Scientific Article
ISSN 1678-2305 online version
BOLETIM DO INSTITUTO DE PESCA
FERREIRA et al. Bol. Inst. Pesca 2018, 44(3): e362. DOI: 10.20950/1678-2305.2018.362 1/5
ASPECTS OF FOOD MANAGEMENT ON AMAZON RIVER PRAWN
LARVICULTURE PHASE*
ABSTRACT
The time supply of live food (Artemia nauplii) at the initial phases of development and the
frequency of feeding with inert feed (egg custard) in Macrobrachium amazonicum larviculture were
evaluated by two experiments: In Experiment I, newly hatched Artemia were offered to the larvae
in three schedules (treatments): at 07:30 h (A07:30); at 12:00 h (A12:00) and 16:30 h (A16:30).
In Experiment II, the inert food was offered in the following frequencies (treatments): twice a
day - at 08:00 and 17:00 h (IF2); three times a day - at 08:00; 12:30 and 17:00 h (IF3) and four
times a day - at 08:00; 11:00, 14:00 and 17:00 h (IF4). Water quality variables (dissolved oxygen,
pH, temperature, salinity, NH
3
+ NH
4
, NO
2
and NO
3
) and production variables (weight, survival
and duration of larviculture) were evaluated. The feeding managements studied did not influence
significantly either the water quality and production variables. The results indicated that it can be
recommended, for M. amazonicum larviculture feeding management, the supply of Artemia nauplii
at early morning and inert feed two times per day (early morning and late afternoon), after
stage V until the metamorphosis.
Key words: frequency of feeding; live food; Artemia nauplii; inert food.
MANEJO ALIMENTAR NA LARVICULTURA DO CAMARÃO-DA-AMAZÔNIA
RESUMO
Avaliou-se o horário de fornecimento de alimento vivo no início do desenvolvimento larval e a
frequência de arraçoamento com alimento inerte em larvicultura Macrobrachium amazonicum.
Foram realizados dois experimentos: no Experimento I, náuplios de Artemia (A) foram ofertados
em três horários (tratamentos): às 07:30 h (A7:30); às 12:00 h (A12:00) e 16:30 h (A16:30).
No Experimento II, o alimento inerte (AI) foi oferecido nas seguintes frequências (tratamentos):
duas vezes ao dia - às 08:00 e 17:00 h (AI2); três vezes ao dia - às 08:00; 12:30 e 17:00 h (AI3)
e quatro vezes ao dia - às 08:00; 11:00, 14:00 e 17:00 h (AI4). Foram avaliadas as variáveis
limnológicas (oxigênio dissolvido, pH, temperatura, salinidade, NH
3
+NH
4
, NO
2
e NO
3
) e as variáveis
de produção (peso, sobrevivência e dias de larvicultura). Os diferentes manejos avaliados não
influenciaram significativamente na qualidade da água e nas variáveis de produção. Os resultados
indicaram que, para o manejo alimentar na larvicultura de M. amazonicum, o alimento vivo
(náuplios de Artemia) pode ser fornecido no início da manhã e, após o estágio V, a dieta pode
ser complementada com o alimento inerte, duas vezes por dia (início da manhã e final da tarde).
Palavras-chave: frequência de alimentação; alimento vivo; náuplio de Artemia; alimento inerte.
INTRODUCTION
After alternating periods of decreasing and expansion, the freshwater prawn farming
in Brazil currently presents a favorable scenario, due to the prospects of improvement
of the organization of the productive chain (MARQUES and MORAES-VALENTI,
2012). The only commercially farmed species in Brazil is Macrobrachium rosenbergii
(DE MAN, 1879), but native species as Macrobrachium amazonicum (HELLER, 1862),
M. acanthurus (WEIGMANN, 1836) and M. carcinus (LINNAEUS, 1758) are exploited
by fishing in the north and northeast regions (KUTTY and VALENTI, 2010). Among
these species, M. amazonicum presents great potential for aquaculture (MACIEL and
VALENTI, 2009), being used, besides human consumption, as ornamental species, live
feed for carnivorous ornamental fish and live bait for sport fishing (MARQUES and
Thaís Monteiro FERREIRA
1
Marcello Villar BOOCK
2
Helenice Pereira BARROS
3
Helcio Luis de Almeida MARQUES
4
1
Instituto de Pesca, Programa de Pós-graduação em
Aquicultura e Pesca, CP 61070, CEP 05001-970, São
Paulo, SP, Brasil.
2
Agência Paulista de Tecnologia dos Agronegócios,
Polo Regional da APTA Centro-Leste, Av. Virgilio
Baggio, 85, CEP 13641-004, Pirassununga, SP, Brasil.
3
Instituto de Pesca, Centro de Pesquisa do Pescado
Continental, CP 1052, CEP 15025-970, São José do
Rio Preto, SP, Brasil.
4
Instituto de Pesca, CP 61070, CEP 05001-970, São
Paulo, SP, Brasil. E-mail: hlamarques@gmail.com
(corresponding author).
*Financial support: Research partially funded by São
Paulo State Research Support Foundation – FAPESP,
Process 2013/16281-9.
Received: January 22, 2018
Approved: March 29, 2018
ASPECTS OF FOOD MANAGEMENT ON AMAZON RIVER…
FERREIRA et al. Bol. Inst. Pesca 2018, 44(3): e362. DOI: 10.20950/1678-2305.2018.362 2/5
MORAES-VALENTI, 2012). Although the larviculture techniques
of the species are well developed, feeding management in the
different larval stages still presents controversial results.
In order to establish feeding management, the behavior of
the larvae facing the diet supplied should be known. Behavior
studies have mainly evaluated the dependence of exogenous
food on larval development (ANGER and HAYD, 2009, 2010);
acceptance of inert food according to the stage of development
(ARAUJO and VALENTI, 2007); ingestion of Artemia according
to stage of development, supply density of nauplii and period
of day (MACIEL et al., 2012) and the influence of the color of
the larvae maintenance tanks in the food intake (MACIEL and
VALENTI, 2014a). Also the replacement of Artemia nauplii by
inert food was investigated (MACIEL and VALENTI, 2014b;
ARAUJO and VALENTI, 2017).
Despite these studies, some aspects of feeding management
need to be better investigated, as the feeding time with live food
during the initial larval stages and the frequency of feeding
with inert feed (custard). Those aspects can influence the food
intake, it’s assimilation by the larvae and, consequently, larval
development and productivity.
Macrobrachium amazonicum larvae feed on Artemia nauplii
from the second stage of larval development (ARAUJO and
VALENTI, 2007), with the recommended frequency of once a day
MACIEL et al. (2012). Additionally, these authors comment that
is necessary establishing the best time of the supply of nauplii,
considering the feeding activity of the prawn larvae.
Regarding to inert feed supply, ARAUJO and VALENTI
(2007, 2017) recommend starting feeding M. amazonicum larvae
from stage VI, as a complement to the feeding with Artemia,
considering that since stage VII, inert feed becomes to be more
consumed than live food. The larger availability of inert feed
appears occurring just after the supply, because even with aeration,
the flakes of feed rapidly precipitate on the bottom, becoming
less accessible for the larvae, which have planktonic behavior.
Thus, the unconsumed feed can be microbiologically decomposed
resulting in an increase of nitrogen compounds, thus prejudicing
the water quality. Additionally, after some time in the water, there
is leaching of the feed nutrients. Consequently, the supply of inert
feed in two or more portions during the daytime could increase
the chance encounter of the larvae with the feed, minimizing the
wastes and improving the absorption of nutrients by the larvae
(MACIEL, 2007).
Considering these aspects, the objective of this study was
establishing a protocol aiming to maximize the feeding efficiency
on M. amazonicum larviculture, determining the most adequate
time for Artemia supply in the initial larval phase and the frequency
of inert feed supply after stage V.
METHODS
Two experiments were carried out during January to March,
2015 at the Freshwater Prawn Laboratory of the Pirassununga
Aquaculture Centre. The general procedures, common for both
experiments were described below and after that, the specific
procedures to experiments I and II were presented.
Larvae of M. amazonicum prawns were obtained from ovigerous
females collected in a breeding pond and transferred to a hatching
tank of 100L, inside the laboratory. After hatching, larvae were
counted and transferred to the experimental tanks (rectangular
plastic 30 L black boxes, with 20 L of useful volume) with water
recirculation system (external biological filter), at a density of
50 L
-1
. The recirculation rate was maintained at 100% of total
volume per hour. Starting 14 days before the beginning of the
experiments, the biofilters were gradually activated, adding
ammonium (NH
3
) solution to them.
The photoperiod was 12 h clear / 12 h dark. The wastes of
food, exoskeletons, dead larvae and feces of the experimental
tanks were syphonated daily, in order to keep good water
quality. Temperature, dissolved oxygen (YSI Pro 20 oxymeter),
pH (EcoSense 100A pH meter) and salinity (INCOTHERM
Salinometer), were measured once a day (from 8:00 to 09:00 a.m.),
and were maintained in the appropriate range for M. amazonicum
larvae (ARAUJO and VALENTI, 2011; HAYD et al., 2014).
In alternate days, the monitoring of ammonium (NH
3
), nitrite (NO
2
)
and nitrate (NO
3
) concentrations inside the tank was determined
by colorimeters kits for marine aquarium (PRODAC tests).
Samples composed by 10 larvae of each tank were daily collected
and analyzed using a stereomicroscope, in order to identifying
the average larval stage, according to the methodology described
by GUEST (1979).
Experiment 1: determination of best timing for
live food supply (Artemia nauplii) in the initial
larviculture phase (II-VI stages)
In Experiment 1, from stage II, larvae were fed only with
newly hatched Artemia nauplii, at 07:30 h, 12:00 h and 16:30 h
(A7:30, A12:00 and A16:30 treatments respectively). The experiment
followed a complete randomized design, with four replicates per
treatment. The amount of Artemia supplied was 4 nauplii mL
-1
in stage II and 6 nauplii mL
-1
in stages III to VI (MACIEL and
VALENTI, 2014a).
Water quality variables (Mean ± SD) for the treatments were:
temperature: A7:30 = 29.4 ± 0.7 °C; A12:00 = 28.8 ± 0.4 °C,
A16:30 = 29.6 ± 0.9 °C; dissolved oxygen: A7:30 = 4.64 ± 0.40 mg L-1;
A12:00 = 5.19 ± 0.35 mg L
-1
; A16:30 = 5.03 ± 0.09 mg L
-1
; pH:
A7:30 = 7.90 ± 0.15; A12:00 = 8.02 ± 0.04; A16:30 = 7.92 ± 0.05;
salinity: A7:30 = 13.7 ± 0.8 g L
-1
; A12:00 = 13.8 ± 0.8 g L
-1
;
A16:30 = 13.6 ± 1.1 g L
-1
.
Larvae were harvested when more than 80% of the population
of each tank reached the stage VI (estimated by random sampling).
The filtering system was turned off, the water drained and the
larvae were individually counted for estimating the survival of
each tank.
The dry mass of the larvae was obtained from random samples
of 200 larvae from each tank, separated into 10 subsamples with
20 individuals. Each subsample was packed into pre-weighed
aluminum foil cartridges (initial mass) and identified according
ASPECTS OF FOOD MANAGEMENT ON AMAZON RIVER…
FERREIRA et al. Bol. Inst. Pesca 2018, 44(3): e362. DOI: 10.20950/1678-2305.2018.362 3/5
to each treatment. These were then placed in Petri dishes and
dried in an electric kiln at 60 °C for 12 hours; the plates were
transferred to a desiccator for 2h, and after, each cartridge was
weighed (final mass) in an analytical balance Mettler Toledo
XP26 (1 mµ precision). The dry mass was determined by the
difference between the final mass and the initial mass of the
cartridges, according to the treatments.
Experiment 2: determination of the best frequency of
inert feed supply (egg custard) on the final phase of
M. amazonicum larval development (stages V-IX)
In Experiment 2, inert food was offered in the following
frequencies (treatments): twice a day - at 08:00 and 17:00 h (IF2);
three times a day - at 08:00; 12:30 and 17:00 h (IF3) and
four times a day - at 08:00; 11:00 h, 14:00 and 17:00 h (IF4).
The experiment was conducted on complete randomized design,
with four replicates per treatment.
The inert food consisted of the “egg custard”, adapted from
the supplementary diet for M. rosenbergii larvae, described
by MALLASEN and VALENTI (1998). The ingredients were
weighed, blended and the resulting mixture was cooked in a pan
under water bath to custard consistency. After cooling, it was
cut into small pieces, individually wrapped with polyethylene
film and frozen at −18 °C. Before being fed to the larvae, the
pieces were made into smaller particles, which were then passed
through a sieve with 1.00 mm mesh and the filtrate was collected
in a 0.5 mm mesh screen for larvae on stages V and VI, and in a
0.7 mm mesh screen for stages VII onward.
Larvae were feed on the basis of the procedures adopted by
MACIEL and VALENTI (2014a), consisting on newly hatched
Artemia supplied daily at 10:00 h, from the second larval stage
onwards, and inert food supplied from stage VI onwards, according
to the treatments described above. The daily amount supplied of
inert food was the same for all treatments, varying of 0.5 g tank
-1
at stages VI and VII and 1.0 g tank
-1
from stage VIII onwards.
Water quality variables (Mean ± SD) for the treatments were:
AI2 = 28.0 ± 0.4 °C; AI3 = 28.4 ± 0.4 °C; AI4 = 27.9 ± 0.9 °C
(temperature); AI2 = 5.66 ± 0.12 mg L
-1
, AI3 = 5.65 ± 0.14 mg L
-1
,
AI4 = 5.80 ± 0.17 mg L
-1
(dissolved oxygen); AI2 = 7.90 ± 0.15;
AI3 – 8.02 ± 0.04, AI4 = 7.92 ± 0.05 (pH) and AI2 = 13.7 ± 0.8 g L
-1
,
AI3 – 13.8 ± 0.8 g L
-1
, AI4 – 13.6 ± 1.1 g L
-1
(salinity).
The tanks were harvested when more than 80% of the larvae
population metamorphosed into post-larvae (PL) (estimated by
random sampling). All the PL and the remaining larvae were
counted in order to calculate survival rate. The dry mass for each
experimental tank was determined as described for the larvae
(experiment I). After that, the means of production variables with
their respective standard deviations (survival rate, dry mass and
duration of larviculture) were calculated to the each treatment.
Statistical analysis
Before the hypothesis test, the survival data were square-root
arc-sine transformed as recommended for ZAR (2010), but they are
presented as non-transformed percentages for easier visualization.
Data of nitrogenous compounds and production were tested for
normality (Shapiro-Wilk) and homoscedasticity (Bartlett). As no
significant deviation was observed, means were subjected to
one-way ANOVA, using Statistica version 7.0. When differences
among variables were observed, the means were compared by
the Tukey Test (p<0.05).
RESULTS
Experiment 1
Apparently, the Artemia supplying time has not significantly
influenced the concentration of ammonium (NH
3
), nitrite (NO
2
)
and nitrate (NO
3
) (Table 1). However, the high standard deviations
may have masked possible effects of treatments on such variables.
Lower concentrations were observed on A7:30 treatment and the
higher, on A16:30 treatment.
Production variables (dry mass, survival rate, and days of
larviculture) did not differ statistically (p<0.05) among treatments,
whereas survival rate presented high SD values in the treatments
A12:00 and A16:30 (Table 2).
Experiment 2
As in the Experiment 1, water variables total ammonium
(NH
3
+ NH
4
), nitrite (NO
2
) and nitrate (NO
3
) were not significantly
influenced (p<0.05) by the frequencies of inert feed supplying
(Table 3).
Table 1. Water quality variables (mean ± SD) total ammonium
(NH
3
+ NH
4
), nitrite (NO
2
) and nitrate (NO
3
), according
to the treatments tested in Experiment 1: A7:30 - Artemia
supplied at early morning; A12:00 - Artemia supplied at noon;
A16:30 - Artemia supplied at late afternoon.
Variable
Treatment
A7:30 A12:00 A16:30
NH
3
+ NH
4
(mg
1
) 0.29 ± 0.36 1.04 ± 1.34 1.18 ± 1.61
NO
2
(mg
1
) 0.02 ± 0.03 0.18 ± 0.33 0.72 ± 1.21
NO
3
(mg
1
) 4.96 ± 3.47 5.06 ± 4.87 5.25 ± 1.66
Table 2. Production variables (mean ± SD) dry mass (DM),
survival rate (SR) and days of larviculture (DL) (Mean ± SD),
according to the treatments tested in Experiment 1: A7:30 - Artemia
supplied at early morning; A12:00 - Artemia supplied at noon;
A16:30 - Artemia supplied at late afternoon.
Variable
Treatment
A7:30 A12:00 A16:30
DM (mg) 1.99 ± 0.47 2.09 ± 0.53 2.26 ± 0.40
SR (%) 74.8 ± 3.5 61.7 ± 11.1 67.3 ± 14.3
DL (days) 8.3 ± 1.3 7.5 ± 1.3 7.5 ± 1.7
ASPECTS OF FOOD MANAGEMENT ON AMAZON RIVER…
FERREIRA et al. Bol. Inst. Pesca 2018, 44(3): e362. DOI: 10.20950/1678-2305.2018.362 4/5
Production variables did not present statistical differences
(p<0.05) among the treatments. However, means of survival rates
showed high standard deviation (Table 4).
DISCUSSION
The concentration of nitrogen compounds remained at the
recommended range to this species (<1.6 mg L
-1
for ammonium,
<0.8 mg L
-1
for nitrite and <80.0 mg L
-1
for nitrate), according to
MORAES-VALENTI and VALENTI (2010). Nitrogen by-products
are resulting from both larvae excretion and decomposition of
organic matter especially wastes of food. Considering that the
food management can influence the food intake by the larvae, it
can be inferred that the biofiltration system was not overloaded
due to the unconsumed food, indicating that the managements
evaluated did not negatively affect the nitrification process and
could be used on M. amazonicum larviculture.
However, it is important to highlight that the high standard
deviations observed in the concentration of nitrogen compounds of
both experiments, could indicate the smaller or the higher adjusting
to the feed management in larval phase. The higher the intake by
larvae, the smaller the waste of feed and, consequently, minor
variation in concentration of nitrogen compounds is expected.
During the initial larval development of M. rosenbergii, the
sensorial and food apprehension structures are barely developed
(HENRIQUES et al., 2014). Consequently, the larvae are not
able to efficiently pursuit their prey. According to BARROS and
VALENTI (1997), this characteristic makes the chance of encounter
is the main mechanism of gathering food in earlier larval stages.
Indeed, MACIEL et al. (2012) verified that for M. amazonicum
larvae, the encounter opportunity is the most important factor of
gathering food during the night whereas the vision is the most
important mechanism under day light, making that the supply
of feed is more easily encountered by larvae along the day.
Based on the results here obtained, it can be recommended, for
M. amazonicum larviculture feeding management, the supply of
Artemia nauplii once a day at early morning, aiming to reduce
labor costs.
The survival rates registered in the second experiment, were
higher than that presented for MURTHY et al. (2008) (between
31.1 and 38.9%), that studied different formulated inert larval
diets. DAVID et al. (2016), studying the effects of intensification
on the M. rosenbergii larviculture, obtained survivals between
55.0 ± 5.7% and 63.4 ± 9.6%, but it must be considered that
the M. amazonicum larviculture protocol is not so well studied
as M. rosenbergii one, and survival rates can oscillate among
different cycles and may be sound improved with further studies.
The supply of inert diet twice a day is generally used both for
M. rosenbergii (DAVID et al., 2016) and M. amazonicum (MACIEL
and VALENTI, 2014b) larvae. In a recent experiment, ARAUJO
and VALENTI (2017) found that productivity and survival were
significantly higher when M. amazonicum larvae was fed twice
a day with inert food and Artemia during all the larval stages,
than when larvae were fed only with inert food four times per
day along the entire cycle.
KOVALENKO et al. (2002) that studied a semi-purified
microbound diet containing alginate was compared to newly
hatched live Artemia nauplii as an exclusive diet for the culture
of larval freshwater prawn M. rosenbergii. Those authors fed
the larvae with the inert diet several times during the light
phase (every 1.5–2 h) and obtained survival rates varying
from 77.3% to 73.3%. The survivals were not significantly different
from that of Artemia-fed larvae. Contrasting to those results, due
to the lack of statistical differences among the treatments in the
second experiment, it can be recommended the supply of inert
feed only twice a day (treatment IF2) after stage V, until the
metamorphosis into post-larvae instead of three or four times
(treatments IF3 and IF4), in order to reduce costs with labor.
CONCLUSION
Once the adjustment of feeding routine is one of the most
important factors in crustacean larviculture, based on the results
obtained in the present study, it can be recommended, for
M. amazonicum larviculture feeding management, the supply of
Artemia nauplii once a day at early morning and inert feed two
times per day (at early morning and late afternoon), after stage
V until the metamorphosis.
Table 3. Water quality variables (mean ± SD) total ammonium
(NH
3
+ NH
4
), nitrite (NO
2
) and nitrate (NO
3
), according to the
treatments tested in Experiment 2: IF2 - inert feed supplied two
times per day (at 08:00 and 17:00 h); IF3 - inert feed supplied three
times per day (at 08:00; 12:30 and 17:00 h) and IF4 - inert feed
supplied four times per day (at 08:00; 11:00 h, 14:00 and 17:00 h).
Variable
Treatment
IF2 IF3 IF4
NH
3
+ NH
4
(mg Lˉ
1
) 0.05 ± 0.04 0.04 ± 0.04 0.00 ± 0.00
NO
2
(mg Lˉ
1
) 0.67 ± 1.22 0.07 ± 0.04 0.09 ± 0.04
NO
3
(mg Lˉ
1
) 3.80 ± 0.59 3.36 ± 1.32 4.08 ± 2.04
Table 4. Production variables (mean ± SD) dry mass (DM),
survival rate (SR) and days of larviculture (DL) (Mean ± SD),
according to the treatments tested in Experiment 2:-IF2 - inert
feed supplied two times per day (at 08:00 and 17:00 h); IF3 - inert
feed supplied three times per day (at 08:00; 12:30 and 17:00 h)
and IF4 - inert feed supplied four times per day (at 08:00; 11:00 h,
14:00 and 17:00 h).
Variable
Treatment
IF2 IF3 IF4
DM (mg) 11.15 ± 0.78 11.09 ± 1.04 11.68 ± 2.58
SR (%) 42.4 ± 13.0 52.5 ± 8.4 47.6 ± 10.0
DL (days) 20.3 ± 1.0 19.8 ± 1.0 20.5 ± 1.7
ASPECTS OF FOOD MANAGEMENT ON AMAZON RIVER…
FERREIRA et al. Bol. Inst. Pesca 2018, 44(3): e362. DOI: 10.20950/1678-2305.2018.362 5/5
ACKNOWLEDGEMENTS
To the São Paulo State Research Support Foundation (FAPESP)
for partially funding this research (Process 2013/16281-9) and
to the CAPES for the scholarship provided.
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