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Aquaculture Research. 2021;00:1–15. wileyonlinelibrary.com/journal/are
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1© 2021 John Wiley & Sons Ltd
1 | INTRODUCTIO N
Production of fish from the aquaculture sector is considered the
cheapest and the most affordable source of animal protein in
developing countries (Tacon, 2020). However, one of the major lim-
itations of this industry is the availability and cost of fish feed that
greatly affect the aquaculture industry's success and sustainability
(Tacon, 2018). One of the main solutions for this problem is to shift
Received: 25 March 2021
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Revised: 2 July 2021
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Accepted: 3 July 2021
DOI: 10.1111/are.15 474
ORIGINAL ARTICLE
Quillaja saponaria and/or Yucca schidigera ameliorate water
quality, growth performance, blood health, intestine and gills
histomorphology of Nile tilapia, Oreochromis niloticus
Ahmed M. Abozeid1 | Mohamed M. Abdel- Rahim2 | Fatma Abouelenien3 |
Asmaa Elkaradawy1 | Radi A. Mohamed1
1Department of Aquaculture, Faculty
of Aquatic and Fisheries Sciences,
Kafrelsheikh University, Kafr El- sheikh,
Egypt
2Aquaculture Division, National Institute
of Oceanography and Fisheries (NIOF),
Cairo, Egypt
3Department of Hygiene and Preventive
Medicine, Faculty of Veterinary Medicine,
Kafrelsheikh University, Kafr El- sheikh,
Egypt
Correspondence
Radi A. Mohamed, Department of
Aquaculture, Facult y of Aquatic and
Fisheries Sciences, Kafrelsheikh
University, Kafr El- sheikh, Egypt.
Email: r.mohamed.vet@gmail.com
Funding information
The authors received no financial support
for the research, authorship and/or
publication of this article.
Abstract
This study aimed to evaluate the synergistic effects of Quillaja saponaria (QS) and
Yucca schidigera (YS) on water quality, growth performance and health status of Nile
tilapia. Fish (n = 120, 11.97 ± 0.497 g) were randomly distributed into four experimen-
tal groups in triplicates. (1) Control group (CG), fish received basal diet; (2) Yucca schi-
digera group (YS); fish received basal diet and 0.11 ml/m3 per week YS extract in water;
(3) Quillaja saponaria group (QS), fish received basal diet supplemented with 300 mg/
kg QS extract; (4) Mixed group (QS/YS), fish received basal diet supplemented with
300 mg/kg QS and 0.11 ml/m3 per week YS extract in water. Results revealed an
improvement of water quality parameters in QS/YS, YS and QS compared with CG
(p ≤ 0.05). Fish received QS and/or YS showed higher growth performance and lower
feed conversion ratio than CG (p ≤ 0.05), with the best findings being reported in QS/
YS. Using QS and/or YS improved gill health, increased intestinal villi length and goblet
cell number compared with CG (p ≤ 0.05). Lymphocytes, total protein, globulin and
lysozyme activity were increased, while cholesterol, triglycerides, glucose and creati-
nine were decreased in fish received QS and/or YS compared with CG (p ≤ 0.05), with
the best results being observed in QS/YS. QS and/or YS supplementation increased
lipase, amylase, superoxide dismutase, catalase while reduced malonaldehyde activity
compared with CG, with the highest activity being recorded in QS/YS. Conclusively,
Nile tilapia received QS and YS prompted synergistic effects that improved water
quality, growth performance, immune- oxidative status, digestive enzymes, gills and
intestine histomorphology.
KEY WORDS
ammonia, blood health, feed efficiency, gills and intestinal histomorphology, Oreochromis
niloticus, Quillaja saponaria, Yucca schidigera
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A BOZEID Et Al.
from an extensive to intensive- scale production system (Robb et al.,
2013). This intensification may be associated with excess feed, which
decreased the concentration of dissolved oxygen and increased a
load of harmful metabolites like ammonia and other nitrogenous
compounds, hydrogen sulphide and carbon dioxide (Datta, 2012;
Francis et al., 2005).
Ammonia is one of the most critical water quality parameters
that affects fish health and its concentrations tend to increase
due to excess or uneaten feed, feed with low- digestible protein,
and it is mainly generated from microbial decomposition of or-
ganic matter (Boyd, 2018). Ammonia present in two forms either
unionized ammonia (NH3), which is more toxic, and ionized ammo-
nium (NH4+) which is less toxic (Abouelenien et al., 2015). Acute
toxicity of unionized ammonia (UIA) affects all aquatic organ-
isms’ survival, while long- term exposure to UIA induces chronic
toxicity effects on growth, reproduction and survival (Arauzo &
Valladolid, 2003; Leung et al., 2011). Additionally, when ammonia
accumulates to toxic levels, the fish cannot extract energy from
feed efficiently, the fish become lethargic and eventually fall into
a coma, and death may occur (Hargreaves & Tucker, 2004). It also
interferes with energy metabolism by impairing the tricarbox-
ylic acid cycle in the mitochondria (Hegazi et al., 2010; Hegazi &
Hasanein, 2010). Hence, ammonia control became an obligatory
procedure for aquaculture operations’ successes, especially in in-
tensive fish production.
Natural growth promoters are favoured over synthetic ones, es-
pecially those containing antibiotics which are dangerous for fish/
human health and the environment and will be prohibited sooner
or later (Francis et al., 2005; Lulijwa et al., 2020; Rajasekaran et al.,
2008). There is a great demand to include natural products in aqua-
culture feed as growth promoters and of these natural products,
Quillaja saponaria (QS) and Yucca schidigera (YS) could be considered
because of their various effects on fish and animals (Francis et al.,
2002). Both QS and YS are the main commercial sources of phenolic
binding ammonia extracts in the aquaculture industry (Angeles et al.,
2017).
QS is endemic to the Mediterranean region of Chile, oc-
curring in mixed forests in the so- called sclerophyllous forest
(Schlotterbeck et al., 2015). Owing to its abundancy of saponins
that are found in the bark, wood and leaves of trees, it is used in
the food and cosmetic industries (Hoseinifar et al., 2020), as well
as vaccine adjuvants (Guerra & Sepúlveda, 2021). In aquaculture,
it was found that QS improves nutrient intake, feed digestibility
and utili zatio n (Elkaradawy et al ., 2021; Serrano, 2013). Moreo ver,
QS induced a decline in the oxygen demand for fish growth, which
has positive implications, especially in tropical aquaculture where
the level of dissolved oxygen is often a limiting factor (Francis
et al., 2005). Furthermore, QS is potential for suppressing tilapia
reproduction (Benie et al., 1990; Francis et al., 2005; Steinbronn,
2002).
Another natural product is the Yucca plant (Yucca schidig-
era), found in arid areas of Mexico and the southwestern USA.
Besides, it is composed of steroidal saponins, polysaccharides
and polyphenols, thus, the previous studies showed that it
could improve the growth performance, feed utilization, body
composition and the water quality of the common carp (Adineh
et al., 2018; Wang et al., 2020) and Nile tilapia (Abdel- Tawwab
et al., 2021; Elbialy et al., 2020). In addition, the application
of YS enhanced the immune response of carp (Dawood et al.,
2021; Wang et al., 2020), seabass (Fayed et al., 2019) and
shrimp (Yang et al., 2015) as well as the intestinal antioxidant
status (Wang et al., 2020). Hence, the use of YS as a growth
promoter is an eco- friendly approach that manages ammo-
nia and ensures the sustainability of aquaculture production
instead of excessive application of antibiotics in aquaculture
(Dawood et al., 2021).
Despite many previous studies that were carried out on the ef-
fect of QS or YS on fish performance, few studies are exploring the
synergistic effect of QS and YS. Additionally, one of the important
goals in the aquaculture industry is to increase fish production with
the least negative environmental impact, especially from excreted
ammonia. Therefore, the current study aims to evaluate the syner-
gistic effects of QS and YS on water quality, especially ammonia con-
centration, growth performance, blood health, immune response,
oxidative status and histomorphological changes in the intestine and
gills of Nile tilapia fingerlings.
2 | MATERIALS AND METHODS
2.1 | Ethical approval
The protocol and conduct of the present experiment were re-
viewed and approved by the Committee of Aquatic Animal
Care and Use in Research, Faculty of Aquatic and Fisheries
Sciences, Kafrelsheikh University, Egypt (approval number:
I A A C U C - K S U - 2 3 - 2 0 1 9 ) .
2.2 | Diet preparation and fish husbandry
For basal diet preparation, all ingredients (Table 1) were ground,
and thoroughly mixed to obtain a homogenous mixture. Then, a
paste was made by adding water, and the mixture was pelleted
using a meat grinder. The pellets were dried at room temperature
for 24 h and stor ed at −20°C in dark plastic containers unt il used.
Nile tilapia (Oreochromis niloticus) fingerlings were obtained
from a private fish farm (Kafr El- Sheikh governorate, Egypt).
Fish were kept in glass aquariums for two weeks for acclimatiza-
tion to the laboratory condition. Fish (n = 120, average weight:
11.97 ± 0.497 g) were randomly distributed into four experimen-
tal groups in triplicates in an intensive culture at a rate of 10
fish per 60 L aquarium. The treatments were: (1) control group
(CG), the fish received basal diet (Table 1); (2) Yucca schidigera ex-
tr ac t gro up (YS), fish received ba sa l diet and 0.11 ml /m3 per week
Yucca schidigera extract (Sanolife AFM®- INVE Aquaculture,
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ABOZEID Et Al .
Belgium) added into the water; (3) Quillaja saponaria group (QS),
fish received a basal diet supplemented with 300 mg/kg Qui llaja
saponaria extract (ENVIRO QS
®- Delacon Biotechnik GmbH,
Austria) mixed with feed during feed manufacturing; (4) Mixed
group (QS/YS), fish received a basal diet supplemented with
300 mg/kg Quillaja saponaria extract mixed with feed during
feed manufacturing and 0.11 ml/m3 per week Yucca schidigera
extract added into the water. Each aquarium was supplied with
air- stones as a source of oxygen and a mechanical filter to collect
the fish wastes. The filters were cleaned daily, and the aquarium
water volume was restored to the normal level using clean, well-
aerated and overnight stored water from a storage tank. Fish
were fed the experimental diets up to satiation for 60 days. The
photoperiod was adjusted to 12 h light/12 h dark. Fish mortality
was recorded daily for each aquarium.
2.3 | Water quality analysis
Daily, water samples were taken from the midpoint of each aquar-
ium to determine the total ammonia nitrogen (TAN) using a portable
photometer (Martini MI 405 MR). Dissolved oxygen (DO), tempera-
ture and pH were determined in each tank using a dissolved oxygen
and temperature meter (Oxy Guard handy Polaris dissolved oxygen
and temperature meter) and pH meter (HACH PHC725- PH meter)
respectively (Abouelenien et al., 2015). Unionized ammonia (UIA)
was determined from the pre- estimated TAN, temperature and pH
(Zhang et al., 2018).
2.4 | Fish growth performance and feed
utilization efficiency
The fish were harvested at the end of the 60- day trial period
and anesthetized by tricaine methane- sulphonate (MS- 222)
at 25 mg/L water. The fish were weighed individually to obtain
the final weight. The total length (L) of each fish was measured
using a measuring board. Growth performance and feed utiliza-
tion were calculated as follows: Body weight gain (BWG) = final
body weight (W1)/g– initial body weight (W0)/g; Weight gain rate
(WG %) = (W1−W0)/W0 × 100; Specific growth rate (SGR %/
day) = 100× (lnW1−lnW0)/t; Feed conversion ratio (FCR) = feed
intake (g)/BWG (g); Condition factor (K) = 100 × (W1/L3) and
Survival rate (SR %) = (total number of fish at the end of the exper-
iment/total number of fish at the start of the experiment) ×100,
where “t” is the experimental period (days).
2.5 | Histomorphology changes
2.5.1 | Gills histomorphology
Gill fragments from the control and experimental groups (6 fish/
treatment) were fixed in 10% buffered formalin solution (37.5%
formaldehyde) for 24 h. Fragments were dehydrated in ascending
series of ethanol (70%), cleared in xylene and embedded in par-
affin. Serial 3 μm in thickness sections were cut on Leica Rotary
Microtome (RM 2145, Leica Microsystems, Wetzlar, Germany) and
Ingredient %Chemical composition %
Fish meal (60% CP) 3.2 Dry matter 90.0
Soybean meal 36.5 Crude protein 30.0
Corn gluten 8.0 Ether extract 6.02
Yellow corn 12.2 Crude fibre 4.95
Wheat middlings 22.5 Ash 5.1
Poultry byproducts meal 4.0 Carbohydratesb 53.93
Rice bran 8.0 Available phosphorus 0.4
Soybean oil +rapeseed oil 2.0 Calcium 0.99
Monocalcium phosphate 0.6 Metabolizable energy (kcal/kg)c 3739.1
Common salt 0.5 Metabolizable energy (MJ/kg)d 15.65
Calcium carbonate 0.5
Premixa 2.0
aPremix (except vitamin E, mg/kg premix): vitamin A (3300 IU), vitamin D3 (410 IU), vitamin B1
(133 mg), vitamin B2 (580 mg), vitamin B6 (410 mg), vitamin B12 (50 mg), biotin (9330 mg), choline
chloride (4000 mg), vitamin C (2660 mg), inositol (330 mg), para- amino benzoic acid (9330 mg),
niacin (26.60 mg), pantothenic acid (2000 mg), manganese (325 mg), iron (200 mg), copper (25 mg),
iodine, cobalt (5mg).
bNFE: nitrogen- free extract calculated as follow: NFE = 100− (crude protein +ether extract +crude
fibre +ash).
cMetabolizable energy was calculated using a value of 4.5 kcal/g proteins, 8.51 kcal/g fat, and
3.48 kcal/g carbohydrates.
dOne kcal = 0.0041858 MJ.
TABLE 1 Feed formulation and
proximate chemical composition of the
basal diet (on dry matter basis)
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A BOZEID Et Al.
mounted on glass slides. Then, slides are routinely stained with
haematoxylin and eosin (H&E), according to Carson and Cappellano
(2009).
2.5.2 | Intestine histomorphology and
morphometric changes
Intestine tissues from control and treated groups were ob-
tained by dissection of 6 fish/treatment. The intestinal tissues
(anterior, middle and posterior part) were collected and sub-
merged in 10% neutral- buffered formalin for 3 days for tissue
fixation. After that, the samples were dehydrated and rinsed
several times in absolute alcohol and then embedded in paraf-
fin. Serial 5- μm longitudinal sections were cut on Leica Rotary
Microtome (RM 2145, Leica Microsystems, Wetzlar, Germany)
and mounted on glass slides. Then, slides are routinely stained
with haematoxylin and eosin (H&E), according to Feldman and
Wolfe (2014). The histomorphometric analysis was performed
using Imag e j analysis software (National Institutes of Health,
MD, USA), whereas the villus height (measured from the tip of
the villus to the villus- crypt junction) and villus width from the
mid of the villus. The density of goblet cells was calculated as
the number of goblet cells per unit of surface area (mm2) (Al-
Deriny et al., 2020).
2.6 | Blood sampling and serum separation
At the end of the experimental period, blood samples (9 fish/treat-
ment) were collected from the caudal vein in vacuum tubes contain-
ing EDTA as an anticoagulant agent for haematological analysis. For
blood serum collection, plain tubes without anticoagulants were
used. The clotted blood was centrifuged at 300 rpm for 15 min at
4°C then the supernatant serum was aspirated and kept in plastic
Eppendorf tubes at −20°C.
2.6.1 | Haematological analysis
An automatic blood cell counter (Exigo- Vet., Boule Medical AB
Inc., Stockholm, Sweden) was used to assess red blood cells
(RBCs) count, haemoglobin content, packed cell volume (PCV),
and total and differential white blood cells (WBCs) count (Thrall
et al., 2004).
2.6.2 | Serum biochemical analysis and
lysozyme activity
Total proteins and albumins were determined according to Doumas
et al. (1981) and Dumas and Biggs (1972). Globulins content was
calculated mathematically. Aspartate aminotransferase (AST) and
alanine aminotransferase (ALT) activities were determined using
the colorimetric method at the wavelength of 540 nm (Reitman &
Frankel, 1957). Serum triglyceride and total cholesterol were assayed
following the manufacturer's instructions described in the GPO- PAP
and CHOD- PAP commercial clinical kit methods, Elabscience, USA
respectively. Serum glucose level was determined using glucose en-
zymatic PAP by kits obtained from Bio- Merieux, France, according
to Trinder (1969). Serum creatinine was determined using the colori-
metric method (Heinegård & Tiderström, 1973). At the wavelength
of 45 0 nm usin g ELISA Microplate Reader, th e serum lys ozyme activ-
ity was assayed (Demers & Bayne, 1997) using clinical kits obtained
from Sigma, USA.
2.6.3 | Oxidative status
The antioxidant activity was measured in 9 fish/treatment. Using
ELISA kits (Inova Biotechnology, China) at the wavelength 450 nm
using ELISA Microplate Readers, the activity of superoxide dis-
mutase (SOD), catalase (CAT), and malonaldehyde (MDA) were
measured.
2.6.4 | Digestive enzymes activity
Fish digestive enzyme activities (9 fish/ treatment) were assayed in
serum using the diagnostic reagent kits (Cusabio Biotech, Wuhan,
Hubei, China), according to the manufacturer's instructions.
Activities of digestive enzymes (lipase and amylase) were measured
according to the methods described by Abdel- Tawwab et al. (2018).
2.7 | Statistical analysis
Data were tested for distribution normality, and the normality was
confirmed by analysis of the residuals. An arcsine transformation
was used before processing percentage data. Data were analysed
using Graph Pad Prism 6 statistical package (Graph Pad Prism v6.0,
San Diego, CA, USA). The results were reported as means ± SEM.
One- way ANOVA was used for comparison among different treat-
ments. Tukey's multiple comparison was used as a post hoc test. The
significance level was set at p ≤ 0.05.
3 | RESULTS
3.1 | Water quality analysis
The water quality parameters (Table 2) showed significant dif-
ferences (p ≤ 0.05) between experimental groups except for
temperature and pH. The highest significant values of dis-
solved oxygen were recorded in fish received QS/YS compared
with CG. Fish received QS and YS recorded non- significant
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ABOZEID Et Al .
higher values when compared with CG (p > 0.05). While the
lowest significant values of total ammonia nitrogen were re-
ported in fish received QS/YS and YS in respect to QS and
CG. For unionized ammonia, the lowest significant values were
reported in fish received QS/YS and YS followed by QS com-
pared with CG (p ≤ 0.05).
3.2 | Growth performance, feed utilization
efficiency, and biometric indices
Table 3 represents results of growth performance, feed utilization
efficiency and biometric indices of Nile tilapia. The fish received QS
and/or YS showed a significant increase in the final weight, weight
gain, weight gain rate and SGR compared with CG (p ≤ 0.05). The
highest significant growth performance values were reported in fish
received QS/YS among all experimental groups (p ≤ 0.05). However,
the fish received QS and/or YS showed a significant decrease in FCR
value compared with CG (p ≤ 0.05). The fish received QS/YS exhib-
ited the lowest FCR, followed by QS and YS, while the highest value
was recorded in CG. However, feed intake, condition factor (K) and
survival rate showed non- significant (p > 0.05) differences between
all experimental groups.
3.3 | Histomorphology changes
3.3.1 | Gills histomorphology
Gills of CG showed necrotic tissues within the primary gill lamel-
lae associated with severe loss of secondary gill lamellae which
revealed marked inflammatory cell infiltration including lym-
phocytes, macrophages and mostly eosinophilic granular cells
(Figure 1a). While gills of QS group showed a decrease in the
necrotic and degenerative changes with a subsequent decrease
in the adhesion of secondary gill lamellae and decreased inflam-
matory cells infiltration eosinophilic granular cells (Figure 1b).
Besides, gills of fish received YS showed a marked reduction in
the necrosis, degeneration and inflammation associated with
adhesion of secondary gill lamellae with a marked decrease in
the eosinophilic granular inflammatory cells between gill lamel-
lae (Figure 1c). Furthermore, gills of fish received QS/YS showed
TABLE 2 Water quality analysis of fish exposed to different experimental treatments for 60 days
CG QS YS QS/YS
Dissolved oxygen (mg/L) 4.984 ± 0.129b5.105 ± 0.139ab 5.385 ± 0.182ab 5.618 ± 0.122a
Temperature (°C) 26.81 ± 0.399 26.80 ± 0.406 26.57 ± 0 .351 26.91 ± 0.435
pH 7.950 ± 0.065 7.77 5 ± 0.053 7.8 42 ± 0.079 7. 867 ± 0.084
Total ammonia nitrogen (mg/L) 0.618 ± 0.190a0.445 ± 0.082a0.112 ± 0.033b0.107 ± 0.033b
Unionized ammonia (mg/L) 0.035 ± 0.0001a0.017 ± 0.0001b0.005 ± 0.0001c0.005 ± 0.0001c
Note: Means within the same row with different superscripts are significantly different (p ≤ 0.05). Control group (CG); the fish received basal diet.
Quillaja saponaria group (QS); fish received basal diet contain 300 mg/kg Quillaja saponaria extract. Yucca schidigera group (YS); fish received 0.11 ml/
m3 per week Yucca schidigera extract in tank water. Group four (QS/YS); fish received basal diet contain a mixture of 300 mg/kg Quillaja saponaria
extract and 0.11 ml/m3 per week Yucca schidigera extract in tank water.
CG QS YS QS/YS
Initial body weight (g) 11.98 ± 0.098 11.94 ± 0 .117 12.00 ± 0.073 11.96 ± 0.128
Final body weight (g) 48.47 ± 1.370c54.32 ± 1.555b54.26 ± 1.196b58.80 ± 1.542a
Body weight gain (g) 36.49 ± 1.369c42.38 ± 1.554b42.26 ± 1.165b46.84 ± 1.599a
Weight gain rate (%) 304.7 ± 3.585c355.1 ± 5.188b352.2 ± 2.912b392.0 ± 6.734a
Specific growth rate
(% /day)
2.330 ± 0.015c2.525 ± 0.019b2.515 ± 0.007b2.654 ± 0.024a
Feed intake (g) 51.82 ± 4. 251 53.40 ± 2.214 54.94 ± 3.259 55.36 ± 1.928
Feed conversion ratio 1.420 ± 0.037a1.260 ± 0.058b1.300 ± 0.052b1.182 ± 0.059c
Condition factor (K) 1.124 ± 0.021 1.222 ± 0.061 1.250 ± 0.045 1.234 ± 0.095
Survival rate (SR %) 90.00 ± 10.00 93.33 ± 3.333 93.33 ± 3.333 93.33 ± 3.333
Note: Means within the same row with different superscripts are significantly different (p ≤ 0.05).
Control group (CG); the fish received basal diet. Quillaja saponaria group (QS); fish received basal
diet contain 300 mg/kg Quillaja saponaria extract. Yucca schidigera group (YS); fish received
0.11 ml/m3 per week Yucca schidigera extract in tank water. Group four (QS/YS); fish received basal
diet contain a mixture of 300 mg/kg Quillaja saponaria extract and 0.11 ml/m3 per week Yucca
schidigera extract in tank water.
TABLE 3 Growth performance
and feed utilization of fish exposed to
different experimental treatments for
60 day
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A BOZEID Et Al.
slight necrosis, degeneration and inflammation associated with
adhesion of secondary gill lamellae. The eosinophilic granular in-
flammatory cells were also markedly decreased between gill la-
mellae (Figure 1d).
3.3.2 | Intestine histomorphology and
morphometric changes
In the anterior, middle and posterior intestinal sections, the villi width,
villi leng th and the numb er of goblet cells showe d a significant ( p ≤ 0.05)
increase in fish received QS and/or YS (Table 4 and Figure 2) in respect
to CG except for villi width in the middle and posterior intestinal seg-
ment. The better results were observed in the fish received QS/YS in
the intestines’ different sections. While inter villi space showed a sig-
nificant decrease in anterior, middle and posterior intestinal sections in
fish received QS and/or YS compared with CG, with the bet ter finding s
being observed in fish received QS/YS followed by QS, YS and CG.
3.4 | Haematological parameters
Blood haematological parameters of Nile tilapia received QS and/or
YS showed no significant differences except for the lymphocytes (%)
(Table 5). The lymphocytes (%) showed a significant increase in fish re-
ceived QS and QS/YS in respect to that received YS and CG (p ≤ 0.05).
3.5 | Biochemical parameters and lysozyme activity
Blood biochemical parameters of Nile tilapia received QS and/or
YS in the current experiment were within the normal reference
standard of Nile tilapia (Table 5). The results showed significant
differences (p ≤ 0.05) between the measured parameters except
for albumin, ALT and AST. Total protein and globulin increased
significantly in fish received QS/YS in respect to the QS, YS
and CG (p ≤ 0.05) and the highest values were recorded in fish
treated with QS/YS. Yet, cholesterol, triglycerides, glucose and
creatinine were decreased significantly in fish received QS and/
or YS compared with CG (p ≤ 0.05). The lowest values of the
same parameters were recorded in fish received QS/YS followed
by QS.
Lysozyme activity of Nile tilapia received QS/YS and QS showed
higher significant differences (p ≤ 0.05) compared with the other ex-
perimental groups (Figure 3), with better findings being reported in
QS/YS followed by QS, YS and CG. The highest significant (p ≤ 0.05)
lysozyme activity was reported in fish received QS/YS followed by
QS, YS and CG.
FIGURE 1 Gills histomorphology of
fish exposed to different experimental
treatments for 60 days. (a) Control group
(CG); the fish received basal diet. (b)
Quillaja saponaria group (QS); fish received
basal diet contain 300 mg/kg Quillaja
saponaria extract. (c) Yucca schidigera
group (YS); fish received 0.11 ml/m3
per week Yucca schidigera extract in
tank water. (d) Group four (QS/YS); fish
received basal diet contain a mixture of
300 mg/kg Quillaja saponaria extract and
0.11 ml/m3 per week Yucca schidigera
extract in tank water
A- Gills of control group (CG) showing
adhesion of secondary gill lamellae
associated with marked inflammatory cells
infiltration mostly eosinophilic granular cells
(arrows), H&E,X200, bar= 50 µm
B- Gills of Quillaja saponaria group (QS)
showing decrease the adhesion of
secondary gill lamellae with decrease the
inflammatory cells infiltration especially
the eosinophilic granular cells (arrows),
H&E,X200, bar= 50 µm.
C- Gills of Yucca schidigera group (YS)
showing marked decrease the inflammation
associated with adhesion of secondary gill
lamellae (arrows), H&E,X200, bar= 50 µm.
D- Gills of QS/YS group showing marked
decrease the adhesion of secondary gill
lamellae accompanied with marked
decrease the inflammatory cells infiltration
(arrows), H&E,X200, bar= 50 µm.
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ABOZEID Et Al .
3.6 | Oxidative status
Superoxide dismutase activity of Nile tilapia received QS/YS and
QS showed higher significant differences (p ≤ 0.05) when com-
pared with the other experimental groups (Figure 4a) and the bet-
ter findings being reported in QS/YS and QS group compared with
YS and CG. The highest significant (p ≤ 0.05) superoxide dismutase
activity was reported in fish received QS/YS followed by QS, YS
and CG. However, catalase activity of Nile tilapia received QS/
YS and QS showed higher significant differences (p ≤ 0.05) com-
pared with the other experimental groups (Figure 4b) and the best
findings were reported in QS/YS followed by QS, YS and CG. The
results of malonaldehyde activity (Figure 4c) showed a significant
decrease (p ≤ 0.05) in fish received QS/YS and QS compared with
YS and CG. The best finding being observed in QS/YS group fol-
lowed by QS, YS and CG.
3.7 | Digestive enzymes activity
The activity of digestive enzymes of Nile tilapia received QS and/or
YS showed significant differences (p ≤ 0.05) among the experimen-
tal groups (Table 6), with the best findings being reported in QS/YS
group compared with CG. The highest significant (p ≤ 0.05) lipase
activity was reported in fish received QS/YS followed by QS, YS and
CG. Furthermore, the amylase activity showed a significant differ-
ence (p ≤ 0.05) between fish received QS/YS and QS compared with
YS and CG.
4 | DISCUSSION
The global aquaculture industry aims for a continuous increase in fish
production through farm intensification and proper feed utilization.
FIGURE 2 Haematoxylin- eosin- stained (H&E, .100, bar = 80 μm) photomicrograph of the anterior, middle and posterior parts of
theintestine of fish exposed to different experimental treatments for 60 days. Control group (CG); the fish received basal diet. Quillaja
saponariagroup (QS); fish received basal diet contain 300 mg/kg Quillaja saponaria extract. Yucca schidigera group (YS); fish received 0.11
ml/m3 perweek Yucca schidigera extract in tank water. Group four (QS/YS); fish received basal diet contain a mixture of 300 mg/kg Quillaja
saponaria
CG QS YS QS/YS
Anterior part
Normal villiIncrease villi length Increase villi length Marked increase villi
length
Middle part
Normal thin and
branched villi lined
with pseudostratified
epithelium
Marked increase of
villi length and
branches
Increase of intestinal
villi length and
branches
Marked increase of
intestinal villi length
and branches
Posterior part
Normal mucosal
folds
Increase the length of
mucosal folds
Increase the length of
mucosal folds
Marked increase the
length of mucosal
folds
8
|
A BOZEID Et Al.
Hence, appropriate farm management, an adequate balanced diet
and high- quality water (source and parameters) are considered
critical components required for successful aquaculture (Abdel- Hay
et al., 2020; Abdel- Razek et al., 2019; El Saidy et al., 2020; Ghazi et al.,
2021; Figure 4).
The present study demonstrated that the lowest significant value
of TAN and UIA was reported in QS/YS, YS and QS compared with
CG. These results correspond with Güroy et al. (2016) who found a
significant reduction in TAN excretion with 0.3% dietary inclusion of
YS and QS extract to the ju venile striped catfish diet, compared to the
control. In this context, many studies have focused on the role of YS
in mitigating ammonia in aquaculture water with promising findings
(Castillo Vargasmachuca et al., 2015; Hassan et al., 2017; Yang et al.,
2015; Yu et al., 2015). In this regard, YS inclusion can lower TAN and
UIA in the carp fish (Dawood et al., 2021; Wang et al., 2020), Nile
tilapia (Abdel- Tawwab et al., 2021; Engler et al., 2018), catfish (Güroy
et al., 2014; Kelly & Kohler, 2003) and Pacific white shrimp (Litopenaeus
vannamei) and Kuruma shrimp (Marsupenaeus japonicus) (Santacruz-
Reyes & Chien , 2012). Sar kar (1999a, 1999b) con cluded that th e water
addition of YS at 6 mg/L, every 15 days, to fish and freshwater prawn
ponds caused a 58– 60% reduction in TAN excretion levels compared
with the control group at the end of the trial. Moreover, Santacruz-
Reyes and Chien (2009, 2010) found a TAN reducing effect by YS in
freshwater and seawater. Concurrently, Fayed et al. (2019) found that
UIA concentrations in the culture water decreased significantly with
the addition of 0.5 or 0.75 mg/L YS to the water of European seabass
(Dicentrarchus labrax) juveniles. TAN and UIA reduction in response to
the application of YS and QS can be attributed to ammonia's adsorp-
tion by saponin content and glycocomponents/glycoproteins in YS
and QS or the conversion of ammonia to nitrite and nitrate (Cheeke,
1996; Headon & Dawson, 1990; Piacente et al., 2005; Santacruz-
Reyes & Chien, 2009, 2010). Interes tingly, Santacr uz- Reyes and Chien
(2012) found that YS can reduce TAN by lowering the ammonia ex-
creted from shrimp and the ammonia generated from the uneaten
feed. Fayed et al. (2019) explained the decrease of UIA by YS's ca-
pacity to lower water pH, which in turn reduced UIA level in water. In
FIGURE 3 Lysozyme activity of fish exposed to different
experimental treatments for 60 day. The columns (mean ± SE)
with different letters are significantly different (P≤0.05, one- way
ANOVA).
Experimental groups
L y s o z ym eac t ivity(u n ite/m l
)
C G
Q S
Y S
Q S / Y S
0
2
4
6
8
10
12
14
a
a
b
b
Variable CG QS YS QS/YS
Anterior part
Villi width (µm) 89. 09 ± 8.542c145.3 ± 3.401a136.8 ± 4.133b147. 4 ± 6.112a
Villi length (µm) 244.2 ± 23.59c410.5 ± 12.65ab 352.4 ± 32.30b472.5 ± 17.28 a
Inter villi space (µm) 66.01 ± 7.09 3a52.01 ± 5.071b58.23 ± 4.266ab 48.09 ± 3.115b
Goblet cell no/mm27. 667 ± 0.882c12.67 ± 0.881b12.00 ± 0.577b16 .67 ± 0.890a
Middle part
Villi width (µm) 103. 8 ± 8.911 108.1 ± 3.016 104.4 ± 9.0 35 110 .2 ± 8.438
Villi length (µm) 396.5 ± 35.43b544.6 ± 29.85a540.6 ± 12.62a594.3 ± 8.963a
Inter villi space (µm) 94.10 ± 6.383a89.92 ± 8.231a91.98 ± 5.477a62.18 ± 2.957b
Goblet cell no/mm21 7.0 0 ± 1.528c24.33 ± 1.856ab 20.00 ± 1.155bc 29. 00 ± 1.577a
Posterior part
Villi width (µm) 118. 5 ± 3.287 120.8 ± 14.87 123.7 ± 9. 824 1 27.9 ± 2.663
Villi length (µm) 92.22 ± 7.241b177.1 ± 21.71a167.3 ± 6.891a189. 5 ± 14.17a
Inter villi space (µm) 153.9 ± 8.292a93 .19 ± 5.365b102.9 ± 3.480b89. 64 ± 5.837b
Goblet cell no/mm26.667 ± 0.334b7. 66 7 ± 0.882b7.6 67 ± 0.333b11.33 ± 0.667a
Note: Means within the same row with different superscripts are significantly different (p ≤ 0.05).
Control group (CG); the fish received basal diet. Quillaja saponaria group (QS); fish received basal
diet contain 300 mg/kg Quillaja saponaria extract. Yucca schidigera group (YS); fish received
0.11 ml/m3 per week Yucca schidigera extract in tank water. Group four (QS/YS); fish received basal
diet contain a mixture of 300 mg/kg Quillaja saponaria extract and 0.11 ml/m3 per week Yucca
schidigera extract in tank water.
TABLE 4 Intestinal histomorphology
of fish exposed to different experimental
treatments for 60 day
|
9
ABOZEID Et Al .
addition, the increase in intestinal permeabilization by saponins leads
to a better nitrogen absorption that could better manage the total
ammonia nitrogen excretion (Engler et al., 2018).
Dissolved oxygen is one of the most important parameters
of aquaculture water quality. Additionally, low dissolved- oxygen
concentration is a major cause of stress, poor appetite, slow
growth, disease susceptibility and mortality in aquatic species
(Boyd & Tucker, 2012; Li et al., 2018). The results revealed the
highest significant DO values were recorded in fish received QS/
YS compared with CG. Likewise, Engler et al. (2018) stated that
the inclusion of saponin- rich plants (Norponin®) in the Nile tilapia
diet at a dose of 500 ppm displayed the highest mean DO value
among all tested groups. The high level of DO associated with YS
inclusion is in consistent with Elbialy et al. (2020) who found a
significant increase in DO level in YS supplemented diet of the
Nile tilapia group when compared with the control group. High
DO in QS/YS group could be explained by the effect of saponins
that improve the oxygen uptake per body gain mass in fish, which
means that less oxygen is consumed in the supplemented group to
achieve the same growth (Francis et al., 2002).
The inclusion of YS and QS improved the growth performance
in terms of increased final body weight, weight gain, weight gain
rate and specific growth rate, and decreased feed conversion rate.
The growth- promoting effect of both YS and QS corresponds with
Güroy et al. (2016), who stated that dietary inclusion of a mixture
of 0.03% Yucca schidigera and Quillaja Saponaria enhanced SGR
and feed utilization of juvenile striped catfish. Similarly, dietary
supplementation of a mixture of Yucca schidigera and Quillaja
Saponaria resulted in a substantial rise in FBW, WG, SGR and a
decrease in the FCR in shrimp (Hernández- Acosta et al., 2016)
and Nile tilapia (Angeles et al., 2017). It has been reported that di-
etary QS ex tract can enhance the growth of common carp (Francis
et al., 2002; Serrano, 2013; Serrano et al., 2000) and Nile tilapia
(Elkaradawy et al., 2021; Francis et al., 2001). On the other hand,
previous studies have demonstrated that YS can enhance the
growth of catfish (Amoah et al., 2017; Güroy et al., 2014; Kelly
& Kohler, 2003), carp (Dawood et al., 2021; Wang et al., 2020),
Atlantic salmon (Gu et al., 2015), European seabass (Elkhayat et al.,
2019), Pacific white shrimp (Yang et al., 2015) and Nile tilapia
(Elbialy et al., 2020; Gaber, 2006; Njagi et al., 2017). In contrast,
YS's dietary supplementation did not improve the FCR or growth
of channel catfish (Tidwell et al., 1992). The enhancement of
growth performance coincides with our findings of the improve-
ment of water quality parameters. This could be attributed to the
effect of saponins in YS and QS, which increases cell membrane
permeability and, accordingly, improves nutrient absorption via
enhancing intestinal microbiota activity that can secrete digestive
enzymes (Güroy et al., 2016; Serrano, 2013; Wang et al., 2020).
Furthermore, the growth rate improvement associated with the
supplementation of YS extract could be attributed to its high con-
tent of polyphenolic and phytochemical compounds (e.g., yuccaols
A, B, C, D and E and resveratrol) which act as antioxidants and
natural growth promoters (Adegbeye et al., 2019; Piacente et al.,
2005).
CG QS YS QS/YS
Hb (g/dl) 8.450 ± 0.202 7.850 ± 0.433 7.4 50 ± 0.375 8.100 ± 0.924
RBCs (106/μl) 1.395 ± 0.113 1.050 ± 0.029 1.330 ± 0.185 1.150 ± 0.040
PCV (%) 25.25 ± 1.433 24.85 ± 1.588 25.30 ± 1.328 24.15 ± 1.779
WBCs (103/mm3) 25.75 ± 1.318 25.70 ± 1.732 23.50 ± 1.289 24.60 ± 1.905
Neutrophils (%) 1.500 ± 0.287 2.50 0 ± 0.866 2.500 ± 0.280 1.500 ± 0.278
Lymphocytes (%) 92.00 ± 0.577b97.5 0 ± 0.288a93.50 ± 0.866b97. 00 ± 0.577a
TP(g/dl) 3.967 ± 0.167b4.233 ± 0. 841b4.200 ± 0.153b5.633 ± 0.285a
Albumin (g/dl) 2.367 ± 0.467 1.800 ± 0.173 2.000 ± 0.100 2.367 ± 0.644
Globulin (g/dl) 1.600 ± 0.351c2.433 ± 0.318b2.200 ± 0.058bc 3.267 ± 0.167a
ALT (U/L) 17. 00 ± 4. 041 15.17 ± 1.691 20.33 ± 3.756 18.00 ± 2.309
AST(U/L) 182.0 ± 34.32 201.0 ± 27.3 4 196. 2 ± 50.31 165.7 ± 19.98
Cholesterol (mg/dl) 156.4 ± 1.097a137. 3 ± 3.839b141 .8 ± 2.433b127. 3 ± 1.732c
Triglycerides (mg/dl) 216.3 ± 2.771a153.2 ± 8.631b211.7 ± 2 .511a130.1 ± 3.549c
Glucose (mg/dl) 50.03 ± 4.533a42.37 ± 1.910b39.00 ± 3.704b36.63 ± 3.123b
Creatinine(mg/dl) 0.403 ± 0.025a0.430 ± 0.023a0.447 ± 0.044a0.338 ± 0.001b
Note: Means within the same row with different superscripts are significantly different (p < 0.05).
Control group (CG); the fish received basal diet. Quillaja saponaria group (QS); fish received basal
diet contain 300 mg/kg Quillaja saponaria extract. Yucca schidigera group (YS); fish received
0.11 ml/m3 per week Yucca schidigera extract in tank water. Group four (QS/YS); fish received basal
diet contain a mixture of 300 mg/kg Quillaja saponaria extract and 0.11 ml/m3 per week Yucca
schidigera extract in tank water.
Abbreviations: ALT, alanine aminotransferase; AST, aspartate aminotransferase; Hb, haemoglobin;
PCV, packed cell volume; RBCs, red blood cells; TP, total protein.
TABLE 5 Haemato- biochemical profile
of fish exposed to different experimental
treatments for 60 day
10
|
A BOZEID Et Al.
Gills are the primar y target of UIA in aquaculture water which
can cause impairment of gills’ respiratory func tions when it increases
more than the recommended range (Sattari et al., 2013). According
to our results, dietary supplementation of fish with QS/YS induced
a noticeable decrease in primary gill lamellae necrosis, degeneration
of secondary gill lamellae and inflammatory cell infiltration between
gill lamellae of Nile tilapia fingerlings, as compared with the control
group. Notably, the deterioration of gills in the control group reflects
the epithelial damage induced by relatively higher ammonia levels
(Abdel- Tawwab et al., 2021; Dawood et al., 2021). The potential
impact of QS/YS on the protection of gills from inflammation and
degeneration could be due to their effect on reducing the TAN and
UIA. Thus, this can decrease the toxic action of UIA on the gills and
maintain gills’ function and health. Interestingly, these results coin-
cide with our findings of antioxidant activity of the mixture of QS/
YS and, hence, this protects gills’ tissues from the inflammatory and
degenerative influences of free radicals (Dawood et al., 2021; Elbialy
et al., 2020; Elkaradawy et al., 2021).
Intestinal morphometry is an indicator of the digestive and ab-
sorptive potential of the aquatic species. The height of intestinal villi,
the width of villi and the goblet cells count affect the absorption
area's capacity, which in turn increases the feed utilization and is
considered a good indicator of a healthy intestine (Banan Khojasteh,
2012; Mohamed et al., 2020). The results exhibited an improvement
of intestinal histomorphology (increase in intestinal villi length and
width, decrease in inter- villi space, and the rise of goblet cells count)
of the Nile tilapia fed QS and/or YS in comparison with the CG.
Concurrent with our results, Huang et al. (2005) and Wang et al.
(2020) explained the YS's role in improving intestinal health and
intestinal epithelial permeability of mirror carp. In a similar sense,
Dawood et al. (2021) elucidated that YS could increase the height
and branching of the intestinal villi and increase the intestinal muco-
sa's thickness; therefore, this can enhance the integrity of the intes-
tinal wall of common carp. On the other hand, Francis et al. (2005)
found that QS could not induce any obvious damage to the intestinal
membranes in tilapia fry. Similarly, results from the study by Francis
et al. (2001) reported an increase in paracellular transport of inert
markers on the application of QS to the mucosal side of isolated tila-
pia intestinal membrane. Interestingly, the improvement of intestinal
morphometry coincides with our findings of the high activity of di-
gestive enzymes and improved growth performance.
Haematological and biochemical characteristics levels are im-
portant indicators of fish health. The present study showed a sig-
nificant increase in lymphocytes percent in fish received QS/YS
and QS compared with that received YS and CG. The increase in
lymphocytes coincided with Güroy et al. (2014), who found that
the percentage of lymphocytes was higher in juvenile striped cat-
fish (Pangasianodon hypophthalmus) fed the diet containing 1.5 g/kg
dry matter YS than in those fed the control diet. Notably, increased
lymphocytes production improved the lysozyme activity, which
modulated fish's immune status (Choi et al., 2013; Ruchin, 2020).
Conversely, the present study showed no significant differences
in the other haematological parameters. In contrast to our results,
Güroy et al. (2016) found that YS and QS extract supplementation in
juvenile striped catfish diets increased PCV value. Similarly, Roy and
Munshi (1989) observed a rise in haemoglobin, red blood corpuscles
and PCV levels of the climbing perch, Anabas testudineus, after the
fish was exposed to QS at 5 mg/L for 24 h.
FIGURE 4 Oxidative parameters [SOD (A), CAT (B) and MDA (C)]
of Nile tilapia exposed to different experimental treatments for 60
day. The columns (mean± SE) with different letters are significantly
different (P<0.05, one- way ANOVA). SOD= Superoxide dismutase,
CAT= catalase, MDA= malonaldehyde
Experimental groups
S O D(IU /m L)
C G
Q S
Y S
Q S / Y S
0
20
40
60
80
100
120
140
a
a
b
b
Experimental groups
CAT (IU/L)
C G
Q S
Y S
Q S / Y S
0
5
10
15
20
25
30
a
b
c
c
Experimental groups
MDA(IU/L)
C G
Q S
Y S
Q S / Y S
0
10
20
30
40
50
aa
b
b
(a)
(b)
(c)
|
11
ABOZEID Et Al .
According to the present results, total protein and globu-
lin increased significantly in fish received QS and/or YS than the
CG group. Consistent with the present study, Abdel- Tawwab
et al. (2021), Dawood et al. (2021), Elbialy et al. (2020) and Faggio
et al. (2014) clarified that fish (Nile tilapia, common carp, and Mugil
Cephalus) fed dietary YS displayed elevation of TP and globulin level.
The increased TP and globulin levels are probably attributed to the
stimulation of DNA, ribosomes synthesis and protein production in
the fish liver tissues (Akrami et al., 2015; Mohammadi et al., 2020).
More specifically, Gaber (2006) reported that the increased TP is
attributed to the highest protein apparent digestibility coefficient
(ADC) that was observed for Nile tilapia diets supplemented with
YS, which was significantly higher than that observed for the control
diet. On the other hand, (Serrano et al., 2000) attributed TP's in-
crease to the augmented secretion of trypsin in carp supplemented
with QS in the diet. Interestingly, YS and QS combination can induce
an increase in TP and globulin concentration, which could be related
to their role in enhancing protein metabolism (Adegbeye et al., 2019;
Wang et al., 2020).
Glucose and triglycerides act as indicators of stress and the ex-
tent of fish response to different stressors, which is vital to attain
homeostasis (Barton & Iwama, 1991; Mommsen et al., 1999). The
current findings revealed that glucose decreased significantly in fish
received QS and/or YS than the CG. Correspondingly, Angeles et al.
(2017) showed lower glucose levels in the Nile tilapia fed a mixture
of QS and YS than in the control fish. The high glucose level ob-
served in control fish is likely due to stimulation of gluconeogene-
sis, particularly from amino acids mobilized from peripheral stores
(Mommsen et al., 1999). On the contrary, YS and QS combination
could be effective in stabilizing the metabolic response to maintain
homeostasis (Angeles et al., 2017). The decrease of cholesterol in
the serum reported in this study corroborates with findings reported
by Malinow et al. (1977), Oakenfull and Sidhu (1983) and Sauvaire
et al. (1991). The lower serum cholesterol associated with the higher
cholesterol content of muscle could be related to the higher carcass
lipid content in the saponin- fed groups (Francis et al., 2001).
The creatinine level estimation in the blood indicates renal tis-
sue's capacity to control the creatinine level in the muscles of fish
(Campbell, 2004). The current findings revealed that creatinine de-
creased significantly in fish received QS and/or YS compared with
CG. Concurrent with the present study, Dawood et al. (2021) re-
ported that blood creatinine level of common carp treated with YS
was at lower level compared with that of fish exposed to ammonia.
Additionally, Abdel- Tawwab et al. (2021) reported that YS may con-
trol creatinine levels in Nile tilapia blood and enhance its resistance
to the deleterious effect of ammonia accumulation. The role of YS
and QS in regulating the level of creatinine in the kidney is associated
with high contents of saponin and stilbenes (Duffy et al., 2001).
Lysozyme activity is an important natural defence mechanism
that causes lysis of pathogenic bacteria and induces specific and non-
specific immune responses in teleosts (Chen et al., 2014; Saurabh &
Sahoo, 2008). The present study revealed that the highest significant
lysozyme activity was reported in fish received QS/YS followed by QS,
YS and CG. This finding was consistent with Wang et al. (2020) who re-
ported that YS incre ased the lys ozyme activ it y of mi rror carp . Likewise ,
Njagi et al. (2017) stated that Nile tilapia fed a diet containing 100 mg/
kg YS had the highest lysozyme activity, which was significantly higher
than that of the control. The increased lysozyme activity may be at-
tributed to the higher lymphocytes production which modulated fish's
immune status (Choi et al., 2013; Ruchin, 2020).
Free radicals can cause damage to different fish tissues and
organs. CAT, SOD and MDA activities are used to evaluate the
anti- oxidative status of fish (Kong et al., 2017; Kumar et al., 2016;
Mohamed et al., 2020). CAT and SOD are responsible for scaveng-
ing free radicals and preventing lipid peroxidation; MDA production
reflects the degree of cell damage and lipid peroxidation of tissues
(Salama et al., 2019; Yao et al., 2010). According to our study, the
highest activity of CAT and SOD of Nile tilapia fingerlings was ob-
served in QS/YS. Further, supplementation of Nile tilapia with QS
and/or YS significantly reduced MDA activity. Conversely, our results
are inconsistent with Angeles et al. (2017), who found that SOD of
Nile tilapia fed a mixture of QS and YS was 48% lower than that of
control fish. Consistent with our results, Dawood et al. (2021), Elbialy
et al. (2020) and Wang et al. (2020) showed increased ac tivity of CAT
and SOD and reduced MDA activity following YS- supplemented
diets. The antioxidant capacity of YS is elucidated in several studies
(Ahmadifar et al., 2020; Angeles et al., 2017; Cheeke et al., 2006;
Wang et al., 2020; Zubair et al., 2013). The antioxidant potential of YS
can be explained by its high content of polyphenols which scavenges
the excessive formation of reactive radicals (hydroxyl peroxide) in
the cell and consequently prevent its DNA damage by inhibiting lipid
peroxidation and lowering MDA content (Abdel- Tawwab et al., 2021;
Cigerci et al., 2009; Martínez- Álvarez et al., 2005).
One of the im portant par ameters of the diges tion ability of aqu atic
animals is the activity of digestive enzymes. This study displays a
significant increase in the lipase and amylase activity of Nile tilapia
CG QS YS QS/YS
Lipase (U/ml) 57. 20 ± 2.598b72.50 ± ± 5.023a71.25 ± 1.819a76.22 ± 2.825a
Amylase (U/ml) 71.83 ± 3.632b91.50 ± 5.965a71.50 ± 2.598b95.50 ± 3.175a
Note: Means within the same row with different superscripts are significantly different (p < 0.05).
Control group (CG); the fish received basal diet. Quillaja saponaria group (QS); fish received basal
diet contain 300 mg/kg Quillaja saponaria extract. Yucca schidigera group (YS); fish received
0.11 ml/m3 per week Yucca schidigera extract in tank water. Group four (QS/YS); fish received basal
diet contain a mixture of 300 mg/kg Quillaja saponaria extract and 0.11 ml/m3 per week Yucca
schidigera extract in tank water.
TABLE 6 Digestive enzyme activity of
fish exposed to different experimental
treatments for 60 day
12
|
A BOZEID Et Al.
fingerlings in fish received QS/YS and QS compared with CG. In line
with the present study, Hernández- Acosta et al. (2016) unveiled that
the highest values of lipase and α- amylase were detected in shrimp
feeding with 0.5 g/kg of the mixture of YS and QS. In this context,
Serrano et al. (2000) demonstrated that dietary QS significantly en-
hanced gut enzymes of carp, including amylase and trypsin, and liver
enzymes. This showed that saponins could stimulate the digestion of
proteins and carbohydrates in the gut (Francis et al., 2005).
5 | CONCLUSION
Supplementation of Nile tilapia with QS and YS induced synergistic
effects that improved culture water quality, growth performance,
immune- oxidative status, digestive enzymes, gills and intestine
histomorphology.
ACKNOWLEDGMENT
The authors would like to thank the Department of Aquaculture,
Faculty of Aquatic and Fisheries Sciences, Kafrelsheikh University,
Egypt, for providing facilities to carry out this experiment. The au-
thors would like to express their gratitude to Delacon Biotechnik
GmbH, Austria, for providing Quillaja saponaria extract (ENVIRO
QS®) and INVE Aquaculture, Belgium, for providing Yucca schidigera
extract (Sanolife AFM®).
CONFLICT OF INTEREST
The authors declare that they have no conflict of interest.
AUTHOR CONTRIBUTIONS
All authors contributed equally to this work (conception, acquisition,
samples analysis, statistical analysis, data interpretation, manuscript
drafting and manuscript revision).
DATA AVAIL ABILI TY STATEMENT
All relevant data are available from the authors upon request.
ORCID
Ahmed M. Abozeid https://orcid.org/0000-0002-9878-9331
Mohamed M. Abdel- Rahim https://orcid.org/0000-0003-2527-4780
Radi A. Mohamed https://orcid.org/0000-0003-2538-404X
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How to cite this article: Abozeid, A. M., Abdel- Rahim, M. M.,
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