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Revised: 26 August 2022
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Accepted: 5 September 2022
DOI: 10.1111/are.16118
ORIGINAL ARTICLE
Growth performance and mineral composition of the white
shrimp Penaeus vannamei and the sea grape Caulerpa lentillifera
in a co-­culture system
Alexia Omont1
| Alberto Peña-­Rodríguez1
| Shuma Terauchi2
| Ayako Matsui2 |
Francisco Magallón-­Barajas1
| Erika Torres-­Ochoa3
| Masato Endo2
1
Centro de Investigaciones Biológicas del
Noroeste (CIBNOR), Instituto Politécnico
Nacional 195, La Paz, Mexico
2
Tokyo University of Marine Science and
Technology (TUMSAT), Tokyo, Japan
3
Universidad Autónoma de Baja California
Sur (UABCS), La Paz, Mexico
Correspondence
Masato Endo, Tokyo University of Marine
Science and Technology (TUMSAT), 4-­5-­7
Konan, Minato, Tokyo 108-­8 477, Japan.
Email: asteroid@kaiyodai.ac.jp
Funding information
CIBNOR, Grant/Award Number: 808
and 809; Consejo Nacional de Ciencia
y Tecnología, Grant/Award Number:
894930
Abstract
Integrated systems have been proposed as a sustainable solution to minimize the environmental impact of shrimp intensive aquaculture practices. The increasing demand
for seafood is largely attributed to a growing need for healthy food recommended
in a human balanced diet, but information on the nutritional quality of the resulting
products is still scarce. In this study, a co-­culture system (CO) of white shrimp Penaeus
vannamei and sea grape Caulerpa lentillifera were evaluated in 50-­L tanks during 28-­
days. Water nutrients and mineral composition were measured every 4 days using
spectrophotometry and ICP-­AES, respectively. At the end of the experiment, growth
performance of shrimp and seaweed, proximal composition of shrimp and mineral
composition of shrimp and seaweed were evaluated. Shrimps in CO revealed a better final weight (15.4 ± 0.02 g) and lower feed conversion rate (1.4) compared with
monoculture system (13.5 ± 0.4 g; 1.9). C. lentillifera, in the CO system, bioremediate 64.0% of ammonium, 62.5% of nitrite, 82.4% of nitrate and 53.3% of phosphate.
Regarding minerals, there were less P, Ca, Mn, Fe and Zn in CO water than in shrimp
monoculture water. Concerning products' compositions, in CO, sea grapes had higher
protein content and shrimps revealed higher lipid content in muscle, lower whole-­
body cholesterol, higher concentrations in Fe (+70.2%), Zn (+14.8%), Co (+62.7%), Mn
(+49.9%) and lower concentrations in Na (−13.7%). Thus, cultivating P. vannamei and C.
lentillifera in a co-­culture system led to an increase the nutritional value of aquaculture
products and to improve their interest in a human healthy diet.
KEYWORDS
dietary requirements intake, integrated culture, nutritional quality, seaweed, shrimp, water
bioremediation
1
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I NTRO D U C TI O N
digestibility have been used excessively and improperly, in addition
to fertilizers and antibiotics (Martínez-­Córdova et al., 2009; Páez-­
The growth of aquaculture has caused an increase in environmen-
Osuna, 2001). The white shrimp Penaeus vannamei represents the
tal pollution due to the lack of treatment of the effluents gener-
main marine species cultivated in the world and the expansion of
ated by this industry (Ottinger et al., 2016; Max Troell et al., 2013).
its production is largely attributed to its disease resistance and
To accelerate production feeds with high levels of protein or low
growth rates compared to other species (Cock et al., 2009) and the
Aquaculture Research. 2022;00:1–13.
wileyonlinelibrary.com/journal/are
© 2022 John Wiley & Sons Ltd.
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Received: 27 January 2022
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OMONT et al.
improved performance in intensive shrimp systems (FAO, 2019; Van
the seaweed C. lentillifera, to determine water quality and changes in
Wyk, 2001). In fact, the shrimp industry is one of the main activi-
the tissue composition of both organisms for further inclusion and
ties responsible for environmental impact (Cao et al., 2007; Hatje
potential interest for a human healthy diet.
et al., 2016), associated with the increasing degree of intensification,
use of water, food and fertilizers, which results in a higher load of
organic and inorganic matter in the wastewater (Páez-­Osuna, 2001).
2
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M ATE R I A L S A N D M E TH O DS
To counteract this effect, the use of integrated systems has been
proposed as a possible solution for the degradation of organic and
The bioassay was carried out in the rearing facility of the Laboratory
inorganic waste, mainly with the use of bivalve filter molluscs, mi-
of Fish Culture, Tokyo University of Marine Science and Technology
croalgae and marine algae (Neori et al., 2004; Ostroumov, 2005;
(TUMSAT), Tokyo, Japan.
Subasinghe et al., 2003). These organisms promise to be a solution
that can be integrated into aquaculture systems to minimize the environmental impact (Otoshi et al., 2003).
2.1 | Bioassay
Caulerpa lentillifera is an edible alga, also known as sea grape,
with a high growth rate and high economic value (Paul et al., 2014;
Juvenile P. vannamei shrimps, 6.85 ± 0.54 g average weight, were
Paul & de Nys, 2008). It is a powerful food source rich in protein,
obtained from IMT Engineering Inc., Niigata, Japan, and seaweed
minerals, dietary fibres, vitamins, saturated fatty acids and unsatu-
C. lentillifera was obtained from Olive Garden Co., Okinawa, Japan,
rated fatty acids (Chen et al., 2019). Few studies have shown the ef-
both were maintained during an acclimatization period of 1 week
ficiency of this alga in wastewater treatment. C. lentillifera has shown
under laboratory conditions before the experiment. Artificial marine
a potential ability to remove basic dyes and heavy metals from in-
seawater was prepared according to Kester et al. (1967).
dustrial wastewater (Apiratikul & Pavasant, 2008; Marungrueng &
Three treatments were evaluated in triplicate for 28 days, shrimp
Pavasant, 2007) and nutrients from fish (Paul & de Nys, 2008) and
monoculture system (SM), algae monoculture system (AM) and
shrimp effluents (Ly et al., 2021; Saputra et al., 2017).
shrimp and seaweed co-­culture system (CO). Each replica consisted
Demand for seafood products is in part due to its recommended
of a 50-­L glass tank provided with continuous aeration (dissolved
inclusion in high-­quality healthy food for a balanced human diet
oxygen, 6.59 ± 0.07 mg · L−1), and stable conditions of temperature
(Fallah et al., 2011; Silva et al., 2016). Shrimp meat provides high-­
(28.4 ± 0.04 °C), salinity (35.2 ± 1.2 psu) and pH (7.20 ± 0.07), under
quality proteins, polyunsaturated fatty acids and other useful miner-
a photoperiod of 12:12 h light: dark. Water exchange was carried out
als essential for human health (Oksuz et al., 2009; Sriket et al., 2007).
weekly at 20%.
P. vannamei contains Ca, Mg, P, K, Na and Mn, which are essential
For shrimp under a monoculture system (SM), eight P. van-
minerals for human metabolism to maintain colloidal systems and an
namei shrimps (7.58 ± 0.06 g of initial weight) were placed in each
acid–­base equilibrium (Gunalan et al., 2013). Moreover, according
tank. For the seaweed monoculture system (AM), C. lentillifera algae
to the World Health Organization (WHO), trace elements such as
(15.23 ± 0.02 g of initial wet weight, i.e., 0.3 g · L−1) were placed in
Fe, Zn, Cu and Mo at the right doses are considered essential for
each tank. Finally, for the co-­culture system (CO), eight shrimps of
human health (WHO, 1996, 2001); therefore, the mineral composi-
7.62 ± 0.07 g and 15.23 ± 0.10 g of algae were placed per tank. In
tion of shrimp should be considered to check raw material quality
order to permit C. lentillifera fixation and growth, seaweeds were
in shrimp culture industries and to label nutritional requirements
placed between two 1-­cm plastic meshes fixed to polyvinyl chloride
for human health (Gunalan et al., 2013). Some of them are nonbio-
tubes filled with sand to allow maintenance at the bottom of the
degradable, known to be potential carcinogens and naturally found
tank.
in seawater (Silva et al., 2016). However, anthropogenic activity, in-
Shrimps of both culture treatments were fed twice a day with a
cluding intensive shrimp farming, promotes their bioaccumulation in
commercial feed (43% protein, 7.7% lipids, 1.4% calcium and 2.6%
aquatic ecosystems (Fallah et al., 2011; Wu & Chen, 2004). Because
phosphorus, a collaborative development by IMT Engineering Inc.
shrimp farms draw seawater directly from coastal areas, they tend
and Higashimaru Co.), starting with 5% biomass feeding rate and ad-
to bioaccumulate along trophic levels, and suitable methods need to
justing the daily dose to satiety, based on the food remains. Seaweeds
be established for their efficient removal from wastewater (Yadav
from the monoculture system were fertilized once a day, with 15 ml
et al., 2019). Finally, cholesterol, as the predominant sterol in shrimp,
of Provasoli-­enriched seawater (PES) medium (Provasoli, 1958)
is still considered for its negative nutritional aspect in the human diet
and the ammonium nitrogen concentration was kept at 0.5 ppm.
(Pires et al., 2018). Even if shrimp can be incorporated into a heart-­
Seaweeds from the co-­culture system were not fertilized.
healthy dietary pattern when paired with other lean or plant-­based
protein sources, the interest in new shrimp farming practices to lower
cholesterol levels could be advantageous for consumers concerned
2.2 | Growth parameters
about a healthy diet (Carson et al., 2020; Cheng & Hardy, 2004).
The present study aims to evaluate a co-­culture system of two
Every week, the seaweed and shrimp were weighed. At the end of
economically important species, the white shrimp P. vannamei and
the experiment, growth rates of seaweeds and shrimp productivity
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2
3
parameters were calculated: survival, final weight, weight gain, indi-
difference, calcination at 600°C for 5 h; nitrogen-­free extract (NFE),
vidual feed intake (IFI), specific growth rate (SGR) and feed conver-
calculated using difference.
On shrimp samples, total cholesterol quantification was pro-
sion rate (FCR). The equations are given in Table 1.
cessed using the Lieberman-­Burchard reaction (Arranz et al., 1994).
Concentration was expressed in milligrams per 100 g dry weight (mg
2.3 | Water quality
· 100 g−1 DW).
Every 4 days, nutrients in water in terms of ammonium, nitrite, nitrate nitrogen, phosphate and phosphorus concentrations were
quantified using spectrophotometric analysis. Water samples were
2.5 | Trace elements contents in water,
seaweed and shrimp
filtered with a 2-­μm filter paper. Hach® water test kits were used for
ammonium, nitrite, nitrate and phosphate. The concentrations were
For ICP-­AES analyses, the concentration in all samples was meas-
expressed in ppm.
ured for five essential macroelements: Na, Mg, P, K and Ca; and eight
In addition, in a plastic bottle, 99-­ml of a filtered sample was
essential trace elements: B, Mn, Fe, Co, Ni, Cu, Zn and Mo.
mixed with 1-­ml of 98% hydrochloric acid. The solution was kept
For the water samples, the necessary dilutions were first made
at room temperature until the elemental analysis. Elemental anal-
to measure the mentioned elements, in which 0.1 ml of Y was added
ysis was performed using an Inductively Coupled Plasma Atomic
as a measurement control and the hydrochloric acid volume was ad-
Emission Spectrometer, ICP-­AES (SPS7800, Seiko Instruments, Inc.).
justed to 98% to preserve the 1:100 ratio.
For solid samples, 0.1 g of each sample was weighed and trans-
2.4 | Proximal composition of seaweed and shrimp
ferred into a high-­pressure digestion quartz vessel (maximum pressure of 100 bar and maximum temperature of 260°C) to which 10 ml
of 98% sulfuric acid had been added. Digestion was carried out using
At the end of the experiment, samples of muscle were taken from
the following microwave heating program: 7-­min ramp and hold 5-­
three shrimps, as well as from the whole body from three shrimps,
min at 120°C followed by 5-­min ramp and 20-­min at 250°C. A black
and a minimum of 5-­g seaweed, in each replicate. To remove salt
liquid was obtained, indicating the complete carbonization of the
and other suspended particles, samples were washed 3-­times with
sample to which 8 ml of 30% w/w hydrogen peroxide was added
drinking water. Then, they were lyophilized, ground and stored in
and the microwave program was repeated. After cooling (65°C), the
a moisture-­free medium until analysis of proximal composition and
chamber was depressurized. The pale-­
yellow solutions obtained
ICP-­AES.
were placed in plastic bottles. Then, the necessary dilutions were
Proximal analysis was performed according to the following
made to measure the mentioned elements, in which 0.1 ml of Y was
methods: humidity, determination using weight difference at 105°C
added as a measurement control, and the volume of sulfuric acid was
for 4 h; protein, method of Dumas Equipment Leco FP-­528; ethereal
adjusted to 98% to preserve the 1:10 ratio.
extract (lipids), Soxtec-­Avanti method, TECATOR; crude fibre, suc-
The ICP-­AES analyses were performed according to the protocol
cessive hydrolysis method (acid/base); ash, determination by weight
of the supplier's user manual. A standard curve of Y in hydrochloric
TA B L E 1 Growth parameters of shrimp P. vannamei and seaweed C. lentillifera after 28 days under shrimp monoculture system (SM),
seaweed monoculture system (AM) and a co-­culture system with both species (CO)
Shrimp
Survival (%)
Seaweed
SM
CO
AM
CO
61.9 ± 8.2
71.4 ± 0
ND
ND
Initial weight (g)
7.58 ± 0.06
7.62 ± 0.07
15.23 ± 0.02
15.23 ± 0.10
Final weight (g)
13.5 ± 0.4b
15.4 ± 0.2a
188.4 ± 41.4a
26.6 ± 6.8b
92 ± 5.9b
120 ± 3.5a
Weight gain, WG (%)
−1
Specific growth rate, SGR (% · day )
Individual feed intake, IFI (g · shrimp−1)
Feed conversion rate, FCR
b
2.0 ± 0.1
12.0 ± 0.1
1.9 ± 0.1a
2.5 ± 0.04
1137 ± 273a
a
12.1 ± 0.2
1.4 ± 0.03b
40.6 ± 9.8
a
74 ± 11b
2.6 ± 0.4b
ND
ND
ND
ND
Note: Values are given as mean ± SD (n = 10). Different superscripts in the row for each organism indicate a significant difference determined by
t-­test (p < 0.05). ND: not determined.𝖲𝗎𝗋𝗏𝗂𝗏𝖺𝗅 = 𝖿𝗂𝗇𝖺𝗅𝗇𝗎𝗆𝖻𝖾𝗋𝗈𝖿𝗌𝗁𝗋𝗂𝗆𝗉𝗌 ∕ 𝗂𝗇𝗂𝗍𝗂𝖺𝗅𝗇𝗎𝗆𝖻𝖾𝗋𝗈𝖿𝗌𝗁𝗋𝗂𝗆𝗉𝗌 × 𝟣𝟢𝟢.
[
] [
]
𝖶𝖦 ( % ) = 𝖿𝗂𝗇𝖺𝗅𝗐𝖾𝗂𝗀𝗁𝗍 (𝗀) − 𝗂𝗇𝗂𝗍𝗂𝖺𝗅𝗐𝖾𝗂𝗀𝗁𝗍 (𝗀) ∕ 𝗂𝗇𝗂𝗍𝗂𝖺𝗅𝗐𝖾𝗂𝗀𝗁𝗍 (𝗀) × 𝟣𝟢𝟢.
)
[
]
[
]
(
𝖲𝖦𝖱 % ⋅ 𝖽𝖺𝗒−𝟣 = 𝗅𝗇 𝖿𝗂𝗇𝖺𝗅𝗐𝖾𝗂𝗀𝗁𝗍 (𝗀) − 𝗅𝗇 𝗂𝗇𝗂𝗍𝗂𝖺𝗅𝗐𝖾𝗂𝗀𝗁𝗍 (𝗀) ∕ 𝖾𝗑𝗉𝖾𝗋𝗂𝗆𝖾𝗇𝗍𝖺𝗅𝗉𝖾𝗋𝗂𝗈𝖽 (𝖽𝖺𝗒𝗌) × 𝟣𝟢𝟢.
)
(
𝖨𝖥𝖨 𝗀 ⋅ 𝗌𝗁𝗋𝗂𝗆𝗉−𝟣 = 𝗍𝗈𝗍𝖺𝗅𝖿𝖾𝖾𝖽𝖼𝗈𝗇𝗌𝗎𝗆𝖾𝖽𝗂𝗇𝗍𝗁𝖾𝗍𝖺𝗇𝗄 (𝗀) ∕ 𝗇𝗎𝗆𝖻𝖾𝗋𝗈𝖿𝗌𝗁𝗋𝗂𝗆𝗉𝗌.
) [
]
(
𝖥𝖢𝖱 = 𝖨𝖥𝖨 𝗀 ⋅ 𝗌𝗁𝗋𝗂𝗆𝗉−𝟣 ∕ 𝖿𝗂𝗇𝖺𝗅𝗐𝖾𝗂𝗀𝗁𝗍 (𝗀) − 𝗂𝗇𝗂𝗍𝗂𝖺𝗅𝗐𝖾𝗂𝗀𝗁𝗍 (𝗀) .
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OMONT et al.
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OMONT et al.
acid was used for the water samples, expressed in ppm and a stan-
algae, which were notably saturated. In CO, the consumption of sea-
dard curve of Y in sulfuric acid for solid samples. Concentrations
weed by the shrimp and a reduction in seaweed growth to 0.37 g ·
were expressed in milligrams per 100 g of dry weight (mg · 100 g−1
day−1 (R 2 = 0.5181) were observed, maintaining an average seaweed
density of 22.3 ± 3.2 g (i.e., 0.45 ± 0.08 g · L−1) in tanks during all the
DW).
experiment.
2.6 | Data analysis
Statistical analyses were performed using the R software ver-
3.2 | Water bioremediation and trace elements
composition
sion 4.1.2. All data were analyzed for normal distribution with the
Shapiro-­test and for homoscedasticity with the Bartlett-­test and
The water from AM showed very little variation in concentrations of
transformed if necessary. Data were subjected to a one-­way ANOVA
ammonium, nitrite, nitrate-­nitrogen and phosphate-­phosphorus dur-
(culture system), followed, if applicable, using a t-­test to compare
ing the experimental period (Figure 2). On the contrary, significant
two experimental groups or a Tukey's multiple comparison test to
differences in these concentrations could be observed between SM
compare three or more experimental groups (95% confidence).
and CO waters during the experiment. CO-­treatment allowed a reduction in up to 64.0% of ammonium nitrogen on day 16 compared
3
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R E S U LT S
3.1 | Growth parameters
with SM. Nitrite-­nitrogen and nitrate-­nitrogen started to appear in
the water content after 2 weeks of culture and were reduced in CO
up to 62.5% and 82.4%, respectively, compared with SM. Finally,
phosphate-­phosphorus concentration in water increased in all systems after day 16 and was bioremediated up to 53.3% in CO on day
The survival rate of shrimp in the co-­culture system (CO) was higher
28, compared with SM.
than that in shrimp monoculture (SM), but it was not significantly
Considering the macroelements in the water (Figure 3), there
different between treatments (Table 1). Significant differences be-
was no significant difference in Na content due to the salinity con-
tween the two culture systems were observed, during the 4-­weeks
trol of the water during the experiment. P concentration was consis-
experiment, in the final weight of the shrimp (Figure 1), which re-
tent with phosphate-­phosphorus. It was negligible in AM (<0.3 ppm).
sulted higher in CO by almost 2 g at the end of the experience. After
P concentration increased during the first 16 days for CO and SM
4 weeks, shrimp under CO presented a significantly higher weight
and, on day 28, CO water presented 53.2% less P (1.5 ± 0.05 ppm)
gain (up to 28%) and specific growth rate and reduced feed conver-
compared with SM (3.1 ± 0.02 ppm). K concentration constantly in-
sion rate compared with the monoculture system (p < 0.05), with
creased and was 21.2% higher in average in the water of culture sys-
similar individual feed intake in both systems (Table 1).
tems containing C. lentillifera (AM and CO) compared with SM. Mg
The seaweed in monoculture (AM) presented a linear growth
underwent an increase throughout the experiment in all treatments
(R 2 = 0.9985) of 6.14 g · day−1 (i.e., 40% · day−1) during the 4 weeks of
from 1327 ± 12 ppm to 1688 ± 14, 1684 ± 13 and 1526 ± 2 ppm for
culture. The weight gain was more than 1100% on average. A growth
SM, AM and CO, respectively. Ca concentration was unstable with
deceleration was observed during the last week probably due to the
all treatments during the experiment with values ranging from 141
lack of space in the devices used for the fixation and growth of the
to 197 ppm.
F I G U R E 1 Changes in the body weight
(g) of shrimp P. vannamei in monoculture
system (SM) and in a CO-­culture system
(CO) with C. lentillifera for 28 days. Values
are given as mean ± SD (n = 10). Different
superscripts indicate a significant
difference between culture systems
determined by t-­test (p < 0.05)
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F I G U R E 2 Changes in the concentrations of total ammonium nitrogen (TAN = NH3+4-­N), nitrite nitrogen (NO2-­N), nitrate-­nitrogen
(NO3-­N) and phosphate-­phosphorus (PO 4-­P) (ppm) in culture water of shrimp P. vannamei in monoculture system (SM), in the water of
seaweed C. lentillifera monoculture system (AM) and in a co-­culture system with both species (CO) for 28 days. Values are given as mean ± SD
(n = 3). Different superscripts indicate a significant difference between culture systems determined by Tukey test (p < 0.05)
Among the microelements (Figure 4), B concentration increased
in the water of AM and, by the end of the experiment, was 25.2%
3.3 | Seaweed and shrimp composition and
trace elements
higher on average compared with shrimp systems (SM and CO).
For AM water, Mn concentration remained stable and lower than
Shrimps from SM contained slightly higher protein in both the whole
0.01 ppm. On the contrary, it increased during the first 16 days for
body and muscle compared with shrimps from CO (Table 2). In con-
shrimp systems, stabilized around 0.03 ppm in CO. whereas it con-
trast, CO shrimp muscle had 2-­fold more lipids concentration com-
tinued to increase at a significantly higher concentration in SM
pared to SM shrimps. Moreover, total cholesterol concentration was
(0.04 ppm). Fe concentration in the water was significantly lower
62% reduced in CO shrimp compared with SM shrimp's whole body,
in shrimp systems than in AM (peak at 0.123 ± 0.002) the first
whereas remained without significant difference in muscle.
20 days of the experiment, then it decreased. At this time, water
Shrimps in SM and CO (Table 3) presented similar concentrations
in SM started to present significantly higher Fe concentration
in Mg, Ca, K, P, Cu and Ni. Shrimps in CO presented 70.2% higher Fe
(0.078 ± 0.002 ppm) compared with AM (0.048 ± 0.0006 ppm) and
concentrations, 14.8% of Zn, 62.7% of Co and 49.9% of Mn; whereas
CO (0.028 ± 0.0008 ppm). AM water presented a stable Cu concen-
lower concentrations of Na by 13.7%, Mo by 67.1% and B by 49.4%
tration (0.03 ppm on average). By the end of the experiment, seawa-
than shrimps in SM were found. The Na:K ratio of shrimps in CO was
ter in SM had significantly higher content in Cu (0.036 ± 0.003 ppm)
0.98, significantly lower than in SM shrimps (Na:K 1.21).
compared with CO (0.024 ± 0.0005 ppm). Zn concentration pre-
Regarding
seaweed,
protein
content
almost
doubled
sented a constant increase in AM water during the whole experi-
(12.7 ± 0.06%) whereas ash was reduced (50.4 ± 0.1%) in CO
ment, significantly higher than in other treatments. Comparing
compared with AM (7.11 ± 0.16 and 56.6 ± 0.07%, respectively).
shrimp systems, SM water had higher Zn content (0.05 ± 0.001 ppm)
Seaweed (Table 3) presented similar concentrations in Mg, Ca, P, Cu,
than CO water (0.03 ± 0.0008 ppm) from day 12 to day 28. Finally,
Ni, Fe, Mn and Zn. Seaweed in CO contained significantly more Na
no significant difference was observed for Co, Ni and Mo among
by 12.5%, Mo by 78.0%, B by 50.8% and less Co by 43.5%. The Na:K
treatments.
ratios in the two treatments resulted in similar values.
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OMONT et al.
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F I G U R E 3 Changes in the concentration of macroelements (ppm) in culture water of shrimp P. vannamei in monoculture system (SM), in
the water of seaweed C. lentillifera monoculture system (AM) and a co-­culture system with both species (CO) for 28 days. Values are given as
mean ± SD (n = 3). Different superscripts indicate a significant difference between culture systems determined by Tukey's test (p < 0.05)
4
|
DISCUSSION
4.1 | Growth parameters
(Paul et al., 2014; Ratana-­arporn & Chirapart, 2006). Ly et al. (2021)
also emphasize that the sea grape biomass acts as a safe place for
shrimp during the moulting phase contributing to reducing cannibalism and enhancing total production in the co-­culture systems.
P. vannamei shrimp performance was significantly improved in the
Although there was no significant difference in this study, shrimps
co-­culture system with C. lentillifera seaweed at 300 g · m−3, com-
in CO showed a tendency to higher survival rate compared with SM.
pared with monoculture after 28 days, showing a final weight gain
Finally, in many studies, the growth and survival of shrimp have been
of 30% higher and a feed conversion rate reduced by 16%. Ly
related closely to the improvement of water quality due to the pres-
et al. (2021) evaluated different densities of C. lentillifera in the co-­
ence of a secondary species in the co-­culture systems (Martínez-­
culture system with P. vannamei and obtained better results with
Porchas et al., 2010).
seaweed biomass of 1 kg · m−3. At the lowest density studied (500 g
−3
Regarding seaweed growth, Paul and de Nys (2008) reported that
· m ), they achieved a final weight improved by 29% and a feed con-
C. lentillifera grew better under low nitrogen content (0.017 mg · L−1)
version rate reduced by 11% compared with control. They associ-
compared with high nitrogen content (1.4 mg · L−1) in culture water.
ated the reduction in shrimp FCR with sea grape consumption as
On the contrary, Saputra et al. (2017) demonstrated that higher am-
supplemental food. Putra et al. (2019) included different levels of
monium, nitrate and phosphate concentrations in water (4.58, 3.34
sea grape dry powder in the diet of Penaeus monodon, and the best
and 2.03 ppm, respectively) induced higher growth rates for C. lentil-
shrimp performance was found at 30 g · kg−1 of feed. In this study,
lifera (3.64 g · day−1) and Paul et al. (2014) reported a growth of 2 kg ·
consumption of sea grapes by shrimps was observed all along the
week−1 of C. lentillifera when cultivated with an average nitrate water
experiment which impedes seaweed growth in the coculture sys-
content of 1.8 mg · L−1. In the seaweed monoculture system of this
tem. According to Putra et al. (2019), higher shrimp growth and feed
study, the average nitrate content of 1.8 mg · L−1 was lower than in
utilization can be associated with C. lentillifera composition, which
the co-­culture system (9.2 mg · L−1), which might have contributed to
is rich in high-­quality proteins since the essential amino acids rep-
the lower seaweed growth in the latter, additionally to the evident
resent 38% of the total amino acid content, vitamin E and minerals
seaweed consumption by shrimp.
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6
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7
F I G U R E 4 Changes in the concentration of microelements (ppm) in culture water of shrimp P. vannamei in monoculture system (SM), in
the water of seaweed C. lentillifera monoculture system (AM) and in a co-­culture system with both species (CO) for 28 days. Values are given
as mean ± SD (n = 3). Different superscripts indicate a significant difference between culture systems determined by Tukey's test (p < 0.05)
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OMONT et al.
|
OMONT et al.
Shrimp whole body
SM
CO
a
Protein
69.7 ± 0.25
72.1 ± 0.07
Lipid
Cholesterol
Fibre
Ash
TA B L E 2 Proximal composition and
total cholesterol content (%DW) of shrimp
P. vannamei after 28 days under shrimp
monoculture system (SM) and in a co-­
culture system with both species (CO)
Shrimp muscle
SM
b
CO
87.4 ± 0.23
a
84.8 ± 0.24b
b
2.4 ± 0.05a
3.9 ± 0.03
4.0 ± 0.03
1.2 ± 0.03
0.16 ± 0.006a
0.10 ± 0.003b
0.12 ± 0.006
0.11 ± 0.001
5.4 ± 0.06
5.3 ± 0.003
0.1 ± 0.06
0.3 ± 0.16
5.7 ± 0.03
5.7 ± 0.03
11.6 ± 0.08
11.6 ± 0.08
Note: Values are given as mean ± SD (n = 3). Different superscripts in the row for each shrimp
sample indicate a significant difference determined by t-­test (p < 0.05).
TA B L E 3 Composition of microelements and macroelements in shrimp P. vannamei and seaweed C. lentillifera after 28 days under shrimp
monoculture system (SM), seaweed monoculture system (AM) and in a co-­culture system with both species (CO)
Shrimp
Seaweed
SM
CO
AM
CO
Macroelements (mg · 100 g−1 DW)
Na
95.9 ± 4.0a
82.8 ± 4.2b
1579 ± 80 b
1776 ± 67a
Mg
30.9 ± 0.9
29.4 ± 2.3
163 ± 19
155 ± 10
Ca
200.3 ± 13.8
208.5 ± 18.0
65.4 ± 2.0
62.0 ± 3.0
K
79.8 ± 1.4
84.7 ± 9.2
235 ± 26
267 ± 11
P
119.1 ± 6.6
114.1 ± 4.2
77.4 ± 4.8
76.2 ± 8.4
6.82 ± 0.89
6.68 ± 0.29
69.0 ± 10.1
78.9 ± 2.6
1.21 ± 0.08a
Na/K
−1
Microelements (μg · 100 g
0.98 ± 0.08b
DW)
Cu
602.3 ± 77.0
Co
b
30.1 ± 5.5
483.7 ± 68.3
49.0 ± 3.2
a
67.8 ± 1.5
76.3 ± 2.3
a
43.1 ± 6.4b
Ni
67.0 ± 2.5
22.3 ± 7.7
26.9 ± 17.4
Fe
436.4 ± 58.4b
742.8 ± 117.2a
1375 ± 241
1397 ± 229
Mn
6.7 ± 1.1b
10.0 ± 1.4a
480.0 ± 72.9
477.2 ± 55.4
51.1 ± 4.6b
537.9 ± 80.0 b
811.4 ± 49.7a
781.8 ± 57.1a
240.2 ± 86.6
269.8 ± 75.3
56.4 ± 3.0 b
45.7 ± 8.2b
81.3 ± 19.6a
a
B
101.1 ± 16.9
Zn
680.9 ± 19.0 b
Mo
171.6 ± 5.6
a
Note: Values are given as mean ± SD (n = 3). Different superscripts in the row for each organism indicate a significant difference determined by t-­test
(p < 0.05).
4.2 | Water bioremediation and trace elements
composition
this element in this study (H. Guo et al., 2015; Liu et al., 2016). In Ly
et al. (2021), similar bioremediation values have been obtained at
higher densities of seaweed (from 0.5 to 2 g · L−1). Thus, C. lentillifera
The presence of the C. lentillifera seaweed at 0.3 g · L−1 in the co-­
seems to be a good candidate to maintain water quality in P. van-
culture system with P. vannamei, allowed reducing the load in am-
namei shrimp tanks.
monium, nitrite, nitrate and phosphate to 64.0%, 62.5%, 82.4% and
Caulerpa sp. has also been studied to remove lead, copper, cad-
53.3%, respectively, compared with shrimp monoculture during the
mium, zinc (Apiratikul & Pavasant, 2008; Pavasant et al., 2006), man-
28 days of the experiment. Bambaranda, Sasaki, et al. (2019) evalu-
ganese, iron (Misheer et al., 2006), arsenic (Bambaranda, Tsusaka,
ated the nutrient uptake efficiency of C. lentillifera after 24 h and
et al., 2019; Misheer et al., 2006) and boron (Bursali et al., 2009) in
demonstrated similar nitrogen uptake efficiency at 20 g · L−1 of sea-
wastewater. In the present study, the iron, copper and zinc concen-
weed, and at 40 g · L−1 for phosphate. They observed that C. lentillif-
trations in water were reduced by 64%, 33% and 40%, respectively,
−1
era at 30 g · L allowed the maximum bioremediation for all elements
when cultivating C. lentillifera with shrimps P. vannamei. Augusto Da
(> 80%) and they also revealed a higher affinity for nitrate. It has
Costa et al. (2001) demonstrated, for Sargassum sp., resorption of
been demonstrated that C. lentillifera mainly depends on nitrate for
potassium, calcium and magnesium at the moment of zinc absorp-
growth, which could explain the higher bioremediation efficiency of
tion. After the release of these elements, they observed a decrease
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8
9
in calcium and magnesium concentrations attributed to the absorp-
and molybdenum (Rao, 1986) of Caulerpa sp. and their bioaccumula-
tion capacity of the seaweed. Apiratikul and Pavasant (2008) discov-
tion in seaweed tissues. Nonetheless, no difference was observed
ered that calcium, magnesium and manganese were the major ions
for boron, molybdenum and cobalt concentrations between waters
released from C. lentillifera biomass during the sorption of copper,
from co-­culture and monoculture of shrimp that could have revealed
cadmium and lead, revealing that ion exchange was one of the main
an uptake of these minerals from marine water. The changes ob-
sorption mechanisms. In this work, the presence of C. lentillifera in
served might be attributed to the post-­harvest seaweed treatment.
the co-­culture system also resulted in higher potassium concentra-
For shrimp, 3% lower protein content and 2-­fold higher lipid con-
tions by 21%, and an increase in manganese, calcium and magnesium
tent were observed in shrimp muscle from the co-­culture system
concentrations by 63%, 17% and 10%, respectively. We suggest that
compared with the monoculture system. Brito et al. (2016) found
the ability of C. lentillifera to absorb metals might be associated with
shrimps with higher protein content when integrated with G. birdiae.
the same ion exchange processes as observed for Sargassum sp.
Cruz-­Suárez et al. (2010) also found higher protein and lipid contents
Finally, in the water of the seaweed monoculture system, the high-
in shrimps fed 90% on commercial feed and cocultured with Uiva
est concentrations observed for boron, iron and zinc are related to
clathrata. Elizondo-­González et al. (2018) reported higher lipid con-
the composition of the PES used as fertilizer for C. lentillifera in this
tent in shrimp whole body when supplemented with 3% U. lactuca
system. Scarce information is available on the guideline's values for
meal and attributed it to the carotenoids in algae (Elizondo-­González
marine water quality. The ANZECC and ARMCANZ (2000) estab-
et al., 2018). Seaweeds contain phytosterols which can be converted
lished reliability values for metals according to their toxicity in or-
to cholesterol using the shrimp metabolism (Guo et al., 2020).
ganisms to ensure 95% protection of marine waters: boron, 5.1 ppm;
Chen (1993) revealed that the increased supplementation of cho-
manganese, 80 ppb; iron, 300 ppb; cobalt, 1 ppb; nickel, 70 ppb; cop-
lesterol resulted in an increase in total lipid content in P. monodon
per, 13 ppb; zinc, 15 ppb and molybdenum, 23 ppb. Therefore, the
shrimp muscle, which could explain the higher lipid content observed
co-­culture system in this study helped to maintain or reduce the
in shrimp muscle from the co-­culture system. Moreover, C. lentillifera
concentrations of boron, manganese, iron, copper and zinc down
contains high levels of polyunsaturated fatty acids (Saito et al., 2010)
to these recommended values compared with both monoculture
that can provide a significant nutritional supply to cultured organ-
systems.
isms (Gamboa-­Delgado et al., 2011) and/or improve the utilization of
nutrients from the artificial feed (Cruz-­Suárez et al., 2010). The un-
4.3 | Seaweed and shrimp composition and
trace elements
saturated fatty acids are known for their hypocholesterolemic effect
on organisms. Vegetal oil in shrimp feed resulted in the reduction in
cholesterol content in P. vannamei whole body and hepatopancreas
(Cheng & Hardy, 2004), and seaweeds in livestock diets have ex-
The co-­culture system of P. vannamei with C. lentillifera presented
erted the same hypocholesterolemic effect in egg yolks and rabbits
an almost 2-­
fold protein content compared with monocultured
(Makkar et al., 2016). In this study, integrating P. vannamei and, thus,
seaweed and significantly less ash. The seaweed protein content
feeding with C. lentillifera resulted in a reduction in total cholesterol
from the co-­culture system was in the range of values (10%–­13%)
in the whole body compared with the monoculture system, even if
reported in wild seaweed by Pereira (2011) whereas monocultured
no significant difference in shrimp muscle were observed between
seaweed protein content was lower. Seaweed cultured in polycul-
the two culture systems, the same tendency can be observed, which
ture systems takes up the nutrients discharged into the water by the
would be of potential interest for human consumption.
fed organisms and improves their protein content (Brito et al., 2016;
In terms of human nutrition, shrimps are considered an excel-
M Troell et al., 2003). Regarding ash content, Brito et al. (2016) also
lent source of dietary cholesterol, and since they are particularly
reported a reduction in the ash content of Gracilaria birdie seaweed
poor in saturated fatty acids, they have been suggested for a heart-­
in an integrated system with P. vannamei. Regarding the protein con-
healthy diet (Carson et al., 2020; Soliman, 2018). Actually, con-
tent, the results registered in this study for C. lentillifera were signifi-
sumption of shrimp has been associated with an overall favourable
cantly higher (24%–­37%) than the range reported by Pereira (2011)
effect on lipid profiles and decreased prevalence of cardiovascular
for wild seaweed. The mineral composition of seaweed was different
risks (Narasimhan et al., 2021). Thus, the reduction in cholesterol in
from that reported in previous studies (Matanjun et al., 2009; Paul
shrimp's whole body and not in shrimp muscle in the co-­culture sys-
et al., 2014; Ratana-­arporn & Chirapart, 2006). Any generalization
tem would not affect the nutritional value of shrimp for the human
related to the mineral content of Caulerpa sp. is difficult, since the
diet. Finally, the difference in the shrimp composition in macro-­and
quality of the culture water affects the mineral types and concentra-
micro-­elements was significant for various elements between cul-
tions (Paul et al., 2014). Furthermore, little variation has been found
ture systems. First, a lower Na:K ratio was observed in co-­cultured
between the two cropping systems in this study. As significant dif-
shrimp compared with the monoculture system. Yang et al. (2011)
ferences, higher concentrations of sodium, boron, and molybdenum
found a beneficial protective effect of food with a Na:K ratio lower
and lower concentrations of cobalt were observed in the co-­cultured
than 1.0 resulting in a reduced risk of cardiovascular disease and
seaweed compared with the monocultured seaweed. Several studies
mortality in general. Considering the microelements, the co-­cultured
revealed the bioremediation capacity for boron (Bursali et al., 2009)
shrimp contained more iron and zinc than monoculture shrimp. Iron
13652109, 0, Downloaded from https://onlinelibrary.wiley.com/doi/10.1111/are.16118 by Tokyo University Of Marine, Wiley Online Library on [18/10/2022]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
|
OMONT et al.
|
OMONT et al.
and zinc are regularly present in plants and animals in similar concen-
AC K N OW L E D G E M E N T S
trations and are essential for green algae (Ansari et al., 2003). These
The authors particularly thank the students of TUMSAT for their
elements are bio-­accessible in seaweeds (Intawongse et al., 2018)
welcoming and their help during all the experiments: Ryusei
and the consumption of C. lentillifera would have increased their con-
Arakawa, Misaki Kurihara, Maki Sonobe and Koki Okuda. We also
centration in the shrimp organisms of this study. In the human body,
thank CIBNOR staff: María Dolores Rondero Astorga and Sindi Areli
iron occupies a dominant role in haemoglobin oxygen transport, and
Juan Antúnez from the laboratory of proximal chemical analysis for
zinc is involved in the production and function of several hormones
all the facilities and technical support. We also thank CIBNOR for
and their deficiency has severe consequences (Ansari et al., 2003).
the institutional scholarships #808 and #809 and CONACyT for the
In addition, shrimp in the co-­culture system contained more cobalt
national scholarship #894930.
and manganese, which are essential to human health since cobalt is
a key constituent of vitamin B12, and manganese possesses anti-
AU T H O R C O N T R I B U T I O N S
oxidant properties and balances cholesterol in the body (Al-­fartusie
Alexia Omont conducted rearing and cultivation experiment, the
& Mohssan, 2017). Seaweeds are considered an excellent source
analysis of water quality proximal composition and elemental com-
of manganese, which is one of the most bioaccessible element
position, and writing of original manuscript. Alberto Peña-­Rodríguez
(Intawongse et al., 2018), therefore, C. lentillifera consumption, rich
and Francisco Magallón-­Barajas made significant contribution to the
in Mn (1397 μg · 100 g−1 DW), would enrich shrimp in this element
design of the work. Shuma Terauchi and Ayako Matsui contributed
in the co-­culture system and its consumption would benefit human
to the preparation of shrimp and seaweed, water quality analysis.
health. On the contrary, the uptake pattern of cobalt was associ-
Erika Torres substantially contributed to proximal composition anal-
ated with the exoskeleton and modified by moulting in the shrimp
ysis. Masato Endo supervised the conduct of this study, especially
Crangon crangon (Weers, 1975). Even if no significant difference
involved in the experimental design, editing of the original manu-
was observed in water quality between treatments, C. lentillifera
script. All authors have approved the final version of the manuscript
seaweed from the co-­culture system had less cobalt content, which
to be published.
might be related to the lower absorption availability as shrimp absorbed it. Therefore, the consumption of shrimp from the co-­culture
C O N FL I C T O F I N T E R E S T
system with C. lentillifera would improve the intake of macro-­and
The authors declare that they have no conflict of interests.
micro-­elements essential for human health.
Finally, it could be mentioned that, regarding the Dietary
DATA AVA I L A B I L I T Y S TAT E M E N T
Reference Intakes (DRIs) of the Institute of Medicine (OIM) of the
All data are presented in the article and are available from the cor-
National Academies (United States) (Trumbo et al., 2001), consum-
responding author on request.
ing 100-­g of fresh sea grapes (equivalent to 5-­g by weight dry (Paul
et al., 2014)) from either culture systems would allow providing up
ORCID
https://orcid.org/0000-0002-4337-3128
to 7% of the daily requirements in molybdenum, 2% in magnesium,
Alexia Omont
1% in manganese and less than 0.5% in the other elements. On the
Alberto Peña-­Rodríguez
other hand, consuming 100-­g of P. vannamei from the co-­culture sys-
Shuma Terauchi
tem (approximately 70% humidity) would provide the DRIs by 37% in
Francisco Magallón-­Barajas
cobalt and molybdenum, 20% in nickel, 18% in copper, 6% in calcium,
org/0000-0001-6234-7251
5% in phosphorus, 2.5% in magnesium, iron and zinc, 1% in potas-
Erika Torres-­Ochoa
sium and less than 0.5 for the other elements while in monocultured
Masato Endo
https://orcid.org/0000-0002-7015-5361
https://orcid.org/0000-0003-1767-7651
https://orcid.
https://orcid.org/0000-0001-5252-7187
https://orcid.org/0000-0001-7325-101X
system essential elements intakes would be lower.
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5
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How to cite this article: Omont, A., Peña-­Rodríguez, A.,
Terauchi, S., Matsui, A., Magallón-­Barajas, F., Torres-­Ochoa,
E., & Endo, M. (2022). Growth performance and mineral
composition of the white shrimp Penaeus vannamei and the
sea grape Caulerpa lentillifera in a co-­culture system.
Aquaculture Research, 00, 1–13. https://doi.org/10.1111/
are.16118
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