 inclusion)
Fishmeal % 12.00 12.00 12.00 12.00 12.00
Salmon meal % 8.00 7.54 6.82 6.10 5.38 0 1.86 ± 0.20ns 6.51 ± 0.76ns 85.29 ± 17.18ns 1.59 ± 0.37ns
Tilapia silage % 0.00 1.50 3.00 4.50 6.00 1.5 1.90 ± 0.14ns 6.62 ± 0.60ns 90.15 ± 6.27ns 1.56 ± 0.10ns
Wheat midlings % 5.24 3.90 3.62 3.33 3.04 3.0 1.93 ± 0.18ns 6.79 ± 0.80ns 92.93 ± 9.74ns 1.38 ± 0.29ns
Salmon oil % 3.18 3.48 2.99 2.50 2.01 4.5 1.83 ± 0.23ns 6.43 ± 0.94ns 94.32 ± 4.30ns 1.61 ± 0.15ns
Powder molasses % 3.00 3.00 3.00 3.00 3.00 6.0 2.07 ± 0.11ns 7.46 ± 0.56ns 88.88 ± 13.94ns 1.35 ± 0.23ns
Soybean lecithin % 2.81 2.81 2.81 2.81 2.81
Calcium phosphate % 2.00 2.00 2.00 2.00 2.00 System
Sardine hydrolysate % 2.00 2.00 2.00 2.00 2.00 Clear- 1.82 ± 0.20b 6.35 ± 0.54b 87.50 ± 12.12ns 1.65 ± 0.23b
Vitamin and mineral % 1.00 1.00 1.00 1.00 1.00 water
premixa Biofloc 2.01 ± 0.12a 7.17 ± 0.79a 94.23 ± 6.25ns 1.35 ± 0.18a
Aglutinantb % 0.50 0.50 0.50 0.50 0.50
Coline chloride 60% % 0.22 0.22 0.22 0.22 0.22 No interactions were observed (P > 0.05). Values are means ( ± standard
Ascorbic acidc % 0.04 0.04 0.04 0.04 0.04
error) of treatments (diets or system); Different letters in columns denote sig-
Antioxidantc % 0.01 0.01 0.01 0.01 0.01
nificant differences between experimental systems with α = 0.05 level by
Chemical compositiond Tukey's HSD multiple range test; NS, not statistically different (P > 0.05); SGR,
Ash % 8.33 8.52 8.72 8.91 9.11 specific growth rate; FCR, feed conversion ratio.
Crude Fat % 9.24 10.00 10.00 10.00 10.00
Crude Fiber % 3.14 3.02 2.99 2.96 2.93 settling solids that maintained below to 15 mL/L. Schveitzer et al.
Crude Protein % 35.00 35.00 35.00 35.00 35.00
(2013) demonstrated that high concentrations of settling solids and TSS
Digestible Energy kcal/kg 3036 3015 2942 2868 2794
Digestible Protein % 30.83 30.41 29.98 29.56 29.13 appear to be more harmful for culture of L. vannamei.
Total Energy kcal/kg 3746 3709 3624 3538 3453 In our experimental conditions, both biofloc (BS) and clear-water
Moisture % 10.42 10.46 10.59 10.73 10.86 (CWS) systems, tilapia processing waste silage (TPWS) could be in-
4
cluded at the highest level (6.0%) without losses in growth performance
Etoxiquim 66% (Impextraco, Impextraco Latin America, Curitiba, PR, Brazil).
a and survival. On the other hand, in BS condition shrimp presented the
DSM (DSM Nutritional Products, São Paulo, SP, Brazil): Vitamin A
best performance as compared to CWS, probably due to the continuous
1.250.000UI; Vitamin D3 350.000 UI; Vitamin E 25.000 UI; Vitamin K3 500 mg;
Vitamin B1 5.000 mg; Vitamin B2 4.000 mg; Vitamin B6 10,0 mg; Nicotinic acid availability of natural food. This natural productivity is normally pre-
15.000 mg; Pantothenic acid 10.000 mg; Biotin 150 mg; Folic acid 1.250 mg; sent in a form of bacteria, microalgae, protozoa, nematodes, copepods
Vitamin C 25.000 mg; Choline 50.000 mg; Inositol 20.000,0 mg; Iron 2.000 mg; and rotifers (Azim & Little, 2008; Ballester et al., 2010; Decamp et al.,
Copper 3.500 mg; Chelated Cooper 1.500 mg; Zinc 10.500 mg; Chelated Zinc 2002; Ray et al., 2010). These microorganisms are a rich source of lipids
4.500 mg; Manganese 4.000 mg; Selenium 15, mg; Chelated Selenium 15 mg; (Maica, Borba, & Wasielesky, 2012), vitamins and essential amino acids
Iodine 150 mg; Cobalt 30 mg. (Ju, Forster, Conquest, & Dominy, 2008), as well as highly diverse
b
Pegabind™ (Bentoli Agrinutrition Inc., Austin, EUA). “native protein”. The concept of “native protein” is related to protein
c
Stay C™, DSM (DSM Nutritional Products, Sao Paulo, SP, Brazil). source without previous treatment mainly including live food
d
Estimated values.
(Emerenciano, Cuzon, Goguenheim, Gaxiola, & Aquacop, 2012b). Is
important to note that bacteria protein-source plays an important role
Table 2 in the equilibrium and re-ingestion of particulate organic matter and
Proximate composition of tilapia processing waste silage (TPWS – acid silage)
faeces (coprophagia) left by shrimp results in a form of the constant
using residues of Nile tilapia (Oreochromis niloticus) produced using the meth-
food supply. The colonization of shrimp gut by bacteria had been shown
odology described by Arruda et al. (2006).
positive effects such as improvement of shrimp digestive enzymes ac-
Dry matter (%) Crude protein (%) Ash (%) Crude lipid (%) tivity (Xu, Pan, Sun, & Huang, 2012) and increasing the availability of
extracellular enzymes (Xu & Pan, 2012) acting as “natural probiotic”
TPWS 83.8 ± 2.3 33.7 ± 0.6 21.5 ± 0.2 37.4 ± 0.8
(De Schryver, Boon, Verstraete, & Bossier, 2012).
In the recent years, the interests on alternative dietary protein
0.25 mg/L stayed in safe concentration to the animals during all the sources such as vegetable grains and terrestrial animal industry by-
experiment. Settling solids increased over time although levels main- products has increased. On the other hand, special attention on palat-
tained below 15 mL/L. ability, digestibility, deficiency of essential amino acids, and the pre-
Regarding the growth performance (Table 3), no interactions be- sence of anti-nutritional factors still need to be done (Forster et al.,
tween system and diet were observed (P > 0.05). Survival was not 2003; Naylor et al., 2009). Although problems exist, many cases of
affected by both system and diet; and presented averages above 85% in success have been reported using alternative dietary protein such as
all treatments. FCR presented significantly lower values in BFT (1.35) cattle by-product and a mixture of canola and soya (Forster et al., 2003;
as compared to CWS (1.65). Following the same trend, mean final Suarez et al., 2009), poultry by-product (Amaya et al., 2007; Cruz-
weight and SGR was statistically influenced by the system but not by Suárez et al., 2007; Samocha et al., 2004), swine by-product
the diet (P > 0.05), presenting higher values in BFT with 7.17 g and (Hernández et al., 2008), and soy protein concentrate (Paripatananont,
2.01%/d as compared to 6.35 g and 1.82%/d in CWS. Boonyaratpalin, Pengseng, & Chotipuntu, 2001). Bauer et al. (2012)
suggested that a mixture of soy protein concentrate and microbial floc
meal can be utilized as a substitute for fishmeal in diets for L. vannamei
4. Discussion juveniles. These studies have been carried out in clear-water condition
and few efforts have been done to investigate alternative sources in
The water quality parameters remained within the recommended biofloc conditions. Scopel et al. (2011) evaluated the replacement of
range for L. vannamei culture (Van Wyk & Scarpa, 1999), including fishmeal (0, 12.5% and 21.0%) by a combination of soy and animal

216
J. da Rocha Soares Neto, et al.
terrestrial by-products. The authors found that 12.5% of replacement
did not affect shrimp growth, resulting in growth rates of 0.7 g/week
similar to those found in our study in clear-water condition, but less
than 0.9 g/week observed in biofloc.
No literature was found related to the use of TPWS in L. vannamei
diets under biofloc condition. Although low levels of silage were in-
cluded in the diets due to the high lipid content in the fish silage, the
highest level of 6% still could represent a significant reduction in costs
in shrimp formulations. In a study using clear-water, Gallardo et al.
(2012) evaluated in L. vannamei juveniles feeds containing (i) fish waste
silage, (ii) fish waste silage with soybean meal and (iii) fish waste meal
as a protein source. The authors reported that shrimp fed with diets
containing fish waste silage combined with soybean meal gained 0.7 g/
week higher than those fed with fish waste silage or fish waste meal
(0.3 g/week). It is important to note that these values are lower than
observed in our study e.g. with biofloc conditions (0.9 g/week). Ad-
ditionally, in our study values of FCR were 1.3 and 1.6 for BS and CWS,
respectively, lower than 2.8 and 2.5 observed by Ray et al. (2010) and
Xu et al. (2012) using soy protein-based diets and low protein content
diets, respectively, both in biofloc conditions for L. vannamei.
In contrast with our work, Costa, Portz, Hisano, Druzian, and Ledo
(2009) did an interesting study evaluating shrimp silage in juvenile
tilapia (O. niloticus) diets. The authors concluded that it is possible to
include 2.75% of shrimp silage, reducing the diets costs in 3.3%
without losses in fish performance. In a similar work, Cavalheiro,
Souza, and Bora (2007) tested shrimp head silage (approximately 40%
protein) as a substitute for fishmeal in tilapia diets at 0, 33.3%, 66.6%
and 100% dietary levels. The results indicate that the shrimp silage
could replace fishmeal at 100% level with economic advantages and
without sacrificing the quality of the feed.
5. Conclusion
In our experimental conditions, the inclusion of tilapia processing
waste silage (TPWS) in L. vannamei diets was possible up to 6% without
compromise shrimp performance and survival. In addition, shrimp
raised in BS demonstrated better growth performance as compared to
CWS.
Acknowledgements
The authors would like to thankthe Funding of Studies and Projects
FINEP-Brazil (1550/10) and the Brazilian National Council for
Scientific and Technological Development CNPq Brazil (475609/2010-
7) for the financial support received, Larvi and Aquatec for the shrimp
post-larvae supply, Darlimeire Dantas de Aquino (Scholarship PIVIC –
CNPq/UFERSA) and Professor Alberto J. P. Nunes for the contribution
in the diet formulation and manufacture.
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