Aquaculture International (2021) 29:399–415

https://doi.org/10.1007/s10499-020-00636-8

Growth performance and acoustic feeding

behavior of two size classes of Litopenaeus vannamei
fed pelleted and extruded diets

Roberta Soares 1,2 & Silvio Peixoto

1,2
& Harsha S. C. Galkanda-Arachchige
1,3
&
D. Allen Davis 1

Received: 13 May 2020 / Accepted: 14 December 2020 / Published online: 9 January 2021
# The Author(s), under exclusive licence to Springer Nature Switzerland AG part of Springer Nature 2021

Abstract
This study aimed to compare the growth performance, food consumption, and acoustic
feeding behavior of two size classes of Litopenaeus vannamei fed on extruded and
pelleted diets. Two similar diets (35% crude protein) prepared by extrusion or pelletizing
methods were offered to two shrimp size classes: small (3.83 ± 0.16 g) and large (10.28 ±
0.37 g). Shrimp were reared in 100-L aquaria (salinity 6 ppt, temperature 28 °C); growth
performance and survival were analyzed at the end of 4 and 8 weeks for small and large
size classes, respectively. Hydrophones recorded the sounds of shrimp feeding activity for
30-min intervals, after food remains were collected to evaluate consumption. Physical
(pellet durability index, hardness, water absorption, density, sinking velocity, dry matter
retention) and chemical (aromatic amino acids (AAA) leaching) characteristics of the
diets were evaluated before and after soaking. Extruded diet presented higher durability
and hardness before soaking, but its higher water absorption resulted in markedly texture
softened and higher AAA leaching. Both shrimp size classes presented no significant
differences in final mean weight, biomass, weight gain, survival, food conversion, and
food consumption between pelleted or extruded diets. The mean acoustic energy did not
differ between diets, but larger shrimp produced higher energy during feeding activity.
The energy showed a significant progressive decrease along time intervals (10, 20, and
30 min) for both size classes and diets. Despite the different characteristics between
pelleted and extruded diets, both resulted in similar shrimp performance and acoustic
feeding profile activity under laboratory conditions.

Keywords Passive acoustics monitoring . Feeding management . Food consumption . Leaching .

Low salinity

* Roberta Soares
beta.ufrpe@gmail.com

Extended author information available on the last page of the article

400 Aquaculture International (2021) 29:399–415

Introduction

Understanding shrimp behavior provides a starting point to improve feeding management

efficiency. Shrimp are typically slow feeders that explore the pond bottom for potential food
particles and eat almost continuously. The small size of penaeids foreguts and the high passage
rate of food through the digestive tract require feed frequently; but as feeding proceeds, the
digestive glands fills and ingestion slows (Dall et al. 1990). Additionally, molting is a recurring
event that affects the amount of feed consumed (Dall et al. 1990; Hill and Wassenberg 1992).
Due to these feeding habits, physiology and morphological features, shrimp requires sinking
pellets with high water stability, which means that pellet must preserve its physical integrity
with minimal disintegration and nutrient leaching until it be consumed (Lim and Cuzon 1994).
Aquatic animal production relies on the use of artificial diets, which may be processed by
extrusion or pelleting technologies. Pelleting process consists of compressing the mixture of
ingredients with moderate temperature and pressure, whereas extruded feeds are produced under
much higher temperature, pressure, and moisture, resulting in physical and nutritional benefits
and biosecurity (Allan and Booth 2004; Barrows et al. 2007; Delgado and Reyes-Jaquez 2018;
Khater et al. 2014). The use of extruded diets in aquaculture has been extensively investigated for
fish nutrition, but limited studies are available regarding shrimp farming. Several advantages of
using extrusion systems to produce aquafeeds have been pointed out, such as better digestibility,
food conversion, water stability, elimination of pathogens, deactivation of antinutritional factors,
production of smaller pellets, high durability, floatability control, less water pollution, and cost-
effectiveness (Misra et al. 2002; Allan and Booth 2004; Venou et al. 2009; Muñoz 2011; Welker
et al. 2018). Extruded feeds have become very popular in fish production and its interest is
growing in shrimp farming, although there is no agreement about improvement in shrimp
performance (Misra et al. 2002; Adedeji et al. 2015; Guo et al. 2020).
Feed manufacturing process affects its physical characteristics, as texture and water stability,
and it may influence shrimp consumption (Misra et al. 2002). The hardness and water stability
can be controlled during extrusion adjusting the moisture and temperature (Delgado and Reyes-
Jaquez 2018). Despite the higher hardness, extruded pellets absorb water faster than pellet diets
and become soft allowing shrimp to break it easily to ingest. The nutrients trapped in the diets
start to leaching rapidly after immersion in the water (Lim and Cuzon 1994), and it may attract
shrimp; however, the longer the feed stays in the water, the more it loses nutritional value and
attractiveness. Feeding a commercial diet leached for 1 h significantly reduced the growth of
Litopenaeus vannamei in a green-water tank system (Ullman et al. 2019a). This strengthens the
concept that multiple feedings at appropriate times ensures the ingestion of “fresh” feed before
nutrients are lost due to leaching. This issue can be addressed by using automatic timer feeders
that delivery multiple feedings throughout the day and night but monitoring daily feed
consumption in murky pond waters is still challenging and may result in imprecise estimations.
Automated acoustic demand-feeding system has been used to release feed according to the
“click” signals emitted by shrimps during feeding activity, resulting significant improvements in
L. vannamei growth and yield under research (Jescovitch et al. 2018; Ullman et al. 2019b, 2019c;
Reis et al. 2020) and commercial conditions (Bador et al. 2013; Ching 2020). The emission of
these clicks occurs during mandibular occlusion to shred the food (Smith and Tabrett 2013; Silva
et al. 2019; Peixoto et al. 2020a), and the relationship between the textural characteristics of the
pelleted and extruded diets and the acoustic activity of L. vannamei was evaluated in specially
designed acoustic chambers by Peixoto et al. (2020b). These authors found similar clicking
acoustic signature between the diets but suggested that the greater hardness of extruded diet could
Aquaculture International (2021) 29:399–415 401

be an advantage to produce high intensity sounds during the feeding activity in culture systems.
Nevertheless, passive acoustic monitoring (PAM) could also be useful to evaluate feeding
behavior of L. vannamei when fed extruded and pelleted diets under laboratory conditions.
Furthermore, PAM is a novel approach to studying shrimp feeding behavior as an alternative to
traditional methods of visual observation or video recordings, which may be impaired by shrimp
benthic habits and characteristics of the rearing system (Smith and Shahriar 2013; Smith and
Tabrett 2013; Silva et al. 2019; Bardera et al. 2019a; Peixoto et al. 2020a).
Therefore, the aim of this study was to compare the growth performance, food consumption
and acoustic feeding behavior of two size classes of L. vannamei fed on the same diet
formulation processed by extrusion and compression pelleting.

Materials and methods

Diets characteristics

Shrimp growth performance and acoustic feeding behavior were performed using two com-
mercial feeds, pelleted (P) and extruded (E), produced by Zeigler, Inc. (Gardners, PA, USA).
The diets were formulated to be equivalent, with 95% match of ingredients, and were
manufactured with the same grinding specifications and pellet size (diameter, 2.4 mm; length,
6.8 mm) by using extrusion or pelletizing methods. The dietary nutrient values were reported
by the feed manufacturer as 35% of crude protein, 7% of crude fat, and 4% of crude fiber.

Feed bulk density and sinking velocity

Bulk density of feeds was calculated as feed mass per unit volume of space based on Welker
et al., (2018). Five grams of feed was placed in a 50-mL graduated cylinder and filled with
30 mL of water. The total volume was recorded after shaken the cylinder gently to remove air
trapped by the feed pellets. Feed bulk density (g cm−3) was calculated by dividing the weight
of feed (g) by difference in the water volume in mL (before and after adding feeds). The
sinking velocity was measured by monitoring the time taken for a pellet to reach the bottom of
a 500-mL measuring cylinder filled with distilled water (Das et al. 1993). Distance traveled for
the time taken gave the sinking velocity (cm/s) as an average of 25 values.

Pellet durability index

Approximately 100 g of each diet were manually sieved to remove initial fines, and then
tumbled in a pellet durability tester (Holmen NHP 100, Willow Park, North Walsham,
Norfolk, NR28 0BD, UK) for 120 s. Afterwards, the samples were weighed on an electronic
analytical balance (Mettler Toledo ML6001E precision balances, Switzerland). Pellet durabil-
ity index was calculated as follow: Pellet Durability Index (%) = Mat/Mbt × 100.
where Mat is the mass of pellet after tumbling (g) and Mbt is the mass before tumbling (g).

Water stability

Water stability (WS) was measured as the ratio of pellet retained in a wire mesh bottom
container after immersion of pellet samples during different time intervals (adapted from
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Forster 1972). Feed samples (1 g) were placed in round shaped sieves with 1-mm mesh size
hold on the top of 1-L glass beaker, filled with water (30 g/L salinity, 25 °C) to create a water
bath during 15, 30, or 60 min. During the water bath, a constant air flow was maintained in the
bottom of the beaker (under the meshed container) to create a continuously gentle water flow.
At the end of each test, all material remaining in the sieve was removed, oven-dried at 105 °C
for 24 h and weighed. Each test was made in triplicate.

Hardness over soaking time

The hardness of feed pellets was measured using a texture analyzer (TA XT plus, Stable
Microsystems Inc., Godalming, Surrey, UK) fitted with an incisor knife blade (#17, Razor
Blade Company, Van Nuys, CA, USA). Pelleted and extruded diets were soaked at room
temperature for 0, 1, 5, 15, 30, 60, and 120 min without shaking. After each soaking time, the
maximum cutting force (N) was recorded for a single pellet placed perpendicularly to the
blade. Calibration parameters were set in the software to generate a blade speed of 2 mm/s,
target distance of 1.5 mm and trigger force of 10 g. This procedure was repeated 30 times for
each combination of diet and time.

Water absorption over soaking time

Five samples (2 g) of each experimental diet were used to determine the water absorption level
with each soaking time. The diets were soaked with 100 mL water in a 125-mL Erlenmeyer at
room temperature for 0, 1, 5, 15, 30, 60 min without shaking. Following the contents were
poured through a 20-μ filter and the soaked feed was placed into pre-weighed aluminum trays
and dried by heating in a forced air oven at 60 °C overnight. The moisture content (%) of a
sample was determined from the difference in weight between the wet and dried samples.

Aromatic amino acids leaching

The lixiviation of the aromatic amino acids (phenylalanine, tyrosine, tryptophan) from the diets
was assessed as a reference for water-soluble compounds. Leaching was determined by
measuring the levels of AAA in the water, released from feed samples that have been immersed
for a fixed amount of time (Soller et al. 2018; Guo et al. 2020). Two grams of each feed (pelleted
and extruded), in triplicate, were placed in 150-mL Erlenmeyer flasks filled with 100 mL of
deionized water. All samples were arranged in a horizontal water bath shaker (140 rpm) at room
temperature. A 10-mL syringe with a 1.6-μm glass fiber filter (Whatman Inc., Florham Park,
NJ, USA) was used to take 7-mL samples at time 15, 30, and 60 min. The standards consisted of
a 0% aromatic amino acids (AAA) concentration blank sample (deionized water), and an 100%
AAA concentration sample where 2 g of commercial feed grinded was completely dissolved in
100 mL of DI water. Aromatic amino acids content (%) in samples were analyzed in a
spectrophotometer for their characteristic light absorbance at different wavelengths: 257 nm
for phenylalanine, 274 nm for tyrosine, and 280 nm for tryptophan.

Growth and food consumption

Two shrimp size classes, named as small (S; wet weight, 3.83 ± 0.16 g) and large (L; wet
weight, 10.28 ± 0.37 g) were used to separately evaluate growth performance when fed
Aquaculture International (2021) 29:399–415 403

pelleted and extruded diets during 4 and 8 weeks for S and L, respectively. For each shrimp
size class, two treatments were applied (diets E and P) with six replicates, each stocked with 10
shrimp per 100-L glass aquaria (50 × 50 × 50 cm) with constant aeration, salinity of 6 ppt and
temperature of 28 °C in an indoor clear water recirculation system. The system includes a
circulation pump, bead filter, and fluidized bed biological filter for maintaining water quality
and received 24 h of artificial light. The experiment was performed at the E. W. Shell Fisheries
Center (Auburn, AL, USA). The diets (E or P) were offered four times a day and feed inputs
were calculated assuming a weekly weight gain of 1.5 g with food conversion ratio (FCR) of
1.2. Shrimp were counted once a week to access survival and adjust the daily feed input.
At the 5th day of the trial, four aquaria of each treatment from small and large size classes
were randomized chosen to perform the shrimp food consumption analysis. The consumption
was measured as the amount of food eaten by shrimp group (N = 10) in each aquarium over a
30-min period. The measurements were performed in the morning (8:30) after a period of 16 h
fasting. Prior the test, each aquarium was siphoned to remove debris, after cleaning feed (1.5 g)
was offered in excess. After 30 min, uneaten feed was collected by siphoning residuals onto
pre-weighed dry cellulose filters (20 μ), which were then oven-dried (80 °C) overnight and
weighed. Five measurements were collected for each aquarium (20 samples/treatment) during
five consecutive days. To estimate the amount of dry matter lost in water during the test, 12
measurements (six for each diet) were performed without shrimp in the aquaria.
Mean food consumption was calculated as follows:
FC = (Fo – Fr) × Fl, where FC = food consumption (g); Fo = feed offered (g); Fr = feed
recovered (g); Fl = feed leaching, proportion of feed recovery from aquaria without shrimp,
calculated as Fl = (Fr/Fo). Results were calculated on a dry matter basis.
At the end of the trial, all shrimp in each tank were counted and weighed to calculate
survival, biomass, mean weight, FCR, and weight gain.

Acoustics of feeding behavior

The acoustic tests started at the 5th day of the growth trial to allow shrimp to acclimate to the
experimental conditions and diets. Sound recordings were made in the aquaria at the first feeding in
the morning, by randomly assigning two aquaria per day of each combination of shrimp size classes
and diets (2 aquaria × 2 size classes (S, L) × 2 diets (P, E) = 8 recordings/day) for 10 days (5th to 14th
day). Two omnidirectional AS-1 hydrophones (Aquarian Hydrophones) were used simultaneously,
with a linear frequency range between 1 Hz and 100 kHz and receiving sensitivity of – 208 dBV.
Preamplifiers with 26 dB gain (PA-4, Aquarian Hydrophones) were used for connecting the
hydrophones to digital multitrack recorder (H5, Zoom) with sampling frequency of 96 kHz
(16 Bit). The hydrophones were placed inside each aquarium (20 cm from the bottom) and
recordings lasted 30 min after the feed was offered. Water aeration was turned off during the
recordings to reduce the background noise. The amount of feed offered for audio recordings was
fixed in 1.5 g.
The audio recordings (n = 20) for each combination of size classes and diets were transferred
from the recorder to a high-performance computer for further analysis. The Raven 1.5 Pro
software (Cornel Laboratory of Ornithology, Cornell University, USA) was used to evaluate
the sound energy (dB) related to the feeding (clicking) behavior. The oscillogram and spectrogram
of the audio files were first analyzed to manually remove any additional noise in the recordings,
such as the feed dropping in the water or accidental bumps into hydrophone by shrimps.
Additionally, a bandpass filter was applied to remove the frequency band above 10 kHz avoiding
404 Aquaculture International (2021) 29:399–415

potential interference of low frequency noises (water pumps and air blowers of adjacent tanks)
and improving the homogeneity among audio files. After this step, automatic selections with fixed
duration of 15 s were generated in the 30 min audio and signal energy values (dB) were calculated
for each time interval. These values were further used to analyze the acoustic feeding behavior by
comparing the mean energy values of every 10 min time intervals (n = 40 energy values) for each
shrimp size class and diet. A similar recording protocol and data analysis was performed in three
empty aquaria in the same rearing system to calculate the mean background energy value of
71.3 dB, considered the lowest limit of energy level for acoustic feeding activity.

Statistical analysis

Data of pellet physical measurements (sinking velocity (cm/s), pellet durability index (%),
hardness (N), moisture content (%) and AAA leaching (%)), growth (final weight (g), biomass
(g), weight gain (g), survival (%) and FCR) and food consumption (g) were compared between
pelleted and extruded diets using two sample T test with a significance level of P < 0.05. The
mean values of acoustic energy (dB) of every 10-min time intervals during recordings (10, 20,
and 30 min) of two shrimp size classes (small and large) fed pelleted and extruded diets were
analyzed by factorial ANOVA (2 × 2 × 3), using a significance level of P < 0.05. The
necessary premises of normality (Kolmogorov-Smirnov) and equal variance (Cochran) were
tested for ANOVA, and Tukey’s HSD test was used as the mean separation procedure. All
analyses were performed using the Statistica 10 software (Statsoft, Inc).

Results

Diet characteristics

The mean (± SD) pellet size of the diets (n = 20 samples/diet) was 6.43 ± 0.49 mm length ×
2.38 ± 0.07 mm diameter for the extruded and 6.47 ± 0.73 mm length × 2.39 ± 0.05 mm
diameter for the pelleted diet. The pellet durability index was significantly higher in the
extruded pellets (97.73 ± 0.17%) in comparison to the pelleted diet (92.60 ± 0.14%)
(Table 1). When exposed to water, both diets sunk immediately and achieved 100% of
sinkability. The pelleted diet presented higher bulk density (1.25 ± 0.01 g/cm3) and sinking
velocity (8.55 ± 1.22 cm/s) than extruded pellets (Table 1).
The water stability was similar between diets as their pellet dry matter retention
after each soaking time (15, 30, and 60 min) did not differ (Table 1). The feed
moisture content before soaking in water (time 0) was significantly lower in the
extruded (7.5%) than in the pelleted diet (8.8%). However, after soaking, the percent-
age of water absorption was significantly higher in the extruded diet from one to
120 min (Fig. 1). The hardness (N) was significantly higher in the extruded pellets at
time zero (before soaking) and during the first 15 min immersed in the water. Both
diets softened markedly upon soaking and from 30 min there was no significant
difference between the hardness of the pellets (Fig. 1).
The leaching values for the AAA phenylalanine, tyrosine, and tryptophan are
presented in Fig. 2. After 15 min of soaking, no significant differences were found
between the average AAA leaching from pelleted and extruded diets. Phenylalanine
leached 21.34% (P) and 25.57% (E), tyrosine leached 20.74% (P) and 23.62% (E),
Aquaculture International (2021) 29:399–415 405

Table 1 Pellet durability index (PDI), density, sink velocity and dry matter retention (15, 30 and 60 min after
soaking) of extruded and pelleted diets for Litopenaeus vannamei

Extruded Pelleted p value

PDI (%) 97.73 ± 0.17a 92.60 ± 0.14b 0.000

Density (g/cm3) 1.11 ± 0.01a 1.25 ± 0.01b 0.000
Sink velocity (cm/s) 7.54 ± 1.46a 8.55 ± 1.22b 0.011
Dry matter retention (%): 15 min 91.6 ± 0.9 91.0 ± 1.3 0.515
Dry matter retention (%): 30 min 90.3 ± 0.3 91.2 ± 1.1 0.206
Dry matter retention (%): 60 min 90.8 ± 0.3 90.5 ± 0.5 0.341

Values within a row with different superscripts are significantly different based on two sample T test (p ˂ 0.05)

tryptophan leached 20.37% (P) and 21.94% (E). Significant higher leaching was
observed in the extruded diet at 30 and 60 min for all AAA. At 30 min, the leaching
from pelleted and extruded was respectively, 40.2 and 54.02% (phenylalanine), 39.11
and 50.09% (tyrosine), 38.49 and 46.65% (tryptophan). After 60 min, the leaching
from pelleted and extruded was respectively, 66.75 and 93.03% (phenylalanine), 65.15
and 86.75% (tyrosine), 64.24 and 81.05% (tryptophan).

Growth and food consumption

Growth performance and food consumption of shrimp offered pelleted or extruded diets are
presented in Table 2. In both shrimp size classes, there were no significant differences in final
mean weight, biomass, weight gain, survival, FCR, and food consumption between shrimp fed
pelleted or extruded diets.

Fig. 1 Lines represent the water absorption (moisture, %) and bars represent the hardness (force, N) of the
pelleted (P) and extruded (E) diets from 0 to 120 min after soaking. Values are expressed as average and standard
deviation. Different superscript letters within each parameter indicate significant differences (p < 0.05) between
treatments at each time as evaluated by two sample T test
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Fig. 2 Percentage of leaching (average ± SD bar) of the aromatic amino acids (AAA) phenylalanine, tyrosine,
and tryptophan from pelleted and extruded diets after 15, 30, and 60 min of immersion in water. Spectropho-
tometer wavelength light absorbance of each AAA is showed between parentheses. Different superscript letters
indicate significant differences (p < 0.05) between treatments at each immersion time as evaluated by two sample
T test

Acoustics of feeding behavior

The mean acoustic energy (dB) showed significant differences between shrimp size classes, as
larger shrimp produced higher energy during the feeding activity. The effect of time was also
observed, with a significant progressive decrease of mean energy along time intervals (10, 20,
and 30 min) during recordings. The interaction of these factors (shrimp size and time) was also
Aquaculture International (2021) 29:399–415 407

Table 2 Average values (± SD) of growth performance parameters and food consumption of two size classes of
Litopenaeus vannamei fed on pelleted (P) or extruded (E) diets during 4 and 8 weeks for small (S) and large (L)
size classes, respectively

Diet Size Final Biomass (g) Weight Survival (%) FCR Food
class weight (g) gain (g) consumption* (g)

P S 8.37 ± 0.60 77.02 ± 10.62 4.63 ± 0.69 91.67 ± 7.5 1.63 ± 0.29 0.35 ± 0.09
E S 8.08 ± 0.88 66.15 ± 10.16 4.15 ± 0.89 84.0 ± 8.94 1.84 ± 0.38 0.40 ± 0.11
p value 0.5227 0.1189 0.3419 0.1564 0.3383 0.1881
P L 20.8 ± 1.36 183.17 ± 13.49 10.51 ± 1.42 88.00 ± 4.47 1.36 ± 0.19 0.79 ± 0.32
E L 20.6 ± 1.88 188.73 ± 24.78 10.32 ± 1.62 91.67 ± 7.53 1.40 ± 0.24 0.89 ± 0.38
p value 0.7917 0.6657 0.8396 0.3655 0.7699 0.2702

S, small shrimp size class (initial weight, 3.83 ± 0.16 g); L, large shrimp size class (initial weight,10.28 ± 0.37 g).
Means without superscripts are not statistically different (p > 0.05) based on two sample T test
* Measured as the amount of food eaten by shrimp group (N = 10) per aquarium over a 30-min period

significant in the factorial analysis (Table 3). Results of acoustic energy for each combination
of diet, shrimp size class and time interval are presented in the Table 3 and Fig. 3. The feeding
behavior showed a similar pattern for both diets and shrimp size classes with a significant
progressive decrease in the mean acoustic energy (dB) of 10 min time intervals towards the
end of the 30-min recordings (Fig. 3). Large shrimp produced a significant lower acoustic
energy when fed pelleted diet in the last time interval (30 min) in comparison to extruded diet
at the same interval (Fig. 3).

Discussion

Diet characteristics

The benthic habit and slow feeding behavior of shrimps require diets that sink immediately
and retain their properties without disintegration for a longer period than most fish feeds. Both
tested diets settled fast when dropped in the water being immediately available to shrimp
consumption. The higher sinking velocity of the pelleted diet was related to its higher bulk
density.
Regarding the physical characteristics of the diets prior to soaking, extruded diet showed
higher durability (PDI) and hardness, these features may lead to more resistance to handling
and transportation, and it is an important characteristic for automations relating to feed
dispersion and to reduce economic loss by fine particles (Thomas and Van Der Poel 1996;
Aarseth et al. 2006; Molina and Espinoza 2018). The hardness of the extruded diets depends
on ingredients composition, extrusion moisture, shear, and temperature adjustments (Obaldo
et al. 2000; Delgado and Reyes-Jaquez 2018).
Immediately after immersion both diets started to absorb water, especially the extruded diet,
even so this diet maintained higher hardness then the pelleted diet during the first 15 min
underwater. The higher water absorption by extruded diets is usual and it has been associated
to the greater porosity resulting of the extrusion process, which facilitates the penetration of
water into the pellet softening the texture (Hilton et al. 1981; Misra et al. 2002; Welker et al.
2018). Soft pellets are easier to be consumed by shrimp; thus, they need to absorb some water
and become soft but without disintegrate easily when submerged (Bortone 2016; Delgado and
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Table 3 Average values (± SD) of acoustic energy and p values of factorial ANOVA (2 × 2 × 3) of every 10-min
time intervals during recordings (10, 20, and 30 min) of two size classes (small and large) of Litopenaeus
vannamei fed pelleted and extruded diets

Factors Energy (dB) p value

Diet 0.21257
Pelleted 74.55 ± 3.44
Extruded 74.93 ± 3.68
Shrimp size < 0.00001
Small 73.45 ± 2.30 b
Large 76.04 ± 4.09 a
Time < 0.00001
10 min 77.75 ± 3.89 a
20 min 74.19 ± 2.15 b
30 min 72.29 ± 1.75 c
Diet × shrimp size < 0.00001
Pelleted × small 73.44 ± 2.08 b
Pelleted × large 75.67 ± 4.12 a
Extruded × small 73.46 ± 2.52 b
Extruded × large 76.41 ± 4.06 a
Diet × time < 0.00001
Pelleted × 10 min 77.64 ± 3.71 a
Pelleted × 20 min 74.08 ± 1.95 b
Pelleted × 30 min 71.94 ± 1.21 c
Extruded × 10 min 77.86 ± 4.08 a
Extruded × 20 min 74.30 ± 2.34 b
Extruded × 30 min 72.64 ± 2.12 c
Shrimp size × time < 0.00001
Small × 10 min 75.30 ± 2.27 b
Small × 20 min 73.32 ± 1.79 c
Small × 30 min 71.74 ± 1.17 d
Large × 10 min 80.20 ± 3.62 a
Large × 20 min 75.06 ± 2.14 b
Large × 30 min 72.85 ± 2.05 c
Diet × shrimp size × time < 0.00001
Pelleted × Small × 10 min 75.20 ± 1.98 b
Pelleted × small × 20 min 73.24 ± 1.55 c
Pelleted × small × 30 min 71.89 ± 1.11 d
Pelleted × large × 10 min 80.09 ± 3.42 a
Pelleted × large × 20 min 74.92 ± 1.96 b
Pelleted × large × 30 min 71.99 ± 1.31 d
Extruded × small × 10 min 75.40 ± 2.54 b
Extruded × small × 20 min 73.40 ± 2.02 c
Extruded × small × 30 min 71.58 ± 1.22 d
Extruded × large × 10 min 80.32 ± 3.85 a
Extruded × large × 20 min 75.20 ± 2.32 b
Extruded × large × 30 min 73.70 ± 2.30 c
Factorial ANOVA
Diet 0.06987
Size < 0.00001
Time < 0.00001
Diet × size 0.08271
Diet × time 0.55635
Size × time < 0.00001
Diet × size × time 0.09049

Number of recordings analyzed (n) is 20 for each combination of size classes and diets (total N = 80)
a-d Differentsuperscript letters within each factor and interaction mean values indicate significant differences
(p < 0.05) as evaluated by Tukey’s HSD test
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Fig. 3 Acoustic signal energy of the different diets (extruded and pelleted) during the feeding activity of
Litopenaeus vannamei of small and large classes. Bars represent the mean energy values (+ SD) of every 10-
min time intervals during recordings (10, 20, and 30 min). Different lowercase letters above bars denote
significant differences (p < 0.05) evaluated by Tukey’s HSD test. The shaded box bellow 71.3 dB represents
the background sound energy and the lowest limit of energy level considered for acoustic feeding activity

Reyes-Jaquez 2018). Despite the difference in water absorption rates, both diets presented the
same of hardness after 30 min indicating no further effect of the production method. The fish
and shrimp extruded feeds have been reported as more hydrostable and maintain its shape
longer, since the higher degree of starch gelatinization attained by extrusion promotes better
durability to physical breakdown (Hilton et al. 1981; Misra et al. 2002; Welker et al. 2018).
However, in the present study, the diets produced by pelleting or extrusion presented the same
water stability (dry matter retention), which is possible a result from improved processing
techniques of pelleting shrimp feed. Many factors during manufacture can affect water stability
of shrimp diets including ingredients composition, particle size, mixing, moisture, processing
temperature, and time in the machinery configuration (Lim and Cuzon 1994; Bortone and
Kipfer 2016; Obaldo et al. 1999a; Bortone 2017). The feed water stability prevent pellet from
dissolving before the shrimp start to consume it. Despite shrimp be able to handle and ingest
very small food particles (8 to 20 μm diameter) (Hunt et al. 1992), it is possible that
disintegrated food pellets have lower attractability due to nutrients leaching, increasing the
chance to be rejected by shrimp and increase waste in the culture environment.
Since nutrients are released rapidly from diets after immersion, it is important to attract
shrimp and stimulate consumption as soon as possible but at the same time the bulk of
nutrients must be retained in the food particles until ingestion (Lim and Cuzon 1994). The
lixiviation of the aromatic amino acids (phenylalanine, tyrosine, and tryptophan) was mea-
sured as a proxy for water-soluble compounds and revealed higher leaching from the extruded
than the pelleted diet from 30 min of immersion (Fig. 2). The higher water absorption by the
extruded diets may have increased the interaction of the nutrients with water and induced to
more leaching. Guo et al. (2020) also observed higher AAA leaching from experimental
extruded diets for L. vannamei after only 15 min of hydration, after the leaching values at 30
and 60 min were more influenced by the level of a test ingredient than from the feed
410 Aquaculture International (2021) 29:399–415

production method. Thus, feed not consumed after a short time will have reduced nutrient
levels, and the impact on shrimp performance may vary from different feeds.

Shrimp growth

In the present study, the diet processing methods did not influence shrimp growth performance
significantly in both size classes evaluated (Table 2). The two diets used had basically the same
composition and grind to allow a fair comparation of the effect of the feed production method.
The main differences observed in the pellets physical characteristics and loss of AAA during
soaking were not sufficient to affect growth. The number of daily feedings (n = 4) may have
contributed to reduce the effect of nutrient leaching on shrimp performance. Despite there is no
agreement on the ideal number of daily meals, it is reasonable that increased feeding frequency
results in higher nutritional value of the feed available. Alternatively, it may be that all feeds are
formulated and developed in an environment where nutrients are leaching consequently even
after leaching for a short period of time they are nutritionally adequate. Work conducted by
Ullman et al. (2019a) demonstrated in a green-water outdoor system that there was no effect of
leached feeds on L. vannamei growth, as long as it was less than 1 h. Since our experiment was
run in a clear water system, the diets offered were the only source of food. Shrimp were
observed grabbing and consuming the pellets as soon as they were dropped into the water which
would minimize any effects of leaching.
A previously study with M. rosenbergii fed on extruded diets showed better feed
conversion ratio and protein efficiency, but there was no significant difference in
growth and survival from the shrimp group fed steam pelleted diet (Misra et al.
2002). Penaeus monodon juveniles growth was also unaffected by the feed processing
method (Rout and Bandyopadhyay 1999). Comparing extruded and pelleted feed
containing levels of distillers dried grain with solubles from sorghum, Adedeji et al.
(2015) observed some benefits of extrusion on L. vannamei growth performance, but
the results from different growth trials were inconclusive. Conversely, L. vannamei
had better growth performance fed formed diets as compared to those fed on extruded
diets with levels of salmon by-product (Guo et al. 2020).
There is a limited number of publications using comparable extruded and pelleted
diets on shrimp performance and the variations on their results may be associated
with the lack of pattern for extrusion and pelleting processes and the ingredients
content. For example, Obaldo et al. (1999b, 2000) studied the effects of dry and wet
extrusion processing parameters (shear, moisture, temperature) and observed effect of
extrudate moisture content on growth of L. vannamei. However, the authors also
observed that the ideal parameters values for extrusion processing could differ in
different types of extruder. Because the extrusion process modifies the structure of the
nutrients, as carbohydrates and proteins, this processing may cause more differences
in the final product than pelleting process. For example, it has been shown that
gelatinization of starch resulted in increased nutritional value of feedstuffs for
L. vannamei (Davis and Arnold 1993), although increased gelatinization did not
always relate to increased digestibility (Davis and Arnold 1995). Overall, comparison
of feed produced through a pelleting or extrusion process is not a simple task as there
are numerous consideration which are beyond the scope of this work. However, this
work does bring into question some of the arguments often presented to choose one
type of processing over the other.
Aquaculture International (2021) 29:399–415 411

Food consumption and acoustics of feeding behavior

Shrimp food consumption, measured for 30 min, was similar irrespective of the diet, animals
from both size classes were attracted by the diets and active intake was observed during the
trials. Although some physical and chemical characteristics of the pellets has changed during
30 min of soaking it was not sufficient to interfere with the feed intake. It may also be that
fasted shrimp are less selective about feed. According to Bardera et al. (2019b), L. vannamei
submitted to longer periods of feed deprivation (24 and 48 h) significantly increased attraction
to feed and feeding activity.
Shrimp benthic habits and anatomical characteristics of mouthparts are major setbacks to
visualize and quantify their feeding behavior using traditional methods of direct visual obser-
vation or video recordings analysis under laboratory conditions (Hunt et al. 1992; Sanchez et al.
2005; Nunes et al. 2006; Obaldo and Masuda 2006; Pontes et al. 2008; Lima et al. 2009; Suresh
et al. 2011; Silva et al. 2012; Derby et al. 2016; Bardera et al. 2019b). These difficulties are
increased under field conditions due to water depths and low visibility in production ponds. In
this case, feeding behavior of large shrimp populations have been commonly assessed by
feeding trays (Martinez-Cordova et al. 1998; Casillas-Hernandez et al. 2006), which is a labor-
intensive and imprecise technique to evaluate feeding behavior (Ullman et al. 2019b). However,
the problems related to traditional methods are not observed when using acoustics to study
shrimp feeding behavior in the aquatic environment, as the clicking signals generated by the
mandibles during feeding activity can be captured by hydrophones under different conditions of
laboratory (Smith and Tabrett 2013; Silva et al. 2019; Peixoto et al. 2020a, 2020b) and farming
rearing systems (Smith and Tabrett 2013; Smith and Shahriar 2013; Jescovitch et al. 2018;
Ullman et al. 2019 b,c; Reis et al. 2020). Furthermore, Peixoto et al. (2020a) observed a
significant correlation between feed consumption and feeding acoustic energy emitted by
L. vannamei, which could greatly contribute to feeding behavioral research.
The sound parameters of L. vannamei clicking signature (e.g., click duration, low and high
frequency, peak frequency and maximum energy) were not affected by different size classes of
L. vannamei (13 to 35 g) when fed a pelleted diet (Silva et al. 2019). Similar results were also
reported by Peixoto et al. (2020b) for L. vannamei (15 g) fed extruded and pelleted diets
offered dry “as is” or after soaking times of 1 and 2 h. Furthermore, the acoustic intensity
(RMS) during the feeding activity of L. vannamei was similar when extruded and pelleted diets
were offered dry but decreased progressively with increasing the soaking times (Peixoto et al.
2020b). These authors attributed this RMS decrease to the softer texture of soaked pellets,
which could be ingested without the need of mandibles occlusion. Although the mean acoustic
energy (dB) did not differ between extruded and pelleted diets when offered dry in the present
study, small shrimp produced lower energy than large shrimp during feeding activity (Table 3).
It is reasonable to hypothesize that acoustic energy is affected by the mandibles size, as well as
their occlusal force applied to cut the pellets, which may increase according to the size of the
shrimps. Accordingly, Reis et al. (2020) observed a reduction in feed input for the acoustic
demand-feeding system (AQ1 Systems, Tasmania, Australia) during the initial phase (38 to
45 days) of the culture cycle of L. vannamei in ponds, suggesting that the minimal acoustic
signals produced by small size shrimps resulted in low feed inputs. While this result support
our hypothesis, that small shrimp produced lower energy during feeding activity, the relation-
ship between acoustic signal and shrimp size still needs to be verified. Controlled experiments
are required to better characterize the acoustics of click signatures and feeding behavior of a
wide size range of shrimps from post-larvae or early juvenile to adult phase.
412 Aquaculture International (2021) 29:399–415

Overall acoustics of the feeding behavior showed a similar pattern for both shrimp size
classes when fed extruded and pelleted diets. However, small shrimp attained energy levels near
to the lowest limit considered as feeding activity (71.3 dB) after 20 min (20–30-min time
interval) when fed both diets, while the same occurred only for large shrimp fed the pelleted diet
(Fig. 3). This decline in the acoustic energy of the feeding activity is probably related to the time
for penaeids reach their stomach capacity, which was estimated between 1 and 10 min of
continuous feeding (Hill and Wassenberg 1987; Dall et al. 1990). Additionally, the lower food
consumption of small shrimp (0.35 to 0.40 g) in comparison with larger shrimp (0.79 to 0.89 g)
is probably associated with their smaller stomach size and lesser time required to achieve
satiety. The present results are supported by previous studies with acoustics of P. monodon in
ponds, showing that the feeding activity is heavily concentrated soon after food offering and
then declined after 15 to 23 min (Smith and Tabrett 2013; Smith and Shahriar 2013).
Furthermore, the similarities observed in the acoustics of feeding behavior between extruded
and pelleted diets are also reflecting that the consumption of the diets followed the same pattern
after food offering for each size class, which in turn resulted in similar growth performance.
In conclusion, our results reinforce the benefits of using acoustics to study feeding behavior
as an alternative to traditional methods of monitoring shrimp feeding activity. The decision for
pelleted or extruded diets in shrimp farming is a complex question which should also be
further evaluated in terms of economic and technical viability. Extruded pellets may have
better physical characteristics before soaking (durability and hardness), but after soaking our
data indicated that they lose water-soluble compounds faster, which can be a concern for slow
feeders depending on the feeding frequencies applied. Under our study conditions, both diets
resulted in similar shrimp performance and acoustic profile of feeding activity. Consequently,
the choice of processing conditions should be based on other attributes and not necessarily
based on consumption or growth which was not notably different.

Acknowledgements The authors would like to thank the Brazilian Federal Foundation for Support and
Evaluation of Graduate Education (CAPES) for providing the postdoctoral scholarship for Silvio Peixoto
(Process: CAPES-PRINT-88887.368344/2019-00). Silvio Peixoto and Roberta Soares are fellow productivity
researchers of the National Council for Scientific and Technological Development (CNPq). The authors also
express their gratitude to Dr. Leandro F. Castro from Zeigler Bros., Inc., as well as the students and staff from
Auburn University who collaborate with this research project.

Funding information This work was supported in part by the Alabama Agricultural Experiment Station and the
Hatch program (ALA016-08027) of the National Institute of Food and Agriculture and U.S. Department of Agriculture.

Compliance with ethical standards

Conflict of interest The authors declare that they have no conflicts of interest.

Ethical approval All applicable international, national, and/or institutional guidelines for the care and use of
animals were followed by the authors.

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Affiliations

Roberta Soares 1,2 & Silvio Peixoto 1,2 & Harsha S. C. Galkanda-Arachchige 1,3 & D. Allen
Davis 1
1
Aquaculture and Aquatic Sciences, Auburn University - School of Fisheries, Auburn, AL 36849, USA
2
Department of Fisheries and Aquaculture, Federal Rural University of Pernambuco, Recife, PE 52171-900,
Brazil
3
Department of Aquaculture and Fisheries, Faculty of Livestock, Fisheries and Nutrition, Wayamba
University of Sri Lanka, Makandura, Sri Lanka