ABSTRACT
The experiment aimed to evaluate the combined effects of supplementing Japanese quail diets with Moringa oleifera leaf meal (MOLM) and pomegranate peel powder (PPP) on growth, carcass quality and ileum histology. Four groups were formed: a control group, MOLM (0.2%), PPP (7.5%) and a combination of both (0.2% MOLM + 7.5% PPP). The control group exhibited the highest weight gain, followed by the MOLM group, with no significant differences in feed intake or conversion ratio. Carcass analysis showed significant differences in liver, heart and gizzard weights, with the mixed diet group having the highest values. However, wings and dressed weight percentages were unaffected by the treatments. Sensory evaluation revealed improved organoleptic properties in the mixed diet group. Histological examination demonstrated enhanced ileum morphology in the mixed diet group, with significant improvements in villi length and villus/crypt depth ratio. Overall, supplementation with 0.2% MOLM and 7.5% PPP positively impacted carcass quality, sensory attributes and bird health. These findings suggest the potential benefits of combining MOLM and PPP in quail diets to enhance growth and overall health, highlighting the importance of further research in poultry nutrition.
Introduction
To meet the growing demand for animal protein while ensuring food safety for humans using antibiotic-free feed resources poses a significant challenge for animal scientists, especially with the continual increase in the global population (Mahfuz and Piao Citation2019; Hafeez, Ahmad et al. Citation2023). Poultry farming serves as a crucial income source for small-scale farmers in developing nations (Raza et al. Citation2023). Its importance lies in meeting the daily protein needs of people through the consumption of meat and eggs (Hafeez, Hassni et al. Citation2023). Different poultry species such as layers, broiler chicken, ducks, turkeys and quails are commonly raised for both meat and egg production due to their efficiency and suitability for different markets and consumer preferences (Imtiaz et al. Citation2023).
For decades, the protection of food-producing animals from various diseases has conventionally relied on the administration of antibiotics in animal feed and disease treatment (Naz et al. Citation2024). This practice has notably bolstered feed production, facilitated animal growth and improved meat quality (Saeed et al. Citation2023). However, an escalating concern arises from the overuse of antibiotics over time, leading to the emergence of antibiotic-resistant bacterial populations (Khan et al. Citation2023). The transmission of these resistant bacteria from poultry products to humans through the consumption or handling of contaminated meat poses a significant health risk. In response, the prohibition of antibiotics in poultry diets has been implemented, prompting scientific endeavours to explore viable alternatives. Researchers have investigated diverse substitutes for antibiotics, among which herbal extracts have emerged as promising alternatives due to their effectiveness, low cost, minimal toxicity and reduced health risks (Khan et al. Citation2021; Saeeda et al. Citation2023).
Undeniably, Japanese quails have gained prominence as an experimental model in scientific investigations due to their fast-breeding cycles and disease resistance (Nasir et al. Citation2023). Their high egg and meat production, coupled with low production costs make them a preferable option for farmers worldwide. However, feeding expenses comprise a substantial portion (65–70%) of overall poultry production costs because of which scientists are focusing on exploring inexpensive unconventional feed sources and enhancing their nutritional quality (Khan et al. Citation2010). Moreover, apart from intensified food demand, another limitation of poultry production is antibiotic resistance (Hafeez, Piral et al. Citation2023). Its harmful consequences, in both poultry and consumers, has led to its global ban, which diverted the focus towards alternative sources such as dietary inclusion of plants and their extracts with growth-promoting and medicinal effectiveness (Khan et al. Citation2021; Subhan et al. Citation2023).
Moringa oleifera, a fast-growing, drought-resistant tree found in tropical and subtropical areas, is renowned for its medicinal properties (Khan et al. Citation2022). Its leaves are highly nutritious comprising substantial quantities of the vitamin B complex, vitamin C, pro-vitamin A in the form of beta-carotene, vitamin K, manganese and protein, along other essential components (Leone et al. Citation2015). Moringa oleifera leaf meal (MOLM) has been reported to possess antioxidant properties, attributed to its content of polyphenols, tannins, anthocyanin, glycosides and thiocarbamates (Ullah et al. Citation2022). It contains antibacterial, antimicrobial, anti-septic, anticancer and immunological properties and also increases production in poultry industry (Khan, Tahir et al. Citation2022).
On the other hand, pomegranate, a non-climacteric deciduous plant, extensively cultivated across various regions worldwide, including South Africa. Valued for its resilience, it demonstrates exceptional hardiness, thriving in adverse climatic and environmental conditions (Hafeez, Piral et al. Citation2023). The inedible-antioxidant rich by-product of the pomegranate, its peel, constitutes approximately 50% of the total fruit weight. The pomegranate peel has gained popularity over time among natural feed additives as a growth promoter and role in medicine for its antimicrobial, antioxidant, hepatoprotective and anti-inflammatory properties (Akuru et al. Citation2021). It is noted for its various active compounds that are tannin, flavonoids, ellagic acid, anthocyanidins and catechins, alkaloids, aromatic compounds, enzymes, phenolic and other polyphenolic compounds constituents (Kishawy et al. Citation2019). The hypolipidemic and hypoglycaemic properties of pomegranate peel have also been known to facilitate the immune system in quails and broilers (Sharifian et al. Citation2019; Akuru et al. Citation2021).
Several studies have reported that using MOLM and pomegranate peel powder (PPP) separately in poultry diet enhanced production performance, dressed weight percentages (Kamel et al. Citation2021; El-rayes et al. Citation2023), egg production (Abdel-Wahab and Mosad Citation2018; Rehman et al. Citation2022) and extended meat shelf-life (Saki et al. Citation2014; Mahfuz and Piao Citation2019; Nduku et al. Citation2021). Therefore, with the knowledge of well-reported benefits of MOLM and PPP supplementation on different species of poultry, the aim of this investigation was to estimate the potential of mixed supplementation by integration of MOLM and PPP in the basal diet on productive performance, visceral organ weight and ilium morphology of Japanese quail.
Materials and methods
Preparation of supplementation for experimental rations
Moringa oleifera leaves were harvested from the branches of almost two-year-old trees from the region of Faisalabad. Due to different types of water soluble anti-nutritional components and saponins of Moringa oleifera leaves, they were soaked in water overnight to get rid of all these components. The branches were then shade-dried in a well-ventilated environment for three to four days. After that leaves were separated carefully before milling in a hammer mill to make a leaf meal. The leaf meal was stored in airtight nylon bags during the entire period of the study to avoid possible contamination from any foreign material (Tesfaye et al. Citation2013). Chemical composition of Moringa oleifera leaf is given in .
Table 1. Chemical composition of MOLM (Ahmad et al. Citation2018).
Pomegranates were purchased from the local market in Faisalabad. Initially, the fruits were washed with distilled water, and subsequently, the arils and peels were separated through cutting. The peels were then sliced into small pieces using a sharp knife and left to dry in the shade. Once fully dried, the peel pieces were ground into a fine powder to create peel powder (Rehman et al. Citation2017). The chemical composition of pomegranate is given in .
Table 2. Gross chemical composition, % on dry weight basis of PPP (Abbas et al. Citation2017).
Experimental design
A total of 480 one-day-old Japanese quails were allocated to 8 pens, accommodating 60 quails per pen (0.8 × 1.5 m2), with 4 pens serving as replicates for each treatment. The pens were furnished with a layer of wood shavings measuring 6–8 cm in thickness on the floor. Infrared lamps were utilized to provide heat, while feed and water were accessible ad libitum via a semi-automatic system. Initially, the temperature was maintained at 33°C during the first week, gradually decreasing to approximately 20–22°C thereafter. The formulation and analysis of the diet are presented in . The formulated diet was prepared to satisfy the quails requirements for nutrition (Khosravi et al. Citation2016). The treatments were assigned as follows:
Table 3. Ingredients and chemical composition of basal and experimental diets.
• Control group (G) was provided with basal diet (g/kg).
• Treatment group (G2) basal diet + 0.2 g/kg MOLM.
• Treatment group (G3) basal diet + 7.5 g/kg Punica granatum peel powder.
• Treatment group (G4) basal diet + 0.2% MOLM + 7.5% Punica granatum peel powder or 7.7 g/kg.
The composition of the basal diet is given in . The birds were fed on basal diets () and experimental diets (treatment diets) for 42 days (6 weeks). All birds were individually weighed at weekly intervals. The feed intake was calculated daily while the feed conversion ratio (FCR) was recorded every week.
Carcass characteristics
On final day of experimental period 10 birds from each pen were selected randomly weighed and slaughtered following a 12-hour fasting period to minimize the movement of material through the intestines. After bleeding, de-feathering and evisceration were carried out to calculate carcass weight and dressing proportion. Then by random selection, 10 slaughtered birds from each pen were selected and their liver, heart and gizzard were weighed for calculating their proportion.
Histology of ileum
The extraction of small intestinal samples was carried out using sterile surgical instruments in a controlled, cool setting to ensure the cleanliness of the histology specimens. The entire length of the small intestine was isolated, cleaned and weighed. A 3-cm segment of the ileum of each selected bird was precisely cut. This segment was rinsed with a 1% sodium chloride (normal saline) solution to eliminate intestinal contents, which was followed by fixation using 10% neutral buffered formalin for 24 h. After 24 h, tissue samples were dehydrated with ethanol and then cleared using xylene for transparency. Subsequently, the cleared tissues were embedded in paraffin wax, forming blocks for sectioning. Using a microtome, sections of 5 µm thickness were cut for further analysis. Sections were stained with haematoxylin & eosin (H&E). Morphometric variables including villus height, width and crypt depth were quantitatively analysed using a light microscope.
Sensory evaluation
For sensory evaluation, meat samples were washed properly with tap water and then stored in labelled plastic bags at 4°C in the refrigerator for the next 24 h (Ayerza et al. Citation2002). After 24 h of refrigeration meat samples from all four groups were refreeze and put in an electric oven to roast for 15 min at 165° C (Hamad and Kareem Citation2019). Then sensory attributes of cooked meat were evaluated by five members of trained panelists. In this analysis juiciness, colour, tenderness, flavour and overall acceptability of meat samples were examined. Panelist marked these cooked meat samples with the help of a nine-point hedonic scale (Karthika et al. Citation2016).
Statistical analysis
The data were analysed using one-way ANOVA with Tukey’s range test (P < 0.05) in Statistix 8.1 software for conducting multiple comparisons between groups.
Results
Productive performance
Analysis of reveals that quail fed the basal diet (control group) exhibited a mean weight of 99.32 g, while those on the experimental MOLM diet weighed 96.34 g, followed by the mixed diet group at 90.49 g and the lowest weight was recorded in the PPP experimental group at 88.99 g. Further examination of data indicates that the analysis of variance on feed intake and FCR among the groups revealed non-significant (P > 0.05) variations. Hence, it can be concluded that supplementation of MOLM, PPP and the combination of both MOLM + PPP at varying levels in the test diets did not improve feed intake and FCR in quail.
Table 4. Effect of diets containing different levels of MOLM, PPP and mixture of MOLM + PPP on quail performance.
Carcass characteristics
indicates carcass characteristics of quail fed with MOLM and PPP and their mixture on carcass characteristics in quails. Dressing percentage was significantly (P < 0.01) higher in the control group and 0.2% MOLM compared to the mixed groups of quails. Similarly, dressing percentage was significantly (P < 0.01) lower in 0.2% MOLM and mixed group compared to the control. The mixed group had significant (P < 0.05) higher values for liver and heart compared to the other groups. For gizzard, the highest value was observed in the mixed group and PPP 7.5% compared to the control.
Table 5. Measurements of the carcass characteristics of quail fed with MOLM, PPP and their mixture.
Histological features of ileum
Measurements of the villus dimensions of ileum of quail fed with MOLM, PPP and their mixture are given in . The results indicate that villi length, villus depth and villus length: crypt depth were significantly (P < 0.05) higher in the mixed group compared to the control, MOLM and PPP groups. Crypt depth was significantly (P < 0.05) lower in the mixed group compared to MOLM, PPP and the control groups ().
Figure 1. Villi histology of ilium of Japanese quail (a) control group, (b) MOLM diet group, (c) PPP diet group and (d) mixed (MOLM & PPP) diet group. No abnormality in treatment group was seen.
Table 6. Measurements of the villus dimensions of ileum of quail MOLM, PPP and their mixture.
presents a comparison of sensory factors in Japanese quails fed with basal diet, MOLM, PPP and their mixture. Results indicate significantly higher scores for meat colour, tenderness, flavour and overall acceptability in the treatment groups compared to the control.
Table 7. Comparison of mean concentration (mean ± SE) of sensory factors of Japanese quails fed with basal diet, MOLM, PPP and their mixture.
Discussion
The poultry industry stands as the most rapidly expanding sector within livestock worldwide, notably thriving in tropical and subtropical regions. This sector serves not only as a crucial food resource but also contributes significantly to revenue generation. Within poultry, Japanese quail meat holds considerable value due to its reduced fat content, lower calorie levels and superior quality protein (Nasr et al. Citation2017). Body weight consistently showed improvement in the control group followed by the MOLM group. Nwogor and Ifeyinwa (Citation2017) who concluded in their study, that the inclusion of MOLM is concentration dependent, with moderate concentration (10%) showing better weight gain than higher ones (20%). These findings are consistent with the observations of Atuahene et al. (Citation2019) who observed weight gain in Japanese quail-fed MOLM at level 10% as compared to levels 5% and 15% and therefore suggested that further studies should be carried out to ascertain the optimum level of inclusion of MOLM in the diet of quail. In a study by El-Tazi (Citation2014), the diet supplemented with 1.5% Moringa meal resulted in the most significant body weight gain compared to other diets with 3.0%, 4.5% and 6.0% inclusion of Moringa meal. Several studies, including Khan et al. (Citation2017), reported notable increases in live body weight with the addition of Moringa leaf meal to broilers’ feed. Talukdar et al. (Citation2020) observed a substantial weight gain in Japanese quail-fed MOLM compared to the control group. Moringa oleifera leaves contain high protein content and a low level of tannins, alkaloids and glycosides, which play a vital role in efficient digestion and weight gain in birds. The crude extract of Moringa oleifera may enhance digestion, fostering the growth of beneficial bacteria and suppressing harmful microbes, influencing poultry growth and intestinal microbiota. The heightened digestibility and nutrient absorption from the intestine in Moringa meal-supplemented birds could account for their higher body weight (Dey and De Citation2013). Various studies have investigated the impact of PPP on the growth performance of birds. The decreasing body weight with a group of birds that they fed PPP supported the findings with Hamad and Kareem (Citation2019) who reported that the birds fed with PPP lead to decrease body weight and feed intake. Similar results were reported by Abbas et al. (Citation2017) who demonstrated that PPP at levels 5% and 7.5% significantly reduced body weight gain as compared to level 2.5%. Akuru et al. (Citation2021) observed enhanced weight gain and feed efficiency in birds supplemented with 2 and 4 g/kg of PPP. Hamady et al. (Citation2015) conducted a six-week study with 0.1% pomegranate peel extract powder in broilers’ diet, noting continuous supplementation led to increased weight gain. Rezvani and Rahimi (Citation2017) explored pomegranate peel extract and their effects on weight gain, nutrient digestibility, immune response and microbial population in broiler chickens, finding improved digestibility, microbial growth and immune response. This enhancement is attributed to pomegranate peel's growth-promoting and antimicrobial properties, along with its proanthocyanidins facilitating improved digestive enzyme functions and counteracting oxidative stress on intestinal enterocytes, ultimately enhancing nutrient digestion (Middha et al. Citation2013; Reddy et al. Citation2014).
The carcass characteristics, specifically the weights of the heart, liver and gizzard, displayed noteworthy variation (P < 0.05) among the groups. Japanese quail fed on diet incorporating a mixture of MOLM and PPP exhibited the highest percentages of liver, heart, except for gizzard in the carcass cuts. This aligns with the findings of Francois et al. (Citation2020) indicating significant effects of MOLM on overall carcass characteristics and the percentage composition of liver, heart, and gizzard. Moreover, Abbas et al. (Citation2017) described the highest percentages of liver and heart carcass cuts in diets containing 2.5%, 5.0% and 7.5% PPP that is consistent with our study's outcomes. Similarly, significantly increased percentages of internal organs in Japanese quail-fed diets comprising 3, 5 and 7 g of MOLM, supporting our findings (Ahmed and El-Rayes Citation2019).
In the present study, ileum villi length increased, while crypt depth significantly decreased (P < 0.05) in the mixed groups of quails. While MOLM and PPP have individually demonstrated effectiveness, their mixed supplementation (MOLM + PPP) showed promising effects, enhancing nutrient digestibility and promoting villi length proliferation across all groups. This improvement is likely linked to the growth-promoting characteristics of MOLM and PPP, attributed to their antimicrobial and antioxidant properties, along with other multiple benefits (Khan et al. Citation2021; Hafeez, Piral et al. Citation2023b). In the current study, the highest villi length was observed in Japanese quails fed the mixed (MOLM & PPP) diet compared to other groups, aligning with results from another study where diets supplemented with 5.0% and 7.5% PPP showed a significant increase in villi length (Abbas et al. Citation2017). Similarly, a study on Japanese quails reported higher villi length with MOLM supplementation compared to other groups (Mahmud et al. Citation2016). However, to our knowledge, no study has investigated the synergistic effect of MOLM and PPP on the ilium morphology of Japanese quail. Rao et al. (Citation2018) conducted a study on broiler chickens, examining the effects of supplementing MOLM and pomegranate peel meal, but the physiological attributes of the small intestine were not considered in that study.
The sensory quality of Japanese quail meat was evaluated by a panel of five trained panelists using a hedonic scale. Results revealed no significant (P > 0.05) differences in juiciness among all treated groups, consistent with findings by Sasidhar et al. (Citation2016). However, meat colour exhibited highly significant (P < 0.05) differences among the groups, as observed in similar studies by Kolodziej-Skalska et al. (Citation2011), who noted the efficacy of herbal extract supplementation on meat colour. No significant differences in meat tenderness were observed among the groups, although tenderness is crucial for consumer acceptance, as noted by Kolodziej-Skalska et al. (Citation2011) and Hamad and Kareem (Citation2019). However, sensory evaluation of meat flavour showed highly significant differences among all groups, with treatment groups scoring higher than the control group, consistent with findings by Sasidhar et al. (Citation2016) and Kolodziej-Skalska et al. (Citation2011), who reported positive effects of herbal extract supplementation on meat flavour. Additionally, the overall acceptability of quail meat from the four diets showed highly significant differences among all treated groups, similar to results reported by Sasidhar et al. (Citation2016), indicating improved acceptability with herbal extract supplementation.
Conclusion
The present study indicated that mixed supplemented diet (0.2% MOLM + 7.5% PPP) did not lead to increase weight, while offering mixed supplemented diet (0.2% MOLM + 7.5% PPP) to birds feed leads to a significant effect on the carcass characteristics, organoleptic properties and villus dimensions in Japanese quails.
Ethical approval statement
The Committee on Animal Rights and Welfare, GC University Faisalabad, Pakistan approved this study (ZP/12/2020).
Acknowledgments
We extend our appreciation to the Researchers Supporting Project (no. RSP2024R218), King Saud University, Riyadh, Saudi Arabia.
Disclosure statement
No potential conflict of interest was reported by the author(s).
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